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Journal of Anatomy logoLink to Journal of Anatomy
. 2017 May 23;231(1):140–155. doi: 10.1111/joa.12620

Osteoarthritis in two marine mammals and 22 land mammals: learning from skeletal remains

Korakot Nganvongpanit 1,✉, Ratsadakorn Soponteerakul 1,†, Piyatida Kaewkumpai 1,†, Veerasak Punyapornwithaya 2, Kittisak Buddhachat 3, Raksiri Nomsiri 4, Patcharaporn Kaewmong 5, Kongkiat Kittiwatanawong 5, Rachanchai Chawangwongsanukun 6, Taweepoke Angkawanish 7, Chatchote Thitaram 8, Pasuk Mahakkanukrauh 9,10
PMCID: PMC5472524  PMID: 28542897

Abstract

The occurrence of osteoarthritis (OA) in marine mammals is still questionable. Here we investigated the prevalence of OA in marine (dolphin and dugong) and terrestrial mammals (Asian elephant, Asiatic buffalo, camel, cat, cattle, deer, dog, domestic goat, horse, human, hyena, impala, lion, Malayan tapir, Assam macaque, mule, pig, rabbit, red kangaroo, sheep, tiger and waterbuck). Skeletal remains obtained from five institutes were used as subjects; a total of 45 different parts (locations) of bones were observed for OA lesions. The prevalence of OA was reported as number of OA lesions/total number of bones. Our results revealed that the presence of OA in marine species (dolphin and dugong) was 2.44% and 3.33%, respectively. In dolphins, the highest OA occurrence was on the left and right humeral trochlea, with 13.68% and 12.63%, respectively, while the highest number of OA lesions in dugongs was on the lumbar vertebrae (8.79%). No significant difference (P > 0.05) in the prevalence of OA between sexes in dolphins and dugongs was observed, but we found a significant difference (P < 0.05) in 24 bone locations of human bones, which had the highest OA prevalence (48.93%), followed by dogs (3.94%). In conclusion, OA can occur in marine mammals, similar to terrestrial mammals, even though their natural habitat is the ocean.

Keywords: bone, degenerative joint disease, land mammal, marine mammal

Highlights.

  • Dugongs and dolphins showed the presence of OA.

  • Gender did not influence OA occurrence in marine species.

  • OA is more prevalent in male humans.

Introduction

Osteoarthritis (OA) or degenerative joint disease is one of the most common and important non‐inflammatory joint diseases in many mammalian species, such as human, dog and cat (Sarzi‐Puttini et al. 2005; Lawrence et al. 2008; Arzi et al. 2013; Nganvongpanit et al. 2014). The primary characterization of this disease includes degradation of the articular surface of joints associated with thickening of the underlying bone by subchondral bone sclerosis and osteophyte formation (Sarzi‐Puttini et al. 2005; Buckwalter & Martin, 2006). Several risk factors are implicated in the etiology of OA (Sarzi‐Puttini et al. 2005; Buckwalter & Martin, 2006), such as traumatic joint disease, septic arthritis, joint dysplasia, medicine or chemical irritation or toxicity, obesity and genetics. Major clinical signs contributing to suffering are joint pain and discomfort during movement. Animals are often killed when suffering from this disease (Kolmstetter et al. 2000; Sarzi‐Puttini et al. 2005; Buckwalter & Martin, 2006).

Investigation of the prevalence or incidence of OA in some mammal species is important for a better understanding of the etiology of this disease. Several studies surveying the occurrence of OA have been conducted. For example, nearly 27 million adults in the USA in 2008 were estimated to have clinical OA (Lawrence et al. 2008), and in 2006 there were an estimated 100 million people with OA in the European Union (Altman et al. 2006). It has also been reported that 20% of adult dogs are affected with OA (Marshall et al. 2009). In 2000, 30.3% of tarsal joints from 614 horses were found to have radiographic signs of OA, and the prevalence was strongly correlated with age (Björnsdóttir et al. 2000). In 2013, Arzi et al. reported on temporomandibular joint (TMJ) disorders in dogs (n = 41) and cats (n = 17); 36% of dogs and 23% of cats showed OA of the TMJ. However, most of the reported prevalence of OA in these species focused on certain joints, not all joints in the body, which contributed to the limitation of those studies: (i) several studies focused only on some joints that presented clinical signs; and (ii) those studies were almost all conducted in humans and some animals (dog, cat and horse). With respect to these two constraints, there are two principal unanswered questions about the nature of OA in mammal species. The first question is whether entire mammalian species (both marine and terrestrial animals) can develop OA. The second question is whether OA can occur in all joints of the body.

To attempt to answer the questions above, we designed a study on the prevalence of OA from skeletal remains kept in anatomy museums. Studies of bone remains have previously been used in osteoarchaeology (Greer et al. 1977; Woo & Sciulli, 2011). However, unlike other studies on humans or some companion animals that have employed standard radiographic imaging (Lawrence et al. 2008), we were not able to take radiographs of whole joints in the bodies of terrestrial and marine mammals or to perform necropsies on large numbers of these animals.

Therefore, this study aimed to survey: (i) the prevalence of OA in 24 mammals, both marine and terrestrial; and (ii) to investigate OA lesions in all diarthrodial and intervertebral joints in the body. A major objective of this study was to assess the prevalence of OA in marine mammals because of the scarcity of this information, except for a few studies that have reported on arthritis from clinical examinations or necropsies in dolphins (Kompanje, 1995; Watson et al. 2008; Gomerčić et al. 2009; Davison et al. 2013, 2014). Dolphins and dugongs, which belong to the orders Cetartiodactyla and Sirenia, live in the ocean throughout their lives, while other marine mammals such as those in the suborders Caniformia and Pinnipedia inhabit both ocean and land. Our hypothesis is that OA can occur in marine mammals just as in other terrestrial mammal species such as human and dog.

Materials and methods

Animal bone samples

In this study, bones of adult animals were obtained from five different museums:

(i) Animal Anatomy Museum, Department of Veterinary Biosciences and Public Health, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, Thailand; (ii) Department of Pre‐clinical Sciences and Applied Animal Science, Faculty of Veterinary Science, Mahidol University Salaya Campus, Nakhon Pathom, Thailand; (iii) Animal Bone Collection Center, Phuket Marine Biological Center, Phuket, Thailand; (iv) Animal Bone Collection Center, National Elephant Institute, Forest Industry Organization, Lampang, Thailand; and (v) Department of Anatomy, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand.

Bone samples were derived from two marine and 22 land mammals. The marine animals were dugong (Dugong dugon) and dolphin (family Delphinidae). Land mammals consisted of Asian elephant (Elephas maximus), Asiatic buffalo (Bubalus bubalis), camel (Camelus dromedarius), cat (Felis catus), cattle (Bos taurus), deer (family Cervidae), dog (Canis lupus familiaris), domestic goat (Capra hircus), horse (Equus ferus caballus), human (Homo sapiens), hyena (Hyaena hyaena), impala (Aepyceros melampus), lion (Panthera leo), Malayan tapir (Tapirus indicus), monkey (Assam macaque; Macaca assamensis), mule (Equus asinus × Equus caballus), pig (Sus scrofa domesticus), rabbit (Oryctolagus cuniculus), red kangaroo (Macropus rufus), sheep (Ovis aries), tiger (Panthera tigris tigris) and waterbuck (Kobus ellipsiprymnus). Figure 1 illustrates the genetic relationships among the studied animals, excluding mules.

