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J Forensic Sci, 2018

doi: 10.1111/1556-4029.13972
PAPER Available online at: onlinelibrary.wiley.com

ANTHROPOLOGY

Allysha Powanda Winburn , Ph.D.

Validation of the Acetabulum As a Skeletal


Indicator of Age at Death in Modern
European-Americans†,‡

ABSTRACT: Progressive changes in the acetabulum have been used in modern skeletal age estimation, but they have not been completely
understood. If their age correlations are weakened by the influence of factors like physical activity and obesity, acetabular changes should not
be used for age estimation. To investigate their utility for aging, the acetabular variables of Rissech et al. (2006) were analyzed in 409 modern
European-Americans (Bass Collection, Tennessee). Correlation tests assessed potential associations between acetabular data, osteoarthritis scores
(collected per Jurmain, 1990), and documented demographic information (age, body mass index [BMI], metabolic intensity of physical activi-
ties). Acetabular changes had statistically significant, positive correlations with osteoarthritis (p < 0.001 in most joints/regions) and age
(p < 0.001), indicating their degenerative nature and relevance for age estimation. Acetabular changes showed no associations with BMI or
metabolic values, suggesting resistance to obesity and activity effects. These results suggest that acetabular degeneration is a valid skeletal age-
at-death indicator.

KEYWORDS: forensic science, forensic anthropology, age estimation, pelvis, skeletal degeneration, arthritis, obesity, physical activity

The acetabulum has been a focus of age-estimation research whether this joint surface is a valid age indicator must be
for over a decade, and several acetabulum-based aging methods answered.
have been proposed (1–3). However, the progressive changes
that occur in the acetabulum remain poorly understood. These
Background
changes may constitute skeletal metamorphoses (akin to the for-
mation of the ventral rampart of the pubic symphysis), which Accurate and precise methods of skeletal age-at-death estima-
are generally believed to be linked with age. Alternately, acetab- tion are vital to the generation of the biological profiles that
ular changes may represent osteoarthritis (OA)—generally enable individual identifications. Broad age intervals contribute
viewed as degenerative, less strongly correlated with age, and little to the elimination of potential matches from the universe of
more influenced by factors like physical activity and obesity. missing-persons, while narrow intervals may exclude the correct
This research investigated the nature of progressive changes in missing-person from consideration. Still, adult age estimation
the acetabulum. It aims to determine whether acetabular changes remains challenging.
are metamorphic or degenerative, ascertain whether they are Forensic anthropologists frequently examine joint surfaces to
valid indicators of age at death, and scrutinize the overall utility inform their adult age estimates (1–42). All joints change with
of a dichotomous, “metamorphic vs. degenerative” approach to age, but some exhibit metamorphic change, while others exhibit
age estimation. By focusing on the skeletal biology underlying degenerative change (39). Metamorphic skeletal changes occur
acetabular changes, this research contributes to an understanding after the attainment of skeletal maturity but independent of
of acetabular age progression that will enhance future method skeletal degeneration. They are often portrayed as more relevant
testing and validation. Before acetabular aging methods continue to age estimation than degenerative changes, since the latter pro-
to be developed and refined, the fundamental question of cesses are complicated by intra-individual variation and inter-
individual differences—both hereditary and environmental (e.g.,
nutrition, bone density, mechanical loading, hormonal influences
1
Department of Anthropology, University of West Florida, 11000 Univer- [39,43,44]). The degenerative processes that complicate adult
sity Parkway, Bldg. 13, Pensacola, FL 32514. age estimation can become more pronounced and variable over
Corresponding author: Allysha Powanda Winburn, Ph.D. E-mail: awinburn
an individual’s lifetime, and this trajectory effect (45) can trans-
@uwf.edu

Presented in part at the 70th Annual Scientific Meeting of the American late to further-decreased accuracy with advancing age (43,46; cf.
Academy of Forensic Sciences, February 19-24, in Seattle, WA. 47). Thus, age estimates for elderly adults are often more diffi-

Financial support for this study was provided by the National Institute of cult to achieve, less accurate, and less precise than age estimates
Justice Graduate Research Fellowship Program in Science, Technology, for younger adults, and anthropological aging methods tend to
Engineering, and Mathematics (Grant #: 2015-R2-CX-0009) and the Univer-
sity of Florida Graduate School Doctoral Research Travel Award. underestimate age in the oldest individuals (46,48,49).
Received 25 July 2018; and in revised form 8 Oct. 2018; accepted 13
Yet, due to advances in health care and standards of living,
Nov. 2018. modern individuals are more likely than past peoples to reach

© 2018 American Academy of Forensic Sciences 1


2 JOURNAL OF FORENSIC SCIENCES

advanced ages at death (50). This presents a particular problem activities. Thus, it is also possible that differing levels of physi-
for forensic anthropologists, who face the challenge of providing cal activity can influence the way the acetabulum changes with
the accurate age estimates that enable identifications for a world age. Further, diarthrodial joints commonly develop OA—the
population with a rising mean age at death. According to breakdown of normal relationships among articular tissues that is
missing-persons data curated by the FBI’s National Crime Infor- often visible in skeletal remains (via osteophytes, eburnation,
mation Center—a dataset approximating the universe of uniden- and ankylosis). Biological anthropologists have long noted that
tified decedents analyzed by forensic scientists—of 43,646 OA increases with age (35,39); certainly, elderly individuals suf-
active adult missing-persons cases, approximately 50% of miss- fer more frequently from OA than younger individuals (54).
ing adult females and 65% of missing adult males are 40 years However, the correlation between advancing age and increasing
of age or older (51). OA is generally viewed as weak, due to the many other factors
Forensic anthropologists must identify skeletal indicators of influencing OA development (17,43). These factors include both
adult aging processes and validate methods based on these indi- vigorous physical activity (55–57) and obesity (58–63). If the
cators, so that they can estimate age with accuracy and precision changes observed in the acetabulum are akin to the processes of
even in older individuals. Much research on adult age estimation OA observed in the other diarthrodial joints, then acetabular
has centered on the pelvis, due to the late-onset age-related changes could be strongly correlated with factors like activity
changes that occur in its amphiarthrodial joints (the relatively and obesity rather than with age.
immobile pubic symphysis and sacro-iliac joint). The age-related The effects of activity and obesity on the age-related changes
changes of the pubic symphysis have been studied for over a of the acetabulum—and the relationship of these changes with
century (4,5,9,10,12–14,16,21,36,37,41). In particular, the meta- OA—have not been investigated. Before forensic anthropologists
morphic changes of the ventral rampart have been emphasized can responsibly use the acetabulum to estimate age, research
for their role in enabling accurate and precise age estimates in must ascertain the following: Are acetabular changes affected by
adults younger than 40 years (5,16). However, degenerative patterns of physical activity and obesity? Are the changes truly
changes of the pubic symphysis are also informative for estimat- metamorphic, or are they degenerative? What does that mean in
ing age in older individuals (4,14). Unfortunately, the often-poor terms of their correlation with age? If they merely constitute
preservation of the pubic symphysis in adverse depositional degenerative change, are they still useful for adult age estima-
environments undermines its utility as an age indicator (7,18). tion? Thus, this research aims to illuminate the potential utility
The auricular surface of the ilium has also been widely studied or unreliability of acetabular age changes and critically evaluate
(7,11,15,18,23–26,33,35,36). However, iliac auricular surface the dichotomy between metamorphic and degenerative changes
methods either tend to downplay the variability of age-related for skeletal age estimation.
change in the joint (18) or classify it into broad phases resulting
in imprecise age estimates (26). The auricular surface of the
sacrum has also been considered for age estimation, though age- Materials and Methods
related changes are even less pronounced in this region than in
Skeletal Sample
the iliac auricular surface (6,27,28). The auricular surfaces lack
regions of metamorphic change analogous to the ventral rampart In order to investigate these problems, acetabular changes and
of the pubic symphysis, but it is unclear whether the difficulties OA were analyzed in a sample of European-American skeletal
of auricular surface aging stem from the degenerative nature of individuals from the W.M. Bass Donated Skeletal Collection
their age changes. (University of Tennessee [UT], Knoxville) with documented
Recently, biological anthropologists have also begun to antemortem data on age, ancestry, sex, height, body mass, and
explore the age-estimation potential of the acetabulum (1– habitual/occupational activities. A stratified random sample was
3,8,19,20,22,29–34,40,42). The acetabulum is a robust joint with assembled from individuals previously determined to meet the
a relatively protected anatomical location (8,31) and the potential study’s documentary requirements. These 409 European-Ameri-
to survive the burial and fragmentation scenarios common in can females (n = 198) and males (n = 211) populated eight age
forensic cases (42,52). Accurate acetabular age estimates have groups approximating 10-year intervals (Table 1, Fig. 1). A goal
been reported, even for older individuals (2,8,30). Evidence that of 30 individuals per age cohort was set for both females and
the changes observed in this joint are not degenerative but meta- males. However, because of the demographic makeup of the
morphic—akin to the tightly age-correlated changes of the pubic Bass Collection (fewer females than males; fewer extremely
symphysis ventral rampart—might also constitute an argument young and extremely old individuals), some of these 10-year age
for the use of the acetabulum in age estimation. However, after categories could not be fully populated (see Table 1; also see
more than a decade of research, the nature of acetabular changes below discussion of the study’s ancestral limitations).
(i.e., metamorphic vs. degenerative) remains obscure. Further,
the metamorphic vs. degenerative dichotomy itself is still rela-
Data Collection
tively unexplored. Thus, it also remains unclear to what degree,
if any, metamorphic changes truly outperform degenerative For each individual in the sample, left and right acetabula
changes as skeletal indicators of age. were observed and scored using the method developed by Ris-
Several factors have the potential to complicate the straightfor- sech et al. (2), in which seven acetabular variables are assigned
ward age correlation of the progressive changes observed in the ordinal scores which can range from 0–3 to 0–6 (Table 2,
acetabulum. Like the pubic symphysis and auricular surface, Fig. 2). In order to enable parametric, multivariate statistical test-
the acetabulum participates in the transfer of body mass from ing of normally distributed acetabular scores, composite acetabu-
the upper body to the lower limb. It is thus possible that obesity lar scores (CAS) were also created (19). The ordinal acetabular
—an excess of adipose tissue—may affect acetabular changes variable scores were transformed into a common scale of 0–10,
(53). Unlike the amphiarthrodial joints of the pelvis, however, so that each variable would be weighted equally. For example, if
the acetabulum is diarthrodial, mobile, and used in daily physical a variable received a score of 1 on a scale of 0–3 (2), this was
WINBURN . VALIDATION OF THE ACETABULUM FOR AGING 3

