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Skeletal pathology and variable anatomy in elephant feet assessed using computed tomography

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  • Rainbow Equine Hospital, UK

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Foot problems are a major cause of morbidity and mortality in elephants, but are underreported due to difficulties in diagnosis, particularly of conditions affecting the bones and internal structures. Here we evaluate post-mortem computer tomographic (CT) scans of 52 feet from 21 elephants (seven African Loxodonta africana and 14 Asian Elephas maximus), describing both pathology and variant anatomy (including the appearance of phalangeal and sesamoid bones) that could be mistaken for disease. We found all the elephants in our study to have pathology of some type in at least one foot. The most common pathological changes observed were bone remodelling, enthesopathy, osseous cyst-like lesions, and osteoarthritis, with soft tissue minerali-sation, osteitis, infectious osteoarthriti, subluxation, fracture and enostoses observed less frequently. Most feet had multiple categories of pathological change (81% with two or more diagnoses, versus 10% with a single diagnosis, and 9% without significant pathology). Much of the pathological change was focused over the middle/lateral digits, which bear most weight and experience high peak pressures during walking. We found remodelling and osteoarthritis to be correlated with increasing age, more enthesopathy in Asian elephants, and more cyst-like lesions in females. We also observed multipartite, missing and misshapen phalanges as common and apparently incidental findings. The proximal (paired) sesamoids can appear fused or absent, and the predigits (radial/tibial sesamoids) can be variably ossified, though are significantly more ossified in Asian elephants. Our study reinforces the need for regular examination and radiography of elephant feet to monitor for pathology and as a tool for improving welfare.
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Submitted 6 October 2016
Accepted 6 December 2016
Published 18 January 2017
Corresponding author
Sophie Regnault, sregnault@rvc.ac.uk
Academic editor
Philip Kass
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DOI 10.7717/peerj.2877
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2017 Regnault et al.
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OPEN ACCESS
Skeletal pathology and variable anatomy
in elephant feet assessed using computed
tomography
Sophie Regnault1, Jonathon J.I. Dixon1, Chris Warren-Smith1,2,
John R. Hutchinson1and Renate Weller1
1Royal Veterinary College, Hertfordshire, United Kingdom
2Langford Veterinary Services, University of Bristol, Bristol, United Kingdom
ABSTRACT
Foot problems are a major cause of morbidity and mortality in elephants, but are
underreported due to difficulties in diagnosis, particularly of conditions affecting the
bones and internal structures. Here we evaluate post-mortem computer tomographic
(CT) scans of 52 feet from 21 elephants (seven African Loxodonta africana and 14
Asian Elephas maximus), describing both pathology and variant anatomy (including
the appearance of phalangeal and sesamoid bones) that could be mistaken for disease.
We found all the elephants in our study to have pathology of some type in at least
one foot. The most common pathological changes observed were bone remodelling,
enthesopathy, osseous cyst-like lesions, and osteoarthritis, with soft tissue minerali-
sation, osteitis, infectious osteoarthriti, subluxation, fracture and enostoses observed
less frequently. Most feet had multiple categories of pathological change (81% with
two or more diagnoses, versus 10% with a single diagnosis, and 9% without significant
pathology). Much of the pathological change was focused over the middle/lateral digits,
which bear most weight and experience high peak pressures during walking. We found
remodelling and osteoarthritis to be correlated with increasing age, more enthesopathy
in Asian elephants, and more cyst-like lesions in females. We also observed multipartite,
missing and misshapen phalanges as common and apparently incidental findings. The
proximal (paired) sesamoids can appear fused or absent, and the predigits (radial/tibial
sesamoids) can be variably ossified, though are significantly more ossified in Asian
elephants. Our study reinforces the need for regular examination and radiography of
elephant feet to monitor for pathology and as a tool for improving welfare.
Subjects Veterinary Medicine, Pathology, Radiology and Medical Imaging
Keywords Enthesopathy, Osteoarthritis, Radiography, Proboscidea, Bone, Sesamoid, CT,
Remodelling
INTRODUCTION
Elephants not only provide education and entertainment as zoological attractions, but also
have ecological significance as umbrella (or keystone) species, whose conservation indirectly
protects others (Choudhury et al., 2008). They also have economic importance as tourist
attractions and working animals. Welfare of elephants is an active area of discussion, both in
professional fields and in general society. Although the welfare of captive elephants has been
improving through husbandry initiatives and advances in knowledge of veterinary care for
these species, there remain several areas that continue to be obstacles to optimum welfare.
How to cite this article Regnault et al. (2017), Skeletal pathology and variable anatomy in elephant feet assessed using computed tomog-
raphy . PeerJ 5:e2877; DOI 10.7717/peerj.2877
Pathological foot conditions are one such problem area, thought to constitute the
single most important health problem of captive elephants, with up to 50% of elephants in
captivity suffering from foot problems, although the actual prevalence of carious conditions
remains unknown (Fowler, 2006). Accurate diagnosis is challenging, treatment is expensive
and time-consuming (Lewis et al., 2010) and chronic unresponsive conditions of the feet
are a major reason for euthanasia in captivity (Csuti, Sargent & Bechert, 2008).
Some foot problems are visible externally (e.g., solar pad or cuticle lesions), do not
require diagnostic imaging, and seem to be improving with the near-universal adoption of
daily examination and foot care routines in elephants (Lewis et al., 2010). However, other
pathological lesions—particularly those affecting the osseous structures—are challenging
to identify and monitor. Originally superficial lesions may lead to further problems through
ascending infection, resulting in osteomyelitis and/or infectious arthritis. Osteoarthritis
(OA, also called degenerative joint disease/DJD) is commonly encountered and other
problems are described.
Management conditions are thought to be the one of the most important factors
in the development of distal limb osseous pathologies (Fowler, 2006;Miller, Hogan &
Meehan, 2016). Osteomyelitis and septic arthritis are generally an extension of a soft
tissue infection or penetrating solar trauma. Hard floors, lack of exercise, and repeated
concussive forces (potentially including stereotypic behaviour; Haspeslagh et al., 2013) have
all been proposed to contribute to the development of OA (Hittmair & Vielgrader, 2000)
or general musculoskeletal foot health (Miller, Hogan & Meehan, 2016) . Additionally, the
conformation of the large and relatively straight limbs of elephants may predispose them
to pathology (Fowler, 2006), as might the inherent biomechanics of the feet. Pathological
changes have been speculated to occur more frequently in regions that normally experience
high pressures (i.e., mechanical stresses) during walking; namely the distal structures of
the lateral digits (Panagiotopoulou et al., 2012).
Lameness is not always an obvious feature in elephants with foot problems (Lewis et al.,
2010), and radiography of the distal limb has been described to diagnose and monitor foot
problems (e.g., Hittmair & Vielgrader, 2000;Siegal-Willott et al., 2008;Kaulfers et al., 2010;
Mumby et al., 2013). Over the recent years advanced imaging modalities such as computed
tomography (CT) and magnetic resonance imaging (MRI) have been more commonly used
in veterinary practice for musculoskeletal and other problems, but their use for elephants
is precluded by body size and transport issues. As a result of the limited availability of
imaging, the frequencies of these bony conditions in captive elephants are unknown and
they are almost certainly under-reported based on what we know in other large animals
such as cows (Nigam & Singh, 1980;Kofler, Geissbühler & Steiner, 2014) or rhinoceroses
(Regnault et al., 2013;Galateanu et al., 2013).
The aims of this study were to identify pathological bone lesions in the feet of captive
African (Loxodonta africana Blumenbach 1797) and Asian (Elephas maximus Linnaeus
1758) elephants using post-mortem CT. We hypothesise that when there is pathological
change, it will be present in multiple feet of the same individual and also that there will be
multiple kinds of pathological change, which may be due to shared predisposing factors
(e.g., management conditions, as above) and/or altered use. By exploring the locations of
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 2/21
pathological changes, we further hypothesise that foot regions typically exposed to high
pressures (i.e., lateral digits) are predisposed to developing lesions. When assessing any
structures for pathology it is essential that the clinician is aware of normal anatomical
variation, therefore, we also describe other osseous features that likely represent non-
pathological, variable distal limb anatomy.
MATERIALS AND METHODS
CT scans of 52 cadaver feet (16 right fore, 12 left fore, 14 right hind, 10 left hind) from
21 captive elephants (seven African Loxodonta africana, and 14 Asian Elephas maximus)
were evaluated for evidence of pathology. All elephants were adult or near-adult: ranging
from 17 to 61 years old. Feet or CT scans were donated to the Royal Veterinary College
from various sources (zoos and safari parks) in the European Union. Data on morbidity
and mortality was later compiled from an online database (http://www.elephant.se/) as
well as from donating institutions, and details on the individual elephants are summarised
in Table 1.