Figure 1.

Figure 1

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Based on cytochrome b (CYTB), a phylogenetic tree was constructed using a neighbor‐joining model to illustrate the genetic relationship and osteoarthritis (OA) occurrence among species, including dog, cat, pig, buffalo, camel, cow, waterbuck, deer, goat, sheep, horse, hyena, impala, kangaroo, lion, tiger, rabbit, tapir, elephant, monkey, human, dugong and dolphin. Numbers are bootstrap values (in percent 1000 replications) of neighbor joining. + = OA occurrence; − = no OA lesions; and ? = species not determined for OA lesions. Green indicates the herbivore groups, and red indicates carnivores and omnivores.

All bone samples were dry and maintained at room temperature. Based on their recorded history, they were suggested to be adult bones. In the case of samples of unknown age, we assumed their age through the closure of the epiphyseal plate as an indicator of mature animal bone (Kohn et al. 1997; Strand et al. 2007; Wolpert, 2010). Human bone samples (dry bone) were obtained from donated cadavers at the Department of Anatomy, Faculty of Medicine, Chiang Mai University, Thailand. To use these skeletons, consent was waived by the Human Ethics Committee, Faculty of Medicine, Chiang Mai University (NONE‐2559‐04108), and the samples were also anonymized in our study. The use of animal bones from all animal museums did not require approval by the Animal Ethics Committee, Faculty of Veterinary Medicine, Chiang Mai University.

OA evaluation and joint observation

Bone remains were observed for indications of degradation of articular cartilage. Osteophyte formation and subchondral bone degradation, which are specific characteristics of OA in many species (Sarzi‐Puttini et al. 2005; Kraus et al. 2010; Little et al. 2010; McIlwraith et al. 2010), were thoroughly noted as to whether they were present or absent in each sample (Fig. 2). In this study, we were not able to grade the severity of OA because standard guidelines for grading OA consider several signs in the joint structure, such as joint capsule, articular cartilage and bone (Kraus et al. 2010; Little et al. 2010; McIlwraith et al. 2010). Lesions from osteophyte formation after death cannot alter the appearance of bone samples caused by chemical or environmental degradation, or even pathological lesions such as fracture (Fig. 3). However, almost all bone samples were immediately prepared after animal death using a protocol according to each institute, taking care not to damage the bones. All diarthrodial joints and some amphiarthrodial joints (intervertebral joints) in the animal body were observed (Table 1). The carpal, tarsal and phalangeal joints (forelimb and hindlimb) are complex and include many small joints. If at least one joint was found with an OA lesion, it would be recorded as positive OA of the joint.

Figure 2.

Figure 2

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Representative photos of the normal articular surface of canine acetabulum (A), osteophyte formation as a reference for osteoarthritis (OA) (B), and severe osteophyte formation with subchondral bone degradation as a reference for OA (C).

Figure 3.

Figure 3

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Representative photos of abnormal structures (arrows) such as pathological lesions from fracture (A), and bone degradation from the environment (B).

Table 1.

Anatomical position used for OA observation, and the reference number

Axial skeleton Forelimb skeleton Hindlimb skeleton
Skull
TMJ; 1
Atlanto‐occipital joint; 2
Intervertebral joint
Cervical vertebrae; 3
Thoracic vertebrae; 4
Lumbar vertebrae; 5
Sacral vertebrae; 6
Coccygeal vertebrae; 7 		Glenoid cavity of scapula; 8
Humeral head; 9
Humeral trochlea; 10
Head of radius; 11
Carpal articular surface of radius; 12
Trochlear notch of ulna; 13
Styloid process of ulna; 14
Articular surface of carpal bone; 15
Metacarpophalangeal joint; 16
Interphalangeal joint; 17 		Articular surface of ilium; 18
Acetabular fossa; 19
Femoral head; 20
Femoral trochlea; 21
Tibial condyle; 22
Distal articular surface of tibia; 23
Articular surface of tarsal bones; 24
Metacarpophalangeal joint; 25
Interphalangeal joint; 26
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For the appendicular skeleton, the right (r) or left (l) side is added after the number: for example, 9r = right humeral head.

TMJ, temporomandibular joint.

Statistical analysis

The OA score was calculated by two different experts, and the agreement of the obtained results was tested by kappa (κ) statistics, the reliability of the score (Viera & Garrett, 2005). A kappa value of 1 represents perfect agreement, whereas a kappa value of 0 implies agreement comparable to chance. The data reported the number of OA occurrences and total number of bones (percentage) for each bone position; this is because some bones from museums were incomplete bones, or did not include the entire skeleton because some bones were missing. Hence, the number of samples for each animal was not similar between bone types.

The association of sex and OA was analyzed by chi‐square test, based on the known sex data acquired from cat, dog, dolphin, dugong and human. Moreover, a significant difference between sexes was analyzed by odds ratio to determine the risk factor. Only human bones had an age history for analyzing the association between age and OA occurrence by chi‐square test. Human age (minimum of 15 years to maximum of 100 years) was classified into four quartiles by calculating the three points that divide the data set into four equal groups: the middle value between the lowest age and the median age; the median age; and the middle value between the median age and the highest age. The resulting quartiles were: Q1 for age lower than 56 years (n = 125; male = 79, female = 46); Q2 for age between 56 and 67 years (n = 106; male = 61, female = 45); Q3 for age between 67 and 79 years (n = 110; male = 71, female = 39); and Q4 for age over 79 years (n = 115; male = 72, female = 43). The level of significance for all statistical analyses was chosen as P < 0.05.

Results

Prevalence of OA lesions on 45 different bone locations in two marine and 22 mammalian species

The kappa test score of OA lesions by two observers was 0.94 [95% confidence interval (CI): 0.93–0.94]. The percentage of OA in each bone in the axial, forelimb and hindlimb skeleton of each animal is presented in Tables 2, 3, 4. In this study, we noted OA lesions in both dolphins (Fig. 4) and dugongs (Fig. 5) at different bone locations. In dolphins, OA lesions did not exist in 12 out of 25 locations, including the TMJ, head of humerus (right and left), right carpal articular surface of radius, styloid process of ulna (right and left), articular surface of carpal bone (right and left), metacarpophalangeal joint (right and left) and interphalangeal joint of forelimb (right and left). The highest OA occurrence in dolphins was found on the left and right humeral trochlea (13.68% and 12.63%, respectively). Eleven parts of dugong bones did not present OA lesions: the TMJ, articular surface of carpal bone (right and left), metacarpophalangeal joint (right and left), interphalangeal joint of forelimb (right and left), articular surface of ilium (right and left) and acetabular fossa (right and left). Lumbar vertebrae showed the highest prevalence of OA lesions (8.79%), followed by the left and right glenoid cavity of the scapula (8.64% and 8.54%, respectively).

