microvascular healing over temporalis

7/28/2019 Microvascular Healing Over Temporalis

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infusion media: Indian ink solution, lead ox-ide solution or methyhnethacrylate resin.The composi t ion of the infus ion media andthe methods of prep ara t ion of the maxi llaryspecimens have been reported previously4.

The cats were randomly assigned into oneof 3 groups and the choice of infusion me-

dium was made according to the defined sac-rifice time for that group. The lead oxidesolution was selected to i l lustrate the arterialpat tern in the TMF fol lowing i t s t ransferinto the oral cavity for maxillary reconstruc-t ion. The In dian ink solut ion would demon-strate the microvascular network and thechanges of the TMF dur ing the heal ing pro-cess. The methylmethacrylate resin wouldform vascular corros ion cas ts to complementthe result of the Indian ink findings and toillustrate the microvasculatures in three di-mensions underneath the repai red ora l mu-cosa and compared wi th the contra la tera lnormal palatal mucosa. The lead oxide in-

fused head specimens were radiographed(Hewlett Packard x-ray system 43805N,USA) at 70 kvp for 2-5 minutes. The ex-posure t ime was adjusted according to t ire

thickness of the specimens and the imageswere captmzd using instant fi lms (Polaroid550 positive & negative films, USA). The In-dian ink infused specimens were embedded inparaffin blocks and prepared into thin sec-

tions of 10/~m thickness and thick sectionsof 300 #m thickness. The thin sections weres ta ined wi th haematoxylin and eos in (H&E)and the thick sections remained unstained;bo th were mo unt ed o n glass slides. Th e speci-

Fig. 1. Macrovascular network changes fol-lowing temporalis flap transposition to max-ilia by lead oxide infusion. On the radio-graphic submental vertex view following re-moval of the mandible in cat, the right side(R) was the normal and the left (L) was theoperated side. On the normal side, the pathof the internal maxillary artery is i l lustratedwith its branches supplying the maxilla: (a)internal maxillary artery, (b) infra-orbital ar-tery, (c) posterior palatine artery, (d) de-scending palatine artery, and (e) sphenopa-latine artery. However, on the operated side,obvious medial displacement of the internalmaxillary artery by the muscle was noted.

Fine branches derived directly from the retemirabile (*) and the inte rnal maxillary arterywere seen.

Fig. 2. Microvascular changes in the superficial layer of the tempo ratis flap during th e healingprocess. A: In the acute inflammatory phase during the first 6 weeks, the microvasculaturesof the superficial layer were dilated, formin g bush-like bundles. The vascu lar con tribut ion tothis layer was derived from the muscle flap rather than the normal side of the palate (Indianink x20). B: Histological section of the corresponding palate/flap junction as in A. (H&E 50). C: In the chronic inflamm atory phase durin g the 8th-14 th weeks, the dilated microvas-cular bundles abov e the temporalis m uscle fibres became more discrete but sti l l separated fromthe surface by an avascular layer. New microvasculatures (I~) were introduc ed by the migratingepithelium from the palatal side (Indian ink D: Histological section of similar site as inC, showing onset of chronic inflamm atory phase on the flap (H&E E: At higher magni-fication of the advanc ing front at the buecal side of the flap, details of the new vascular plexus(*) could be seen (Indian ink F: Histological section of similar site as in E, showingepithelial migrat ion an d hy perplastic changes (H&E ?


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mens were examined under light microscopy(Leitz Orthoplan, Germany). The corrosionvascular casts infused by methylm ethacrylateresin were sectioned into small seganents andmounted on copper stubs with conductivecolloidal carbon. The casts were sputtercoated with gold and examined under scan-

ning electron microscopy (Joel JXA-840SEM, Japan).