The following distal limb structures were assessed on the CT scans for all five digits
(denoted DI to DV by convention); the carpometacarpal (CMC) or tarsometatarsal
(TMT) joints, metapodial (metacarpal/metatarsal) bones, paired proximal sesamoids,
metacarpophalangeal (MCP) or metatarsophalangeal (MTP) joints, proximal and distal
interphalangeal (PIP and DIP) joints, phalangeal bones, and surrounding soft tissues.
Lesions were identified and interpreted by a large animal veterinary radiologist and resident
(J.D. and R.W.), and categorised in consensus using an established scheme previously used
for elephants and rhinoceroses (Regnault et al., 2013). This grading scheme is provided in
Table 2. Severity of each lesion was graded as slight, moderate, or severe (grades 1, 2 or 3
respectively; see Table 2 for grading criteria).
The degree of ossification of ‘‘predigits’’ (prepollex/prehallux, or radial/tibial sesamoids;
e.g., Hutchinson et al., 2008;Hutchinson et al., 2011) was also noted, and categorised as:
non-ossified (code 0), minimally ossified (code 1), moderate ossification embedded in
(presumably) cartilaginous soft tissue (code 2), or extensively ossified single structure
(code 3). Anatomical variability in the proximal sesamoid bones was described.
For analysis, each pathology category was expressed as the number of affected structures
per foot e.g., if osseous cyst-like lesions were observed only in metacarpals III and IV, the
foot would have two affected structures. For the more frequently observed pathological
categories (remodelling, enthesopathy, osseous cyst-like lesions and osteoarthritis), a
generalised estimating equation (GEE) was used to test age, sex, foot type (fore or hind), and
species (Asian or African) as predictors on the amount of observed pathology (modelled as
count data with a negative binomial distribution). The models ran as multi-variable negative
binomial regressions with backwards selection. For statistical assessment, significance was
set at p=0.05. Multiple feet from the same elephant were treated as repeated measures.
Similar GEE models were run for sesamoid fusion, and atypically-shaped and multipartite
phalanges (though only with Asian elephants for the latter, as no African elephants had
multipartite phalanges). A GEE (ordinal logistic) model was also used to test whether
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 3/21
Table 1 Details of seven African (Loxodonta africana) and 14 Asian (Elephas maximus) elephants in
this study. Asterisks indicate elephants known to have foot or locomotor problems. ‘Feet scanned’ indi-
cates how many feet had available CT scan data, ‘Reason for death/euthanasia’ details the cause of death
(from donating institutions or the online database http://www.elephant.se/).
Elephant Feet
scanned
Reason for death/euthanasia Sex Age
(years)
African1 4 ? M 19
African2 4 Euthanasia (vaginal/urogenital tract disease) F 24
African3 1 ? M 27
African4 1 Disease (infection, gastrointestinal, unspecified mechanical
abnormality)
M 28
African5 1 ? F 30
African6 4 Disease (suspected cardiac disease) F 32
African7 2 Disease (unspecified) M 32
Asian1 2 ? M 17
Asian2* 1 Euthanasia (forelimb lameness) M 17
Asian3* 4 Euthanasia (arthritis and aggression) F 26
Asian4 3 ? F 40
Asian5* 4 Euthanasia (foot abscess) F 35
Asian6 2 ? M 40
Asian7* 1 Euthanasia (chronic arthritis) F 40
Asian8 3 ? F 42
Asian9* 2 Disease (osteomyelitis and foot disease) F 52
Asian10 2 Euthanasia (unspecified illness) M 50
Asian11 1 Euthanasia (unspecified) F 50
Asian12 4 Euthanasia (unspecified) F 55
Asian13 2 Sudden collapse F 61
Asian 14 4 ? ? ?
Notes.
M, male; F, female; ?, unknown.
species was a significant predictor of degree of predigit ossification (modelled as categorical
data), and then separately within each species as bi-variable models to test if age and foot
type were significant predictors. Statistical analyses were performed in IBM SPSS Statistics
for Windows (Version 24.0).
To examine whether elephants with pathological lesions in one foot were more likely to
have lesions in other feet, we compared the proportion of elephants with one vs. two or
more feet diagnosed with pathology (only for the 15 elephants with scans of multiple feet,
and pathology in at least one foot) for all categories.
RESULTS
Pathological changes
All of the elephant feet in this study (i.e., all adults and near-adults) were observed to
have pathology of some type under our grading scheme. However, the majority of these
lesions (63%) were grade 1, thus considered to be clinically insignificant or anatomical
variants. We considered lesions of grade 2 or 3 (moderate and marked/severe) likely to
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Table 2 Grading scheme used for categorising pathological changes in this study.
Lesion type Changes observed Severity
Mineralisation Mineral opacity within soft tissues at a site distant to other
osseous structures
Slight =solitary short linear foci, occasionally
coalescing Moderate =multiple linear or
irregularly shaped mineral attenuating areas
Severe =extensive mineralisation, frequently linear
coalescing mineral structures, elongated
Osteitis Disruption of normal trabecular bone pattern, mottled
appearance, multiple hypoattenuating foci, loss of parts of
bone, destruction of normal bone outline, periosteal new
bone formation
Slight/Moderate/Severe based on extent of changes
Enthesopathy Discrete new bone formation at attachment sites of tendons
and ligaments
Slight/Moderate/Severe: based on size and extent of the
mineral attenuation at the site of the soft tissue structures
insertion onto the bone, if multiple sites affected in the
same bone then interpretation based on all affected sites for
overall grade.
Cyst-like lesions Well-defined radiolucencies (with hyperattenuating rim) Grade based on size (not measured), small/medium/large
(observer experience-based only)
Fractures Sclerotic linear areas, may be with new bone formation at
bone surface (old), linear hypoattenuation (acute)
Not graded (just present/absent)
Osteoarthritis Discrete new bone at periarticular surface, subchondral
bone sclerosis, narrowing or obliteration of joint space,
subchondral lysis, widening of joint space
Mild: small pointed periarticular osteophytes,
mild increased bone attenuation or
thickening of the subchondral bone plate
Moderate: Multiple medium sized periarticular
osteophytes, evidence of widening or narrowing
of the joint space not considered to be related to
limb position only, thickening of the subchondral
bone and adjacent increased mineral attenuation.
Severe: Numerous and extensive periarticular osteophytes,
marked narrowing of the articular space, marked
subchondral bone thickening/hyperattenuation.
Infectious arthritis Florid new bone formation at periarticular surface,
subchondral bone lysis, widening of joint space,
subchondral bone sclerosis, narrowing or obliteration
of joint space
Slight/Moderate/Severe based on extent of changes
Remodelling Enlargement of vascular channels and synovial fossae,
irregular contour to the osseous structures away from the
joint surfaces and not considered entheseophyte formation,
sometimes deep excavations in the bone, alterations in
shape of a bone.
Subjective scale of the overall shape of the bone, degree of
periosteal change identified, alterations in the cortices. No
fixed categorical variables.
Subluxation Loss of articular surface contact between the bones forming
a joint
Not graded (just present/absent)
represent clinically significant pathology. Based on this assessment, only grade 2 and 3
lesions were analysed further below. Forty seven of 52 feet (21/21 elephants) were found
to contain pathological changes graded moderate (2) or greater. Percentages are reported
for descriptive purposes.
The most frequent change observed was remodelling, especially observed as bone
surface irregularities (Figs. 1A and 1D), representing 31% of all pathologies observed (see
Table 3 for breakdown). Remodelling was present in 18 out of 21 elephants (39/52 feet).
Commonly remodelled bones were the metapodials (with 31% of all remodelling observed
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 5/21
Figure 1 Sagittal CT slices of digits in elephant feet, exhibiting pathological changes. (A) Remodelling
of the metacarpal (arrow) and fracture of the middle phalanx (filled arrowhead) in DIV of the right hind
foot of ‘Asian8’. (B) Enthesopathy of the proximal sesamoid (filled arrowhead) and evidence of DJD (os-
teophytes, altered joint spacing) at the proximal and middle interphalangeal joints (arrows) in DIV of the
right forefoot of ‘Asian10’. (C) Focal hyperattenuating region (arrow) and misshapen, scalloped proxi-
mal phalanx (filled arrowhead) in DII of the right forefoot of ‘Asian13’. (D) Remodelling of the bones (ar-
row), subluxation of the proximal interphalangeal joint (unfilled arrowhead) and soft tissue mineralisa-
tion (filled arrowheads) in DIII of the right hind foot of ‘Asian4’.
here), proximal phalanges (30%), sesamoid bones (16%) and middle phalanges (8%).
Commonly affected digits were DIII (27% of remodelling), DIV (25%), DV (21%) and DII
(17%), whilst DI appeared least affected (10%). A GEE (negative binomial model) found
that observed remodelling increased with age (p=0.01 in the final univariate model);
age remained significant (p=0.03) after accounting for species (p=0.2), sex (p=0.8),
and foot type (fore vs. hind; p=0.7) in the multivariable modelling. For the affected
elephants with multiple feet scanned, remodelling was commonly observed in multiple feet
(10/13 elephants with two or more affected feet, with only three elephants having a single
foot affected).
