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A Test of The Effectiveness of The Coimbra Method in Capturing Activity-Induced Entheseal Changes PDF
A Test of The Effectiveness of The Coimbra Method in Capturing Activity-Induced Entheseal Changes PDF
ABSTRACT The current paper tests the effectiveness of entheseal changes in expressing activity patterns when the
former have been recorded using the new Coimbra method. Changes on the subscapularis and biceps
brachii were recorded using the Coimbra method on 78 men from the documented Athens Collection.
Generalised linear models were adopted with entheseal changes as dependent variable and
cross-sectional geometric properties, age and body mass as predictors. The results suggest that age is
the factor most frequently affecting entheseal changes; however, its impact is not as systematic as found
in previous studies. Body mass is rarely statistically significant, again contradicting earlier studies. Finally,
activity proxied by cross-sectional geometric properties is occasionally significant, but no clear pattern
emerges that can associate specific entheseal morphological changes with specific directions of mechanical
loading. Copyright © 2016 John Wiley & Sons, Ltd.
Key words: activity patterns; Coimbra method; entheses; generalised linear models
Copyright © 2016 John Wiley & Sons, Ltd. Received 5 July 2016
Revised 18 August 2016
Accepted 24 August 2016
410 E. Michopoulou et al.
linked to the different body size (Weiss, 2003, 2004, by the method encompass the spectrum of changes
2007), as well as hormonal differences between the seen at fibrocartilaginous entheses from new bone
two sexes (Wilczak, 1998; Niinimäki, 2011). Finally, formation, erosions, textural change, porosity (both
body size affects ECs because bigger individuals fine porosity and macroporosity) and cavitations
exhibit more pronounced changes (Weiss, 2003, (Henderson et al., 2013, 2015; Villotte et al., 2016).
2004, 2007; Niinimäki, 2011). This may be explained Due to the higher fibrous content at the acute attach-
by the fact that individuals with greater body size ment of the fibres to the bone, this zone (zone 1) is
require more effort for movement. recorded separately from the remaining bone surface.
Given the multifactorial aetiology of ECs, recent To date, there are limited clinical data on the underly-
studies exploring these markers to deduce past activity ing aetiology of the observed changes on entheseal
patterns have adopted statistical models such as analy- sites, and this is one of the reasons that the new
sis of covariance or generalised linear models (GLM), Coimbra method records and analyses each feature sep-
which allow the study of the simultaneous impact of arately, to determine which feature or features are most
multiple variables, namely, age, sex, body mass and closely linked to biomechanics and thus are most appro-
activity, on ECs (Villotte et al., 2010; Niinimäki, priate for identifying activity patterns in the skeleton.
2011, 2012; Nikita, 2014; Henderson & Nikita, Therefore, it is interesting to see if this method has
2015). Such methods allow the study of the impact of the potential to capture activity-related markers more
activity patterns on ECs while controlling for the effect effectively but also to examine which of the recorded
of other contributing factors. The results have so far morphological changes appear to be more strongly
supported the primary role of age in EC expression, influenced by activity, rather than other factors.
