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1 Institute of Zoology, The Zoological Society of London, Regents Park, London NW1 4RY, UK
2 29a Brook Street, London W1Y 1AJ, UK
3 Corresponding author (email: tony.sainsbury{at}ioz.ac.uk)
| ABSTRACT |
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Key words: Incisors, malocclusion, molars, periodontal disease, rodent, rodentia.
| INTRODUCTION |
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Oral disease was believed to be a potential cause of red squirrel morbidity and mortality based on the frequency that these diseases, especially malocclusion, is seen in captive, and in some species of free-living, rodents (Miles and Grigson, 1990; Hoff and Hoff, 1996). Sainsbury (1997) stated that malocclusion of the incisors was found in free-living red and grey squirrels and was the probable cause of death in one case in each species, but that the prevalence of malocclusion is unknown.
Variations in the number, size, and shape of rodents teeth are documented in the literature (Miles and Grigson, 1990). Instances of extra incisors, supernumerary cheek teeth, absence of teeth, variation in molar size, variation in molar cusp pattern, variation in the position, and number of roots are frequently recorded in various species of free-living rodents. No irregularities in the position of the teeth were observed in 622 specimens of Sciurus spp. examined (Miles and Grigson, 1990).
Periodontal disease seems to be common in captivity, but in free-living rodents is not well documented. It has been recorded in populations of house mice (Mus musculus), deer mice (Peromyscus oreas), pocket mice (Perognathus longimembris), and lemmings (Lemmus trimucronatus), and associated with infectious, genetic, and/or age-related causes (Miles and Grigson, 1990).
Dento-alveolar abscesses in rodents usually involve the incisor teeth. Depending on the position of the incisor in relation to the molar teeth and the bone of the jaw, the infection spreads to cause discharging sinuses at the base of a molar or alternatively osteomyelitis. Dento-alveolar abscesses have been observed in an alpine marmot (Marmotta marmotta), an American beaver (Castor canadensis), and a field vole (Microtus agrestis; Miles and Grigson, 1990).
Caries seldom occur naturally in rodents due to an inhibitive combination of high oral pH, absence of cariogenic microflora, and low-sugar diet (Wiggs and Lobprise, 1997). Caries were not found in 3,800 skulls of a variety of free-living rodents examined in various museums (Miles and Grigson, 1990).
There have been few investigations into the etiology of oral disease in free-living rodents; most authors limit themselves to describing the lesions found (Miles and Grigson, 1990). Most of the dental problems documented in pet and captive, wild rodents and lagomorphs are associated with incorrect husbandry and management, or are induced experimentally (Robinson, 1979a,b, 1986; Yankell, 1985; Clark and Olfert, 1986; Eisele, 1986; van Foreest, 1993; Crossley et al., 1997). Dental abnormalities in eruption, occlusion, and attrition are probably much more common in captive than free-living animals (Robinson, 1979a,b; Amand and Tinkelman, 1985).
The teeth of red squirrels are heterodont and the cheek teeth are brachyodont (Kertesz, 1993). Rodent incisors grow continuously and have enamel coating on the full length of their labial surfaces while at the buccal aspect of the incisors only the softer dentine is present, which wears to a chisel-shaped cutting edge (Laidler, 1980). A tooth root is defined as any part of a dental structure that is devoid of enamel externally or internally. Therefore, by definition, rodent teeth do not have anatomical roots and are classified as aradicular elodonts (Kertesz, 1993). In this paper, the whole length of an incisor tooth is termed the anatomical crown, any part of that tooth that is visible in the oral cavity is termed the clinical crown (Scott and Symons, 1977), whereas that part of the tooth that is covered by gingival tissues or alveolus will be termed pseudo-root. In this paper, when indicating a position on an elodont tooth, incisal will denote the intraoral extremity of the tooth, and apical or apex the intra-alveolar extremity of the pseudo-root.