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Table 3 Summary of Grade 2+pathological lesions detected in this study. In the first column, ‘‘Af’’ and ‘‘As’’ with numbers correspond to our elephant subjects from
Table 1; also ‘‘Path,’’ number of unique pathology categories observed per individual elephant, and asterisks indicate elephants known to have foot or locomotor prob-
lems. Second column: ‘‘Foot’’: LH, left hind; LF, left fore; RH, right hind; RF, right fore.
Elephant Foot Calcification Osteitis Enthesophyte Cyst Fracture OA Infectious OA Remodelling Subluxation Misc.
Af1 Path: 2 LF 0 0 1 1 0 0 0 0 0 0
LH 0 0 1 0 0 0 0 0 0 0
RF 0 0 0 0 0 0 0 0 0 0
RH 0 0 0 0 0 0 0 0 0 0
Af2 Path: 2 RH 0 0 0 1 0 0 0 0 0 0
RF 0 0 1 0 0 0 0 0 0 0
LF 0 0 1 1 0 0 0 0 0 0
LH 0 0 0 0 0 0 0 0 0 0
Af3 Path: 7 RH 6 3 7 3 0 6 2 8 0 0
Af4 Path: 1 RF 0 0 0 0 0 0 0 0 0 1
Af5 Path: 5 LF 4 0 6 6 0 7 0 9 0 0
Af6 Path: 5 LF 0 0 1 3 0 2 0 3 0 0
LH 0 0 0 3 0 0 0 1 0 0
RF 0 0 1 5 0 0 0 0 0 0
RH 0 1 2 6 0 1 0 3 0 0
Af7 Path: 3 RF 0 0 0 0 0 0 0 0 0 0
LF 0 0 2 3 0 0 0 3 0 0
As1 Path:3 RF 0 0 0 1 0 0 0 1 1 0
LF 0 0 0 0 0 0 0 0 0 0
As2* Path: 6 RH 2 0 8 1 1 1 0 8 0 0
As3* Path: 4 LF 0 0 8 2 0 0 0 9 0 0
LH 0 0 0 0 0 0 0 2 0 0
RF 0 0 8 1 0 1 0 4 0 0
RH 0 0 3 3 0 4 0 2 0 0
As4 Path: 8 LF 0 1 4 3 0 3 0 4 0 0
RF 9 0 7 3 0 4 0 4 0 0
RH 6 5 10 11 0 9 2 12 1 0
As5* Path: 4 LF 0 0 2 0 0 1 0 1 0 0
LH 0 0 9 1 0 2 0 6 0 0
RF 0 0 9 1 0 0 0 6 0 0
RH 0 0 4 0 0 0 0 3 0 0
(continued on next page)
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Table 3 (continued)
Elephant Foot Calcification Osteitis Enthesophyte Cyst Fracture OA Infectious OA Remodelling Subluxation Misc.
As6 Path: 3 LF 0 0 2 1 0 0 0 0 0 0
RF 0 0 2 0 0 0 0 1 0 0
As7* Path: 6 RF 0 2 4 1 0 1 1 5 0 0
As8 Path: 7 LH 0 0 12 6 0 7 0 12 0 0
RF 3 2 7 2 0 3 1 5 0 0
RH 0 0 4 4 0 3 0 7 0 0
As9* Path: 8 LH 6 1 3 2 0 2 1 6 1 0
RH 0 0 3 0 0 3 0 4 1 0
As10 Path: 4 RF 0 0 12 3 0 10 0 20 0 0
RH 0 0 2 1 0 0 0 3 0 0
As11 Path: 2 RH 0 0 0 3 0 0 0 4 0 0
As12 Path: 6 LF 1 0 6 0 0 3 0 9 2 0
LH 4 0 5 0 0 1 0 8 1 0
RF 2 0 13 2 0 3 0 13 0 0
RH 2 0 2 1 0 0 0 5 1 0
As13 Path: 9 LH 3 0 5 3 1 1 0 4 0 0
RF 1 0 7 6 0 6 1 8 1 2
As14 Path: 7 LF 3 4 9 5 0 6 3 14 0 0
LH 0 0 3 3 0 1 0 5 0 0
RF 3 2 7 4 0 6 2 11 0 0
RH 0 0 1 7 0 1 0 4 0 0
Total: 55 21 204 113 2 98 13 237 9 3
755
observations
(7%) (3%) (27%) (15%) (0.3%) (13%) (2%) (31%) (1%) (0.4%)
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The second most commonly identified pathology was enthesopathy (Fig. 1B),
representing 27% of all pathologies observed (Table 3). Enthesopathy was present in 18/21
elephants (43/52 feet). Commonly affected regions were the metapodial bones (32%),
proximal phalanges (27%), sesamoids (21%) and CMC/TMT joints (18%). Commonly
affected digits were DIII (27%), DIV (24%), DV (23%) and DII (19%), whilst DI appeared
least frequently affected (6%). A GEE (negative binomial model) found enthesopathy
was more commonly observed in Asian compared to African elephants (p=0.001 in the
final univariate model); species remained significant (p=0.03) after accounting for age
(p=0.3), sex (p=0.6), and foot type (p=0.8) in the multivariable modelling. For the
affected elephants with multiple feet scanned, enthesopathy was almost always observed
in multiple feet (13/14 elephants with two or more affected feet versus one elephant with
only a single foot affected).
Osseous cyst-like lesions of bone (Figs. 2A and 2B) represented 15% of all pathologies
observed (Table 3), present in 20/21 elephants (39/52 feet). Commonly affected structures
were the metapodial (56%) and proximal phalangeal bones (28%). Commonly affected
digits were DIV (27%), DIII (24%), DII (21%) and DV (19%), whilst DI appeared least
affected (10%). A GEE (negative binomial model) found that osseous cyst-like lesions were
more commonly observed in females compared to males (p=0.01 in the final univariate
model); sex remained significant (p=0.03) after accounting for species (p=0.3), age
(p=0.5) and foot type (p=0.2) in the multivariate modelling. For the affected elephants
with multiple feet scanned, osseous cyst-like lesions were generally observed in multiple
feet (10/15 elephants with two or more affected feet, versus five elephants with only a single
foot affected).
Osteoarthritis (OA; Fig. 1B) represented 13% of all pathologies observed (Table 3),
present in 14/21 elephants (28/52 feet). Commonly affected joints were the
carpometacarpal/tarsometatarsal joints (46%), metacarpophalangeal/metatarsophalangeal
joint (36%), and proximal interphalangeal joint (10%). Commonly affected digits were
DIII (28%), DIV (25%), DII (24%) and DI (12%), whilst DV appeared least affected by
OA (11%). A GEE (negative binomial model) found that OA increased with age (p=0.02
in the final univariate model); age remained significant (p=0.05) after accounting for foot
type (p=0.6), sex (p=0.6), and species (p=0.9) in the multivariate modelling. For the
affected elephants with multiple feet scanned, OA was almost always observed in multiple
feet (9/10 elephants with two or more affected feet, versus one elephant with only a single
foot affected).
Soft tissue mineralisation (Figs. 1D and 2C) represented 7% of all pathologies observed
(Table 3), present in 9/21 elephants (17/52 feet). These mineralisations were identified
having similar interdigital, frequently linear structure in all limbs. For the affected elephants
with multiple feet scanned, mineralisation was generally observed in multiple feet (4/6 ele-
phants with two or more feet affected, versus two elephants with only a single foot affected).
Osteitis (Fig. 2D) represented 3% of all pathologies observed (Table 3), present in
7/21 elephants (9/52 feet). Commonly affected regions were the proximal and middle
phalanges (33% and 29% of observations, respectively), metapodials (24%), and sesamoids
(14%). Commonly affected digits were DIV (48% of osteitis observed here), DIII (38%),
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Figure 2 Transverse CT slices of digits in elephant feet, exhibiting pathological changes. (A) Multiple
osseous cyst-like lesions in metacarpal (filled arrowhead) in DV of the right hind foot of ‘African2.’ (B)
Solitary osseous cyst-like lesions in the proximal phalanges (filled arrowheads) of DIII and DIV of the left
forefoot of ‘African6.’ (C) Soft tissue mineralisation on the palmar aspect of digits (filled arrowheads) in
the right forefoot of ‘Asian4’. (D) Osteitis of the proximal phalanx (arrow) and infectious osteoarthritis of
the proximal interphalangeal joint (filled arrowhead) in DIV of the left forefoot of ‘Asian14.’
whilst DV (10%) and DII (5%) appeared least affected. DI was not affected in any limb
studied. For the affected elephants with multiple feet scanned, osteitis was observed roughly
equally affecting multiple feet versus just one foot (2/5 elephants versus three elephants,
respectively).
