Radiographic findings in several joints of nine bears

Institut für Genetik, Ernährung und Haltung von Haustieren der Vetsuisse-Fakultät der
Universität Bern, Abteilung Tierhaltung und Tierschutz
(Leiter: Prof. Dr. A. Steiger)
Zoo Basel
(Direktor: Dr. O. Pagan)
Departement für klinische Veterinärmedizin, Abteilung für bildgebende Verfahren der
Vetsuisse-Fakultät der Universität Bern
(Leiter: Prof. Dr. J. Lang)
Arbeit unter der Leitung von
Dr. C. Wenker und Dr. U. Geissbühler
Symptoms, radiographic examinations and pathologies:
development of a scoring system to evaluate physical condition
and quality of life in geriatric zoo mammals
Inaugural-Dissertation
zur Erlangung der Doktorwürde
der Vetsuisse-Fakultät der Universität Bern
vorgelegt von
Jérôme Föllmi
von Genf-Stadt, GE
2005

Von der Vetsuisse-Fakultät der Universität Bern auf Antrag
von Prof. Dr. A. Steiger als Dissertation genehmigt.
Bern, Der Dekan der
Vetsuisse-Fakultät der Universität Bern
3

Table of contents
Summary 7
I. A scoring system to evaluate physical condition and
quality of life in geriatric zoo mammals 11
Summary 11
Résumé 12
Introduction 12
Animals, Materials and Methods 13
Animals 13
Symptoms 13
Retrospective and prospective cases 14
Age 14
Pathologies 14
Evaluation of pain, discomfort and quality of life 15
Scoring system 15
Statistics 15
Table scoring system 18
Results 21
Symptom and pathology 21
Age and pathology 22
Radiographic examination of living animals 22
Evaluation of pain, discomfort and quality of life 23
Scoring system 23
Discussion 24
Acknowledgements 26
References 26
Figure 1 29
Figure 2 29
Figure 3 29
Figure 4 30
Figure 5 30
Figure 6 30
Figure 7 31
Figure 8 31
Figure 9 31
II. Radiographic findings in several joints of nine bears 35
Summary 35
Résumé 36
Introduction 36
Material and Methods 36
Results 39
Discussion 40
Acknowledgments 41
References 41
Figure 1 43
Figure 2 43
Figure 3 44
Figure 4 44
Figure 5 45
Figure 6 45
III. Remerciements 47
5

Summary
Nowadays, the longevity of captive zoo animals has been increasing. Consequently, agerelated
diseases are becoming more common. The diagnosis and the treatment can be difficult,
so welfare might be compromised. The aim of this study was to improve decision making for
euthanasia in geriatric zoo animals at an appropriate time using a scoring system.
The first paper “A scoring system to evaluate physical condition and quality of life in
geriatric zoo mammals” deals with the decision to perform euthanasia by means of a scoring
system. This scoring system was created with the aid of medical records, necropsy reports,
evaluation of pain, discomfort and quality of life of 60 retrospective cases and 10 prospective
cases of old zoo mammals belonging to 24 different species in five European zoos. A
radiographic examination of the 10 prospective cases was included. It was found that 79.3%
of animals with an age equal or superior to 100% of the life span in the wild suffered from
dysfunction of the musculoskeletal system (41.4%) or had developed neoplasia (37.9%). This
scoring system utilizes the age, symptoms, therapy, evaluation of pain, discomfort and quality
of life, radiological examination and the importance of the genetical value of the animal.
The paper will be submitted to Animal Welfare. The study will be submitted as a
presentation at the meeting of the European Association of Zoo and Wildlife Veterinarians in
Budapest, Hungary, in May 2006.
The second paper “Radiographic findings in several joints of nine bears” deals with the
alterations of joints in nine bears (brown bear, Ursus arctos; black bear, Ursus americanus;
polar bear, Ursus maritimus; sun bear, Helarctos malayanus). Radiographs of the elbows,
hips, stifles and tarsal joints were performed. The radiographs were scored according to the
presence of signs of osteoarthritis. All bears without and with gait abnormality showed
osteoarthritic changes in their joints. Not only the age seem to be responsible for these
osteoarthritic changes, but the nutrition and / or the enclosures could play a role. We would
like to continue to make radiographic examinations of bears and to try to find a correlation
between nutrition, ground of enclosures and osteoarthritic changes. The results of this study
was used for the part “radiographic examination” of the scoring system of the first paper.
The paper will be submitted to Veterinary Radiology &Ultrasound. The study will be
presented at the joint scientific conference of the International Veterinary Radiology
Association in Vancouver, Canada, in August 2006.
7

Part I
A scoring system to evaluate physical condition and
quality of life in geriatric zoo mammals
9

A SCORING SYSTEM TO EVALUATE PHYSICAL CONDITION AND
QUALITY OF LIFE IN GERIATRIC ZOO MAMMALS
J Föllmi 1 , A Steiger 1 , C Walzer 2 , N Robert 3 , U Geissbühler 4 , M G Doherr 5 and C Wenker 6
1 Institute of Animal Genetics, Nutrition and Housing, Division of Animal Housing and
Welfare, Vetsuisse Faculty, University of Berne, Bremgartenstrasse 109a, CH 3001 Berne,
Switzerland
2Research Institute of Wildlife Ecology, University of Veterinary Medicine,
Savoyenstrasse 1, A 1160 Vienna, Austria
3Centre for Fish and Wildlife Health, Institute of Animal Pathology, Vetsuisse Faculty,
University of Berne, Länggassstrasse 122, CH 3001 Berne, Switzerland
4 Radiology Section, Department of Clinical Veterinary Medicine, Vetsuisse Faculty,
University of Berne, Länggassstrasse 124, CH 3001 Berne, Switzerland
5Department of Clinical Veterinary Science, Vetsuisse Faculty, University of Berne,
Bremgartenstrasse 109a, CH 3001 Berne, Switzerland
6Zoo Basel, Binningerstrasse 40, CH 4054 Basel, Switzerland
Correspondence: Jérôme Föllmi 1 , e-mail: jerome.foellmi@itz.unibe.ch
Tel: +41.31.305.90.50, Fax: +41.31.631.26.40
Keywords: euthanasia, geriatrics, pathology, scoring system, symptom, zoo mammals
Abstract
The decision to perform euthanasia in geriatric zoo mammals is usually a highly complex
procedure involving ethical, medical, emotional and sometimes political factors. However,
subsequent necropsies often show that the pathological changes of organs and / or the
musculoskeletal system are already advanced. Therefore we hypothesize that euthanasia is
often delayed to the detriment of the animal’s welfare. The purpose of this study was to
facilitate and establish an initial objective decision making framework for the euthanasia of
geriatric zoo mammals. A scoring-system to assess the physical condition and quality of life
in old zoo mammals is presented, based on retrospective and prospective investigation of 70
geriatric zoo mammals in five European zoos. Medical records and necropsy reports were
studied in retrospective cases. Symptoms were monitored and recorded in prospective cases.
Radiographic investigations under general anesthesia or at necropsy were performed
additionally. A significant association between symptoms and pathological findings revealed
that 63.1% of the examined animals (n = 41/65) had pathological alterations of the
musculoskeletal system (36.9%), or suffered from neoplasia (26.2%). Based on the individual
reports, 28 veterinarians from different fields of veterinary medicine concluded that these
animals had mild to severe pain, discomfort and a significantly reduced quality of life, thus
welfare was strongly reduced. The proposed scoring system includes all these factors and
offers a simple and reliable tool to support decision-making for euthanasia in geriatric zoo
mammals.
11

Mots-clé: euthanasie, gériatrie, mammifères de zoo, pathologie, scoring system, symptôme
Résumé
La décision d’effectuer une euthanasie d’un animal gériatrique est une procédure très
complexe incluant des facteurs éthiques, médicaux, émotionnels et parfois politiques.
Cependant, la nécropsie ultérieure de ces animaux met souvent en évidence des changements
pathologiques déjà bien avancés des organes et / ou du système locomoteur. C’est pourquoi
nous faisons l’hypothèse que l’euthanasie est souvent retardée au détriment du bien-être de
l’animal. Le but de cette étude est de faciliter et d’établir un cadre pour une décision initiale
objective lors d’euthanasie chez les animaux gériatriques. Un « scoring system » sur la
condition physique et la qualité de vie des vieux animaux de zoo y est présenté, basé sur une
investigation rétrospective et prospective sur 70 mammifères gériatriques de zoo dans cinq
zoos européens. Les dossiers médicaux et les rapports de nécropsie ont été étudiés pour les
cas rétrospectifs. Des symptômes ont été observés et archivés pour les cas prospectifs. Des
investigations radiographiques sous anesthésie générale ou avant nécropsie ont été effectuées
en plus. Une association significative entre les symptômes et les pathologies a révélé que
63.1% des animaux examinés (n = 41/65) présentaient des pathologies du système locomoteur
(36.9%) ou souffraient de néoplasie (26.2%). Sur la base de rapports individuels, 28
vétérinaires de différents domaines en médecine vétérinaire ont par ailleurs conclu que ces
animaux présentaient des douleurs et un inconfort allant de léger à sévère ainsi qu’une qualité
de vie significativement réduite, entraînant un bien-être fortement restreint de l’animal. Le
« scoring system » proposé inclut tous ces facteurs et offre un outil simple et efficace pour
soutenir la décision d’effectuer une euthanasie chez les mammifères gériatriques de zoo.
Introduction
In the last years of the 20 th century zoos became increasingly focused on conservation
(through captive breeding), research and education. This has been in part due to changing
public attitudes towards zoos and the appropriate methods of keeping wild animals in
captivity (Young 2003). In addition, the conditions of captivity of zoo animals have
improved and the animal longevity has been increased. As a result, problems arising from
the management of long-lived species and age-related diseases are increasing. Some of the
problems may be difficult to diagnose and treat, thereby potentially compromising animal
welfare (Kitchener 2004). In many cases, the subjects are apparently healthy, but old zoo
animals at necropsy are found to suffer from a range of health problems that may not have
been apparent when they were alive (Richardson 2000). Animals in captivity invariably live
longer than their wild counterparts (Nowak 1999; Richardson 2000; Erwin et al 2002).
Enabling zoo animals to live in better conditions for a long period is presently viewed as
important. However, zoos often unwittingly condemn their animals to long painful lives. In
some instance this may benefit the conservation of genetic lineages. However, in other
instances the already well-represented animal occupies much needed space well beyond
making a significant contribution to the breeding program. A good zoo strives to improve
the quality of its animals’ lives, not necessarily their length of life (Richardson 2001).
Suffering is an unpleasant state of mind that disrupts the quality of life. It is the mental
state associated with unpleasant experiences such as pain, malaise, distress, injury and
emotional numbness (Gregory 2004). In the present study we focused on pain, because pain,
probably more than any other state, directly reduces welfare (Duncan 2004).
Generally, it is very difficult to determine the appropriate time when to perform
euthanasia. Besides the medical aspect, the zoo veterinarian must take into consideration the
different interests of zoo managers and staff, visitors, animal welfare organizations, sponsors
and possibly the needs of the respective breeding programs (e.g. European Endangered
12

