Puma Jairo.pdf

J. Comp. Path. 2017, Vol. 156, 251e263

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DISEASE IN WILDLIFE OR EXOTIC SPECIES

Dental and Temporomandibular Joint Pathology of the California Mountain Lion (Puma concolor couguar) A. Aghashani*, A. S. Kim*, P. H. Kass† and F. J. M. Verstraete* * Department of Surgical and Radiological Sciences and † Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, California, USA

Summary Skulls from 91 California mountain lions (Puma concolor couguar) were examined macroscopically and radiographically. The majority of the skulls were from young adult animals (57.1%). The skull specimens were from 42 male (46.1%) and 34 female (37.4%) animals, while the gender was unknown for the remainder. The majority (94.5%) of teeth were present for examination. Only 11 teeth were identified as absent congenitally; five of these teeth were maxillary first molar teeth and three were maxillary second premolar teeth. Abnormal tooth morphology was identified in 3.5% of teeth. The most common abnormality in tooth form was abnormally large crowns of the maxillary first molar teeth. Teeth with an abnormal number of roots were uncommon (n ¼ 21). Ninety-one teeth were found to have an abnormal number of roots, most often two-rooted maxillary first molar teeth instead of the expected one root. The most prevalent dental lesions found in the California mountain lion were attrition/abrasion (93.4%), tooth fractures (80.2%) and periodontitis (38.5%). Less common dental lesions were tooth resorption (n ¼ 32 teeth) and endodontal disease (n ¼ 29 teeth). Ó 2016 Elsevier Ltd. All rights reserved. Keywords: California mountain lion; dental pathology; Puma concolor couguar; temporomandibular joint

Introduction The mountain lion (Puma concolor), with its slender body, long back legs and large feet is greater in size when compared with other members of the Felidae family. The average body length of a mountain lion ranges from 105 to 196 cm; their long tails can add 67e78 cm to this length (Grzimek, 2004). The body weight of a mountain lion ranges from 29 to 100 kg. With the exception of the males being larger and more muscular, there is little sexual dimorphism in this species. The current habitat range of the mountain lion includes southern Canada through the USA, through South America and to the southern tip of Chile (Nielsen et al., 2015). From the arid desert to various

forest habitats, the mountain lion can inhabit a broad array of environments (Grzimek, 2004). Six extant mountain lion subspecies are recognized, five of which are solely found in Latin America. The California mountain lion (Puma concolor couguar, formerly known as a separate subspecies P. c. californica) inhabits southern Oregon, California and Nevada. Males commonly have larger home ranges than females; male territories tend to encompass one or more female territories. Mountain lions tend to avoid physical aggression via scent marking, calling and through visual signals like claw marks on trees. If physical aggression does occur, it often occurs during competition for a female exhibiting oestrus or due to a territorial disturbance (Grzimek, 2004). Mountain lions are considered to be a threat to livestock and as a result, they are regularly persecuted by

Correspondence to: F. J. M. Verstraete (e-mail: [email protected]). 0021-9975/$ - see front matter http://dx.doi.org/10.1016/j.jcpa.2016.11.269

Ó 2016 Elsevier Ltd. All rights reserved.

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ranchers. Mountain lions are known to take calves and sheep, but true predation rates are low. Although historically infrequent, mountain lion attacks on people are a growing concern. These attacks have been gradually increasing in occurrence due to the close proximity of mountain lions to settled areas in western North America (Grzimek, 2004). Since 1890, there have been 16 verified mountain lion attacks on people in California; six of these attacks were fatal (Department of Fish and Wildlife, 2007). Although mountain lions are hunted legally in many states across the USA, mountain lion hunting was banned by a referendum in California in 1990 (Nielsen et al., 2015). The IUCN Red List of Threatened Species categorizes P. concolor in the category of ‘Least Concern’ due to their wide-distribution in the Western Hemisphere. Populations are considered healthy enough for regulated harvest in western North America, but are declining in other parts of the USA (Nielsen et al., 2015). The two largest threats to mountain lion populations include habitat loss and loss of prey species. Felidae are typically strict carnivores who sit at the top of the food chain. Larger Felidae prefer ungulates, but feed opportunistically on any available prey, including insects, birds and small rodents. Deer make up 60e80% of the mountain lion’s diet in North America. The mean weight of prey taken by the mountain lion is 39e48 kg (Nielsen et al., 2015). The adult mountain lion has a total of 30 teeth (Fig. 1), with a dental formula of I 3/3, C 1/1, P3/2, M 1/1 ¼ 30. The maxillary second premolar tooth has received considerable attention in the zoological

Fig. 1. An adult male mountain lion skull with normal dentition.

literature, as it is believed that this tooth is disappearing over the course of evolution. This tooth persists in the mountain lion, but is lost in the bobcat (Lynx rufus) (Verstraete and Terpak, 1997; Aghashani et al., 2016). Felidae hunt prey using powerful jaws and secodont dentition for cutting and gnawing meat. Large felids tend to gnaw meat off of the bone or pull the meat off in pieces to swallow whole; they complete this shearing action by grasping the meat with their maxillary fourth premolar, mandibular first molar, incisor and canine teeth by jerking the head up. Felidae also have a rough tongue covered with conical papillae used to lick bones clean (Grzimek, 2004). The integrity and functionality of mountain lion dentition is an integral component of their overall health. Without functional dentition, the ability to hunt and kill prey is greatly diminished and can contribute to morbidity and mortality of the species. Documentation of dental pathology of wild animals, in particular that of wild felids, is an area of open research. Dental lesions are common in the family Felidae and can be a significant source of morbidity and mortality (Verstraete et al., 1996a,b; Aghashani et al., 2016). These lesions have only begun to be classified in wild felids. The aim of this study was to provide detailed information regarding the dental and temporomandibular joint pathology of the California mountain lion. It was hypothesized that dental lesions in wild felines may be similar to those found in domestic and other wild felids, based on similarities or differences in disease susceptibility, behaviour and diet.

