American Journal of Physical Anthropology Volume 135 Issue 4 2008Claudia Rojas-Sepúlveda; Paleoepidemiology of Vertebral Degenerative Disease in a Pr

Paleoepidemiology of Vertebral Degenerative Disease ina Pre-Columbian Muisca Series From Colombia

Claudia Rojas-Sepulveda,1 Yann Ardagna,1 and Olivier Dutour1,2*

1Unite dAnthropologie: Adaptabilite biologique et culturelle, UMR 6578, Universite de la Mediterranee,Faculte de Medecine, 13385 Marseille cedex 5, France2Department of Anthropology, University of Toronto, Toronto, ON, Canada M5S 2S2

KEY WORDS osteoarthritis; DJD; spine; occupational stress; South America

ABSTRACT Major manifestations of vertebral degen-erative joint disease were observed on a Pre-ColumbianMuisca series from the Soacha Cemetery (11th to 13thcenturies) Colombia, South America. In total, 1,646 verte-brae of 83 individuals were examined. Osteophytes, verte-bral body joint surface contour change (lipping), and ver-tebral body pitting were evaluated for each vertebral body.For apophyseal joints, joint surface contour change, pit-ting, and eburnation were recorded. Two methods of fre-quency calculation and ve for vertebral degenerative dis-ease diagnosis were applied and compared, allowing dis-cussion of methodological considerations. Our studyshowed that 83% of individuals and 32% of vertebrae were

classied as positive when diagnosed by the presence of atleast one of the following manifestations: osteophytes, ver-tebral body joint surface contour change (lipping), apo-physeal joint surface contour change, or eburnation(method called Pitting excluded). No signicant differen-ces were found between the sexes. In the youngest cohort(1530 years), 65% of individuals and 10% of vertebrae ex-hibit at least one of the previously mentioned manifesta-tions. High prevalences suggest a high level of physical ac-tivity beginning in childhood which may have acceleratedthe aging process in this Pre-Columbian population. His-torical data are compatible with this hypothesis. Am JPhys Anthropol 135:416430, 2008. VVC 2008 Wiley-Liss, Inc.

Among manifestations of life conditions observed onbones, degenerative joint disease (DJD) is most common.This disease has been the subject matter of a number ofresearch projects in paleopathology for several reasons.First of all, DJD has affected animals and humansthroughout prehistory; second, it is the most frequentlyobserved disease among archaeological series; and third,DJD affects living populations (Ortner and Putschar,1981; Cohen, 1984; Peyron, 1986; Bridges, 1992; Thil-laud, 1992). Additionally, DJD can be related to manyvariables: age, sex, trauma, genetic predisposition (meta-bolic and endocrine factors), and biomechanical stress orphysical activity (Ingelmark, 1959; Nathan, 1962; Ortnerand Putschar, 1981; Goodman et al., 1984; Ubelaker,1984; Peyron, 1986; Larsen, 1987; Rogers et al., 1987;Bridges, 1992; Jurmain and Kilgore, 1995; Rogers andWaldron, 1995; Resnick, 2002; Ortner, 2003). The ques-tion of the relationship between DJD and the level ofphysical activity is still debated. According to somescholars, several studies demonstrate a positive relation-ship between DJD and stress (Jurmain, 1990; Bridges,1991, 1992). However, others have suggested that thesemanifestations are only consequences of the aging pro-cess (Bourke, 1967; Waldron, 1991, 1992).Because of its structure, the human spine plays an im-

portant role in the study of degenerative disease andoccupational stress (Chapman, 1972; Clark and Del-mond, 1979; Ortner and Putschar, 1981; Goranov et al.,1983; Jurmain, 1990; Bridges, 1991, 1992; Lovell, 1994;Stirland and Waldron, 1997; Kahl and Ostendorf, 2000;Sofaer, 2000; Campo, 2003). Nevertheless, some authors,seeing its pattern as a mirror of the natural curvaturesof the spine, relate the location of this disease in thespine directly to human bipedality (Jankauskas, 1992;Knusel et al., 1997; Weber et al., 2003). Some paleopa-thologists have taken into account results of clinical

research on living people who perform high levels ofphysical activity, such as athletes or laborers, as well asdata from veterinary research. Khal and Ostendorf(2000) present an extensive review of this literature.Although it is hazardous to link the pattern of physi-

cal activity markers to any specic occupation (Dutour,1992; Waldron, 1994; Rogers and Waldron, 1995), somestudies have evaluated the impact and pattern of degen-erative disease manifestations, particularly in the spine,to reconstruct a part of a past populations lifestyle andits relationship with the environment (Cohen and Arme-lagos, 1984). Signicant research has described the pat-tern and prevalence of vertebral degenerative disease incertain geographical areas. Specic works have beenpublished, especially for past populations from NorthAmerica (Chapman, 1972; Clark and Delmond, 1979;Jurmain, 1990; Bridges, 1989, 1991, 1992; Kahl andOstendorf, 2000; Merbs, 2001); Europe (Berato et al.,1990; Jankauskas, 1992; Waldron, 1991, 1992; Knuselet al., 1997; Sofaer, 2000; Weber et al., 2003) and someothers in Asia (Lovell, 1994; Hukuda et al., 2000). Untilnow, paleoepidemiology of DJD in South America is

Grant sponsor: French Ministry of Education and Research.

*Correspondence to: Olivier Dutour, Department of Anthropology,University of Toronto, 19 Russell Street, Toronto, ON, Canada M5S2S2 (or) Unite dAnthropologie biologique, UMR 6578, Faculte deMedecine, 27 Boulevard Jean Moulin, 13385 Marseille, France.E-mail: [email protected]

Received 17 November 2006; accepted 15 October 2007

DOI 10.1002/ajpa.20762Published online 10 January 2008 in Wiley InterScience

(www.interscience.wiley.com).

VVC 2008 WILEY-LISS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 135:416430 (2008)

poorly documented. Current literature is focused mostlyon individual case studies (Gerszten et al., 2001) withoutthe benet of an epidemiological approach, while otherspresent mainly general paleopathological overviews orthe epidemiology of different diseases, being notablyfocused on Peruvian and Chilean samples.The aim of this article is to present the results of the

paleoepidemiological study of vertebral degenerative dis-ease on a Pre-Columbian Muisca series from the Sabanade Bogota in Colombia (South America). As previous bio-archaeological studies have highlighted the presence ofDJD in this series as linked to life conditions and activ-ities (Rodrguez, 1999), specic research on vertebralstructures has the potential to further elucidate thisissue. On the basis of a populational approach, ourresults can contribute to the debate about DJD andphysical activity.Methodological considerations related to the calcula-

tion of frequencies of vertebral disease and diagnoses arepresented here. The goal of this article is twofold: i) toshow how different conclusions in paleoepidemiologymay be reached depending on methods of reconstructionof past prevalence; and ii) to propose a method for stand-ardizing comparisons between studies, which currentlyremains difcult.

MATERIALS

Muisca culture

The Muiscas was a large Chibcha-speaking agricul-tural society that developed in the plateau of Cundina-marca and Boyaca, on the Eastern Range in present-daycentral Colombia (South America) (see Fig. 1), chronolog-ically dated between 700 and 1600 AD (Langebaek,1995; Rodrguez, 1999). Specialists from various disci-plines have discussed the Muisca cultures origin, as wellas its social and political systems (Enciso and Therrien,2000).At the time of the Spanish Conquest, the Muiscas

were living as confederations of chiefdoms, a period ofexpansion and unication characterized by intensivemilitary activity, which may have led to a state level po-litical structure (Broadbent, 1964; Tovar, 1980; Lange-

baek, 1995; Langebaek, 1998; Langebaek, 2000). Muiscasociety was stratied (Zubiria, 1986; Rodrguez, 1999),some groups were subject to the absolute power of a sin-gle chief (Broadbent, 1964; Tovar, 1980). Political and re-ligious power were closely linked (Londono, 1996).Chiefs, priests, and their families had the highest status,being recipients of special treatment even after deathwhen they were mummied and richly ornamented. Atthe time of European contact, the Muiscas practicedpolygyny, exogamy, and matrilineal inheritance (Broad-bent, 1964; Londono, 1996; Langebaek, 1998; Rodrguez,1999). They took advantage of the ecological diversity oftheir territory where altitude variation resulted inresource variability (The vertical archipelago (Murra,1972, 1981). The Muiscas practiced microvertical exploi-tation, applied technological developments such as hy-draulic systems (canals for water control and terracing),and had contact with their neighbors living at lower ele-vation or established Muisca families in those territories(Botiva, 1989; Langebaek, 1998; Rodrguez, 1999). Theywere maize agriculturalists, hunters, gatherers, shers,craftsmen, (potters, goldsmiths, weavers), emerald andsalt miners, and traders with an extensive trading net-work (Duque, 1945; Rodrguez, 1999; Groot, 2000).