Infectious osteoarthritis (Fig. 2D) represented 2% of all pathology observed (Table 3),
present in 7/21 elephants (8/52 feet), or 13 joints in total. In 7/8 feet, bone(s) adjacent
to the affected joints were also observed with osteitis. Commonly affected joints were the
MCP/MTP (46%), PIP (38%) and DIP joints (15%). Commonly affected digits were DIV
(54%), DIII (38%) and DV (8%). DI and DII were unaffected in any limb. For the affected
elephants with multiple feet scanned, infectious OA was generally only observed in one
foot (5/6 elephants with a single affected foot, versus only one elephant with multiple
feet affected).
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 10/21
Subluxation (Fig. 1D) of a joint represented 1% of all pathology observed (Table 3),
present in five out of 21 elephants (8/52 feet). The MCP/MTP, PIP and DIP joints were
equally affected. Digits were also fairly equally affected. For the affected elephants with
multiple feet scanned, subluxation was observed roughly equally affecting multiple feet
versus just one foot (two elephants versus three elephants, respectively). Complete luxation
was not observed in any joint in this study.
Fractures (Fig. 1A) represented <1% of all pathology observed (Table 3), present in only
3/21 elephants (3/52 feet). Two of the fractures were identified in the distal phalanx of
DIII, and one was of the middle phalanx of DIV.
In addition to the categories of pathology listed in Table 2, we observed focal
hyperattenuating (i.e., highly dense) regions within the medullary cavities of long bones
(Fig. 1C) in two out of 21 elephants (2/52 feet). Three hyperattenuating regions were
observed in total: two in the metacarpals of digit III (different feet of different elephants),
and one in the proximal phalanx of digit II.
In this study, multiple types of pathology were identified in most feet: out of 52 feet, two
were observed with all nine pathological categories listed in Table 2, two feet with eight
categories, three feet with seven categories, seven feet with six categories, 12 feet with five
categories, six feet with four categories, three feet with three categories, and eight feet with
two categories. Only three feet were observed with a single category of pathology, and six
feet (11.5% of limbs) had no evidence of pathology.
Anatomical variations
In the CT images evaluated, the configuration of the proximal sesamoid bones was variable:
they were sometimes present as a pair, commonly fused together (appearing as a single
bone), and occasionally absent from scans altogether (i.e., not visible as either an ossified
bone or as an obvious soft tissue structure; Figs. 3A and 3D).
In digit I, the sesamoids often had the appearance of a single bone (42/52 feet); very
occasionally they appeared as a fused pair (3/52 feet), and in only one foot appeared as
an unfused pair. The digit I sesamoids were always present in African elephants, but were
sometimes missing in the hind feet of Asian elephants (absent in 6/14 Asian elephants, or
8/35 hind feet).
In our sample of African elephants, the sesamoid bones in the other digits were almost
always paired; only two feet out of 17 had fused sesamoids (in digits III and IV in one hind
foot, and digit V in another elephant’s forefoot). In Asian elephants the appearance of
sesamoids in the other digits varied much more. In digit II, 22 were fused, 12 were paired,
and one appeared single. In digit III, 26 were fused, eight were paired, and one was lytic
and difficult to assess. In digit IV, 24 were fused, 10 paired, and one absent. In digit V, 12
were fused, 22 paired, and one appeared single. In both species, the lateral sesamoid of digit
V was sometimes appreciably larger than the medial sesamoid (Fig. 3C). A GEE (negative
binomial model) found that species was a statistically significant predictor (p<0.0005
in both the multivariate and final univariate model) of amount of sesamoid fusion (i.e.,
number of fused pairs per foot, not distinguishing which pairs), with Asian elephants
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 11/21
Figure 3 Transverse CT slices of elephants’ feet, showing the sesamoids. (A) Completely unossified
prepollex (red box) in the right forefoot of ‘Asian4.’ Note also the single sesamoid of DI (arrow) and the
paired proximal sesamoids of other digits (filled arrowheads). (B) Sparsely mineralised prepollex (red
box) in right forefoot of ‘African6.’ (C) Medium-sized, discrete ossification of the prepollex (red box) in
right forefoot of ‘African2.’ Note also the larger lateral sesamoid of DV (filled arrowhead) compared to the
medial sesamoid. (D) Large ossification bounding the outer edges of the prepollex (red box) in right fore-
foot of ‘Asian12.’ Often, the middle of the predigit will remain partially unossified resulting in a rod-like
appearance. Note also fusion of the paired proximal sesamoids (filled arrowheads) in DII–DIV, compared
to the unfused sesamoids in (A).
possessing more fused sesamoids than African elephants. Sex (p=0.9), foot type (p=0.4),
and age (p=0.7) were not significant.
Ossified predigits (i.e., radial/tibial sesamoids associated with digit I) were more
frequently identified in Asian than African elephants. In African elephants, 9/17 feet (3/7
elephants) had evidence of ossified predigits, compared to 27/35 feet (13/14 elephants) in
Asian elephants. The extent of ossification was lower in African elephants: seven predigits
were minimally ossified and two had intermediate ossification, versus one minimally
ossified predigit, six with intermediate ossification, and 20 extensively ossified predigits
in Asian elephants. Figure 3 shows the different degrees of predigit ossification observed.
A GEE (repeated measures ordinal logistic model) found that species was a statistically
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 12/21
Figure 4 Three-dimensional reconstructions from CT scans. (A) Dorsal view of the left forefoot of
‘Asian5’, showing tripartite distal phalanx of DIII (arrows; also CT appearance inset) and misshapen mid-
dle phalanges of DII and DIV (unfilled arrowheads). The middle phalanx of DII is wedge shaped, whilst
that of DIV is wedged-shaped with a scalloped distal aspect and missing distal phalanx (filled arrowhead).
(B) Dorso-lateral view of the right hind foot of ‘Asian9’ showing the bipartite distal phalanx (arrow) and
missing middle phalanx (filled arrowhead) of DV.
significant predictor of presence and extent of predigit ossification (p=0.009). Within
each species, neither age (p<0.9 in African elephants and p=0.5 in Asian elephants) nor
foot type (fore versus hind; p<0.9 for African elephants and p=0.7 for Asian elephants)
were found to be statistically significant predictors of predigit ossification.
We observed multipartite distal phalanges (Fig. 4) in 36 digits of 23 feet (12 elephants;
all Asian). Most were bipartite (27/36), but some were tripartite (9/36). Multipartite distal
phalanges were most frequently identified in DV (16/36), DIII (9/36), DIV (6/36), and DII
(5/36). DI had none. A GEE (negative binomial model) found that, within Asian elephants,
neither age, sex nor foot type were statistically significant predictors of multipartite distal
phalanges (p=0.3, p=0.1, p=0.1 respectively).
We observed 25 atypically shaped phalanges in 17 feet of 11 elephants (10 Asian and
one African). Affected bones were most often middle phalanges (23/25 bones), but one
proximal and one distal phalanx were also observed to have atypical shapes. The shape of
the bones varied, but most appeared wedge-shaped (Fig. 4A) due to relative shortening of
the bone’s abaxial aspect and/or mediolateral narrowing (18/25 bones). Others appeared
very rounded with loss of the typical rhomboidal shape (5/25 bones), and occasionally
bones had a scalloped appearance of the articular surface (2/25 bones; see Figs. 1C and 4A).
Atypically shaped phalanges were most often observed in DIV (11/25 bones) and DII (9/25
bones), with fewer seen in DI (3/25 bones) and DV (2/25 bones). No atypically shaped
bones were observed in DIII. A GEE (negative binomial model) found age (p=0.002),
species (p=0.02) and foot type (p=0.01) to be statistically significant predictors of
atypically-shaped phalanges, being more frequent in younger elephants, Asian elephants,
and hind feet (20 bones in 12 hind feet vs five bones in five forefeet) in multivariate
modelling. Sex was not significant (p=0.8).
Phalangeal number varied between digits and feet. All African elephants had only the
proximal phalanx in DI of their forefeet, and no phalangeal bones visible in DI of their
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 13/21
hind feet. The distal phalanx of DII was occasionally absent (2/10 African forefeet and
3/7 hind feet). The distal phalanx was always absent from DV in all African elephant feet.
Subjectively, Asian elephants appeared to exhibit slightly more variability in phalangeal
number. All Asian elephants lacked at least the middle phalanx in DI of their forefeet,
however some also lacked the distal phalanx (9/18 Asian forefeet), and one foot lacked all
phalanges in DI. In the hind feet of Asian elephants, some lacked only the distal phalanx
from digit I (2/17 hind feet), some also lacked the middle phalanx (4/17), and most lacked
all three (11/17). In DII, 1/17 hind feet was missing a middle phalanx and 1/17 was missing
a distal phalanx. In DIII, 1/18 forefeet was missing a distal phalanx. In DIV, 4/18 forefeet
were missing the distal phalanx and 1/18 forefeet was missing all three phalanges (suspected
digital amputation, given the CT appearance). In DV, 3/18 forefeet and 11/17 hind feet
were missing the middle phalanx (Fig. 4B), whilst 1/17 hind feet was missing both middle
and distal phalanges.