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Table 1 Congenital, developmental and acquired abnormalities and inclusion criteria Observation

Criteria

Tooth artefactually absent

Jaw fragment missing or tooth absent, but a well-defined, sharp-edged, normally shaped, empty alveolus present; no pathological signs in the alveolar bone; tooth presumed lost during preparation or post-mortem manipulation of the skull. Tooth absent; alveolus or remnant alveolus visible; alveolar bone shows pathological signs (i.e. rounding of the alveolar margin, shallow alveolus, periosteal reaction on alveolar bone, increased vascular foramina). Tooth and alveolus absent; smooth, morphologically normal bone present at the site; no physical space for that tooth to have occupied. Presence of an abnormally shaped crown, as in two fused teeth. One, two or three roots. Presence of a supernumerary tooth adjacent to an expected tooth (or alveolus). A persistent deciduous tooth adjacent to an erupted or unerupted permanent tooth. Rounding or flattening of the cusp tip; exposure of dentine, with or without tertiary dentine formation. A chip or fracture in the enamel only. A fracture involving enamel and dentine, but not exposing the pulp. A fracture involving enamel, dentine and cementum, with pulp exposure. A fracture involving enamel, dentine and cementum, but not exposing the pulp.

Tooth absent (presumably acquired) Tooth absent (presumably congenital) Malformed tooth Number of roots Supernumerary tooth Persistent deciduous tooth Attrition/abrasion Enamel fracture Uncomplicated crown fracture Complicated crown fracture Uncomplicated crowneroot fracture Complicated crowneroot fracture Root fracture Periapical lesions

A fracture involving enamel, dentine and cementum, with pulp exposure. A fracture affecting dentine, cementum and the pulp. Macroscopically visible periapical bone loss, root tip resorption, sinus tract formation originating peri-apically or obvious focal periosteal reaction overlying the apex. Evidence of increased vascularity at the alveolar margin (more prominent vascular foramina in, and slightly rougher texture of, the bone of the alveolar margin). Rounding of the alveolar margin; moderate horizontal or vertical bone loss. Widening of the periodontal ligament space; severe horizontal or vertical bone loss; tooth mobile in the alveolus. Irregular pitting or a band-shaped absence or thinning of the enamel, consistent with the clinical signs of enamel hypoplasia.

Periodontitis stage 2 Periodontitis stage 3 Periodontitis stage 4 Enamel hypoplasia

Materials and Methods Macroscopic examination of 29 skull specimens from the Department of Ornithology and Mammalogy, California Academy of Sciences, San Francisco, and 62 skull specimens from the Museum of Vertebrate Zoology, University of California, Berkeley, was performed. Both collections of skulls were obtained from carcass recovery and donations from the public and government agencies. Each skull had been previously labelled with a unique catalogue number, the collec-

tion date (if known), collection location and sex of the animal (if known). Each skull specimen was categorized as ‘young adult’ or ‘adult’. Age status of the skulls was determined based on the stage of development of the teeth, evaluated through dental radiography. ‘Juveniles’ were identified through the presence of deciduous or mixed dentition and excluded from the study. The teeth and surrounding bony tissues were inspected systematically, according to predefined criteria (Table 1) utilized in previous studies (Verstraete

Table 2 Stages of tooth resorption and inclusion criteria Observation Tooth resorption stage 2 Tooth resorption stage 3 Tooth resorption stage 4 Tooth resorption stage 5

Criteria Moderate dental hard tissue loss (i.e. cementum or cementum and enamel with loss of dentine that does not extend to the pulp cavity). Deep dental hard tissue loss (i.e. cementum or cementum and enamel with loss of dentine that extends to the pulp cavity); most of the tooth retains its integrity. Extensive dental hard tissue loss (i.e. cementum or cementum and enamel with loss of dentine that extends to the pulp cavity); most of the tooth has lost its integrity. Remnants of dental hard tissue are visible only as irregular radiopacities, and gingival covering is complete.

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Table 3 Temporomandibular joint osteoarthritis scoring criteria Observation

Criteria

TMJ-OA 1

Mild TMJ-OA: early lesions of periarticular new bone formation/osteophytes with minimal or no subchondral bone change. Moderate TMJ-OA: presence of periarticular new bone formation and/or subchondral bone changes that are more pronounced. Severe TMJ-OA: signs of TMJ-OA 1 and 2 present and more pronounced or presence of subchondral bone lysis, or partial/complete ankylosis.

