Anthrop Anz 693 pp 351ndash366 ArticleJ Biol Clinic Anthroppublished online April 2012

wwwschweizerbartde0003-5548120165 $ 400

2012 E Schweizerbartrsquosche Verlagsbuchhandlung Stuttgart Germany

DOI 1011270003-554820120165

Absence of foramen spinosum and abnormal middlemeningeal artery in cranial series

Silviya Y Nikolova1 Diana H Toneva1 Yordan A Yordanov1 andNikolai E Lazarov2 3

1Institute of Experimental Morphology Pathology and Anthropology with Museum Bulgar-ian Academy of Sciences Sofia Bulgaria2Department of Anatomy and Histology Medical University ndash Sofia Sofia Bulgarianlazarovmedfacacadbg3Institute of Neurobiology Bulgarian Academy of Sciences Sofia Bulgaria

With 9 figures and 1 table

Summary In comparative and evolutionary aspects in humans the middle meningeal arteryenters the cranium through the foramen spinosum whereas in great apes the middle menin-geal artery can enter the cranium through foramen spinosum through foramen ovale orthrough petrosphenoid fissure Generally in nonhuman primates the anterior meningeal sys-tem is associated with the ophthalmic branch of the internal carotid artery The vessels join-ing the two systems pass through the additional channels the superior orbital fissure orthrough the cranio-orbital foramen

In anatomically modern humans the absence of foramen spinosum involves abnormaldevelopment and course of the middle meningeal artery and it is usually accompanied withreplacement of the conventional middle meningeal artery with such arising from the oph-thalmic artery system In these cases the middle meningeal artery most often enters the mid-dle cranial fossa through the superior orbital fissure and rarely through the meningo-orbitalforamen

All skulls investigated in the present study belonged to adult individuals of both sexesconditionally grouped into three cranial series ndash contemporary male medieval male andmedieval female series The absence of foramen spinosum was established only among themedieval male and female series ndash in 1 (070 ) male and in 1 (072 ) female skull on theright side and in 3 (213 ) female skulls on the left side In 1 (072 ) female skull a smallatypically located foramen spinosum was established on the right side In all of the describedcases the intracranial meningeal grooves started from the lateral edge of the superior orbitalfissure and probably reflect the ophthalmic origin of the middle meningeal artery

Key words foramen spinosum absence meningo-orbital foramen middle meningeal arteryophthalmic artery stapedial artery

IntroductionForamen spinosum is an opening in the base of the skull on the greater wing of thesphenoid bone situated directly posterior and lateral to foramen ovale It transmitsthe recurrent branch of the mandibular nerve and the middle meningeal vessels The

eschweizerbart_XXX

middle meningeal artery is the largest and the most important artery supplyingmainly dura mater The anatomical variations regarding foramen spinosum arerelated either to incomplete osteogenesis or to abnormal development of the middlemeningeal artery It is believed that the absence of foramen spinosum in the presenceof normal foramen ovale reflects anomalous formation of the middle meningealartery (Shapiro amp Robinson 1967) The absence of foramen spinosum often accom-panies aplasia of the conventional middle meningeal artery and its substitution withmiddle meningeal artery of ophthalmic origin or persistent stapedial artery wouldalso be expected in such cases (Yang et al 1999 Manjunath 2001) In cases when themiddle meningeal artery arises from the ophthalmic artery it most often enters themiddle cranial fossa through the lateral edge of the superior orbital fissure and rarelythrough a foramen located in the orbital surface of the greater wing of the sphenoidbone In the human anatomical literature this foramen has been referred to as themeningo-orbital foramen the lacrimal foramen the foramen of Hyrtl (H-foramen)the anastomotic foramen and as the stapedial ophthalmo-lacrimal foramen In thecomparative anatomical literature the foramen is known as the cranio-orbital fora-men the sphenofrontal foramen and as the sinus canal foramen However none ofthese terms found their place in the international anatomical nomenclature (Termino-logia Anatomica 1998)

The middle meningeal artery is developed from the stapedial artery which origi-nates as a dorsal branch of the second arch of the internal carotid artery When thestapedial artery is fully developed it possesses three branches ndash supraorbital (supe-rior) infraorbital and mandibular The infraorbital and mandibular branches arisefrom a common stem (ramus inferior) In the 15 mm embryo the common stem isjoined by an anastomosis with the external carotid artery this trunk forming the inter-nal maxillary artery At about the same time the trunk of the stapedial artery atro-phies and transmits its branches to the internal maxillary artery In the 20 mm embryothe supraorbital branch of the stapedial artery gives off a branch which is the middlemeningeal artery and then continues on to the orbit Thus the intracranial part of themiddle meningeal artery is developed at an earlier stage than the extracranial part(Fisher 1913)

The arteries of the orbit except for those directly supplying the eyeball are alsoderived from the superior branch of the embryonic stapedial artery At the 20 mmstage of development the stem of the ophthalmic artery annexes the ramus superiornear the optic nerve Subsequently the connection between the intracranial andintraorbital portions of the ramus superior involutes The intraorbital part of theramus superior along with its lacrimal branch are transformed into the definitivelacrimal artery of the human adult The ramus superior persists into adulthood asthe intracranial part of the middle meningeal artery (Diamond 1991) In adult indi-viduals the anterior branch of the middle meningeal artery often gives off a minoranastomotic ramus (in 96 of individuals according to Lippert amp Reinhard 1985)that enters the orbit to join the lacrimal artery (ramus anastomoticus cum ameningea media) through the superior orbital fissure through the meningo-orbitalforamen or simultaneously through both of them (Gabriele amp Bell 1967 Royle1973 Santo Neto et al 1984 Mysorekar amp Nandedkar 1987 Diamond 1991Georgiou amp Cassell 1991 Manjunath 2000 Patnaik et al 2001 Burkat amp Lemke2005 Erdogmus amp Gosva 2005 Erturk et al 2005 Perrini et al 2007) The branchthat runs through the meningo-orbital foramen is referred to as the meningolacri-

352 Silviya Y Nikolova et al

eschweizerbart_XXX

mal artery while the branch that runs through the lateral end of the superior orbitalfissure is referred to as the sphenoidal artery (Diamond 1991) According to Geor-giou amp Cassell (1992) when a meningo-orbital foramen is present it indicates thepoint where the supraorbital division of the stapedial artery entered the orbital cavity

The ophthalmic origin of the middle meningeal artery involves two separate pro-cesses ldquo1 failure of the proximal intraorbital and retroorbital branches to involuteso that the intracranial segments of the middle meningeal artery remain connectedwith the intraorbital stapedial branches 2 defective involution of the maxillofacialdivision (ramus inferior) of the stapedial artery so that the extracranial segment of themiddle meningeal artery is never formed As a result no connection forms betweenthe maxillary artery and the intracranial segment of the middle meningeal arteryrdquo(Manjunath 2001)

There are no reports of clinical symptoms in cases of ophthalmic origin of themiddle meningeal artery The presence of a middle meningeal artery originatingfrom the persistent stapedial artery is correlated with conductive hearing loss proba-bly attributed to stapes ankylosis because of pulsations of the artery and should beconsidered in the operations of the middle ear (Jaint et al 2004 Kwok et al 2010)Anomalous origin of the middle meningeal artery from the ophthalmic artery is ofsurgical interest because it would be difficult to ligate its main trunk since it will notbe found in its normal place compared to the conventional middle meningeal arterylocated in the floor of the middle cranial fossa where it would be within easy access(Manjunath 2001)