The series

The study sample is from the Muisca cemetery of Soa-cha-Portalegre, excavated in 1987 by archaeologists ofthe Instituto Colombiano de Antropologa. Recovered inthe middle of the urban settlement, the cemeterys popu-lation and physical extent are undocumented (Botiva,1989; Boada, 2000). Apparently, the entire present-dayvillage was a large Muisca cemetery inhabited betweenthe 11th and 13th centuries (Reichel-Dolmatoff, 1943,n.d.; Rodrguez, 1994, 1999). According to the literaturetwo uncalibrated 14C dates are available: 1035 6 115 ADfor tomb 45; and 1230 6 110 AD for tomb 35 (Boada,2000; Etxeberria et al., 1997). Traces of four bohos(constructions mainly made of wood) were found duringexcavation, as were fragments of ceramic, stone andmetal objects, sea shells, animal remains as well as 133

Fig. 1. Muisca territory in the central area of Colombia(South America). [Color gure can be viewed in the online issue,which is available at www.interscience.wiley.com.]

Fig. 2. Stages recorded for the manifestations of vertebraldegenerative conditions in the vertebral body (osteophytes, jointsurface contour change or lipping, and pitting). [Color gurecan be viewed in the online issue, which is available at www.interscience.wiley.com.]

417PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

American Journal of Physical Anthropology

tombs. No European objects were recovered, indicatingthat the site belongs to a period earlier to the Conquest(Botiva, 1988, 1989). According to archeological studieson funerary habits and objects, this cemetery, or at leastthe excavated part of it, was where members of lowersocial class, and probably some warriors were buried(Boada, 2000; Rodrguez, 1994, 1999). The total numberof recovered individuals is 135; 36 of them are children,99 are adults (64 female, 39 male). The low proportion ofyoung individuals has been ascribed to archaeological(cemetery partially excavated) and cultural factors (chil-dren buried in a different place) (Rodrguez, 1994, 1999).Bioanthropological studies on this series have found agood general health condition for these individuals,apparently they did not suffer any nutritional stress;nevertheless, these studies have observed that femalescondition seems to be inferior to that of males (Rodr-guez, 1994, 1999).For this research, we studied the vertebral columns of

male and female individuals of the series (15 to 451years of age) represented by at least six vertebrae. Sam-ple composition is presented in Table 1, representing atotal of 83 vertebral columns.

METHODS

Data collection

We inspected each vertebra of every skeleton includedin our study. An individual recording system wasemployed following the recommendations of Campo Mar-tin (1997, 2003) and Buikstra and Ubelaker (1994). Datarecorded for each individual include age, sex, preserva-tion state and vertebral manifestations of DJD. Sexdetermination and age estimation were made by conven-tional anthropological methods (Brothwell, 1965; Iscanet al., 1984, 1985; Suchey and Brooks, 1988).A complete evaluation of vertebral preservation was

done. For the vertebral body, four codes were employed:Complete, when more than the 75% of the body waspresent; Incomplete, when its presence was between 25and 75%; Very incomplete, when less than 25% wasfound; and, Absent when it was not assessable. For theright and left vertebral arches, the presence of the supe-rior and inferior apophyseal joints was recorded usingthe same codes.All morphological changes were macroscopically

observed and recorded by the same researcher to avoidinterobserver error. Some vertebral columns were eval-uated several times over a period of time to verify the di-agnosis and the reliability of the recorded information.Concerning terminological usage, degenerative condi-

tions of the spine are frequently named spinal DJD.However, it should be noted that the joints of the spinehave fundamental anatomic differences and they do notdeteriorate identically (Resnick, 2002).These differenceshave led some authors to distinguish changes in the ver-

tebral bodies known as Intervertebral Disc Degenera-tion or Degenerative Disc Degeneration, from thoseobserved in the synovial joints named Apophyseal JointOsteoarthritis (Resnick, 2002). Accordingly, we observedand separately recorded manifestations for these twolocalizations, the vertebral body and the apophysealjoints.For the vertebral body we recorded osteophytes, joint

surface contour change (lipping), and pitting. Forthe apophyseal joints, joint surface contour change(lipping), pitting, and eburnation were recorded.Osteophytes are also referred to as marginal prolifera-

tion; they are new bone growths which arise around thejoint margins (Nathan, 1962; Rogers et al., 1987; Rogersand Waldron, 1995). Joint surface contour change hasalso been referred to as remodeling of joint contours orfacet remodeling; it may produce attening and/orenlargement of joint surfaces, being a proliferative reac-tion (Rogers et al., 1987). Facet remodeling, especially ofapophyseal joints, is an important response to appliedpressure, thus being a very good indicator of repeatedactivity-induced stress in humans (Sofaer, 2000). Osteo-phytes (OP) were distinguished from joint surface con-tour change in the vertebral bodies. While OP refers tolocalized growths commonly known as parrots beak,joint surface contour change was recorded as a ring-shaped manifestation around body margins. Pitting ormicroporosity has been dened as the discontinuity ofthe subchondral bone which manifests as a pitted anddisorganized lesion (Rothschild, 1997). Ortner (2003)describes erosion as a subchondral surface breakdown,where the underlying trabeculae of the bone may beexposed.1 Eburnation, described as an ivory like as-pect, is a severe subchondral bone reaction; it is theshiny or polished area found on an articular surface,the product of bony joint surfaces rubbing after losing allthe cartilage between them. Eburnation is consideredpathognomonic of the disease (Rogers et al., 1987; Bridges,1992; Rogers and Waldron, 1995) or a marker of its se-verity (Rothschild, 1997; Ortner, 2003); in any case, it isa clear manifestation of DJD.A stage or score was assigned to each bone change on

a scale from 0 to 3: the Code 0 for absent; 1 for barelyvisible; 2 for moderate; and 3 for severe. An illustrationof the scoring system is shown in Figures 2 and 3. Formore severe manifestations Code 4 may be assigned. Thestage method seems to be subjective, but it has beenextensively used in the literature (Nathan, 1962; Chap-man, 1972; Clark and Delmond, 1979; Bridges, 1989;Jurmain, 1990; Lovell, 1994; Kahl and Ostendorf, 2000;Sofaer, 2000; Weber, 2003). A code for damaged elementswas also assigned unobservable.For vertebral bodies, superior and inferior surfaces

were observed and manifestations recorded separately.Vertebral ankylosis produced in disorders other thanDJD (such as DISH, ankylosing spondylitis, congenitalfusion) was excluded. Special attention was paid to dif-ferentiate the lesions according to their main cause(Rogers et al., 1987). For C1, the facet joint for the C2odontoid process was evaluated for joint surface contourchange and pitting but not for osteophytes (because wedened joint surface contour change as a ring-shapedmanifestation while osteophytes as a localized one).Even if superior, inferior, right and left apophyseal joints

TABLE 1. Age and sex composition of the sample

Young(1530)

Middle age(3045)

Old(451) Adult Total

Female 12 18 15 1 46Male 13 13 8 0 34Indeterminate 1 0 0 2 3Total 26 31 23 3 83

1Ortner does not mention the word pitting, but these descrip-tions are similar to that recorded in our study.

418 C. ROJAS-SEPULVEDA ET AL.


were recorded independently, almost all differences be-tween them were not statistically signicant; hence, theresults concerning the apophyseal joints consider themas a whole. Four vertebral columns with a 6th lumbarvertebra were found; these vertebrae were excluded fromthe calculations.