Table 2.

Number of samples with OA lesions/number of total samples observed (percentage) in axial skeletal bones of 13 mammalian species

Species Axial skeleton
1 2 3 4 5 6 7
Asian elephant 1/15
(6.67) 		0/15
(0) 		5/14
(35.71) 		10/15
(66.67) 		8/12
(66.67) 		4/17
(23.53) 		1/7
(14.29)
Cat 0/40
(0) 		0/40
(0) 		1/38
(2.63) 		3/38
(7.89) 		1/37
(2.70) 		1/37
(2.70) 		0/36
(0)
Cattle 0/12
(0) 		0/12
(0) 		0/12
(0) 		1/2
(50) 		1/2
(50) 		N.D. N.D.
Dog 0/181
(0) 		0/181
(0) 		13/174
(7.47) 		26/170
(15.29) 		32/173
(18.49) 		13/169
(7.69) 		2/158
(1.27)
Dolphin 0/115
(0) 		1/115
(0.87) 		7/109
(6.42) 		3/109
(2.75) 		9/109
(8.26) 		N.D. N.D.
Dugong 0/65
(0) 		3/66
(4.55) 		7/91
(7.69) 		4/91
(4.39) 		8/91
(8.79) 		N.D. N.D.
Horse 0/23
(0) 		1/23
(4.35) 		0/13
(0) 		0/9
(0) 		3/11
(27.27) 		2/11
(18.18) 		0/6
(0)
Human 1/455
(0.22) 		43/455
(9.45) 		384/443
(86.68) 		385/444
(86.71) 		390/443
(88.04) 		388/467
(83.08) 		N.D.
Hyena 0/2
(0) 		0/2
(0) 		0/2
(0) 		1/2
(50) 		1/2
(50) 		0/2
(0) 		0/2
(0)
Malayan tapir 0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0)
Monkey 0/8
(0) 		0/8
(0) 		0/7
(0) 		2/7
(28.57) 		2/7
(28.57) 		1/6
(16.67) 		0/5
(0)
Sheep 0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0)
Tiger 0/5
(0) 		0/5
(0) 		0/7
(0) 		0/7
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0)
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1 = TMJ, 2 = atlanto‐occipital joint, 3 = cervical vertebrae, 4 = thoracic vertebrae, 5 = lumbar vertebrae, 6 = sacral vertebrae, 7 = coccygeal vertebrae, N.D. = not determined.

Table 3.

Number of samples with OA lesions/number of total samples observed (percentage) in axial skeletal bones of 13 mammalian species

Species Forelimb skeleton
8r 8l 9r 9l 10r 10l 11r 11l 12r 12l 13r 13l 14r 14l 15r 15l 16r 16l 17r 17l
Asian elephant 1/15
(6.67) 		2/15
(13.33) 		1/15
(6.67) 		1/15
(6.67) 		2/15
(13.33) 		2/15
(13.33) 		3/15
(20) 		3/15
(20) 		1/15
(6.67) 		1/14
(7.14) 		2/14
(14.29) 		2/14 (14.29) 1/14
(7.14) 		1/13
(7.69) 		0/8
(0) 		0/8
(0) 		0/8
(0) 		0/8
(0) 		0/8
(0) 		0/8
(0)
Cat 1/39
(2.56) 		1/39
(2.56) 		0/38
(0) 		0/37
(0) 		1/38
(2.63) 		1/37
(2.70) 		0/38
(0) 		0/39
(0) 		0/38
(0) 		0/39
(0) 		2/39
(5.13) 		1/39
(2.56) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0)
Cattle 1/6
(16.67) 		0/8
(0) 		0/3
(0) 		0/3
(0) 		0/3
(0) 		0/3
(0) 		0/3
(0) 		0/4
(0) 		0/3
(0) 		0/4
(0) 		0/3
(0) 		0/4
(0) 		0/3
(0) 		0/4
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0)
Dog 8/180
(4.44) 		10/176
(5.68) 		9/168
(5.36) 		11/174
(6.32) 		4/169
(2.37) 		3/174
(1.72) 		6/169
(3.55) 		6/170
(3.53) 		0/169
(0) 		1/170
(0.59) 		5/168
(2.98) 		5/171
(2.92) 		0/168
(0) 		0/171
(0) 		1/156
(0.64) 		1/156
(0.64) 		1/156
(0.64) 		1/156
(0.64) 		1/156
(0.64) 		1/156
(0.64)
Dolphin 4/114
(3.51) 		3/113
(2.65) 		0/95
(0) 		0/96
(0) 		12/95
(12.63) 		13/95
(13.68) 		7/89
(7.87) 		7/90
(7.78) 		0/89
(0) 		1/90
(1.11) 		7/89
(7.87) 		7/89
(7.87) 		0/89
(0) 		0/89
(0) 		0/88
(0) 		0/88
(0) 		0/88
(0) 		0/88
(0) 		0/88
(0) 		0/88
(0)
Dugong 7/82
(8.54) 		7/81
(8.64) 		3/72
(4.17) 		3/71
(4.23) 		2/72
(2.78) 		2/71
(2.82) 		1/57
(1.75) 		1/57
(1.75) 		1/56
(1.79) 		1/56
(1.79) 		1/56
(1.79) 		1/56
(1.79) 		1/56
(1.79) 		1/56
(1.79) 		0/55
(0) 		0/55
(0) 		0/55
(0) 		0/55
(0) 		0/55
(0) 		0/55
(0)
Horse 0/18
(0) 		0/15
(0) 		0/17
(0) 		0/15
(0) 		0/17
(0) 		0/15
(0) 		0/14
(0) 		1/14
(7.14) 		0/14
(0) 		0/14
(0) 		0/14
(0) 		0/14
(0) 		0/14
(0) 		0/14
(0) 		0/19
(0) 		0/19
(0) 		0/19
(0) 		0/19
(0) 		0/19
(0) 		0/19
(0)
Human 316/468 (67.52) 318/468 (67.95) 214/469 (45.62) 209/467 (44.75) 161/467 (34.48) 159/466 (34.12) 153/469 (32.62) 152/469 (32.41) 217/469 (46.27) 211/469 (44.99) 270/468 (57.69) 262/467 (56.10) 146/468 (31.19) 144/467 (30.84) 193/465 (41.51) 193/465 (41.51) 193/465 (41.51) 193/465 (41.51) 193/465 (41.51) 193/465 (41.51)
Hyena 0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		1/2
(50) 		1/2
(50) 		1/2
(50) 		1/2
(50) 		1/2
(50) 		1/2
(50) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0)
Malayan tapir 0/1
(0) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100) 		1/1
(100)
Monkey 0/6
(0) 		0/7
(0) 		1/6
(16.67) 		2/7
(28.57) 		0/6
(0) 		0/7
(0) 		1/6
(16.67) 		1/6
(16.67) 		0/7
(0) 		0/7
(0) 		1/7
(14.29) 		1/7
(14.29) 		1/7
(14.29) 		0/7
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0)
Sheep 0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0)
Tiger 1/7
(14.29) 		1/7
(14.29) 		1/6
(16.67) 		1/6
(16.67) 		0/6
(0) 		1/6
(16.67) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0)
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8 = glenoid cavity of scapula, 9 = humeral head, 10 = humeral trochlea, 11 = head of radius, 12 = carpal articular surface of radius, 13 = trochlear notch of ulna, 14 = styloid process of ulna, 15 = articular surface of carpal bone, 16 = metacarpophalangeal joint, 17 = interphalangeal joint, l = left, r = right.