TMJ-OA 2

TMJ-OA 3

TMJ-OA, temporomandibular joint osteoarthritis.

et al., 1996a,b; Abbott and Verstraete, 2005; Aghashani et al., 2016). The presence or absence (i.e. congenital, acquired or artefactual) of all teeth was recorded. Empty tooth alveoli with sharply delineated edges were considered to reflect tooth loss during skull preparation. The number of teeth present was used to calculate the prevalence of attrition/abrasion, fractures, periodontitis, tooth resorption and endodontal disease. Teeth were assessed for normal or abnormal form through gross and radiographical examination. The number of roots was determined by assessing the visible part of the coronal root, with radiographical evaluation of the roots. The majority of teeth were glued into the alveoli during preparation. If the tooth could be removed, the roots were examined. The presence of supernumerary teeth adjacent to normal teeth was recorded, as well as the presence of any persistent deciduous teeth. The teeth were examined for signs of attrition and/or abrasion (i.e. flattening of the tooth cusp or exposed dentine), although severity was not recorded. Any defects to the enamel were noted, particularly signs of enamel hypoplasia. Tooth fractures were classified according to the World Health Organization classification of human dental fractures, as modified for use in carnivores (Verstraete, 2003). Periapical lesions communicating with the tooth in question were noted during the macroscopic examination and later examined radiographically. Teeth with periapical lesions resulting from complicated tooth fractures were examined radiographically for additional indications of endodontal disease. Additional signs of endodontal disease can include external inflammatory root resorption as well as failure of the pulp cavity to narrow. The periodontal status of the teeth was assessed based on a well-established classification system developed for use with skull specimens (Verstraete et al., 1996a). In this classification system, periodontitis stages 2e4

were assigned based on bony lesions indicative of periodontitis. Stage 1 was excluded, as this refers to gingivitis, a soft tissue lesion that cannot be assessed on skull specimens. The extent of tooth resorption was noted and classified according to predefined criteria (Table 2) established by the American Veterinary Dental College (2015). Feline tooth resorption was differentiated from external inflammatory root resorption by a lack of an external inflammatory lesion in the periodontal ligament or tissues surrounding the teeth (Peralta et al., 2010). Tooth resorption is characterized by osteoclastic destruction that results in replacement of the tooth roots by osteoclasts. Radiographically, the tooth appears to be less radiopaque and may have loss of the periodontal ligament space (Niemiec and DuPont, 2010). Stage 1 classification of tooth resorption was not included, as it is virtually impossible to determine this stage of tooth resorption grossly. Stage 4 classification of tooth resorption was not given a sub-classification during the radiographical examination. Stage 5 classification of tooth resorption was initially excluded, but later evaluated during radiographical examination since radiographs are required to classify this stage of tooth resorption. Any additional relevant observations were made, such as the presence of head trauma or gunshot wounds to the skull. The temporomandibular joint (TMJ) and surrounding bony tissues were evaluated for signs of disease. A semiquantitative scoring system

Fig. 2. Distribution of the age and sex of skulls examined.

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(Table 3) for osteoarthritis was applied to each diseased TMJ (Arzi et al., 2013). Any malocclusion or bony abnormalities were noted. The second part of the study included obtaining dental radiographs of the teeth. A previously identified limitation to this type of study is that it is difficult to assess the tooth roots; this limitation was addressed with the addition of dental radiographs in order to allow for more accurate diagnosis of dental lesions and anatomical variations. Radiographs were obtained using a portable handheld dental Xray unit (Nomad Pro-Vet, Aribex, Charlotte, North Carolina, USA), intraoral phosphor storage plates size 2 and 4 (ScanX, Air-Techniques, Melville, New York, USA) and diagnostic imaging software (Metron, EponaTech, Creston, California, USA). A standard 10 maxillary and mandibular radiographical views were obtained for each skull specimen. These views included the left/right maxillary premolaremolar quadrants (i.e. extraoral near-parallel technique), the mandibular and maxillary incisor and canine occlusal views (i.e. bisecting angle technique), the left/right mandibular premolaremolar quadrants (i.e. parallel technique) and the left/right lateral maxillary and mandibular canine teeth (i.e. bisecting angle technique). Each radiograph was evaluated and compared with the findings on gross examination. The presence or absence (i.e. congenital, acquired or artefactual loss) of all teeth was verified. The number of roots, abnormal crowns and abnormal root formation was confirmed radiographically for each tooth. Tooth fractures were confirmed and the classification of the fracture type was verified (Verstraete, 2003). Periodontitis was confirmed and the stage assigned was verified. Tooth resorption was evaluated and the stage assigned was confirmed. Endodontal disease (e.g. failure of the pulp cavity to narrow) and periap-

Fig. 3. Bilateral congenitally-absent maxillary second premolar teeth (double arrow). Scale, 1 cm.

ical disease, including external inflammatory root resorption (Peralta et al., 2010) were also documented. The prevalence of dental lesions was compared between skulls from mountain lions of different age (adult and young adult) and sex (male, female and unknown) using Fisher’s exact test. Count data for dental pathology were compared between age and sex groups using the KruskaleWallis test, followed by post-hoc pairwise ManneWhitney test using a BonferronieHolm adjustment for multiple comparisons. P <0.05 was considered significant.

Results Of the 91 skull specimens, 46.1% were from male mountain lions, 37.4% were from female mountain lions and 16.5% were from animals of unknown sex. Adult mountain lion skull specimens comprised 42.9% of the skulls examined, while young adult mountain lion skull specimens comprised 57.1% of the skulls examined. Fig. 2 illustrates the age and sex distribution of the skulls examined. Presence of Teeth

The total number of teeth available for examination was 2,580 (94.5%), out of a potential total of 2,730 teeth. Artefactual tooth absence accounted for 90.7% of missing teeth (i.e. lost during skull preparation post mortem). Teeth lost through acquired means accounted for 7.3% of missing teeth (i.e. lost throughout the life of the animal). One specimen was found to have lost the right maxillary first molar tooth and a second specimen was found to have lost the left maxillary fourth premolar tooth and left maxillary first molar tooth. Congenitally absent teeth

Fig. 4. Abnormal tooth form. An abnormally small right maxillary second premolar tooth (closed arrow) when compared with the contralateral tooth (open arrow). Scale, 1 cm.