followed by body size, while activity patterns also
appear to exert a subtle impact on the observed
changes (for example, Henderson & Nikita, 2015; Materials and methods
Michopoulou et al., 2015, but see also Villotte et al.,
2010 for a more pronounced impact of activity). The sample under examination included 78 male skele-
Despite the availability of statistical tests that allow tons, which form part of the Athens collection, housed
the effective study of multifactorial phenomena, such at the Department of Biology, Division of Animal and
as ECs, the optimum way to record ECs in order to Human Physiology, National and Kapodistrian Univer-
capture activity-induced alterations remains unclear. A sity of Athens, and consists of individuals that lived and
recent study by Michopoulou et al. (2015) showed that died in Greece during the 20th century (Eliopoulos
when ECs are scored using the most commonly et al., 2007). The documented age of these individuals
adopted recording protocols, that is, the Hawkey and ranges from 24 to 96 years and has the following distri-
Merbs (1995), Mariotti et al. (2004) and Villotte et al. bution: 20–40 years: 7 individuals, 40–60 years: 29 indi-
(2010) methods, there does not appear to be a system- viduals, 60–80 years: 31 individuals and over 80 years:
atic significant contribution of activity [proxied by 11 individuals. Individuals suffering from seronegative
archival profession data and cross-sectional geometric spondyloarthropathy, Diffuse Idiopathic Skeletal
(CSG) properties] on ECs. However, the same paper Hyperostosis (DISH) and/or acromegaly (conditions
noted a differential contribution of age, and secondar- identified following Ortner, 2003 and Waldron, 2008)
ily body mass, on EC expression on the right-sided were excluded because these conditions demonstrably
and left-sided upper limbs, which is potentially related influence entheseal morphology (e.g. Belanger & Rowe,
to the underlying impact of activity. 2001; Benjamin & McGonagle, 2001; Henderson,
The current paper examines whether recording ECs 2008). Note that the individuals included in the current
using the new Coimbra method (Henderson et al., study are a subset of the 90 individuals used in the paper
2013, 2015) can reveal a more systematic significant of Michopoulou et al. (2015). Twelve individuals of the
contribution of activity to EC expression. The new original study had to be excluded from the current one
Coimbra method for recording fibrocartilaginous because of their unavailability at the time of data
entheses was developed as a method to score different collection.
features of the ECs and determine their aetiology Only fibrocartilaginous entheses of the upper limbs
(Henderson et al., 2013, 2015). The method is only were examined, namely, the subscapularis on the
defined for fibrocartilaginous entheses because, unlike humerus and biceps brachii on the radius. The reasons
fibrous entheses, these have a ‘normal’ baseline appear- underlying our decision to focus only on
ance devoid of any roughness, pores or other alter- fibrocartilaginous entheses were two: (i) it has been
ations (Henderson et al., 2013). The features recorded suggested that fibrocartilaginous entheses exhibit a
Copyright © 2016 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 27: 409–417 (2017)
Effectiveness of the Coimbra Method 411
higher correlation with activity than fibrous entheses should be as large as possible. Our decision was addi-
(Villotte et al., 2010), and (ii) the baseline normal tionally based on a number of inherent limitations of
appearance of fibrocartilaginous entheses is recognised, documented profession as an activity proxy that have
whereas the fibrous entheses have no identifiable base- been identified by other scholars (see discussion in
line normal appearance. The subscapularis and biceps Alves Cardoso and Henderson, 2013), and the fact that
brachii were chosen because their zones are most in the paper of Michopoulou et al. (2015), the conclu-
clearly described in the original publication of the sions drawn when using profession and CSG properties
Coimbra method by Henderson et al. (2013); thus, they were largely similar.
can be easily identified and accurately recorded. Both In order to examine the impact of activity, age and
right and left elements were included in the sample. body mass on ECs, as captured by the new Coimbra
The EC recording scheme used was developed method, GLM were used. In these models, ECs were
during a workshop organised in Coimbra, Portugal, in assigned as dependent variable and CSG, age and body
2009, and its latest version is described in detail in mass as independent variables. It must be noted that
Henderson et al. (2015). In brief, the Coimbra method whereas in the paper of Michopoulou et al. (2015),
divides each enthesis into two zones and subsequently the GLM models included all independent variables
records a series of morphological alterations manifest- simultaneously, in the current paper two approaches
ing as new bone formation or resorption using an ordi- were followed. First, the models were run including
nal scale, as described in the Introduction section. A the main effects of all variables, like in the paper of
single observer (E. M.) performed all EC data collection Michopoulou et al. (2015). Second, the models were
in order to avoid biases because of interobserver error. run including the main effects and the two-way interac-
The possible impact of intraobserver error was tested tions between TA-body mass, TA-age and body mass-
by repeating data collection on 10 individuals 3 weeks age. In the latter case, due to the large number of inde-
after the original data collection was completed. The pendent variables, the optimum model was identified
results of the two rounds of data collection showed a based on the Akaike information criterion, which is a
high and significant correlation (Spearman's ρ or ϕ measure of the relative quality of the GLM model,
coefficient always >0.9 and p-value <0.05). and this is the one reported in the following sections.