DISCUSSION
All elephants and almost all feet in this study were found with lesions likely to represent
clinically important pathology. The elephants in our study are a biased population in this
regard—though cause of death was not always clearly specified, it appears at least five of
the 21 elephants died or were euthanised in part due to foot or joint problems. Despite this,
our findings reinforce the longstanding concern that foot problems are frequent causes of
morbidity and mortality in captive elephants (Steel, 1885;Fowler, 2001;Luikart & Stover,
2005;Siegal-Willott, Alexander & Isaza, 2012).
In addition to foot problems that are widely acknowledged in the literature on elephant
pathologies (OA, infectious OA, osteitis, fractures and subluxation), we have observed
remodelling of bones, enthesopathy, osseous cyst-like lesions, soft tissue mineralisation
and hyperattenuating bone foci. We also found atypically shaped and absent phalanges,
though any pathological significance of these features is unclear. Most of the elephant
feet in this study had several pathological diagnoses (Table 3), supporting the notion
that the different types of pathology have common causes, and/or that the establishment
of one disease process may predispose elephants to developing others. For many types
of pathology, multiple feet from the same elephant were affected, consistent with a
generalised predisposition (e.g., husbandry, obesity; see also Miller, Hogan & Meehan,
2016) rather than singular cause. Most of our findings generally fall into three (sometimes
overlapping) categories: lesions related to weight-bearing and loading of tissues, lesions
related to ascending infection, and variable anatomy with unclear pathological significance.
Loading appears to have a significant influence on the development of pathology. A
large proportion of the identified pathology was concentrated on the lateral three digits
(remodelling, enthesopathy, osteitis, and infectious OA) or middle three digits (OA and
osseous cyst like lesions); digits III and IV being the common denominator in both
cases. The body weight of elephants is thought to be principally borne by the middle
three digits (DII, DIII, and DIV) (Siegal-Willott, Alexander & Isaza, 2012), with the lateral
three digits (DIII, DIV, DV) typically experiencing the greatest pressures during walking
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 14/21
(Panagiotopoulou et al., 2012). Contrary to expectations, we did not find the forelimbs to be
significantly more affected by pathology than the hind limbs (Hittmair & Vielgrader, 2000),
despite bearing a greater proportion of bodyweight (60%; Genin et al., 2010). However,
pressures on the forefeet are only higher in some instances and regions (Panagiotopoulou
et al., 2012). Additionally, the digital cushions and predigits differ between fore and hind
feet (Weissengruber, 2006;Hutchinson et al., 2011), and the limbs may be used differently
in different styles of locomotion or other behaviours, potentially resulting in different
patterns of loading between feet.
In OA, the link to increased or altered loading (via obesity or poor conformation) is fairly
well established, though other factors (including trauma) may be involved (Fowler, 2006;
Siegal-Willott, Alexander & Isaza, 2012). For other (putative) types of pathology, such as
remodelling, enthesopathy and soft tissue mineralisation, the link to large or abnormal loads
is hypothesised from other species. Enthesopathy in humans can be seen in degenerative,
inflammatory or metabolic diseases (Ruhoy, Schweitzer & Resnick, 1998), and with aging
(Shaibani, Workman & Rothschild, 1993). But animal models show that enthesopathy can
also occur without tendon microtears or inflammation and may be an adaptive response
to loading (Benjamin, Rufai & Ralphs, 2000). Remodelling and enthesopathy are both
frequently observed in rhinos and thought to reflect tissue loading (Regnault et al., 2013;
Galateanu et al., 2013;Stilson, Hopkins & Davis, 2016). The linear appearance and the
location of soft tissue mineralisation in our elephants suggest that the digital flexor tendons
are the affected structures. Mineralisation of the deep digital flexor tendon in horses has
been observed as a response to chronic injury (Dyson, 2003b), and general mineralisation
has been described as a feature of tendinopathy (tendon disease arising from overuse) and
following trauma in other species (O’Brien et al., 2012). The magnitude of load experienced
by structures may be a factor (especially in OA and remodelling, which both increase with
increasing age and therefore presumably body weight), as might the type of loading; e.g.,
altered locomotion or long periods of standing. As elephants are both very large and
long-lived, they may be more predisposed to loading-associated pathology and/or bone
remodelling (perhaps including the variable sesamoid and phalangeal bone appearances
described below) compared with other species. Indeed, as ossification of the foot and other
limb bones tends to begin relatively late in elephants (Hautier et al., 2012) and their growth
plates also tend to close late in life (uncertain and variable timing but roughly at 8–20
years of age; Roth, 1984;Siegal-Willott et al., 2008), the growth patterns of elephant feet
(and perhaps limbs more generally) may leave them more vulnerable to accumulation of
pathologies, although much more research is required to test this speculation.
Osteitis and infectious OA often result from spreading soft tissue infections, or
penetration of a foreign object into the foot (Fowler, 2006). Our study found the proximal
bones and joints to be more affected, compared to the distal and middle phalanges more
often reported in other studies (Fowler, 2006 citing Gage, 1999 and Hittmair & Vielgrader,
2000); this apparent discrepancy might be best explained by variability and sample sizes in
both cases.
We observed subluxation and fracture, which may result from trauma but may also
sometimes be incidental findings (for example, fracture of the distal phalanx in elephants;
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 15/21
Fowler, 2006). Post-mortem fracture or manipulation of bones out of congruency also
cannot be ruled out. Interestingly, we frequently observed multipartite distal phalanges that
appear very similar to fractured phalanges but that we inferred to be a distinct entity, based
on the lack of callus or bone reaction. The phalanges resembled the incompletely ossified
distal phalanges observed radiographically in juvenile Asian elephants (Siegal-Willott et
al., 2008). The affected elephants in our study were also all Asian (no African), and the
distal phalanges of the lateral digits (DV and to a lesser degree, DIV) were most frequently
observed to be multipartite. Like Siegal-Willott et al. (2008), we found bipartite phalanges
(called ‘unilateral wing lucencies’) more common that tripartite phalanges (‘bilateral wing
lucencies’). We observed multipartite distal phalanges in elephants up to 55 years old, and
so it seems that the ossification centres of these bones may not always fuse with age (similar
to multipartite sesamoids). We acknowledge that the distinction between fracture and a
congenitally multipartite bone can be subtle (or even impossible with chronic fractures;
Morandi, 2012), and that the pathological significance of either condition appears negligible
in the distal phalanx.
It is important that veterinarians and radiologists are aware of such apparently normal
anatomical variations and incidental lesions when evaluating pathology in the feet. Best-
known amongst these is variable phalangeal number, especially in DI and DV (Ramsay &
Henry, 2001;Fowler, 2006;Hutchinson et al., 2008;Siegal-Willott, Alexander & Isaza, 2012).
Our data also support this longstanding observation of elephants, and confirm that digits II,
III and IV generally have three phalanges (although exceptions existed, especially amongst
Asian elephants). Atypically shaped phalanges are another source of anatomical variation
observed in this study.
Sesamoid bones also had variable appearances—not only the proximal sesamoid bones
(generally paired bones in other species but which may be fused or asymmetrical in
elephants), but also the predigits. These false ‘sixth toes’ seem to be modified sesamoids
that start out as cartilaginous rods but may later ossify (Hutchinson et al., 2011). In our
elephant sample (with sample overlap from those of Hutchinson et al., 2011), the predigits
ranged from completely non-ossified (visible as a hollow cartilaginous rod), to small and
patchy regions of mineral attenuation, to large discrete pieces of bone, to long, elaborate
and jointed structures curving around to the back of the foot. Within the same animal,
the degree of mineralisation in pairs of forefeet or hind feet was consistent, but could vary
between fore and hind limbs.
We found that Asian elephants showed a greater tendency towards ossification of the
predigits. Presence of sesamoid bones at joints has been linked to increased OA by some
studies (e.g., Pritchett, 1984;Hagihara et al., 1993), though not others (e.g., Muehleman,
Williams & Bareither, 2009). The possible link to OA in humans has prompted the
hypothesis that sesamoids may predispose joints to developing disease, or that both OA and
sesamoids are linked by an underlying process (i.e., tendency for endochondral ossification;
Sarin et al., 1999). Although we did not find significantly more OA in Asian compared to
African elephants, we did find more enthesopathy, more sesamoid fusion, and multipartite
distal phalanges (indicating multiple unfused ossification centres). Along with their greater
predigit ossification, these findings lead us to speculate that Asian elephants might have
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 16/21
an increased tendency for endochondral ossification (in their distal limbs) than African
elephants. This could explain some differences in disease prevalence and bone anatomy.