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Fig. 5. A male adult mountain lion with odontodysplasia of the left maxillary fourth premolar tooth (closed arrow) and bilateral congenitally-absent maxillary second premolar teeth (open arrow).

only accounted for 2.0% of missing teeth. Congenitally absent teeth were found to have a relatively even spread between the maxillary first molar teeth, incisor teeth and maxillary second premolar teeth (Fig. 3). These congenitally absent teeth were found in 8.8% of the population examined. Tooth Form

Abnormal tooth form was considered to be any irregular structure or formation of the crown of the tooth, root of the tooth, or both. This did not include teeth with an abnormal number of tooth roots, as these are evaluated in the following section. Only 91 teeth with abnormal form were found (3.5% of teeth available for examination). Teeth with abnormal form were found in 50.5% of specimens examined. The

Fig. 6. A female adult mountain lion with a supernumerary left maxillary second premolar tooth (arrow). Scale, 1 cm.

most common abnormality in tooth form was unusually large crowns of the maxillary first molar teeth (36 teeth), with the left side being more commonly affected. This abnormality was bilateral in 14 specimens. An abnormally large crown was seen in one left maxillary second premolar tooth. Teeth with abnormally small crowns were also noted, most commonly affecting the maxillary first molar teeth (12 teeth) and the maxillary second premolar teeth (four teeth) (Fig. 4). Abnormally small crowns of the maxillary first molar teeth were bilateral in two specimens. Fused double roots (partial and complete) were another finding, most commonly affecting the mandibular fourth premolar teeth (eight teeth; bilateral in three specimens). The maxillary second premolar teeth (two teeth), maxillary first molar teeth (three teeth) and mandibular first molar teeth (three teeth) were also seen with this abnormality, but with decreased incidence. Convergence of roots was identified in 13 teeth; this was more closely evaluated on radiographical examination and is further detailed below. Other much less common abnormalities in form were noted. Dilaceration of tooth roots was identified in three teeth, affecting one left maxillary first molar tooth in one specimen and both mandibular first molar teeth in another specimen. Odd angulation of tooth roots was noted in two specimens, affecting four teeth. One specimen showed bilateral rostromedial deviation of the roots of the maxillary second premolar teeth. The second specimen had a caudal deviation of the maxillary first molar teeth roots. Additional abnormalities in tooth form included: one male young adult mountain lion with an unerupted left maxillary canine tooth with surrounding pericoronitis, and another male adult mountain lion with

Fig. 7. A male adult mountain lion with generalized attrition/ abrasion with tertiary dentine visible on the incisal edges of the canine teeth (arrows). Scale, 1 cm.

Dental Pathology of the Mountain Lion

odontodysplasia of the left maxillary fourth premolar tooth (Fig. 5). These defects can be attributed to trauma during tooth development. Number of Roots

Out of the teeth examined, only 0.8% were found to have an abnormal number of roots. These teeth were found in 14.3% of the specimens examined. Out of the teeth with abnormal roots, the majority were maxillary first molar teeth seen with two roots instead of the expected one. This aberration of the maxillary first molar tooth was bilateral in seven individuals. Other findings included one specimen that had bilateral double-rooted maxillary second premolar teeth (instead of the expected one root) and another seen with a three-rooted left mandibular third premolar tooth (instead of the expected two roots). Supernumerary Teeth

One supernumerary left maxillary second premolar tooth was identified in a female adult mountain lion (Fig. 6). The supernumerary tooth was rotated 90 and caused crowding of the normal maxillary second premolar tooth and maxillary third premolar tooth. Persistent Deciduous Teeth

No persistent deciduous teeth were noted in any of the skull specimens examined. Enamel Hypoplasia

No enamel hypoplasia was identified in any of the skull specimens examined. Bony Changes Consistent with Periodontitis

Periodontitis was assessed in 4.1% of teeth examined and observed in 38.5% of specimens. Stage 2 periodontitis was found in 51.4% of teeth with periodontitis, stage 3 periodontitis was found in 40.0% of teeth with periodontitis and stage 4 periodontitis was found in 8.6% of teeth with periodontitis. The most common teeth affected with periodontitis were the maxillary fourth premolar teeth. Adult mountain lions were more likely to have periodontitis than young adults (P ¼ 0.029). Young adult mountain lions had a greater number of teeth affected by periodontitis than adults (P ¼ 0.019). Male mountain lions were more likely to have periodontitis than females or those of unknown sex (P ¼ 0.011). Males had a greater number of teeth affected by periodontitis than females (P ¼ 0.011).

