AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 135:416430 (2008)

Paleoepidemiology of Vertebral Degenerative Disease in

a Pre-Columbian Muisca Series From Colombia
Claudia Rojas-Sepulveda,1 Yann Ardagna,1 and Olivier Dutour1,2*
1

Unite dAnthropologie: Adaptabilite biologique et culturelle, UMR 6578, Universite de la Mediterranee,

Faculte de Medecine, 13385 Marseille cedex 5, France
2
Department of Anthropology, University of Toronto, Toronto, ON, Canada M5S 2S2
KEY WORDS

osteoarthritis; DJD; spine; occupational stress; South America

ABSTRACT
Major manifestations of vertebral degenerative joint disease were observed on a Pre-Columbian
Muisca series from the Soacha Cemetery (11th to 13th
centuries) Colombia, South America. In total, 1,646 vertebrae of 83 individuals were examined. Osteophytes, vertebral body joint surface contour change (lipping), and vertebral body pitting were evaluated for each vertebral body.
For apophyseal joints, joint surface contour change, pitting, and eburnation were recorded. Two methods of frequency calculation and ve for vertebral degenerative disease diagnosis were applied and compared, allowing discussion of methodological considerations. Our study
showed that 83% of individuals and 32% of vertebrae were

classied as positive when diagnosed by the presence of at

least one of the following manifestations: osteophytes, vertebral body joint surface contour change (lipping), apophyseal joint surface contour change, or eburnation
(method called Pitting excluded). No signicant differences were found between the sexes. In the youngest cohort
(1530 years), 65% of individuals and 10% of vertebrae exhibit at least one of the previously mentioned manifestations. High prevalences suggest a high level of physical activity beginning in childhood which may have accelerated
the aging process in this Pre-Columbian population. Historical data are compatible with this hypothesis. Am J
Phys Anthropol 135:416430, 2008. V 2008 Wiley-Liss, Inc.

Among manifestations of life conditions observed on

bones, degenerative joint disease (DJD) is most common.
This disease has been the subject matter of a number of
research projects in paleopathology for several reasons.
First of all, DJD has affected animals and humans
throughout prehistory; second, it is the most frequently
observed disease among archaeological series; and third,
DJD affects living populations (Ortner and Putschar,
1981; Cohen, 1984; Peyron, 1986; Bridges, 1992; Thillaud, 1992). Additionally, DJD can be related to many
variables: age, sex, trauma, genetic predisposition (metabolic and endocrine factors), and biomechanical stress or
physical activity (Ingelmark, 1959; Nathan, 1962; Ortner
and Putschar, 1981; Goodman et al., 1984; Ubelaker,
1984; Peyron, 1986; Larsen, 1987; Rogers et al., 1987;
Bridges, 1992; Jurmain and Kilgore, 1995; Rogers and
Waldron, 1995; Resnick, 2002; Ortner, 2003). The question of the relationship between DJD and the level of
physical activity is still debated. According to some
scholars, several studies demonstrate a positive relationship between DJD and stress (Jurmain, 1990; Bridges,
1991, 1992). However, others have suggested that these
manifestations are only consequences of the aging process (Bourke, 1967; Waldron, 1991, 1992).
Because of its structure, the human spine plays an important role in the study of degenerative disease and
occupational stress (Chapman, 1972; Clark and Delmond, 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 curvatures
of the spine, relate the location of this disease in the
spine directly to human bipedality (Jankauskas, 1992;
Knusel et al., 1997; Weber et al., 2003). Some paleopathologists have taken into account results of clinical

research on living people who perform high levels of

physical activity, such as athletes or laborers, as well as
data from veterinary research. Khal and Ostendorf
(2000) present an extensive review of this literature.
Although it is hazardous to link the pattern of physical activity markers to any specic occupation (Dutour,
1992; Waldron, 1994; Rogers and Waldron, 1995), some
studies have evaluated the impact and pattern of degenerative disease manifestations, particularly in the spine,
to reconstruct a part of a past populations lifestyle and
its relationship with the environment (Cohen and Armelagos, 1984). Signicant research has described the pattern and prevalence of vertebral degenerative disease in
certain geographical areas. Specic works have been
published, especially for past populations from North
America (Chapman, 1972; Clark and Delmond, 1979;
Jurmain, 1990; Bridges, 1989, 1991, 1992; Kahl and
Ostendorf, 2000; Merbs, 2001); Europe (Berato et al.,
1990; Jankauskas, 1992; Waldron, 1991, 1992; Knusel
et al., 1997; Sofaer, 2000; Weber et al., 2003) and some
others in Asia (Lovell, 1994; Hukuda et al., 2000). Until
now, paleoepidemiology of DJD in South America is

C 2008
V

WILEY-LISS, INC.

Grant sponsor: French Ministry of Education and Research.

*Correspondence to: Olivier Dutour, Department of Anthropology,
University of Toronto, 19 Russell Street, Toronto, ON, Canada M5S
2S2 (or) Unite dAnthropologie biologique, UMR 6578, Faculte de
Medecine, 27 Boulevard Jean Moulin, 13385 Marseille, France.
E-mail: oj.dutour@utoronto.ca
Received 17 November 2006; accepted 15 October 2007
DOI 10.1002/ajpa.20762
Published online 10 January 2008 in Wiley InterScience
(www.interscience.wiley.com).

PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

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.]

poorly documented. Current literature is focused mostly

on individual case studies (Gerszten et al., 2001) without
the benet of an epidemiological approach, while others
present mainly general paleopathological overviews or
the epidemiology of different diseases, being notably
focused on Peruvian and Chilean samples.
The aim of this article is to present the results of the
paleoepidemiological study of vertebral degenerative disease on a Pre-Columbian Muisca series from the Sabana
de Bogota in Colombia (South America). As previous bioarchaeological studies have highlighted the presence of
DJD in this series as linked to life conditions and activities (Rodrguez, 1999), specic research on vertebral
structures has the potential to further elucidate this
issue. On the basis of a populational approach, our
results can contribute to the debate about DJD and
physical activity.
Methodological considerations related to the calculation of frequencies of vertebral disease and diagnoses are
presented here. The goal of this article is twofold: i) to
show how different conclusions in paleoepidemiology
may be reached depending on methods of reconstruction
of past prevalence; and ii) to propose a method for standardizing comparisons between studies, which currently
remains difcult.

MATERIALS
Muisca culture
The Muiscas was a large Chibcha-speaking agricultural society that developed in the plateau of Cundinamarca and Boyaca, on the Eastern Range in present-day
central Colombia (South America) (see Fig. 1), chronologically dated between 700 and 1600 AD (Langebaek,
1995; Rodrguez, 1999). Specialists from various disciplines have discussed the Muisca cultures origin, as well
as 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 of
expansion and unication characterized by intensive
military activity, which may have led to a state level political structure (Broadbent, 1964; Tovar, 1980; Lange-

417

Fig. 2. Stages recorded for the manifestations of vertebral

degenerative conditions in the vertebral body (osteophytes, joint
surface contour change or lipping, and pitting). [Color gure
can be viewed in the online issue, which is available at www.
interscience.wiley.com.]

baek, 1995; Langebaek, 1998; Langebaek, 2000). Muisca

society was stratied (Zubiria, 1986; Rodrguez, 1999),
some groups were subject to the absolute power of a single chief (Broadbent, 1964; Tovar, 1980). Political and religious power were closely linked (Londono, 1996).
Chiefs, priests, and their families had the highest status,
being recipients of special treatment even after death
when they were mummied and richly ornamented. At
the time of European contact, the Muiscas practiced
polygyny, exogamy, and matrilineal inheritance (Broadbent, 1964; Londono, 1996; Langebaek, 1998; Rodrguez,
1999). They took advantage of the ecological diversity of
their territory where altitude variation resulted in
resource variability (The vertical archipelago (Murra,
1972, 1981). The Muiscas practiced microvertical exploitation, applied technological developments such as hydraulic systems (canals for water control and terracing),
and had contact with their neighbors living at lower elevation or established Muisca families in those territories
(Botiva, 1989; Langebaek, 1998; Rodrguez, 1999). They
were maize agriculturalists, hunters, gatherers, shers,
craftsmen, (potters, goldsmiths, weavers), emerald and
salt miners, and traders with an extensive trading network (Duque, 1945; Rodrguez, 1999; Groot, 2000).