The red squirrels dental formula is:
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Red squirrels lower incisors erupt at 1921 days of age, and the upper incisors erupt at 3142 days (Gurnell, 1991). The cheek teeth (molars and premolars) erupt from 7 weeks of age onward, and by 10 weeks of age all the cheek teeth are present (Tittensor, 1980). Primary first lower and only the second upper premolars are shed at 16 weeks of age and are replaced by permanent teeth (Holm, 1987). The first upper premolar is vestigial. There are no canine teeth, and the gap between the incisors and the cheek teeth is called the diastema (Gurnell, 1987).
The cheek teeth are quadrate with rounded blunt, cone-shaped bunodont marginal cusps and a concave central area (fossa) on their occlusal surfaces. The occlusal surfaces of the upper cheek teeth are traversed by weak transverse ridges (Gurnell, 1991; Kertesz, 1993). The prominent inner cusps of the upper cheek teeth grind food in the concavity of the opposing lower teeth while the cusps on the outer surface of the upper cheek teeth shear food against those of the lower cheek teeth (Shorten, 1954). A young squirrel has a layer of enamel covering the surface of each cheek tooth, including the cusps and ridges. As age progresses, this layer gets worn, exposing the underlying dentine (Shorten, 1954). Several authors have used tooth wear for age determination in red squirrels (Naumov, 1934; Kyris, 1937; Shengkan and Mingshu, 1979; Shadrina, 1988).
Squirrels, like all rodents, have a marked degree of rostra-caudal gliding movement in their temporomandibular articulations and can move their jaws backward and forward (Crossley, 1995). The two hemi-mandibles of squirrels are connected by the transversus mandibular muscle that can pull them together. The deep and superficial masseters can act to stretch the transversus mandibular muscle and thus pull the two hemi-mandibles apart slightly. In this way the incisors of the lower jaw can be moved either toward (closed) or away (open) from each other and can be used to seize and crack nuts (Holm, 1987; Laidler, 1980).
An investigation of the prevalence of oral disease in free-living red squirrels from the UK was initiated to assess the significance of oral disease as a cause of morbidity and mortality and also to discover any factors in the etiology of oral disease in free-living red squirrels.
| MATERIALS AND METHODS |
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Ninety-one red squirrels from the UK collected between January 1994 and August 1998 were examined postmortem and, together with four red squirrels from the 273 examined earlier, were given a detailed oral examination using an oral examination chart (Fig. 1
). The red squirrels examined were collected by members of the public, research workers, forest rangers, and others who took part in an appeal for carcasses for a mortality survey and several genetic and ecologic research projects (Sainsbury et al., 1995). The time interval between collection and postmortem examination varied. The carcasses of 16 animals were examined after refrigeration, and 75 following freezing at 20 C. The red squirrels were aged according to the techniques of Kyris (1937), Naumov (1934), Shadrina (1988), and Shengkan and Mingshu (1979).
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The universal dental notation system proposed by Kertesz (1993) was used for identifying teeth. The length of the dental arch (the measurement from the rostral surface of the first premolar to the caudal surface of the third molar) and its width (at the level of the third molar [M3] of the left maxilla and mandible) were measured. The clinical crown of the incisors and molars was measured from the gingival margin to the coronal end of the tooth at both the labial and lingual or palatal surface. Measurements were taken with calipers (accuracy ±1 mm) and refer to length in a straight line. Teeth were examined visually and missing and supernumerary teeth and positioning of teeth were recorded in the dedicated chart. Cases of malocclusion secondary to excessive wear or overgrowth were noted. Loss of tooth substance and cases of attrition, caries, fractures, discolored teeth, enamel defects, and pulp exposure were also recorded.
The periodontal tissues were examined for abnormalities: edema, inflammation, and bleeding of the gingivae were scored from 1 to 4 according to severity. These changes could not be assessed in frozen carcasses. The gingival sulci could not be probed with a Williams periodontal probe because this instrument was too thick, so a 27 G (0.4x12 mm) needle was filed down and graduated in millimeters, and the sulci were measured ±1 mm. A sharp probe was used to assess mobility of the teeth, and bone loss was assessed radiographically. Gingivae were evaluated for the presence of gum recession, gum hyperplasia, and epulis. The oral cavity was examined for lesions of the soft tissue (cheeks, lips, tongue), tumors, abscesses, jaw deformities, and jaw movement range.
