the occurrence and possible aetiology of spondylolysis in a pre-contact california population

The Occurrence and Possible Aetiology ofSpondylolysis in a Pre-contact CaliforniaPopulationM. A. PILLOUDa* AND C. CANZONIERIba Joint POW/MIA Accounting Command, Central Identification Laboratory, JBPHH, HI, USAb Basin Research Associates, Inc., San Leandro, CA, USA

ABSTRACT The occurrence of spondylolysis (neural arch separation at the pars interarticularis) is reported in a pre-contact(720–550 Cal BP) Central California population, CA-CCo-647 (n=46). Spondylolysis was examined within thispopulation to assess differences in sex, age, and possible relationships with biological affinity. Furthermore,prevalence rates of spondylolysis were compared across various populations to discern the aetiology of thedefect. Within CA-CCo-647, spondylolysis was found in 17.4% (8/46) of the population. All occurrences arecomplete, bilateral separations of the neural arch in the lower lumbar (L4 and L5). The defect is not seen inindividuals below the age of 18, and there is no correlation between adult age and spondylolysis. Male indivi-duals display the defect at a higher rate (30.8% - 4/13) than female individuals (12.1% - 4/33); however, this isnot a statistically significant finding. There does seem to be a correlation between an individual’s sex and theonset of the defect; male individuals display spondylolysis at a younger age than female individuals. This findingcould represent differences in activity patterns among young male and female individuals. In a biologicaldistance analysis using craniometric data, male and female individuals with spondylolysis clustered closely,suggesting a genetic component for the defect. Finally, significant differences were found in spondylolysisprevalence between various populations representing distinct geographic and temporal settings. Significantdifferences were found among Native pre-contact samples and even between two comparable pre-contactCalifornia skeletal samples. These populations all engaged in distinct activities and were likely composed ofgenetically distinct groups of individuals, which may account for the differences in spondylolysis prevalence.All of these findings, both within CA-CCo-647 and between the various samples, suggest that the aetiology ofspondylolysis is likely an interaction of genes and activity. Copyright © 2012 John Wiley & Sons, Ltd.

Key words: biological distance; Miwok; pre-contact California; spondylolysis

Introduction

Spondylolysis is a spinal condition defined as theseparation of the vertebral neural arch at the pars inter-articularis. This failure of ossification union results intwo vertebral parts: an anterior portion composed ofthe vertebral body, pedicles, and the transverse andsuperior articular processes; and a posterior portionwith the spinous and inferior articular processes, andthe laminae (Aufderheide & Rodriguez-Martin, 1998).Spondylolysis most commonly occurs in the fifth andfourth lumbar vertebrae. When observed, the condition

is generally bilateral; although a unilateral defect canoccur, this presentation is much rarer (Porter & Park,1982). Spondylolysis can also lead to spondylolisthesis,in which the vertebral body slides forward owing tothe loss of the inferior articular facet that holds thevertebral body in place (Ortner, 2003).The aetiology of spondylolysis is not completely

understood, although several hypotheses have beenpresented. The most prevalent, and generally accepted,proposal for the cause of spondylolysis by cliniciansand anthropologists is that the condition represents afatigue fracture caused by repetitive activity and micro-trauma (Standaert & Herring, 2000). A biomechancialstudy simulated the forces of compression, flexion,extension, rotation, and lateral bending in the low backto evaluate stress on the pars interarticularis. The modelfound that the region of greatest stress was consistent

* Correspondence to:Marin A. Pilloud, Joint POW/MIA Accounting Com-mand, Central Identification Laboratory, 310 Worchester Ave, Bldg 45,JBPHH, HI 96853, USA.e-mail: marin.pilloud@jpac.pacom.mil

Copyright © 2012 John Wiley & Sons, Ltd. Received 17 November 2011Revised 31 January 2012Accepted 11 March 2012