The series
The study sample is from the Muisca cemetery of Soacha-Portalegre, excavated in 1987 by archaeologists of
the Instituto Colombiano de Antropologa. Recovered in
the middle of the urban settlement, the cemeterys population and physical extent are undocumented (Botiva,
1989; Boada, 2000). Apparently, the entire present-day
village was a large Muisca cemetery inhabited between
the 11th and 13th centuries (Reichel-Dolmatoff, 1943,
n.d.; Rodrguez, 1994, 1999). According to the literature
two uncalibrated 14C dates are available: 1035 6 115 AD
for 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 during
excavation, as were fragments of ceramic, stone and
metal objects, sea shells, animal remains as well as 133
American Journal of Physical Anthropology

 LVEDA ET AL.
C. ROJAS-SEPU

418

TABLE 1. Age and sex composition of the sample

Female
Male
Indeterminate
Total

Young
(1530)

Middle age
(3045)

Old
(451)

Adult

Total

12
13
1
26

18
13
0
31

15
8
0
23

1
0
2
3

46
34
3
83

tombs. No European objects were recovered, indicating

that the site belongs to a period earlier to the Conquest
(Botiva, 1988, 1989). According to archeological studies
on funerary habits and objects, this cemetery, or at least
the excavated part of it, was where members of lower
social class, and probably some warriors were buried
(Boada, 2000; Rodrguez, 1994, 1999). The total number
of recovered individuals is 135; 36 of them are children,
99 are adults (64 female, 39 male). The low proportion of
young individuals has been ascribed to archaeological
(cemetery partially excavated) and cultural factors (children buried in a different place) (Rodrguez, 1994, 1999).
Bioanthropological studies on this series have found a
good general health condition for these individuals,
apparently they did not suffer any nutritional stress;
nevertheless, these studies have observed that females
condition seems to be inferior to that of males (Rodrguez, 1994, 1999).
For this research, we studied the vertebral columns of
male and female individuals of the series (15 to 451
years of age) represented by at least six vertebrae. Sample composition is presented in Table 1, representing a
total of 83 vertebral columns.

METHODS
Data collection
We inspected each vertebra of every skeleton included
in our study. An individual recording system was
employed following the recommendations of Campo Martin (1997, 2003) and Buikstra and Ubelaker (1994). Data
recorded for each individual include age, sex, preservation state and vertebral manifestations of DJD. Sex
determination and age estimation were made by conventional anthropological methods (Brothwell, 1965; Iscan
et 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 was
present; Incomplete, when its presence was between 25
and 75%; Very incomplete, when less than 25% was
found; and, Absent when it was not assessable. For the
right and left vertebral arches, the presence of the superior and inferior apophyseal joints was recorded using
the same codes.
All morphological changes were macroscopically
observed and recorded by the same researcher to avoid
interobserver error. Some vertebral columns were evaluated several times over a period of time to verify the diagnosis and the reliability of the recorded information.
Concerning terminological usage, degenerative conditions of the spine are frequently named spinal DJD.
However, it should be noted that the joints of the spine
have fundamental anatomic differences and they do not
deteriorate identically (Resnick, 2002).These differences
have led some authors to distinguish changes in the verAmerican Journal of Physical Anthropology

tebral bodies known as Intervertebral Disc Degeneration or Degenerative Disc Degeneration, from those
observed in the synovial joints named Apophyseal Joint
Osteoarthritis (Resnick, 2002). Accordingly, we observed
and separately recorded manifestations for these two
localizations, the vertebral body and the apophyseal
joints.
For the vertebral body we recorded osteophytes, joint
surface contour change (lipping), and pitting. For
the apophyseal joints, joint surface contour change
(lipping), pitting, and eburnation were recorded.
Osteophytes are also referred to as marginal proliferation; they are new bone growths which arise around the
joint margins (Nathan, 1962; Rogers et al., 1987; Rogers
and Waldron, 1995). Joint surface contour change has
also been referred to as remodeling of joint contours or
facet remodeling; it may produce attening and/or
enlargement of joint surfaces, being a proliferative reaction (Rogers et al., 1987). Facet remodeling, especially of
apophyseal joints, is an important response to applied
pressure, thus being a very good indicator of repeated
activity-induced stress in humans (Sofaer, 2000). Osteophytes (OP) were distinguished from joint surface contour change in the vertebral bodies. While OP refers to
localized growths commonly known as parrots beak,
joint surface contour change was recorded as a ringshaped manifestation around body margins. Pitting or
microporosity has been dened as the discontinuity of
the subchondral bone which manifests as a pitted and
disorganized lesion (Rothschild, 1997). Ortner (2003)
describes erosion as a subchondral surface breakdown,
where the underlying trabeculae of the bone may be
exposed.1 Eburnation, described as an ivory like aspect, is a severe subchondral bone reaction; it is the
shiny or polished area found on an articular surface,
the product of bony joint surfaces rubbing after losing all
the cartilage between them. Eburnation is considered
pathognomonic of the disease (Rogers et al., 1987; Bridges,
1992; Rogers and Waldron, 1995) or a marker of its severity (Rothschild, 1997; Ortner, 2003); in any case, it is
a 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 barely
visible; 2 for moderate; and 3 for severe. An illustration
of the scoring system is shown in Figures 2 and 3. For
more severe manifestations Code 4 may be assigned. The
stage method seems to be subjective, but it has been
extensively used in the literature (Nathan, 1962; Chapman, 1972; Clark and Delmond, 1979; Bridges, 1989;
Jurmain, 1990; Lovell, 1994; Kahl and Ostendorf, 2000;
Sofaer, 2000; Weber, 2003). A code for damaged elements
was also assigned unobservable.
For vertebral bodies, superior and inferior surfaces
were observed and manifestations recorded separately.
Vertebral ankylosis produced in disorders other than
DJD (such as DISH, ankylosing spondylitis, congenital
fusion) was excluded. Special attention was paid to differentiate the lesions according to their main cause
(Rogers et al., 1987). For C1, the facet joint for the C2
odontoid process was evaluated for joint surface contour
change and pitting but not for osteophytes (because we
dened joint surface contour change as a ring-shaped
manifestation while osteophytes as a localized one).
Even if superior, inferior, right and left apophyseal joints
1
Ortner does not mention the word pitting, but these descriptions are similar to that recorded in our study.

PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

were recorded independently, almost all differences between them were not statistically signicant; hence, the
results concerning the apophyseal joints consider them
as a whole. Four vertebral columns with a 6th lumbar
vertebra were found; these vertebrae were excluded from
the calculations.

Frequency calculations
The state of bone preservation may result in variation
in disease prevalence. For this reason, calculation of frequencies and prevalences were made taking into account
only the observable aspects (Waldron, 1994). As dened

Fig. 3. Stages recorded for the manifestations of vertebral

degenerative conditions in the apophyseal joints (pitting, joint
surface contour change or lipping, and eburnation). [Color gure can be viewed in the online issue, which is available at
www.interscience.wiley.com.]