The age of each individual was obtained from docu- To identify the optimum model, initially, all indepen-
mented records. Body mass was used as a proxy for dent variables (main effects and selected two-way inter-
body size, and it had already been calculated in the actions) were included in the model; then, the
context of the paper of Michopoulou et al. (2015). independent variable exhibiting the highest p-value
Activity was proxied by the CSG properties of the (thus the least significant contribution to the model)
humerus and radius. These properties had been calcu- was eliminated, and the test was repeated with the
lated in the context of the study of Michopoulou et al. remaining variables until the lowest Akaike value was
(2015) and included TA, Ix/Iy and Imax/Imin, whereby reached. All tests were run in R version 3.3.1 using
the total subperiosteal area of the diaphyseal cross the clm() function of the ‘ordinal’ library, whereas for
section (TA) expresses resistance to tension, compres- the determination of the optimum model based on
sion or shear, whereas the second moments of area the Akaike criterion, the stepAIC() function of the
(Ix, Iy, Imax and Imin) express resistance to bending forces ‘MASS’ library was used.
(Stock & Pfeiffer, 2001; Ruff, 2008). The CSG proper-
ties were calculated based on periosteal moulds, which
were obtained at the midshaft of the radius and at 35% Results
distance from the distal end of the humerus in order to
avoid the deltoid tuberosity (see Nikita et al., 2011 for Table 1 presents the sample sizes for the material under
details). study per side and element, as well as descriptive statis-
It must be noted that in the paper by Michopoulou tics. Tables 2–5 show the p-values for the model coef-
et al. (2015), additionally to CSG properties, docu- ficients, as well as the Akaike information criterion.
mented profession was also used as an activity proxy, Note that Tables 2, 3 present the results obtained when
and the individuals under study were divided into a the main effect of all predictors is included in the
‘manual’ and a ‘non-manual’ group. In the current paper, model, whereas Tables 4, 5 show the best models,
it was decided to restrict our activity markers to CSG based on the smallest Akaike information criterion,
because data on profession were available for less than when all main effects as well as the interactions be-
two-thirds of our sample and in order for complex sta- tween TA-age, TA-body mass and body mass-age are
tistical tests to provide accurate results, sample sizes considered. The reason TA was preferred over the
Copyright © 2016 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 27: 409–417 (2017)
412 E. Michopoulou et al.
R L R L R L R L
0 1 2 0 1 2
BF, bone formation; ER, erosion; TC, textural change; FPO, fine porosity; MPO, macro-porosity; CA, cavitation.
second moments of area in the examination of interac- right subscapularis. In contrast, age only affects signif-
tions was because this is the only true CSG property icantly bone formation in zone 1 in the remaining
calculated from periosteal moulds. cases, as well as microporosity in the left biceps brachii,
Regarding age, it can be seen that this predictor only and bone formation in zone 2 in the right biceps
has a systematically significant impact in the right brachii. In addition, the interaction of age with other
subscapularis (Table 2). However, in the left independent variables relating to activity and body
subscapularis, as well as the right and left biceps mass does not appear to have a significant impact on
brachii, the impact of age is small and inconsistent any of the ECs.
(Tables 2, 3). This observation applies to both when Activity, expressed as CSG properties, rarely
uncorrected and Holm–Bonferroni corrected p-values appears to have a significant effect on ECs when
are inspected. When the best models, including inter- the main effect of all predictors is input in the model
actions, are examined (Tables 4, 5), it is seen that age (Tables 2, 3). It is striking that after Holm–
is the main factor exhibiting a significant association Bonferroni correction, the only significant relation-
with ECs, but again, this is mostly prevalent in the ship is that between TA and bone erosion in zone
Table 2. p-values for the model coefficients when only main effects are included in the model – data for the right and left humerus (M.