Species Program). The final decision to perform euthanasia is greatly influenced by the
general clinical condition of the animal. In this regard, the correct interpretation of clinical
symptoms in zoo animals plays a central role in the evaluation of the animal’s welfare.
Persistence of clinical signs in spite of medical treatment should rapidly give rise to
discussions on the future quality of life in the individual. In some cases a change of drug may
be helpful, sometimes a surgical intervention under general anesthesia may be indicated and
in other instances the decision for euthanasia must be taken. Treatment invariably raises many
questions about its efficacy, and each veterinarian must exercise the highest standards of
animal welfare (EAZA 1999; WAZA 1999). Interventions invariably cause stress and are a
risk for the animals. Additionally, this mobilizes personnel and material, takes time, and
generates costs.
Based on the correlation of symptoms, professional perceptions and necropsy results
we propose an initial scoring-system to evaluate physical condition and quality of life in
geriatric zoo mammals, with the aim of improving the decision process for euthanasia at an
appropriate time.
Animals, Materials and Methods
Animals
This study included 70 old zoo mammals belonging to 24 different species (Table 1). Sixtyfive
animals died or were euthanized between 1979 and 2005 in five European zoos and five
animals were still alive at the time of manuscript submission. Only cases whose symptoms
(Table 2) were documented reliably and with pathological reports were chosen for this study.
Sixty animals were retrospective cases and 10 were prospective cases.
The age of the zoo animals is expressed in percentage of the reported maximal age in
the wild when available and of the maximal reported longevity in captivity. (Haltenorth 1977;
Grzimek 1993; Nowak 1999; Cat Specialist Group 2004; International Association for Bear
Research and Management 2004).
Symptoms
A variable factor of multiplication which depends on the frequency of the symptoms observed
is allocated in the scoring system. Frequency between 11% and 33% for each symptom
obtained a factor 2 (group 1), frequency between 5% and 6% for each symptom obtained a
factor 1.5 (group 2) and frequency between 1.0% and 4.5% for each symptom obtained a
factor 1 (group 3).
Table 2 The 18 symptoms observed in all animals, two symptoms observed only
in bears and three symptoms observed only in primates in this study.
All animals, including
Observations in bears Observations in
bears and primates
only
primates only
Vomiting Diarrhoea Reduced bathing Social pressure
Dysorexia Reluctance to move Increased bathing Bite wounds
Cachexia Pain when standing up Isolation from group
Anorexia Lameness
Weakness Muscle atrophy
Apathy Polydipsia/Polyuria
Dehydration Position in hierarchy ↓
Dyspnoea Hypersalivation
Coughing Recumbency
13

Retrospective and prospective cases
For the retrospective cases, the medical records of the participating zoos were used and
persons (veterinarians, keepers) involved in the care of the concerned animals were
interviewed to precisely define the symptoms, which the animals had shown before their
euthanasia or natural death. The symptoms, which were taken into consideration, were
defined as the predominating symptoms during the last year of life. In addition, the necropsy
report was analyzed for each case.
For the prospective cases, a similar procedure was performed in six bears (U. arctos,
U. maritimus), one giraffe (G. camelopardalis tippelskirchi), one okapi (O. johnstoni) and one
camel (C. bactrianus) (Table 3); symptoms were monitored, and, after euthanasia or death of
the animal, necropsy was performed either on site or at the Institute for Animal Pathology,
University of Berne. Each prospective case was examined radiographically, five of them in
general anesthesia including four adult brown bears (U. arctos) and one polar bear (U.
maritimus).
Prior to necropsies, postmortem radiographic examination (Siemens Polydoros 100
system, with a performance of 80 kW at 100 kV) was performed in four animals: one giraffe
(G. camelopardalis tippelskirchi), one okapi (O. johnstoni), one Bactrian camel (C.
bactrianus) and one brown bear (U. arctos).
Table 3 Symptoms of the prospective cases (n = 10) of this study
Animal Age Sex Symptom
Brown bear 29 Female mild to moderate weakness, mild lameness, mild
(U. arctos)
reluctance to move, mild dysorexia
Brown bear
(U. arctos)
Brown bear
(U. arctos)
Brown bear
(U. arctos)
Polar bear
(U. maritimus)
Sun bear
(H. malayanus)
Brown bear
(U. arctos)
Giraffe
(G. camelopardalis)
Okapi
(O. johnstoni)
Bactrian camel
(C. bactrianus)
23 Female severe lameness, severe reluctance to move, pain when
standing up, mild dysorexia, cachexia
33 Female mild lameness, stiff neck, mild dysorexia
33 Female gait abnormality, mild dysorexia
27 Male dysorexia, paraparesis
21 Male No clinical symptoms
28 Female severe lameness, severe reluctance to move
18 Female Moderate lameness, moderate reluctance to move
13 Female colic, dysorexia, reluctance to move, anorexia during
eight days
19 Female severe lameness, severe reluctance to move,severe pain
when standing up, moderate cachexia, moderate to
severe muscle atrophy
Pathologies
Pathological findings were classified per system or per organ including pancreas,
hepatobiliary system, musculoskeletal system, respiratory system, genital system, lymphatic
system, cardiovascular system, kidney and adrenal gland, gastrointestinal tract, skin, oral
diseases including teeth, and trauma. Pathologies were classified into three groups: neoplasia,
dysfunction of the musculoskeletal system and other pathologies (Table 4). Further, we
subdivided neoplasia into two groups: “neoplasia of visceral organs” and “neoplasia of non
14

visceral organs”. Neoplasia and dysfunctions of the musculoskeletal system were the most
common diseases recorded in our study.
Evaluation of pain, discomfort and quality of life
A data card was created for each animal (n = 65), including species, name, age, symptoms and
the diagnosed pathologies of the animal followed by three scales for evaluation of pain,
discomfort and quality of life (Table 5). Each scale was graduated from zero (no pain, no
discomfort, good quality of life) to ten (high level of pain, high level of discomfort, poor
quality of life). The sum of the three scales gave the general assessment factor (from 0 to 30).
Twenty-eight veterinarians evaluated these data cards. Groups were created according to the
specialty of each veterinarian: zoo veterinarians (n = 12), residents (n = 7) (two in clinic and
five in pathology), veterinary pathologists (n = 2), internists (n = 2), surgeons (n = 3) and
anesthetists (n = 2). Two data cards were double in each set of 65 cards to control the
objectivity of the veterinarians’ evaluation. No veterinarians were informed of these doubled
cards.
Scoring system
The proposed scoring system is based on the scoring system “4 a vet” (association 4avet)
created to evaluate pain in small companion animals which is used at the Veterinary Faculty
of the Berne University, and has been adapted to evaluate the physical condition and quality
of life in geriatric zoo mammals. It includes five parts (Table Scoring system). The first part is
the “history assessment” with age and clinical symptoms. The second part ”therapy” contains
the response on the therapy with specific and tentative therapy. The third part is the
“evaluation of pain, discomfort and quality of life”. The fourth part contains the “radiographic
examination”. The fifth part contains the “additional assessment” including breeding interest,
gender, ability to reproduce and hindrance of new breeder. In the result section we
differentiate the evaluation without or with “radiographic examinations”.
Statistics
Descriptive statistics include frequency tables, measures of central tendency and spread,
and the respective graphs. The association between the specific symptoms and
pathologies was assessed using cross-tabulation and the chi-square test or, when any of
the expected cell frequencies was below 5, the Fisher’s Exact test. In addition, odds
ratios (OR) with 95% confidence intervals were calculated. All statistical procedures
were performed with NCSS 2001 software (Number Cruncher Statistical Systems,
Kaysville, UT, USA) and Microsoft Excel. The overall level of statistical significance
was set to P < 0.05.
Table 4 Pathologies classified in three pathological groups found in different familiae of animals (n=65)
of this study
Familiae Neoplasia (n = 17) Dysfunction of the musculoskeletal
system (n = 24)
Other pathologies (n = 24)
Ursidae Hepatocellular carcinoma (n=1)
Pancreas adenocarcinoma (n=1)
Bile duct carcinoma and
adenocarcinoma of the
duodenum(n=1)
Arthrosis and spondylarthropathy,
moderate to severe (n=5)
15
Pancreas necrosis (n=1)
Myokardiose, severe (n=1)
Bronchopneumonie (n=1) Enteritis,
colitis and Glomerulonephritis
(n=1)

Familiae Neoplasia (n = 17) Dysfunction of the musculoskeletal
system (n = 24)
Felidae Pancreas adenocarcinoma with Arthrosis, severe (n=2)
metastasis (n=1)
Adenocarcinoma of the duodenum
(n=1)
Bile duct carcinoma (n=1)
Phaeochromozytom (n=1)
Chondroma (n=1)
Chondrofibrosarcoma with metastasis
(n=1)
Leiomyoma cervix (n=1)
Lymphosarcoma (n=1)
Leukose (n=1)
Squamous cell carcinoma of the
omentum (n=1)
Spondylarthropathy (n=2)
Canidae Haemangiosarcoma (n=1) Spondylarthropathy (n=1)
Other pathologies (n = 24)
Infarction (n=1)
Perforation of the stomach (n=1)
Pyelonephritis (n=1)
Necrotizing Hepatitis (n=1)
Camelidae Cholangiocarcinoma (n=1) Arthrosis, moderate to severe (n=3) Sand impaction (n=1)
Giraffidae Fracture, distal phalanx (n=2) Kidney infarct (n=1)
Deformation of claws (n=1) Congestion of the abomasum(n=1)
Elephantidae Arthritis, severe (n=1)
Equidae Trauma of the cannon bone(n=1)
Laminitis (n=1)
Fracture of the pelvis (n=1)
Tapiridae Anomaly of teeth, severe (n=1)
Pneumonia, severe (n=1)
Rhinocerotidae Arthrosis, moderate to severe (n=2) Pancreatitis (n=1)
Sand impaction (n=1)
Moschidae Adenocarcinoma of the ileum (n=1)
Bovidae Arthrosis, severe (n=1) Bronchopneumonia, severe (n=2)
Cebidae Squamous cell carcinoma of the
stomach (n=1)
Fracture, distal phalanx (n=1) Infected skin lesion (n=1)
Cercopithecidae Bite wounds (n=1)
Colitis, chronic (n=1)
Gingivitis and periodonditis,
chronic (n=1)
Hernia (n=1)
Amyloidosis of the liver (n=1)
Hepatitis (n=1)
16