Because of the tight structural relationship between the inner table of the vault andthe brain the endocranial surface is a useful record of the pre-existent soft tissuesuch as the arterial networks and the venous drainage (Bruner 2003) The endocranialgrooves are impressed by the veins but also indicate the position of the arteries asthey lie upon the cerebral aspect of the veins (Wood Jones 1912)

The aim of this study is to identify and describe the cases of absence of foramenspinosum to trace the connection between its absence the presence or absence of themeningo-orbital foramen and the related possible aberration in the origin and thecourse of the conventional middle meningeal artery The most probable origin andcourse of the middle meningeal artery in our cases of absence of foramen spinosumare described and discussed in the context of the endocranial meningeal grooves

Material and methodsThe skulls examined in this study belong to adult individuals of both sexes They were condi-tionally grouped into three cranial series ndash contemporary male medieval male and medievalfemale series

The contemporary male cranial series includes 200 almost completely preserved skulls ofadult individuals aged between 20ndash43 years from the ossuary of the Bulgarian NationalMuseum of Military History who died in the wars from the beginning of the 20th century

The medieval male and female cranial series consist of the bone material from medievalnecropoles available at the Institute of Experimental Morphology Pathology and Anthropol-ogy with museum (IEMPAM) Bulgarian Academy of Sciences (BAS)

The data on the age and sex of the individuals from the medieval cranial series wereobtained from previous research at IEMPAM BAS and were provided by Yordanov Age andsex were determined using metric and morphological features of the skulls and the bones of

Absence of foramen spinosum and abnormal middle meningeal artery 353

eschweizerbart_XXX

the postcranial skeleton (Gerasimov 1955 Martin amp Saller 1957 Nikityuk 1960 Pashkova1961 Alekseev amp Debets 1964)

Plastic endocranial casts were made of Stomaflex Putty Silicon impression material bySpofaDental for additional visualization and documentation of the intracranial meningealgrooves in the middle cranial fossa

ResultsThe complete absence of foramen spinosum without any trace of its fusion with fora-men ovale was found only among the medieval male and female series (Table 1)There were no cases of bilateral absence of foramen spinosum Absence of foramenspinosum was established in 1 (070 ) male and in 1 (072 ) female skull on theright side and in 3 (213 ) female skulls on the left side In 1 (072 ) female skullan atypically located small foramen spinosum was established on the right side Themeningo-orbital foramen was missing in all of the cases with one exception ndash a skullin which the absence of foramen spinosum on the left side was accompanied by thepresence of an opening located on the orbital plate of the frontal bone

Description of the cases

Case 1 (female adultus 20ndash25)

Foramen spinosum was absent unilaterally on the left side (Fig 1) The meningealgroove on the inner cranial surface started from the lateral edge of the superior orbitalfissure (Fig 2d) On the orbital plate of the frontal bone laterally from the superiororbital fissure an opening was established (Fig 3) It was located 13 mm away fromthe lateral corner of the superior orbital fissure 5 mm above the edge of the spheno-frontal suture at a distance of 23 mm from the frontozygomatic suture and 29 mmfrom the supraorbital notch The opening was with one entrance and then split andcontinued as two separated canals The superior canal opened into the anterior cranialfossa and a small groove started from it (Fig 4) The inferior canal opened into themiddle cranial fossa 8 mm laterally to the lateral edge of the superior orbital fissureand below the lesser wing of the sphenoid bone

Table 1 Foramen spinosum absence among the investigated cranial series

Foramenspinosum

Medieval femaleseries

Medieval maleseries

Contemporary maleseries

Right Left Right Left Right Leftn n n n n n

absence 1 072 3 213 1 070 0 000 0 000 0 000small foramen 1 072 0 000 0 000 0 000 0 000 0 000total 139 141 143 136 200 200individuals 131 126 200Total ndash a total number of investigated skulls on the right side and on the left sideIndividuals ndash a total number of skulls in which the feature is simultaneously investigat-ed on both sides

354 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 1 Case 1 absence of foramen spinosum on the left side FO ndash foramen ovale Scale bar= 5 mm (corresponds to the length of foramen ovale)

Case 2 (female adultus 25ndash30) Case 3 (female maturus 40ndash45) Case 4(female adultus 25ndash30) Case 5 (male maturus 50ndash55)

Cases 2 3 4 and 5 were similar Foramen spinosum was absent unilaterally in allspecimens ndash in cases 2 3 and 4 on the left side (Figs 5ndash8) and in case 5 on the rightside On the inner cranial surface the meningeal groove started from the lateral edgeof the superior orbital fissure (Fig 2b)

Case 6 (female adultus 30ndash35)

Foramen spinosum on the right side was small and located significantly more posteri-orly and laterally compared to its normal position in relation to foramen ovale (adja-cent to the sphenosquamosal suture at the level of the mandibular fossa) (Fig 9) Thissmall foramen spinosum opened behind foramen ovale on the inner cranial surfaceand a small groove started from it After a short passage this groove fused with a sig-nificantly larger one which started from the lateral edge of the superior orbital fissure(Fig 2c)

Absence of foramen spinosum and abnormal middle meningeal artery 355

eschweizerbart_XXX

Fig 2 Plastic casts of the meningeal grooves in the middle cranial fossa Scale bar = 10 mma) prints from foramen spinosum (FS) and the groove from the conventional middle menin-geal artery starting from it (case 2 on the right side) and the orbital branch of middle menin-geal artery entering the superior orbital fissure (SOF) b) absence of FS and middle menin-geal artery passing through the SOF (case 2 on the left side) c) prints of small and atypicallylocated FS through which passes a small vessel and middle meningeal artery of ophthalmicorigin entering middle cranial fossa through SOF (case 6 on the right side) d) absence of FSand middle meningeal artery of ophthalmic origin in case 1 on the left side

DiscussionIn all 3 cranial series investigated in the present study the absence of foramen spino-sum is established only among the medieval male and female series The absence offoramen spinosum often accompanies aplasia of the conventional middle meningealartery and its substitution with middle meningeal artery of ophthalmic origin

In comparative and evolutionary aspects in humans the middle meningeal arteryenters the cranium through the foramen spinosum whereas in great apes the middlemeningeal artery can enters the cranium through foramen spinosum through fora-men ovale or through petrosphenoid fissure (Kunz amp Iliadis 2007) The middle men-ingeal artery is generally formed by three branches anterior (bregmatic) middle(obelic) and posterior (lambdatic) The most applied classification is the Adachi sys-tem (1928) based on the derivation of the obelic branch In great apes the Adachipattern system cannot be used as both orbital and middle meningeal vessels supplythe middle cranial fossa In great apes there are eight patterns (A1-4 E1-4) for thedifferent types of blood supply (Kunz amp Iliadis 2007)

356 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 3 An opening on the orbital plate of the left frontal bone in case 1 with one entrancewhich splits in two separated canals Scale bar = 13 mm (corresponds to the distance from theinferior canal to the superior orbital fissure)

Fig 4 Case 1 a superior canal opens into the anterior cranial fossa with a small groove start-ing from it Scale bar = 10 mm (corresponds to the length of the groove in a straight line)