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Attrition/Abrasion

Of the teeth examined, 35.9% had varying levels of attrition/abrasion (Fig. 7). The majority (93.4%) of specimens had some amount of attrition/abrasion. The incisor teeth accounted for 52.6% of teeth with attrition/abrasion, the molar teeth accounted for 18.9% and premolar teeth accounted for 17.0% of affected teeth. Male mountain lions were more likely to have attrition/abrasion than females or those of unknown sex (P ¼ 0.002). Adult mountain lions had more teeth with attrition/abrasion than young adults (P <0.001). Tooth Fractures

Tooth fractures were identified in 16.5% of teeth with a prevalence of 80.2%. Severe tooth fractures (i.e. complicated crowneroot, complicated crown and root fractures) accounted for only 3.0% of teeth, making up a much lower percentage than the total number of tooth fractures. Enamel fractures accounted for 42.6% of fractured teeth. Uncomplicated crown fractures accounted for 38.4% of fractured teeth. Complicated crown fractures accounted for 8.0% of fractured teeth; the most commonly afflicted teeth were the mandibular and maxillary canine teeth. Only four uncomplicated crowneroot fractures (0.9% of fractured teeth) were seen. Complicated crowneroot fractures accounted for 2.6% of fractured teeth. Root fractures accounted for 7.5% of fractured teeth; the most commonly afflicted teeth were the mandibular and maxillary first incisor teeth. The two most common fracture types were enamel fractures followed by uncomplicated crown fractures. Young adult mountain lions were more likely to have fractures than adults (P ¼ 0.048). Adult mountain lions had more teeth fractured than young adults (P <0.001). Male mountain lions were more likely to have fractured teeth than females and those of unknown sex (P <0.001). Endodontal Disease

Endodontal disease was assessed via dental radiography and recognized by the presence of a complicated tooth fracture with resulting periapical lesion, external inflammatory root resorption and/ or a pulp cavity that failed to narrow. Complicated tooth fractures (i.e. complicated crowneroot, complicated crown and root fractures) were found to affect 3.0% of teeth. Periapical lesions were diagnosed subsequently in 0.9% of teeth. Teeth diagnosed with periapical lesions were found in 17.6% of specimens. The most commonly affected teeth

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Fig. 8. Male young adult mountain lion with a complicated crown fracture (closed arrow) of the left mandibular canine tooth and resulting periapical lesion (open arrow). Scale, 1 cm.

were the mandibular and maxillary canine teeth, comprising 69.6% of teeth with periapical lesions (Fig. 8). Male mountain lions were more likely to have periapical lesions than females or those of unknown sex (P ¼ 0.001). Male mountain lions had more teeth with periapical lesions than females (P ¼ 0.005). Adult mountain lions were more likely to have teeth with periapical lesions than young adults (P ¼ 0.021). In addition to periapical lesions resulting from complicated tooth fractures, radiographs were also

analyzed for the presence of other indicators of endodontal disease (i.e. external inflammatory root resorption and/or a pulp cavity that had failed to narrow). These additional radiographical features of endodontal disease were present in 29 teeth. The most frequently affected teeth were the mandibular and maxillary canine teeth (Fig. 9). In addition to the canine teeth, four maxillary incisor teeth, two maxillary fourth premolar teeth and one mandibular first molar tooth also exhibited additional radiographical features of endodontal disease. Adult mountain lions

Fig. 9. Male adult mountain lion with a complicated crown fracture of the right maxillary canine tooth (open arrow). Radiographical evaluation of the tooth shows a periapical lesion (closed arrows) and a pulp cavity with failure to narrow when compared with the contralateral tooth. Scale, 1 cm.

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Fig. 10. Male adult mountain lion with severe TMJ osteoarthritis characterized by an irregular articular surface, subchondral bone exposure and porosity of the mandibular condylar processes (open arrows). The left TMJ exhibits periarticular bony proliferation at the retroarticular process (closed arrows) partially encircling the mandibular head, resulting in partial ankylosis. Scale, 1 cm.

were more likely to have additional radiographical signs of endodontal disease than young adults (P <0.001). Adult mountain lions had more teeth afflicted with additional radiographical signs of endodontal disease than young adults (P <0.001).

Male mountain lions were more likely to have tooth resorption than females and those of unknown sex (P ¼ 0.012). Male mountain lions had more teeth afflicted with tooth resorption than female mountain lions (P ¼ 0.014).

Tooth Resorption

Head Trauma and Gunshot Wounds

Tooth resorption was found in 1.2% of teeth examined and in 11.0% of mountain lion specimens. Stage 2 tooth resorption was found to affect 21.9% of teeth with resorption, stage 3 tooth resorption affected 18.7% of teeth with resorption, stage 4 tooth resorption affected only 6.3% of teeth with resorption and stage 5 tooth resorption affected 53.1% of teeth with resorption. Stage 2 tooth resorption affected the maxillary incisor teeth and the mandibular third premolar teeth. Stage 3 tooth resorption affected mostly the mandibular and maxillary premolar teeth. Stage 4 tooth resorption had an even spread, affecting a maxillary premolar and mandibular first molar tooth. Stage 5 tooth resorption most frequently affected the maxillary and mandibular incisor teeth. Adult mountain lions were more likely to have tooth resorption than young adults (P ¼ 0.001).

During gross examination, each skull was assigned a status of ‘head trauma’, ‘gunshot wound’ or ‘intact’. Of the 91 skull specimens, the majority (59.3%) were intact, 22.0% of the specimens had gunshot wounds and 18.7% of the specimens had head trauma. Out of the specimens that had gunshot wounds, the most commonly afflicted animals were male adult and female young adult mountain lions. Out of the specimens that had sustained head trauma, the most commonly afflicted animals were male young adult and female adult mountain lions. Temporomandibular Joint Disease

TMJ osteoarthritis was found to afflict 19.8% of specimens examined. The majority of specimens with TMJ osteoarthritis had only mild disease (13 specimens), four specimens exhibited moderate TMJ

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Fig. 11. Radiographs of the left (L) and right (R) maxillary canine teeth of a young adult mountain lion with squared root apices (open arrows).

osteoarthritis and only one specimen displayed marked TMJ osteoarthritis (Fig. 10). Other Findings

While examining radiographs, a few frequently seen variations in root form were observed. These variations in root form were found to affect 7.2% of teeth and 83.5% of the population of mountain lions examined. Many maxillary canine teeth were noted to have a squared shape of the root apex (Fig. 11). This variation in root form was found to affect the right and left maxillary canine teeth evenly. In addition, some mandibular third premolar teeth and mandibular first molar teeth had convergence of roots (Fig. 12); in all cases the left side was most commonly affected. Male mountain lions were found to have more teeth with abnormal root form compared with female mountain lions (P ¼ 0.040).