Table 4.

Number of samples with OA lesions/number of total samples observed (percentage) in hindlimb bones of 13 mammalian species.a

Species Hindlimb skeleton
18r 18l 19r 19l 20r 20l 21r 21l 22r 22l 23r 23l 24r 24l 25r 25l 26r 26l
Asian elephant 3/20
(15) 		3/20
(15) 		3/20
(15) 		3/20
(15) 		0/13
(0) 		0/12
(0) 		6/12 (50) 4/12
(33.33) 		4/11
(36.36) 		3/12 (25) 3/11
(27.27) 		2/12
(16.67) 		1/9
(11.11) 		1/9
(11.11) 		1/9
(11.11) 		1/9 (11.11) 1/9 (11.11) 1/9
(11.11)
Cat 0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/37
(0) 		0/37
(0) 		1/37
(2.70) 		0/37
(0) 		1/37
(2.70) 		0/37
(0) 		0/37
(0) 		0/37
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0) 		0/39
(0)
Cattle 0/2
(0) 		0/2
(0) 		0/8
(0) 		0/8
(0) 		0/8
(0) 		0/8
(0) 		0/2
(0) 		0/1
(0) 		0/2
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0)
Dog 22/170
(12.94) 		22/170
(12.94) 		22/170
(12.94) 		22/170
(12.94) 		14/167
(8.38) 		13/167
(7.78) 		13/167
(7.78) 		1/167
(0.59) 		2/162
(1.23) 		2/163
(1.23) 		1/162
(0.62) 		1/162
(0.62) 		1/154
(0.65) 		1/154
(0.65) 		1/154
(0.65) 		1/154
(0.65) 		1/154
(0.65) 		1/154
(0.65)
Dugong 0/53
(0) 		0/53
(0) 		0/53
(0) 		0/53
(0) 		N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D.
Horse 0/13
(0) 		0/13
(0) 		0/13
(0) 		0/13
(0) 		0/13
(0) 		0/15
(0) 		0/13
(0) 		0/15
(0) 		0/14
(0) 		0/10
(0) 		0/14
(0) 		0/10
(0) 		1/16
(6.25) 		1/16
(6.25) 		1/16
(6.25) 		1/16
(6.25) 		1/16
(6.25) 		1/16
(6.25)
Human 350/469
(74.63) 		350/469
(74.63) 		350/469
(74.63) 		350/469
(74.63) 		151/450
(33.56) 		148/446
(33.18) 		222/446
(49.78) 		229/442
(51.81) 		221/446
(49.55) 		221/447
(49.44) 		210/446
(47.09) 		208/447
(46.53) 		201/457
(43.98) 		201/457
(43.98) 		201/457
(43.98) 		201/457
(43.98) 		201/457
(43.98) 		201/457
(43.98)
Hyena 0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0) 		0/2
(0)
Malayan tapir 0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		1/1
(100) 		1/1
(100) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		1/1
(100) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0)
Monkey 0/7
(0) 		0/7
(0) 		2/7
(28.57) 		0/7
(0) 		2/7
(28.57) 		1/7
(14.29) 		1/7
(14.29) 		0/7
(0) 		1/7
(14.29) 		1/7
(14.29) 		0/7
(0) 		0/7
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0) 		0/6
(0)
Sheep 0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0) 		0/1
(0)
Tiger 2/6
(33.33) 		2/6
(33.33) 		2/6
(33.33) 		2/6
(33.33) 		1/6
(16.67) 		1/5
(20) 		1/6
(16.67) 		1/5
(20) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0) 		0/5
(0)
Open in a new tab

18 = articular surface of ilium, 19 = acetabular fossa, 20 = femoral head, 21 = femoral trochlea, 22 = tibial condyle, 23 = distal articular surface of tibia, 24 = articular surface of tarsal bones, 25 = metacarpophalangeal joint, 26 = interphalangeal joint, N.D. = not determined.

a

Dolphin was excluded because of no hindlimb skeleton.

Figure 4.

Figure 4

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Osteoarthritis (OA) lesions (arrows) were found in dolphin bones at different locations, such as occipital condyle (A), glenoid cavity of scapula (B), head of humerus and carpal joint (C), and body of vertebrae (D and E).

Figure 5.

Figure 5

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Osteoarthritis (OA) lesions (arrows) were found in dugong bones at different locations, such as the occipital condyle (A), body of vertebrae (B–D), glenoid cavity of scapula (E), head of humerus (F) and styloid process of ulna/radius (G).

Half of the terrestrial species studied did not exhibit OA lesions on their bone remains, including Asiatic buffalo (n = 2), camel (n = 1), deer (n = 6), goat (n = 2), impala (n = 2), kangaroo (n = 1), lion (n = 2), mule (n = 1), pig (n = 7), rabbit (n = 8) and waterbuck (n = 1). The other species reported OA lesions in at least one bone location (Fig. 6).

Figure 6.

Figure 6

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Representative photos showing osteoarthritis (OA) lesions (arrows) in carpal joint of Malayan tapir (A), acetabulum of tiger (B), elbow joint of sheep (C), articular surface of distal phalanx of horse (D), tibial condyle of cat (E), femoral head of monkey (F), femoral head of dog (G), trochlear notch of hyena (H), articular surface of tarsal bone of cattle (I), lumbar vertebra of human (J), and phalanx of Asian elephant (K).

In dogs, the highest prevalence of OA lesions was found on the lumbar vertebrae (18.49%); otherwise, there were only five bones showing OA lesions: the TMJ, atlanto‐occipital joint, carpal articular surface of radius (right) and styloid process of ulna (right and left).

In cats, we found that 11 bone locations were affected by OA lesions, including: cervical vertebrae, thoracic vertebrae, lumbar vertebrae, sacral vertebrae, glenoid cavity of scapula (right and left), humeral trochlea (right and left), trochlear notch of ulna (right and left) and right femoral trochlea. The most frequent OA lesions were found in the thoracic vertebrae (7.89%), followed by the right trochlear notch of the ulna (5.13%).

In cattle, OA lesions could be observed on four types of bone, including the left articular surface of tarsal bone (100% because just one bone was noted), thoracic vertebrae (50%), lumbar vertebrae (50%) and right glenoid cavity of scapula (16.67%).