In addition to the morphological descrip-tion o f the microvascular networks at the dif-ferent healing times, morphometric analysisof the vascular density in the Indian ink in-fused thick sections was performed. The im-ages of the vascular networks were capturedthrough a video camera (JVC TK-1280E, To-kyo, Japan) mounted on the microscope (Ni-kon Ophtihot, Japan) to a computerized im-age analyzer system (Leica Quantimet 500+,Cambridg e, England). A standard field wascreated and the microvascular networkswithin this field were quantified as the vascu-

lar density percentage. The vascular densityat the wound margin, wound centre andcontralateral normal palatal mucosa wasmeasured 5 times from separate slides at eachof the sacrifice times. The means and stan-dard deviations of the vascular density per-centage of the three selected fields were com-pared by one-way analysis of variance(ANOVA). If the P v alue was less than 0.05,then further comparison of the groups wasconducted by a Tukey-Kramer multiple com-parison test to identify the significant pairs.Instat software (Instat Ver 3.0, Graph PadSoftware Ltd., S an Diego, USA ) was used forthe statistical analysis.

Microvasculatures of healing TM F 471

R e s u l t s

Wi t h t h e T M F t r a n s p o se d i n t o th e o ra lcav i ty, t he mos t obv ious change was them e d i a l d i s p l a c e m e n t o f t h e i n t e r n a lmax i l l a ry a r t e ry by the musc le bu lk(F ig . 1). The no rm a l a r r ang emen t o fthe an te r io r pa l a t ine a r t e ry and i t sb ranches d i sappea red and was r ep lacedby f ine b ranches de r ived f rom the r e t emi rab i l e o r d i r ec t ly f rom the in t e rna lmax i l l a ry a r t e ry fu r the r back . Th i s i n -d i c at e s t h e m a i n t e n a n c e o f m a c r o v a s c u -l a r s up p l y t o t h e T M F f r o m i ts o r i gi n a lsou rce wi th no s ign i f i can t a l t e r a t iondur ing the hea l ing phases . The musc lef ib re s r ema in ed w e l l pe r fused by mic ro -vesse l s a s con f i rmed by the Ind ian inkin fus ion o f t he fib res . The hea l ing T M Fwas sh i e lded f rom the o ra l cav i ty by ath i ck l aye r o f vascu la r t i s sue a t a l l t imesdur ing the hea l ing p rocess . Th i s supe r-f i c i a l vascu la r l aye r was found tochange i t s pa t t e rn and dens i ty, co r r e l a t -ing wi th the d i f f e ren t phases o f h i s to -

log ica l hea l ing .I n t h e a c u t e i n f l a m m a t o r y p h a s e o fthe TMF hea l ing du r ing the f i r s t 6

Fig. 3. Com pariso n o f sub-epithelial microvascular plexus between the repaired mucosa andnorm al palat al muco sa at 6 month s postoperatively. A: The tempo ralis muscle remained well-perfused and was covered by a flat mucosa (Indian ink ?420). B: The microvascular networkon the no rma l side of hard palate (Indian ink ?


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472 C h e u n ge r a ll y, w i t h n o a p p a r e n t c o n t r i b u t i o nf r o m t h e p a l a t a l s i d e . Wi t h t h e p r o -gress ive change in to the chron ic in -f l a m m a t o r y p h a s e d u r i n g t h e 8 t h - 1 4 t hw e e k s , t h e d i l a t e d v a s c u l a r b u n d l e sa b o v e t h e t e m p o r a l i s m u s c l e f i b r e s b e -

c a m e m o r e d i s c r e te b u t w e r e s ti l l s e p a r -a t e d f r o m t h e s u r f a c e b y a n a v a s c u l a rl a y e r. F o r m a t i o n o f a n e w v a s c u l a rp l e x u s w a s n o t e d b e l o w t h e a d v a n c i n ge p i t h e l i u m a t t h e p a l a t a l a n d b u c c a ls i d es o f t h e f l a p ( F i g . 2 c - f ). A t t h e1 8 hweek, the vesse l s in the super f ic ia l vas -c u l a r l a y e r h a d b e c o m e l e s s d e n s e a n ds m a l l e r i n d i a m e t e r, w h i l e t h e f l a p w a sp r o g r e s s i n g t h r o u g h t h e p r o l i f e r a t i v ep h a s e o f h e a l i n g ( F i g . 2 g , h ).