Discussion The California Academy of Sciences, San Francisco, and the Museum of Vertebrate Zoology, University of California, Berkeley, house a small but pristine

collection of California mountain lion skulls. The known collection dates of the skulls spanned a 100year period from 1906 to 2006 and were obtained from carcass recovery, donations from the public (often trappers and hunters) and other wildlife care institutions. Due to the random nature of specimen acquisition over this 100-year period, no obvious trends over time or location were identified. Some of the teeth possessed hairline cracks and artefactual sharp-edged fractures due to excessive heat and drying during specimen preparation. These defects did not obscure true dental pathology. The vast majority (90.7%) of missing teeth were lost through artefactual means (i.e. post mortem). Only three teeth were lost throughout the life of the animal via acquired means; this was identified in two specimens and found to affect two maxillary first molar teeth and one maxillary first molar tooth. Congenitally absent teeth were rare and only identified in a total of eight specimens. Of the total teeth examined, only 11 teeth were identified as being absent congenitally. In previous studies on the anatomical variation in dentition of the domestic cat (Verstraete and Terpak, 1997) and feral cat (Verstraete et al., 1996a), the most frequent

Fig. 12. Radiographs of the left (L) and right (R) mandibular third premolar (open arrows) and first molar teeth (white arrows) displaying convergence of roots. Additionally, the mandibular fourth premolar teeth (black arrows) display convergence of roots with partial root fusion.

Dental Pathology of the Mountain Lion

congenitally absent teeth were found to be the maxillary second premolar tooth followed by the maxillary first molar tooth. In the California bobcat the two most common congenitally absent teeth were identified to be the mandibular and maxillary incisor teeth (Aghashani et al., 2016). The population of California mountain lions examined had a relatively even spread of congenitally absent teeth, including five maxillary first molar teeth, three incisor teeth and three maxillary second premolar teeth. The anatomical variation in dentition of the mountain lion closely resembles that of the domestic cat, feral cat and the bobcat. Abnormal tooth morphology was identified infrequently, afflicting only 3.5% of teeth; however, it was found to afflict up to 50.5% of specimens examined. The most common morphological abnormality was unusually large crowns of the maxillary first molar teeth, with a left-sided predilection. This finding is similar to results from the California bobcat except for a right-sided predilection in that animal (Aghashani et al., 2016). The second most common abnormality in tooth form noted in the California mountain lion were abnormally small crowns of the maxillary first molar and maxillary second premolar teeth. Enamel hypoplasia was not identified in any California mountain lion or California bobcat specimens (Aghashani et al., 2016). In a past study of the dentition of feral cats, enamel hypoplasia was identified at a prevalence of 24.6% (Verstraete et al., 1996a). Morbillivirus infections are known to cause disease in dogs and people that result in enamel hypoplasia; there is a rare feline paramyxovirus that can be associated with a similar disease in felines (Verstraete et al., 1996a). An abnormal number of tooth roots was a rare finding that was noted in only 0.8% of teeth, affecting 14.3% of specimens examined. The majority of teeth with an abnormal number of roots in the California mountain lion were maxillary first molar teeth with two roots instead of the expected one (85.7%). This finding was bilateral in just over half (53.8%) of specimens with this type of root abnormality. When comparing the California bobcat to the California mountain lion, the number of teeth present with an abnormal number of roots was similar, but the overall prevalence was noted to be higher in the bobcat (16.6%). Studies of the dentition of domestic (Verstraete and Terpak, 1997) and feral cats (Verstraete et al., 1996a) show the most commonly affected tooth to be a three-rooted maxillary third premolar tooth. This variation was not appreciated in the California mountain lion or bobcat. The most prevalent dental lesions seen in the California mountain lion were identified to be attrition/ abrasion (93.4%), tooth fractures (80.2%) and peri-