In horses, we found the highest occurrence of OA lesions in the lumbar vertebrae (27.27%), followed by sacral vertebrae (18.18%), and low percentages in eight other locations including the atlanto‐occipital joint, left head of radius, articular surface of tarsal bones (right and left), metacarpophalangeal joint of hindlimb (right and left) and interphalangeal joint of hindlimb (right and left).

Malayan tapir and sheep were reported as having 100% OA prevalence, due to a single animal of each species being available for observation. Malayan tapir displayed OA lesions in 20 bone parts, including the left glenoid cavity of the scapula, humeral head (right and left), left humeral trochlea, left head of radius, left carpal articular surface of radius, trochlear notch of ulna (right and left), styloid process of ulna (right and left), articular surface of carpal bone (right and left), metacarpophalangeal joint (right and left), interphalangeal joint (right and left), femoral trochlea (right and left), left tibial condyle and left distal articular surface of tibia. In sheep, only the right elbow joint (humeral trochlea, head of radius and trochlear notch of ulna) had OA lesions.

In hyenas, OA lesions were present on the thoracic vertebrae (50%), lumbar vertebrae (50%), right and left head of radius (50%), right and left trochlear notch of ulna (50%), and right and left carpal articular surface of radius (50%).

In tigers, OA lesions were found on the glenoid cavity of the scapula (right and left), humeral head (right and left), left humeral trochlea, articular surface of ilium (right and left), acetabular fossa (right and left) and femoral head (right and left); the highest percentage of OA lesions was found on the articular surface of the ilium (right and left) and acetabular fossa (right and left), in 33.33% of cases.

In monkeys (macaques), we found OA lesions on 16 parts of bones; the highest number of OA lesions (28.57%) was noted in five areas, including the thoracic vertebrae, lumbar vertebrae, left humeral head, right acetabular fossa and right femoral head.

Most elephant bones exhibited OA lesions, except the articular surface of carpal bone (right and left), metacarpophalangeal joint of forelimb (right and left), interphalangeal joint of forelimb (right and left) and femoral head (right and left). The highest prevalence of OA lesions on elephant bones was found on the thoracic and lumbar vertebrae (66.67%), followed by the femoral trochlea (50%).

Humans showed the highest prevalence of OA lesions when compared with other species; OA affected all of 45 observed bone locations. The highest percentage of OA lesions was found on the lumbar vertebrae (88.04%), and the lowest was found on the TMJ (0.22%).

Although the grading of OA lesions was done as mentioned previously, we noticed that terrestrial species had varying severity of OA lesions; for example, different sizes of osteophytes, both smaller (Fig. 6D) and larger (Fig. 6H) ones at the articular facet rim. In marine mammals (dolphin and dugong), formation of larger osteophytes can be observed in only a single sample (on the spinal column of a dolphin; Fig. 4E), while other samples showed small osteophytes at the articular facet rim.

OA lesions on 45 different bone locations in relation to sex in five mammalian species, and in relation to age in humans

As shown in Table 5, we compared the number of bones affected with OA between males and females in five mammalian species, including humans. There were no significant differences between sexes (P > 0.05) in cat, dog, dolphin and dugong. In contrast, in human remains we found that OA lesions in 24 bone locations were significantly more prevalent in males than in females (P < 0.05), whereas in 20 other bone locations there was no significant difference (P > 0.05). The highest odds ratio (OR), indicating a significant difference between sexes (P < 0.05), was found for the right glenoid cavity of scapula (OR = 2.40, P = 0.00), followed by lumbar vertebrae (OR = 2.29, P = 0.01) and carpal articular surface of radius (OR = 2.06, P = 0.00). Other bone parts (see reference numbers in Table 1) displaying a significant difference between sexes had ORs as follows: 12l (OR = 1.96); 18r, 18l, 19r and 19l (OR = 1.90); 13l (OR = 1.59); 10r (OR = 1.56); and 15r, 15l, 16r, 16l, 17r, 17l, 24r, 24l, 25r, 25l, 26r and 26l (OR = 1.50). Moreover, in human skeletal remains there was a considerable association (P < 0.05) between OA lesions and age in 43 out of 43 bone sites (Table 5).

Table 5.

Comparison of the number (percentage) of male and female animals affected with OA.a