419

by Waldron (1994), paleoepidemiological prevalence is

based on modication of the n/N ratio, being n (the
numerator) the total number of affected individuals or
anatomical elements and N (the denominator) the total
number of observable individuals or anatomical elements. Our method is based on modication of the numerator and the denominator. Variation of the numerator depends on diagnostic criteria for a vertebra, a vertebral region or a whole vertebral column (counted as
positive). Denominator variation is limited by the state
of preservation for individual or anatomical elements
(vertebra, region, whole vertebral column). To evaluate
the presence of vertebrae and their elements (preservation state), the numerator is the number of vertebrae
found and the denominator is the theoretical number of
vertebrae (assuming 7 vertebrae for cervical, 12 for thoracic, and 5 for lumbar).
Two methods were used to analyze manifestation frequencies and vertebral degenerative disease prevalence
in the vertebral regions or in the whole vertebral
column:
Frequency by individual (FI) is the proportion of vertebral regions or vertebral columns affected, where
the numerator is the number of individuals which
had the manifestation or positive diagnosis of vertebral degenerative conditions and the denominator is
the total of individuals who had at least one vertebra observable for the manifestation considered in
the region or in the vertebral column. When the
sample was divided by population groups, the denominator was the number of individuals of the chosen age and sex category who presented at least one
vertebra in the observed region or in the vertebral
column.
Frequency by vertebra (FV) is the proportion of vertebrae
involved, where the numerator is the number of vertebrae affected by one manifestation or the number
of vertebrae classied as positive for degenerative

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

American Journal of Physical Anthropology

420

LVEDA ET AL.
C. ROJAS-SEPU
conditions, and the denominator is the total number
of vertebrae found for the corresponding region or
for the vertebral column in the considered age and
sex category (Hukuda et al., 2000).

Diagnostic methods and vertebral degenerative

disease 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 considered positive if it presented at least one manifestation
(osteophyte, body joint surface contour change, body pitting, apophyseal joint surface contour change, apophyseal pitting or eburnation).
Two together. In this method, if eburnation was not
present, at least two of the other manifestations (osteophytes, joint surface contour change or pitting) had to be
present in a single vertebra to make a positive diagnosis.
According to Rogers and Waldron (1995) eburnation is
pathognomonic of DJD; if eburnation was present, the
vertebra, the vertebral region or the individual were considered also positive. If one vertebra was considered
positive, the corresponding entire region and entire
vertebral column was also considered positive.
Two separated. This is a variant of the previously
described method, following the criteria for the diagnosis
in the vertebra. In the region and in the whole vertebral
column, 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 vertebra. This means that if in the region or in the whole vertebral column one vertebra presented osteophytes (or
joint surface contour change) and another pitting, that
was enough to classify it as positive. Hence, any isolated vertebra were not classied as positive.
Only Eburnation. Because eburnation is pathognomonic, this method restricted the diagnosis to eburnation presence or absence; only the presence of eburnation
made a vertebra, a region or a vertebral column positive. As published data has been obtained with these
criteria (Waldron, 1992), it is interesting to compare this
method with the others.
Pitting excluded. Some authors have considered pitting
as a bone change which is not related to DJD (Rothschild, 1997; Sofaer, 2000). According to this method, the
positive diagnosis was recorded when any of the
observed manifestations was present excluding pitting
(on vertebral body or apophyseal joints). Contrary to At
least One, here isolated pitting was not enough to classify 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 according
to the diagnostic method applied and N (the denominator) was the number of specic vertebrae coded as present.
For the anatomical region (cervical, thoracic, or lumbar), when the FI was calculated, the numerator was the
number of individuals coded as positive in the region
according to the diagnostic method and the denominator
American Journal of Physical Anthropology

was the number of individuals with at least one vertebra

in the region. When the FV was calculated, the numerator was the number of vertebrae coded as positive
according to the diagnostic method and the denominator
was the total number of vertebrae coded as present in
the region.
For the whole vertebral column, when the FI was calculated, the numerator was the number of individuals
considered positive according to the diagnostic method
and the denominator was the number of individuals
with at least one vertebra coded as present in the vertebral column. When the FV was calculated, the numerator was the number of vertebrae coded as positive
according to the diagnostic method and the denominator
was the total number of vertebrae coded as present.
Comparisons between sex and age groups were conducted. The signicance of the differences between frequencies was calculated by applying chi-square (v2) tests
(P  0.05). To apply v2 tests, expected frequencies must
be 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. The
most frequently found vertebra was T2 (76/83), while
T12 was the least often recorded vertebra (51/83). Good
preservation state of the vertebrae made almost always
possible the identication and location of each one of
them. C5 is the qualitatively best preserved vertebra
(64/83 coded as complete), while T6 was the least commonly coded as complete (31/83). From C1 to T7 and for
the whole lumbar region, the presence of the elements is
up to 60%. In the cervical region, the presence of complete vertebrae was recorded over 50% of the time, in
the other regions, complete vertebrae were recorded
around 40% of the time.
The cervical region is the best represented with 488
vertebrae present (83.99%, assuming seven cervical vertebrae by individual). The rst sacral vertebra is present
in 69 vertebral columns (83.13%, assuming one sacral
vertebra by individual). The lumbar region is represented by 322 vertebrae (77.59%, assuming ve lumbar
vertebrae by individual), and the thoracic region is represented by 768 vertebrae (77.11%, assuming twelve thoracic vertebrae by individual). A total of 1,646 vertebrae
were observed and coded. The preservation in different
sex and age categories is similar. In each vertebral
region, at least 73% of vertebrae with at least 1/4 of the
body were observed.
Apophyseal joints were well preserved too, varying
from 60 to 82% for the different regions. The superior
apophyseal joints are better represented than the inferior ones, but these differences are statistically signicant only for the thoracic region. Differences of preservation between right and left side are not signicant.

Type of pathological conditions

Vertebral body. Table 2 presents the frequencies and
percentages (FI and FV) of recorded manifestations in
the complete sample and in the groups by sex, providing
results for each vertebral region and for the whole vertebral column. For complete vertebral columns, Table 2
shows that pitting is the most frequently encountered
manifestation in the entire series when the calculation is

421

PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

TABLE 2. Observed manifestations in the anatomical regions of the vertebral column in the whole sample and by sex categories
Females (all ages)
FI
n/N
Cervical
Osteophytes
12/43
B. change
22/42
Body pitting
26/44
Ap. Change
21/42
Ap. pitting
33/41
Eburnation
12/43
Thoracic
Osteophytes
16/36
B. change
12/35
Body pitting
8/44
Ap. Change
17/42
Ap. pitting
31/43
Eburnation
7/43
Lumbar
Osteophytes
24/38
B. change
24/41
Body pitting
22/43
Ap. change
22/41
Ap. pitting
30/41
Eburnation
7/43
Whole vertebral column
Osteophytes
28/46
B. change
30/46
Body pitting
31/46
Ap. Change
35/46
Ap. pitting
43/46
Eburnation
22/46

Males (all ages)