International Journal of OsteoarchaeologyInt. J. Osteoarchaeol. (2012)Published online in Wiley Online Library(wileyonlinelibrary.com) DOI: 10.1002/oa.2245

with the affected area found in clinical cases of spondy-lolysis. Stress was highest under extension and rotation,suggesting these loadings to be particularly high riskfactors for the development of the defect (Chosa et al.,2004).Recent research has supported this idea demonstrat-

ing a high prevalence of spondylolysis among indivi-duals that are active in sports. These include childrenand adolescents (Morita et al., 1995); tennis players(Ruiz-Cotorro et al., 2006); Japanese rugby, judo, base-ball, and soccer players (Sakai et al., 2010); weightlifters(Risser, 1991; Rossi & Dragoni, 1990); divers andwrestlers (Rossi & Dragoni, 1990); among others (seeShrier, 2001, for summary). While extensive, these find-ings are not conclusive. For example, Soler and Calderon(2000) found that the occurrence of spondylolysis in astudy of Spanish elite athletes was not significantly dif-ferent from the rates reported for the general population.Other researchers point to biological factors that

could contribute to the occurrence of spondylolysis.Stewart (1956) measured the angle of the superiorsurface of the sacrum in relation to the vertical planeand compared it with the occurrence of spondylolysis.He found a slightly greater angle in the individuals withthe defect, but the differences were not statisticallysignificant. Wiltse (1962) conducted a similar studyusing juvenile sacra. In this study, the angle was verysimilar in children who both displayed and did notdisplay the defect; leading to the conclusion that lordosisis not a contributing factor. Weiss (2009) conducted asimilar study on a pre-contact skeletal population inCalifornia and reached a similar conclusion. Her studyanalysed the occurrence of spondylolysis and found thatno variable of sacral anatomy (sacral base angle, facetorientation, curvature, or sacralization) could adequatelyaccount for differences in defect occurrence.Merbs (1996) argues that spondylolysis is likely the

result of an erect posture and may be an adaptationallowing for more flexibility in the lower back. Part ofthe evidence for his argument is that the conditiononly develops in humans and only after an individualcan walk. Many authors have reported that spondyloly-sis does not occur in newborns, and only rarely beforethe age of five (Aufderheide & Rodriguez-Martin, 1998;Fredrickson et al., 1984; Wiltse, 1962). However, thereare a few cases of very young children exhibiting thecondition. Borkow and Kleiger (1971) report on a caseof spondylolisthesis and related pars interarticularisdefect in a four-month-old child. And, Wiltse et al.(1975) describe a case of spondylolysis in an eight-month-old child. These findings suggest an alternatecause for the condition besides bipedality or repetitiveactivity as these young children are not walking and

are too young to suffer the effects of trauma fromrepetitive activity.A study by Fredrickson and colleagues (1984)

followed several hundred children over a span of 25 years.Their study found a correlation between spondylolysisand the presence of spina bifida occulta, with no evidencethat patients over the age of six had a non-united stressfracture. For a subset of these children, data were alsoavailable on families and the occurrence of spondylolysis,32% of fathers and 17% of mothers also had the condi-tion. These findings led the authors to conclude that agenetic predisposition for the defect was likely. Pedigreestudies seem to agree. Haukipuro et al. (1978) foundspondylolysis, along with several other pathologicalspinal conditions, to occur at high rates in a Finnishkin group of 192 individuals. Their pedigree analysissuggested a pattern of autosomal dominant inheritancewith incomplete penetrance for spondylolysis. Asimilar study found high rates of the defect in a familyover four generations (Shahriaree et al., 1979). Pedigreestudies on spondylolysis may be difficult as it is possiblefor individuals with spondylolysis to have no associatedpain and they can often heal on their own (Fredricksonet al., 1984; Wiltse et al., 1975). Therefore, the conditioncould be present, but asymptomatic, making it difficultto diagnose and ascertain a solid family history. It istherefore quite possible that an even stronger geneticcomponent for the defect exists than is currentlybelieved.The occurrence of spondylolysis may not be the result

of repeated trauma or genes alone, and a connectionbetween the two may exist. In fact, one can be genetic-ally predisposed to a fracture at the pars interarticularis(Newman, 1963; Porter & Park, 1982; Wiltse et al.,1975). Merbs (1996) emphasises that what is beinginherited is not the defect itself, but rather features ofvertebral anatomy that may predispose one to fracture.Mays (2007) further argues that there could be distinctaetiologies for the condition, which could be determinedthrough an analysis of the defect itself. He found that insome of the cases of spondylolysis in his study sample,a distinct morphology was present suggestive of adiarthrodial joint. The presence of a joint in an areawhere no joint would normally occur suggests a congeni-tal condition rather than an acquired one.Interesting population level patterns have emerged in

studies of spondylolysis that may provide clues about theaetiology of the condition. Several studies reportthat men have spondylolysis at rates twice as high aswomen. Fredrickson et al. (1984) found a ratio of 2:1 ofmale : female by the age of six and into adulthood amongan American sample they followed beginning in the1950s. Wiltse et al. (1975) also found the lesion occurred