Absence of foramen spinosum and abnormal middle meningeal artery 357

eschweizerbart_XXX

Fig 5 Case 2 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 6 Case 3 absence of FS on the left side Scale bar = 7 mm (corresponds to the length offoramen ovale)

358 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

mal artery while the branch that runs through the lateral end of the superior orbitalfissure is referred to as the sphenoidal artery (Diamond 1991) According to Geor-giou amp Cassell (1992) when a meningo-orbital foramen is present it indicates thepoint where the supraorbital division of the stapedial artery entered the orbital cavity

The ophthalmic origin of the middle meningeal artery involves two separate pro-cesses ldquo1 failure of the proximal intraorbital and retroorbital branches to involuteso that the intracranial segments of the middle meningeal artery remain connectedwith the intraorbital stapedial branches 2 defective involution of the maxillofacialdivision (ramus inferior) of the stapedial artery so that the extracranial segment of themiddle meningeal artery is never formed As a result no connection forms betweenthe maxillary artery and the intracranial segment of the middle meningeal arteryrdquo(Manjunath 2001)

There are no reports of clinical symptoms in cases of ophthalmic origin of themiddle meningeal artery The presence of a middle meningeal artery originatingfrom the persistent stapedial artery is correlated with conductive hearing loss proba-bly attributed to stapes ankylosis because of pulsations of the artery and should beconsidered in the operations of the middle ear (Jaint et al 2004 Kwok et al 2010)Anomalous origin of the middle meningeal artery from the ophthalmic artery is ofsurgical interest because it would be difficult to ligate its main trunk since it will notbe found in its normal place compared to the conventional middle meningeal arterylocated in the floor of the middle cranial fossa where it would be within easy access(Manjunath 2001)

Because of the tight structural relationship between the inner table of the vault andthe brain the endocranial surface is a useful record of the pre-existent soft tissuesuch as the arterial networks and the venous drainage (Bruner 2003) The endocranialgrooves are impressed by the veins but also indicate the position of the arteries asthey lie upon the cerebral aspect of the veins (Wood Jones 1912)

The aim of this study is to identify and describe the cases of absence of foramenspinosum to trace the connection between its absence the presence or absence of themeningo-orbital foramen and the related possible aberration in the origin and thecourse of the conventional middle meningeal artery The most probable origin andcourse of the middle meningeal artery in our cases of absence of foramen spinosumare described and discussed in the context of the endocranial meningeal grooves

Material and methodsThe skulls examined in this study belong to adult individuals of both sexes They were condi-tionally grouped into three cranial series ndash contemporary male medieval male and medievalfemale series

The contemporary male cranial series includes 200 almost completely preserved skulls ofadult individuals aged between 20ndash43 years from the ossuary of the Bulgarian NationalMuseum of Military History who died in the wars from the beginning of the 20th century

The medieval male and female cranial series consist of the bone material from medievalnecropoles available at the Institute of Experimental Morphology Pathology and Anthropol-ogy with museum (IEMPAM) Bulgarian Academy of Sciences (BAS)

The data on the age and sex of the individuals from the medieval cranial series wereobtained from previous research at IEMPAM BAS and were provided by Yordanov Age andsex were determined using metric and morphological features of the skulls and the bones of

Absence of foramen spinosum and abnormal middle meningeal artery 353

eschweizerbart_XXX

the postcranial skeleton (Gerasimov 1955 Martin amp Saller 1957 Nikityuk 1960 Pashkova1961 Alekseev amp Debets 1964)

Plastic endocranial casts were made of Stomaflex Putty Silicon impression material bySpofaDental for additional visualization and documentation of the intracranial meningealgrooves in the middle cranial fossa

ResultsThe complete absence of foramen spinosum without any trace of its fusion with fora-men ovale was found only among the medieval male and female series (Table 1)There were no cases of bilateral absence of foramen spinosum Absence of foramenspinosum was established in 1 (070 ) male and in 1 (072 ) female skull on theright side and in 3 (213 ) female skulls on the left side In 1 (072 ) female skullan atypically located small foramen spinosum was established on the right side Themeningo-orbital foramen was missing in all of the cases with one exception ndash a skullin which the absence of foramen spinosum on the left side was accompanied by thepresence of an opening located on the orbital plate of the frontal bone

Description of the cases

Case 1 (female adultus 20ndash25)

Foramen spinosum was absent unilaterally on the left side (Fig 1) The meningealgroove on the inner cranial surface started from the lateral edge of the superior orbitalfissure (Fig 2d) On the orbital plate of the frontal bone laterally from the superiororbital fissure an opening was established (Fig 3) It was located 13 mm away fromthe lateral corner of the superior orbital fissure 5 mm above the edge of the spheno-frontal suture at a distance of 23 mm from the frontozygomatic suture and 29 mmfrom the supraorbital notch The opening was with one entrance and then split andcontinued as two separated canals The superior canal opened into the anterior cranialfossa and a small groove started from it (Fig 4) The inferior canal opened into themiddle cranial fossa 8 mm laterally to the lateral edge of the superior orbital fissureand below the lesser wing of the sphenoid bone

Table 1 Foramen spinosum absence among the investigated cranial series

Foramenspinosum

Medieval femaleseries

Medieval maleseries

Contemporary maleseries

Right Left Right Left Right Leftn n n n n n

absence 1 072 3 213 1 070 0 000 0 000 0 000small foramen 1 072 0 000 0 000 0 000 0 000 0 000total 139 141 143 136 200 200individuals 131 126 200Total ndash a total number of investigated skulls on the right side and on the left sideIndividuals ndash a total number of skulls in which the feature is simultaneously investigat-ed on both sides

354 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 1 Case 1 absence of foramen spinosum on the left side FO ndash foramen ovale Scale bar= 5 mm (corresponds to the length of foramen ovale)

Case 2 (female adultus 25ndash30) Case 3 (female maturus 40ndash45) Case 4(female adultus 25ndash30) Case 5 (male maturus 50ndash55)

Cases 2 3 4 and 5 were similar Foramen spinosum was absent unilaterally in allspecimens ndash in cases 2 3 and 4 on the left side (Figs 5ndash8) and in case 5 on the rightside On the inner cranial surface the meningeal groove started from the lateral edgeof the superior orbital fissure (Fig 2b)

Case 6 (female adultus 30ndash35)

Foramen spinosum on the right side was small and located significantly more posteri-orly and laterally compared to its normal position in relation to foramen ovale (adja-cent to the sphenosquamosal suture at the level of the mandibular fossa) (Fig 9) Thissmall foramen spinosum opened behind foramen ovale on the inner cranial surfaceand a small groove started from it After a short passage this groove fused with a sig-nificantly larger one which started from the lateral edge of the superior orbital fissure(Fig 2c)

Absence of foramen spinosum and abnormal middle meningeal artery 355

eschweizerbart_XXX

Fig 2 Plastic casts of the meningeal grooves in the middle cranial fossa Scale bar = 10 mma) prints from foramen spinosum (FS) and the groove from the conventional middle menin-geal artery starting from it (case 2 on the right side) and the orbital branch of middle menin-geal artery entering the superior orbital fissure (SOF) b) absence of FS and middle menin-geal artery passing through the SOF (case 2 on the left side) c) prints of small and atypicallylocated FS through which passes a small vessel and middle meningeal artery of ophthalmicorigin entering middle cranial fossa through SOF (case 6 on the right side) d) absence of FSand middle meningeal artery of ophthalmic origin in case 1 on the left side