subscapularis)
L humerus R humerus
Character AIC Age Body mass TA Ix/Iy Imax/Imin AIC Age Body mass TA Ix/Iy Imax/Imin
BF (Z1) 134.8 0.001* 0.703 0.949 0.292 0.069 120.0 0.001* 0.645 0.043 0.520 0.902
ER (Z1) 105.8 0.161 0.371 0.354 0.275 0.248 119.1 0.012 0.483 0.584 0.481 0.291
TC – – – – – – – – – – – –
BF (Z2) 132.7 0.067 0.814 0.612 0.955 0.878 145.4 0.002* 0.670 0.428 0.535 0.843
ER (Z2) 40.8 0.465 0.004* 0.000* 0.142 0.152 60.1 0.000* 0.097 0.246 0.620 0.062
FPO 94.6 0.109 0.213 0.718 0.681 0.760 87.9 0.018 0.962 0.742 0.021 0.145
MPO 102.1 0.074 0.947 0.961 0.514 0.821 101.6 0.292 0.093 0.523 0.617 0.766
CA 36.2 0.371 0.459 0.020 0.025 0.138 48.3 0.005* 0.115 0.110 0.356 0.789
Bold values are statistically significant at α = 0.05, whereas the asterisks denote values that remain statistically significant after the
Holm–Bonferroni correction.
BF, bone formation; ER, erosion; TC, textural change; FPO, fine porosity; MPO, macro-porosity; CA, cavitation; AIC, Akaike information
criterion.
Copyright © 2016 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 27: 409–417 (2017)
Effectiveness of the Coimbra Method 413
Table 3. p-values for the model coefficients when only main effects are included in the model – data for the right and left radius (M.
biceps brachii)
L radius R radius
Character AIC Age Body mass TA Ix/Iy Imax/Imin AIC Age Body mass TA Ix/Iy Imax/Imin
BF (Z1) 115.4 0.009* 0.538 0.441 0.124 0.460 151.9 0.001* 0.593 0.533 0.940 0.268
ER (Z1) 99.8 0.178 0.431 0.209 0.399 0.698 114.9 0.403 0.220 0.586 0.467 0.298
TC 75.2 0.394 0.245 0.830 0.668 0.369 66.8 0.823 0.723 0.551 0.556 0.627
BF (Z2) 117.0 0.115 0.949 0.369 0.131 0.100 138.8 0.022 0.814 0.990 0.395 0.641
ER (Z2) 88.3 0.110 0.361 0.773 0.354 0.294 130.2 0.092 0.519 0.431 0.601 0.505
FPO 112.2 0.254 0.845 0.324 0.046 0.272 113.7 0.005* 0.225 0.687 0.858 0.145
MPO 85.5 0.051 0.826 0.842 0.493 0.524 98.1 0.267 0.159 0.201 0.567 0.997
CA 51.8 0.427 0.577 0.423 0.538 0.090 65.4 0.079 0.480 0.130 0.093 0.037
BF, bone formation; ER, erosion; TC, textural change; FPO, fine porosity; MPO, macro-porosity; CA, cavitation; AIC, Akaike information
criterion.
Table 4. p-values for the optimum model coefficients – data for the right and left humerus (M. subscapularis)
Character AIC Age Body mass TA Ix/Iy Imax/Imin TA * body mass TA * age Body mass * age
L humerus
BF (Z1) 128.50 0.001*
ER (Z1) 98.97 0.216
TC – – – – – – – – –
BF (Z2) 120.42 0.058
ER (Z2) 38.34 0.062 0.006*
FPO 88.94 0.082 0.137
MPO 95.28 0.095 0.128
CA 30.32 0.057 0.071 0.113 0.037 0.058
R humerus
* *
BF (Z1) 114.38 0.001 0.043
ER (Z1) 114.82 0.012* 0.017*
TC – – – – – – – – –
BF (Z2) 138.86 0.001*
ER (Z2) 58.52 0.002* 0.028 0.063
FPO 83.53 0.015* 0.028
MPO 96.35 0.193
CA 44.27 0.006* 0.041 0.030 0.095 0.046
BF, bone formation; ER, erosion; TC, textural change; FPO, fine porosity; MPO, macro-porosity; CA, cavitation; AIC, Akaike information
criterion.