M. A. Pilloud and C. Canzonieri

Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

more commonly in boys than in girls. Additionally, dif-ferences in age have been identified. Wiltse et al. (1975)reported that the occurrence of spondylolysis risesabruptly between the ages of 5.5 and 6.5 years, andthat the defect would continue to rise into adulthood.Fredrickson et al. (1984) found the defect at a rate of4.4% in 6-year-old children, increasing to as much as5.8% into adulthood. Finally, the defect is found invarying rates across populations, ranging from 5% in aBritish population (Fibiger & Knüsel, 2005) up to nearly50% in some Alaskan populations (Lester & Shapiro,1968; Stewart, 1953). These reported differences inage, sex, and population could be related to differencesin group activity, biology or genetic composition—orperhaps an interaction between all three.The purpose of the present study is to test some of

the potential causes of spondylolysis by analysing bothbiological and cultural components. To accomplish this,a sample population from prehistoric California is used.Three main goals are identified in this study. First,possible sex and age-related differences in relation tospondylolysis are explored. Second, the possibility of agenetic correlation among individuals displaying thisdefect is examined using a biodistance study with cranialmetrics. Finally, patterns of spondylolysis from thisprehistoric California population are compared withother populations to identify relationships in activity orpossible microevolutionary changes in the occurrenceof the condition.

Biocultural context

The skeletal sample analysed in the present study wasrecovered from CA-CCo-647 (unincorporated Oakley)formerly within an estuarine environment of theSacramento-San Joaquin Delta in the territory of theBay or Eastern Miwok (Figure 1). Radiometric datesand artefact typologies date the site to Cal AD 1230 to1400 (720–550 Cal BP) (Basin Research Associates,2008), placing the site in the middle period late phaseto middle/late period transition (Bennyhoff & Hughes,1987).The Miwok political organisation was united along

ethnically and linguistically defined tribelets of severalhundred individuals. Each tribelet was a localised patrili-neage that had several named settlements all centredaround a capital where the chief resided (Levy, 1978).CA-CCo-647 appears to have been within the Julpuntribelet territory that occupied the area between PortChicago and the mouth of Marsh Creek (Bennyhoff,1977; Kroeber, 1925; Levy, 1978). The tribelet centreappears to have been located at present-day Antioch.

The Miwok were also more broadly divided into twodistinct moieties relating to land and water. Themoieties were meant to be exogamous units, and in factabout 75% of marriages followed this rule (Levy,1978).The project area is centrally located within a low-

lying tule marsh rich in marine resources (fish, turtle,and aquatic fowl). Each tribelet occupied a specificterritory that would utilise several seasonal campsitesat various times during the annual round of subsistenceactivities, making the groups relatively mobile. Ethno-graphically, the Eastern Miwok relied on huntingand gathering for their subsistence. Plants includedacorns, nuts, seeds, roots and various greens. Fishingwas very important to the Miwok. They had tulebalsa boats, and they used various types of nets andharpoons to catch fish (Barrett & Gifford, 1933). TheMiwok were also known to hunt elk, deer, beaver,squirrels and various game fowl (Levy, 1978). Varioustools were employed in the hunting of game. Forexample, net traps were used to hunt deer andrabbit, and squirrels and beaver were shot with a bowand arrow (Barrett & Gifford, 1933). The Miwok wereinvolved in a robust trade network transportingmaterial such as obsidian, olivella shell, and basketsthroughout California to the Great Basin (Levy, 1978).

Figure 1. Map of project location.

Spondylolysis in a Pre-contact California Population

Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

The segregation of industrial activities by sex is poorlydocumented in ethnographic studies of the Miwok, butwith the exception of tribal taboos, most work may havebeen performed in tandem (Bennyhoff, 1977). However,there was likely some division of labour by sex. Sometasks such as hunting, or the preparation of huntingand fishing equipment, were considered the sole respon-sibility of men (Bennyhoff, 1977; Dick-Bissonnette,1977). Likewise, ‘senior’ women were responsible forcoordinating and supervising young women, children,and elderly men in the collection and processing ofacorns and edible plants. Women were also consideredto serve ‘in lieu of beasts of burden’ (Dick-Bissonnette,1977), which may be in reference to their carrying of bas-kets with water and other goods (Barrett & Gifford, 1933).