DiscussionIn all 3 cranial series investigated in the present study the absence of foramen spino-sum is established only among the medieval male and female series The absence offoramen spinosum often accompanies aplasia of the conventional middle meningealartery and its substitution with middle meningeal artery of ophthalmic origin

In comparative and evolutionary aspects in humans the middle meningeal arteryenters the cranium through the foramen spinosum whereas in great apes the middlemeningeal artery can enters the cranium through foramen spinosum through fora-men ovale or through petrosphenoid fissure (Kunz amp Iliadis 2007) The middle men-ingeal artery is generally formed by three branches anterior (bregmatic) middle(obelic) and posterior (lambdatic) The most applied classification is the Adachi sys-tem (1928) based on the derivation of the obelic branch In great apes the Adachipattern system cannot be used as both orbital and middle meningeal vessels supplythe middle cranial fossa In great apes there are eight patterns (A1-4 E1-4) for thedifferent types of blood supply (Kunz amp Iliadis 2007)

356 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 3 An opening on the orbital plate of the left frontal bone in case 1 with one entrancewhich splits in two separated canals Scale bar = 13 mm (corresponds to the distance from theinferior canal to the superior orbital fissure)

Fig 4 Case 1 a superior canal opens into the anterior cranial fossa with a small groove start-ing from it Scale bar = 10 mm (corresponds to the length of the groove in a straight line)

Absence of foramen spinosum and abnormal middle meningeal artery 357

eschweizerbart_XXX

Fig 5 Case 2 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 6 Case 3 absence of FS on the left side Scale bar = 7 mm (corresponds to the length offoramen ovale)

358 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

the postcranial skeleton (Gerasimov 1955 Martin amp Saller 1957 Nikityuk 1960 Pashkova1961 Alekseev amp Debets 1964)

Plastic endocranial casts were made of Stomaflex Putty Silicon impression material bySpofaDental for additional visualization and documentation of the intracranial meningealgrooves in the middle cranial fossa

ResultsThe complete absence of foramen spinosum without any trace of its fusion with fora-men ovale was found only among the medieval male and female series (Table 1)There were no cases of bilateral absence of foramen spinosum Absence of foramenspinosum was established in 1 (070 ) male and in 1 (072 ) female skull on theright side and in 3 (213 ) female skulls on the left side In 1 (072 ) female skullan atypically located small foramen spinosum was established on the right side Themeningo-orbital foramen was missing in all of the cases with one exception ndash a skullin which the absence of foramen spinosum on the left side was accompanied by thepresence of an opening located on the orbital plate of the frontal bone

Description of the cases

Case 1 (female adultus 20ndash25)

Foramen spinosum was absent unilaterally on the left side (Fig 1) The meningealgroove on the inner cranial surface started from the lateral edge of the superior orbitalfissure (Fig 2d) On the orbital plate of the frontal bone laterally from the superiororbital fissure an opening was established (Fig 3) It was located 13 mm away fromthe lateral corner of the superior orbital fissure 5 mm above the edge of the spheno-frontal suture at a distance of 23 mm from the frontozygomatic suture and 29 mmfrom the supraorbital notch The opening was with one entrance and then split andcontinued as two separated canals The superior canal opened into the anterior cranialfossa and a small groove started from it (Fig 4) The inferior canal opened into themiddle cranial fossa 8 mm laterally to the lateral edge of the superior orbital fissureand below the lesser wing of the sphenoid bone

Table 1 Foramen spinosum absence among the investigated cranial series

Foramenspinosum

Medieval femaleseries

Medieval maleseries

Contemporary maleseries

Right Left Right Left Right Leftn n n n n n

absence 1 072 3 213 1 070 0 000 0 000 0 000small foramen 1 072 0 000 0 000 0 000 0 000 0 000total 139 141 143 136 200 200individuals 131 126 200Total ndash a total number of investigated skulls on the right side and on the left sideIndividuals ndash a total number of skulls in which the feature is simultaneously investigat-ed on both sides

354 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 1 Case 1 absence of foramen spinosum on the left side FO ndash foramen ovale Scale bar= 5 mm (corresponds to the length of foramen ovale)

Case 2 (female adultus 25ndash30) Case 3 (female maturus 40ndash45) Case 4(female adultus 25ndash30) Case 5 (male maturus 50ndash55)

Cases 2 3 4 and 5 were similar Foramen spinosum was absent unilaterally in allspecimens ndash in cases 2 3 and 4 on the left side (Figs 5ndash8) and in case 5 on the rightside On the inner cranial surface the meningeal groove started from the lateral edgeof the superior orbital fissure (Fig 2b)

Case 6 (female adultus 30ndash35)

Foramen spinosum on the right side was small and located significantly more posteri-orly and laterally compared to its normal position in relation to foramen ovale (adja-cent to the sphenosquamosal suture at the level of the mandibular fossa) (Fig 9) Thissmall foramen spinosum opened behind foramen ovale on the inner cranial surfaceand a small groove started from it After a short passage this groove fused with a sig-nificantly larger one which started from the lateral edge of the superior orbital fissure(Fig 2c)

Absence of foramen spinosum and abnormal middle meningeal artery 355

eschweizerbart_XXX

Fig 2 Plastic casts of the meningeal grooves in the middle cranial fossa Scale bar = 10 mma) prints from foramen spinosum (FS) and the groove from the conventional middle menin-geal artery starting from it (case 2 on the right side) and the orbital branch of middle menin-geal artery entering the superior orbital fissure (SOF) b) absence of FS and middle menin-geal artery passing through the SOF (case 2 on the left side) c) prints of small and atypicallylocated FS through which passes a small vessel and middle meningeal artery of ophthalmicorigin entering middle cranial fossa through SOF (case 6 on the right side) d) absence of FSand middle meningeal artery of ophthalmic origin in case 1 on the left side

DiscussionIn all 3 cranial series investigated in the present study the absence of foramen spino-sum is established only among the medieval male and female series The absence offoramen spinosum often accompanies aplasia of the conventional middle meningealartery and its substitution with middle meningeal artery of ophthalmic origin

In comparative and evolutionary aspects in humans the middle meningeal arteryenters the cranium through the foramen spinosum whereas in great apes the middlemeningeal artery can enters the cranium through foramen spinosum through fora-men ovale or through petrosphenoid fissure (Kunz amp Iliadis 2007) The middle men-ingeal artery is generally formed by three branches anterior (bregmatic) middle(obelic) and posterior (lambdatic) The most applied classification is the Adachi sys-tem (1928) based on the derivation of the obelic branch In great apes the Adachipattern system cannot be used as both orbital and middle meningeal vessels supplythe middle cranial fossa In great apes there are eight patterns (A1-4 E1-4) for thedifferent types of blood supply (Kunz amp Iliadis 2007)

356 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 3 An opening on the orbital plate of the left frontal bone in case 1 with one entrancewhich splits in two separated canals Scale bar = 13 mm (corresponds to the distance from theinferior canal to the superior orbital fissure)