TABLE 1––Total sample of European-American adults (Bass Collection,

10 15 20 25 30 35
UT) analyzed in the current study, arranged by age group, with mean and
median ages.

Sex Age Group n Mean Age Median Age

Count
Female 20–29 3 27 27
30–39 14 35.7 36.5
40–49 33 45.3 46
50–59 33 54.7 55
60–69 33 64.8 66
70–79 33 74.7 75

5
80–89 33 83.9 84
90+ 16 92.4 92

0
Female total 198 64.3 65.5
Male 19–29 10 24.3 25.5 20-29 30-39 40-49 50-59 60-69 70-79 80-89 90+
30–39 32 34.9 35
40–49 34 45.4 45.5 Female Age Group (Years)
50–59 31 54.5 55
60–69 32 64.2 65
70–79 33 73.9 74
80–89 33 83.5 83

35
90+ 6 94.7 95
Male total 211 58.8 59

30
Total 409 61.5 61

25
transformed to 3.33 (19). Transformed scores were summed and
20
Count
averaged to achieve a CAS for each individual.
Evidence of OA was also observed and scored in the major 15
appendicular joints (shoulder, elbow, wrist, hip, knee, ankle) and
10

the temporomandibular joint (TMJ). Using the Jurmain (64) ordi-


nal scoring system (Fig. 3), each element in a joint was assigned
5

an individual score (e.g., acetabulum, proximal femur), and then,


0

the individual scores were added and divided by the number of


available elements in order to achieve a combined joint score (e.g., 19-29 30-39 40-49 50-59 60-69 70-79 80-89 90+
“left hip” = [left femoral head score + left acetabulum score]/2).
Male Age Group (Years)
Left and right combined joint scores were initially kept separate.
However, subsequent Wilcoxon rank-sum testing indicated no sta-
FIG. 1––Sample distribution by age group and sex (overall n = 409;
tistically significant differences between left and right mean joint female n = 198; male n = 211).
scores for females (largest difference 0.04) or males (largest differ-
ence 0.08). In 14 Wilcoxon rank-sum tests (significance level,
a = 0.004 with Bonferroni correction), female p-values ranged (66). A MET value consists of the measured or estimated meta-
from 0.42 to 0.74 (Spearman’s rho values ranged from 0.641 to bolic rate of a given activity divided by the resting metabolic
0.748), and male p-values ranged from 0.09 to 0.90 (rho values rate for quiet sitting, classified as 1 MET (67,68). In this classifi-
ranged from 0.571 to 0.774). Thus, left and right joint scores were cation system, a 3-MET activity involves three times the energy
combined and averaged following the protocol of Weiss (65). In expenditure of a 1-MET activity. For example, outdoor construc-
the case of missing data (i.e., damaged or missing articular sur- tion work is estimated as a 4-MET activity, and conducting
faces), fewer surfaces were used in the calculation of the combined seated office work is estimated as a 1.5-MET activity (66). The
joint variable. The OA scores were used in the analyses of individ- current version of the Compendium of Physical Activities con-
ual joints (as ordinal data) and averaged to achieve overall, upper tains MET values for 821 activities, many of which were
limb, and lower limb OA scores (which approximated continuous obtained from published measurements (66).
data and were normally distributed). The Compendium is typically used to assign standardized
codes to the physical activities self-reported by survey partici-
pants, in order to facilitate comparison among studies. When the
Coding Demographic Data
activity data recorded for a Bass Collection individual were
Subsequent to data collection, demographic data (e.g., age, specific (e.g., describing a sport played during life), individual
biological sex) were re-associated with each individual in the activities and occupations were assigned to specific Com-
sample. Documented height and body mass data were used to pendium categories. Even when reported activities were less
calculate BMI using the following formula: BMI = mass [kg]/ specific (e.g., reporting “exercise” rather than a specific sport),
height [m]2. Resulting BMI values were then categorized accord- they were sufficient to allow coding using a modified protocol
ing to National Institutes of Health standards current as of 2017: (68). Using this protocol, all associated example activities shar-
obese (≥ 30); overweight (25–29.9); normal-weight (18.5–24.9); ing similar Compendium codes were averaged to create an esti-
and underweight (< 18.5). mated MET value for the overall category (68). If an individual
All occupational and habitual physical activities documented listed more than one activity, the aggregate MET values for each
for the individuals in the sample were assigned a metabolic listed activity were averaged to create an overall estimated MET
equivalent (MET) intensity level using the activity codes and level for that individual. This coding system was applied to both
MET values listed in the Compendium of Physical Activities reported occupations and habitual-activities. In order to enable
4 JOURNAL OF FORENSIC SCIENCES

TABLE 2––Descriptions of the seven acetabular variables and their states, summarized from Rissech et al. (2).

Variable Description of Variable Characteristics of the States


1. Acetabular groove Groove surrounding the internal acetabular rim Younger: no anatomical interruption
between lunate surface and rim.
Older: pronounced groove.
States 0–3
2. Acetabular rim shape Outer rim of the acetabulum Younger: dense, round and smooth.
Older: rough, with osteophytic growth.
States 0–6
3. Acetabular rim porosity Texture and activity of the outer rim Younger: smooth, little porosity.
Older: macroporosity and destruction.
States 0–5
4. Apex activity Osteophytic activity on the apex of the posterior cornu Younger: round, smooth apex.
Older: osteophytic growth of one (sometimes both)
horns of the lunate surface.
States 0–4
5. Fossa edge activity Crest formation between fossa and lunate surface Younger: smooth, no delineation between surfaces
Older: visible crest.
States 0–5
6. Fossa activity Level and activity of the acetabular fossa Younger: dense, level acetabular fossa.
Older: irregular with much activity.
States 0–5
7. Fossa porosity Texture and integrity of the acetabular fossa Younger: dense, smooth fossa.
Older: macroporosity and destruction.
States 0–6

interactions of age, activity, and obesity with acetabular changes


(Hypotheses 2, 3, and 4), and the relative contributions of these
factors to acetabular changes (Hypothesis 5). The following
hypotheses were designed to assess whether acetabular changes
are metamorphic or degenerative (Hypothesis 1) and whether
they are relevant to skeletal age estimation (Hypotheses 2
through 5).

Hypothesis 1 Acetabular Changes Correlate Positively with OA


Individuals with higher CAS (19) and higher individual
acetabulum aging scores for the seven variables (2) were
predicted to exhibit more OA in the other joints of the
body. Transformed CAS and scores for each of the seven
individual acetabular variables were tested for positive associa-
tions with OA scores (64) in individual joints and combined
joint regions (overall OA, upper limb OA, and lower limb
OA).