The skulls of eight red squirrels were radiographed, of which six had signs of oral disease and two were apparently normal and used as controls. The mandible was dislocated and divided at its symphysis. Five views were taken: two oblique, a lateral and a dorsoventral of the skull without the mandible, and a lateral of the two hemi-mandibles. Radiographs were produced using a Dean D.38 Mobile Unit with a Dynamax 40 dual focus tube capable of delivering 75125 KVp and 25300 mA (Dean, Croydon, UK). Radiographs were made on Fuji Medical X-ray Film HR-E30 (high resolution film) or Fuji Medical X-ray Film MI-MA (mammography film; Fuji Photo Film Co., Ltd., Japan) at 79 cm focus film distance. Exposure times varied between 0.1 and 0.12 sec, at 2550 mA and 7478 KVp depending upon the animals size. The films were wet processed in Polycon X-ray developer (May and Baker, Essex, UK) at 20.4 C. Observations on the radiographs were made by two of the authors (A.K. and G.D.B.).
| RESULTS |
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The length of the dental arch in normal squirrels was 8.59.5 mm and its width 2.53 mm. The height of the clinical crown of the cheek teeth was 0.51 mm. Molars and premolars occluded in an oblique line. The gingival sulcus depth of the cheek teeth in normal squirrels was less than 0.5 mm. The clinical crowns of the upper incisors were 56 mm long at the labial surface and 1.5 mm long at the palatal surface (measured from the gingival margin to the caudal aspect of the tooth tip); the sulcus depth of upper incisors was approximately 3 mm. Clinical crowns of the lower incisors were 1113 mm long at the labial surface and 56 mm long at the lingual surface (measured from the gingival margin to the coronal tip); the sulcus depth of the lower incisors was approximately 1 mm. Cheek teeth were classified in two groups: those with a bunodont pattern with prominent cusps and ridges belonging to younger animals, and those with well-worn occlusal surfaces belonging to older animals (Fig. 2
).
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In case 2, the clinical crown of the left upper incisor was overgrown (11 mm in length at the labial surface) and met the lower gum surrounding the lower incisor. The left, lower incisor was deflected medially to accommodate the overgrown upper incisor. The gingivae surrounding both upper incisors were necrotic (black colored tissue, which was easily removed). The clinical crown of the right, lower incisor was 14 mm long at the labial surface (probably overgrown). The cheek teeth appeared normal and were immobile. The radiograph of case 2 indicated that the pelvis was asymmetrical, possibly due to injury. The left, upper incisor was overgrown. The left, upper premolars and molars possibly had a thickened periodontal membrane. Although the incisors were overgrown in case 2, it was unclear whether the malocclusion was sufficiently severe to have caused death.
Gross postmortem examination of case 3 revealed exudative erythematous dermatitis at multiple sites and parapoxvirus particles were found on electromicroscopy of the skin lesions: parapoxvirus infection was believed to be the cause of death. On oral examination no upper or lower cheek teeth were present, just a hard pad of cartilaginous tissue (partial anodontia). The alveolar bone of the absent cheek teeth was probably resorbed because the bone was less elevated than normal (Fig. 3
). The upper incisors were mildly mobile, probably the result of postmortem change, but otherwise appeared normal. On radiograph the bones had a normal appearance. No upper or lower molars were present, which may have been due to the ossification of vacated alveoli (possibly a geriatric squirrel that had lost all of its cheek teeth) or due to a developmental defect. The incisors were normal (Fig. 4
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| DISCUSSION |
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Oral diseases described in free-living red squirrels in this study were probably of degenerative, traumatic, or possibly nutritional origin. The most commonly encountered oral lesions were malocclusion of the incisors and attrition of the cheek teeth. Attrition of the cheek teeth was assumed to be a normal consequence of old age, as described in the reports on age determination of red squirrels (Naumov, 1934; Kyris, 1937; Shengkan and Mingshu, 1979; Shadrina, 1988). However, in one case attrition was severe enough to cause malocclusion leading to asymmetry of the left maxilla (case 5). The emaciated state of case 5 and the presence of undigested food in the gastro-intestinal tract led us to believe that attrition and malocclusion were the cause of death.