FV

FI

Whole series

FV

FI

FV

n/N

n/N

n/N

n/N

n/N

27.9
52.4
59.1
50.0
80.5
27.9

27/234
61/230
67/268
50/248
86/255
28/250

11.5
26.5
25.0
20.2
33.7
11.2

8/31
14/32
14/32
11/32
23/32
8/32

25.8
43.8
43.8
34.4
71.9
25.0

11/176
32/178
49/199
27/183
63/187
17/185

6.3
18.0
24.6
14.8
33.7
9.2

22/77
37/77
48/79
32/77
57/76
20/78

28.6
48.1
60.8
41.6
75.0
25.6

41/430
94/427
120/487
77/448
150/459
45/451

9.5
22.0
24.6
17.2
32.7
10.0

44.4
34.3
18.2
40.5
72.1
16.3

38/205
27/303
28/422
37/346
88/356
9/344

18.5
8.9
6.6
10.7
24.7
2.6

10/27
6/27
3/30
10/31
26/31
7/31

37.0
22.2
10.0
32.3
83.9
22.6

28/221
18/221
5/287
27/236
78/237
19/232

12.7
8.1
1.7
11.4
32.9
8.2

26/66
19/65
11/77
28/76
59/77
14/77

39.4
29.2
14.3
36.8
76.6
18.2

67/544
49/537
33/735
68/609
175/620
28/601

12.3
9.1
4.5
11.2
28.2
4.7

63.2
58.5
51.2
53.7
73.2
16.3

43/171
75/171
47/217
58/174
71/172
26/165

25.1
43.9
21.7
33.3
41.3
15.8

10/31
14/32
11/32
11/29
19/31
3/27

32.3
43.8
34.4
37.9
61.3
11.1

22/128
34/127
18/149
31/121
41/125
5/115

17.2
26.8
12.1
25.6
32.8
4.3

29/71
39/75
33/76
34/71
50/73
19/70

40.8
52.0
43.4
47.9
68.5
27.1

65/306
112/304
65/371
91/300
114/302
32/285

21.2
36.8
17.5
30.3
37.7
11.2

60.9
65.2
67.4
76.1
93.5
47.8

136/710
163/704
142/907
145/768
245/783
63/759

19.2
23.2
15.7
18.9
31.3
8.3

17/34
21/34
24/34
17/33
30/33
12/33

50.0
61.8
70.6
51.5
90.9
36.4

61/525
84/523
72/635
85/540
182/549
41/532

11.6
16.1
11.3
15.7
33.2
7.7

47/83
52/83
57/83
55/83
76/83
36/83

56.6
62.7
68.7
66.3
91.6
43.4

173/1280
255/1268
218/1593
236/1357
439/1381
105/1337

13.5
20.1
13.7
17.4
31.8
7.9

Row frequencies showed as n/N.

FI, frequency by individual; FV, frequency by vertebra.
TABLE 3. Chi-square (v2) and P-values for manifestations in the whole vertebral column
Differences between manifestations (whole vertebral column)
FI
Vertebral body
Osteophytes-cont change
Ostophytes-body pitting
Contour change-body pitting
Apophyseal joints
Ap. contour change-Ap.pitting
Ap. contour change-eburnation
Ap.pitting-eburnation

FV

v2

v2

0.626
2.574
0.668

0.429
0.109
0.414

19.822
0.017
21.124

0.000
0.895
0.000

15.966
8.780
43.915

0.000
0.003
0.000

76.377
55.416
243.1

0.000
0.000
0.000

Signicant values are in bold.

FI, frequencies by individual; FV, frequencies by vertebra.

made by FI (68.7%); nevertheless, no signicant differences were found when compared with the other manifestations (see Table 3). Concerning the results obtained by
the FV for the bodies of the whole vertebral column,
joint surface contour change is the most often recorded
(20.1%). Differences between manifestations in the
bodies are not signicant for osteophytes and body pitting (Table 3). Joint surface contour change is also the
manifestation most frequently recorded as Stage 3 on
vertebral bodies compared with the other studied manifestations, as shown in Figure 4.
For the cervical region, pitting is the most frequently
found manifestation with 60.8% of individuals affected
and 24.6% of the vertebrae (Table 2). Figure 4 shows
that pitting is classied very frequently as Stage 3 in
the cervical region. In the thoracic region osteophytes

are the most frequent manifestation; of 66 thoracic

regions, 26 exhibit the manifestation; and of 544 vertebrae, 67 are positive for osteophytes. In the lumbar vertebrae, joint surface contour change presents the highest
frequencies, 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 as
Stage 3 in the lumbar region (see in Fig. 4). Chi-square
tests show no signicant differences between the presence of osteophytes in the three regions if the proportion
is calculated by individuals, but signicant when comparing FV between lumbar region and the other two
(Table 4). Joint surface contour change also affects the
lumbar region most often; nevertheless, no signicant
difference was found between lumbar and cervical regions
American Journal of Physical Anthropology

0.004
0.000
0.106
8.340
35.854
2.620
0.000
0.000
0.000
83.709
70.753
34.910
0.000
0.004
0.000
47.482
8.221
21.580
0.142
0.474
0.700
2.156
0.513
0.149
Signicant values are in bold.

51.165
8.557
13.214
0.000
0.151
0.589
17.830
2.065
0.291
0.000
0.000
0.001

American Journal of Physical Anthropology

for FI (P 5 0.626). However, signicant differences are

found 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 by
the lumbar region (33/76 individuals and 65/371 vertebrae), which demonstrates the strongest expressions of
the condition (see Fig. 4). For pitting, all differences
between regions are signicant for FV and FI.
Sex comparisons: The pattern in female and male vertebral body manifestations is very similar to those for
the entire group (Table 2). Nevertheless, osteophytes and
joint surface contour change are slightly more frequent
in females and pitting in males. Osteophytes are present
in 60.9% of the females and 50% of the males and in
19.2% of female vertebrae and 11.6% of male vertebrae.
Joint contour change is present in 65.2% of females and
61.8% of males and in 23.2% of female vertebrae and
16.1% of male vertebrae. To compare the presence of the
manifestations between the groups by sex, v2 tests were
applied; results are included in Table 4. There we see
that differences between FI of the different manifestations in female and male vertebral bodies are not signicant. But when FV is calculated, females are more signicantly affected by the three manifestations.
Age comparisons: Table 5 presents the frequencies of
the manifestations studied in the three age groups, in
the three regions, and in the whole vertebral column.
In the youngest group (1530 years), all the manifestations are less frequent than in middle-aged (3045 years)
and old (451) groups. Signicant differences were
revealed by v2 mostly between the youngest group and
the other two (Table 4). In the youngest group (1530
years), the most frequent manifestation is pitting (44%
of the individuals and 2.8% of the vertebrae). Pitting in
middle-age is present in 71% of the individuals and
14.6% of the vertebrae; while in 91.3% of the old individuals 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 frequent
manifestation is joint surface contour change (83.9% of
the individuals and 29% of vertebrae), and in the oldest
individuals the most frequent is joint surface contour
change (78.3% of the individuals and 28.7% of the vertebrae) and also pitting (91.3% of the individuals and
26.6% of the vertebrae).

0.000
0.003
0.000

0.002
4.057
1.030
0.193

13.531
5.157

1.836
1.247
1.691
0.599
0.779
0.043
0.550
0.815
0.262

0.439
0.378
0.836

0.175

0.023
0.671
0.310

4.424

0.035

0.044

0.830
0.046
0.001
10.326
0.000

0.591
0.940
0.000
0.288
0.006
22.700
0.000
0.000
0.000
72.352
90.810
108.8
0.000
0.000
0.000
67.651
97.144
44.915
0.000
0.002
0.016
12.785
9.388
5.825
11.894
96.341
38.736
24.747
36.217
4.109
0.170
0.000
0.000

0.000
0.000
0.043

0.001
0.000
0.000

0.623
0.600
0.067
0.241
0.275
3.367
0.001
0.000
0.001
11.958
14.108
12.063
0.001
0.000
0.041
10.605
20.256
4.159
0.333
0.751
0.760
0.939
0.101
0.093
0.030
7.440
15.847
2.464
0.237
4.667

Vertebral body
Frequency by individuals
Osteophytes
1.867
Cont. change
5.228
Body pitting
35.813
Frequency by vertebrae
Osteophytes
1.884
Cont. change
31.279
Body pitting
108.6
Apophyseal joints
Frequency by individuals
Ap. change
0.357
Ap. pitting
0.055
Eburnation
1.259
Frequency by vertebrae
Ap. change
12.252
Ap. pitting
17.246
Eburnation
11.288

0.172
0.022
0.000

0.116
0.626
0.031

P
v2
P
v2
v2

Thor-lumb
Cerv-thor

0.863
0.006
0.000

Midd age-old
v2
P
Young-old
v2
P

Differences between age-groups

Cerv-lumb

Young-midd
v2
P
Sex differ.