Of our findings, only the osseous cyst-like lesions and hyperattenuating regions
do not clearly fit into the categories of lesions related to loading, infection, or
incidental finding/variable anatomy. Osseous cyst-like lesions may be secondary to OA,
osteochondrosis (particularly if subchondral), ischaemic necrosis, haemorrhage, or vascular
malformation (Carlson & Weisbrode, 2006). Like our elephants, sex-based biases in cyst
prevalence have been noted in humans (O’Donnell, 2009) and some other animals (Craig,
Dittmer & Thompson, 2016). The hyperattenuating regions resemble enostoses (benign
foci of dense bone), which are sometimes associated with lameness in horses (Dyson,
2003a). The cause is unknown, but contributing factors may include excess dietary calcium
(Carciofi & Do Prado Saad, 2008).
CONCLUSIONS
Though a small proportion of our elephants were previously known to have foot or joint
problems, the generally high level of pathology found in our study highlights the need for
continuing vigilance regarding elephant foot health. We should not be complacent with
lack of lameness or externally apparent signs. A comprehensive evaluation of foot health
in elephants should therefore include ‘baseline’ foot radiographs to establish the ‘normal’
anatomy for that individual, and annual assessment thereafter using radiographic protocols
with standard views optimal for the detection of pathological lesions (Mumby et al., 2013).
In addition, weight management, regular exercise, a clean and appropriate environment
(with minimal time spent on hard surfaces; Miller, Hogan & Meehan, 2016), and other
measures to prevent over-loading, injury and infection should not be overlooked.
ACKNOWLEDGEMENTS
We thank Yu-mei Chang for statistical advice, and others who have helped on aspects
of this project before including Louise Ash, Reshma Biljani, Stefania Danika, Zoe Hill,
Sophie Jenkins, Charlotte Miller, Olga Panagiotopoulou, Sharon Warner, and members
of the Structure & Motion Laboratory. We also are grateful to all of the suppliers of
elephant specimens or images used here, including Thomas Hildebrandt, Guido Fritsch,
ZSL Whipsnade Zoo, John Cracknell (Longleat Safari Park), and Drs Daniela Denk and
Mark Stidworthy (IZVG Pathology, UK). Finally, we thank two anonymous reviewers for
their helpful comments on a previous version of this manuscript.
ADDITIONAL INFORMATION AND DECLARATIONS
Funding
This research was funded by BBSRC grants BB/H002782/1 (to JRH and RW) and
BB/C516844/1 (to JRH). The funders had no role in study design, data collection and
analysis, decision to publish, or preparation of the manuscript.
Regnault et al. (2017), PeerJ, DOI 10.7717/peerj.2877 17/21
Grant Disclosures
The following grant information was disclosed by the authors:
BBSRC grants: BB/H002782/1, BB/C516844/1.
Competing Interests
John R. Hutchinson is an Academic Editor for PeerJ.
Author Contributions
Sophie Regnault and Jonathon J.I. Dixon conceived and designed the experiments,
performed the experiments, analyzed the data, wrote the paper, prepared figures and/or
tables, reviewed drafts of the paper.
Chris Warren-Smith conceived and designed the experiments, reviewed drafts of the
paper, development of pathology categorisation.
John R. Hutchinson conceived and designed the experiments, contributed
reagents/materials/analysis tools, wrote the paper, reviewed drafts of the paper.
Renate Weller conceived and designed the experiments, analyzed the data, contributed
reagents/materials/analysis tools, wrote the paper, reviewed drafts of the paper.
Animal Ethics
The following information was supplied relating to ethical approvals (i.e., approving body
and any reference numbers):
The work involved cadaveric material and/or CT scans from vertebrate animals,
euthanised for reasons unrelated to the study and subsequently donated to the RVC,
and did not require ethical approval.
Data Availability
The following information was supplied regarding data availability:
The raw data has been supplied as a Data S1.
Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
peerj.2877#supplemental-information.
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Supplementary resource (1)

... Many factors can cause foot disease in large mammals, but previous research in elephants has linked foot disease with obesity, space limitations and the time the animals spent walking or standing on hard (unnatural) surfaces (Csuti, Sargent & Bechert, 2001;Fowler & Mikota, 2006;Miller, Hogan & Meehan, 2016). Our prior studies proposed that elephants normally have high pressures laterally, on digits III-V (Panagiotopoulou et al., 2012(Panagiotopoulou et al., , 2016, congruent with where elephants tend to exhibit greater incidences of osteopathologies (Regnault et al., 2017). In contrast, there are almost no in vivo studies of locomotion in rhinoceroses (Alexander & Pond, 1992), in any aspects including the pressures experienced by the feet. ...
... In contrast, there are almost no in vivo studies of locomotion in rhinoceroses (Alexander & Pond, 1992), in any aspects including the pressures experienced by the feet. Based on the roughly equivalent occurrence of osteopathologies across rhinoceros digits II-IV (Regnault et al., 2017), we expect that pressures would be evenly distributed across these digits too, and for pressures to be low on the fat pad lobes, without the mediolateral asymmetry of pathologies or pressures observed in elephant feet. ...
... The latter study posited some biomechanical factors that may underlie foot pathologies, including toe horn-cracking, shearing forces on the middle toe, low friction causing low wear, and overgrowth of the middle toe horn, which could inspire future studies building on this one. Regardless, these patterns are opposite those tentatively identified for elephants sampled by Regnault et al. (2017)-they found no clear forefoot vs. hindfoot differences in osteopathologies despite some evidence for higher pressures on elephant forefeet (Panagiotopoulou et al., 2012(Panagiotopoulou et al., , 2016. It is tempting to speculate that the more similar morphology and presumably function of all four rhinoceros feet compared with the disparate morphology of elephant fore-feet vs. hindfeet may explain these discrepancies, but such speculations demand cautious future analysis. ...
Article
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White rhinoceroses (Ceratotherium simum) are odd-toed ungulates that belong to the group Perissodactyla. Being second only to elephants in terms of large body mass amongst extant tetrapods, rhinoceroses make fascinating subjects for the study of how large land animals support and move themselves. Rhinoceroses often are kept in captivity for protection from ivory poachers and for educational/touristic purposes, yet a detrimental side effect of captivity can be foot disease (i.e., enthesopathies and osteoarthritis around the phalanges). Foot diseases in large mammals are multifactorial, but locomotor biomechanics (e.g., pressures routinely experienced by the feet) surely can be a contributing factor. However, due to a lack of in vivo experimental data on rhinoceros foot pressures, our knowledge of locomotor performance and its links to foot disease is limited. The overall aim of this study was to characterize peak pressures and center of pressure trajectories in white rhinoceroses during walking. We asked two major questions. First, are peak locomotor pressures the lowest around the fat pad and its lobes (as in the case of elephants)? Second, are peak locomotor pressures concentrated around the areas with the highest reported incidence of pathologies? Our results show a reduction of pressures around the fat pad and its lobes, which is potentially due to the material properties of the fat pad or a tendency to avoid or limit "heel" contact at impact. We also found an even and gradual concentration of foot pressures across all digits, which may be a by-product of the more horizontal foot roll-off during the stance phase. While our exploratory, descriptive sample precluded hypothesis testing, our study provides important new data on rhinoceros locomotion for future studies to build on, and thus impetus for improved implementation in the care of captive/managed rhinoceroses.
... PSR, processusstyloideus radii; OCA, os carpi accessorium; OCR, os carpi radiale; OCP, oscarpaleprimum; PP, prepollex; I, first metacarpal bone; II, second metacarpal bone; III, third metacarpal bone; V, fifth metacarpal bone; S1, promimalsesamoid bone of the 1st digit; S2, medial proximal sesamoid bone of the 2nd digit. (Weissengruber et al., 2006a) Foot problems are a major cause of morbidity and mortality in elephants, but are underreported due to difficulties in diagnosis, particularly of conditions affecting the bones and internal structures (Regnault et al., 2017). Fowler (2001) while evaluating foot conditions of Asian and African elephants states that 50 % of captive elephants will suffer from foot problems at some point in their life and that untreatable foot infections and arthritis are the major reasons for euthanization. ...
... Computed Tomogaphy (CT) is applied in elephant foot post mortem studies. Regnault et al. (2017) evaluated postmortem computer tomographic (CT) scans of 52 feet from 21 elephants (seven African Loxodonta africana and 14 Asian Elephas maximus), describing both pathology and variant anatomy (including the appearance of phalangeal and sesamoid bones) that could be mistaken for disease. They found all the elephants in their study to have pathology of some type in at least one foot. ...