Frequency calculations

The state of bone preservation may result in variationin disease prevalence. For this reason, calculation of fre-quencies and prevalences were made taking into accountonly the observable aspects (Waldron, 1994). As dened

by Waldron (1994), paleoepidemiological prevalence isbased on modication of the n/N ratio, being n (thenumerator) the total number of affected individuals oranatomical elements and N (the denominator) the totalnumber of observable individuals or anatomical ele-ments. Our method is based on modication of the nu-merator and the denominator. Variation of the numera-tor depends on diagnostic criteria for a vertebra, a verte-bral region or a whole vertebral column (counted aspositive). Denominator variation is limited by the stateof preservation for individual or anatomical elements(vertebra, region, whole vertebral column). To evaluatethe presence of vertebrae and their elements (preserva-tion state), the numerator is the number of vertebraefound and the denominator is the theoretical number ofvertebrae (assuming 7 vertebrae for cervical, 12 for tho-racic, and 5 for lumbar).Two methods were used to analyze manifestation fre-

quencies and vertebral degenerative disease prevalencein the vertebral regions or in the whole vertebralcolumn:

Frequency by individual (FI) is the proportion of verte-bral regions or vertebral columns affected, wherethe numerator is the number of individuals whichhad the manifestation or positive diagnosis of verte-bral degenerative conditions and the denominator isthe total of individuals who had at least one verte-bra observable for the manifestation considered inthe region or in the vertebral column. When thesample was divided by population groups, the de-nominator was the number of individuals of the cho-sen age and sex category who presented at least onevertebra in the observed region or in the vertebralcolumn.

Frequency by vertebra (FV) is the proportion of vertebraeinvolved, where the numerator is the number of ver-tebrae affected by one manifestation or the numberof vertebrae classied as positive for degenerative

Fig. 3. Stages recorded for the manifestations of vertebraldegenerative conditions in the apophyseal joints (pitting, jointsurface contour change or lipping, and eburnation). [Color g-ure can be viewed in the online issue, which is available atwww.interscience.wiley.com.]

Fig. 4. Pitting (A), joint surface contour change (B), and osteophytes (C) in the vertebral bodies of the Soacha Muisca series byvertebrae. [Color gure can be viewed in the online issue, which is available at www.interscience.wiley.com.]



conditions, and the denominator is the total numberof vertebrae found for the corresponding region orfor the vertebral column in the considered age andsex category (Hukuda et al., 2000).

Diagnostic methods and vertebral degenerativedisease prevalence calculations

Because of the lack of consensus among researchers,we used ve diagnostic methods dened as follows.

At least One. For this method one vertebra, one region,or one individual (whole vertebral column) was consid-ered positive if it presented at least one manifestation(osteophyte, body joint surface contour change, body pit-ting, apophyseal joint surface contour change, apophy-seal pitting or eburnation).

Two together. In this method, if eburnation was notpresent, at least two of the other manifestations (osteo-phytes, joint surface contour change or pitting) had to bepresent in a single vertebra to make a positive diagnosis.According to Rogers and Waldron (1995) eburnation ispathognomonic of DJD; if eburnation was present, thevertebra, the vertebral region or the individual were con-sidered also positive. If one vertebra was consideredpositive, the corresponding entire region and entirevertebral column was also considered positive.

Two separated. This is a variant of the previouslydescribed method, following the criteria for the diagnosisin the vertebra. In the region and in the whole vertebralcolumn, eburnation alone made the diagnosis positive,as well the presence of two of the other manifestations(osteophytes, joint surface contour change or pitting),but in this case even if they were not in the same verte-bra. This means that if in the region or in the whole ver-tebral column one vertebra presented osteophytes (orjoint surface contour change) and another pitting, thatwas enough to classify it as positive. Hence, any iso-lated vertebra were not classied as positive.

Only Eburnation. Because eburnation is pathogno-monic, this method restricted the diagnosis to eburna-tion presence or absence; only the presence of eburnationmade a vertebra, a region or a vertebral column pos-itive. As published data has been obtained with thesecriteria (Waldron, 1992), it is interesting to compare thismethod with the others.

Pitting excluded. Some authors have considered pittingas a bone change which is not related to DJD (Roths-child, 1997; Sofaer, 2000). According to this method, thepositive diagnosis was recorded when any of theobserved manifestations was present excluding pitting(on vertebral body or apophyseal joints). Contrary to Atleast One, here isolated pitting was not enough to clas-sify the considered entity as positive.The calculations were made as follows:For a specic vertebra, n (the numerator) was the

number of vertebrae considered as positive accordingto the diagnostic method applied and N (the denomina-tor) was the number of specic vertebrae coded as pres-ent.For the anatomical region (cervical, thoracic, or lum-

bar), when the FI was calculated, the numerator was thenumber of individuals coded as positive in the regionaccording to the diagnostic method and the denominator

was the number of individuals with at least one vertebrain the region. When the FV was calculated, the numera-tor was the number of vertebrae coded as positiveaccording to the diagnostic method and the denominatorwas the total number of vertebrae coded as present inthe region.For the whole vertebral column, when the FI was cal-

culated, the numerator was the number of individualsconsidered positive according to the diagnostic methodand the denominator was the number of individualswith at least one vertebra coded as present in the verte-bral column. When the FV was calculated, the numera-tor was the number of vertebrae coded as positiveaccording to the diagnostic method and the denominatorwas the total number of vertebrae coded as present.Comparisons between sex and age groups were con-

ducted. The signicance of the differences between fre-quencies was calculated by applying chi-square (v2) tests(P 0.05). To apply v2 tests, expected frequencies mustbe higher than 4, thus, stages 1, 2, and 3 were pooled(d.f. 5 1).

RESULTS

Preservation

Each vertebra is present over 50% of the time. Themost frequently found vertebra was T2 (76/83), whileT12 was the least often recorded vertebra (51/83). Goodpreservation state of the vertebrae made almost alwayspossible the identication and location of each one ofthem. C5 is the qualitatively best preserved vertebra(64/83 coded as complete), while T6 was the least com-monly coded as complete (31/83). From C1 to T7 and forthe whole lumbar region, the presence of the elements isup to 60%. In the cervical region, the presence of com-plete vertebrae was recorded over 50% of the time, inthe other regions, complete vertebrae were recordedaround 40% of the time.The cervical region is the best represented with 488

vertebrae present (83.99%, assuming seven cervical ver-tebrae by individual). The rst sacral vertebra is presentin 69 vertebral columns (83.13%, assuming one sacralvertebra by individual). The lumbar region is repre-sented by 322 vertebrae (77.59%, assuming ve lumbarvertebrae by individual), and the thoracic region is rep-resented by 768 vertebrae (77.11%, assuming twelve tho-racic vertebrae by individual). A total of 1,646 vertebraewere observed and coded. The preservation in differentsex and age categories is similar. In each vertebralregion, at least 73% of vertebrae with at least 1/4 of thebody were observed.Apophyseal joints were well preserved too, varying

from 60 to 82% for the different regions. The superiorapophyseal joints are better represented than the infe-rior ones, but these differences are statistically signi-cant only for the thoracic region. Differences of preserva-tion between right and left side are not signicant.

Type of pathological conditions

Vertebral body. Table 2 presents the frequencies andpercentages (FI and FV) of recorded manifestations inthe complete sample and in the groups by sex, providingresults for each vertebral region and for the whole verte-bral column. For complete vertebral columns, Table 2shows that pitting is the most frequently encounteredmanifestation in the entire series when the calculation is



made by FI (68.7%); nevertheless, no signicant differen-ces were found when compared with the other manifes-tations (see Table 3). Concerning the results obtained bythe FV for the bodies of the whole vertebral column,joint surface contour change is the most often recorded(20.1%). Differences between manifestations in thebodies are not signicant for osteophytes and body pit-ting (Table 3). Joint surface contour change is also themanifestation most frequently recorded as Stage 3 onvertebral bodies compared with the other studied mani-festations, as shown in Figure 4.For the cervical region, pitting is the most frequently

found manifestation with 60.8% of individuals affectedand 24.6% of the vertebrae (Table 2). Figure 4 showsthat pitting is classied very frequently as Stage 3 inthe cervical region. In the thoracic region osteophytes

are the most frequent manifestation; of 66 thoracicregions, 26 exhibit the manifestation; and of 544 verte-brae, 67 are positive for osteophytes. In the lumbar ver-tebrae, joint surface contour change presents the highestfrequencies, it affects 52% of the individuals and 36.8%of the vertebrae (see Table 2).Osteophytes are more frequent (40.8% of individuals

and 21.2% of vertebrae) and most often classied asStage 3 in the lumbar region (see in Fig. 4). Chi-squaretests show no signicant differences between the pres-ence of osteophytes in the three regions if the proportionis calculated by individuals, but signicant when com-paring FV between lumbar region and the other two(Table 4). Joint surface contour change also affects thelumbar region most often; nevertheless, no signicantdifference was found between lumbar and cervical regions

TABLE 3. Chi-square (v2) and P-values for manifestations in the whole vertebral column

Differences between manifestations (whole vertebral column)

FI FV

v2 P v2 P

Vertebral bodyOsteophytes-cont change 0.626 0.429 19.822 0.000Ostophytes-body pitting 2.574 0.109 0.017 0.895Contour change-body pitting 0.668 0.414 21.124 0.000

Apophyseal jointsAp. contour change-Ap.pitting 15.966 0.000 76.377 0.000Ap. contour change-eburnation 8.780 0.003 55.416 0.000Ap.pitting-eburnation 43.915 0.000 243.1 0.000

Signicant values are in bold.FI, frequencies by individual; FV, frequencies by vertebra.