Hypothesis 2 Acetabular Changes Correlate Positively with Age


FIG. 2––Acetabular variables scored in the method of Rissech et al. (2): Older individuals were expected to exhibit “older-looking”
the acetabular groove (Variable 1); acetabular rim shape and porosity
(Variables 2 and 3); activity on the apex of the posterior cornu (Variable 4); acetabula. Transformed CAS and scores for each of the seven
crest formation on the edge of the acetabular fossa (Variable 5); and acetab- individual acetabular variables were tested for positive associa-
ular fossa activity and porosity (Variables 6 and 7). Photograph by the tions with age.
author.

an assessment of the impact of strenuous activities utilizing the


Hypothesis 3 Acetabular Changes Correlate Positively with
lower limb, habitual physical activities involving the lower limb
Activity
(e.g., running, wrestling) were noted during scoring so that they
could be tested separately. Individuals who had undertaken more vigorous occupational
and habitual physical activities were expected to exhibit “older-
Hypotheses looking” acetabula than age-matched individuals undertaking less
vigorous physical activities. Transformed CAS and scores for
This research tested a series of hypotheses examining the rela- each of the seven individual acetabular variables were tested for
tionship between acetabular changes and OA (Hypothesis 1), the positive associations with the MET level of documented physical
WINBURN . VALIDATION OF THE ACETABULUM FOR AGING 5

FIG. 3––Images of the acetabulum (left) and distal femur (right), corresponding with OA scores in the Jurmain (64) system: 0 = no OA/slight OA; 1 = mod-
erate OA (small osteophyte and/or pitting over < 10% of articular surface); 2 = severe OA (very large osteophyte/remodeling and/or pitting over > 10% of
articular surface; or any evidence of eburnation); 3 = ankylosis (joint fusion; not pictured). Photographs by the author.

activities (66). In particular, tests assessed whether high


Hypothesis 4 Acetabular Changes Correlate Positively with
acetabular scores were associated with rigorous documented
Obesity
habitual physical activities utilizing the lower limb (e.g.,
running, wrestling). To control for age, individuals were com- Obese individuals were expected to exhibit “older-looking”
pared within age-matched 10-year subsamples (e.g., 30–39 years, acetabula than age-matched normal-weight or underweight indi-
40–49 years). viduals. This hypothesis employed BMI as a proxy for obesity.
6 JOURNAL OF FORENSIC SCIENCES

Transformed CAS and scores for each of the seven individual preservation of the observed skeletal elements (Table 3). Prelimi-
acetabular variables were tested for positive associations with nary statistical analyses (Wilcoxon rank-sum tests) indicated no
BMI values. To control for age, individuals were compared statistically significant differences for left and right CAS
within age-matched 10-year subsamples. (p > 0.25) and acetabular variables (p > 0.02; a = 0.007; Bon-
ferroni correction: a = 0.05/7) for either sex. Spearman’s rank-
order correlation tests also indicated left and right scores to be
strongly correlated (CAS: female q = 0.849, male q = 0.864;
Hypothesis 5 Of the Above Factors, Age has the Most
acetabular variables: rho values ranged from 0.608 to 0.762 for
Influence on Acetabular Changes
females and from 0.592 to 0.793 for males). Thus, left and right
Once the above-proposed associations between acetabular CAS were averaged to create an overall CAS for each individ-
changes and age, activity, and obesity had been supported or ual. This averaging was deemed appropriate for a summary mea-
rejected, this research endeavored to determine the relative sure of acetabular changes, akin to the combined joint OA
importance of these contributing factors. Multivariate statistical scores averaged according to the protocol of Weiss (65). This
analyses assessed the influence of age, occupational activities, also created an approximation of continuous, normally
habitual-activities, and BMI on CAS. distributed data for these variables. Rather than averaging the
acetabular variables, only left-side variables were used in
the below analyses (with right-side variables substituted in cases
Statistical Testing
of damaged or pathological acetabula), following the protocol of
Statistical tests were conducted in R (69) to assess potential Rissech et al. (2). This preserved the original, ordinal nature of
associations between acetabular scores/CAS and OA scores, ages these individual acetabular variable data.
at death, MET values, and BMI. Wilcoxon rank-sum tests Wilcoxon rank-sum tests revealed statistically significant differ-
assessed sex and side differences, as well as differences between ences between the means for female and male CAS (p = 0.01) and
individuals engaging in strenuous physical activities utilizing the female and male MET values for occupations (p = 0.001). Female
lower limb and individuals who did not engage in these rigorous and male OA score means also differed significantly in several
activities. Associations between ordinal datasets (e.g., acetabular joints (seven Wilcoxon rank-sum tests; a = 0.007 with Bonferroni
and OA scores) were assessed via Spearman’s rank-order corre- correction). Because of these significant differences, tests of CAS,
lation tests (rho) and Spearman’s tests calculating p-values using occupational MET values, and TMJ, hip, knee, and ankle OA data
the conditional null distribution of the test statistic (asymptotic utilized separate female and male analyses. Sex-specific results are
approximation of the exact distribution), with ties in rank presented separately, below. Wilcoxon rank-sum tests revealed no
resolved using mid-ranks. Associations between continuous data- statistically significant differences in the female and male means
sets (e.g., CAS, ages at death, BMI, MET values) were visual- of: acetabular variables (a = 0.007; Bonferroni correction:
ized via scatterplots and assessed via Spearman’s rank-order a = 0.05/7); overall, upper limb, and lower limb OA; MET values
correlation tests (rho) and linear regression (p, adjusted r2). The for habitual-activities; or BMI values, so combined-sex analyses
alpha-level was set at 0.05, and the Bonferroni correction was were undertaken. For these data, combined-sex results are pre-
applied in cases of multiple test iterations. sented below, except where comparisons involved distributions
Multivariate statistical testing isolated the variables exerting that showed sex differences (e.g., OA scores).
the greatest influence on acetabular changes. Graphical examina-
tion of the variables suggested that some of the study data (i.e.,
Hypothesis 1
BMI and habitual and occupational activities) did not meet the
assumptions of normality within a variable or linearity when Hypothesis 1 was supported: Testing revealed statistically sig-
plotted against one another. Thus, these variables were each log- nificant positive correlations between CAS and OA in all
transformed prior to multiple regression (MR) analyses, using
the natural logarithm. Combined linear models were then con-
structed for females and males separately, including all potential TABLE 3––Sample sizes for each of the variables used in statistical analy-
ses.
contributing factors and their interaction effects. In some cases,
however, the transformed variables still appeared to violate the Variable n (female) n (male) n (combined-sex)
distributional assumptions for MR. Thus, the raw data were fit-
ted with generalized linear models (GLM), in hopes that the data CAS 198 210 408
Acetabular variables 195 210 405
might be better served by the relaxed distributional assumptions 1, 2, 3, 4, 6, and 7
of these models, and in light of the fact that GLM has previ- Acetabular variable 5 195 209 404
ously proved effective in analyzing the simultaneous impacts of TMJ OA 198 210 408
multiple contributing factors to processes of skeletal degenera- Shoulder OA 198 210 408
Elbow OA 198 210 408
tion (70). The R Gamma-family GLM function was utilized (69, Wrist OA 197 210 407
“stats” package), due to the right-skewness of the non-normally Hip OA 198 210 408
distributed data. In both cases (MR and GLM), the full models Knee OA 195 203 398
were then simplified via automated backward-stepwise selection Ankle OA 194 208 402
informed by Akaike’s Information Criterion (AIC) in order to Overall OA 198 210 408
Upper limb OA 198 210 408
achieve the minimal adequate models. Lower limb OA 198 210 408
BMI 187 188 375
MET level 178 192 370
Results (occupational activities)
MET level 71 69 140
Sample sizes for each of the variables tested in the below (habitual-activities)
analyses differed based on availability of demographic data and
WINBURN . VALIDATION OF THE ACETABULUM FOR AGING 7