Male-female
v2
P

Differences between regions

TABLE 4. Chi-square (v2) and P-values for manifestations in the vertebral regions, by age and sex

0.967

LVEDA ET AL.
C. ROJAS-SEPU

422

Apophyseal joints. Differences in manifestation frequencies among the superior right, superior left, inferior
right, and inferior left apophyseal joints are not signicant (Table 6). Accordingly, we pooled the results.
Frequencies of manifestations studied in the apophyseal joints are presented in Tables 2 and 5. In Table 2,
for the whole series, pitting is the most frequent manifestation on apophyseal joints (91.6% of the individuals
and 31.8% of the vertebrae), followed by joint surface
contour change (66.3% of the individuals and 17.4% of
the vertebrae), and nally by eburnation (43.4% of the
individuals and 7.9% of the vertebrae). The differences
between manifestations are signicant (see Table 3).
Table 2 and Fig. 5 show that the same pattern is repeated
in the three vertebral regions. Joint surface contour
change is more frequent and more often classied as
Stage 3 in the lumbar region (47.9% of the individuals
and 30.3% of the vertebrae) and, second, in cervical vertebrae (41.6% of the individuals and 17.2% of vertebrae).
Between regions, differences in the presence of the mani-

423

PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

TABLE 5. Observed manifestations in the anatomical regions of the vertebral column by age categories
Young (1530)
FI

Middle (3045)
FV

n/N
Cervical
Osteophytes
2/24
B. change
3/23
Body pitting
9/24
Ap. change
2/23
Ap. pitting
11/21
Eburnation
1/23
Thoracic
Osteophytes
1/20
B. Change
0/19
Body pitting
2/23
Ap. change
4/23
Ap. Pitting
15/23
Eburnation
4/23
Lumbar
Osteophytes
3/21
B. change
5/22
Body pitting
1/22
Ap. Change
6/21
Ap. Pitting
10/22
Eburnation
2/19
Whole vertebral column
Osteophytes
6/25
B. change
6/25
Body pitting
11/25
Ap. change
8/25
Ap. pitting
20/25
Eburnation
6/25

FI

Old (451)
FV

FI

FV

n/N

n/N

n/N

n/N

n/N

8.3
13.0
37.5
8.7
52.4
4.3

2/132
7/130
11/152
2/138
33/142
1/139

1.5
5.4
7.2
1.4
23.2
0.7

6/29
18/30
19/31
15/30
24/31
11/31

20.7
60.0
61.3
50.0
77.4
35.5

13/163
51/163
50/182
30/166
52/170
22/169

8.0
31.3
27.5
18.1
30.6
13.0

11/20
14/20
17/20
14/20
19/20
7/20

55.0
70.0
85.0
70.0
95.0
35.0

20/111
32/111
54/129
44/125
61/127
20/124

18.0
28.8
41.9
35.2
48.0
16.1

5.0
0.0
8.7
17.4
65.2
17.4

2/176
0/176
2/228
7/204
43/210
6/205

1.1
0.0
0.9
3.4
20.5
2.9

12/24
8/25
3/30
14/29
24/30
6/30

50.0
32.0
10.0
48.3
80.0
20.0

33/179
22/172
5/276
31/225
56/225
12/221

18.4
12.8
1.8
13.8
24.9
5.4

13/18
10/17
6/20
8/20
17/20
4/20

72.2
58.8
30.0
40.0
85.0
20.0

31/157
23/157
26/191
24/141
65/145
10/138

19.7
14.6
13.6
17.0
44.8
7.2

14.3
22.7
4.5
28.6
45.5
10.5

3/101
8/101
1/117
14/98
6/103
3/95

3.0
7.9
0.9
14.3
5.8
3.2

16/27
19/28
18/30
15/27
21/28
7/28

59.3
67.9
60.0
55.6
75.0
25.0

42/117
58/117
33/145
42/110
42/110
13/99

35.9
49.6
22.8
38.2
38.2
13.1

10/20
14/21
14/21
12/20
18/20
9/20

50.0
66.7
66.7
60.0
90.0
45.0

20/75
43/73
31/97
33/80
48/77
15/79

26.7
58.9
32.0
41.3
62.3
19.0

24.0
24.0
44.0
32.0
80.0
24.0

7/409
15/407
14/497
23/440
98/455
10/439

1.7
3.7
2.8
5.2
21.5
2.3

21/31
26/31
22/31
25/31
30/31
16/31

67.7
83.9
71.0
80.6
96.8
51.6

88/459
131/452
88/603
103/501
150/506
47/489

19.2
29.0
14.6
20.6
29.6
9.6

17/23
18/23
21/23
18/23
22/23
12/23

73.9
78.3
91.3
78.3
95.7
52.2

71/343
98/341
111/417
101/346
174/349
45/341

20.7
28.7
26.6
29.2
49.9
13.2

Row frequencies showed as n/N.

FI, frequency by individual; FV, frequency by vertebra.
TABLE 6. Chi-square (v2) and P-values for manifestations in the apophyseal joints according to side
Differences between apophyseal joints
SL-SR
v2
Apophyseal joints
Frequency by individuals
Ap. change
0.109
Ap. pitting
Eburnation
0.185
Frequency by vertebrae
Ap. change
0.026
Ap. pitting
0.014
Eburnation
0.021

SL-IL

SL-IR

SR-IL

SR-IR

IL-IR

v2

v2

v2

v2

v2

0.741

0.600

0.439

0.041

0.839

1.257

0.262

0.281

0.596

0.311

0.577

0.667

0.055

0.815

0.062

0.803

0.401

0.527

0.028

0.866

0.212

0.645

0.873
0.907
0.885

0.427
0.040
1.042

0.514
0.841
0.307

0.056
0.497
1.792

0.813
0.481
0.181

0.249
0.008
1.354

0.618
0.930
0.245

0.007
0.353
2.197

0.935
0.553
0.138

0.167
0.242
0.097

0.683
0.623
0.756

Signicant values in bold.

SL, superior left; SR, superior right; IL, inferior left; IR, inferior right.

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 cervical region (57/76 individuals), and nally by the lumbar
region (50/73 individuals). Nevertheless, no signicant
differences were found by v2 between the frequencies by
individual for pitting in the regions (Table 4). If calculations are made by FV, the lumbar region exhibits the
highest prevalence of pitting (114/302 vertebrae
observed) after cervical (175/620 vertebrae) and nally,
thoracic (150/459 vertebrae). In this case, signicant differences are found (Table 4). The least frequent manifestation in the three regions is eburnation. In the lumbar
region, 27.1% of the individual and 11.2% of vertebrae

exhibit eburnation. In cervical vertebrae it is present in

25.6% of the individual and 10% of the vertebrae. In thoracic, eburnation was recorded in 18.2% of the individuals and 4.7% of the vertebrae. There are no signicant
differences between regions for FI, and the only signicant difference for FV is between thoracic and the other
two regions, but not between cervical and lumbar (see
Table 4).
Sex comparisons: The pattern of involvement is the
same in female and male individuals as described for the
apophyseal joints of the whole series (pitting, joint surface contour change and eburnation). Apparently,
females are more affected than males (Table 2), but the
differences are not signicant, for FI or FV (with the
exception of joint contour change P 5 0.023) (Table 4).
American Journal of Physical Anthropology

 LVEDA ET AL.
C. ROJAS-SEPU

424

Fig. 5. Pitting (A), joint surface contour change (B), and eburnation (C) in the apophyseal joints of the vertebral columns of the
Soacha 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 column
in the whole sample and by sex categories
Females (all ages)
FI
n/N
Cervical
M. One
40/44
Two together
27/44
Two separat
29/44
Eburnation
12/44
Pitting exc
30/44
Thoracic
M. One
38/45
Two together
16/45
Two separat
23/45
Eburnation
7/45
Pitting exc
27/45
Lumbar
M. One
36/43
Two together
26/43
Two separat
29/43
Eburnation
7/43
Pitting exc
30/43
Whole vertebral column
M. One
46/46
Two together
33/46
Two separat
39/46
Eburnation
22/46
Pitting exc
41/46

Males (all ages)