T h e p a l a t e r e c o n s t r u c t e d b y T M Fw a s c o m p l e t e l y e p i t h e l ia l i z e d a t t h e 2 4 hweek (F ig . 3a , b ) . A f ine vascu la r p lexuso f l o w p r o f i l e w a s n o t e d b e l o w t h i s r e -p a i r e d e p it h e li u m w h e n c o m p a r e d w i t ht h e p r o m i n e n t h a i r p i n c a p i l l a r y l o o p s i nt h e n o r m a l p a l a t a l m u c o s a ( F i g . 3 c , d ) .T h e f i n e v a s c u l a r p l e x u s w a s s e p a r a t e df r o m t h e T M F u n d e r n e a t h b y a w e l l -d e f i n e d c o l l a g e n l a y e r o f l e s s v a s c u l a rd e n si t y. T h e s o u r c e o f t h e v a s c u l a r s u p -p l y t o t h e s u b - e p i t h e l i a l p l e x u s w a sc o n s e q u e n t l y d e r i v e d f r o m t h e b u c c a la n d p a l a t a l s i d e s o f t h e r e c o n s t r u c t e ds i t e , w h e r e a s t h e c o r r e s p o n d i n g p l e x u so n t h e n o r m a l s i de w a s d i r e c tl y s u p -

p l i e d f r o m b e l o w b y t h e s u b m u c o s a lv a s c u l a r n e t w o r k .U n d e r s c a n n i n g e l e c t r o n m i c r o s c o p y

( S E M ) w i t h t h e s e le c ti v e r e m o v a l o f t h ee p i t h e I i u m b y c o r r o s i o n , t h e s u b - e p i -t h e l i a l v a s c u l a r p l e x u s w a s o b s e r v e d a sa f i n e in t e r l a c i n g n e t w o r k o f c a p i l l a r i e s

c o n n e c t e d b y b r a n c h i n g a r t e r i o l e s a n dvenules (F ig . 3e) . A layer o f l a rger ves -se l s cou ld be seen be low th i s super f ic ia lm i c r o v a s c u l a r n e t w o r k a n d t h e y c o r r e -s p o n d e d w i t h t h e i n t r a m u s c u l a r v e s s e l so f th e T M E A t a n o b l i q u e a n g l e v i ew

of the super f ic ia l vesse l s , they demon-s t r a t e d s h o r t h a i r p i n f o l d i n g o f th ecap i l l a r ies (F ig . 3g). In con t ras t , then o r m a l h a r d p a l a t e h a d u n d u l a t i n gr i d g e s o f c a p i l l a r i e s g r o u p i n g t o g e t h e r,w h i c h c o r r e s p o n d e d t o t h e p a l a t a l r u -gae (F ig . 3 f ). On the sur fa ce of th i s vas -c u l a r l a y e r, t h e c a p i l l a r i e s f o r m e d t a l ll o o p s o f h a i r p i n c o n f i g u r a t i o n ( F i g .3h).

T h e v a s c u l a r d e n s i t y o f t h e s u p e r-f i c i a l m i c r o v a s c u l a r l a y e r a t d i f f e r e n tt i m e p e r i o d s o f T M F h e a l i n g i s i l lu s -t ra ted in F ig . 4 . The vesse l s a t the f l apm a rg i n a n d t h e f l a p c e n t r e w e re s t a t i s t i-c a l l y s i g n i f ic a n t l y d i f f e r e n t f r o m t h en o r m a l s i d e ( P < 0 . 0 0 1 ) d u r i n g t h e f i r s t8 weeks , a f te r which there were no obvi -ous d i ffe rences be tween the g roups .W h e n t h e v a s c u l a r d e n s i ty w a s c o m -p a r e d b e t w e e n t h e f l a p m a rg i n a n d t h ef l a p c e n t r e d u r i n g t h e s a m e p e r i o d ,there were no s ign i f ican t d i ffe rencest h r o u g h o u t t h e h e a l i n g p r o c e s s e x c e p ta t t h e 6 h w e e k ( P < 0 . 0 5 ) . W h e n t h e f l a pm a rg i n v a s c u l a r d e n s i t y w a s a s s e s s e don i t s own, there were no s ta t i s t i ca l ly