TABLE 4––Spearman’s rank-order correlations for CAS and OA in the vari- males: a = 0.05/6). For the individual acetabular variables and
ous joints and body regions in females and males. occupational activities, Spearman’s rho values ranged from
0.408 to 0.438, none of which were statistically significant at
Joint/Region rho (Female) rho (Male)
a = 0.001 (Bonferroni correction for females: a = 0.05/35; for
TMJ 0.331* 0.345* males: a = 0.05/42). For CAS and habitual-activities, the highest
Shoulder 0.456* 0.654* r2 value was 0.144, and Spearman’s rho values ranged from
Elbow 0.428* 0.520*
Wrist 0.525* 0.603*
0.395 to 0.409, none of which were statistically significant at
Hip 0.745* 0.772* a = 0.01 (Bonferroni correction for combined-sex sample:
Knee 0.435* 0.564* a = 0.05/5). For the individual acetabular variables and habitual-
Ankle 0.282* 0.498* activities, Spearman’s rho values ranged from 0.565 to 0.443,
Overall 0.664* 0.779* none of which were statistically significant at a = 0.001 (Bonfer-
Upper limb 0.572* 0.703*
Lower limb 0.606* 0.765* roni correction for combined-sex sample: a = 0.05/35).
Further, Wilcoxon rank-sum tests detected no statistically sig-
*Statistically significant at a = 0.007 for joints (Bonferroni correction: nificant differences between CAS and acetabular variable means
a = 0.05/7) and a = 0.02 for body regions (Bonferroni correction: a = 0.05/
3).
from individuals engaging in strenuous physical activities utiliz-
ing the lower limb compared with scores from individuals who
did not engage in these rigorous activities (p > 0.188 for all
groups; a = 0.01; Bonferroni correction: a = 0.05/5). These
individual joints and body regions, in both sexes (Table 4). Rho findings indicate that neither differences in MET values nor vari-
values were particularly high in the hip: The 95% confidence ation in mechanical loading of the lower limb contribute signifi-
intervals for female and male hip OA did not contain the rho cantly to acetabular degeneration.
values of any other joints (see Table 4). Regression of CAS on
overall OA, upper limb OA, and lower limb OA revealed statis- Hypothesis 4
tically significant positive associations between these composite
acetabular and OA scores in both females and males (Fig. 4). Hypothesis 4 was rejected: No statistically significant correla-
Thus, OA seems to be linked with the acetabular aging processes tions were detected between acetabular changes (CAS, acetabular
captured by CAS. variables) and BMI for females or males of any age group. For
Many statistically significant positive correlations were also CAS and BMI, the highest r2 value was 0.159, and Spearman’s
present between the individual acetabular variables and OA in rho values ranged from 0.384 to 0.300, none of which were
the individual joints (Tables 5 and 6); and in the three body statistically significant at a = 0.01 for females and a = 0.008 for
regions, all positive correlations with the variables were statisti- males (Bonferroni correction for females: a = 0.05/5; for males:
cally significant (Table 7). This underscores the link between a = 0.05/6). For the individual acetabular variables and BMI,
acetabular aging processes and OA. Further, the fact that both Spearman’s rho values ranged from 0.172 to 0.410, none of
female and male hip OA exhibited statistically significant posi- which were statistically significant at a = 0.001 (Bonferroni cor-
tive correlations with all acetabular variables (see Table 5) rection: a = 0.05/42). These findings indicate that obesity does
argues for similarities between the acetabular variables and the not contribute significantly to acetabular degeneration.
processes of hip OA. If the variables being scored in the acetab-
ulum per Rissech et al. (2) were metamorphic, this correlation Hypothesis 5
with OA would not be expected.
Hypothesis 5 was supported: After the process of model sim-
plification based on AIC values, age remained in every minimal
Hypothesis 2
adequate model in both of these multivariate approaches (MR,
Hypothesis 2 was supported: Testing revealed statistically sig- GLM). When the data were examined graphically via pairwise
nificant positive correlations between CAS and age in both comparisons of variables, scatterplots showed strong linear rela-
females (q = 0.565; p < 0.001) and males (q = 0.713; tionships between CAS and age. Visualizing the MR models as
p < 0.001), indicating the applicability of acetabular age estima- trees also indicated that age was the most important explanatory
tion to both sexes (Fig. 5). Statistically significant positive corre- variable in every model. In contrast, the other variables appeared
lations were also noted between age and each of the seven to be contributing little more than noise. These results lend sup-
individual acetabular variables in the combined-sex sample, with port for the use of the acetabulum in age estimation.
rho values of 0.405, 0.414, 0.507, 0.484, 0.434, 0.343, and In the female sample, a linear model was created with age,
0.435, respectively (a = 0.007; Bonferroni correction: a = 0.05/ log-transformed habitual-activities, and log-transformed BMI as
7). the explanatory variables and CAS as the response variable
(p = 0.008; r2 = 0.18). In the simplified model, age was the
only remaining term, and it was statistically significant
Hypothesis 3
(p < 0.001; r2 = 0.23). A similar model was created with the
Hypothesis 3 was rejected: No statistically significant correla- larger sample size available for testing the effects of age, log-
tions were detected between acetabular changes (CAS, acetabular transformed occupational activities, and log-transformed BMI on
variables) and MET values for occupational or habitual physical female CAS (p < 0.001; r2=0.32). Again, in the simplified
activities in females or males of any age group. For CAS and model, age was the only remaining term, and it was statistically
occupational activities, the highest r2 value was 0.070, and significant (p < 0.001; r2 = 0.33).
Spearman’s rho values ranged from 0.179 to 0.170, none of In the male sample, a linear model was created with age, log-
which were significant at a = 0.01 for females and a = 0.008 transformed habitual-activities, and log-transformed BMI as the
for males (Bonferroni correction for females: a = 0.05/5; for explanatory variables and CAS as the response variable
8 JOURNAL OF FORENSIC SCIENCES

Females Males
10

10
r 2 =0.329* r 2 =0.478*

9
9

8
8

7
CAS

CAS
7

6
6

5
5

4
4

3
0.0 0.5 1.0 1.5 0.0 0.5 1.0 1.5
Upper Limb OA

10
10

r 2 =0.39* r 2 =0.595*

9
9

8
8

7
CAS
CAS
7

6
6

5
5

4
4

0.0 0.5 1.0 1.5 0.0 0.5 1.0 1.5

Lower Limb OA
10

10

r 2 =0.449* r 2 =0.619*
9
9

8
8

7
CAS

CAS
7

6
6

5
5

4
4

0.0 0.5 1.0 1.5 0.0 0.5 1.0 1.5


Overall OA
FIG. 4––Linear regression revealed statistically significant correlations between acetabular changes (CAS) and OA in females and males, suggesting similari-
ties between these degenerative processes (*p < 0.001).

(p < 0.001; r2 = 0.57). In the simplified model, age and BMI and CAS as the response variable. In the simplified female
remained in the model, and both were statistically significant habitual-activity GLM, age, activity, and the age-activity interac-
(age p < 0.001; BMI p = 0.004; model p < 0.001; r2 = 0.59). A tion remained, but only age was statistically significant
similar model was created with the larger sample size available (p < 0.001; null deviance: 2.23 on 68 degrees of freedom [df];
for testing the effects of age, log-transformed occupational activ- residual deviance: 1.67 on 65 df). In the simplified female occu-
ities, and log-transformed BMI on male CAS (p < 0.001; pational-activity GLM, age was the only remaining term, and it
r2 = 0.41). In the simplified model, age and BMI again was statistically significant (p < 0.001; null deviance: 6.56 on
remained in the model, and both were statistically significant 170 df; residual deviance: 4.53 on 169 df). In the simplified
(age p < 0.001; BMI p = 0.03; model p < 0.001; r2 = 0.42). male habitual-activity model, age and BMI remained in the
The nontransformed data were then fitted to Gamma-family model, and both were statistically significant (p < 0.001; null
GLMs, with age, activities, and BMI as the explanatory variables deviance: 3.44 on 65 df; residual deviance: 1.44 on 63 df). In
WINBURN . VALIDATION OF THE ACETABULUM FOR AGING 9

TABLE 5––Spearman’s rank-order correlations for acetabular variables 1 through 7 and OA in the various joints in females and males.

Summary OA rho (1) rho (2) rho (3) rho (4) rho (5) rho (6) rho (7)
Female TMJ 0.309* 0.089 0.331* 0.206 0.188 0.169 0.229
Female hip 0.515* 0.553* 0.510* 0.472* 0.499* 0.417* 0.371*
Female knee 0.265* 0.302* 0.227 0.326* 0.300* 0.310* 0.241
Female ankle 0.254* 0.245 0.170 0.192 0.209 0.173 0.112
Male TMJ 0.281* 0.215 0.252* 0.234 0.198 0.194 0.158
Male hip 0.537* 0.629* 0.576* 0.645* 0.673* 0.330* 0.363*
Male knee 0.380* 0.445* 0.432* 0.485* 0.414* 0.249* 0.300*
Male ankle 0.357* 0.319* 0.221 0.394* 0.478* 0.328* 0.176
*Statistically significant at a = 0.0007 (Bonferroni correction: a = 0.05/70). Note that separate female and male samples were only used to test joints with
sex differences in OA distributions.

TABLE 6––Spearman’s rank-order correlations for acetabular variables 1 through 7 and OA in the various joints in the combined-sex sample.

Summary OA rho (1) rho (2) rho (3) rho (4) rho (5) rho (6) rho (7)
Shoulder 0.426* 0.372* 0.422* 0.424* 0.368* 0.323* 0.329*
Elbow 0.371* 0.329* 0.346* 0.286* 0.306* 0.300* 0.268*
Wrist 0.424* 0.353* 0.371* 0.381* 0.397* 0.318* 0.265*
*Statistically significant at a = 0.0007 (Bonferroni correction: a = 0.05/70). Note that the combined-sex sample was only used to test joints with no
detected sex differences in OA distributions.

TABLE 7––Spearman’s rank-order correlations for acetabular variables 1 through 7 and summary OA in the combined-sex sample.

Summary OA rho (1) rho (2) rho (3) rho (4) rho (5) rho (6) rho (7)
Overall 0.532* 0.483* 0.495* 0.533* 0.521* 0.401* 0.367*
Upper limb 0.481* 0.417* 0.445* 0.442* 0.430* 0.377* 0.344*
Lower limb 0.469* 0.520* 0.438* 0.531* 0.538* 0.384* 0.331*
*Statistically significant at a = 0.002 (Bonferroni correction: a = 0.05/21).

the simplified male occupational-activity model, age and BMI elbow, and wrist OA had statistically significant positive correla-
again remained in the model, and both were statistically signifi- tions with all acetabular variables. This indicates a systemic com-
cant (age p < 0.001; BMI p = 0.01; null deviance: 6.69 on 178 ponent to both processes—OA and acetabular changes—rather
df; residual deviance: 3.98 on 176 df). than a purely biomechanical etiology. Preliminary research on the
same European-American subset of the UT Bass Collection has
revealed statistically significant OA-age correlations in nearly
Discussion every joint analyzed, with the exception of the ankle (42). Degen-
erative processes of the shoulder and hip emerge from this and
Correlation of Acetabular Changes with OA
other research as particularly strongly correlated with age (42,71),
The statistically significant positive correlations observed possibly due to their proximal and relatively anatomically
between acetabular changes and OA indicate that the changes protected positions within the upper and lower limb (72). That
occurring in the acetabulum are degenerative rather than meta- acetabular changes did not correlate with physical activity or obe-
morphic. There may be a functional component to this correla- sity in the current study (see below) lends further support to the
tion with degenerative joint disease. Higher rho values were possibility that hip degeneration may be relatively resistant to
always seen between the individual acetabular variables and biomechanical effects and influenced largely by systemic effects
overall and lower limb OA (compared with upper limb OA); in (i.e., age).
many cases, differences were marked enough that the 95% confi-
dence intervals for the overall and lower limb rho values did not
Correlation of Acetabular Changes with Age
contain the upper limb rho value. In linear regression analyses
of CAS, r2 values were also higher for lower limb OA than The statistically significant positive correlations observed
upper limb OA in both females and males, as would be expected between acetabular changes and age indicate that, in spite of
if the regular stresses of bipedal locomotion were causing both their degenerative nature, acetabular changes are useful for age
acetabular age change and lower limb OA. estimation. The positive age correlations observed in both
However, there may also be a systemic component to the posi- females and males are consistent with recent research demon-
tive relationship between the acetabular variables and OA. While strating the pattern of acetabular aging to be similar in both
female and male hip OA correlated significantly with all acetabu- sexes (3,34), despite the fact that the original acetabular aging
lar variables, female and male knee and ankle OA did not. In the method was developed and tested on all-male samples (2,30).
ankle, and especially in females, associations with acetabular vari- The current results are consistent with previous research by
ables were particularly weak. In contrast, combined-sex shoulder, San-Millan et al. (3) indicating the strong age correlation of the
10 JOURNAL OF FORENSIC SCIENCES

(19) if the variable descriptions had been more clearly elucidated


r 2 = 0.338*
in the original method (2). To this end, recent research has
90

emended the existing descriptions of the acetabular variables (3),


80

modifying Variables 5 through 7 for clarity and repeatability.