Material and methods

A total of 91 discrete burials were recovered fromCA-CCo-647 of male and female individuals rangingin age from infant to mature adult. However, only adultindividuals of determinate sex with all five lumbarvertebrae were included in this study to obtain trueprevalence rates for spondylolysis, leaving a total of 46individuals for study (Table 1).Recovery of these burials was part of a larger data

recovery project conducted by Basin Research Associ-ates. As skeletons were identified during excavation, theywere given a unique skeleton number. All inhumations,data recovery units, trenches and features were recordedandmapped (Figure 2). Skeletal analyses were conductedin the field at the request of the most likely descendant(Andrew Galvan) appointed by the Native AmericanHeritage Commission. Human remains were removedfrom their individual storage boxes and placed on anexamination table in anatomical position. No clean-ing or alteration of the remains in any way wasallowed. Standard osteological methods were usedto estimate sex and age-at-death (Bass, 1995; Buikstra& Ubelaker, 1994; Dittrick & Suchey, 1986; Dreier,1978; Lovejoy et al., 1985; Meindl & Lovejoy, 1985;

Moorrees et al., 1963; Phenice, 1969; Schwartz, 1995;Todd, 1921a; Todd, 1921b; Ubelaker, 1999). The deter-mination of sex relied heavily on pelvic morphology,closely followed by skull morphology when necessary.The burials in the study were placed in nine approximateage categories: foetal (in utero), infant (birth to 3 years);child (4–12 years), adolescents (13–17 years), youngadult (18–25 years), adult (>25 years), young middleadult (26–35 years), middle adult (36–45 years), andmature adult (46+ years) (Boylston & Roberts, 1996).The vertebral columns were sorted and examined

for pathological conditions affecting the spine (Merbs,2002). When present, any separation was recorded aspartial or complete and unilateral or bilateral. Additionalanomalies were observed in conjunction with those verte-brae exhibiting spondylolysis; including compressionfractures, osteoarthritis, and bifurcated spinous processes.Measurements of the cranium used in biological

distance analyses were collected according to Moore-Jansen et al. (1994) using spreading callipers and digitalsliding callipers. The cranial measurements collectedare outlined in Table 2. Unfortunately, it was notpossible to collect data on dental metrics or morphologybased on the condition of the remains and the limitationsof data collection placed on the anthropologists. Further-more, data on cranial non-metric traits could also not bereliably collected as remains were not allowed to becleaned during field analysis.

Statistical analyses

All analyses were conducted using SPSS 19.0 (IBMCorp.,Armonk, NY, USA). Patterns of spondylolysis withinthis sample were assessed using chi-square analysis andPearson’s and Kendall’s tau-b correlation coefficients.To determine interindividual biological distances, a

principal components analysis was used to reduce thenumber of variables and to remove any correlationbetween measurements. Using those variables with aneigenvalue above one (Kaiser, 1960), a hierarchicalcluster analysis was employed to determine thesquared Euclidean distance of each individual usingWard’s method. Dendrograms were then created toillustrate relationships.As is often the case in archaeological skeletal collec-

tions, several measurements could not be taken for everyindividual, resulting in missing data. It was not feasible toremove individuals with missing data, or to removevariables with missing values, as this would result ineither too few individuals or not enough data points.Therefore, missing values were replaced with the samplemean. This practice was justified as the missing data are

Table 1. Skeletal sample from CA-CCo-647 of adult individualsof determinate sex containing all five lumbar vertebrae

Sex YA YMA MiA MA Total

Female 5 10 7 11 33Male 4 2 4 3 13Total 9 12 11 14 46

YA (young adult, 18–25); YMA (young middle adult, 26–35); MiA(middle adult, 36–45); MA (mature adult, 46+).

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Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

fairly evenly distributed throughout the sample. Onaverage, each individual is missing three measure-ments, and each cranial measurement is missing fivevalues. This distribution of missing data did not causeindividuals with many missing measurements to artifi-cially cluster together as might be expected if theirmeasurements were overly reliant on sample means.

Craniometric data for male and female individualswere analysed separately and jointly. In the analysesof both sexes, data were standardised according todefined means for each sex using Z-scores, effect-ively removing size sexual dimorphism. Thesescores were then used in the population wide bio-distance analysis.