TABLE 2. Observed manifestations in the anatomical regions of the vertebral column in the whole sample and by sex categories

Females (all ages) Males (all ages) Whole series

FI FV FI FV FI FV

n/N % n/N % n/N % n/N % n/N % n/N %

CervicalOsteophytes 12/43 27.9 27/234 11.5 8/31 25.8 11/176 6.3 22/77 28.6 41/430 9.5B. change 22/42 52.4 61/230 26.5 14/32 43.8 32/178 18.0 37/77 48.1 94/427 22.0Body pitting 26/44 59.1 67/268 25.0 14/32 43.8 49/199 24.6 48/79 60.8 120/487 24.6Ap. Change 21/42 50.0 50/248 20.2 11/32 34.4 27/183 14.8 32/77 41.6 77/448 17.2Ap. pitting 33/41 80.5 86/255 33.7 23/32 71.9 63/187 33.7 57/76 75.0 150/459 32.7Eburnation 12/43 27.9 28/250 11.2 8/32 25.0 17/185 9.2 20/78 25.6 45/451 10.0

ThoracicOsteophytes 16/36 44.4 38/205 18.5 10/27 37.0 28/221 12.7 26/66 39.4 67/544 12.3B. change 12/35 34.3 27/303 8.9 6/27 22.2 18/221 8.1 19/65 29.2 49/537 9.1Body pitting 8/44 18.2 28/422 6.6 3/30 10.0 5/287 1.7 11/77 14.3 33/735 4.5Ap. Change 17/42 40.5 37/346 10.7 10/31 32.3 27/236 11.4 28/76 36.8 68/609 11.2Ap. pitting 31/43 72.1 88/356 24.7 26/31 83.9 78/237 32.9 59/77 76.6 175/620 28.2Eburnation 7/43 16.3 9/344 2.6 7/31 22.6 19/232 8.2 14/77 18.2 28/601 4.7

LumbarOsteophytes 24/38 63.2 43/171 25.1 10/31 32.3 22/128 17.2 29/71 40.8 65/306 21.2B. change 24/41 58.5 75/171 43.9 14/32 43.8 34/127 26.8 39/75 52.0 112/304 36.8Body pitting 22/43 51.2 47/217 21.7 11/32 34.4 18/149 12.1 33/76 43.4 65/371 17.5Ap. change 22/41 53.7 58/174 33.3 11/29 37.9 31/121 25.6 34/71 47.9 91/300 30.3Ap. pitting 30/41 73.2 71/172 41.3 19/31 61.3 41/125 32.8 50/73 68.5 114/302 37.7Eburnation 7/43 16.3 26/165 15.8 3/27 11.1 5/115 4.3 19/70 27.1 32/285 11.2

Whole vertebral columnOsteophytes 28/46 60.9 136/710 19.2 17/34 50.0 61/525 11.6 47/83 56.6 173/1280 13.5B. change 30/46 65.2 163/704 23.2 21/34 61.8 84/523 16.1 52/83 62.7 255/1268 20.1Body pitting 31/46 67.4 142/907 15.7 24/34 70.6 72/635 11.3 57/83 68.7 218/1593 13.7Ap. Change 35/46 76.1 145/768 18.9 17/33 51.5 85/540 15.7 55/83 66.3 236/1357 17.4Ap. pitting 43/46 93.5 245/783 31.3 30/33 90.9 182/549 33.2 76/83 91.6 439/1381 31.8Eburnation 22/46 47.8 63/759 8.3 12/33 36.4 41/532 7.7 36/83 43.4 105/1337 7.9

Row frequencies showed as n/N.FI, frequency by individual; FV, frequency by vertebra.



for FI (P 5 0.626). However, signicant differences arefound for the FV between the three regions (see Table 4).The cervical region is the most often affected by pitting(48/79 individuals and 120/487 vertebrae), followed bythe lumbar region (33/76 individuals and 65/371 verte-brae), which demonstrates the strongest expressions ofthe condition (see Fig. 4). For pitting, all differencesbetween regions are signicant for FV and FI.Sex comparisons: The pattern in female and male ver-

tebral body manifestations is very similar to those forthe entire group (Table 2). Nevertheless, osteophytes andjoint surface contour change are slightly more frequentin females and pitting in males. Osteophytes are presentin 60.9% of the females and 50% of the males and in19.2% of female vertebrae and 11.6% of male vertebrae.Joint contour change is present in 65.2% of females and61.8% of males and in 23.2% of female vertebrae and16.1% of male vertebrae. To compare the presence of themanifestations between the groups by sex, v2 tests wereapplied; results are included in Table 4. There we seethat differences between FI of the different manifesta-tions in female and male vertebral bodies are not signi-cant. But when FV is calculated, females are more sig-nicantly affected by the three manifestations.Age comparisons: Table 5 presents the frequencies of

the manifestations studied in the three age groups, inthe three regions, and in the whole vertebral column.In the youngest group (1530 years), all the manifesta-tions are less frequent than in middle-aged (3045 years)and old (451) groups. Signicant differences wererevealed by v2 mostly between the youngest group andthe other two (Table 4). In the youngest group (1530years), the most frequent manifestation is pitting (44%of the individuals and 2.8% of the vertebrae). Pitting inmiddle-age is present in 71% of the individuals and14.6% of the vertebrae; while in 91.3% of the old individ-uals pitting is present and in 26.6% of their vertebrae.Nevertheless, these groups do not differ signicantly(Table 4). For the middle-age group, the most frequentmanifestation is joint surface contour change (83.9% ofthe individuals and 29% of vertebrae), and in the oldestindividuals the most frequent is joint surface contourchange (78.3% of the individuals and 28.7% of the verte-brae) and also pitting (91.3% of the individuals and26.6% of the vertebrae).

Apophyseal joints. Differences in manifestation fre-quencies among the superior right, superior left, inferiorright, and inferior left apophyseal joints are not signi-cant (Table 6). Accordingly, we pooled the results.Frequencies of manifestations studied in the apophy-

seal joints are presented in Tables 2 and 5. In Table 2,for the whole series, pitting is the most frequent mani-festation on apophyseal joints (91.6% of the individualsand 31.8% of the vertebrae), followed by joint surfacecontour change (66.3% of the individuals and 17.4% ofthe vertebrae), and nally by eburnation (43.4% of theindividuals and 7.9% of the vertebrae). The differencesbetween manifestations are signicant (see Table 3).Table 2 and Fig. 5 show that the same pattern is repeatedin the three vertebral regions. Joint surface contourchange is more frequent and more often classied asStage 3 in the lumbar region (47.9% of the individualsand 30.3% of the vertebrae) and, second, in cervical ver-tebrae (41.6% of the individuals and 17.2% of vertebrae).Between regions, differences in the presence of the mani-

TABLE4.Chi-square

(v2)andP-values

formanifestationsin

thevertebralregions,byageandsex

Differencesbetweenregions

Sex

differ.