Future method tests should determine whether these changes
70

have improved the method sufficiently to reduce issues of intra-


Age

and inter-observer error.


60

The lack of age correlation reported by previous authors for


50

acetabular fossa variables could also reflect biological differ-


ences in the aging processes taking place in the region of the
40

acetabular fossa, compared with the more strongly age-correlated


30

acetabular rim. Previous research has indicated that marginal


joint changes (e.g., osteophyte formation) are more strongly cor-
4 5 6 7 8 9 10 related with age than changes to the joint’s articular surfaces
(73). One recent study found that osteophytes of the acetabulum
CAS (Females)
and scapular glenoid exhibit stronger age correlations than osteo-
phytes in other locations (71). Reevaluations of acetabular age-
100

r 2 = 0.52* estimation methods consistently conclude that acetabular rim and


apex variables correlate with age (1,8,19). A recent geometric
morphometric shape analysis of age-related changes to the
80

acetabulum revealed that bone production along the borders of


the lunate surface (i.e., the acetabular rim, apex, and outer edge
Age

of the acetabular fossa) is associated with age in both females


60

and males (34). In the current study, the two acetabular variables
with the highest rho-value correlations with age were Variables
40

3 and 4, and sometimes these differences in age correlation were


marked (e.g., the 95% confidence interval for Variable 3 did not
include the rho values for Variables 1, 2, and 6; the 95% confi-
20

dence interval for Variable 4 did not include the rho values for
3 4 5 6 7 8 9 10
Variables 1 and 6). Variables 3 and 4 describe porosity of the
acetabular rim and osteophyte formation of the apex, respec-
CAS (Males) tively. Both of these strongly age-correlated variables describe
marginal joint changes.
FIG. 5––Linear regression revealed statistically significant correlations
Interestingly, some of the Rissech (2) acetabular rim and
between acetabular changes (CAS) and age in females and males
(*p < 0.001). apex variables (Variables 1, 2, and 4) have also proved resis-
tant to the effects of previous traumatic hip injuries and surgi-
cal interventions, while the variables of the acetabular fossa
seven acetabular variables (2). Other research, however, has indi- (Variables 5 through 7) have showed statistically significant
cated that variables of the acetabular fossa are less strongly cor- trauma effects (42). Since acetabular aging methods should not
related with age than variables of the acetabular rim (1,19). This be applied to hip joints showing evidence of skeletal trauma,
discrepancy could reflect population differences among the sam- surgery, or pathological conditions (2), these limited trauma
ples analyzed by Calce (1; males from the early 20th-century effects can easily be avoided during normal forensic anthropo-
Grant Collection, Toronto, Canada), Mays (19; females and logical practice (i.e., by substituting right for left acetabula or
males from the 18th- to 19th-century Spitalfields Collection, simply utilizing different age indicators). Still, the resistance of
London, U.K.), San-Millan et al. (3; females and males from the Variables 1, 2, and 4 to traumatic injuries and/or surgical inter-
19th- and 20th-century Lisbon Collection, Portugal), and in the ventions argues in favor of these OA-related rim and apex vari-
current research (females and males from the modern Bass Col- ables, and the trauma effects exhibited by Variables 5 through
lection, UT, U.S.A.). 7 argue against the use of these problematic fossa variables
However, discrepancies in the pattern of age correlations of (42). Future acetabular method revisions could focus only on
the acetabular variables could also reflect difficulties of applying the variables of the acetabular rim and apex—or better eluci-
the original acetabular aging method (2), possibly representing date the processes occurring in the poorly understood acetabu-
an artifact of inter-observer error. For example, Mays (19) lar fossa.
reported modifying the method protocol when scoring Variables
6 and 7; it is thus unsurprising that the modified scores do not
Lack of Correlation Between Acetabular Changes and Habitual/
correlate as strongly with age as the original authors reported
Occupational Activities
(2). Other authors have critiqued previously published descrip-
tions of acetabular variables, stating that difficulties in interpret- This study’s results suggest that acetabular changes are resis-
ing the descriptions lead to observer subjectivity (8,40). During tant to physical activity effects, lending support to the use of
the current study, scoring difficulties were noted for the variables acetabular changes for age estimation. The lack of correlation
of the acetabular fossa (Variables 5–7), which assess subtle and between activity and acetabular degeneration accords with cur-
often-ambiguous skeletal traits like bone texture and porosity (2; rent medical and anthropological research, which contradicts the
Table 2). It is possible that fossa variables would have correlated “intuitive” idea that more frequently used joints will age prema-
more strongly with age in the research of Calce (1) and Mays turely and indicates instead the benefit of moderate physical
WINBURN . VALIDATION OF THE ACETABULUM FOR AGING 11

activity (and the detriment of physical inactivity) for joint health Revising the Metamorphic-Degenerative Dichotomy
(54,74–77). Rather than supporting the idea that the daily wear
The current research project has indicated that acetabular
and tear of bipedal locomotion causes premature acetabular
changes constitute skeletal degeneration. However, it also indi-
aging, acetabular variables appeared resistant to mechanical load-
cates that acetabular degeneration has a significant, positive cor-
ing. However, these activity findings must be considered tenta-
relation with age. One of the study’s assumptions was that the
tive, due to the difficulties of assessing the metabolic and
utility of degenerative changes for age estimation would be pre-
biomechanical impacts of occupational and habitual physical
cluded by the multiple other influences on the progression of
activities in a skeletal sample of donated remains (see Discussion
skeletal degeneration. Yet, acetabular degeneration also proved
of study limitations, below).
relatively resistant to the effects of physical activity and obesity
—and, in the same skeletal sample, even overall measures of
Lack of Correlation Between Acetabular Changes and Obesity OA correlated strongly with age (42). This suggests that the
dichotomy between metamorphic and degenerative change (and
This study’s results suggest that acetabular changes are resis-
their probative vs. nonprobative value for age estimation) is a
tant to obesity effects, supporting their use in age estimation.
false one. If both metamorphic and degenerative changes are
These findings are particularly relevant in a forensic setting,
strongly positively correlated with age, the former should not be
considering the prevalence of obesity in modern populations
given preference over the latter in age-estimation studies. After
(78). The findings are also interesting in light of the fact that
all, while some regions of metamorphic change enable reliable
previous research has determined the iliac auricular surface to
age predictions (at least in younger individuals—e.g., the ventral
be affected by obesity—yielding less accurate and more biased
rampart of the pubic symphysis), others have been discounted as
age estimates for obese adults compared with normal-weight
age-relevant for decades (e.g., the cranial sutures [39]). One
adults (53). While the pubic symphysis has been found to be
might speculate that it is the anabolic nature of the formation of
more resistant to obesity effects than the auricular surface (53),
the pubic symphysis ventral rampart that makes this feature more
the acetabulum has been determined to be one of the least
relevant to aging. Yet, there is an anabolic component to “de-
biased and most reliable skeletal age indicators for obese indi-
generative” OA as well: abnormal subchondral bone production,
viduals (79). The results of the present study support this con-
sclerosis, and the formation of marginal osteophytes are integral
clusion, indicating that the acetabulum is resistant to the
facets of the disease in addition to the destructive processes of
increasingly prevalent condition of obesity. However, the cur-
cartilage degradation and bone erosion.
rent results must be compared with these previous findings
Further, the ventral rampart is not the only component of the
(53,79) with caution, as the effects of obesity on the acetabular
pubic symphysis that enables reliable age estimation (4,14).
age estimates themselves were not tested in the current study.
Most pubic symphyseal aging methods also assess degenerative
These results also merit a caveat in light of the fact that multi-
changes (e.g., 5,14)—including both anabolic traits (i.e., osteo-
variate modeling reveals that BMI contributes to variance in
phytes) and catabolic traits (i.e., porosity [80]). Degenerative and
CAS—albeit in males only (see below).
metamorphic processes may also feedback into one another. As
demonstrated in a recent study by Calce et al. (80), OA severity
Age as the Major Contributor to Acetabular Changes has an impact on the age estimates generated by the various pel-
vic joints. Biomechanical differences in the various joints must
Age remained in every minimal adequate MR model and
also be considered in assessing differing patterns of age-related
GLM investigating the contribution of the various factors to
change (42,81). Dichotomous thinking simply may not be an
CAS. Age was a statistically significant term in every minimal
appropriate approach to these related, overlapping, and difficult-
adequate model for both sexes, using both approaches. For
to-distinguish processes of skeletal change. Certainly, there
males, BMI also remained as a statistically significant term in
seems no legitimate basis on which to tout “metamorphic”
all simplified models. The consistency of the results from MR
changes as “good” and dismiss “degenerative” changes as “bad.”
and GLM indicates that the potential violation of distributional
The very assumption that bone production represents a benefi-
assumptions is not impacting the performance of tests—per-
cial process and bone destruction a maladaptive process must be
haps due to the significance of the impact of age on CAS. In
questioned. If bone is building a structure (e.g., a ventral rampart
MR models, age alone explained approximately one-quarter-to-
or osteophyte) where one is not functionally necessary, it could
one-third of the variance in CAS observed in females, and,
be argued that this process is maladaptive regardless of whether
along with BMI, age explained approximately half of the vari-
the formation is classified as metamorphic or degenerative. The
ance in CAS observed in males. It must be noted, however,
fact remains that metamorphic change is a normal part of human
that over two-thirds of the variance in female CAS was not
skeletal aging, while OA is a pathological condition for which
explained by the female age-only MR models, and approxi-
age is a major predisposing factor (82,83). However, if this
mately half of male CAS variance was not explained by the
pathological process is as strongly age correlated as this study
male combined (age-BMI) models. Additional contributing fac-
suggests, then it too should be considered in skeletal estimates
tors undoubtedly influence acetabular changes—they simply
of age.
were not measured in the current study. Future research could
Indeed, it seems imprudent to dismiss degenerative processes
examine the influences of such factors as heredity and (partic-
like OA as “ancillary (if not a last resort)” to other skeletal
ularly in the case of females) hormones on variance in CAS.
indicators of age (43, p. 59). For the purposes of age estima-
Still, these results support the above conclusions that, of the
tion, this dichotomous distinction may be meaningless. Both
three factors investigated herein, age is always a consistent
metamorphic and degenerative skeletal changes are age corre-
and significant contributor to acetabular changes. This is in
lated, and both should be incorporated into skeletal age-estima-
accordance with other recent research on pelvic degeneration
tion methods (14,71,80,84,85). A potential venue for this
(74) and lends support for the use of the acetabulum in age
incorporation might be the multifactorial Bayesian age-
estimation.
12 JOURNAL OF FORENSIC SCIENCES