Figure 2. Plan map of CA-CCo-647.

Spondylolysis in a Pre-contact California Population

Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

Results

Age and sex

Spondylolysis is present in eight individuals out of 46,or 17.4% of the sample (Table 3). Only one vertebra isaffected in each case. The defect is on the fifth lumbarvertebra, except in one case where it is found on thefourth lumbar vertebra of a male. The defect iscomplete in every occurrence (Figure 3).The age and sex distribution of spondylolysis is

outlined in Table 4. No spondylolysis is observed inindividuals below the age of 18. These age distinctionsat the adult level are not statistically significant(w2 = 1.251, p> 0.05), and there is also no correlationbetween age and the occurrence of the defect(r=�0.115, p> 0.05). There is also not a statisticallysignificant difference found between male and femaleindividuals (w2 = 2.257, p> 0.05).Among male individuals, no correlation between age

and spondylolysis is found (r=�0.122, p> 0.05) andthe difference between ages is not statistically signifi-cant (w2 = 1.655, p> 0.05). Similar results are foundamong female individuals; there is no correlationbetween age and spondylolysis (r=�0.078, P> 0.05),and the difference between ages is not statistically

significant (w2 = 4.751, p> 0.05). The condition is notlargely different between the sexes in terms of age;however, it appears to occur in male individuals at anearlier age. In a consideration of just young adults,Kendall’s tau-b correlation found a marginally significantrelationship between sex and the occurrence of spondy-lolysis (r=0.598, p=0.091). Although the p-value inthis analysis is slightly higher than 0.05, the use ofhigher p-values in studies with small sample sizes maybe justified. However, the low sample size may alsomake these results unreliable.

Biodistance

Cranial metrics were used to assess the interindividualbiological distances of this sample in an effort to

Table 2. List of cranial measurements used in biological distance analysis based on Moore-Jansen et al. (1994)

Cranial measurements

Maximum cranial length (g–op, GOL) Orbital breadth (d–ec, OBB)Maximum cranial breadth (eu–eu, XCB) Orbital height (OBH)Basion-prosthion length (ba–pr, BPL) Biorbital breadth (ec–ec, EKB)Biauricular breadth (au–au, AUB) Interorbital breadth (d–d, DKB)Upper facial height (n–pr, UFH) Frontal chord (n–b, FRC)Minimum frontal breadth (ft–ft, WFB) Parietal chord (b–l, PAC)Upper facial breadth (fmt–fmt, UFB) Occipital chord (l–o, OCC)Nasal height (n–ns, NLH) Foramen magnum length (ba–o, FOL)Nasal breadth (al–al, NLB) Foramen magnum breadth (FOB)

Table 3. Distribution of spondylolysis

Burial # Sex AgeVertebraaffected

Complete/Partial

17 M MA L4 Complete21* F YMA L5 Complete22 F YMA L5 Complete39 M MiA L5 Complete41 F YMA L5 Complete59 F MA L5 Complete71 M YA L5 Complete89* M YA L5 Complete

YA (young adult, 18–25); YMA (young middle adult, 26–35); MiA(middle adult, 36–45); MA (mature adult, 46+).*No cranial metric data available for these individuals.

Figure 3. Complete spondylolysis to the fifth lumbar vertebra, scale isin centimetres.

M. A. Pilloud and C. Canzonieri

Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

identify biological affinity in relation to the occurrenceof spondylolysis. The descriptive statistics for cranialmeasurements for each sex are provided in Table 5.For this analysis, several individuals lacking cranio-metrics had to be removed (9 female and 5 male). Tobegin, the principal components scores were calculatedfor each group: female, male, and both sexes combined(Table 6). These values were then used to calculateEuclidean distance measures from which dendrogramswere created. The dendrogram serves as a visual repre-sentation of this type of hierarchical cluster analysisin which similar individuals within this dataset aregrouped together.In an analysis of just the female individuals, each

individual with the defect is in a distinct cluster (Figure 4).In consideration of only the male individuals, thereagain appears to be minimal clustering of individualswith spondylolysis (Figure 5). However, this samplesize is extremely small, and in fact few differences arefound between the male individual and no significantclustering of individuals is found.