s ign i f ican t changes dur ing the f i r s t 6w e e k s . T h e v a s c u l a r d e n s i t y s t a r t e d t or e d u c e f r o m t h e8 th week, s tab i l i zed a tt h e 1 4 h w e e k a n d r e m a i n e d t h e s a m eunt i l the 24 h week . S i mi la r f ind ingsw e r e n o t e d i n t h e v a s c u l a r d e n s i t y a t t h ef lap cen t re over t ime .

M i c r o v a s c u l a rd e n s i t y

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10 - . . . .

1 I I I I ! I I

2 4 6 8 12 14 20 24W e e k s

Fig. 4.Com parison o f the microvascular density between the flap centre, palata l wound m ar-gin and n orm al palate dur ing the healing process of the temporalis flap.

D i s c u s s i o n

T h e c a r o t i d a r t e r i a l s y s t e m o f d o m e s t i cc a t s h a s s e v e r a l c h a r a c t e r i s t i c f e a t u r e sf a c i l i t a t in g t h e i n f u s i o n o f t h e t e m -p o r a l i s m u s cl e . T h e e x t e r n a l c a r o t i d a r -

te ry i s eas i ly iden t i f i ed in the d i ssec t iono f t h e n e c k . T h e r e i s n o c o n f u s i o n a st o w h e t h e r i t i s t h e e x t e r n a l o r i n t e r n a lc a r o t i d a r t e r y b e c a u s e t h e i n t e r n a l c a -r o t i d a r t e r y i n c a t s i s n o r m a l l y d e g e n e r-a t e d t o s u c h a n e x t e n t t h a t a n i n f u s i o nm e d i u m s u c h a s l e a d o x i d e s o l u t i o nd o e s n o t p a s s t h r o u g h 9. T h e l a rg e s tb r a n c h o f t h e e x t e r n al c a r o t i d a r t e r y i nc a t s i s t h e i n t e r n a l m a x i l l a r y a r t e r y,f r o m w h i c h b r a n c h e s s u p p l y t h e t e m -p o r a l i s m u s c l e . I n c a t s , t h e i n t e r n a lm a x i l l a r y a r t e r y f o r m s a d i s t i n c t a r-t e r i a l n e t w o r k i n t h e i n f r a t e m p o r a lf o s s a a r e a , c a l l e d t h e r e t e m i r a b i l e o rex te rna l re te , which i s absen t inh u m a n s 9. We f o u n d t h a t t h e a n t e r i o rd e e p t e m p o r a l a r t e r y c o n s i s t e n t l yb r a n c h e d o u t o f t h e r e te m i r a b i l e . T h ep o s t e r i o r d e e p t e m p o r a l a r t e r y a r o s ee i t h e r f r o m t h e r e t e m i r a b i l e o r d i r e c t l yf r o m t h e i n t e r n a l m a x i l l a r y a r t er y,w h e r e a s t h e p o s t e r i o r a u r i c u l a r a r t e r yc o n s i s t e n t l y b r a n c h e d o u t o f t h e i n t e r -n a l m a x i l l a r y a r t e r y d i r ec t ly. T h e s e 3v e s se l s w e r e f o u n d t o b e t h e m a i n v a s -c u l a r s o u r c e o f t h e t e m p o r a l i s m u s c l e i n

c a t s , a l t h o u g hF U J I M O T O 11

n o t e d t h a ta d d i t i o n a l m i n o r v a s c u la r c o n t r i b u t i o n sm a y a l s o a r i s e f r o m t h e b u c c a l a n ds u p e r f ic i a l t e m p o r a l a r t e r i e s . T h e i n t r a -m u s c u l a r v e s se l n e t w o r k a n d i t s e x t e n -s i v e a n a s t o m o s i s i n t h e t e m p o r a l i sm u s c l e o f c a t s h a s b e e n d e f i n e d b y S A I-TO 14 a n d i s c o m p a r a b l e w i t h t h e r e s u l t sp r e s e n t e d .