Malocclusion of the incisors was observed in four cases (2, 4, 6, and 7). In two instances it was associated with a degenerative process at the incisors pseudo-root (dento-alveolar abscess in case 6; sclerosis and necrosis of the pulp probably associated with trauma and infection in case 7). From radiographic evidence in case 6, it seems that the bony orbit was also involved because there were bone sequestra in the floor of the orbit. There are two possible origins for the malocclusion. The abscess of the soft tissues surrounding the temporomandibular joint may have led to malocclusion of the incisors because pain, swelling, and subsequently fibrosis may have prevented mouth closure. Alternatively, it is possible that a dento-alveolar abscess at the pseudo-root of the incisor caused malocclusion and the infection spread to the soft tissues surrounding it.
Case 4 had malocclusion that was associated with chronic mandibular osteomyelitis due to a periapical infection. Surprisingly, the squirrel was in good condition considering the extent of the infection. The cause of death was trauma, probably due to a road traffic collision. Miles and Grigson (1990) also found that free-living rodents can survive with mal-occlusion: overgrowth of the incisors was noted in a Townsends ground squirrel (Spermophilus townsendi) and in a red squirrel (Tamiasciurus hudsonicus). The Townsends ground squirrel managed to feed by placing one side of its open mouth over long blades of grass and biting them off with its cheek teeth (Miles and Grigson, 1990). Furthermore, in a recent paper by van der Merwe (1997), malocclusion of the incisors was studied in African greater cane rats (Thryonomys swinderianus). Van der Merwe (1997) examined 163 skulls from wild animals and carried out detailed radiographic examination of four cane rat pups at stages during growth and concluded that malocclusion in the cane rat does not necessarily reduce fitness because the overgrown incisors tend to break below the gum line before they impede feeding.
Malocclusion in the cases examined in this study appeared to be caused by mechanical factors affecting the pseudo-roots of the incisors. This finding is consistent with observations by Wiggs and Lobprise (1997) and Chaturvedi (1966) who stated that rodents with brachyodont molars, like squirrels, rarely present with atraumatic malocclusion, but traumatic malocclusion caused by mechanical factors or tooth fracture is common. A variety of factors have been implicated by Wiggs and Lobprise (1995) to predispose to malocclusion: genetics (heredity), trauma, diet, dental habits, and chewing exercise; however, they did not give evidence to support these possibilities.
Disorganized growths, which stimulate odontomes at the apex of injured teeth, have been described (Miles and Grigson, 1990), and the irregular masses at the apex of the incisors of cases 4, 6, and 7 were probably similar.
The cheek teeth were completely absent (partial anodontia) in case 3. It was unclear whether the absence of cheek teeth was a developmental defect or whether it was due to old age. This squirrel was in good condition at the time of death, and therefore was probably feeding adequately. The authors are not aware of other reports of partial anodontia in rodents.
Periodontal disease was not observed, although there were problems associated with its assessment. The evaluation of normal tooth mobility was difficult, because in decomposed carcasses mobility was increased as the result of autolysis of periodontal tissues. Mobility was also increased in the recently erupted teeth of young squirrels, presumably because the periodontal tissues were still developing. In some radiographs the periodontal membrane of teeth appeared thickened and in some cases the lamina dura of the alveolus was not visible. Robinson and Gorrel (1995) state that widening of the periodontal space and reduced clarity of the lamina dura, particularly at the coronal portion of the teeth, may be seen in some cases of periodontal disease. Upon examination of these cases with radiographic evidence of periodontal disease, no mobility of the teeth was observed. It is possible that this radiographic evidence of periodontal disease may have been due to degenerative postmortem change.
Although the sample chosen for this study was selected by a form of convenience sampling and is probably not truly representative of the free-living red squirrel population, the calculated estimate of prevalence of 0.033 indicates that oral disease is probably uncommon in free-living red squirrels. In two of the red squirrels examined, oral disease was believed to be the primary cause of death.
| ACKNOWLEDGMENTS |
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Received for publication 13 October 2003.
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