Table 5 Animal card filled out by veterinarian for each retrospective and prospective cases (n = 65) to evaluate
pain, discomfort and quality of life with the aid of observed symptoms and pathologic findings by animals
N°Ref.: ________________ Name: ______________
Species: __________ Sex: ______________
Age: ________________
Symptom
Vomiting Dehydration Reluctance to move Isolation from the group Recumbency
Dysorexia Dyspnoea Pain when standing up Social pressure
Cachexia Coughing Lameness Bite wounds
Anorexia Diarrhoea Muscle atrophy Influenced by the season
Weakness Bathing ↑ Polydipsia/Polyuria Spring/Summer
Apathy Bathing ↓ Hierarchy↓ Autumn/Winter
Pathology
Pancreas Respiratory System Kidney & Adrenal gland
Pancreas adenocarcinoma Bronchopneumonia Chronic nephritis
Pancreas necrosis _____________________________ Pyelonephritis
__________________________________ Phaeochromozytom
__________________________________ Trauma ________________________________
_____________________________ ________________________________
Hepathobiliary system _____________________________
Hepatocellular carcinoma Gastrointestinal tract
Hepatitis Oral diseases Squamous cell carcinoma stomach
Cyst Abscess Adenocarcinoma of duodenum
Bile duct carcinoma Periodontitis Colitis
Cholangiocarcinoma Anomaly of teeth Gastritis
__________________________________ _____________________________ Perforation of stomach
__________________________________ _ Squamous cell carcinoma omentum
________________________________
Musculoskeletal System Genital System ________________________________
Arthrosis Leiomyoma of cervix
Spondyloarthropathy Skin
Arthritis Lymphatic System Infected skin lesion
Erosion Leucosis ________________________________
Synovialitis Lymphosarcoma ________________________________
Fracture _____________________________
Chondrofibrosarcoma
Chondroma Cardiovascular System
Deformation of claws Cardiac insufficiency
Laminitis Haemangiosarcoma
_________________________________ Infarction
_________________________________ _____________________________
_________________________________ _____________________________
_________________________________
Evaluation
Scale is graduated from 0 to 10. 0 = no, 5 = moderate und 10 = high, severe
0_____1_____2_____3_____4_____5_____6_____7_____8_____9_____10
Pain 0___________________________________________________________10
Discomfort 0___________________________________________________________10
Quality of life good___________________________________________________________very bad
17
Fiche/JF-Diss-ZooBasel

Scoring system to evaluate physical condition and quality of life
in old zoo mammals
Animal: Species:
Age: Maximal age in the wild:
HISTORY ASSESSMENT
Age 100% corresponds to the maximal age estimated for an animal in the wild
< 80% – 2
80–100% – 1
101–120% +2
>120% +4
Symptom Scale is graduated from 0 to 10 0 = no symptoms and 10 = severe symptoms
EXAMPLE
Cardinal symptoms yes /no If yes, severity points
Vomiting
1cm = 1; here 3.6cm = 3.6
During the last two months
Cardinal symptoms yes /no If yes, severity
Other symptoms yes /no If yes, severity
Date
0 10
Score
Points
✕2
Points
Vomiting 0 10 ✕2
Dysorexia 0 10 ✕2
Anorexia 0 10 ✕2
Cachexia 0 10 ✕2
Lameness 0 10 ✕2
Diarrhoea 0 10 ✕1.5
Polydipsia/Polyuria 0 10 ✕1.5
Dyspnoea 0 10 ✕1
Coughing 0 10 ✕1
Bite wounds 0 10 ✕1
Social pressure 0 10 ✕1
Isolation from group 0 10 ✕1
Other: 0 10 ✕1
Other: 0 10 ✕1
Total
Points
Apathy 0 10 ✕2
Pain when standing up 0 10 ✕2
Reluctance to move 0 10 ✕2
Weakness 0 10 ✕2
Muscle atrophy 0 10 ✕1.5
Position in hierarchy 0 10 ✕1.5
Dehydratation 0 10 ✕1
Bathing 0 10 ✕1
Bathing 0 10 ✕1
Other: 0 10 ✕1
Other: 0 10 ✕1
18
Total
Subtotal 1
© jföllmi_ZooBasel

THERAPY
Specific therapy yes yes, go to next two questions
no no, go to tentative therapy
Scale is graduated from 0 to 10 0=good, yes and 10=bad, no
Efficiency of the treatment was 0 10 ✕1
After the treatment, did the
symptoms disappear?
0 10 ✕1
Tentative therapy yes /no yes, go to next two questions
Efficiency of treatment was 0 10 ✕1
After the treatment, did the 0 10 ✕1
symptoms disappear?
EVALUATION
Evaluation of Pain 0 10 ✕1
Evaluation of Quality of life 0 10 ✕1
Evaluation of Discomfort 0 10 ✕1
RADIOGRAPHIC EXAMINATION
Scale is graduated from 0 to 10 0=no, good and 10=severe, bad
Examination yes /no yes, go to next question
Subtotal 2
Subtotal 3
Elbow joint, left 0 none +5 mild +10 moderate/severe signs of alterations
Elbow joint, right 0 none +5 mild +10 moderate/severe signs of alterations
Hip joint, left 0 none +5 mild +10 moderate/severe signs of alterations
Hip joint, right 0 none +5 mild +10 moderate/severe signs of alterations
Knee joint, left 0 none +5 mild +10 moderate/severe signs of alterations
Knee joint, right 0 none +5 mild +10 moderate/severe signs of alterations
Tarsal joint, left 0 none +5 mild +10 moderate/severe signs of alterations
Tarsal joint, right 0 none +5 mild +10 moderate/severe signs of alterations
Shoulder joint, left 0 none +5 mild +10 moderate/severe signs of alterations
Shoulder joint, right 0 none +5 mild +10 moderate/severe signs of alterations
Vertebrate column 0 none +5 mild +10 moderate/severe signs of alterations
Other: 0 none +5 mild +10 moderate/severe signs of alterations
Other: 0 none +5 mild +10 moderate/severe signs of alterations
19
Total
Subtotal 4
Score
Score
Score
© jföllmi_ZooBasel

ADDITIONAL ASSESSMENT
Breeding interest
Gender
Able to reproduce
Hinder the arrival of new breeder
RESULTS
yes –5
no +1
important –5
not important +1
yes –5
no +5
yes +5
no 0
Without «radiographic examination» Sum of the four subtotals
From 1 to 30 Treatment
From 31 to 51 Doubtful
Over 51 Euthanasia recommended
With «radiographic examination» Sum of the five subtotals
From 1 to 45 Treatment
From 46 to 66 Doubtful
Over 66 Euthanasia recommended
20
Subtotal 5
Score
© jföllmi_ZooBasel

Results
Symptoms and pathology
The symptoms included in group 1 (frequency between 11 and 33%) were shown in 95.7% of
the cases (n = 67/70). The animals showing one symptom 20% (n = 14/70), two symptoms
30% (n = 21/70), three symptoms 22.9% (n = 16/70) or four symptoms 11.4% (n = 8/70)
represented 84.3%. The animals showing either five symptoms (5.7%, n = 4/70), six
symptoms (4.3%, n = 3/70), seven symptoms (2.9%, n = 2/70) or eight symptoms (2.9%, n =
2/70) represented 15.7%. We found significant associations between five symptoms and five
pathologies (Table 6). In the following we will focus on the results of the five most frequently
observed symptoms.
Table 6 Observed symptoms significantly associated
with pathologic findings in this sample.
Symptoms Pathologies (p-value)
vomiting neoplasia P = 0.02
apathy neoplasia P = 0.007
anorexia neoplasia P = 0.01
lameness arthrosis P < 0.000001
pain when standing up spondyloarthropathy P = 0.009
Vomiting
In this sample vomiting was observed in bears, in felids and in one tapir (T. terrestris). This
symptom was significantly associated with neoplasia (P = 0.02; OR = 6.2): 29.4% of all
animals with neoplasia (n = 5/17) but only 6.3% of all animals (n = 3/48) without tumors
vomited.
Anorexia
In this sample anorexia was observed in all species and was a consistent findings in bears and
felids (72.2%). This symptom was significantly associated with neoplasia (P = 0.01; OR =
4.3): 52.9% of all animals (n = 9/17) with neoplasia but 20.8% of all animals (n = 10/48)
without neoplasia showed anorexia.
Apathy
In this sample apathy was mainly observed in bears and felids (87.5%, n = 8/9) and was
significantly associated with neoplasia (P = 0.007; OR = 8.2): 35.3% of all animals (n = 6/17)
with neoplasia but only 6.3% of all animals (n = 3/48) without neoplasia showed apathy.
Lameness
In this sample lameness was the symptom with the highest observed frequency and was
recorded in all species. It was found in 37.1% of all studied animals (n = 26/70). Lameness
was significantly associated with dysfunction of the musculoskeletal system (P < 0.000001;
OR = 27.8) and arthrosis (P < 0.000001): 75% of all animals (n = 18/24) with dysfunction of
the musculoskeletal system but only 9.8% of all animals (n = 4/41) without dysfunction of the
musculoskeletal system showed lameness; 100% of all animals (n = 14/14) with arthrosis but
15.7% of all animals (n = 8/51) without arthrosis showed lameness.
Pain when standing up
In this sample we found a significant association between pain when standing up and
spondylosis / spondylarthrosis (P = 0.009; OR = 8.9): 62.5% of all animals (n = 5/8) with
spondylosis / spondylarthrosis but only 15.8% of all animals (n = 9/57) without spondylosis
showed pain when standing up.
21