Chapter
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Elephants, the largest terrestrial mammals, are the representatives of the only surviving family of order Proboscidea, which once had more than 180 members. The current three extant species are declared as endangered by International Union for Conservation of Nature and Natural Resources. Although there is improved husbandry initiatives and advances in knowledge of veterinary care for these species, there remain several areas that continue to be obstacles to optimum welfare and hence conservation. The limbs of elephants reveal many peculiarities both in structure and in kinematic patterns. Foot problems are a major cause of morbidity and mortality in elephants, but are underreported due to difficulties in diagnosis, particularly of conditions affecting the bones and internal structures. Diagnostic imaging creates the visual representations of internal structures of body. In elephants, these imaging which see the unseen helps in detecting the disease conditions or defects in feet and associated structures even at a very early stage, when there is no clinical 153 manifestation or the disease is undetected by the conventional methods of investigations. The era of diagnostic imaging started with the invention of X-ray and moved ahead thorough advances like Computed Radiography (CR), Direct Digital Radiography (DDR), Computed Tomography (CT), Magnetic Resonance Imaging (MRI), and Infrared Thermography (IRT). Some of them are of use in clinical practice for disease diagnosis in foot problems in elephants, while others help in research to understand normal anatomy and its deviations, pathological conditions, evaluation of husbandry practices etc. The future of diagnostic imaging made a quantum leap with the invention of 3D x-ray in humans, but still more researches need for its suitability animals. This doctoral seminar covers the current advances in diagnostic imaging with special emphasis to elephant feet.
... PSR, processusstyloideus radii; OCA, os carpi accessorium; OCR, os carpi radiale; OCP, oscarpaleprimum; PP, prepollex; I, first metacarpal bone; II, second metacarpal bone; III, third metacarpal bone; V, fifth metacarpal bone; S1, promimalsesamoid bone of the 1st digit; S2, medial proximal sesamoid bone of the 2nd digit. (Weissengruber et al., 2006a) Foot problems are a major cause of morbidity and mortality in elephants, but are underreported due to difficulties in diagnosis, particularly of conditions affecting the bones and internal structures (Regnault et al., 2017). Fowler (2001) while evaluating foot conditions of Asian and African elephants states that 50 % of captive elephants will suffer from foot problems at some point in their life and that untreatable foot infections and arthritis are the major reasons for euthanization. ...
... Computed Tomogaphy (CT) is applied in elephant foot post mortem studies. Regnault et al. (2017) evaluated postmortem computer tomographic (CT) scans of 52 feet from 21 elephants (seven African Loxodonta africana and 14 Asian Elephas maximus), describing both pathology and variant anatomy (including the appearance of phalangeal and sesamoid bones) that could be mistaken for disease. They found all the elephants in their study to have pathology of some type in at least one foot. ...
Book
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We are extremely glad to present the book "Reviews of veterinary research-what next?" to our professional community of researchers across the world. It is our humble effort to throw some light on what happens in veterinary research. Research is a critical component in advancement of our scientific knowledge and it is never ending. Research always builds upon future needs and with the strong foundation from past achievements. Veterinary research, most of the time, doesn't limit itself to veterinary medicine, care, treatment or conservation but transcends species boundaries. For example, study about wildlife diseases may be beneficial to conservation in the first hand, but will be helpful to figure out the genesis of zoonotic diseases and even pandemics that surfaces unexpectedly. In this context, at the end of the day, it even contributes the human wellbeing. We have to set priorities for research on a need based expansion of our knowledge to tackle issues in a scientific way. There are so many questions a researcher needs to answer before planning a research study. What was our past? Till where we reached? How far we have to go? What we have with us? What is the scope? And so on. To get a clear picture of this scenario, we have to review the past research. Such reviews will become the directions to future. In this book, we bring some meticulously done reviews about various emerging topics in veterinary field with universal relevance. The young researchers who contributed to this book keep these as base for their research and we can expect better outcome in the near future. This book intended not only to spread knowledge, but aims to develop a scientific temper, promote critical thinking and to help write in a scientific way. As editors, we were critical in our job, but the researchers' good intention, freedom of collection of information and expression in their own writing style in these reviews remains untouched. We blindly believe the contributors for the originality of their effort with a friendly gesture and hence, we editors, wish to inform that, any opinions made in these chapters are the sole responsibility of the contributors. We express sincere gratitude to our contributors, their mentors, guides and advisors for allowing the publication of their hard work. We extend our gratitude to the respective departments, institutions and universities who provide the best platform for these future researchers.
... The stress factors increase foot sole pressure or force area in mammals despite greater foot areas (Strickson et al., 2020). In wild animals, the feet adaptive response to stress are on a very narrow margin, therefore, captive animals kept on walking areas having pressures higher than normal create increased incidences of mechanically induced pathologies (Panagiotopoulou et al., 2019;Regnault et al., 2017). The distal phalanx of the adult chinkara was triangular, smaller than the other phalanxes. ...
Article
Full-text available
This study was designed to study gross morphological and basic osteometric features of the digit bones of Chinkara. The osteometry were performed manually through a digital vernier calliper on twenty (20) adult Chinkara (10 each male and females). The digits of Chinkara in each limb comprised the lateral and medial proximal, middle and distal phalanx. The first two phalanges were long bones. The shaft of the phalanx proximalis (P1) was thick proximally than distally and slightly arched. The phalanx media (P2) was shorter in length than the proximal. Its proximal articular surface was divided into two glenoid cavities "axial and abaxial' by a dorsopalmar ridge. The phalanx distalis (P3) was triangular, with four surfaces and six borders. The descriptive analysis indicates, no statistically significant (p>0.05) differences between the lateral and medial phalanges of all measured parameters. All the measured parameters for the digits of the forelimb were statistically significantly different (p>0.05) between male and female adult Chinkara except greatest Length (Lg) of the phalanx media of the forelimb. Similarly, significant differences (p>0.05) were present in all the studied parameters of the P1, P2 and P3 of the hindlimb except for maximum breadth of the shaft (Bs) of the P2.
... Particular attention in this study was devoted to abnormalities in skeletal remains of the Late Pleistocene megafauna, mainly woolly mammoth. To diagnose individual ages and pathological changes in animals, published sources on normal bone morphology and skeletal system diseases for modern and Pleistocene large mammals, including humans, were used (Logginov, 1890;Rokhlin et al., 1934;Bick and Copel, 1951;Chepurov et al., 1955;Kovalskiy, 1974;Baryshnikov et al., 1977;Nordin, 1997;Kuzmina and Maschenko, 1999;Lister, 1999;Zatsepin, 2001;Maschenko, 2002;Rothschild and Martin, 2003;Laub, 2006, 2008;Haynes and Klimowicz, 2015;Regnault et al., 2017). Our own research and its results were also taken into account (Leshchinskiy, 2006(Leshchinskiy, , 2009(Leshchinskiy, , 2012(Leshchinskiy, , 2015(Leshchinskiy, , 2017. ...
Article
The latest data on holes in the spinous processes of the vertebrae of woolly mammoths, a rare pathology, are presented. This was identified at 19 sites of northern Eurasia. Such destructive changes are recorded ca. 34–12k 14C a bp, and only two sites dated to >50k and >41k 14C a bp. The main hypotheses about hole formation are: vertebral abnormalities; bone infections; genetic traits; and unfavourable geochemical environment. The pathology occurred in mammoths of all age groups, and could have arisen at the embryonic stage. There are two types: classic holes associated with osteolytic changes; and very rarely tumour‐like lesions. The most likely cause of the lesions is alimentary osteodystrophy caused by chronic mineral starvation. The aetiology of this disease is usually associated with a deficiency or excess of macro‐ and microelements in the geochemical landscape, and through forage and water this leads to a severe metabolic disorder. Analysis of palaeopathological data shows two waves of geochemical stress in animals, ca. 26–18k and ca. 16–12k 14C a bp. Therefore, the woolly mammoth extinction can be viewed as a non‐linear function, with two peaks of high mortality corresponding to the Last Glacial Maximum and the Lateglacial.
... In megafauna, foot pressures in wild animals seem to be near their limits, and captive animals show increased incidences of mechanically induced pathologies (e.g. osteoarthritis) in regions where pressures are normally high during walking (Panagiotopoulou et al., 2012(Panagiotopoulou et al., , 2016(Panagiotopoulou et al., , 2019Regnault et al., 2013Regnault et al., , 2017. ...