Cat Dog Dolphin Dugong Human Human age correlation, P‐value
Male Female P‐value Male Female P‐value Male Female P‐value Male Female P‐value Male Female P‐value
1 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/40
(0) 		N.A. 0/40
(0) 		0/52
(0) 		N.A. 0/34
(0) 		0/29
(0) 		N.A. 1/285
(0.35) 		0/170
(0) 		1.00 N.A.
2 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/40
(0) 		N.A. 0/40
(0) 		1/52
(1.92) 		1 2/35
(5.71) 		0/29
(0) 		0.91 32/284
(11.27) 		11/170
(6.47) 		0.12 0.002
3 0/13
(0) 		1/17
(5.88) 		1 3/49
(6.12) 		4/40
(10) 		0.77 2/39
(5.13) 		2/47
(4.26) 		1 2/45
(4.44) 		4/43
(9.30) 		0.63 243/271
(89.67) 		141/172
(81.98) 		0.05 0.002
4 0/13
(0) 		3/17
(17.65) 		0.32 4/49
(8.16) 		6/40
(15) 		0.49 1/39
(2.56) 		1/47
(2.13) 		1 1/45
(2.22) 		2/43
(4.65) 		0.96 243/272
(89.33) 		142/172
(82.56) 		0.05 0.002
5 0/13
(0) 		1/16
(6.25) 		1 6/48
(12.5) 		3/40
(22.5) 		0.33 1/39
(2.56) 		5/47
(10.63) 		0.29 2/45
(4.44) 		5/43
(11.63) 		0.39 248/271
(91.51) 		142/172
(82.56) 		0.01 0.002
6 0/13
(0) 		1/16
(6.25) 		N.A. 2/48
(4.17) 		3/41
(7.32) 		0.85 N.D. N.D. N.A. N.D. N.D. N.A. 244/289
(84.43) 		144/178
(80.89) 		0.39 0.002
7 0/13
(0) 		0/17
(0) 		N.A. 0/45
(0) 		0/42
(0) 		N.A. N.D. N.D. N.A. N.D. N.D. N.A. N.D. N.D. N.A. N.A.
8r 0/13
(0) 		1/17
(5.88) 		1 0/48
(0) 		4/40
(10) 		0.08 1/42
(2.38) 		5/50
(0) 		0.87 5/39
(12.82) 		1/39
(2.56) 		0.20 207/289
(71.63) 		109/179
(60.89) 		0.39 0.002
8l 0/13
(0) 		1/17
(5.88) 		1 1/47
(2.13) 		4/40
(10) 		0.26 1/42
(2.38) 		5/50
(10) 		0.50 4/39
(10.26) 		2/38
(5.26) 		0.69 216/288
(75) 		102/180
(56.67) 		0.00 0.002
9r 0/13
(0) 		0/17
(0) 		N.A. 1/46
(2.17) 		4/40
(10) 		0.14 0/35
(0) 		0/42
(0) 		N.A. 3/38
(8.82) 		0/36
(0) 		0.21 143/289
(49.48) 		71/180
(39.44) 		0.04 0.002
9l 0/13
(0) 		0/17
(0) 		N.A. 2/47
(4.26) 		4/40
(10) 		0.31 0/35
(0) 		0/42
(0) 		N.A. 2/35
(5.71) 		0/33
(0) 		0.49 140/289
(48.44) 		69/178
(38.76) 		0.05 0.002
10r 0/13
(0) 		1/17
(5.88) 		1 0/46
(0) 		3/40
(7.5) 		0.19 5/35
(14.29) 		5/42
(11.90) 		1 2/35
(5.71) 		0/35
(0) 		0.33 106/289
(36.68) 		53/180
(29.44) 		0.03 0.002
10l 0/13
(0) 		1/17
(5.88) 		1 0/47
(0) 		2/40
(5) 		0.40 5/35
(14.29) 		6/42
(14.29) 		0.70 1/35
(2.86) 		0/33
(0) 		1 107/287
(37.28) 		52/179
(29.05) 		0.07 0.002
11r 0/13
(0) 		0/17
(0) 		N.A. 1/45
(2.22) 		3/40
(7.5) 		0.52 4/35
(11.43) 		3/37
(8.11) 		0.93 0/28
(0) 		0/27
(0) 		N.A. 95/289
(32.87) 		50/180
(27.78) 		0.22 0.002
11l 0/13
(0) 		0/17
(0) 		N.A. 1/46
(2.17) 		3/40
(7.5) 		0.51 4/35
(11.43) 		3/38
(7.89) 		0.90 0/28
(0) 		0/27
(0) 		N.A. 98/291
(33.68) 		56/180
(31.11) 		0.56 0.002
12r 0/13
(0) 		0/17
(0) 		N.A. 0/45
(0) 		0/40
(0) 		N.A. 0/35
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/26
(0) 		N.A. 165/289
(57.09) 		63/180
(35) 		0.00 0.002
12l 0/13
(0) 		0/17
(0) 		N.A. 0/46
(0) 		0/40
(0) 		N.A. 0/35
(0) 		1/38
(2.63) 		1 0/28
(0) 		0/26
(0) 		N.A. 146/291
(50.17) 		67/180
(37.22) 		0.00 0.002
13r 0/13
(0) 		2/17
(11.76) 		0.59 1/46
(2.17) 		3/40
(7.5) 		0.51 4/35
(11.43) 		3/37
(8.11) 		0.93 0/28
(0) 		0/26
(0) 		N.A. 175/288
(60.76) 		89/180
(49.44) 		0.10 0.006
13l 0/13
(0) 		1/17
(5.88) 		1 1/47
(2.13) 		1/40
(2.5) 		0.49 4/35
(11.43) 		3/37
(8.11) 		0.93 0/28
(0) 		0/26
(0) 		N.A. 200/288
(69.44) 		84/179
(46.93) 		0.01 0.002
14r 0/13
(0) 		0/17
(0) 		N.A. 0/46
(0) 		0/40
(0) 		N.A. 0/35
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/26
(0) 		N.A. 97/288
(33.68) 		47/180
(26.11) 		0.03 0.002
14l 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/40
(0) 		N.A. 0/39
(0) 		0/34
(0) 		N.A. 0/28
(0) 		0/26
(0) 		N.A. 95/288
(32.99) 		49/179
(27.37) 		0.03 0.002
15r 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/42
(0) 		N.A. 0/34
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/27
(0) 		N.A. 130/289
(44.98) 		63/176
(35.79) 		0.04 0.002
15l 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/42
(0) 		N.A. 0/34
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/27
(0) 		N.A. 130/289
(44.98) 		63/176
(35.79) 		0.04 0.002
16r 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/42
(0) 		N.A. 0/34
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/27
(0) 		N.A. 130/289
(44.98) 		63/176
(35.79) 		0.04 0.002
16l 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/42
(0) 		N.A. 0/34
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/27
(0) 		N.A. 130/289
(44.98) 		63/176
(35.79) 		0.04 0.002
17r 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/42
(0) 		N.A. 0/34
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/27
(0) 		N.A. 130/289
(44.98) 		63/176
(35.79) 		0.04 0.002
17l 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		0/42
(0) 		N.A. 0/34
(0) 		0/37
(0) 		N.A. 0/28
(0) 		0/27
(0) 		N.A. 130/289
(44.98) 		63/176
(35.79) 		0.04 0.002
18r 0/13
(0) 		0/17
(0) 		N.A. 8/49
(16.33) 		4/40
(10) 		0.57 N.D. N.D. N.A. 0/29
(0) 		0/22
(0) 		N.A. 229/289
(79.24) 		121/180
(67.22) 		0.00 0.002
18l 0/13
(0) 		0/17
(0) 		N.A. 8/49
(16.33) 		4/40
(10) 		0.57 N.D. N.D. N.A. 0/29
(0) 		0/22
(0) 		N.A. 229/289
(79.24) 		121/180
(67.22) 		0.00 0.002
19r 0/13
(0) 		0/17
(0) 		N.A. 8/49
(16.33) 		4/40
(10) 		0.57 N.D. N.D. N.A. 0/29
(0) 		0/22
(0) 		N.A. 229/289
(79.24) 		121/180
(67.22) 		0.00 0.002
19l 0/13
(0) 		0/17
(0) 		N.A. 8/49
(16.33) 		4/40
(10) 		0.57 N.D. N.D. N.A. 0/29
(0) 		0/22
(0) 		N.A. 229/289
(79.24) 		121/180
(67.22) 		0.00 0.002
20r 0/13
(0) 		0/17
(0) 		N.A. 3/46
(6.52) 		1/40
(2.5) 		0.27 N.D. N.D. N.A. N.D. N.D. N.A. 93/273
(34.07) 		58/177
(32.77) 		0.79 0.002
20l 0/13
(0) 		0/17
(0) 		N.A. 5/46
(10.86) 		0/39
(0) 		0.09 N.D. N.D. N.A. N.D. N.D. N.A. 93/272
(34.19) 		55/174
(31.61) 		0.73 0.002
21r 0/13
(0) 		1/17
(5.88) 		1 5/46
(10.86) 		0/39
(0) 		0.94 N.D. N.D. N.A. N.D. N.D. N.A. 131/276
(47.46) 		91/170
(53.53) 		0.79 0.006
21l 0/13
(0) 		0/17
(0) 		N.A. 0/46
(0) 		0/39
(0) 		N.A. N.D. N.D. N.A. N.D. N.D. N.A. 140/273
(51.28) 		89/169
(52.66) 		0.46 0.002
22r 0/13
(0) 		1/17 (5.88) 1 0/47
(0) 		1/40
(2.5) 		0.93 N.D. N.D. N.A. N.D. N.D. N.A. 138/277
(49.82) 		83/169
(49.11) 		0.74 0.001
22l 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		1/39
(2.56) 		0.92 N.D. N.D. N.A. N.D. N.D. N.A. 138/278
(49.64) 		83/169
(49.11) 		0.99 0.001
23r 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		1/40
(2.5) 		0.93 N.D. N.D. N.A. N.D. N.D. N.A. 135/277
(48.74) 		75/169
(44.38) 		0.41 0.020
23l 0/13
(0) 		0/17
(0) 		N.A. 0/47
(0) 		1/39
(2.56) 		0.93 N.D. N.D. N.A. N.D. N.D. N.A. 134/278
(48.20) 		74/169
(43.79) 		0.41 0.002
24r 0/13
(0) 		0/17
(0) 		N.A. 1/47
(2.13) 		0/42
(0) 		1 N.D. N.D. N.A. N.D. N.D. N.A. 114/285
(40) 		47/172
(27.33) 		0.04 0.002
24l 0/13
(0) 		0/17
(0) 		N.A. 1/47
(2.13) 		0/42
(0) 		1 N.D. N.D. N.A. N.D. N.D. N.A. 114/285
(40) 		47/172
(27.33) 		0.04 0.002
25r 0/13
(0) 		0/17
(0) 		N.A. 1/47
(2.13) 		0/42
(0) 		1 N.D. N.D. N.A. N.D. N.D. N.A. 114/285
(40) 		47/172
(27.33) 		0.04 0.002
25l 0/13
(0) 		0/17
(0) 		N.A. 1/47
(2.13) 		0/42
(0) 		1 N.D. N.D. N.A. N.D. N.D. N.A. 114/285
(40) 		47/172
(27.33) 		0.04 0.002
26r 0/13
(0) 		0/17
(0) 		N.A. 1/47
(2.13) 		0/42
(0) 		1 N.D. N.D. N.A. N.D. N.D. N.A. 114/285
(40) 		47/172
(27.33) 		0.04 0.002
26l 0/13
(0) 		0/17
(0) 		N.A. 1/47
(2.13) 		0/42
(0) 		1 N.D. N.D. N.A. N.D. N.D. N.A. 114/285
(40) 		47/172
(27.33) 		0.04 0.002
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a