Fig 4 Case 1 a superior canal opens into the anterior cranial fossa with a small groove start-ing from it Scale bar = 10 mm (corresponds to the length of the groove in a straight line)

Absence of foramen spinosum and abnormal middle meningeal artery 357

eschweizerbart_XXX

Fig 5 Case 2 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 6 Case 3 absence of FS on the left side Scale bar = 7 mm (corresponds to the length offoramen ovale)

358 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 1 Case 1 absence of foramen spinosum on the left side FO ndash foramen ovale Scale bar= 5 mm (corresponds to the length of foramen ovale)

Case 2 (female adultus 25ndash30) Case 3 (female maturus 40ndash45) Case 4(female adultus 25ndash30) Case 5 (male maturus 50ndash55)

Cases 2 3 4 and 5 were similar Foramen spinosum was absent unilaterally in allspecimens ndash in cases 2 3 and 4 on the left side (Figs 5ndash8) and in case 5 on the rightside On the inner cranial surface the meningeal groove started from the lateral edgeof the superior orbital fissure (Fig 2b)

Case 6 (female adultus 30ndash35)

Foramen spinosum on the right side was small and located significantly more posteri-orly and laterally compared to its normal position in relation to foramen ovale (adja-cent to the sphenosquamosal suture at the level of the mandibular fossa) (Fig 9) Thissmall foramen spinosum opened behind foramen ovale on the inner cranial surfaceand a small groove started from it After a short passage this groove fused with a sig-nificantly larger one which started from the lateral edge of the superior orbital fissure(Fig 2c)

Absence of foramen spinosum and abnormal middle meningeal artery 355

eschweizerbart_XXX

Fig 2 Plastic casts of the meningeal grooves in the middle cranial fossa Scale bar = 10 mma) prints from foramen spinosum (FS) and the groove from the conventional middle menin-geal artery starting from it (case 2 on the right side) and the orbital branch of middle menin-geal artery entering the superior orbital fissure (SOF) b) absence of FS and middle menin-geal artery passing through the SOF (case 2 on the left side) c) prints of small and atypicallylocated FS through which passes a small vessel and middle meningeal artery of ophthalmicorigin entering middle cranial fossa through SOF (case 6 on the right side) d) absence of FSand middle meningeal artery of ophthalmic origin in case 1 on the left side

DiscussionIn all 3 cranial series investigated in the present study the absence of foramen spino-sum is established only among the medieval male and female series The absence offoramen spinosum often accompanies aplasia of the conventional middle meningealartery and its substitution with middle meningeal artery of ophthalmic origin

In comparative and evolutionary aspects in humans the middle meningeal arteryenters the cranium through the foramen spinosum whereas in great apes the middlemeningeal artery can enters the cranium through foramen spinosum through fora-men ovale or through petrosphenoid fissure (Kunz amp Iliadis 2007) The middle men-ingeal artery is generally formed by three branches anterior (bregmatic) middle(obelic) and posterior (lambdatic) The most applied classification is the Adachi sys-tem (1928) based on the derivation of the obelic branch In great apes the Adachipattern system cannot be used as both orbital and middle meningeal vessels supplythe middle cranial fossa In great apes there are eight patterns (A1-4 E1-4) for thedifferent types of blood supply (Kunz amp Iliadis 2007)

356 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 3 An opening on the orbital plate of the left frontal bone in case 1 with one entrancewhich splits in two separated canals Scale bar = 13 mm (corresponds to the distance from theinferior canal to the superior orbital fissure)

Fig 4 Case 1 a superior canal opens into the anterior cranial fossa with a small groove start-ing from it Scale bar = 10 mm (corresponds to the length of the groove in a straight line)

Absence of foramen spinosum and abnormal middle meningeal artery 357

eschweizerbart_XXX

Fig 5 Case 2 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 6 Case 3 absence of FS on the left side Scale bar = 7 mm (corresponds to the length offoramen ovale)

358 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 2 Plastic casts of the meningeal grooves in the middle cranial fossa Scale bar = 10 mma) prints from foramen spinosum (FS) and the groove from the conventional middle menin-geal artery starting from it (case 2 on the right side) and the orbital branch of middle menin-geal artery entering the superior orbital fissure (SOF) b) absence of FS and middle menin-geal artery passing through the SOF (case 2 on the left side) c) prints of small and atypicallylocated FS through which passes a small vessel and middle meningeal artery of ophthalmicorigin entering middle cranial fossa through SOF (case 6 on the right side) d) absence of FSand middle meningeal artery of ophthalmic origin in case 1 on the left side

DiscussionIn all 3 cranial series investigated in the present study the absence of foramen spino-sum is established only among the medieval male and female series The absence offoramen spinosum often accompanies aplasia of the conventional middle meningealartery and its substitution with middle meningeal artery of ophthalmic origin

In comparative and evolutionary aspects in humans the middle meningeal arteryenters the cranium through the foramen spinosum whereas in great apes the middlemeningeal artery can enters the cranium through foramen spinosum through fora-men ovale or through petrosphenoid fissure (Kunz amp Iliadis 2007) The middle men-ingeal artery is generally formed by three branches anterior (bregmatic) middle(obelic) and posterior (lambdatic) The most applied classification is the Adachi sys-tem (1928) based on the derivation of the obelic branch In great apes the Adachipattern system cannot be used as both orbital and middle meningeal vessels supplythe middle cranial fossa In great apes there are eight patterns (A1-4 E1-4) for thedifferent types of blood supply (Kunz amp Iliadis 2007)

356 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 3 An opening on the orbital plate of the left frontal bone in case 1 with one entrancewhich splits in two separated canals Scale bar = 13 mm (corresponds to the distance from theinferior canal to the superior orbital fissure)

Fig 4 Case 1 a superior canal opens into the anterior cranial fossa with a small groove start-ing from it Scale bar = 10 mm (corresponds to the length of the groove in a straight line)

Absence of foramen spinosum and abnormal middle meningeal artery 357

eschweizerbart_XXX

Fig 5 Case 2 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 6 Case 3 absence of FS on the left side Scale bar = 7 mm (corresponds to the length offoramen ovale)

358 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 3 An opening on the orbital plate of the left frontal bone in case 1 with one entrancewhich splits in two separated canals Scale bar = 13 mm (corresponds to the distance from theinferior canal to the superior orbital fissure)

Fig 4 Case 1 a superior canal opens into the anterior cranial fossa with a small groove start-ing from it Scale bar = 10 mm (corresponds to the length of the groove in a straight line)

Absence of foramen spinosum and abnormal middle meningeal artery 357

eschweizerbart_XXX

Fig 5 Case 2 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 6 Case 3 absence of FS on the left side Scale bar = 7 mm (corresponds to the length offoramen ovale)

358 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 5 Case 2 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 6 Case 3 absence of FS on the left side Scale bar = 7 mm (corresponds to the length offoramen ovale)

358 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 7 Case 4 absence of FS on the left side Scale bar = 9 mm (corresponds to the length offoramen ovale)

Fig 8 Case 5 absence of FS on the right side Scale bar = 7 mm (corresponds to the lengthof foramen ovale)

Absence of foramen spinosum and abnormal middle meningeal artery 359

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

Fig 9 Case 6 a small and atypically located FS adjacent to the sphenosquamosal suture atthe level of the mandibular fossa (MF) Scale bar = 8 mm (corresponds to the length of fora-men ovale)