FV

FI

Whole series

FV

FI

FV

n/N

n/N

n/N

n/N

n/N

90.9
61.4
65.9
27.3
68.2

165/270
75/270

61.1
27.8

52.8
22.1
8.5
31.2

88.6
54.4
59.5
25.3
63.3

56.8
24.8

17/199
62/199

70/79
43/79
47/79
20/79
50/79

277/488
121/488

10.4
39.3

87.5
43.8
50.0
25.0
56.3

105/199
44/199

28/270
106/270

28/32
14/32
16/32
8/32
18/32

45/488
172/488

9.2
35.2

84.4
35.6
51.1
15.6
60.0

158/438
38/438

36.1
8.7

40.4
13.2
6.3
24.5

83.5
39.2
57.0
17.7
62.0

38.3
10.7

19/302
74/302

66/79
31/79
45/79
14/79
49/79

294/767
82/767

2.1
19.6

83.9
41.9
64.5
22.6
64.5

122/302
40/302

9/438
86/438

26/31
13/31
20/31
7/31
20/31

28/767
183/767

3.7
23.9

83.7
60.5
67.4
16.3
69.8

136/222
73/222

61.3
32.9

52.8
23.0
3.1
41.0

81.8
55.8
61.0
24.7
64.9

57.3
28.6

5/161
66/161

63/77
43/77
47/77
19/77
50/77

224/391
112/391

11.7
51.4

81.3
50.0
53.1
9.4
59.4

85/161
37/161

26/222
114/222

26/32
16/32
17/32
3/32
19/32

32/391
183/391

8.2
46.8

99.9
71.7
84.8
47.8
89.1

459/930
186/930

49.4
20.0

47.1
18.3
6.2
30.5

96.4
69.9
79.5
10.8
83.1

48.3
19.1

41/662
202/662

80/83
58/83
66/83
9/83
69/83

795/1646
315/1646

6.8
32.9

94.1
67.6
73.5
35.3
76.5

312/662
121/662

63/930
306/930

32/34
23/34
25/34
12/34
26/34

69/1646
524/1646

5.1
31.8

Row frequencies showed as n/N.

FI, frequency by individual; FV, frequency by vertebra.

Age comparisons: As described for the bodies, the differences in the FI of the three studied manifestations in
the apophyseal joints are very clear between the young
group and the other two (middle-age and old), but not
between these last two (Tables 4 and 5). Observation of
FV suggests that manifestation frequencies increase from
the youngest to the oldest (see Table 5). Differences
American Journal of Physical Anthropology

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

Diagnostic methods
Table 7 summarizes the frequencies of vertebral degenerative disease diagnosed by our ve methods in the

425

PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

2

TABLE 8. Chi-square (v ) and P-values for diagnostic methods in the whole vertebral column
Differences between methods (whole vertebral column)
FI
Diagnostic methods
One-two together
One-two separated
One-eburnation
One-pitting excluded
Two together-two separated
Two together-eburnation
Two together-pitting excluded
Two separated-eburnation
Two separated-pitting excluded
Eburnation-pitting excluded

FV

v2

20.793
11.142
122.1
7.930
2.040
60.088
4.055
79.023
0.357
87.063

0.000
0.001
0.000
0.005
0.153
0.000
0.044
0.000
0.550
0.000

v2

313.2

0.000

677.8
218.6

0.000
0.000

131.7
69.870

0.000
0.000

335.8

0.000

Signicant values are in bold.

FI, frequencies by individual; FV, frequencies by vertebra.

whole series and by sex, as well as the frequencies in

the three regions of the vertebral column and the whole
vertebral column. Almost invariably, the descending
order of frequency rates found by the different diagnostic
methods is At least One, Pitting excluded, Two separated, Two together, and Only Eburnation. For the
whole 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 individuals
positive and 19.1% of the vertebrae. The 79.5% of the
individuals (83/66) suffer vertebral degenerative disease,
according to the method Two separated. For the
method Only Eburnation, 10.8% of the individuals are
affected and 5.1% of the vertebrae, and for the method
Pitting excluded, the percentage of individuals affected
is 83.1% and 31.8% of the vertebrae. The differences
found between frequencies of vertebral degenerative
disease diagnosed by the ve methods are signicant
(Table 8).
Vertebral degenerative disease frequencies by individual for the different regions are very similar as seen in
Table 7. Table 9 shows that the differences are highly
signicant only for Two together method for thoracic
and lumbar regions, with lumbar vertebrae more frequently affected (56% of individuals with a positive diagnosis and 29% of the vertebrae). The same table shows
that FV is signicantly different in almost all cases. The
ve methods demonstrated differences between thoracic
and 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 Table 7. Differences of FI and FV of vertebral degenerative
disease between female and male vertebral columns for
the ve methods are not signicant (see Table 9). Disease prevalence in males and females, region by region,
are not signicantly different if the calculations are
made for FI. If they are made for FV, there are signicant differences between thoracic regions and lumbar
regions with Two together (P 5 0.0467 for thoracic
regions and P 5 0.035 for lumbar regions) and Only
Eburnation (P 5 0.003 for thoracic regions and P 5
0.002 for lumbar regions) methods; and between lumbar
regions using Pitting excluded (P 5 0.045), with female
regions more frequently affected.
Age comparisons: Frequencies of vertebral degenerative disease diagnosed by the ve methods applied in the
three age cohorts are presented in Table 10. They
increase from youngest to oldest individuals. For the

whole vertebral column, the differences between youngest and middle-aged individuals are signicant (Table 9),
with the middle-aged individuals more frequently diagnosed as positive. Table 9 shows that the differences
between middle-age and 451 groups are not statistically
signicant for FI or FV. This table also suggests that,
between the youngest (1530 years) and oldest (451)
cohorts, the differences are signicant with both methods (FI and FV), and are obviously higher for the oldest
group. If FI is calculated, differences among the three
vertebral regions for each age category are not signicant. Taking into account the FV, the differences are
more obvious.
Comparison of females and males by age groups shows
that proportions of vertebral degenerative conditions
diagnosed by all the methods in the whole vertebral column are very similar. Some signicant differences
appear when calculations are made by FV, but none in
the case of FI. Proportions in youngest groups by At
least One and Two together methods demonstrate
absolute differences (young males are more frequently
affected). Comparisons between older male and female
groups (451 years) showed important differences in FV
diagnosed by Pitting excluded method.

DISCUSSION
To approach the pattern of vertebral degenerative disease of the Soacha Muisca series, we applied two methods of proportion calculation and ve methods of diagnosis. Results demonstrate the important variations in
prevalence depending on methods used for paleoepidemiological reconstruction. Considering the high variability of methods applied in data processing in this eld and
the lack of consensus in data treatment between authors
comparisons are extremely difcult. Thus, it seems relevant to analyze the different methods in order to choose
the most appropriate one.

Frequency calculation
These results clearly show that the method of frequency calculation signicantly inuences paleoepidemiological results. Frequencies by number of individuals
were higher in this series than frequencies calculated by
number of vertebrae. Nevertheless, this would not be
observed if the preservation state (or number of vertebrae present by individual vertebral column) strongly
differs among individuals of a sample. Patterns of the
American Journal of Physical Anthropology

 LVEDA ET AL.
C. ROJAS-SEPU
0.083
0.001
3.007
10.252
33.686
186.27
0.000
0.000
19.888
131.46

0.000
0.000

0.000
0.000
37.681
16.956
203.29
124.85
0.000
0.000
89.176
62.726

0.000
0.000

0.854
0.409
0.967
0.409
0.034
0.683
0.002
0.683
0.004
0.012
0.035
0.080
8.349
6.299
4.446
3.071
0.003
0.001
0.028
0.007
8.932
12.029
4.859
7.202

Young-old
v2
P

Differences between age-groups

Young-middle
v2
P

vertebral degenerative conditions and its manifestations

as revealed by FI and FV calculation methods are similar in the Soacha series. FI and FV follow the same prole as can be concluded from Tables 7 and 10 (if FI
decreases or increases, FV reacts similarly). These two
methods seem to be complementary with regard to the
pattern of the degenerative conditions in our sample.
When one of the two methods does not show signicant
differences between proportions, the other provides additional information about the pattern of one manifestation or that of the disease.
For epidemiology, as for paleoepidemiology, the rst
relevant question is: how many individuals are affected
by the disease? However, due to the size and structure of
skeletal samples (an increased presence of old individuals will increase the frequency of DJD), an overestimation of DJD prevalence calculated by individual might be
produced (Dutour et al., 2003; Waldron, 1994). Using the
two methods of frequency calculation simultaneously
offers an opportunity to approach the disease both by
individual and by vertebrae, and bring an enhanced opportunity for comparisons with other published studies.
Thus, our preference is to use these two methods together whenever possible.