The number of male and female samples was not equal to the total number shown in Tables 2, 3, 4 because some bones were of unknown sex.

1 = TMJ, 2 = atlanto‐occipital joint, 3 = cervical vertebrae, 4 = thoracic vertebrae, 5 = lumbar vertebrae, 6 = sacral vertebrae, 7 = coccygeal vertebrae, 8 = glenoid cavity of scapula, 9 = humeral head, 10 = humeral trochlea, 11 = head of radius, 12 = carpal articular surface of radius, 13 = trochlear notch of ulna, 14 = styloid process of ulna, 15 = articular surface of carpal bone, 16 = metacarpophalangeal joint, 17 = interphalangeal joint, 18 = articular surface of ilium, 19 = acetabular fossa, 20 = femoral head, 21 = femoral trochlea, 22 = tibial condyle, 23 = distal articular surface of tibia, 24 = articular surface of tarsal bones, 25 = metacarpophalangeal joint, 26 = interphalangeal joint, l = left, r = right, N.A. = not analyzed, N.D. = not determined.

Discussion

The highlight of our investigation is that this is the first report to provide evidence of the existence of OA lesions in the skeletal remains of dugongs, and also in dolphins, marine mammals in the family Delphinidae. Moreover, our findings indicated that, in addition to humans and other companion animals such as dogs, cats and horses, many other terrestrial animal species also exhibit signs of OA. In this study, we explored OA lesions of the bones in the whole body of the studied species, leading to the discovery of particular joints that are frequently affected by OA, such as the cervical vertebrae and proximal part of the hindlimb and forelimb.

Bones from a total of 24 mammalian species, including marine mammals (dolphin, dugong) and wild animals (e.g. Asian elephant, hyena, Malayan tapir, monkey and tiger), were found to exhibit OA lesions, similar to humans and several domestic animal species (cat, dog, horse and sheep). In contrast, other domestic animals (Asiatic buffalo, rabbit, goat, mule and pig) and terrestrial animals (camel, deer, impala, kangaroo, lion and waterbuck) showed no signs of OA. When considering OA occurrence in relation to the phylogenic tree (Fig. 1), it is postulated that most species of the even‐toed ungulates (Artiodactyla) are prone to be invulnerable to OA, but the odd‐toed ungulates (primates, felines, sirenians and proboscidians) appear to have a high prevalence of OA. One possible reason for the divergence of OA occurrence might be differences in anatomy, in particular between odd‐ and even‐toed ungulates. Moreover, we noted that omnivores and carnivores seem to have a high OA prevalence, while only a slight OA occurrence was observed in herbivores (odd‐toed ungulates, elephants and dugongs). Another possible factor influencing OA occurrence is diet or foraging behavior. However, because of the limited number of some samples, no definitive conclusions can be made. Previously, Greer et al. (1977) reported the presence of OA lesions in numerous wild animal species, including bear (family Ursidae), bushbuck (Tragelaphus spp.), blackbuck (Antilope sp.), gazelle (Gazella spp.), addax (Addax nasomaculatus), American bison (Bison bison), oryx (Oryx gazella), white‐tailed deer (Odocoileus virginianus), barasingha (Cervus duvauceli), sika (C. nippon), wapiti (C. canadensis), dromedary (Camelus dromedarius), Burchell's zebra (Equus burchellii), giant anteater (Myrmecophaga tridactyla), aardvark (Orycteropus afer), African lion (Felis leo), cheetah (Acinonyx jubatus), gray wolf (Canis lupus), wolverine (Gulo gulo) and gray fox (Urocyon cinereoargenteus); in all of these species, the most frequent occurrence of OA lesions was on the vertebrae. A previous study (Föllmi et al. 2007) also observed arthrosis and arthritis (which developed into OA at the final stage of the disease) in wildlife animals living in zoos, such as Ursidae, Felidae, Canidae, Camelidae, Elephantidae, Rhinocerotidae and Bovidae. Felid species (cat, lion and tiger) were surveyed for OA lesions, which were noted in cats and tigers but not lions. Another study of 13 lions (Panthera leo), 16 tigers (Panthera tigris), four leopards (Panthera pardus), one snow leopard (Panthera uncia) and three jaguars (Panthera onca) found that eight individuals (lions = 3, tigers = 4, leopard = 1) had degenerative spinal disease (Kolmstetter et al. 2000). Because they are primates, monkeys, like humans, are susceptible to OA (Duncan et al. 2012); for this reason they have been used as a model for studying OA in humans (Carlson et al. 1994; Little & Smith, 2008). In fact, a recent study found that monkeys had a higher rate of OA than humans; on the other hand, chimpanzees (Pan troglodytes schweinfurthii; Pan troglodytes troglodytes), lowland gorillas (Gorilla gorilla gorilla) and bonobos (Pan paniscus) exhibited a comparatively lower prevalence of OA (Duncan et al. 2012). Differences in the obtained results of these reports may be due to the variety of monkey species and joints studied.