Differencesbetweenage-groups

Cerv-thor

Cerv-lumb

Thor-lumb

Male-fem

ale

You

ng-m

idd

You

ng-old

Middage-old

v2P

v2P

v2P

v2P

v2P

v2P

v2P

Vertebralbody

Frequen

cybyindividuals

Osteophytes

1.867

0.172

2.464

0.116

0.030

0.863

0.939

0.333

10.605

0.001

11.958

0.001

0.241

0.623

Con

t.change

5.228

0.022

0.237

0.626

7.440

0.006

0.101

0.751

20.256

0.000

14.108

0.000

0.275

0.600

Bodypitting

35.813

0.000

4.667

0.031

15.847

0.000

0.093

0.760

4.159

0.041

12.063

0.001

3.367

0.067

Frequen

cybyvertebrae

Osteophytes

1.884

0.170

24.747

0.000

11.894

0.001

12.785

0.000

67.651

0.000

72.352

0.000

0.288

0.591

Con

t.change

31.279

0.000

36.217

0.000

96.341

0.000

9.388

0.002

97.144

0.000

90.810

0.000

0.006

0.940

Bodypitting

108.6

0.000

4.109

0.043

38.736

0.000

5.825

0.016

44.915

0.000

108.8

0.000

22.700

0.000

Apophysealjoints

Frequen

cybyindividuals

Ap.change

0.357

0.550

0.599

0.439

1.836

0.175

5.157

0.023

13.531

0.000

10.326

0.001

0.046

0.830

Ap.pitting

0.055

0.815

0.779

0.378

1.247

0.671

Eburnation

1.259

0.262

0.043

0.836

1.691

0.193

1.030

0.310

4.424

0.035

4.057

0.044

0.002

0.967

Frequen

cybyvertebrae

Ap.change

12.252

0.000

17.830

0.000

51.165

0.000

2.156

0.142

47.482

0.000

83.709

0.000

8.340

0.004

Ap.pitting

17.246

0.000

2.065

0.151

8.557

0.003

0.513

0.474

8.221

0.004

70.753

0.000

35.854

0.000

Eburnation

11.288

0.001

0.291

0.589

13.214

0.000

0.149

0.700

21.580

0.000

34.910

0.000

2.620

0.106

Signicantvalues

are

inbold.



festations by individual are not signicant in any case,but they are when the FV is observed (Table 4).When FI is calculated, pitting is more frequent in the

thoracic region (59/77 individuals) followed by the cervi-cal region (57/76 individuals), and nally by the lumbarregion (50/73 individuals). Nevertheless, no signicantdifferences were found by v2 between the frequencies byindividual for pitting in the regions (Table 4). If calcula-tions are made by FV, the lumbar region exhibits thehighest prevalence of pitting (114/302 vertebraeobserved) after cervical (175/620 vertebrae) and nally,thoracic (150/459 vertebrae). In this case, signicant dif-ferences are found (Table 4). The least frequent manifes-tation in the three regions is eburnation. In the lumbarregion, 27.1% of the individual and 11.2% of vertebrae

exhibit eburnation. In cervical vertebrae it is present in25.6% of the individual and 10% of the vertebrae. In tho-racic, eburnation was recorded in 18.2% of the individu-als and 4.7% of the vertebrae. There are no signicantdifferences between regions for FI, and the only signi-cant difference for FV is between thoracic and the othertwo regions, but not between cervical and lumbar (seeTable 4).Sex comparisons: The pattern of involvement is the

same in female and male individuals as described for theapophyseal joints of the whole series (pitting, joint sur-face contour change and eburnation). Apparently,females are more affected than males (Table 2), but thedifferences are not signicant, for FI or FV (with theexception of joint contour change P 5 0.023) (Table 4).

TABLE 5. Observed manifestations in the anatomical regions of the vertebral column by age categories

Young (1530) Middle (3045) Old (451)

FI FV FI FV FI FV

n/N % n/N % n/N % n/N % n/N % n/N %

CervicalOsteophytes 2/24 8.3 2/132 1.5 6/29 20.7 13/163 8.0 11/20 55.0 20/111 18.0B. change 3/23 13.0 7/130 5.4 18/30 60.0 51/163 31.3 14/20 70.0 32/111 28.8Body pitting 9/24 37.5 11/152 7.2 19/31 61.3 50/182 27.5 17/20 85.0 54/129 41.9Ap. change 2/23 8.7 2/138 1.4 15/30 50.0 30/166 18.1 14/20 70.0 44/125 35.2Ap. pitting 11/21 52.4 33/142 23.2 24/31 77.4 52/170 30.6 19/20 95.0 61/127 48.0Eburnation 1/23 4.3 1/139 0.7 11/31 35.5 22/169 13.0 7/20 35.0 20/124 16.1

ThoracicOsteophytes 1/20 5.0 2/176 1.1 12/24 50.0 33/179 18.4 13/18 72.2 31/157 19.7B. Change 0/19 0.0 0/176 0.0 8/25 32.0 22/172 12.8 10/17 58.8 23/157 14.6Body pitting 2/23 8.7 2/228 0.9 3/30 10.0 5/276 1.8 6/20 30.0 26/191 13.6Ap. change 4/23 17.4 7/204 3.4 14/29 48.3 31/225 13.8 8/20 40.0 24/141 17.0Ap. Pitting 15/23 65.2 43/210 20.5 24/30 80.0 56/225 24.9 17/20 85.0 65/145 44.8Eburnation 4/23 17.4 6/205 2.9 6/30 20.0 12/221 5.4 4/20 20.0 10/138 7.2

LumbarOsteophytes 3/21 14.3 3/101 3.0 16/27 59.3 42/117 35.9 10/20 50.0 20/75 26.7B. change 5/22 22.7 8/101 7.9 19/28 67.9 58/117 49.6 14/21 66.7 43/73 58.9Body pitting 1/22 4.5 1/117 0.9 18/30 60.0 33/145 22.8 14/21 66.7 31/97 32.0Ap. Change 6/21 28.6 14/98 14.3 15/27 55.6 42/110 38.2 12/20 60.0 33/80 41.3Ap. Pitting 10/22 45.5 6/103 5.8 21/28 75.0 42/110 38.2 18/20 90.0 48/77 62.3Eburnation 2/19 10.5 3/95 3.2 7/28 25.0 13/99 13.1 9/20 45.0 15/79 19.0

Whole vertebral columnOsteophytes 6/25 24.0 7/409 1.7 21/31 67.7 88/459 19.2 17/23 73.9 71/343 20.7B. change 6/25 24.0 15/407 3.7 26/31 83.9 131/452 29.0 18/23 78.3 98/341 28.7Body pitting 11/25 44.0 14/497 2.8 22/31 71.0 88/603 14.6 21/23 91.3 111/417 26.6Ap. change 8/25 32.0 23/440 5.2 25/31 80.6 103/501 20.6 18/23 78.3 101/346 29.2Ap. pitting 20/25 80.0 98/455 21.5 30/31 96.8 150/506 29.6 22/23 95.7 174/349 49.9Eburnation 6/25 24.0 10/439 2.3 16/31 51.6 47/489 9.6 12/23 52.2 45/341 13.2


TABLE 6. Chi-square (v2) and P-values for manifestations in the apophyseal joints according to side

Differences between apophyseal joints

SL-SR SL-IL SL-IR SR-IL SR-IR IL-IR

v2 P v2 P v2 P v2 P v2 P v2 P

Apophyseal jointsFrequency by individualsAp. change 0.109 0.741 0.600 0.439 0.041 0.839 1.257 0.262 0.281 0.596 0.311 0.577Ap. pittingEburnation 0.185 0.667 0.055 0.815 0.062 0.803 0.401 0.527 0.028 0.866 0.212 0.645

Frequency by vertebraeAp. change 0.026 0.873 0.427 0.514 0.056 0.813 0.249 0.618 0.007 0.935 0.167 0.683Ap. pitting 0.014 0.907 0.040 0.841 0.497 0.481 0.008 0.930 0.353 0.553 0.242 0.623Eburnation 0.021 0.885 1.042 0.307 1.792 0.181 1.354 0.245 2.197 0.138 0.097 0.756

Signicant values in bold.SL, superior left; SR, superior right; IL, inferior left; IR, inferior right.



Age comparisons: As described for the bodies, the dif-ferences in the FI of the three studied manifestations inthe apophyseal joints are very clear between the younggroup and the other two (middle-age and old), but notbetween these last two (Tables 4 and 5). Observation ofFV suggests that manifestation frequencies increase fromthe youngest to the oldest (see Table 5). Differences

between frequencies of the manifestations in the apophy-seal joints between age groups are signicant (see Table 4).