0.644
0.313
0.214
1.016
0.589
0.136
0.292
2.221

American Journal of Physical Anthropology

Signicant values are in bold.

10.834
12.043
0.000
0.000

0.001
0.001

0.381
0.391
0.767
0.737
0.000
0.000
37.649
59.855
0.025
1.651
0.000
0.000

0.875
0.199

0.693
0.214
0.262
0.129
0.156
1.547
1.256
2.302
0.776
0.038
0.605
0.288
0.706
0.081
4.311
0.268
1.130
0.142
0.232
0.859
0.844
0.926
0.831
1.430
0.032
0.039
0.009
0.046
0.358
0.056
0.747
0.245
0.869

Frequency by individuals
One
0.845
Two together
3.660
Two separated
0.104
Eburnation
1.349
Pitting excl.
0.027
Frequency by vertebrae
One
40.857
Two together
43.756
Two separated
Eburnation
16.894
Pitting excl.
182.07

v2
P
v2
Method

v2

Cerv-lumb

Differences between regions

Thor-lumb

Male-female
v2
P

Sex differences

Diagnostic methods

Cerv-thor

TABLE 9. Chi-square (v2) and P-values for diagnostic methods in the vertebral regions, by age and sex

Midd age-old
v2
P

426

The present article focused on the diagnosis of vertebral degenerative conditions. At the beginning of this
study, we hypothesized that a single manifestation is
enough to make a positive diagnosis in an individual.
The criteria of the At least One in our series, produced
percentages close to 100% of the population affected,
even in the youngest age categories. Although some
examples of vertebral degenerative conditions among the
very young have been reported (Stirland and Waldron,
1997), high frequencies such as those obtained in the
Soacha Muisca series with At least One (88% of individuals and 25% of vertebrae) could be rejected. Additionally, results obtained by this method do not allow
comparison because it generalizes the disease to each anatomical region and subpopulation group.
Restricting the criteria led us to explore another diagnostic method. The method Two together ensured a
correct diagnosis because eburnation is considered pathognomonic of the disease or a marker of its severity
(Rothschild, 1997; Ortner, 2003). However this method
requires the association of at least two of the other manifestations and this may underestimate DJD in poorly
preserved skeletal series. Additionally, osteophytes and
joint surface contour change have also been considered
as pathognomonic of DJD (Nathan, 1962; White and
Folkens, 2000; Ortner, 2003). Counting them only when
they are associated with other manifestations can also
lead to prevalence underestimation.
The method Two separated is a variation of the
method called Two together, discussed above. The
method Two separated provides the possibility of having the manifestations in two different vertebrae. This
avoids some underestimation; nevertheless, here also, we
can argue against the method due to the fact that osteophytes and joint surface contour change have been considered as pathognomonic (Nathan, 1962; White and
Folkens, 2000; Ortner, 2003).
Concerning the Only Eburnation method, it would
not be desirable to reduce the diagnosis to its presence
only, ignoring the other typical and accepted manifesta-

427

PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

TABLE 10. Diagnosed vertebral degenerative disease in the anatomical regions of the vertebral column by age categories
Young (1530)
FI
n/N
Cervical
M. One
18/25
Two together
4/25
Two separat.
6/25
Eburnation
1/25
Pitting exc
11/25
Thoracic
M. One
18/25
Two together
5/25
Two separat.
8/25
Eburnation
4/25
Pitting exc
9/25
Lumbar
M. One
13/23
Two together
7/23
Two separat.
7/23
Eburnation
2/23
Pitting exc
9/23
Whole vertebral column
M. One
23/26
Two together
11/26
Two separat.
14/26
Eburnation
6/26
Pitting exc
17/26

Middle (3045)
FV

FI

Old (451)
FV

FI

FV

n/N

n/N

n/N

n/N

n/N

72.0
16.0
24.0
4.0
44.0

46/159
5/159

28.9
3.1

63.7
28.0
6.0
42.3

99.9
85.0
85.0
35.0
85.0

80.0
46.2

11/182
77/182

20/20
17/20
17/20
7/20
17/20

104/130
60/130

0.6
8.2

93.5
61.3
67.7
19.4
93.5

116/182
51/182

1/159
13/159

29/31
19/31
21/31
6/31
29/31

20/130
74/130

15.4
56.9

72.0
20.0
32.0
16.0
36.0

57/253
10/253

22.5
4.0

38.3
11.4
4.1
27.6

95.0
50.0
75.0
20.0
80.0

57.7
18.0

12/290
80/290

19/20
10/20
15/20
4/20
16/20

112/194
35/194

2.4
6.3

87.1
45.2
64.5
19.4
71.0

111/290
33/290

6/253
16/253

27/31
14/31
20/31
6/31
22/31

10/194
64/194

5.2
33.0

56.5
30.4
30.4
8.7
39.1

33/127
14/127

26.0
11.0

65.6
33.1
8.4
56.5

99.9
71.4
81.0
42.9
85.7

86.1
44.6

13/154
87/154

21/21
15/21
17/21
9/21
18/21

87/101
45/101

2.4
18.1

93.3
66.7
73.3
23.3
73.3

101/154
51/154

3/127
23/127

28/30
20/30
22/30
7/30
22/30

15/101
70/101

14.9
69.3

88.5
42.3
53.8
23.1
65.4

136/539
29/539

25.2
5.4

52.4
21.6
7.5
39.0

99.9
82.6
87.0
52.2
87.0

71.3
32.9

47/626
244/626

23/23
19/23
20/23
12/23
20/23

303/425
140/425

1.9
9.6

99.9
80.6
93.5
51.6
93.5

328/626
135/626

10/539
52/539

31/31
25/31
29/31
16/31
29/31

45/425
208/425

10.6
48.9

Row frequencies showed as n/N.

FI, frequency by individual; FV, frequency by vertebra.

tions of DJD. This procedure underestimates disease

prevalence, not only because eburnation is present exclusively on apophyseal joints, but also because it is uncommon. Additionally, one damaged surface that does not
permit observation may signicantly inuence the prevalence.
Finally, the Pitting excluded method as a modication of the At least One does not consider isolated body
or apophyseal pitting as diagnostic criteria. This possibility was contemplated in light of preliminary results
where pitting appeared to be a ubiquitous manifestation.
Pitting was seen in females, males, and in every age
group in a generalized way at all vertebral levels. Determination of pitting presents intrinsic difculties, being
easily confused with taphonomic damage or normal pits
in young vertebral bodies. As already mentioned, isolated pitting has been demonstrated to be a manifestation without a clear relationship with DJD (Rothschild,
1997; Sofaer, 2000). Thus, Pitting excluded seems to be
a very good choice that permits standardization.