Age and pathology
Animals with neoplasia represented 26.2% (n = 17/65) of the total set, animals suffering from
dysfunction of the musculoskeletal system represented 36.9% (n = 24/65) and animals
suffering from other diseases represented 36.9% (n = 24/65) (Table 7 and 8). In the group
“neoplasia” 50% of the animals (n = 5/10) with “neoplasia of visceral organ” and 87.5% of
the animals (n = 6/7) with “neoplasia of non visceral organ” had an age equal and superior to
100% of the life expectancy in the wild. In the group “other pathologies”, 100% of the
animals (n = 7/7) with an age equal or superior to 100% of the life expectancy in the wild
suffered either from dysfunction of the cardiovascular system or from dysfunction of the
kidneys or from the liver.
Table 7 Frequency of the three pathological groups of this study in correlation
with an age of animals ≥ 100% of the life expectancy in the wild (%) and in
correlation with an age ≥ 50% of the maximal age in captivity (%)
Pathologies Animals (n = 29) with an age Animals (n = 62) with an age ≥
≥ 100% of the life expectancy 50% of the maximal age in
in the wild (%)
captivity (%)
Neoplasia 36.6% 25.0%
Dysfunction of the
musculoskeletal system
39.0% 34.4%
Other pathologies 24.4% 40.6%
Table 8 Frequency of all animals of this study with the same group of pathology in
correlation with an age of animals ≥ 100% of the life expectancy in the wild (%) and
in correlation with an age ≥ 50% of the maximal age in captivity (%)
Pathologies Animals (n = 29) with an age ≥
100% of the life expectancy in the
wild (%)
All animals with neoplasia 73.3% 81%
All animals with dysfunction of
the musculoskeletal system
All animals with other
pathologies
75% 81.8%
60% 84.6%
Animals(n = 62) with an age ≥
50% of the maximal age in
captivity (%)
Radiographic examination of anesthetized animals
Four brown bears (U. arctos) and one polar bear (U. maritimus) showed mild lameness, gait
abnormalities or paraparesis, and one brown bear (U. arctos) showed severe lameness.
Radiographs showed none to mild osteoarthritic changes in the elbow joints of four bears. In
the brown bear (U. arctos) with severe lameness severe osteoarthritis was diagnosed in both
elbow joints. Concerning the hip joint, five bears with mild lameness showed none
radiographic alterations, and the radiographs of the brown bear (U. arctos) with severe
lameness revealed severe osteoarthritic alterations. The stifle joint in one brown bear (U.
arctos) was not examined. Three bears had mild to moderate osteoarthritis in the stifle joint
and the bear with severe lameness had moderate osteoarthritic changes. Furthermore, three
bears showed enthesiophytes in the right patella proximally. One bear showed enthesiophytes
in the left patella proximally and one other bear showed enthesiophytes in the left patella
proximally and distally. One stifle in a brown bear (U. arctos) with gait abnormalities showed
changes consistent with osteochondromatosis. The same bear showed an extraarticular bone
lesion consistent with an enostosis-like lesion in the tibia. Radiographs showed mild
22

osteoarthritic changes of the tarsal joint in three bears, mild to moderate osteoarthritic
alterations in four bears and in two bears moderate osteoarthritic changes. Two bears with
lameness and/or gait abnormalities showed enthesiophytes, one bear dorsally in the right
metatarsus and the other one in the plantar ligament. In one bear with lameness marked cufflike,
periarticular mineralizations were detected in the left tarsal joint (Table 9) (publication in
preparation).
Table 9 Radiographic examinations of anesthetized animals (n = 6) in this study
Joints Brown bear Brown bear Brown bear Brown bear Polar bear Malayan bear
Maxilla (inlet) x x x x
Mandible (inlet) x x x x x
Cervical vertebrae (ll) x x
Thoracal vertebrae (ll) x x
Thoraco-lumbar vertebrae (ll) x x x x
Lumbar vertebrae (ll) x x
Elbow left (ml) x x x x x
Elbow right (ml) x x x x x x
Elbow left (dp) x x x x x
Elbow right (dp) x x x x
Hip (vd) x x x x x x
Stifle left (ml) x x x x
Stifle right (ml) x x x x x
Stifle left (dp) x x
Stifle right (dp) x x
Tarsal left (ml) x x x x x x
Tarsal right (ml) x x x x x
Tarsal left (dp) x x x
Tarsal right (dp) x x
ll = latero-lateral; ml = medio-lateral; dp = dorso-palmar/-plantar; vd = ventro-dorsal
x = joint radiographed
Evaluation of pain, discomfort and quality of life
The scoring for pain, discomfort, quality of life and general assessment between the groups of
veterinarians differed. In the group “zoo veterinarians” the median score was 8 for pain (in a
scale from 1 to 10), 8 for discomfort (in a scale from 1 to 10), 8.5 for quality of life (in a scale
from 1 to 10) and 24 for the general assessment (in a scale from 0 to 30). The scores were
very similar in the group “pathologists” and in the group “residents” with a median score of 7
and 7.5 for pain; 8 and 8 for discomfort; 8 and 8.5 for quality of life; and 23 and 24 for the
general assessment, respectively. The scores obtained by the “internists”, “surgeons” and
“anesthetists” were 5, 6 and 6 for pain; equal with 7 for discomfort and quality of life, and 18,
19 and 18.5 for the general assessment, respectively.
In the group “zoo veterinarians” the control with the two double cards resulted with a low
variation of the evaluation of the general assessment with mean difference of 0.9. In the group
“residents” the mean difference is of 1.6, in the group “anesthetist” the mean difference is of
2.2 and in groups “pathologist”, “internists” and “surgeons” the mean difference is of 2.5.
Scoring system
The section “results of the scoring system” was established as follows: for each symptom
observed in an animal five points were allocated and multiplied with a variable factor (as
defined under “Symptoms”). An evaluation of the therapy could not be established in each
case. Therefore a mean value of five points was allocated for each question concerning
23

efficacy and disappearance of symptoms during treatment. The result of the zoo veterinarian
with the highest evaluation as well as of the zoo veterinarian with the lowest evaluation of
pain, quality of life and discomfort was used to calculate the mean for each animal. Minus
five points were allocated to the part “additional assessment”, and plus 15 points to the part
“radiographic examination”. A mean was calculated for each animal. On this basis, treatment
can be recommended when the obtained result lies between one to 30 points for result without
additional examination, and between one to 45 points with additional examination. The
prognosis is considered to be doubtful when the result lies between 31 to 51 or 46 to 66,
respectively. Euthanasia should be considered with a score over 51 or 66, respectively.
Discussion
The aim of this study was to develop a systematic approach to defining the appropriate time to
euthanize a geriatric zoo mammal. For this purpose, we studied retrospective and prospective
cases from five different European zoos in order to evaluate a correlation between symptoms
and pathologic findings. Additionally, 28 veterinarians evaluated pain, discomfort and quality
of life of these animals. Combining these results the study presents a scoring procedure to
allow the zoo veterinarian to evaluate the general condition of an old animal and if necessary
to support the decision for euthanasia.
In the geriatric zoo mammals, similar symptoms were described independently of the
zoo and of the species. Of the five predominant clinical symptoms, vomiting, anorexia and
apathy were significantly associated with neoplasia whereas lameness, pain when standing up
and anorexia were significantly associated with “dysfunction of the musculoskeletal system”.
These five symptoms were very frequent. Neoplasia was diagnosed in 26.2% of all examined
animals, but if we consider only the species from which life expectancy in the wild is known,
this value reached 37.9% (with an age equal or superior to 100% of the life expectancy in the
wild). Dysfunction of the musculoskeletal system was recorded in 36.9% of all examined
animals, but in 41.4% considering only species with known maximal age in the wild , and
other diseases were diagnosed in 36.9% of all examined animals, but this value diminished to
20.7% considering only species with known maximal age in the wild. The groups neoplasia
and dysfunction of the musculoskeletal system represented 63.1% of all animals in this study,
but this value reached 79.3% considering only species with known maximal age in the wild.
As far as neoplasia is concerned, it is known that age has an influence on the risk of
developing neoplasia (Kennedy & Strafuss 1976; Port et al 1981; Gage 1999; de Magalhaes &
Toussaint 2002; Nimmervoll et al 2005). The present study showed that an animal with
symptoms and with an age equal and superior to 100% of the maximal age reached in wild
animals had a probability of 33.3 % to develop neoplasia. In addition, tumors were either
malignant (82.3%, n = 14/17) and / or surgery was impossible due to their localization
(recurring leiomyoma of the cervix, chondroma of thoracic vertebra).
Old animals are often affected with dysfunctions of the musculoskeletal system (Jack
& Thacker 1985; George et al 1990; Canfield & Spencer 1993; Kompanje & Klaver 1998;
Kompanje et al 2000; Colman & Binkley 2002; Erwin et al 2002; Morbeck et al 2002;
Nichols & Zihlman 2002; Kitchener et al 2003, Kitchener 2004). Degenerative skeletal
lesions represent a major portion of old zoo mammal pathologies. In a study involving 27 bear
skeletons of different bear species that were about 15 years of age, 96% had evidence of
skeletal pathologies (Kitchener 2004). Lions (Panthera leo), tigers (Panthera tigris), gorillas
(Gorilla gorilla), orangutans (Pongo pygmeus), babirusas (Babyrousa babyrussa) and pygmy
hippos (Hexaprotodon liberiensis) suffer from similar problems as bears, but with varying
degrees (Kitchener 2004). The pathological alterations were considered significant and in
human terms these would be regarded as very painful (Kitchener 2003; Gregory 2004). In the
present study, animals suffering from arthrosis and / or spondylarthropathy represent 66.7%
(n = 16/24) of all animals with dysfunction of the musculoskeletal system. Lameness and
24