Among marine mammals, there have been no reports on the existence of OA in dugongs, while a few studies have noted the presence of arthritis lesions in dolphins due to bacterial infection (Davison et al. 2013, 2014) or unknown causes (Kompanje, 1995; Watson et al. 2008; Gomerčić et al. 2009). In dolphins, most arthritis lesions have been observed in the vertebrae (Kompanje, 1995; Gomerčić et al. 2009; Davison et al. 2013, 2014), while some have been found on the appendicular skeleton (Watson et al. 2008). On the other hand, our exploration for OA lesions across a wide range of mammalian species revealed that the largest number of OA lesions appeared on the left humeral trochlea (13 individuals or locations or species out of 95 animals) followed by the right humeral trochlea (12 of 95 animals) and the lumbar vertebrae (nine of 109 animals). In dugongs, the highest number of OA lesions was found on the lumbar vertebrae (eight of 91 animals), followed by the glenoid cavity of the scapula (seven out of 82 and 81 animals, right and left side, respectively).

When considering the influence of sex on OA occurrence in the skeletal remains of various species, chi‐square tests indicated that the prevalence of OA in cat, dog, dolphin and dugong was unlikely to be related to sex. However, in humans we found a remarkably higher presence of OA lesions in males than females. This result was contrary to a report by Duncan et al. (2012), who observed no significant difference between males and females in the prevalence of spinal OA in humans, while the occurrence of spinal OA in rhesus monkeys was higher in males, consistent with our results for humans. Many factors, such as age, joint, body mass, behavior, occupation and lifestyle, can lead to this discrepancy between males and females (Corti & Rigon, 2003; Haara et al. 2003; Srikanth et al. 2005). We believe that our study is more reliable than other studies because of the large number of observations in 44 different bone locations of the human skeleton, with an age range between 15 and 100 years, and because of the homogeneous source of bones (all of which were acquired from northern Thai people). We propose that human males appear to be more susceptible to OA than females.

In addition to the influence of sex on the prevalence of OA lesions, age might also be implicated in the appearance of OA in mammalian species, both marine and terrestrial. The human skeletons in this study could possibly be used to exemplify this phenomenon in marine mammals such as dolphins and dugongs, as: (i) age data for individual human skeletons were recorded; and (ii) the life span of humans is similar to that of dolphins, 55–60 years (Ridgway & Harrison, 1999), and dugongs, 65–70 years (Baldwin, 1985). A substantial association between human age and OA lesions among 43 bone locations was seen, which is in accordance with previous studies (Corti & Rigon, 2003; Haara et al. 2003). OA lesions in all joints tend to increase with increased age, indicating that age is a risk factor of OA appearance (Haara et al. 2003; Srikanth et al. 2005). We believe that this phenomenon might occur in marine mammalian species in a pattern similar to that of humans, a hypothesis that merits further study.

Currently, many etiologies of OA have been established, such as articular cartilage or joint abnormality, abnormal force on normal articular cartilage or joint, infection, hormonal imbalance, age, and obesity or body weight (Sarzi‐Puttini et al. 2005; Buckwalter & Martin, 2006; Marshall et al. 2009). Aquatic exercise is one of the recommended rehabilitation therapies for patients with OA because the buoyancy, hydrostatic pressure, viscosity, resistance and surface tension of water increase the efficacy of the exercise, together with a reduction of weight bearing during exercise, contributing to alleviating the severity of OA (Nganvongpanit et al. 2014; Bartels et al. 2016). This would seem to imply a low prevalence of OA in marine mammals, because their joints do not bear their entire body weight. However, our findings disclosed a high incidence of OA in both dolphins and dugongs, with an average prevalence of 3.33% (range 0–13.68%) in dolphins and 2.44% (range 0–8.79%) in dugongs; OA lesions of the articular facet were found in 52% and 62.06% of afflicted dolphins and dugongs, respectively. The incidence of OA lesions in dolphins and dugongs appeared to be higher than in cats (0.89%, range 0–7.89%), but not dogs (3.94%, range 0–18.49%) or, especially, humans (48.93%, range 0.22–88.04%). Thus, we questioned why dolphins and dugongs are affected with OA as, in accordance with the principle of buoyancy in water, marine mammals would not experience OA conditions directly caused by body weight. We assumed that it might be secondary OA caused by another disease or condition, such as obesity (high body weight), repeated trauma or abnormal joint at birth, because several studies have reported the appearance of arthritis lesions during necropsy (Kompanje, 1995; Föllmi et al. 2007; Gomerčić et al. 2009); moreover, these animals are continually moving during their entire lives, which in turn is the cause of joint loading in the vertebral column and trauma from foraging, especially in canivores such as felines. A study on the etiology of OA in marine mammals would be illuminating as to why a high incidence of OA can be found in marine mammals in spite of their living in an aquatic habitat. Although OA is not a main cause of death, animals with OA will suffer from joint pain and, in turn, impaired mobility. Most marine animals must constantly move in order to remain afloat in the water. Hence, marine animals with OA will likely suffer from joint pain throughout their lifetimes. However, most of the evaluated severity of OA in marine mammal bones was a mild grade (Figs 3 and 4), and only one case of severe OA was found (in a dolphin; Fig. 3E). On the other hand, most of the terrestrial mammals studied showed a greater variety of OA lesions, i.e. mild, moderate and severe grade (Fig. 5). It is plausible that the properties of water play a significant role in the alleviation of OA progression. Meanwhile, we postulated that living in an aquatic habitat may be a factor in both the etiology of OA and the reduction of OA progression, as a result of the high prevalence of mild OA. However, to prove this hypothesis, further work needs to be performed.

In this study, we encountered three limitations. Firstly, this study could not analyze the risk factors of OA, such as age, sex and breed, in all species because of a lack of information. Secondly, the number of animals in each species was low, especially among wild animals. Finally, the OA grade could not be evaluated because the standard grading system using dry bones was not available.

In conclusion, OA can occur in marine mammals, similar to terrestrial mammals, but the severity of OA might be less in marine mammals due to the fact that the properties of water facilitate support of the joints for bearing their body weight while moving. The present findings offer strong evidence that both terrestrial and marine mammals can experience an OA condition, possibly indicating that OA is the most common joint disease in all mammalian species.

Conflict of interest

The authors declare that they have no conflict of interest regarding the publication of this paper.

Author contributions

R.S. and P.K. evaluated OA lesions in bones and analyzed all data in this study. V.P. and K.B. assisted in the statistical investigation. R.N., P.K., K.K., R.C., T.A., C.T. and P.M. examined bone samples. K.N. was the major contributor, who designed and conducted this study and wrote the manuscript. All authors have read and approved the manuscript for publication.

Acknowledgements

The authors are grateful for research funding from the Faculty of Veterinary Medicine, Chiang Mai University, and additional funding through the Chiang Mai University research administration office that provided the budget to our Excellence Center in Osteology Research and Training Center, Chiang Mai University.

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