When the sex standardised values of all individualsare analysed, distinct clusters of individuals with thedefect can be seen (Figure 6). This indicates that maleand female individuals with the defect are clusteringtogether. In this analysis, individuals 41 and 39 are ina related subcluster, as are individuals 71 and 22. Onthe other hand, individuals 17 and 59 continue toseparate in this analysis at about the same level fromthe remainder of the sample as they did in the sexspecific analyses.An examination of Figure 2 reveals minimal relation-

ship between burial location, that is, presence of spondy-lolysis and phenotypic similarities. Individuals 41 and 39cluster together and are buried in the south of the site.However, individual 22, also buried in the south andhaving spondylolysis, clusters with individual 71 whois buried with the group of skeletons to the north. Indivi-duals 17 and 59 do not cluster with other individualswith spondylolysis, and they appear to be buried in areasseparated from these individuals (e.g. skeletons 41, 39,22, and 71).

Spondylolysis prevalence in other populations

A broad range of spondylolysis frequencies have beenreported both temporally and spatially (Table 7).Weiss (2009) found a frequency of spondylolysis of16.4% in a study of California Native Americans datingto 2180–250 BP, with male individuals showing thedefect at a rate of 26% and female individuals at 11%.This population is located in the same general vicinityas the CA-CCo-647 sample and encompassed roughlythe same time period. The rates of spondylolysis in thesetwo populations are highly comparable.Roughly similar rates of spondylolysis are reported

in other prehistoric Native populations. In an Archaicsample from Northwestern Alabama, the defect wasfound in 17% of male individuals and 20% of femaleindividuals, with the defect occurring at a youngerage in male individuals (Bridges, 1989). A pre-contactpopulation in Guam showed spondylolysis at a rate of21%, seen in 29.4% of male individuals and 14.3% of

Table 4. Distribution of spondylolysis by age and sex

YA YMA MiA MA Total

Sex N % N % N % N % N %

Female 0/5 0 3/10 30.0 0/7 0 1/11 9.1 4/33 12.1Male 2/4 50.0 0/2 0 1/4 25.0 1/3 33.3 4/13 30.8Total 2/9 22.2 3/12 25.0 1/11 9.1 2/14 14.3 8/46 17.4

YA (young adult, 18–25); YMA (young middle adult, 26–35); MiA (middle adult, 36–45); MA (mature adult, 46+).

Table 5. Descriptive statistics of cranial metrics for males andfemales at CA-CCo-647

Female Male

Measurement N Mean SD N Mean SD

GOL 21 172.21 17.02 7 181.43 5.71XCB 22 138.61 8.84 5 140.00 6.60BPL 20 103.18 14.18 6 107.54 13.45AUB 22 120.30 3.78 5 128.32 2.72UFH 21 66.05 3.02 6 71.23 11.78WFB 23 95.28 4.22 6 96.66 3.40UFB 22 105.94 3.92 5 108.55 1.01NLH 21 47.48 2.22 6 52.83 3.36NLB 21 23.36 1.61 6 23.18 1.63OBB 23 38.36 1.91 7 40.40 2.82OBH 23 34.72 1.96 7 36.36 1.83EKB 21 96.28 3.18 4 99.37 0.26DKB 24 13.33 4.07 7 11.81 2.24FRC 23 108.90 5.00 7 113.61 5.14PAC 23 107.29 5.30 7 113.67 9.02OCC 20 101.14 5.69 8 101.28 11.30FOL 22 34.05 1.71 7 35.28 1.24FOB 22 29.42 1.65 7 29.88 1.56

Spondylolysis in a Pre-contact California Population

Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

female individuals (Arriaza, 1997). And, a prehistoricJomon site in Japan reported frequencies at 12.75%(Suzuki, 1998). Archaeological samples of Inuit popu-lations were found to have spondylolysis at a rate of21.6% (Merbs, 2002). The exception appears to be insome Alaskan native populations where frequencyrates are reportedly much higher. In some populations,Stewart (1953) reports frequencies nearing 50%. And,Lester and Shapiro (1968) found the frequency to be45% among the Tigara from Point Hope, Alaska.The frequency of spondylolysis drops when later

populations are considered. Waldron (1991) foundfrequencies of 3.74%, 4.5%, and 1.42% in a Romano-British site, an Anglo-Saxon site, and a crypt fromChrist Church Spitalfields, respectively. The preva-lence in a late historic population in Hawaii was4.8% (Peitrusewsky & Douglas, 1992). And, on aver-age, the defect is found in contemporary Europeanand American populations at about 4.2% (Roche &Rowe, 1951).