difficulty when standing up are significantly associated with arthrosis and spondylarthropathy,
implying that these animals have pain. In these cases treatment only has a palliative character.
As far as other pathologies are concerned, the results show that age has an influence
on the development of pathologies, such as, for instance, pancreas or liver necrosis,
dysfunction of the kidney or dysfunction of the cardiovascular system.
The median score for the general assessment of pain, discomfort and quality of life
was 24 (scale from 0 to 30) in the group “zoo veterinarians”. This means that the pathologic
findings were assumed by the veterinarians to be of moderate to severe clinical significance,
implying a high degree of pain, discomfort as well as a poor quality of life. The pathologists
and the residents made a similar estimation. The anesthetists, internists and surgeons had a
lower median score, equal to 18.5. A reason for this difference probably is that they are not
used to work with zoo or wild animals.
Thorough observation of the clinical signs is very important as they give significant
information about the general condition of the animal. When an old animal shows symptoms,
it is often too late for an effective treatment. Our study shows that an animal with an age equal
or superior to 100% of the maximum age in wild animals with one or more symptoms had a
poor prognosis. If a treatment turns out to be ineffective it should be stopped and euthanasia
considered, as the animal has a high (79.3% according to this study) risk to suffer from
neoplasia or a dysfunction of the musculoskeletal system.
Combining the results, a scoring system is proposed to evaluate the general condition
and the quality of life of geriatric zoo mammals. The scoring system includes five parts: the
first part refers to the “history assessment” with points attributed for age and for symptoms.
The symptoms have a variable factor of multiplication, which depends on the frequency of the
symptoms. This variable factor has been created in order to differentiate the value of the
symptom according to its frequency. The second part includes the “therapy” with points for
the efficacy of the treatment. For instance the treatment of neoplasia, osteoarthritis, chronic
nephritis, cardiac insufficiency or stomach perforation has a poor efficacy or are difficult to
apply. The third part refers to the “evaluation of pain, discomfort, and quality of life” and
represents a subjective evaluation performed by the examining veterinarian, based on the
observed symptoms, therapy, radiology, other potential information and on the experience of
the veterinarian. The fourth part involves the “radiographic examination”. In this part the
radiographic examination of the joints is included, considering that dysfunction of the
musculoskeletal system represents a major problem in geriatric animals (37%). Finally, the
fifth part refers to the “additional assessment” which includes further factors such as breeding
interest, gender, and ability to reproduce.
For the establishment of the section “results of the scoring system”, in the part “history
assessment” we allocated five points for each symptom observed. This value was defined due
to the fact that the degree of symptom was described with words and not with numbers in the
medical records. In all retrospective and prospective cases of this study, the efficacy and / or
response to treatment played an important role in the euthanasia decision. Consequently, in
the part “therapy” of the scoring system, five points were allocated for the efficacy of the
treatment and five points for the disappearance of symptoms. In the part “additional
assessment” an animal can receive positive or negative points depending, for example, on its
breeding interest or its gender. A proven breeder male black rhinoceros (D. bicornis), has
much more “value” than, for example, a male European wolf (C. lupus), which is over
represented in the population. In the part “radiographic examination” points were given based
on the type of alteration in a joint, the number of joints affected in each animal and the
localization in the joint.
The mean total score for each animal was 52.72. Therefore, based on this sample set
we would recommend euthanasia when the total score is over 51 points. An animal’s
prognosis with a score between 31 and 51 is considered doubtful. In this category we had few
animals (n = 5/65) which had treatment options and euthanasia might not have been justified
in this moment, for example a bear with colitis or a leopard with pyelonephritis. Therefore,
25

we cannot justify euthanasia in all cases with a score from 31 to 51 but we would suggest
treatment for all animals with a score below 30.
The scoring system was tested on nine animals for evaluation. Based on these results
five animals were euthanized. Three animals had a score between 67 and 102 without
radiographic examination and two animals had a score of 81 and 140 with radiographic
examination. Subsequent necropsy and pathologic findings proved that euthanasia was
justified in all five cases. Based on the results of the scoring system four animals are still
alive. Three animals have a score between 20 and 28 without radiographic examination. One
animal with a score of 42 without radiographic examination is in category “doubtful”. This
animal will be reevaluated on a regular basis.
In conclusion, a geriatric zoo mammal showing one or more of the described
symptoms has a reduced quality of life. With the support of the proposed scoring system, the
general condition of the old animal can be systematically and rapidly evaluated. Furthermore,
it allows evaluation of therapeutic efficacy at any stage. This scoring system provides a
decision aid to the veterinarian for appropriate euthanasia in geriatric zoo mammals.
Acknowledgements
The authors thank Prof. Jean-Michel Hatt, Zoo Zürich, Switzerland; Dr. Christelle Vitaud,
Safari Peaugres, France; Dr. Pierre Moisson and Dr. David Gomis, Zoo Mulhouse, France,
and Dr. Willi Häfeli, Tierpark Dählhölzli, Switzerland, for their contributions to this study.
We thank all the veterinarians who evaluated pain, discomfort and quality of life of the study
animals.
References
Bourne D and Boardman SI 2004 Consideration for pain management in ruminants.
European Association of Zoo- and Wildlife Veterinarians (EAZWV), Ebeltoft, Denmark pp
177-182.
Canfield PJ and Spencer AJ 1993 Secondary degenerative arthropathy (osteoarthrosis) of
the hip joints in aging, free-living koalas. Australian Veterinary Journal 70(10): 394-395
Colman RJ and Binkley N 2002 Skeletal aging in macaque monkeys. Interdisciplinary Top
Gerontology 31: 32-47
Cat Specialist Group 2004 http://lynx.uio.no/catfolk/
de Magalhaes JP and Toussaint O 2002 The evolution of mammalian aging. Experimental
Gerontology 37: 769-775
Duncan IJH 2004 Pain, fear and distress. Global conference on animal welfare: an OIE
initiative, Paris, France pp 163-178. World Organisation for Animal Health: Luxembourg
European Association of Zoos and Aquariums EAZA 1999 Code of ethics and animal
welfare.http://www.eazwv.org
Erwin JM, Hof PR, Ely JJ and Perl DP 2002 One gerontology: advancing understanding
of aging through studies of great apes and other primates. Interdisciplinary Top Gerontology
31: 1-21
26

Föllmi J, Wenker C, Steiger A, Geissbühler U (in preparation) Radiographic findings in
several joints of nine bears
Gage LJ 1999 Geriatric medicine in aged captive pinnipeds. International Association for
Aquatic Animal Medicine, Boston, USA pp 130-131.
George PO, Rajan A, Varkey CA, Balagopalan TP and Rajankutty K 1990 Osteoarthritis
in an elephant (Elephas Maximus Indicus). Journal of Veterinary and Animal
Sciences 21(1): 157-159
Gregory NG 2004 Physiology and behaviour of animal suffering. Oxford: Blackwell
publishing
Grzimek B 1993 Grzimeks Enzyklopädie des Tierreichs. München, Germany: Deutscher
Taschenbuch Verlag GmbH & Co. KG
Haltenorth T 1977 Säugetiere Afrikas und Madagaskars. BLV Verlagsgesellschaft.
München, Germany
International Association for Bear Research and Management (IBA) 2004
http://www.bearbiology.com
International Veterinary Information Service (www.ivis.org) 2002 A core curriculum for
professional education for management of animal pain.P.-M. J. Ludders JW, Robertson S,
Gaynor J, Hellyer PW, Wong P, and Barakatt C (eds)
Jack SW and Thacker HL 1985 Degenerative joint disease in a Nile hippopotamus.
American Veterinary Medical Association. Journal 187(11): 1235
Kennedy GA and Strafuss AC 1976 Multiple neoplasia in an aged cougar. Journal of zoo
Animal Medicine 7(1): 24-26
Kitchener AC 2004 The problems of old bears in zoos. International Zoo News 51(5): 282-
293
Kitchener AC, Kolter L and Brownstein D 2003 Problems with old bears in zoos. EEP
Yearbook 1999 / 2000 including Proceedings of the 17th EAZA Conference, Aalborg 19 - 24
September 2000 pp 625-628.
Kompanje EJO and Klaver PSJ 1998 Spondarthritis (spondyloarthropathy) and
osteoarthrosis in an old female sloth bear (ursus ursinus cuvier, 1823), a case report.
European Association of Zoo- and Wildlife Veterinarians (EAZWV), Chester, United
Kingdom pp 473 - 479.
Kompanje EJO, Klaver PSJ and de Vries GT 2000 Spondyloarthropathy and
osteoarthrosis in three indomalayan bears: ursus ursinus Cuvier, 1823, ursus thibetanus
Raffles, 1821, and ursus malayanus Shaw & Nodder, 1791 (Mammalia:Carnivora: Ursidae).
Contributions to Zoology 69(4)
Morbeck ME, Galloway A and Sumner DR 2002 Getting old at gombe: skeletal aging in
wild-ranging chimpanzees. Interdisciplinary Top Gerontology 31: 48-62
Nichols KA and Zihlman AL 2002 Skeletal and dental evidence of aging in captive western
lowland gorillas: a preliminary report. Interdisciplinary Top Gerontology 31: 22-31
27

Nimmervoll H, Eggenberger U and Robert N 2005 Metastazing mammary carcinoma and
nephrolithiasis in a Rothschild's giraffe (giraffa camelopardalis rothshildi). Erkrankungen der
Zootiere, Verhandlungsbericht des 42. Internationalen Symposiums über die Erkrankungen
der Zoo- und Wildtiere, Prague, Czech Republic pp 264. Institute for Zoo and Wildlife
Research: Berlin, Germany
Nowak RM 1999 Walker's Mammals of the world. 6th Edition. Baltimore, USA: The Johns
Hopkins University Press
Port CD, Maschgan ER, Pond J and Scarpelli DG 1981 Multiple neoplasia in a jaguar
(Panthera onca). Journal of Comparative Pathology 91(1): 115-122
Richardson DM 2000 Euthanasia: a nettle we need to grasp Bioparco Rome Zoo, Italy
Richardson DM 2001 Is management euthanasia a necessary tool for realising an
institutional or a regional collection plan? Bioparco Rome Zoo, Italy
World Association of Zoos and Aquariums WAZA 1999 Code of ethics and animal
welfare.http://www.waza.org
Young RJ 2003 Environmental enrichment for captive animals. UFAW Animal Welfare
Series, Oxford, UK: Blackwell Science
28

Pathologies of the group “Neoplasia”
Fig. 1. Polar bear (Ursus maritimus), 25 yr-old. Hepatocellular carcinoma.
Fig. 2a
Fig. 2 a and b. Brown bear (Ursus arctos), 32 yr-old. Adenocarcinoma of the
exocrine pancreas (red arrow) with severe dilation of the ductus choledocus and of
the gallbladder due to obstruction of the bile flow (white arrows).
Fig. 3a
Fig. 2b
Fig. 3b Fig. 3c
Fig. 3 a, b and c. Muskox (Ovibos moschatus), 15 yr-old. Ileal adenocarcinoma (red
arrow) with invasion into the wall of an artery (white arrow) and metastasis in the
ruminal serosa (green arrow).
29