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odontitis (38.5%). These dental lesions correlate to common dental lesions seen in other members of the family Felidae. ‘Attrition’ refers to the physiological wear of teeth as they move against one another or food during mastication, most commonly affecting the occlusal surfaces. ‘Abrasion’ is defined as pathological wear due to an abnormal mechanical process (Shafer et al., 1983). Attrition and abrasion were grouped together for the purposes of this study, since assigning either process to a tooth would be speculative. Attrition/abrasion was the most prevalent dental lesion encountered in this study, affecting almost all of the specimens examined (93.4%) and 35.9% of teeth. More than half of the teeth afflicted with attrition/ abrasion were incisor teeth. Other commonly afflicted teeth included the premolar and molar teeth. The California mountain lion displayed a similar pattern of attrition/abrasion when compared with the California bobcat (Aghashani et al., 2016). The pattern of tooth wear seen in the mountain lion and bobcat is common for the family Felidae (Grzimek, 2004). This is speculated to be the result of the mechanical action of removing meat from prey. Tooth fractures were the second most prevalent dental lesion seen in this study, affecting 80.2% of specimens and 16.5% of teeth. Tooth fractures of all six types were noted. However, severe tooth fractures (i.e. complicated crown, complicated crowneroot and root fractures) only accounted for 3.0% of teeth examined. The California mountain lion greatly surpassed the California bobcat (50.9% prevalence, 7.7% of teeth) in both prevalence and percentage of tooth fractures (Aghashani et al., 2016). In a study of feral cats, the majority of fractures were complicated crown fractures and root fractures (Verstraete et al., 1996a). In the California mountain lion and bobcat the two most common types of tooth fractures were enamel fractures followed by uncomplicated crown fractures (Aghashani et al., 2016). The diagnosis of periodontal lesions from dry skulls is flawed due to the lack of soft tissue, which is essential for diagnosis. However, the hyperaemia associated with inflammation in bony tissues is revealed by increased vascular foramina, a rough texture of the alveolar process and bone loss (Verstraete et al., 1996b). Periodontitis was the third most common dental lesion in this study, affecting 38.5% of specimens and 4.1% of teeth. The California mountain lion and bobcat were similar in that periodontitis was found most often to afflict the maxillary fourth premolar tooth (Aghashani et al., 2016). Prevalence of periodontitis was noted to be higher in the California bobcat (56.0%) as was the percentage of teeth

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affected with all stages of periodontitis (7.7%). Periodontitis is an important cause of tooth loss in felines. In addition to tooth loss, severe bone loss can result in pulpitis, pulp necrosis and endodontic disease (Lommer and Verstraete, 2001). The long-term impact of periodontitis can have severe consequences on the functionality and integrity of a cat’s dentition, especially for felids that depend on their teeth in order to hunt and consume prey. TMJ osteoarthritis was found to afflict 19.8% of specimens. The majority of specimens suffered from mild disease; however, more advanced cases can result in possible joint ankyloses severely limiting a predator from effectively hunting prey. Other dental lesions included endodontal disease and tooth resorption. In this study periapical lesions were found to be present in 17.6% of specimens and in 0.9% of teeth. Periapical lesions typically result from pulp exposure and subsequent pulp necrosis. Periapical rarefaction is seen radiographically and is a lucency of the periapical bone, caused by loss of mineralization of the alveolar bone (Lemmons, 2013). Inflammation of the periapical tissues can result in lesions of varying intensity and chronicity (Lommer and Verstraete, 2000). In this study, dental radiographs were implemented to aid in the diagnosis of smaller and subtle lesions. While examining radiographs for signs of disease, a few common variations in root form were noted in the California mountain lion. These frequent variations in root form included a squared root apex of the maxillary canine teeth and convergence of mandibular tooth roots. These variations had a prevalence of 83.5% and were identified in 7.2% of teeth. These variations in root form do not have any specific clinical significance, but are interesting findings. It is peculiar for such a large mandible with so few teeth to display such frequent convergence of roots. Endodontal disease includes periapical lesions, external inflammatory tooth resorption and failure of the pulp cavity to narrow. In the California mountain lion and bobcat, the teeth most commonly afflicted with endodontal disease proved to be the maxillary and mandibular canine teeth (Aghashani et al., 2016). Pulp cavity width was assessed by comparing contralateral teeth. A healthy tooth will age and continue to deposit secondary dentine, thickening the dentine layer and in turn narrowing the pulp cavity (Lemmons, 2013). A tooth with a pulp cavity that is wider than its counterpart is assumed to have stopped maturation due to pulp death. External inflammatory root resorption can lead to the blunted appearance of the apex of the root; this process can be severe enough to result in a noticeably shortened root tip (Lemmons, 2013).

Periapical lucencies are associated commonly with fractured teeth and severe periodontitis (Lommer and Verstraete, 2000). The resulting endodontal disease seen in the canine teeth of the California mountain lion and bobcat were most commonly due to complicated crown fractures obtained via traumatic means throughout the life of the animal. This type of dental pathology can have potentially severe consequences for wild felids, which require healthy functional dentition for hunting. The subject of tooth resorption is of interest in the family Felidae, especially in wild felids. One of the aims of the present study was to diagnose and document the prevalence of tooth resorption in this population of wild cats, since data are generally lacking in this area. This was accomplished through the use of dental radiography, which allows for a more accurate and thorough diagnosis of lesions than through gross examination alone. In a study examining the diagnostic value of full-mouth dental radiographs in domestic cats, dental radiographs yielded additional clinically relevant information in 41.7% of cats that was not detected on examination alone, and in 98.4% of domestic cats that had already been clinically diagnosed with tooth resorption (Verstraete et al., 1998). In the population of mountain lions studied, tooth resorption was identified in 11.0% of specimens, affecting 1.2% of teeth. Tooth resorption in the California mountain lion was seen as a slightly higher prevalence and percentage of teeth affected with tooth resorption when compared with the California bobcat (9.4% of specimens, <1.0% of teeth) (Aghashani et al., 2016). In domestic cats, there are less data on prevalence in the general population and it has been estimated that tooth resorption affects anywhere between 20% and 67% of domestic cats (Lemmons, 2013). Tooth resorption in felines is known to be a progressive resorption of the dental hard tissues by osteoclasts (odontoclasts), although the exact aetiology is still unknown (Lemmons, 2013). Many factors have been considered as potential causes for the initiation of tooth resorption; however, no definitive answers exist. The present study adds to the body of evidence showing that tooth resorption is not a disease of domestication, but a common disease of felines. Tooth resorption is known to be a painful process as it progresses in severity (Lemmons, 2013). It can be inferred that in the advanced stages, tooth resorption and other dental diseases have a negative impact on the welfare and survival of wild felids. In conclusion, the California mountain lion was found to display a range of dental lesions and abnormalities. The prevalence of congenital and