Generally in nonhuman primates the anterior meningeal system is associated withthe ophthalmic branch of the internal carotid artery The vessels joining the two sys-tems pass through the additional chanels ndash through the superior orbital fissure (sphe-noidal artery) or through the cranio-orbital foramen (meningolacrimal artery) Ahigh prevalence of this trait is evident in humans and orangs both genera also show-ing a lateral expansion of the superior orbital fissure When the ophthalmic arterysubstitutes the middle meningeal network entirely the foramen spinosum is absentand there are no imprints on the middle fossa as is in the gibbons In general orangsalso show a larger contribution of the orbital system while chimps show a dominanceof the middle meningeal network as described in humans (Diamond 1991 Bruner ampSherkat 2008)

According to the available fossil record gracile Australopithecinae (genus Austra-lopithecus) display two middle meningeal branches a developed anterior (ophthal-mic) vascular system and the superior orbital fissure show a morphology compara-ble with the African apes Compared with anatomically modern humans almost allthe extinct species show very simple meningeal networks at least when consideringtheir endocranial imprints (Bruner amp Sherkat 2008) In some Homo erectus endo-casts (Chinese Homo erectus dated 412 ka) the anterior vascular network has beenhypothesized to be derived from the orbital system namely from the internal carotidartery and not from the middle meningeal vessels (Wu et al 2006) An anteriorbranch which is quite isolated from the posterior system and which originates aroundthe anterior portion of the lateral sulcus (ie possibly entering the endocranium formthe superior orbital fissuremeningo-orbital foramen) can be similarly hypothesized

360 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

for other Afro-European Middle Pleistocene specimens As a whole in evolutionaryaspect as soon as modern cranial morphology becomes fully evolved the middlemeningeal traces show a definite increase in the whole vascularization pattern andanastomoses notably around the parietal surface It is believed that there are twobasic possible functional roles for the middle meningeal vessels oxygenation andthermoregulation Obviously any functional relevance of the middle meningeal ves-sels possibly more exerted in the early life stages must be properly interpretedwithin the endocranial structural context and within the evolutionary and phyloge-netic variation (Bruner amp Sherkat 2008)

In anatomically modern humans the absence of foramen spinosum is usuallyaccompanied with replacement of the conventional middle meningeal artery withsuch arising from the ophthalmic artery system or from a persisting stapedial arteryAccording to Lippert amp Pabst (1985) the frequency of occurrence of a middle men-ingeal artery of ophthalmic origin reflects population specific differences Theauthors state that in skulls of people from Papua for instance foramen spinosum isabsent in about 10 of the cases According to Adachi (1928) foramen spinosum isabsent in 04 (n = 800 hemicrania) of the skulls of people from Japan and in 14 (n = 800 hemicrania) of the Russiansrsquo skulls Ginsberg et al (1994) establishedabsence of foramen spinosum in 32 (n = 123 patients) of the cases they examined

In all 6 cases described in the present study the complete absence of foramen spi-nosum (in 5 cases) or its small size in combination with atypical position (in 1 case)are obviously related with variations in the origin and the course of the conventionalmiddle meningeal artery because there is no groove from its stem on the inner cranialsurface According to Bergman et al (1988) in 99 of the cases the middle menin-geal artery enters the skull through foramen spinosum but when the foramen isabsent the artery enters through foramen ovale along with the mandibular nerve Inall of our cases there was no groove starting from the foramen ovale to indicate pas-sage of the middle meningeal artery as in 2 (n = 1200) cases reported by Chandler ampDerezinski (1935)

In all 5 cases of complete absence of foramen spinosum considered here a groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure similarly to the cases described by Royle ampMotson (1973) Santo Neto et al (1984) and Diamond (1991) In our case of smalland atypically located foramen spinosum (adjacent to the sphenosquamosal suture)in the middle cranial fossa a small groove started from the foramen A larger groovewhich probably housed the stem of the middle meningeal artery started from the lat-eral edge of the superior orbital fissure According to Manjunath (2001) the presenceof a small foramen spinosum also suggests hypoplasia of the conventional middlemeningeal artery and under such circumstances a second source of the meningealblood supply must be sought Curnow (1873) was the first to describe a case of asmall foramen spinosum where the middle meningeal artery was of ophthalmic ori-gin Later Adachi (1928) reported 2 (n = 31) similar cases of small foramen spinosumin European skulls where the meningeal groove started from the orbit According toLindblom (1936) foramen spinosum is small or altogether absent in 04 of thecases mainly when the middle meningeal artery is with ophthalmic origin It isbelieved that the ossification of the posterior border of the greater wing of the sphe-noid bone progressively developed around the middle meningeal artery because thelocation of foramen spinosum was not always confined to the sphenoid bone during

Absence of foramen spinosum and abnormal middle meningeal artery 361

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

the course of human evolution In some earlier species foramen spinosum is found inthe squamous part of the temporal bone or on the sphenosquamosal suture (similar toour case 6) or it is absent (Krayenbuumlhl et al 2008)

There is no groove on the lateral wall of the orbit in all 6 investigated casesAccording to Low (1946) the presence of such a groove from the meningo-orbitalforamen to the inferior orbital fissure and the absence of foramen spinosum indicatethat the middle meningeal artery originates from the third part of the maxillary arteryfrom the infraorbital artery Later Royle (1973) Santo Neto et al (1984) Mysorekaramp Nandedkar (1987) also established the presence of such a groove connecting moreoften the superior orbital fissure and rarely the meningo-orbital foramen with theinferior orbital fissure According to Diamond (1990) this groove marks only thetransition from cancellous to compact bone and has no relation with a vessel in thisarea

In case 1 along with the absence of foramen spinosum we observed an openingon the orbital plate of the frontal bone The distances measured between the openingand fixed points (superior orbital fissure frontozygomatic suture and supraorbitalnotch) are comparable to those established by Jovanovic et al (2003) Kwiatkowskiet al (2003) Perrini et al (2007) Krishnamurthy et al (2008) In this case it is mostlikely that the meningeal branch which usually pierces the orbital plate of the frontalbone and supplies the anterior cranial fossa passed through the superior canal of theopening The meningeal branch is a feature restricted to hominids In humans themeningeal foramen through which this branch passes is found in 19 (n = 410) ofthe investigated cases (Diamond 1991) OrsquoBrien amp McDonald (2007) reported twocases in which the meningo-orbital foramen communicated with the anterior cranialfossa and both were associated with a more posterior foramen that communicatedwith the middle cranial fossa In our case there was no such connection The inferiorcanal probably corresponds to the meningo-orbital foramen and the meningolacrimalartery passes through it In this case the canal is too small to have transmitted anartery large enough to supply the territory covered by the meningeal grooves This isconfirmed by the presence of a large groove emerging through the lateral edge of thesuperior orbital fissure ie in this case despite of the presence of the meningo-orbitalforamen and the meningolacrimal artery passing through it the middle meningealartery passed through the superior orbital fissure and the sphenoidal artery wasenlarged as observed in the 2 (n = 638 hemicrania) similar cases reported by Dia-mond (1991)