Pathologies of the group “Dysfunction of the musculoskeletal system”
Fig. 4a
Fig. 4b Fig. 4c
Fig. 4 a, b and c. Brown bear (Ursus arctos), 28 yr-old. Fig. 4a: osteoarthrosis with loss of the
articular cartilage and presence of linear grooving in subchondral plate (arrow) of the processus
anconaeus. Fig. 4b: osteoarthrosis with focal-extensive loss of the articular cartilage of the distal
humerus (arrow). Fig. 4c: Degeneration of the intervertebral disk and sclerosis of the vertebral bone
(Th2-Th3).
Fig. 5a
Fig. 5b
Fig. 5c
Fig. 5 a, b and c. Leopard (Panthera pardus), 17 yr-old. Fig. 5a: osteoarthrosis with flattening of
the caput humeri. Osteophyte proliferation around caput humeri and in sulcus intertubercularis.
Fig. 5b: complete loss of articular cartilage and eburnification of the condylus lateralis and severe
deep linear grooving in the epiphyseal bone of the condylus medialis of the right humerus. Fig. 5c:
severe deep linear grooving and osteophyte proliferation of the ulna head with fracture of the
incisura trochlearis.
Fig. 6a Fig. 6b
Fig. 6c
Fig. 6 a, b and c. Giraffe (Giraffa camelopardalis), 18 yr-old. Third phalanx of the medial claw of the
right forelimb with articular fracture (arrows). 30

Pathologies of the group “Others pathologies”
Fig. 7a Fig. 7b
Fig. 7c
Fig. 7d
Fig. 8a
Fig. 8b
Fig. 7 a, b, c and d. Okapi, 13 yr-old. Fig. 7a: okapi
(Okapia johnstoni) with signs of colic. Fig. 7b:
impaction of the abomasum. Fig. 7c: dilation of
abomasum and of ostium omaso-abomasicum (white
arrows). Fig. 7d: obstruction in small intestine with
compacted food content.
Fig. 8 a and b. Crab-eating macaque (Macaca fascicularis), 20 yr-old. Liver, diaphragmatical and
visceral face, with cysts of ecchinococcus multilocularis.
Fig. 9a Fig. 9b
Fig. 9 a and b. Crab-eating macaque (Macaca fascicularis), 19 yr-old. Abdomen with
severe splenomegalie. Pale and firm liver due to chronic amyloidosis.
31

Part II
Radiographic findings in several joints of nine bears
33

Radiographic findings in several joints of nine bears
Jérôme Föllmi, Christian Wenker, Andreas Steiger, Urs Geissbühler
From the Institute of Animal Genetics, Nutrition and Housing, Division of Animal Housing
and Welfare (Jérôme Föllmi, Andreas Steiger) and from the Department of Clinical
Veterinary Medicine, Radiology Section (Urs Geissbühler), Vetsuisse Faculty, University of
Berne, Bremgartenstrasse 109a, CH 3001 Berne, Switzerland.
From Zoo Basel Binningerstrasse 40, CH 4011 Basel, Switzerland. (Christian Wenker)
Correspondence: Jérôme Föllmi, Institute of Animal Genetics, Nutrition and Housing,
Division of Animal Housing and Welfare, Vetsuisse Faculty, University of Berne,
Bremgartenstrasse 109a, CH 3001 Berne, Switzerland. Phone: +41.31.305.90.50,
Fax: +41.31.631.26.40, Email: jerome.foellmi@itz.unibe.ch
Urs Geissbühler, Department of Clinical Veterinary Medicine, Section
of Radiology, Vetsuisse Faculty, University of Berne, Länggass-Strasse 124, CH 3001 Bern,
Switzerland. Phone: +41.31. Fax: +41., Email: urs.geissbuehler@.unibe.ch
Summary
Radiographic examinations of the elbows, hips, stifles and tarsal joints of nine captive bears
of four genera ranging from 11 to 33 years were performed in five European zoos . Five
individuals showed lameness and/or gait abnormality, four individuals did not suffer from any
gait abnormality. The radiographs were scored by the presence of signs of osteoarthritis.
Degenerative changes were detected in both groups. Lameness or gait abnormality seemed to
be associated with the radiographic findings only in two bears. Osteoarthritis was present
radiographically in most of the joints. Osteoarthritis appears to be very prevalent in the
population of bears examined in this report. However, correlation of the radiographic findings
to clinical disease is not always evident.
Key words: aging, bear, lameness, osteoarthritis, radiography, zoo, degenerative joint disease
Résumé
Etude radiographique des coudes, des hanches, des genoux et des tarses chez neuf ours en
captivité de quatre espèces différentes avec un âge allant de 11 à 33 ans. Cette étude a été
effectuée dans cinq zoos européens. Cinq individus ont montré une boiterie et / ou une allure
anormale et quatre individus ne présentaient pas de signe clinique. Les radiographies ont reçu
des points lors de présence d’ostéoarthrite. Des changements dégénératifs ont été trouvés dans
les deux groupes. Une boiterie ou une allure anormale semble être associée par diagnostic
radiographique seulement chez deux ours. L’ostéoarthrite était présente radiographiquement
35

dans la plupart des articulations. La prévalence de l’ostéoarthrite se révèle être importante
dans la population d’ours examinée de cette étude. Cependant, la corrélation entre le
diagnostic radiographique et la clinique ne se révèle pas toujours évident.
Mots-clé: ours, boiterie, ostéoarthrite, radiographie, zoo, maladie dégénérative des
articulations, vieillissement
Introduction
The conditions of keeping wild animals in captivity are improving and the longevity of these
animals is increasing. Consequently, management of long-living species and age-related
diseases are becoming common, some of which may be difficult to diagnose and treat, thereby
potentially compromising welfare. 1 Animals in captivity invariably live longer than their wild
counterparts. 2-4 There are many consequences of old age in captive mammals 1 including
problems of skeleton and teeth. 1,2,5-13 This is also one major problem of captive bears, because
they usually live a long life in zoos. Individuals of most bear species may live more than 20
years and for the larger species, some individuals get till 30 years old and beyond. 14
The care of these animals and especially the decision to perform euthanasia of geriatric
zoo bears is usually a highly complex procedure involving ethical, medical, emotional and
sometimes political factors.. In old animals, euthanasia has to be considered, but it is very
difficult to evaluate the appropriate time. Besides the medical aspect, the zoo veterinarian
must take into consideration the different interests of zoo managers and staff, visitors, animal
welfare organizations, sponsors and possibly the needs of the respective breeding programs
(e.g. European Endangered Species Program). Consecutive necropsy of animals often shows
that the pathological changes of organs and / or the musculoskeletal system are already
advanced. Therefore we hypothesize that the decision to perform euthanasia might be often
delayed to the detriment of the animal’s welfare. The aim of this study was to gain
radiographic data from joints of zoo bears in order to evaluate the incidence of osteoarthritis.
The radiographic findings then serve as one parameter of a scoring system to support the
decision making for euthanasia in geriatric zoo bears and zoo mammals (publication in
preparation).
Material and Methods
Several joints of nine zoo bears (in the following text numbered from 1 to 9) of four genera,
examined for health problems, were radiographed. The bears live in five European zoos. Four
adult brown bears (Ursus arctos) (1-4) and one polar bear ( Ursus maritimus) (5) suffered
from lameness and / or gait abnormalities or paraparesis. One sun bear (Helarctos malayanus)
(6) and three black bears (Ursus americanus) (7-9) revealed no gait abnormalities and have
been anesthetized for other reasons (Table 1).
36

Table 1 Age, sex and clinical signs of examined bears (n = 9)
Bears Age Sex Clinical signs
Brown bear (Ursus arctos) (1) 29 F mild lameness forelimb right, mild dysorexia, mild weakness, mild
reluctance to move, apathy
Brown bear (Ursus arctos) (2) 23 F severe lameness of the left forelimb and the right hind limb, severe
reluctance to move, pain when standing up, mild dysorexia,
cachexia
Brown bear (Ursus arctos) (3) 33 F mild gait abnormalities, mild dysorexia
Brown bear (Ursus arctos) (4) 33 F mild lameness of the forelimb right, stiff neck, mild dysorexia
Polar bear (Ursus maritimus) (5) 27 M paraparesis since one week, mild dysorexia
Sun bear (Helarctos malayenus) (6) 21 M Control of the oro-nasal sinus tract, control of the eyes
Black bear (Ursus americanus) (7) 17 M no, check-up
Black bear (Ursus americanus) (8) 15 M no, check-up
Black bear (Ursus americanus) (9) 11 M no, check-up
A brown bear (1) was immobilized with etorphine/acepromazine (0,02 mg/kg IM, Large
Animal Immobilon ®, C-Vet Veterinary Products, Leyland, UK); two brown bears (3, 4) were
immobilized with tiletamine/zolazepame (2,5 mg/kg IM, Zoletil 100 ®, Laboratories Reading-
Virbac, Carros, England) and with medetomidine (42,5 µg/kg IM, Domitor®, Orion Corporation
Animal Health, Turku, Finland). Another brown bear (2) and the polar bear (5) were
immobilized with S-ketamine (1,5 mg/kg IM, S-Ketamin, non-commercial preparation, Graeub
AG, Berne, Switzerland) and with medetomidine (20 µg/kg IM, Zalopine ®, Orion Corporation
Animal Health, Turku, Finland). Following endotracheal intubation, anesthesia was maintained
with isoflurane (IsoFlo ®, Abott AG, Baar, Switzerland) delivered in O2 100% using a large
animal circle system (Matrx VML Large Animal, USA). The sun bear (6) was immobilized with
ketamine (3 mg/kg IM) and medetomidine (0,07 mg/Kg IM, Zalopine ®, Orion Corporation
Animal Health, Turku, Finland). Two bolus of ketamine (1,25 mg/kg, Ketasol-100 ®, Graeub
AG, Berne, Switzerland) were administered IM to prolong anesthesia. The three black bears (7-
9) were also immobilized with tiletamine/zolazepame (5mg/kg IM, Zoletil 100 ®, Laboratories
Reading-Virbac, Carros, England).
Radiographs of all bears were performed in autumn 2004 and spring 2005 with three
different mobile x-ray equipments. The systems consisted of a Mobilett® (Siemens,
Germany) with a performance of 20 kW at 100 kV for four brown bears (1-4) and one sun
bear (6), a Unimax 200® (Generay, Italy) with a performance of 32 kW at 100 kV for the
polar bear (5) and a Gierth HF 80/15 plus® (Gierth, Germany) with a performance of 24 kW
at 80 kV for the three black bears (7-9).
All radiographs were registered by fifth generation phosphor storage plates
(ST V, 18 x 24 / 24 x 30 / 35 x 43 cm) from Fuji. For the reading out of the plates two
different systems were used: a Fuji FCR 5000R (Veterinary Clinic at the University of Berne)
and a Fuji XG1 (Human Hospital of the University of Basel).
The radiographs were scored by the presence of either none to mild, moderate and
severe signs of osteoarthritis. In three bears (7-9) the radiographic examination of the hip
joints and of the stifle joints were not performed (Table 2).
37