estimation methods that are currently gaining support among (e.g., underwater body density studies) are often time-consuming
forensic anthropologists (33,86–89). and expensive (95). Calculating BMI remains a conveniently
simple approximation for adiposity (98), and while imperfect, its
lower and upper limits likely do capture extremes of adiposity
Study Limitations and Future Avenues for Research
(i.e., underweight, BMI <18.5; obese, BMI ≥30). More accurate
This research employed an ordinal scoring system to analyze methods of measuring adiposity are impractical when dealing
skeletal evidence of OA. While such systems are widely used in with deceased individuals and impossible when analyzing skele-
biological anthropology, they oversimplify the complexity of tal remains. Further, the lack of ancestral diversity in the devel-
anabolic and catabolic processes that comprise the OA disease opment and testing of BMI equations is not a factor in the
process—which is nonlinear in its progression, differing from current study. Percent body fat is strongly correlated with BMI
joint to joint and involving both degenerative and reparative pro- in European-American populations (99), and this sample is com-
cesses (80,90,91). Further, the sensitivity of ordinal scores to prised exclusively of European-American individuals. Thus,
identifying clinical markers of OA remains unknown, as does BMI is an indirect indicator of adiposity valid for use this study.
the correspondence of those scores with actual OA symptoms in It should also be stated that the steps taken in the current
living patients. In absence of the articulated-joint radiographs study to control for the effects of age in analyses of activity and
and patient-reported pain experiences used in clinical diagnoses obesity (restricting testing to within age-matched subsamples)
of OA (63,92), anthropologists rely on the presence of macro- reduce the statistical power of those analyses. This increases the
scopically observable osteophytes, eburnation, and porosity to chances of achieving results that support the null hypotheses
diagnose OA indirectly in a deceased individual (90). Yet, the of no activity and obesity effects. In turn, this makes the results
correlation of these indicators with OA symptoms is not clear of these analyses less directly comparable with the analyses of
even in the clinical setting, where radiographic evidence of the Hypotheses 1 and 2 (investigating correlations between acetabu-
disease does not always correlate with actual symptoms of dis- lar changes and OA and age), which include larger sample sizes.
ability (82,93). Future analyses should explore the correlation of Future studies could attempt to replicate these results across lar-
skeletal indicators of OA with actual experiences of pain and ger, age-matched samples that are more comparable with this
impairment. study’s overall sample size.
This study’s activity coding system is subject to similar limita- Finally, there are ancestral limitations to the current study.
tions. Simply, it is unclear how well (or poorly) averaged MET Within the overall Bass Collection (which, at the time of data
values from the Compendium of Physical Activities reflect the collection, included over 1500 individuals), approximately 700
actual energetic exertions of the deceased individuals in the Bass individuals included information on height, body mass, and
Collection. The Compendium was designed for use in self- occupational/habitual-activities. Most of these completely docu-
reported activity surveys in which participants quantify their mented individuals were of European-American ancestry.
daily activities in a standardized fashion (66,67). In contrast, the Because this documentation disparity prevented the assemblage
occupational and habitual-activity data tested in the current study of sufficient sample sizes for non-European individuals, all indi-
were nonstandardized—captured by open-ended prompts on viduals in the current sample were of European-American des-
skeletal donor forms. It is also difficult to assess whether aver- cent. This precluded an analysis of the effects of ancestry—a
aged MET values can differentiate among real, in vivo activity factor linked with heredity that almost undoubtedly contributes
differences to a degree that would be meaningful biomechani- both to OA and to acetabular changes (30). As previous acetabu-
cally and in terms of skeletal response. Metabolic equivalency lar age-estimation research has also focused almost entirely on
values reflect energy exertion, not skeletal biomechanics, so the individuals of European ancestry (2,3,8,19,30), the ancestral
use of MET data as a proxy for the actual joint forces to which makeup of this skeletal sample is appropriate to the current capa-
an individual’s joints were regularly subjected may be ques- bilities of the age-estimation methods. Still, the absence of
tioned. For these reasons, this study’s lack of positive correlation ancestry data is a limitation of the current study—one that
between physical activity and acetabular degeneration should be should be remedied in future studies of acetabular aging.
considered tentative. Still, this finding is consistent with recent
medical research on the benefits of physical activity for aging
Conclusions
individuals (54,75,76) and anthropological research indicating a
negative correlation between activity and OA (74). In summary, the degenerative changes of the acetabulum are
This study approximated obesity using BMI—a description of valid skeletal age indicators that are relatively resistant to the
the relationship of an individual’s height to body mass. How- effects of physical activity and obesity in European-Americans.
ever, BMI does not measure an individual’s percent body fat, This study’s results demonstrate the utility of the acetabulum for
differentiate adipose tissue from muscle, bone, or organs, or age estimation and indicate that the metamorphic-degenerative
describe an individual’s abdominal girth (94,95). A muscular dichotomy of skeletal age change is in need of revision. Further,
athlete may have a high BMI but a low percent body fat, for the tentative finding that physical activity has no effect on
example; conversely, an older individual may have a higher per- acetabular degeneration suggests that an activity-led etiology for
cent body fat than a younger individual with the same BMI. joint degeneration is overly simplistic.
Body fat proportions may also differ among individuals of dif- The current research is particularly relevant to forensic anthro-
ferent ancestries (96,97) and biological sexes (94). Thus, critics pological age estimation in an increasingly elderly U.S. popula-
assert that BMI is not sensitive enough to identify the dangerous tion, since acetabular degeneration continues with advancing
levels of adiposity that have been correlated with morbidity and age. By demonstrating the validity of this skeletal age indicator,
mortality in obese individuals (95)—at least in non-European this research paves the way for future method revisions and pop-
populations, for whom relationships between BMI and adiposity ulation validations. Acetabular age changes could prove particu-
have not been sufficiently established (97). However, methods larly relevant to the development of multifactorial aging
that do directly measure or approximate body fat composition methods. This study’s results will enable more effective method
WINBURN . VALIDATION OF THE ACETABULUM FOR AGING 13