The occurrence of spondylolysis among these popu-lations was compared to assess potential spatial andtemporal differences. Concerns have been raised aboutcomparing population studies based on potentialdifferences in scoring (Fibiger & Knüsel, 2005). How-ever, this is a broad analysis to make initial assessmentsabout population differences. In a chi-square analysis ofall the population frequencies listed in Table 7, signifi-cant differences were found (w2 = 517.865, p< 0.01).This would be generally expected as these populationshave widely varying frequencies and span large timeperiods and geographic locations. In a considerationof just the prehistoric populations (CA-CCo-647,CA-Ala-329, Guam, Jomon, and Archaic Alabama)the frequencies are much more similar; however, thereis still a statistically significant difference between thepopulation frequencies (w2 = 11.753, p< 0.05). Finally,in a consideration of differences just between the twoprehistoric California populations, statistically significantdifferences were found (w2 = 6.497, p< 0.05) despitesimilarities in spondylolysis frequency.

Table 6. Principal component scores using cranial metrics of male and female individuals, and both sexes based on calculated Z-scores

Female Male Both sexes

Component EigenvalueVariance

(%)Total

variance EigenvalueVariance

(%)Total

variance EigenvalueVariance

(%)Total

variance

1 5.383 29.906 29.906 5.701 31.670 31.670 4.840 26.890 26.8902 2.485 13.807 43.713 3.598 19.991 51.661 2.246 12.478 39.3693 2.239 12.441 56.154 2.931 16.282 67.943 1.861 10.340 49.7094 1.615 8.974 65.129 2.305 12.807 80.750 1.729 9.608 59.3175 1.331 7.393 72.521 1.638 9.102 89.852 1.253 6.962 66.2796 1.192 6.625 79.146 1.222 6.788 96.640 1.157 6.428 72.706

Figure 4. Dendrogram of female individuals in CA-CCo-647. The as-terisk indicates presence of spondylolysis.

Figure 5. Dendrogram of male individuals in CA-CCo-647. The aster-isk indicates presence of spondylolysis.

M. A. Pilloud and C. Canzonieri

Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

Discussion

Within CA-CCo-647, few distinctions between age andsex were identified. Similar to other studies, the defectwas only found in adult individuals. Although otherstudies report higher rates among male individuals(Arriaza, 1997; Fredrickson et al., 1984; Merbs, 2002;Weiss, 2009; Wiltse et al., 1975), this was not foundto be a statistically significant difference in the CA-CCo-647 sample. However, spondylolysis does appearto occur at a younger age among male individuals. This

is similar to other studies among hunter-gatherer Nativepopulations (Bridges, 1989; Weiss, 2009). Differences inactivities among male and female individuals couldexplain these results, specifically, activities that requirestrenuous extension and rotation of the low back.Younger male individuals may be more active andengaged in demanding hunting and fishing activitiesthat require this type of movement of the spine in thelumbar region. Activities such as net throwing or huntingwith a bow and arrow could make them more likely tosuffer acute stress fractures resulting in spondylolysis.Female individuals, on the other hand, might have beenmore subjected to repetitive injuries resulting from activ-ities focused on gathering and food preparation leadingto the appearance of spondylolysis at a later age. Whilemen likely played some role in gathering plant materialsin prehistoric California (McGuire & Hildebrant, 2004),there may be a distinct pattern here where younger maleindividuals are engaging in more strenuous activitiesresulting in spondylolysis sooner than it is seen in femaleindividuals. Alternatively, perhaps female individuals areengaging in more strenuous activities at a later age, moresimilar to that of male individuals, accounting for the agedistribution seen here. Unfortunately, there is not muchethnographic information available on the Miwok andsexual division of labour. There is also a lack of bioarch-aeological work that thoroughly addresses this topic forthe pre-contact period.The results of the biodistance analysis demonstrate

a likely genetic component, and that perhaps thereis an interaction between activity and genes in theoccurrence of spondylolysis. The sample size here isextremely small, making these interpretations prelim-inary. However, it is possible that genetics could pre-dispose one to a fracture at the pars interarticularisresulting in neural arch separation that may be aggravateddue to various activities that are stressful to this region ofthe lower spine.

Figure 6. Dendrogram with both male and female individuals afterstandardisation of size in CA-CCo-647. The asterisk indicates presenceof spondylolysis.