Diagnostic methods

Table 7 summarizes the frequencies of vertebral de-generative disease diagnosed by our ve methods in the

Fig. 5. Pitting (A), joint surface contour change (B), and eburnation (C) in the apophyseal joints of the vertebral columns of theSoacha Muisca series by vertebrae. [Color gure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

TABLE 7. Diagnosed vertebral degenerative disease in the anatomical regions of the vertebral columnin the whole sample and by sex categories

Females (all ages) Males (all ages) Whole series

FI FV FI FV FI FV

n/N % n/N % n/N % n/N % n/N % n/N %

CervicalM. One 40/44 90.9 165/270 61.1 28/32 87.5 105/199 52.8 70/79 88.6 277/488 56.8Two together 27/44 61.4 75/270 27.8 14/32 43.8 44/199 22.1 43/79 54.4 121/488 24.8Two separat 29/44 65.9 16/32 50.0 47/79 59.5Eburnation 12/44 27.3 28/270 10.4 8/32 25.0 17/199 8.5 20/79 25.3 45/488 9.2Pitting exc 30/44 68.2 106/270 39.3 18/32 56.3 62/199 31.2 50/79 63.3 172/488 35.2

ThoracicM. One 38/45 84.4 158/438 36.1 26/31 83.9 122/302 40.4 66/79 83.5 294/767 38.3Two together 16/45 35.6 38/438 8.7 13/31 41.9 40/302 13.2 31/79 39.2 82/767 10.7Two separat 23/45 51.1 20/31 64.5 45/79 57.0Eburnation 7/45 15.6 9/438 2.1 7/31 22.6 19/302 6.3 14/79 17.7 28/767 3.7Pitting exc 27/45 60.0 86/438 19.6 20/31 64.5 74/302 24.5 49/79 62.0 183/767 23.9

LumbarM. One 36/43 83.7 136/222 61.3 26/32 81.3 85/161 52.8 63/77 81.8 224/391 57.3Two together 26/43 60.5 73/222 32.9 16/32 50.0 37/161 23.0 43/77 55.8 112/391 28.6Two separat 29/43 67.4 17/32 53.1 47/77 61.0Eburnation 7/43 16.3 26/222 11.7 3/32 9.4 5/161 3.1 19/77 24.7 32/391 8.2Pitting exc 30/43 69.8 114/222 51.4 19/32 59.4 66/161 41.0 50/77 64.9 183/391 46.8

Whole vertebral columnM. One 46/46 99.9 459/930 49.4 32/34 94.1 312/662 47.1 80/83 96.4 795/1646 48.3Two together 33/46 71.7 186/930 20.0 23/34 67.6 121/662 18.3 58/83 69.9 315/1646 19.1Two separat 39/46 84.8 25/34 73.5 66/83 79.5Eburnation 22/46 47.8 63/930 6.8 12/34 35.3 41/662 6.2 9/83 10.8 69/1646 5.1Pitting exc 41/46 89.1 306/930 32.9 26/34 76.5 202/662 30.5 69/83 83.1 524/1646 31.8




whole series and by sex, as well as the frequencies inthe three regions of the vertebral column and the wholevertebral column. Almost invariably, the descendingorder of frequency rates found by the different diagnosticmethods is At least One, Pitting excluded, Two sepa-rated, Two together, and Only Eburnation. For thewhole vertebral column, At least One classied 96.4%of the individuals and 48.3% of the vertebrae as positive.Method Two together found 69.9% of the individualspositive and 19.1% of the vertebrae. The 79.5% of theindividuals (83/66) suffer vertebral degenerative disease,according to the method Two separated. For themethod Only Eburnation, 10.8% of the individuals areaffected and 5.1% of the vertebrae, and for the methodPitting excluded, the percentage of individuals affectedis 83.1% and 31.8% of the vertebrae. The differencesfound between frequencies of vertebral degenerativedisease diagnosed by the ve methods are signicant(Table 8).Vertebral degenerative disease frequencies by individ-

ual for the different regions are very similar as seen inTable 7. Table 9 shows that the differences are highlysignicant only for Two together method for thoracicand lumbar regions, with lumbar vertebrae more fre-quently affected (56% of individuals with a positive diag-nosis and 29% of the vertebrae). The same table showsthat FV is signicantly different in almost all cases. Theve methods demonstrated differences between thoracicand cervical regions and thoracic and lumbar regions,but not always between cervical and lumbar regions.Sex comparisons: The pattern of females and males is

very similar to that of the whole series presented in Ta-ble 7. Differences of FI and FV of vertebral degenerativedisease between female and male vertebral columns forthe ve methods are not signicant (see Table 9). Dis-ease prevalence in males and females, region by region,are not signicantly different if the calculations aremade for FI. If they are made for FV, there are signi-cant differences between thoracic regions and lumbarregions with Two together (P 5 0.0467 for thoracicregions and P 5 0.035 for lumbar regions) and OnlyEburnation (P 5 0.003 for thoracic regions and P 50.002 for lumbar regions) methods; and between lumbarregions using Pitting excluded (P 5 0.045), with femaleregions more frequently affected.Age comparisons: Frequencies of vertebral degenera-

tive disease diagnosed by the ve methods applied in thethree age cohorts are presented in Table 10. Theyincrease from youngest to oldest individuals. For the

whole vertebral column, the differences between young-est and middle-aged individuals are signicant (Table 9),with the middle-aged individuals more frequently diag-nosed as positive. Table 9 shows that the differencesbetween middle-age and 451 groups are not statisticallysignicant for FI or FV. This table also suggests that,between the youngest (1530 years) and oldest (451)cohorts, the differences are signicant with both meth-ods (FI and FV), and are obviously higher for the oldestgroup. If FI is calculated, differences among the threevertebral regions for each age category are not signi-cant. Taking into account the FV, the differences aremore obvious.Comparison of females and males by age groups shows

that proportions of vertebral degenerative conditionsdiagnosed by all the methods in the whole vertebral col-umn are very similar. Some signicant differencesappear when calculations are made by FV, but none inthe case of FI. Proportions in youngest groups by Atleast One and Two together methods demonstrateabsolute differences (young males are more frequentlyaffected). Comparisons between older male and femalegroups (451 years) showed important differences in FVdiagnosed by Pitting excluded method.

DISCUSSION

To approach the pattern of vertebral degenerative dis-ease of the Soacha Muisca series, we applied two meth-ods of proportion calculation and ve methods of diagno-sis. Results demonstrate the important variations inprevalence depending on methods used for paleoepide-miological reconstruction. Considering the high variabili-ty of methods applied in data processing in this eld andthe lack of consensus in data treatment between authorscomparisons are extremely difcult. Thus, it seems rele-vant to analyze the different methods in order to choosethe most appropriate one.

Frequency calculation

These results clearly show that the method of fre-quency calculation signicantly inuences paleoepide-miological results. Frequencies by number of individualswere higher in this series than frequencies calculated bynumber of vertebrae. Nevertheless, this would not beobserved if the preservation state (or number of verte-brae present by individual vertebral column) stronglydiffers among individuals of a sample. Patterns of the

TABLE 8. Chi-square (v2) and P-values for diagnostic methods in the whole vertebral column

Diagnostic methods

Differences between methods (whole vertebral column)

FI FV

v2 P v2 P

One-two together 20.793 0.000 313.2 0.000One-two separated 11.142 0.001One-eburnation 122.1 0.000 677.8 0.000One-pitting excluded 7.930 0.005 218.6 0.000Two together-two separated 2.040 0.153Two together-eburnation 60.088 0.000 131.7 0.000Two together-pitting excluded 4.055 0.044 69.870 0.000Two separated-eburnation 79.023 0.000Two separated-pitting excluded 0.357 0.550Eburnation-pitting excluded 87.063 0.000 335.8 0.000

Signicant values are in bold.FI, frequencies by individual; FV, frequencies by vertebra.



vertebral degenerative conditions and its manifestationsas revealed by FI and FV calculation methods are simi-lar in the Soacha series. FI and FV follow the same pro-le as can be concluded from Tables 7 and 10 (if FIdecreases or increases, FV reacts similarly). These twomethods seem to be complementary with regard to thepattern of the degenerative conditions in our sample.When one of the two methods does not show signicantdifferences between proportions, the other provides addi-tional information about the pattern of one manifesta-tion or that of the disease.For epidemiology, as for paleoepidemiology, the rst

relevant question is: how many individuals are affectedby the disease? However, due to the size and structure ofskeletal samples (an increased presence of old individu-als will increase the frequency of DJD), an overestima-tion of DJD prevalence calculated by individual might beproduced (Dutour et al., 2003; Waldron, 1994). Using thetwo methods of frequency calculation simultaneouslyoffers an opportunity to approach the disease both byindividual and by vertebrae, and bring an enhanced op-portunity for comparisons with other published studies.Thus, our preference is to use these two methods to-gether whenever possible.