Dental Pathology of the Mountain Lion

developmental abnormalities was relatively low, but acquired lesions were common, especially attrition/ abrasion, tooth fractures and periodontitis. As a result of acquired lesions, some specimens suffered from endodontal and periapical disease. Acquired lesions affected adult mountain lions more frequently and severely than young adults. Male mountain lions also showed a predilection for acquired dental lesions when compared with females. It was of particular interest to demonstrate tooth resorption in the California mountain lion. Specimens that exhibited severe generalized dental disease would have likely suffered from considerable morbidity while alive, possibly leading to an increase in mortality.

Acknowledgments The authors thank M. Flannery of the Department of Ornithology and Mammalogy of the California Academy of Sciences and C. Conroy of the Museum of Vertebrate Zoology of the University of California, Berkeley, for making their collections available for this study. The authors thank J. Doval for specimen photography. This research was funded by the School of Veterinary Medicine, University of California e Davis, Students Training in Advanced Research (STAR) Program, which had no role in study design, in the collection, analysis and interpretation of data, in the writing of the manuscript or in the decision to submit the manuscript for publication.

References Abbott C, Verstraete FJM (2005) The dental pathology of northern elephant seals (Mirounga angustirostris). Journal of Comparative Pathology, 132, 169e178. Aghashani A, Kim AS, Kass PH, Verstraete FJM (2016) Dental pathology of the California bobcat (Lynx rufus californicus). Journal of Comparative Pathology, 154, 329e340. American Veterinary Dental College (2015) AVDC Nomenclature. Tooth Resorption. http://www.avdc.org/Nomenclature/ Nomen-Teeth.html#resorption (Accessed 18 May 2016). Arzi B, Winer JN, Kass PH, Verstraete FJM (2013) Osteoarthritis of the temporomandibular joint in southern sea otters (Enhydra lutris nereis). Journal of Comparative Pathology, 149, 486e494. Department of Fish and Wildlife, California (2007) Mountain Lion FAQ. Commonly Asked Questions about Mountain Lions. https://www.wildlife.ca.gov/Conservation/ Mammals/Mountain-Lion/FAQ (Accessed 18 May 2016). Grzimek B (2004) Cats (Felidae). In: Grzimek’s Animal Life Encyclopedia, 2nd Edit., Vol. 14, M Hutchins,

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DG Kleiman, V Geist, MC McDade, Eds., Gale Virtual Reference Library, Detroit, pp. 369e392, (Mammals III). Lemmons M (2013) Clinical feline dental radiography. Veterinary Clinics of North America: Small Animal Practice, 43, 533e554. Lommer MJ, Verstraete FJM (2000) Prevalence of odontoclastic resorption lesions and periapical radiographic lucencies in cats: 265 cases (1995e1998). Journal of the American Veterinary Medical Association, 217, 1866e1869. Lommer MJ, Verstraete FJM (2001) Radiographic patterns of periodontitis in cats: 147 cases (1998e1999). Journal of the American Veterinary Medical Association, 218, 230e234. Nielsen C, Thompson D, Kelly M, Lopez-Gonzalez CA (2015) Puma Concolor. The IUCN Red List of Threatened Species 2015: e.T18868A50663436. http://dx.doi. org/10.2305/IUCN.UK.2015-4.RLTS. T18868A50663436.en (Accessed 18 May 2016). Niemiec BA, DuPont G (2010) Pathologies of the dental hard tissues. In: Small Animal Dental, Oral and Maxillofacial Disease: A Color Handbook, Manson, London, pp. 127e157. Peralta S, Verstraete FJM, Kass PH (2010) Radiographic evaluation of the types of tooth resorption in dogs. American Journal of Veterinary Research, 71, 784e793. Shafer WG, Hine MK, Levy BM (1983) Regressive alterations of the teeth. In: A Textbook of Oral Pathology, 4th Edit., WG Shafer, MK Hine, BM Levy, Eds., WB Saunders, Philadelphia, pp. 318e338. Verstraete FJM. Dental pathology and microbiology. In: Textbook of Small Animal Surgery, Vol. 2, DH Slatter, Ed., WB Saunders, Philadelphia, pp. 2638e2651. Verstraete FJM, Kass PH, Terpak CH (1998) Diagnostic value of full-mouth radiography in cats. American Journal of Veterinary Research, 59, 692e695. Verstraete FJM, Terpak CH (1997) Anatomical variations in the dentition of the domestic cat. Journal of Veterinary Dentistry, 14, 137e140. Verstraete FJM, van Aarde RJ, Nieuwoudt BA, Mauer E, Kass PH (1996a) The dental pathology of feral cats on Marion Island. Part I: congenital, developmental and traumatic abnormalities. Journal of Comparative Pathology, 115, 265e282. Verstraete FJM, van Aarde RJ, Nieuwoudt BA, Mauer E, Kass PH (1996b) The dental pathology of feral cats on Marion Island. Part II: periodontitis, external odontoclastic resorption lesions and mandibular thickening. Journal of Comparative Pathology, 115, 283e297.

September 16th, 2016 ½ Received, Accepted, November 19th, 2016