Article
Full-text available
Giant land vertebrates have evolved more than 30 times, notably in dinosaurs and mammals. The evolutionary and biomechanical perspectives considered here unify data from extant and extinct species, assessing current theory regarding how the locomotor biomechanics of giants has evolved. In terrestrial tetrapods, isometric and allometric scaling patterns of bones are evident throughout evolutionary history, reflecting general trends and lineage-specific divergences as animals evolve giant size. Added to data on the scaling of other supportive tissues and neuromuscular control, these patterns illuminate how lineages of giant tetrapods each evolved into robust forms adapted to the constraints of gigantism, but with some morphological variation. Insights from scaling of the leverage of limbs and trends in maximal speed reinforce the idea that, beyond 100–300 kg of body mass, tetrapods reduce their locomotor abilities, and eventually may lose entire behaviours such as galloping or even running. Compared with prehistory, extant megafaunas are depauperate in diversity and morphological disparity; therefore, turning to the fossil record can tell us more about the evolutionary biomechanics of giant tetrapods. Interspecific variation and uncertainty about unknown aspects of form and function in living and extinct taxa still render it impossible to use first principles of theoretical biomechanics to tightly bound the limits of gigantism. Yet sauropod dinosaurs demonstrate that >50 tonne masses repeatedly evolved, with body plans quite different from those of mammalian giants. Considering the largest bipedal dinosaurs, and the disparity in locomotor function of modern megafauna, this shows that even in terrestrial giants there is flexibility allowing divergent locomotor specialisations.
... Other osteopathology is rarely diagnosed antemortem because neither magnetic resonance imaging (MRI) nor CT are logically possible, and two orthogonal views cannot be achieved with conventional radiography for interphalangeal joints. 20,24,25 because of superimposition owing to the anatomy of the elephant foot. Diagnostic accuracy and severity assessment of bone pathology from radiographs require high levels of experience from the viewing clinician. ...
Article
Diagnosis of foot disease in elephants is challenging. Owing to their large size, the available diagnostic tools and the expense of imaging are diagnostically limiting. Stereoradiography is the preparation of paired radiographs that form a three-dimensional (3D) image when viewed stereoscopically. Clinicians and veterinary students graded osteoarthritis in the feet of African (Loxodonta africana) and Asian (Elephas maximus) elephants taken postmortem with standard 2D radiographs, as well as 3D stereoradiographs. These gradings were compared with the actual gross pathology identified in the specimens. Although veterinary students diagnoses were no better than chance from 2D radiographs, 83.6% of the students could correctly differentiate severity between joints on stereoradiography; this is an absolute improvement of 30.1% (95% confidence interval [CI] = 19.6%-40.6%). Overall, participants were 27.4% (95% CI = 18.4%-36.3%) more successful at diagnosing pathology on stereoradiographs. Half of participants were shown standard 2D radiographs first, the others stereoradiographs first, but the difference in gradings between the two groups was not statistically significant. Stereoradiography appears to hold the potential to improve diagnosis of osteoarthritis in elephant feet, particularly by less experienced clinicians, and the technique is low-cost and applicable under field conditions.
... Larger enclosures and more time spent outside and on naturalistic, soft surfaces (e.g. grass) were also correlated with better foot health, an area of particular concern for elephants [21][22][23]. ...
Article
Full-text available
African elephants, the largest land animal, face particular physiological challenges in captivity and the wild. Captive elephants can become over- or under-conditioned with inadequate exercise and diet management. Few studies have quantified body composition or water turnover in elephants, and none to date have examined longitudinal responses to changes in diet or air temperature. Using the stable isotope deuterium oxide (2H2O), we investigated changes in body mass, estimated fat-free mass (FFM, including fat-free gut content) and body fat in response to a multi-year intervention that reduced dietary energy density for adult African elephants housed at the North Carolina Zoo. We also examined the relationship between air temperature and water turnover. Deuterium dilution and depletion rates were assayed via blood samples and used to calculate body composition and water turnover in two male and three female African elephants at six intervals over a 3-year period. Within the first year after the dietary intervention, there was an increase in overall body mass, a reduction in body fat percentage and an increase in FFM. However, final values of both body fat percentage and FFM were similar to initial values. Water turnover (males: 359 ± 9 l d−1; females: 241 ± 28 l d−1) was consistent with the allometric scaling of water use in other terrestrial mammals. Water turnover increased with outdoor air temperature. Our study highlights the physiological water dependence of elephants and shows that individuals have to drink every 2–3 days to avoid critical water loss of approximately 10% body mass in hot conditions.
... Similar results were found in the post-mortem examintation of 21 elephants (seven African Loxodonta africana and 14 Asian Elephas maximus), describing both pathology and variant anatomy. The most common pathological changes observed were bone remodelling, aging and Degenerative joint disease (Regnault et al., 2017). ...
... Localised foot pressures in large bodied animals may result in foot pathologies such as inflammation, enthesopathies, cracks, defects and horn growth that could impact the animals' health and ability to locomote effectively e.g. [50][51][52] . Although many factors likely contribute to foot pathologies, exposure to hard surfaces (asphalt, concrete) can further compromise the effectiveness of the fat pad and accelerate these pathologies [53][54][55] . ...
Article
Full-text available
From the camel’s toes to the horse’s hooves, the diversity in foot morphology among mammals is striking. One distinguishing feature is the presence of fat pads, which may play a role in reducing foot pressures, or may be related to habitat specialization. The camelid family provides a useful paradigm to explore this as within this phylogenetically constrained group we see prominent (camels) and greatly reduced (alpacas) fat pads. We found similar scaling of vertical ground reaction force with body mass, but camels had larger foot contact areas, which increased with velocity, unlike alpacas, meaning camels had relatively lower foot pressures. Further, variation between specific regions under the foot was greater in alpacas than camels. Together, these results provide strong evidence for the role of fat pads in reducing relative peak locomotor foot pressures, suggesting that the fat pad role in habitat specialization remains difficult to disentangle.
Article
Full-text available
For more than three decades, foot and musculoskeletal conditions have been documented among both Asian [Elephas maximus] and African [Loxodonta africana] elephants in zoos. Although environmental factors have been hypothesized to play a contributing role in the development of foot and musculoskeletal pathology, there is a paucity of evidence-based research assessing risk. We investigated the associations between foot and musculoskeletal health conditions with demographic characteristics, space, flooring, exercise, enrichment, and body condition for elephants housed in North American zoos during 2012. Clinical examinations and medical records were used to assess health indicators and provide scores to quantitate conditions. Using multivariable regression models, associations were found between foot health and age [P value = 0.076; Odds Ratio = 1.018], time spent on hard substrates [P value = 0.022; Odds Ratio = 1.014], space experienced during the night [P value = 0.041; Odds Ratio = 1.008], and percent of time spent in indoor/outdoor exhibits during the day [P value < 0.001; Odds Ratio = 1.003]. Similarly, the main risk factors for musculoskeletal disorders included time on hard substrate [P value = 0.002; Odds Ratio = 1.050] and space experienced in indoor/outdoor exhibits [P value = 0.039; Odds Ratio = 1.037]. These results suggest that facility and management changes that decrease time spent on hard substrates will improve elephant welfare through better foot and musculoskeletal health.
Article
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Individual elements of many extinct and extant North American rhinocerotids display osteopathologies, particularly exostoses, abnormal textures, and joint margin porosity, that are commonly associated with localized bone trauma. When we evaluated six extinct rhinocerotid species spanning 50 million years (Ma), we found the incidence of osteopathology increases from 28% of all elements of Eocene Hyrachyus eximius to 65-80% of all elements in more derived species. The only extant species in this study, Diceros bicornis, displayed less osteopathologies (50%) than the more derived extinct taxa. To get a finer-grained picture, we scored each fossil for seven pathological indicators on a scale of 1-4. We estimated the average mass of each taxon using M1-3 length and compared mass to average pathological score for each category. We found that with increasing mass, osteopathology also significantly increases. We then ran a phylogenetically-controlled regression analysis using a time-calibrated phylogeny of our study taxa. Mass estimates were found to significantly covary with abnormal foramen shape and abnormal bone textures. This pattern in osteopathological expression may reflect a part of the complex system of adaptations in the Rhinocerotidae over millions of years, where increased mass, cursoriality, and/or increased life span are selected for, to the detriment of long-term bone health. This work has important implications for the future health of hoofed animals and humans alike.
Book
Elephants are possibly the most well-known members of the animal kingdom. The enormous size, unusual anatomy, and longevity of elephants have fascinated humans for millenia. Biology, Medicine, and Surgery of Elephants serves as a comprehensive text on elephant medicine and surgery. Based on the expertise of 36 scientists and clinical veterinarians, this volume covers biology, husbandry, veterinary medicine and surgery of the elephant as known today. Written by the foremost experts in the field. Comprehensively covers both Asian and African elephants. Complete with taxonomy, behavioral, geographical and systemic information. Well-illustrated and organized for easy reference.
Chapter
What makes so many animals, living and extinct, so popular and distinct is anatomy; it is what leaps out at a viewer first whether they observe a museum’s mounted Tyrannosaurus skeleton or an elephant placidly browsing on the savannah. Anatomy alone can make an animal fascinating — so many animals are so physically unlike human observers, yet what do these anatomical differences mean for the lives of animals?