Table 7. Frequency of spondylolysis in various published studies

Population Time period Reference Frequency (%) N

CA-CCo-647 720–550 cal. BP — 17.4 8/46CA-Ala-329 2180–250 BP Weiss (2009) 16.4 24/146Archaic Northwestern Alabama 10 000–6000 BC Bridges (1989) 18.6 8/43Prehistoric Guam 1200–1521 AD Arriaza (1997) 21.1 8/38Late Historic Hawaii c. 1900 Peitrusewsky & Douglas (1992) 4.8 2/42Prehistoric Jomon 10 000–300 BC Suzuki (1998) 12.8 38/294Inuit 1000–1900 AD Merbs (2002) 21.6 90/417Tigara, Point Hope, Alaska 15th century Lester & Shapiro (1968) 45.0 111/248Romano-British England Appr. 1st–6th century Waldron (1991) 3.7 8/214Anglo-Saxon England Appr. 6th–11th century Waldron (1991) 4.6 5/110Spitalfields 18th–19th century Waldron (1991) 1.4 10/706Anatomical collection 19th century Roche & Rowe (1951) 4.2 178/4200

Spondylolysis in a Pre-contact California Population

Copyright © 2012 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. (2012)

The results of the biological distance analysis are alsointeresting in terms of post-marital residence practices.There does not appear to be a strong impact on geneticcomposition because of post-marital residence practicewithin CA-CCo-647; as it is possible to see phenotypic-ally similar adult male and female individuals that sharethe condition. This may speak to the genetic homogen-eity of the population or to a more endogamous practiceof post-marital residence within the Miwok than isethnographically reported.The temporal and spatial distinctions seen across

populations may relate to a variety of factors. Stewart(1953) cites unusual postural stresses for the highincident of arch defects in the Eskimo populations hestudied. Arriaza (1997) and Lessa (2011) likewisesuggest that high incidence rates of spondylolysis intheir study population are likely related to strenuousactivity. However, as these are all isolated populations,it is also likely that microevolutionary forces such asgenetic drift and a lack of gene flow were also at play.Particularly interesting are the two California popula-tions, which were significantly different in the occur-rence of spondylolysis. These two populations likelyengaged in similar activities and subsistence practices;therefore, their differences may be related to geneticisolation resulting from a lack of gene flow betweenthe two populations. However, more research is neededto verify this hypothesis. Additionally, the samplefrom CA-Ala-329 covers a large span of time (nearly2000 years), which may affect spondylolysis prevalencerates as temporal changes in activity pattern, gene flow,or genetic drift can be incorporated. The sampledescribed in this study covers a span of approximately200 years, representing a much more confined periodof time.Based on the results of this analysis, it appears that the

aetiology of spondylolysis cannot be related to a singlecause. Instead, the interaction of two factors (genes andactivity) likely accounts for the variation seen bothwithin and between populations in various geographicand temporal settings. However, results must be tem-pered by the fact that the sample size is extremely smallin this study, which may affect results. Future researchshould incorporate larger sample sizes with a morerobust data set, which would ideally include dentalmetrics and morphology as well as cranial non-metricsin a biological distance analysis.

Conclusions

Within this prehistoric California population, onlythe lower lumbar (L4 and L5) of adults displayed

spondylolysis. Significant differences were not foundbetween male and female individuals or between agecohorts, with the exception of young adults, wherethe defect occurs more frequently in male individuals.This finding may be related to differences in activitiesbetween male and female individuals in general, andthe age in which they engage in these activities. Therealso appears to be a connection between genes and theoccurrence of spondylolysis. Individuals (male andfemale) displaying spondylolysis cluster in a biologicaldistance analysis of craniometrics, suggesting a geneticcomponent to the defect. Differences between variouspopulations also suggest that there is a link betweenspondylolysis, activity patterns, and genes. Genes maypredispose one to neural arch separation that is aggra-vated by various repetitive activities resulting in spondy-lolysis. This study builds upon previous research bylinking both activity and genes in an archaeologicalpopulation to construct a more robust view of theaetiology of spondylolysis. However, future research isneeded to examine this connection in more detail withlarger sample sizes.

Acknowledgments

We thank Andrew Galvan, an Ohlone/Bay Miwok man,and Most Likely Descendant on this project. BasinResearch Associates Inc. provided use of their extensivelibrary and support on graphics and access to data.Joseph T. Hefner provided valuable comments onthis paper.

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