An ophthalmic origin for the middle meningeal artery is easily detected in skullswhich exhibit one or both of the following characteristics 1 absence or extremereduction of foramen spinosum 2 absence attenuation or interruption of the mainstem sulcus that courses anterosuperiorly from the floor of the middle cranial fossaCorrespondingly some or all of the middle meningeal grooves are found to emergefrom the lateral corner of the superior orbital fissure (Diamond 1991) Therefore themiddle meningeal artery in all 6 studied cases was probably of ophthalmic origin andthe sphenoidal artery was enlarged

In most of the cases similar to the ones presented here the authors state that themiddle meningeal artery is of ophthalmic origin but rarely specify whether it arisesas a branch directly from the ophthalmic artery stem or from the lacrimal artery ierepresents an enlarged channel of otherwise normally occurring anastomosisbetween the middle meningeal artery and the lacrimal artery (sphenoidal and menin-

362 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

golacrimal artery) According to Diamond (1991) the sphenoidal artery usually joinsthe definitive lacrimal artery close to the optic nerve so that only a short segmentseparates it from the stem of the ophthalmic artery Sometimes the point at which thesphenoidal artery anastomoses with the definitive lacrimal artery and the point atwhich the primitive ophthalmic artery stem annexes the ramus supraorbitalis coin-cide so that the sphenoidal artery appears to join directly the stem of the ophthalmicartery According to Perrini et al (2007) the anastomosis between the recurrent men-ingeal artery ie sphenoidal artery and the lacrimal artery is located in the apex ofthe superior orbital fissure In cases of absence of foramen spinosum and ophthalmicorigin of the middle meningeal artery the sphenoidal artery is more often theenlarged vessel as probably was in our cases too So in such cases it would be mostlikely that the middle meningeal artery arose from the lacrimal artery close to theophthalmic artery stem near the apex of the superior orbital fissure rather thandirectly from the stem itself On the basis of the intracranial meningeal groovesobserved in our cases we can hypothesize that the middle meningeal artery was withophthalmic origin and the sphenoidal artery was the enlarged channel but we cannotspecify whether the artery arose from the lacrimal artery or directly from the ophthal-mic artery stem

Here arises the question why in the cases where foramen spinosum is absent andthe ophthalmic artery supplies one or all of the branches of the middle meningealartery most often the sphenoidal artery is enlarged and enters the middle cranialfossa through the superior orbital fissure Meanwhile the meningo-orbital foramen ismissing along with the meningolacrimal artery passing through it If the involutionfails to occur the connection between the intraorbital and intracranial part of ramussuperior of the stapedial artery is preserved (Manjunath 2001) and if the meningolac-rimal artery is homologous with the ramus superior (Diamond 1991 Georgiou ampCassell 1992) it would be expected that exactly the meningolacrimal artery shouldbe enlarged in order to supply the middle meningeal artery but there are few similarreports in the literature (Greig 1929 Toumlndury 1934 McLennan et al 1974) It is alsoobvious that when foramen spinosum is absent and both the meningolacrimal and thesphenoidal artery are present the preferred course of the middle meningeal arterywould be through the superior orbital fissure and the sphenoidal artery is enlarged(Diamond 1991 case 1)

In many primates the ophthalmic artery supplies ramus superior of the stapedialartery andor its meningeal branches and the route taken is via ramus supraorbitalisand trough the meningo-orbital foramen The fact that humans rely on a differentroute suggests that due to haemodynamic or developmental constraints they madeuse of a neomorphic channel (sphenoidal artery) (Diamond 1991) According toGeorgiou amp Cassell (1992) the meningo-orbital foramen represents the path of thesupraorbital branch of the stapedial artery but the branching point of the artery (giv-ing off the proximal part of the lacrimal artery) at a position in embryo which corre-sponds to the adult middle cranial fossa alleviates the necessity of proposing a neo-morphic vessel (for the sphenoidal artery) The authors believed that since the greaterwing of the sphenoid bone had not ossified the position of the meningo-orbital fora-men would vary in accordance to the position of the supraorbital division of the sta-pedial artery Variations in the medio-lateral position with respect to the superiororbital fissure determine whether the supraorbital branch will pass through it(medial position) or the meningo-orbital foramen will be formed (lateral position) or

Absence of foramen spinosum and abnormal middle meningeal artery 363

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

in intermediate situations a ldquohalf rdquo meningo-orbital foramen will appear (meningo-orbital foramen fused with the superior orbital fissure) Due to the variations in thecranio-caudal position in which the supraorbital division enters the orbit the proxi-mal portion of the lacrimal artery or a part of it may be located within the orbit ormiddle cranial fossa According to the theory of Georgiou amp Cassel (1992) themedial position of the supraorbital division could explain the course of the middlemeningeal artery through the superior orbital fissure when it originates from the oph-thalmic artery and the meningo-orbital foramen is absent Still remains the questionwhy in cases identical to our case 1 where there is simultaneous presence of both themeningolacrimal and the sphenoidal artery the middle meningeal arteryrsquos course isagain through the superior orbital fissure An intracranial point of branching of thesupraorbital division ie giving off the lacrimal branch intracranially would explainthis variation but in this case the meningolacrimal artery would represents the lacri-mal branch which enters through the meningo-orbital foramen and then the sphenoi-dal artery would represent the continuation of ramus supraorbitalis This contradictsthe assertion that the meningo-orbital foramen represents the path of the supraorbitaldivision of the embryonic stapedial artery (Diamond 1991 Georgiou amp Cassell1992) Moreover according to Diamond (1991) ramus superior has never beenshown to give off the lacrimal branch outside the orbit in placental mammals Thelacrimal branch always arises within the orbit from ramus supraorbitalis or its deriva-tive Comparative anatomy provides extensive embryological and phylogenetical evi-dence that the meningolacrimal artery is homologous with ramus superior of theembryologically and phylogenetically primitive stapedial artery (Diamond 1991Georgiou amp Cassell 1992) Obviously the described mechanism by which this varia-tion arises is not fully understood and further studies are needed for its clarification

It can be inferred that in our cases the absence of foramen spinosum and the pres-ence of a small and atypically located foramen reflect variations in the origin and thecourse of the conventional middle meningeal artery In these cases the middle menin-geal artery probably was of ophthalmic origin and the sphenoidal artery was theenlarged channel which passes through the lateral edge of the superior orbital fissureand gives off the branches of the middle meningeal artery after entering the middlecranial fossa

AcknowledgementsThe authors thank Nina Petkova and Elena Petrova for technical assistance

ReferencesAdachi B (1928) Das Arteriensystem der Japaner Band 1 ndash Verlag der Kaiserlich Japani-

schen Universitaumlt zu Kyoto KyotoAlekseev VP amp Debets GF (1964) Kraniometriya ndash Nauka MoskvaBergman RA Thompson SA Afifi AK amp Saadeh FA (1988) Compendium of

Human Anatomic Variations Text Atlas and World Literature ndash Urban amp Schwarzen-berg Baltimore-Munich

Bruner E (2003) Fossil traces of the human thought paleoneurology and the evolution ofthe genus Homo ndash J Anthropol Sci 81 29ndash56

Bruner E amp Sherkat S (2008) The middle meningeal artery from clinics to fossils ndashChilds Nerv Syst 24 1289ndash1298

364 Silviya Y Nikolova et al

eschweizerbart_XXX

Burkat CN amp Lemke BN (2005) Anatomy of the orbit and its related structures ndash Otola-ryngol Clin N Am 38 825ndash856