T h e v a s c u l a r p a t t e r n o n t h e n o r m a lh a r d p a l a t e h a s b e e n e x t e n s iv e l y s t u d i e din m am m al s 12,13,~6,18,19. A lt ho ug h the reare recognizab le d i ffe rences in the vas -c u l a r n e t w o r k b e t w e e n d i f f e r e n t s p e c ie s ,t h e b l o o d s u p p l y i s e s s e n t i a l ly d e r i v e df r o m t h e g r e a t e r p a l a t i n e a r t e r y a n df o r m s d i f f e r e n t v a s c u l a r l a y e r s i n t h esubm ucosa and mu cosa 13. The spec i f icv a s c u l a r p a t t e r n i n t h e c a t 's p a l a t a l m u -c o s a w a s p u b l i s h e d b y TO D ATM a n d i s i na g r e e m e n t w i t h o u r f i n d i n g s o f 2 d i s -t i n c t la y e r s, t h e l a m i n a p r o p r i a a n d s u b -m u c o s a l v a s c u l a r n e t w o r k s . I n a c e r t a i nl o c a t i o n o f t h e h a r d p a l a t e , t h e r e w asa l s o a p a l a t i n e v e n o u s p l e x u s j u s t b e -n e a t h t h e s u b l n u c o s a l v a s c u l a r n e t w o r k .N o t a b l e c a p i l la r y l o o p s o f h a i r p i n c o n -

f i g u r a t i o n w e r e p r o j e c t i n g u p w a r d a tr i g h t a n g l e s f r o m t h e l a m i n a p r o p r i av a s c u la r ne t w o r k f o u n d b y o u r S E M


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Microvasculatures of healing TM F 47 3

study. The configuration of these capil-lary loops was generally of simple hair-pin shape as noted in animals, unlikethe development of a more complexform in humans with triple loopingsformed by additional secondary and

tertiary capillaries 19. The capillaryloops were found to project into themucos al papilla e; LEE et al. 12 note d thatthe spacing, height and orientation ofthese loops closely correlated with theepithelial connective tissue interlace.On the hard palate, there were also well-developed rugae or plicae lying trans-versely in multiple rows formed by fold-ing of the mucosa. These are consideredimportant for the apprehension, trans-portation and mashing of food in ani-mals. The capillary pattern immediatelybelow these rugae was foun d to be morepronounced. In cats and dogs, the ru-gae have been noted to create undu-lation in the lamina propria vascularnetwork when compared with othermam ma ls ~3.

Adequate information on two-di-mens iona l changes of the vasculature inthe reconstructed maxilla could be ob-tained from correlating the Indian inkspecimens with histology. The changin gmicrovascular pattern and vasculardensity of the surface layer corre-sponde d well with the histological heal-

ing sequence. The vasculature of thehealing muscle was at all times pro-tected from the surface by an avascularlayer before the epithelium was able toform a cover. On histology, this layerwas made up of fibrin and inflamma-tory cells with eosinophilic staining.Since the deep temporal fascia has ablood supply distinct from that of themuscle, it may undergo ischaemicchanges and form part of this avascularlayer as well. However, the muscle re-mained viable and its intramuscularvessels well-perfused. These intramus-cular vessels were confirmed to be themain source of vascular transformationon the surface layer of reconstruction.It was surprising to note that the nor-mal side of the palate did not contrib-ute s ignificantly to the vasc ular changesin the hea ling flap. The vascular contri-bution of the muscle flap was graduallytaken over by the vessels derived fromthe buccal side. When the temporaliswas completely covered by mucosa at24 weeks after surgery, the vascularsource to the repaired mucosa became

totally dependent on the palatal andbuccal sides, with no cont ribu tion fromthe muscle.