Diagnostic methods

The present article focused on the diagnosis of verte-bral degenerative conditions. At the beginning of thisstudy, we hypothesized that a single manifestation isenough to make a positive diagnosis in an individual.The criteria of the At least One in our series, producedpercentages close to 100% of the population affected,even in the youngest age categories. Although someexamples of vertebral degenerative conditions among thevery young have been reported (Stirland and Waldron,1997), high frequencies such as those obtained in theSoacha Muisca series with At least One (88% of indi-viduals and 25% of vertebrae) could be rejected. Addi-tionally, results obtained by this method do not allowcomparison because it generalizes the disease to each an-atomical region and subpopulation group.Restricting the criteria led us to explore another diag-

nostic method. The method Two together ensured acorrect diagnosis because eburnation is considered pa-thognomonic of the disease or a marker of its severity(Rothschild, 1997; Ortner, 2003). However this methodrequires the association of at least two of the other man-ifestations and this may underestimate DJD in poorlypreserved skeletal series. Additionally, osteophytes andjoint surface contour change have also been consideredas pathognomonic of DJD (Nathan, 1962; White andFolkens, 2000; Ortner, 2003). Counting them only whenthey are associated with other manifestations can alsolead to prevalence underestimation.The method Two separated is a variation of the

method called Two together, discussed above. Themethod Two separated provides the possibility of hav-ing the manifestations in two different vertebrae. Thisavoids some underestimation; nevertheless, here also, wecan argue against the method due to the fact that osteo-phytes and joint surface contour change have been con-sidered as pathognomonic (Nathan, 1962; White andFolkens, 2000; Ortner, 2003).Concerning the Only Eburnation method, it would

not be desirable to reduce the diagnosis to its presenceonly, ignoring the other typical and accepted manifesta-

TABLE9.Chi-square

(v2)andP-values

fordiagnosticmethodsin

thevertebralregions,byageandsex

Method

Differencesbetweenregions

Sex

differences

Differencesbetweenage-groups

Cerv-thor

Cerv-lumb

Thor-lumb

Male-fem

ale

You

ng-m

iddle

You

ng-old

Middage-old

v2P

v2P

v2P

v2P

v2P

v2P

v2P

Frequen

cybyindividuals

One

0.845

0.358

1.430

0.232

0.081

0.776

Twotogether

3.660

0.056

0.032

0.859

4.311

0.038

0.156

0.693

8.932

0.003

8.349

0.004

0.034

0.854

Twoseparated

0.104

0.747

0.039

0.844

0.268

0.605

1.547

0.214

12.029

0.001

6.299

0.012

0.683

0.409

Eburnation

1.349

0.245

0.009

0.926

1.130

0.288

1.256

0.262

4.859

0.028

4.446

0.035

0.002

0.967

Pittingexcl.

0.027

0.869

0.046

0.831

0.142

0.706

2.302

0.129

7.202

0.007

3.071

0.080

0.683

0.409

Frequen

cybyvertebrae

One

40.857

0.000

0.025

0.875

37.649

0.000

0.767

0.381

89.176

0.000

203.29

0.000

37.681

0.000

Twotogether

43.756

0.000

1.651

0.199

59.855

0.000

0.737

0.391

62.726

0.000

124.85

0.000

16.956

0.000

Twoseparated

Eburnation

16.894

0.000

10.834

0.001

0.292

0.589

0.214

0.644

19.888

0.000

33.686

0.000

3.007

0.083

Pittingexcl.

182.07

0.000

12.043

0.001

2.221

0.136

1.016

0.313

131.46

0.000

186.27

0.000

10.252

0.001

Signicantvalues

are

inbold.



tions of DJD. This procedure underestimates diseaseprevalence, not only because eburnation is present exclu-sively on apophyseal joints, but also because it is uncom-mon. Additionally, one damaged surface that does notpermit observation may signicantly inuence the preva-lence.Finally, the Pitting excluded method as a modica-

tion of the At least One does not consider isolated bodyor apophyseal pitting as diagnostic criteria. This possibil-ity was contemplated in light of preliminary resultswhere pitting appeared to be a ubiquitous manifestation.Pitting was seen in females, males, and in every agegroup in a generalized way at all vertebral levels. Deter-mination of pitting presents intrinsic difculties, beingeasily confused with taphonomic damage or normal pitsin young vertebral bodies. As already mentioned, iso-lated pitting has been demonstrated to be a manifesta-tion without a clear relationship with DJD (Rothschild,1997; Sofaer, 2000). Thus, Pitting excluded seems to bea very good choice that permits standardization.

Vertebral degenerative conditions in SoachaMuisca series

Paleoepidemiology must take into account severalaspects. First of all, as Waldron (1994) pointed out, asample from a cemetery represents a community ofskeletons which is different from a population of livingpeople. Paleoepidemiology has indeed very little to dowith present epidemiology because of a set of specicbiases (Waldron, 1994; Dutour et al., 1998, 2003). TheSoacha Muisca series is the result of the excavation ofone part of an extensive cemetery (Rodrguez, 1999;Boada, 2000); so our conclusions do not apply to theentire Muisca population but only to those Muiscas bur-ied in the sector of Soacha-Portalegre. Second, the bone

preservation is a very important issue. Soacha materialswere well preserved allowing good observation of theaspects studied (additionally, frequency calculations usedonly preserved elements). Considering the age structureof the series, the children are under-represented, butthis under-representation does not have direct repercus-sions on the study of DJD. On the other hand, the pres-ence of individuals between 15 and 20 years in the exca-vated area of the cemetery may suggest that at this age,an individual was already considered an adult, involvedin economic life with obligations which could haveexposed them to very early stress, causing the accelera-tion of the aging process (Stirland and Waldron, 1997).DJD does not contribute directly to death, which meansthat its prevalence in a skeletal population can reectthe prevalence in the living one (Waldron, 1994).Considering the results from our study of the Soacha

Muisca individuals, after apophyseal and body pitting(the earlier manifestations), joint surface contour changeand osteophytes are very frequent. The least frequentmanifestation in each subpopulation is eburnation. Man-ifestations are more frequent in the lumbar region. Thepattern on female vertebral columns follows the samegeneral prole. In male individuals, osteophytosis morefrequently involves the thoracic region, but when thelumbar region is involved, several vertebrae show osteo-phytes. In the young age group (1530 years), the pat-tern is very similar to that described for the whole se-ries, but eburnation predominates in the thoracic area.This is not common, especially because a very youngindividual presented this manifestation (1520 years).Vertebral degenerative conditions in the Soacha

Muisca series more frequently involved cervical and lum-bar areas. The pattern in females is the same. In males,the pattern is repeated with almost all diagnostic meth-ods, with the exception of Two separated and Pitting

TABLE 10. Diagnosed vertebral degenerative disease in the anatomical regions of the vertebral column by age categories

Young (1530) Middle (3045) Old (451)

FI FV FI FV FI FV

n/N % n/N % n/N % n/N % n/N % n/N %

CervicalM. One 18/25 72.0 46/159 28.9 29/31 93.5 116/182 63.7 20/20 99.9 104/130 80.0Two together 4/25 16.0 5/159 3.1 19/31 61.3 51/182 28.0 17/20 85.0 60/130 46.2Two separat. 6/25 24.0 21/31 67.7 17/20 85.0Eburnation 1/25 4.0 1/159 0.6 6/31 19.4 11/182 6.0 7/20 35.0 20/130 15.4Pitting exc 11/25 44.0 13/159 8.2 29/31 93.5 77/182 42.3 17/20 85.0 74/130 56.9