revision in the future, informed by a more complete understand- the determination of adult skeletal age at death. Am J Phys Anthropol
ing of the complexity of acetabular changes. 1985;68:15–28.
19. Mays S. An investigation of age-related changes at the acetabulum in
In a STEM-based field where standards matter, it is important 18th-19th century AD adult skeletons from Christ Church Spitalfields.
not only to test and refine age-estimation methods, but also to London. Am J Phys Anthropol 2012;149:485–92.
understand the biology underlying method success or failure. 20. Mays S. A test of a recently devised method of estimating skeletal age
This research constitutes a response to the call for studies estab- at death using features of the adult acetabulum. J Forensic Sci
2014;59:184–7.
lishing the scientific bases on which forensic methods are built
21. McKern TW, Stewart TD. Skeletal age changes in young American
(100,101). The results indicate that the use of the acetabulum for males (Technical Report EP-45). Natick, MA: Quartermaster Research
age estimation indeed has scientific merit. and Development Command, 1957.
22. Miranker M. A comparison of different age estimation methods of the
adult pelvis. J Forensic Sci 2016;61:1173–9.
Acknowledgments 23. Moraitis K, Zorba E, Eliopoulos C, Fox SC. A test of the revised auric-
ular surface aging method on a modern European population. J Forensic
To the faculty and students of the University of Florida Sci 2014;59:188–94.
Department of Anthropology and Institute on Aging—especially 24. Mulhern DM, Jones EB. Test of revised method of age estimation
Dr. David Daegling and Dr. Michala Stock—thank you for your from the auricular surface of the ilium. Am J Phys Anthropol
kind help and support. Many thanks go to the terrific team at the 2005;126:61–5.
25. Murray KA, Murray T. A test of the auricular surface aging technique.
University of Tennessee Forensic Anthropology Center who J Forensic Sci 1991;36:1162–9.
facilitated my access to the Bass Collection. Special thanks are 26. Osborne DL, Simmons TL, Nawrocki SP. Reconsidering the auricular
due to the skeletal donors and their families, without whose gift surface as an indicator of age at death. J Forensic Sci 2004;49:905–11.
this type of research would not be possible. 27. Passalacqua NV. Forensic age-at-death estimation from the human
sacrum. J Forensic Sci 2009;54:255–62.
28. Passalacqua NV. Applications of the human sacrum in age at death esti-
References mation. In: Latham KE, Finnegan M, editors. Age estimation of the
human skeleton. Springfield, IL: Charles C Thomas, 2010;102–17.
1. Calce SE. A new method to estimate adult age-at-death using the 29. Powanda AI. A comparison of pelvic age-estimation methods on two
acetabulum. Am J Phys Anthropol 2012;148:11–23. modern Iberian populations: bioarchaeological and forensic applications
2. Rissech C, Estabrook GF, Cunha E, Malgosa A. Using the acetabulum [thesis]. New York, NY: New York University, 2008.
to estimate age at death of adult males. J Forensic Sci 2006;51:213–29. 30. Rissech C, Estabrook GF, Cunha E, Malgosa A. Estimation of age-at-
3. San-Millan M, Rissech C, Turbon D. New approach to age estimation death for adult males using the acetabulum, applied to four Western
of male and female adult skeletons based on the morphological charac- European populations. J Forensic Sci 2007;52:774–8.
teristics of the acetabulum. Int J Legal Med 2016;131:501–25. 31. Rouge-Maillart C, Jousset N, Viella B, Gaudin A, Telmon N. Contribu-
4. Berg GE. Pubic bone age estimation in adult women. J Forensic Sci tion of the study of the acetabulum for the estimation of adult subjects.
2008;53:569–77. Forensic Sci Int 2007;171:103–10.
5. Brooks S, Suchey JM. Skeletal age determination based on the os 32. Rouge-Maillart C, Telmon N, Rissech C, Malgosa A, Rouge D. The
pubis: a comparison of the Ascadi-Nemeskeri and Suchey-Brooks meth- determination of male adult age at death by central and posterior coxal
ods. J Hum Evol 1990;5:227–38. analysis—a preliminary study. J Forensic Sci 2004;49:208–14.
6. Brown CA. A test of the Passalacqua sacral age estimation method in a 33. Rouge-Maillart C, Vielle B, Jousset N, Chappard D, Telmon N, Cunha
Japanese sample. Proceedings of the 67th Annual Scientific Meeting of E. Development of a method to estimate skeletal age at death in adults
the American Academy of Forensic Sciences; 2015 Feb 16-21; Orlando, using the acetabulum and the auricular surface on a Portuguese popula-
FL. Colorado Springs, CO: American Academy of Forensic Sciences, tion. Forensic Sci Int 2009;188:91–5.
2015. 34. San-Millan M, Rissech C, Turbon D. Shape variability of the adult
7. Buckberry JL, Chamberlain AT. Age estimation from the auricular sur- human acetabulum and acetabular fossa related to sex and age by geo-
face of the ilium: a revised method. Am J Phys Anthropol metric morphometrics. Implications for adult age estimation. Forensic
2002;119:231–9. Sci Int 2017;272:50–63.
8. Calce SE, Rogers TL. Evaluation of age estimation technique: testing 35. Sashin D. A critical analysis of the anatomy and pathological changes
traits of the acetabulum. J Forensic Sci 2011;56:302–11. of the sacro-iliac joints. J Bone Joint Surg 1930;12:891–910.
9. Cleland J. On certain distinctions of form hitherto unnoticed in the 36. Schmitt A. Age-at-death assessment using the os pubis and the auricular
human pelvis, characteristic of sex, age, and race. Mem Memor Anat surface of the ilium: a test on an identified Asian sample. Int J Osteoar-
1889;1:95–103. chaeol 2004;14:1–6.
10. Djuric M, Djonic D, Nikolic S, Popovic D, Marinkovic J. Evaluation of 37. Sinha A, Gupta V. A study on estimation of age from pubic symphysis.
the Suchey-Brooks method for aging skeletons in the Balkans. J Foren- Forensic Sci Int 1995;75:73–8.
sic Sci 2007;52:21–3. 38. Snodgrass JJ. Sex differences and aging of the vertebral column. J
11. Falys CG, Schutkowski H, Weston DA. Auricular surface aging: worse Forensic Sci 2004;49:458–63.
than expected? A test of the revised method on a documented historic 39. Stewart TD.Essentials of forensic anthropology. Springfield, IL: Charles
skeletal assemblage. Am J Phys Anthropol 2006;130:508–13. C Thomas, 1979.
12. Gilbert BM, McKern TW. A method for aging the female os pubis. Am 40. Stull KA, James DM. Determination of age-at-death using the acetabu-
J Phys Anthropol 1973;38:31–8. lum. In: Latham KE, Finnegan M, editors. Age estimation of the human
13. Hanihara K, Suzuki T. Estimation of age from the pubic symphysis by skeleton. Springfield, IL: Charles C Thomas, 2010;134–46.
means of multiple regression analysis. Am J Phys Anthropol 41. Todd TW. Age changes in the pubic bone. Am J Phys Anthropol
1978;48:233–40. 1920;3:285–337.
14. Hartnett KM. Analysis of age-at-death estimation using data from a 42. Winburn AP. Skeletal age estimation in modern European-American
new, modern autopsy sample—Part I: pubic bone. J Forensic Sci adults: the effects of activity, obesity, and osteoarthritis on age-related
2010;55:1145–51. changes in the acetabulum [dissertation]. Gainesville, FL: University of
15. Igarashi Y, Uesu K, Wakebe T, Kanazawa E. New method for estima- Florida, 2017.
tion of adult skeletal age at death from the morphology of the auricular 43. Aykroyd RG, Lucy D, Pollard AM, Roberts CA. Nasty, brutish, but not
surface of the ilium. Am J Phys Anthropol 2005;128:324–39. necessarily short: a reconsideration of the statistical methods used to
16. Katz D, Suchey JM. Race differences in pubic symphyseal aging pat- calculate age at death from adult human skeletal and dental age indica-
terns in the male. Am J Phys Anthropol 1989;80:167–72. tors. Am Antiq 1999;64:55–70.
17. Listi GA, Manhein MH. The use of vertebral osteoarthritis and osteo- 44. Meindl RS, Russell KF. Recent advances in method and theory in pale-
phytosis in age estimation. J Forensic Sci 2012;57:1537–40. odemography. Annu Rev Anthropol 1998;27:375–99.
18. Lovejoy CO, Meindl RS, Pryzbeck TF, Mensforth RP. Chronological 45. Nawrocki SP. The nature and sources of error in the estimation of age
metamorphosis of the auricular surface of the ilium: a new method for at death from the skeleton. In: Latham KE, Finnegan M, editors. Age
14 JOURNAL OF FORENSIC SCIENCES