Table 2. Radiological examination of joints in the nine bears
Bears
Joints Brown bears (1) Brown bears (2) Brown bears (3) Brown bears (4) Polar bear (5) Malayan bear (6) Black bear (7) Black bear (8) Black bear (9)
Maxilla (inlet) x x x x
Mandible (inlet) x x x x x
Cervical vertebrae (ll) x x
Thoracal vertebrae (ll) x x
Thoraco-lumbar vertebrae (ll) x x x x
Lumbar vertebrae (ll)
x x
Elbow left (ml) x x x x x x x x
Elbow right (ml) x x x x x x x x x
Elbow left (dp) x x x x x
Elbow right (dp)
x x x x
Hip (vd) x x x x x x
Stifle left (ml) x x x x
Stifle right (ml) x x x x x
Stifle left (dp) x x
Stifle right (dp) x x
Tarsus left (ml) x x x x x x x x x
Tarsus right (ml) x x x x x x
Tarsus left (dp) x x x
Tarsus right (dp) x x
ll = latero-lateral; ml = medio-lateral; dp = dorso-palmar/-plantar; vd = ventro-dorsal
x = joint radiographed
38

Results
Radiographs showed none osteoarthritic alterations in the elbow of one bear (5), none to mild
osteoarthritic changes in six bears (1, 3, 4, 7-9), moderate osteoarthritic changes in one bear
(6) and severe osteoarthritic alterations in one bear (2). This bear with severe osteoarthritis
showed a severe lameness (Figure 1). Moreover, two bears with lameness and/or gait
abnormalities showed enthesiophytes, one bear (1) in the medial and the other one(3) in the
lateral epicondyle of the left elbow joint. The joint of the same both bears and a third brown
bear (9) showed osteophytes in the left elbow. Marked cuff-like lesions (periarticular
mineralization) were detected in both elbow joints of one and in the right elbow of another
bear (9) (Figure 2).
The radiographs of the hip joint showed none bone modifications in five bears (1, 3-6).
Severe osteoarthritic changes were detected in one bear (2) with severe lameness (Figure 3).
In three bears (7-9) without lameness and/or gait abnormalities, radiographs of the hip joints
were not performed.
Radiographs of the stifle joint were performed in six bears; four bears (1-4) with
lameness or gait abnormality, one bear (5) with paraparesis and one bear (6) without
lameness. Five bears (1, 3, 4-6) have none to mild osteoarthritic changes including the bear
without lameness having mild osteoarthritis in the stifle joint (Figure 4). One bear (2) with
severe lameness has moderate osteoarthritic alterations. In one stifle joint of a bear (3) with
gait abnormality we detected changes consistent with osteochondromatosis (Figure 5). The
same bear showed an extraarticular bone lesion consistent with an enostosis-like alteration in
the tibia.
Radiographs show none to mild osteoarthritic changes of the tarsal joints in seven
bears (1, 2, 4-6, 8, 9) including three animals without gait abnormality and / or lameness. Two
bears (3, 7), including one without lameness, delivered moderate osteoarthritis. One bear with
lameness and / or gait abnormality showed an enthesiophyte in the origin of the left plantar
ligament. In one bear with lameness marked cuff-like, periarticular mineralizations were
detected in the left tarsal joint. In two bears without lameness and in two bears with lameness
and/or gait abnormality, signs of a bilateral partial collapse of the central tarsal bone (Figure
6) and concurrent degenerative joint disease were present. In another bear (7) without signs of
lameness marked linear mineralizations in the soft tissue of the crural region were present.
Radiographs of the brown bear (1) with mild lameness of the right forelimb and with
mild reluctance to move show none to mild osteoarthritic changes in both elbow joints and in
both tarsal joints. An association between the clinical symptoms (severe lameness and severe
reluctance to move) and osteoarthritic alterations is suspected in a brown bear (2).
Radiographs show in this case mild osteoarthritic changes in the tarsal joints, moderate
osteoarthritic changes in both stifle joints and severe osteoarthritic alterations in the elbow
and in the hip joints. In two brown bears (3, 4) with the same age, one with mild lameness of
the right forelimb and the other one with gait abnormality, the radiographs show nearly the
same alterations: None to mild osteoarthritic changes in the left elbow joint and none
osteoarthritic alterations in the right elbow joint. Radiographs show in one tarsal joint of one
bear moderate osteoarthritic changes, thus that none to mild osteoarthritic changes in the stifle
joints. In the other one, the left tarsal joint has moderate osteoarthritic alterations and the right
tarsal joint has mild changes. Radiographs of the stifle joints of this bear show none to mild
osteoarthritic changes. The polar bear (5) with paraparesis presents none alterations of both
forelimbs and of the hip joints. On the other hand, radiographs show none to mild
osteoarthritic changes in tarsal and in the stifle joints. The radiographs of the sun bear (6)
without lameness, show moderate osteoarthritic changes in both elbow joints and in both stifle
joints. The left tarsal joint presents mild osteoarthritic alterations. The three black bears (7-9)
without lameness present mild osteoarthritic changes of the right elbow joints. Radiographs of
one bear show mild osteoarthritic changes of the left elbow. In three black bears the tarsal
joints have mild osteoarthritic alterations.
39

Discussion
In the literature skeletal pathologies in captive bears are described. These observations were
made, without any exception, directly at necropsy or on skeletons in collections of museums
and in addition they were recorded in old adults. The patients of our study consisted of nine
captive bears with an age from 11 to 33 years and the examinations were performed under
general anesthesia.
Considerable problems arose during the radiographic examination. An important
factor was the security (flight tracks) of all involved people (technicians, veterinarians, animal
keepers, but also zoo visitors). In most instances we decided therefore to leave the bears
within the stable. Where possible, we moved them to the room in front of the stable. The
examination room was quite confined in almost every zoo. Under these conditions,
positioning of the animals, the cassette and the x-ray-tube was generally difficult. Some bears
weighted up to 280 kg and at least four strong men were necessary to move and elevate the
patients. The examinations were additionally hindered by the inhalation anesthesia and the
consideration of the radiation protection. We were not able to finish our examination protocol
in one case due to the unexpected early recovery of a patient anesthetized with an injection
protocol. Due to the limited number of phosphor storage plates sometimes we were forced to
read out some plates during the examination in a local human hospital. The limited
performance of mobile systems furthermore disabled acquiring hip joint radiographs in some
instances. And sometimes the wet wrap of bears created artifacts when it was raining.
A great number of secondary causes of osteoarthritis are discussed in the literature
such as trauma, metabolic disorder, immune-mediated arthritis or crystal induced arthritis. 15
One of them is “physiological” aging. Other factors are genetic predispositions (joint
dysplasia, osteochondrosis), captivity (characteristic of floor of the enclosure), nutrition and
infection. 15, 16 Degenerative joint disease are described in humans and a lot of mammals such
as horse and dog. 17, 18 The disease in these species may be primary or secondary to a
developmental or acquired disorder. The aetiopathogenesis, the specific locations and the
radiographic signs of this joint disease are quite well known.
16, 17, 18, 19
In our patientload we detected changes resembling to alterations described in other mammals.
In analogy to alterations found in horses for example, we detected a collapse of the small
tarsal bones 16 , changes in the strong part of the tarsus resembling to bone spavin 20 and
osteochondromatosis-like lesions in one stifle joint 21 . Other changes resembled to
radiographic findings in dogs. The type of radiographic changes in some stifle joints, for
example, are comparable to changes found in cranial cruciate ligament lesions and some
alterations in hip joints were similar to dogs with bilateral hip displasia and concurrent
coxarthrosis. 18, 22 The cuff-like type of lesion in two elbow joints, however, resembles to the
changes detected in cats suffering from a chronic hypervitaminosis A. 15 And comparable
enostotic lesions as detected in the tibia of one of the brown bears have been described in
horses and dogs (endostal reaction).
15, 16, 17
The nutrition can play a role at two levels in zoo bears. Large quantities of food can
induce an overweight and afterwards can cause osteoarthritic changes as described in other
animals. An inadequate food for bears, might influence the upset of skeletal disorders such as
it is described in osteochondrosis of dogs and pigs with possible consequent osteoarthritis. 18,
23
Polyarthritis is thought to be followed by osteoarthritic changes. In the literature
infectious and non-infectious causes are mentioned. Some authors 8, 10, 11 suggest that
osteoarthritis in bears and in felids could be caused by reactive arthritis, which is described in
humans as a sequale to infectious diarrhea due to Salmonella, Shigella, Yersinia,
Campylobacter or to transmitted infection (Chlamydia trachomatis). 24 This type of
polyarthritis is called Reiter’s Syndrome in human medicine. Many enthesiophytes were
visible on the radiographs of the tarsal and the stifle joints in our patientload, which have
comparable characteristic to Reiter’s syndrome. But a human being with the Reiter’s
syndrome shows often asymmetrical peripheral nonpurulent arthritis in more than five joints,
40

what we didn’t observe in the bears of our study. Furthermore, we do not have in one history
assessment of these bears a mention of an infectious diarrhea.
A correlation between the radiographic findings and clinical symptoms is not evident,
but the degree of radiographic change does not necessarily correlate with the clinical signs. 16
A correlation was found in a bear (2) with severe lameness showing moderate to severe signs
of osteoarthritis in elbow joints, hip joints and in stifle joints. But the radiographs of all bears
(1, 3-5) with mild lameness, gait abnormality or parapraresis showed radiographically none,
mild and moderate alterations of the joints. One possible explication is that a gait abnormality
is caused by osteoarthritic changes in other joints, which we did not examine in our study, like
the shoulder or the vertebral column. These bears presented alterations in the left and the right
joints, and therefore the lameness was not as pronounced as expected. The clinical
localization of a lameness is very difficult in zoo animals because the unique possibility to
make palpation or provocation test is under general anesthesia. The weight of the animal can
cause some problems to perform these provocation tests.
It was our intention to use the radiographic findings as one factor in a scoring system,
which provides an aid to the responsible persons in decision making of euthanasia in geriatric
zoo animals (publication in preparation). The scoring system aids to evaluate the general
condition and the quality of life in geriatric zoo mammals. It includes five parts. The fourth
part involves the “radiographic examination”. In this part the radiographic examination of the
joints is included, considering that dysfunction of the musculoskeletal system represents a
major problem in geriatric animals (37%). On the basis of this study in the part “radiographic
examination” points for the scoring system were given based on the type of alteration in a
joint, the number of joints affected in each animal and the localization in the joint.
In conclusion all bears without and with gait abnormality show osteoarthritic changes
in joints. We noticed that the three youngest bears of this study showed osteoarthritic
modifications but no clinical signs. For this reason we would like to compare our results with
x-rays of wild bears. It would be interesting to pursue further radiographic examinations to
correlate them with the clinical signs.
Acknowledgments
The authors thank Dr. Christelle Vitaud, Safari Peaugres, France; Dr. Pierre Moisson
and Dr. David Gomis, Zoo Mulhouse, France; Dr. Willi Häfeli, Tierpark Dählhölzli,
Switzerland; and René Strickler, Zoo Subigen, Switzerland, for their kind hospitality in their
zoos, as well as Dr. Christian Walzer and Dr. Nadia Robert for their scientific contributions to
this study.
We thank Mr. Kamm from Fuji, Switzerland for the technical support and the
technicians at the section of radiology at University of Basel
References
1. Kitchener AC. The problems of old bears in zoos. International Zoo News 2004; 5(5):
282-293
2. Erwin JM, Hof PR, Ely JJ, Perl DP. One gerontology: advancing understanding of
aging through studies of great apes and other primates. Interdisciplinary Top Gerontology
2002; 31: 1-21
3. Richardson D. Euthanasia: a nettle we need to grasp, Bioparco Rome Zoo, Italy. 2000
4. Nowak RM. Walker's mammals of the world. Baltimore, USA: The Johns Hopkins
University Press; 1999
41