ThoracicM. One 18/25 72.0 57/253 22.5 27/31 87.1 111/290 38.3 19/20 95.0 112/194 57.7Two together 5/25 20.0 10/253 4.0 14/31 45.2 33/290 11.4 10/20 50.0 35/194 18.0Two separat. 8/25 32.0 20/31 64.5 15/20 75.0Eburnation 4/25 16.0 6/253 2.4 6/31 19.4 12/290 4.1 4/20 20.0 10/194 5.2Pitting exc 9/25 36.0 16/253 6.3 22/31 71.0 80/290 27.6 16/20 80.0 64/194 33.0

LumbarM. One 13/23 56.5 33/127 26.0 28/30 93.3 101/154 65.6 21/21 99.9 87/101 86.1Two together 7/23 30.4 14/127 11.0 20/30 66.7 51/154 33.1 15/21 71.4 45/101 44.6Two separat. 7/23 30.4 22/30 73.3 17/21 81.0Eburnation 2/23 8.7 3/127 2.4 7/30 23.3 13/154 8.4 9/21 42.9 15/101 14.9Pitting exc 9/23 39.1 23/127 18.1 22/30 73.3 87/154 56.5 18/21 85.7 70/101 69.3

Whole vertebral columnM. One 23/26 88.5 136/539 25.2 31/31 99.9 328/626 52.4 23/23 99.9 303/425 71.3Two together 11/26 42.3 29/539 5.4 25/31 80.6 135/626 21.6 19/23 82.6 140/425 32.9Two separat. 14/26 53.8 29/31 93.5 20/23 87.0Eburnation 6/26 23.1 10/539 1.9 16/31 51.6 47/626 7.5 12/23 52.2 45/425 10.6Pitting exc 17/26 65.4 52/539 9.6 29/31 93.5 244/626 39.0 20/23 87.0 208/425 48.9




excluded calculated by FI, where the thoracic regionwas the most frequently involved. This could reect asubtle difference between sexes, perhaps reecting dif-fering postures adopted by Soacha Muisca females andmales. On the basis of the similarity in frequencies ofaffected vertebrae, equality in quantity and strength ofphysical activity could be suggested between sexes, butdifferences in location may suggest a difference in thetype of activities.At the beginning of adulthood, the three regions of the

vertebral column were involved. At age 30, degenerativealterations are most severe in the cervical and lumbarregions, a pattern that continues into the oldest agegroups. The degenerative conditions were frequentlypresent from early adulthood, but involved progressivelymore and more vertebrae as individuals aged.High frequencies in young individuals are not only

based on the occurrence of apophyseal pitting, they are aresult of the recording of the others manifestations stud-ied. This suggests that hard physical activities beganearly in the Soacha Muiscas life. A very strenuous life-style reected in the high prevalence of the disease inthe whole series (8083% of the observed vertebral col-umns) is suggested.

Vertebral degenerative conditions in the SoachaMuisca series in perspective

As already pointed out, it is not easy to make compari-sons with available published data. Nevertheless, anextensive comparison of vertebral degenerative condi-tions between the Soacha Muisca series and other pastpopulations previously described was carried out. Thiscould be done by adapting our data to the methodologiesused in the previous studies. As we applied severalmethods of diagnosis and proportion calculations, we areable to compare our data to previous works. For somecomparisons, osteophytes and joint surface contourchange were pooled according to the descriptions of therecorded data in the considered study. In some cases,only the graphs were used to make comparisons. Briey,some key points from the comparisons with the geo-graphically nearest populations are worthy of comment.Comparison of the Soacha Muisca osteophyte fre-

quency with series from Central and Southern Mexicostudied by Chapman (1972) indicates lower frequenciesin Soacha. In the Dickson Mounds population (Clark andDelmond, 1979), osteophytosis occurred earlier in malelumbar regions than in those of females, a prole notfound in the Soacha Muisca series. Frequencies of osteo-phytosis found by Jurmain (1990) in a precontacthunter-gatherer population of California are higher thanthose calculated for the Soacha Muisca series. Neverthe-less, apophyseal joints in Jurmains series are lessinvolved than in the Soacha sample. Frequencies in thestudied Muisca series are higher than frequenciesobtained by Kahl and Ostendorf (2000) in prehistoricNew Mexican populations.In agreement with Bridges (1992) study, there is not a

constant level (frequency) of arthritis and on patternbetween populations. Bridges points out that differencesbetween males and females from ancient agriculturalistpopulations of North America are evident, ndinggreater thoracic osteophytosis in females and more osteo-arthritis of the apophyseal facets in the cervical regionin males (Bridges, 1992). The Soacha series shows thehighest differences in osteophytes and body joint surface

contour change between males and females in the lum-bar area, with females being more strongly affected. Thehigh cervical involvement of apophyseal facets in malesseen by Bridges (1992) seems to be true in our series.Following Bridges (1992), the lower extent of sexualdimorphism in some prehistoric groups suggest a simi-larity in sex roles or in some cases more strenuousduties for females.Differences between populations have supported the

relationship of DJD and physical activity in many publi-cations. Accepting the hypothesis of a positive relation-ship between DJD and physical activity (Chapman,1972; Clark and Delmond, 1979; Goranov et al., 1983;Jurmain, 1990; Bridges, 1991, 1992; Lovell, 1994; Stir-land and Waldron, 1997; Kahl and Ostendorf, 2000;Sofaer, 2000), results presented here suggest that theindividuals recovered from the Soacha Muisca cemeterywere exposed to a high level of physical activity. Thisshould accelerate the aging process, with an early onsetand no sex differences in terms of quantity of degenera-tive lesions.

CONCLUSION

It has been shown that calculation of manifestationsand disease frequencies should be done by applying thetwo methods, FI and FV. From the ve diagnostic meth-ods considered, the most suitable seems to be the methodcalled Pitting excluded. This method takes into accountthe manifestations related to vertebral degenerative con-ditions (body and apophyseal joint surface contourchange, osteophytes and eburnation), excluding the iso-lated body and apophyseal pitting as diagnostic criteria.Pitting excluded reduces underestimation because itdoes not require association between manifestations, andit also avoids overestimation by ignoring the isolated pit-ting as a diagnostic criterion (pitting observed as a gen-eral manifestation).Our article also underscores the lack of discussion con-

cerning prevalence calculation in paleopathological liter-ature. Explicit explanation of calculation and diagnosticmethods can allow relevant interpopulational compari-sons. In spite of these difculties, it is possible to placevertebral degenerative disease in the Soacha Muisca se-ries within the frequencies and patterns of variabilityfrom the published literature. This variability supportsthe hypothesis of a relationship between DJD and physi-cal activity. Furthermore, our results suggest that theSoacha Muisca population does not completely follow theclassical pattern of agricultural populations (higher per-centages of disease than hunter-gatherers and genderdifferences; Bridges, 1992). Individuals recovered fromthe Soacha Muisca cemetery were exposed to a highlevel of work which accelerated the aging process of thespine with a very early onset and without discriminationby sex.Our results t very well with ethnohistorical data

from the region. Although for the chroniclers of theSpanish conquest the justication of conquest and Chris-tianization led them to write mostly negative commentsabout indigenous work habits (Rodrguez, 1999; Encisoand Therrien, 2000), some selected information doescome out that the Muiscas undertook heavy labor. Thereare references to heavy load-bearing, especially relatedto the salt trade. This product was packed in loaves of24 kg which were carried by Muiscas on the back for dis-tances longer than 50 km through very difcult terrain



(Groot, 2000). Agricultural activities and the construc-tion of canals and terracing demanded a large amount ofphysical work. Because these activities were assistedneither by pack animals nor by iron tools (Rodrguez,1999), all the stress they caused went directly to peoplesbodies. This stress produced traces on their bones andmore specically on their vertebral remains that nowa-days may testify it.

ACKNOWLEDGMENTS

The rst author is indebted to Dr. Jose Vicente Rodr-guez for help, encouragement and supervision of the ini-tial part of this research. We thank to the ICANH (Insti-tuto Colombiano de Antropologa e Historia) for access tothe series. We are grateful with Dr. Elie Sanchez for sta-tistical advice. Many thanks are also due to our threeanonymous reviewers and Dr. Clark Larsen who contrib-uted to greatly improve this article. We are indebted toMr. Timothy Sexton who kindly made a grammatical re-vision of our manuscript.

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