On histology, the repaired mucosawas shown to have different character-istics from the normal palatal mucosa.The normal microvascular layer andcapillary loops were also confirmed tobe quite different. This repaired mucosa

was found to have a modified sub-epi-thelial vascular plexus with sh ort capil-lary loops. The lack of promin ent capil-lary loops correlates well with the de-ficient mucosal papilla a nd rug ae in therepaired thin mucosa. STABLEIN et al. 15postulated that the capillary supply andits pattern might also be influenced bythe thickness of the overlying epithel-ium. This reduced blood supply belowthe repaired mucosa explains the clin-ically pale-loo king fibrotic mucosa thathealed over the TMF in the long-term.

An understanding of the microvas-cular changes of the healing temporalisflap not only complements the pub-lished histological changes 6, but mayhave some clinical implications as well.The finding that a submucosal vascularplexus introduced by migrating epi-thelial cells forms the vascular supplyto the repaired mucosa means that thereis no fear of conducting secondarysurgery on the healed TMF. The re-paired mucosal flap can be raised fromthe muscle flap without runn ing the riskof ischaemic necrosis. This enables

bony reconstruction of the maxilla by atitanium tray supporting cortico-can-cellous chips at a secondary stage fordental implant rehabilitation, similar tothe primary reconstruction methodpublished by our depar tment 17. Thespace for the bony re constru ction iscreated by debulking of the musclefibres and at the same time avoidingperforation of the repaired mucosa lin-ing the maxillary sinus or nasal cavity.The repaired oral mucosal flap maythen provide a cover over the tray, thusforming the oral barrier to facilitatebony healing.

Acknowledgments'.This was part of a PhDthesis of Hong Kong University and wassupervised by Professor Tideman, whosehelp is gratefully acknowledged. The authorwould also like to thank the technicians ofthe Oral Bio-Science Laboratory and Dr.Nabil Samman for commenting on themanuscript. This investigation was supportedby the Hong Kong University CRCG re-search grant 337/253/0002.

R e f e r e n c e s

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rosion cast study. J Anat 1996: 189: 431-8.4. CHEUNG LK. The vascular anatomy of

the human temporatis muscle: impli-cations for surgical splitting techniques.Int J Oral Maxillofac Surg 1996: 25: 414~21.

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6. CHEUNG LK. The epithelialization pro-cess in the healing temporalis myofascialflap in oral reconstruction. Int J OralMaxillofac Surg 1997: 26:303 9.

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8. COLMENERO C, MARTOR ELL V, COL-MENERO B, SmRRA I. Temporalis myofas-cial flap for maxillofacial reconstruction.J Oral Maxillofac Su rg 1991: 49: 1067-73.

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11. FUnMOTO T. Cubical anatomy of severalducts and vessels by injection methods ofacrylic resin. V. Arterial distribution ofthe temporal muscle in some mammals.Okajimas Folia Anat Jpn 1959: 33: 389-424.

12. LEE D, SIMS MR, DREYZR CW, SAMP-SON WJ. A scanning electro n micro-scope study of microcorrosion casts ofthe microvasculature of the marmoset

palate, gingiva and periodontal liga-ment. Arch Oral Bio l I991: 36:21 120.

13. OHTA Y, OKADA S, TODA ][, IKE H. Sca n-n i n g electron microscopic studies of theoral mucosa and its microvasculature: areview of the palatine rnucosa and itsmicrovascular architecture in mammals.Scanning Microsc 1992: 6: 463-74.

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15. STABLEINMJ, MEYER , WATERHOUSE JP.Epithelial dimensions and capillary sup-ply in the oral mucosa of the rat, Arch

Oral Bio l 1982: 27: 243-53_16. SUGIOKA S, IKE H .Scanning electron

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Palate and lip. Scanning Microsc 1994: 8:133-9.

Address:Professor L. K. CheungOral & Maxillofacial SurgeryPrince Philip Dental Hospital34 Hospital RoadHong Kong

microvascular healing over temporalis

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