Chandler SB amp Derezinski CF (1935) The variations of the middle meningeal artery inthe middle cranial fossa ndash Anat Rec 62 309ndash319

Curnow J (1873) Two instances of irregular ophthalmic and middle meningeal arteries ndash JAnat Physiol 8 155ndash156

Diamond MK (1990) The groove in the orbital face of the greater wing of the sphenoid Anew interpretation ndash J Anat 173 97ndash99

Diamond MK (1991) Homologies of the meningeal-orbital arteries of humans a reap-praisal ndash J Anat 178 223ndash241

Erdogmus S amp Govsa F (2005) Importance of the anatomic features of the lacrimal arteryfor orbital approaches ndash J Craniofac Surg 16 957ndash964

Erturk M Kayalioglu G Govsa F Varol T amp Ozgur T (2005) The cranio-orbital fora-men the groove on the lateral wall of the human orbit and the orbital branch of the middlemeningeal artery ndash Clin Anat 18 10ndash14

Fisher AGT (1913) A case of complete absence of both internal carotid arteries with apreliminary note on the developmental history of the stapedial artery ndash J Anat Physiol48 37ndash46

Gabriele OF amp Bell D (1967) Ophthalmic origin of the middle meningeal artery ndash Radiol-ogy 89 841ndash844

Georgiou C amp Cassell MD (1992) The foramen meningo-orbitale and its relationship tothe development of the ophthalmic artery ndash J Anat 180 119ndash125

Gerasimov MM (1955) Vosstanovlenie litsa po cherepu ndash MoskvaGinsberg LE Prett SW Chen MY amp Elster AD (1994) Skull-base foramina of the

middle cranial fossa reassessment of normal variation with high-resolution CT ndash Am JNeuroradiol 15 283ndash291

Greig DM (1929) Congenital anomalies of the foramen spinosum ndash Edinburgh Med J 3363ndash37l

Jain R Gandhi D Gujar S amp Mukherji S (2004) Case 67 Persistent Stapedial Artery ndashRadiology 230 413ndash416

Jovanovic I Vasovic L Ugrenovic S Zdravkovic D Vlajkovic S Dakovic-BjelakovicM amp Stojanovic V (2003) Variable foramen of Hyrtl of the human skull ndash Acta MedMediane 42 1ndash5

Krayenbuumlhl N Isolan GR amp Al-Mefty O (2008) The foramen spinosum a landmark inmiddle fossa surgery ndash Neurosurg Rev 31 397ndash402

Krishnamurthy A Nayak SR Prabhu LV Mansur DI Ramanathan L Madhyastha Samp Saralaya V (2008) The morphology of meningo-orbital foramen in south Indian popu-lation ndash Bratisl Lek Listy 109 517ndash519

Kunz AR amp Iliadis C (2007) Hominid evolution of the arteriovenous system through thecranial base and its relevance for craniosynostosis ndash Childs Nerv Syst 23 1367ndash1377

Kwiatkowski J Wysocki J amp Nitek S (2003) The morphology and morphometry of theso-called ldquomeningo-orbital foramenrdquo in humans ndash Folia Morphol (Warsz) 62 323ndash325

Kwok KY Lo SSM Tsang TK Fang TW amp Kwan TW (2010) Persistant stapedialartery computed tomography and magnetic resonance imaging features ndash Hong KongCollege of Radiologists 12 139ndash142

Lindblom K (1936) A roentgenographic study of the vascular channels of the skull withspecial reference to intracranial tumors and arteriovenous aneurysms ndash Acta Radiol(Suppl) (Stockholm) 30 1ndash146

Lippert H amp Pabst R (1985) Arterial Variations in Man Classification and Frequency ndashJF Bergmann Munich

Low FN (1946) An anomalous middle meningeal artery ndash Anat Rec 95 347ndash351Manjunath KY (2000) The course relations and the branching pattern of the middle men-

ingeal artery in South Indians ndash Anat Soc India 49 133ndash138

Absence of foramen spinosum and abnormal middle meningeal artery 365

eschweizerbart_XXX

Manjunath KY (2001) Anomalous origin of the middle meningeal artery ndash a review ndashAnat Soc India 50 179ndash183

McLennan JE Rosenbaum AE amp Haughton VM (1974) Internal carotid origins of themiddle meningeal artery ndash Neuroradiology 7 265ndash275

Martin R amp Saller K (1957) Lehrbuch der Anthropologie in systematischer DarstellungBand I ndash Gustav Fischer Verlag Stuttgart

Mysorekar VR amp Nandedkar AN (1987) Anatomical note The groove in the lateral wallof the human orbit ndash J Anat 151 255ndash257

Nikityuk BA (1960) Opredelenie pola po skeletu i zubam cheloveka ndash Voprosi antropolo-gii 3 135ndash139

OrsquoBrien A amp McDonald SW (2007) The meningo-orbital foramen in a Scottish popula-tion ndash Clin Anat 20 880ndash885

Pashkova V (1961) Kraniometriya kak odin iz metodov povisheniya dostovernosti opredele-niya pola po cherepu ndash Voprosi antropologii 7 95ndash101

Patnaik VVG Bala Sanju amp Rajan SK (2001) Anatomy of the bony orbit-some appliedaspects ndash J Anat Soc India 50 59ndash67

Perrini P Cardia A Fraser K amp Lanzino G (2007) A microsurgical study of the anatomyand course of the ophthalmic artery and its possibly dangerous anastomoses ndash J Neuro-surg 106 142ndash150

Royle G (1973) A groove in the lateral wall of the orbit ndash J Anat 115 461ndash465Royle G amp Motson R (1973) Anomalous origin of the middle meningeal artery ndash J Neu-

rol Neurosurg Psychiatr 36 874ndash 876Santo Neto H Penteado CV amp De Carvalho VC (1984) Presence of a groove in the lat-

eral wall of the human orbit ndash J Anat 138 631ndash633Shapiro R amp Robinson F (1967) The foramina of the middle fossa a phylogenetic ana-

tomic and pathologic study ndash Am J Roentgenol 101 779ndash794Terminologia Anatomica International Anatomical Terminology (1998) Federative Com-

mittee of Anatomical Terminology ndash Georg Thieme Verlag StuttgartToumlndury G (1934) Einseitiges Fehlen der A carotis interna ndash Gegenbaurs Morphol Jb 74

625ndash638Wood Jones F (1912) On the grooves upon the ossa parietalia commonly said to be caused

by the arteria meningea media ndash J Anat Physiol 46 228ndash238Wu W Schepartz LA Folk D amp Liu W (2006) Endocranial Cast of Hexian Homo erec-

tus from South China ndash Am J Phys Anthropol 130 445ndash454Yang CM Huang KM amp Li YW (1999) Ophthalmic origin of the middle meningeal

artery due to variation in embryonic stapedial artery development ndash a case report ndash ChinJ Radiol 24 171ndash173

Submitted 2011-May-30accepted 2011-October-04

Author for correspondence Nikolai E Lazarov PhD DSc Department of Anatomy andHistology Faculty of Medicine Medical University-Sofia 2 Zdrave Street BG-1431 SofiaBulgarianlazarovmedfacacadbg

366 Silviya Y Nikolova et al

eschweizerbart_XXX