Copyright © 2016 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 27: 409–417 (2017)
414 E. Michopoulou et al.
Table 5. p-values for the optimum model coefficients – data for the right and left radius (M. biceps brachii)
Character AIC Age Body mass TA Ix/Iy Imax/Imin TA * body mass TA * age Body mass * age
L radius
BF (Z1) 110.89 0.006* 0.058
ER (Z1) 94.40 0.132 0.037 0.067 0.092 0.051
TC 70.40 0.168 0.126
BF (Z2) 112.49 0.093
ER (Z2) 82.81 0.259
FPO 107.69 0.061
MPO 79.70 0.010*
CA 39.87 0.300 0.128 0.120 0.225 0.256 0.117 0.117
R radius
*
BF (Z1) 146.05 0.003
ER (Z1) 109.24 0.048 0.223 0.025 0.022 0.053
TC 59.26 0.127 0.008* 0.065 0.065 0.157
BF (Z2) 131.79 0.009*
ER ( 123.94 0.064
Z2)
FPO 108.60 0.013 0.054 0.698 0.146 0.068 0.023
MPO 92.87 0.435
CA 62.47 0.138 0.079
BF, bone formation; ER, erosion; TC, textural change; FPO, fine porosity; MPO, macro-porosity; CA, cavitation; AIC, Akaike information
criterion.
and right upper limbs, suggesting that activity must different recording protocols (e.g. Wilczak, 1998;
play a subtle role in the bilateral expression of ECs. Weiss, 2003, 2004, 2007; Benjamin et al., 2009;
Based on the results of the current study, ECs Niinimäki, 2011; Milella et al., 2012). Note that in the
recorded using the new Coimbra method rarely exhibit original publication of the Coimbra method, the
a significant correlation with CSG properties, used as authors had tested the effect of age using ordinal
activity markers. This lack of correlation applies both regression and found that bone formation in either
when examining the main effects of all predictors as zone was most commonly associated with age;
well as when using optimum models with selected however, this was not uniform across all entheses,
interactions. In addition, no systematic association is while even when there was a statistically significant
traced between a specific aspect of the ECs (e.g. association, the effect of age was at most approximately
porosity, bone formation etc.) and CSG; therefore, 40% (Henderson et al., 2013).
there do not appear to be any specific osseous Our statistical analysis shows that age is the primary
responses to mechanical loading that are more informa- factor affecting EC expression using the new Coimbra
tive regarding past activity patterns than others. method, but the number of statistically significant
At this point, it must be stressed that using CSG associations between age and EC is overall rather small.
properties as a proxy for activity has certain limitations, Specifically, with the exception of the right
which may underline the observed lack of association subscapularis, age rarely had a significant impact on
between CSG and ECs. In specific, by means of ECs in our sample, both as an individual factor and in
CSG, in the current study, we have captured the interaction with other predictors. This lack of a strong
rigidity of skeletal elements against bending and association between age and ECs is striking considering
compressive forces. However, we cannot exclude the the age distribution of the sample under study, which
possibility that different types of mechanical stress, largely consisted of individuals aged between 40 and
such as high peak strain or shear strain, were more 80 years. Our findings may be explained by the
important in producing ECs. In addition, the ontogeny ‘levelling off’ process. In specific, even though muscle
of CSG and EC responses may be different, and this is strength increases during growth, it plateaus between
potentially an important issue, especially given the 25–30 years of age and starts declining after that time
likelihood that profession/activity would change over (Henderson et al., 1995). Similarly, entheses, and
the life cycle of an individual/population. subsequently ECs, increase with age until approxi-
What is striking in our current findings is the much mately the age of 40–50 years, but after that age, the
less pronounced overall impact of age, which contra- process levels off (Klein et al. 2002; Milella et al.,
dicts both our earlier findings (Michopoulou et al., 2012; Niinimäki, 2011; Robb, 1998). This phenome-
2015) and studies by other authors, who have used non has been attributed to physical activity decreasing
Copyright © 2016 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 27: 409–417 (2017)
Effectiveness of the Coimbra Method 415
Copyright © 2016 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 27: 409–417 (2017)
416 E. Michopoulou et al.
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