Vertebral degenerative conditions in Soacha

Muisca series
Paleoepidemiology must take into account several
aspects. First of all, as Waldron (1994) pointed out, a
sample from a cemetery represents a community of
skeletons which is different from a population of living
people. Paleoepidemiology has indeed very little to do
with present epidemiology because of a set of specic
biases (Waldron, 1994; Dutour et al., 1998, 2003). The
Soacha Muisca series is the result of the excavation of
one part of an extensive cemetery (Rodrguez, 1999;
Boada, 2000); so our conclusions do not apply to the
entire Muisca population but only to those Muiscas buried in the sector of Soacha-Portalegre. Second, the bone

preservation is a very important issue. Soacha materials

were well preserved allowing good observation of the
aspects studied (additionally, frequency calculations used
only preserved elements). Considering the age structure
of the series, the children are under-represented, but
this under-representation does not have direct repercussions on the study of DJD. On the other hand, the presence of individuals between 15 and 20 years in the excavated area of the cemetery may suggest that at this age,
an individual was already considered an adult, involved
in economic life with obligations which could have
exposed them to very early stress, causing the acceleration of the aging process (Stirland and Waldron, 1997).
DJD does not contribute directly to death, which means
that its prevalence in a skeletal population can reect
the 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 change
and osteophytes are very frequent. The least frequent
manifestation in each subpopulation is eburnation. Manifestations are more frequent in the lumbar region. The
pattern on female vertebral columns follows the same
general prole. In male individuals, osteophytosis more
frequently involves the thoracic region, but when the
lumbar region is involved, several vertebrae show osteophytes. In the young age group (1530 years), the pattern is very similar to that described for the whole series, but eburnation predominates in the thoracic area.
This is not common, especially because a very young
individual presented this manifestation (1520 years).
Vertebral degenerative conditions in the Soacha
Muisca series more frequently involved cervical and lumbar areas. The pattern in females is the same. In males,
the pattern is repeated with almost all diagnostic methods, with the exception of Two separated and Pitting
American Journal of Physical Anthropology

428

LVEDA ET AL.
C. ROJAS-SEPU

excluded calculated by FI, where the thoracic region

was the most frequently involved. This could reect a
subtle difference between sexes, perhaps reecting differing postures adopted by Soacha Muisca females and
males. On the basis of the similarity in frequencies of
affected vertebrae, equality in quantity and strength of
physical activity could be suggested between sexes, but
differences in location may suggest a difference in the
type of activities.
At the beginning of adulthood, the three regions of the
vertebral column were involved. At age 30, degenerative
alterations are most severe in the cervical and lumbar
regions, a pattern that continues into the oldest age
groups. The degenerative conditions were frequently
present from early adulthood, but involved progressively
more and more vertebrae as individuals aged.
High frequencies in young individuals are not only
based on the occurrence of apophyseal pitting, they are a
result of the recording of the others manifestations studied. This suggests that hard physical activities began
early in the Soacha Muiscas life. A very strenuous lifestyle reected in the high prevalence of the disease in
the whole series (8083% of the observed vertebral columns) is suggested.

Vertebral degenerative conditions in the Soacha

Muisca series in perspective
As already pointed out, it is not easy to make comparisons with available published data. Nevertheless, an
extensive comparison of vertebral degenerative conditions between the Soacha Muisca series and other past
populations previously described was carried out. This
could be done by adapting our data to the methodologies
used in the previous studies. As we applied several
methods of diagnosis and proportion calculations, we are
able to compare our data to previous works. For some
comparisons, osteophytes and joint surface contour
change were pooled according to the descriptions of the
recorded 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 geographically nearest populations are worthy of comment.
Comparison of the Soacha Muisca osteophyte frequency with series from Central and Southern Mexico
studied by Chapman (1972) indicates lower frequencies
in Soacha. In the Dickson Mounds population (Clark and
Delmond, 1979), osteophytosis occurred earlier in male
lumbar regions than in those of females, a prole not
found in the Soacha Muisca series. Frequencies of osteophytosis found by Jurmain (1990) in a precontact
hunter-gatherer population of California are higher than
those calculated for the Soacha Muisca series. Nevertheless, apophyseal joints in Jurmains series are less
involved than in the Soacha sample. Frequencies in the
studied Muisca series are higher than frequencies
obtained by Kahl and Ostendorf (2000) in prehistoric
New Mexican populations.
In agreement with Bridges (1992) study, there is not a
constant level (frequency) of arthritis and on pattern
between populations. Bridges points out that differences
between males and females from ancient agriculturalist
populations of North America are evident, nding
greater thoracic osteophytosis in females and more osteoarthritis of the apophyseal facets in the cervical region
in males (Bridges, 1992). The Soacha series shows the
highest differences in osteophytes and body joint surface
American Journal of Physical Anthropology

contour change between males and females in the lumbar area, with females being more strongly affected. The
high cervical involvement of apophyseal facets in males
seen by Bridges (1992) seems to be true in our series.
Following Bridges (1992), the lower extent of sexual
dimorphism in some prehistoric groups suggest a similarity in sex roles or in some cases more strenuous
duties for females.
Differences between populations have supported the
relationship of DJD and physical activity in many publications. Accepting the hypothesis of a positive relationship between DJD and physical activity (Chapman,
1972; Clark and Delmond, 1979; Goranov et al., 1983;
Jurmain, 1990; Bridges, 1991, 1992; Lovell, 1994; Stirland and Waldron, 1997; Kahl and Ostendorf, 2000;
Sofaer, 2000), results presented here suggest that the
individuals recovered from the Soacha Muisca cemetery
were exposed to a high level of physical activity. This
should accelerate the aging process, with an early onset
and no sex differences in terms of quantity of degenerative lesions.

CONCLUSION
It has been shown that calculation of manifestations
and disease frequencies should be done by applying the
two methods, FI and FV. From the ve diagnostic methods considered, the most suitable seems to be the method
called Pitting excluded. This method takes into account
the manifestations related to vertebral degenerative conditions (body and apophyseal joint surface contour
change, osteophytes and eburnation), excluding the isolated body and apophyseal pitting as diagnostic criteria.
Pitting excluded reduces underestimation because it
does not require association between manifestations, and
it also avoids overestimation by ignoring the isolated pitting as a diagnostic criterion (pitting observed as a general manifestation).
Our article also underscores the lack of discussion concerning prevalence calculation in paleopathological literature. Explicit explanation of calculation and diagnostic
methods can allow relevant interpopulational comparisons. In spite of these difculties, it is possible to place
vertebral degenerative disease in the Soacha Muisca series within the frequencies and patterns of variability
from the published literature. This variability supports
the hypothesis of a relationship between DJD and physical activity. Furthermore, our results suggest that the
Soacha Muisca population does not completely follow the
classical pattern of agricultural populations (higher percentages of disease than hunter-gatherers and gender
differences; Bridges, 1992). Individuals recovered from
the Soacha Muisca cemetery were exposed to a high
level of work which accelerated the aging process of the
spine with a very early onset and without discrimination
by sex.
Our results t very well with ethnohistorical data
from the region. Although for the chroniclers of the
Spanish conquest the justication of conquest and Christianization led them to write mostly negative comments
about indigenous work habits (Rodrguez, 1999; Enciso
and Therrien, 2000), some selected information does
come out that the Muiscas undertook heavy labor. There
are references to heavy load-bearing, especially related
to the salt trade. This product was packed in loaves of
24 kg which were carried by Muiscas on the back for distances longer than 50 km through very difcult terrain

PRE-COLUMBIAN VERTEBRAL DEGENERATIVE CONDITIONS

(Groot, 2000). Agricultural activities and the construction of canals and terracing demanded a large amount of
physical work. Because these activities were assisted
neither by pack animals nor by iron tools (Rodrguez,
1999), all the stress they caused went directly to peoples
bodies. This stress produced traces on their bones and
more specically on their vertebral remains that nowadays may testify it.

ACKNOWLEDGMENTS
The rst author is indebted to Dr. Jose Vicente Rodrguez for help, encouragement and supervision of the initial part of this research. We thank to the ICANH (Instituto Colombiano de Antropologa e Historia) for access to
the series. We are grateful with Dr. Elie Sanchez for statistical advice. Many thanks are also due to our three
anonymous reviewers and Dr. Clark Larsen who contributed to greatly improve this article. We are indebted to
Mr. Timothy Sexton who kindly made a grammatical revision of our manuscript.

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