estimation of the human skeleton. Springfield, IL: Charles C Thomas, 74. Calce SE, Kurki HK, Weston DA, Gould L. The relationship of age,
2010;79–101. activity, and body size on osteoarthritis in weight-bearing skeletal
46. Latham KE, Finnegan M, editors. Age estimation of the human skele- regions. Int J Paleopathol 2018;22:45–53.
ton. Springfield, IL: Charles C Thomas, 2010. 75. Tak E, Staats P, Van Hespern A, Hopman-Rock M. The effects of an
47. Milner GR, Boldsen JL. Transition analysis: a validation study with exercise program for older adults with osteoarthritis of the hip. J
known-age modern American skeletons. Am J Phys Anthropol Rheumatol 2005;32:1106–13.
2012;148:98–110. 76. Urquhart DM, Tobing JFL, Hanna FS, Berry P, Wluka AE, Ding C,
48. Buikstra JE, Ubelaker DH, editors. Standards for data collection from et al. What is the effect of physical activity on the knee joint? A sys-
human skeletal remains. Fayetteville, AK: Arkansas Archeological Sur- tematic review. Med Sci Sports Exerc 2011;43:432–42.
vey Research Series (No. 44), 1994. 77. Wallace IJ, Worthington S, Felson DT, Jurmain RD, Wren KT, Maija-
49. Komar DA, Buikstra JE. Forensic anthropology: contemporary theory nen H, et al. Knee osteoarthritis has doubled in prevalence since the
and practice. New York, NY: Oxford University Press, 2008. mid-20th century. Proc Natl Acad Sci USA 2017;114:9332–6.
50. Vaupel JW. The biodemography of aging. Pop Dev Rev 2004;30:48– 78. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood
62. and adult obesity in the United States, 2011-2012. JAMA
51. Center NationalCrimeInformation. Missing persons dataset. Washington, 2014;311:806–14.
DC: Federal Bureau of Investigation, 2014. 79. Merritt CE. Inaccuracy and bias in adult skeletal age estimation: assess-
52. Haglund WD, Reay DT, Swindler DR. Canid scavenging/disarticulation ing the reliability of eight methods on individuals of varying body sizes.
sequence of human remains in the Pacific Northwest. J Forensic Sci Forensic Sci Int 2017;275(315):e1–11.
1989;34:587–606. 80. Calce SE, Kurki HK, Weston DA, Gould L. Effects of osteoarthritis on
53. Wescott DJ, Drew JL. Effect of obesity on the reliability of age-at-death age-at-death estimates from the human pelvis. Am J Phys Anthropol
indicators of the pelvis. Am J Phys Anthropol 2015;156:595–605. 2018;167:3–19.
54. Hunter DJ, Eckstein F. Exercise and osteoarthritis. J Anat 81. Brennaman AL. Examination of osteoarthritis for age-at-death estima-
2009;214:197–207. tion in a modern population [thesis]. Boston, MA: Boston University,
55. Felson DT, Zhang Y. An update on the epidemiology of knee and hip 2014.
osteoarthritis with a view to prevention. Arthritis Rheum 1998;41:1343– 82. Loeser RF. Aging cartilage and osteoarthritis cartilage: differences and
55. shared mechanisms. In: Sharma L, Berenbaum F, editors. Osteoarthritis:
56. Kennedy KAR. Skeletal markers of occupational stress. In: Is _ßcan MY, a companion to rheumatology. Philadelphia, PA: Mosby, Inc. (Elsevier),
Kennedy KAR, editors. Reconstruction of life from the skeleton. New 2007;77–84.
York, NY: Alan R. Liss Inc., 1989;129–60. 83. Wollheim FA, Lohmander LS. Pathology and animal models of
57. Larsen CS. Bioarchaeology: interpreting behavior from the human osteoarthritis. In: Sharma L, Berenbaum F, editors. Osteoarthritis: a
skeleton. Cambridge, U.K.: Cambridge University Press, 1997. companion to rheumatology. Philadelphia, PA: Mosby, Inc. (Elsevier),
58. Coggon D, Reading I, Croft P, McLaren M, Barrett D, Cooper C. Knee 2007;104–112.
osteoarthritis and obesity. Int J Obes 2001;25:622–7. 84. Brennaman AL, Love KR, Bethard JD, Pokines JT. A Bayesian
59. Couchman J. Past, present and future insights into the understanding approach to age-at-death estimation from osteoarthritis of the shoulder
and treatment of osteoarthritis: molecular and mechanical approaches. in modern North Americans. J Forensic Sci 2017;62:573–84.
Int J Exp Pathol 2009;90:A30–84. 85. Falys CG, Prangle D. Estimating age of mature adults from the degen-
60. Felson DT, Anderson JJ, Naimark A, Walker AM, Swift M, Meenan eration of the sternal end of the clavicle. Am J Phys Anthropol
RF. Obesity and knee osteoarthritis: the Framingham Study. Ann Intern 2015;156:203–14.
Med 1988;109:18–24. 86. Boldsen JL, Milner GR, Konigsberg LW, Wood JW. Transition anal-
61. Felson DT, Lawrence RC, Dieppe PA, Hirsch R, Helmick CG, Jordan ysis: a new method for estimating age from skeletons. In: Hoppa
JM, et al. Osteoarthritis: new insights. Part 1: the disease and its risk RD, Vaupel JW, editors. Paleodemography: age distributions from
factors. Ann Intern Med 2000;133:635–46. skeletal samples. Cambridge, U.K.: Cambridge University Press,
62. Fransen M, Bridgett L, March L, Hoy D, Penserga E, Brooks P. The 2002;73–106.
epidemiology of osteoarthritis in Asia. Int J Rheum Dis 2011;14:113– 87. Bullock M, Marquez L, Hernandez P, Ruız F. Paleodemographic age-
21. at-death distributions of two Mexican skeletal collections: a comparison
63. Mandl LA. Epidemiology of osteoarthritis. In: Sharma L, Berenbaum F, of transition analysis and traditional aging methods. Am J Phys Anthro-
editors. Osteoarthritis: a companion to rheumatology. Philadelphia, PA: pol 2013;152:67–78.
Mosby, Inc. (Elsevier), 2007;1–14. 88. Cappella A, Cummaudo M, Arrigoni E, Gibelli DM, Porta D, Cattaneo
64. Jurmain RD. Paleoepidemiology of a Central California prehistoric pop- C. The issue of age estimation in a modern skeletal population: are cur-
ulation from CA-ALA-329: II. Degenerative disease. Am J Phys rent aging methods satisfactory for the elderly? Proceedings of the 67th
Anthropol 1990;83:83–94. Annual Scientific Meeting of the American Academy of Forensic
65. Weiss E. Osteoarthritis and body mass. J Archaeol Sci 2006;33:690–5. Sciences; 2015 Feb 16-21; Orlando, FL. Colorado Springs, CO: Ameri-
66. Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett DR Jr, can Academy of Forensic Sciences, 2015.
Tudor-Locke C, et al. 2011 Compendium of Physical Activities: a sec- 89. Langley-Shirley N, Jantz RL. A Bayesian approach to age estimation in
ond update of codes and MET values. Med Sci Sports Exerc modern Americans from the clavicle. J Forensic Sci 2010;55:571–83.
2011;43:1575–81. 90. Calce SE, Kurki HK, Weston DA, Gould L. Principal component analy-
67. Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath sis in the evaluation of osteoarthritis. Am J Phys Anthropol
SJ, et al. Compendium of Physical Activities: an update of activity 2017;162:476–90.
codes and MET intensities. Med Sci Sports Exerc 2000;32(S1):S498– 91. Dieppe P. Developments in osteoarthritis. Rheumatology 2011;50:245–
516. 7.
68. Tudor-Locke C, Washington TL, Ainsworth BE, Troiano RP. Linking 92. Kellgren JH, Lawrence JS. Radiological assessment of osteoarthritis.
the American Time Use Survey (ATUS) and the Compendium of Physi- Ann Rheum Dis 1957;16:494–502.
cal Activities: methods and rationale. J Phys Act Health 2009;6:347–53. 93. Rothschild BM. Porosity: a curiosity without diagnostic significance.
69. R Core Team. R: A language and environment for statistical computing Am J Phys Anthropol 1997;104:529–33.
(Version 3.2.2, “Fire Safety”), 2015; http://www.R-project.org/ (ac- 94. Smalley KJ, Knerr AN, Kendrick ZV, Colliver JA, Owen OE.
cessed November 13, 2018). Reassessment of body mass indices. Am J Clin Nutr 1990;52:405–8.
70. Nikita E, Mattingly D, Lahr MM. Methodological considerations in the 95. Wellens RI, Roche AF, Khamis HJ, Jackson AS, Pollock ML, Siervogel
statistical analysis of degenerative joint and disc disease. Int J Paleopath RM. Relationships between the body mass index and body composition.
2013;3:105–12. Obes Res 1996;4:35–44.
71. Alves-Cardoso F, Assis S. Can osteophytes be used as age at death esti- 96. Rush EC, Freitas I, Plank LD. New standards of weight and body com-
mators? Testing correlations in skeletonized human remains with known position by frame size and height for assessment of nutritional status of
age-at-death. Forensic Sci Int 2018;288:59–66. adults and the elderly. Br J Nutr 2009;102:632–41.
72. Jurmain RD. Stress and the etiology of osteoarthritis. Am J Phys 97. Wang J, Thornton JC, Russell M, Burastero S, Heymsfield S, Pierson
Anthropol 1977;46:353–66. RN. Asians have lower body mass index (BMI) but higher percent body
73. Weiss E, Jurmain R. Osteoarthritis revisited: a contemporary review of fat than do whites: comparisons of anthropometric measurements. Am J
aetiology. Int J Osteoarchaeol 2007;17:437–50. Clin Nutr 1994;60:23–8.
WINBURN . VALIDATION OF THE ACETABULUM FOR AGING 15

98. Keys A, Fidanza F, Karvonen MJ, Kimura N, Taylor HL. Indices of 101. National Research Council Committee on Identifying the Needs of the
relative weight and obesity. J Chronic Dis 1972;25:329–43. Forensic Sciences Community. Strengthening forensic science in the
99. Flegal KM, Carroll MD, Ogden CL, Curtin LR. Prevalence and trends United States: a path forward (Document No. 228091). Washington,
in obesity among US adults, 1999-2008. JAMA 2010;303:235–41. DC: The National Academies Press, 2009.
100. Daubert V. Merrell Dow Pharmaceuticals, Inc., 509 U.S. 579 (1993).

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