5. Colman RJ, Binkley N. Skeletal aging in macaque monkeys. Interdisciplinary Top
Gerontology 2002; 31: 32-47
6. Nichols KA, Zihlman AL. Skeletal and dental evidence of aging in captive western
lowland gorillas: a preliminary report. Interdisciplinary Top Gerontology 2002; 31: 22-31
7. Rotschild BM, Rotschild C, Woods RJ. Inflammatory arthritis in canids:
spondyloarthropathy. Journal of Zoo and Wildlife Medicine 2001; 32(1): 58-64
8. Rotschild BM, Rotschild C, Woods RJ. Inflammatory arthritis in large cats: an
expanded spectrum of spondyloarthropathy. Journal of Zoo and Wildlife Medicine 1998;
29(3): 279-284
9. Rotschild BM, Rotschild C. No laughing matter: spondyloarthropathy and osteoarthritis
in hyaenidae. Journal of Zoo and Wildlife Medicine 1994; 25(2): 259-263
10. Kompanje EJO, Klaver PSJ, De Vries GT. Spondyloarthropathy and osteoarthrosis in
three indomalayan bears: ursus ursinus Cuvier, 1823, ursus thibetanus Raffles, 1821, and
ursus malayanus Shaw & Nodder, 1791 (Mammalia: Carnivora: Ursidae). Contributions to
Zoology 2000; 69(4)
11. Kompanje EJO, Klaver PSJ. Spondarthritis (spondyloarthropathy) and osteoarthritis in
an old female sloth bear (ursus ursinus Cuvier, 1823), a case report. European Association of
Zoo- and Wildlife Veterinarians (EAZWV), Chester, UK 1998: 473-479
12. Wenker CJ, Müller M, Berger M, et al. Dental health status and endodontic treatment
of captive brown bears (ursus arctos ssp.) living in the bernese bear pit. Journal of veterinary
dentistery 1998; 15(1): 27-34
13. Jack SW, Thacker HL. Degenerative joint disease in a nile hippopotamus. Journal of
American Veterinary Medical Association 1985; 187(11): 135
14. Kitchener AC, Kolter L, Brownstein D. Problems with old bears in zoos. In: *EEP
Yearbook 1999/2000 including Proceedings of the 17th EAZA Conference, Aalborg 19-24
September 2000 2001: 625-628
15. Kealy JK, Mc Allister H. Bones and joints. In: Diagnostic radiology and
ultrasonography of the dog and cat. 3rd ed. Philadelphia: W.B. Saunders Company; 2000:
253-338
16. Thrall DE. Radiographic signs of joint disease. In: Textbook of veterinary diagnostic
radiology. 4th ed. Philadelphia: W. B. Saunders Company; 2002: 187-208
17. Auer JA, Strick JA. Angular limb deformities. In: Equine surgery. 2nd ed.
Philadelphia: W.B. Saunders Company; 1999: 736-751
18. Slatter D. Osteoarthritis. In: Textbook of small animal surgery. 3 rd ed. Philadelphia:
W.B. Saunders Company; 2003: 2208-2245
19. Cotran RS, Kuman V, Collins T. Bones, joints and soft tissue tumors. In: Pathologic
basis of diseases. 6 th ed. Philadelphia: W.B. Saunders Company; 1999:1246-1259
20. Auer JA, Strick JA. The tarsus. In: Equine surgery. 2nd ed. Philadelphia: W.B.
Saunders Company; 1999: 848-861
21. Auer JA, Strick JA. The radius and ulna. In: Equine surgery. 2nd ed. Philadelphia:
W.B. Saunders Company; 1999: 831-841
22. Kealy JK, Mc Allister H. Hip dysplasia: pathogenesis. In: Diagnostic radiology and
ultrasonography of the dog and cat. 3rd ed. Philadelphia: W.B. Saunders Company; 2000:
2009-2018
23. Straw BE, D’allaire S, Mengeling WL, et al. Diseases of the nervous and locomotor
systems. In: Diseases of swine. 8 th ed. Ames, Iowa: Iowa state university press; 1999: 861-882
24. Khan MA. Arthritis and autoimmunity. Report on the 15th Sigrid Jusélius Symposium
Rheumatology Int 1995; 15: 39-42
42

Figure 1. Brown bear, 23 year-old, mediolateral view of the right elbow. Severe cufflike
lesions (articular and periarticular mineralisations), comparable to changes seen in
elbow joints of cats with hypervitaminosis A.
Figure 2. Black bear, 17 year-old, mediolateral radiograph of the right elbow. Ovoid,
vertically oriented soft tissue mineralization cranially to the radial head (arrow).
Concurrent osteophyte formation dorsoproximally at the radial head.
43

Figure 3. Brown bear, 23 year-old, ventrodorsal flexionview of both hip joints. The
marked bilateral incongruence of the articular contours, subluxation and marked
osteophytic and periarticular reactions are consistent with bilateral osteoarthritic
alterations of the hip joints as a sequale of hip displasia. The changes are comparable
to hip displasia in dogs.
Figure 4. Polar bear, 27 years-old, mediolateral view of the left stifle. Presence of
entesiophytes and osteophytes proximally and distally at the patella, cranially and
caudally at the tibial plateau and caudally at the femoral condyles. The infrapatellar fat
pad is partially dislocated or opacified by a soft tissue structure. A soft tissue opaque
structure is bowing in caudal direction of the femorotibial joint (articular border).
44

Figure 5. Brown bear, 33 years-old, mediolateral radiograph of the left stifle joint.
Multiple mineral-opaque, ovoid structures following the outlining of the caudal part
of the femorotibial joint comparable to an osteochondromatosis seen in other animals
(arrow). Formation of small enthesiophytes at the proximal border of the patella.
Figure 6. Black bear, 11 years-old, mediolateral view of the left tarsus. Presence of a
marked linear, shell-like mineralization in the soft tissue of the crural region (white
arrow). Partial collapse of the central (third?) tarsal bone (red arrow) and osteo- and
enthesiophytic rections dorsally at the distal intertarsal and tarsometatarsal joint.
Similar changes have been detected in foals after premature birth.
45

III Remerciements
J’aimerais remercier tous ceux qui pendant ces deux années ont permis la réalisation de ce
travail, ainsi que ceux qui ont cru en ce travail et qui m’ont fait confiance.
Tout particulièrement :
Dr. Christian Wenker, Dr. Christian Walzer et Dr. Nadia Robert pour leurs conseils
scientifiques et compétents, pour leur initiative, pour leur confiance, pour leur soutien, pour le
climat de travail agréable et amicale et aussi pour leur conviction en ce travail.
Prof. Andreas Steiger pour son intérêt, son enthousiasme et son soutien dans ce travail.
Dr. Urs Geissbühler pour ses conseils scientifiques et compétents, pour sa confiance, pour son
soutien, pour ses initiatives et pour son enthousiasme.
Dr. Marcus Doherr pour ses conseils et son aide pour la statistique.
La direction du zoo de Bâle, plus particulièrement le Dr. Olivier Pagan, pour l’intérêt et le
soutien dans ce travail, ainsi que le Dr. Jürg Völlm et le Dr. Friederike von Houwald pour leur
intérêt, leur collaboration et leur sympathie.
Dr. Jean-Michel Hatt, Dr. Christelle Vitaud, Dr Pierre Moisson et Dr. David Gomis, Dr. Willi
Häfeli, Dr. Martin Wehrle et René Strickler pour leur intérêt, leur collaboration et leur
hospitalité lors de la venue dans leurs zoos.
Prof. Ewald Isenbügel, Dr. Hanspeter Steinmetz and Dr. Gaby Hürlimann du Zoo Zürich, Dr.
Willem Schaftenaar du Zoo Rotterdam pour leur collaboration.
Tous les soigneurs des différents zoos pour leur aide et leur collaboration.
Les différentes cliniques et sections du Tierspital de Berne pour leur collaboration, à savoir :
Dr. Claudia Spadavecchia, Dr. Alessandra Bergadano, Dr. Peter Kronen, Dr. Olivier
Leviennois, Dr. Christoph Peterbauer et Dr. Shannon Gerber de l’anesthésiologie ; Dr. Peter
Schawalder, Dr. David Spreng, Dr. Karin Hurter, Dr. Judith Howard de la clinique des petits
animaux ; Dr. Adrian Steiner et Dr. Mireille Meylan de la clinique des ruminants ; Dr. Ana
Overmann, Dr. Stefan Hoby, Med vet. Veronika Sieber, Med. vet Helena Nimmervoll, Med
vet Valeria Cafe-Marcal de la pathologie.
Paul Schmid, du musée d’histoire naturelle de Berne, Burkart Engesser du musée d’histoire
naturelle de Bâle et Jacqueline Studer du musée d’histoire naturelle de Genève pour leur
hospitalité et pour le temps consacré à me guider dans les souterrains de leurs musées
respectifs.
Tous mes amis et tout particulièrement Grégoire Blaudszun, Gilles Steiner, Stefan Hoby,
Edoardo Giani, Michael Marti pour leur amitié et les bons moments passés ensemble.
Eva Scheidegger pour son soutien, sa confiance et son sourire quotidien.
Ma famille et plus particulièrement mes parents, Martine et Marco Föllmi pour le soutien
moral et financier.
47