This study is the first study since 1963 to describe dental anomalies, variations, and pathology in the Swedish red fox. It shows that deviations are common, both to regard as normal variation and pathologic conditions potentially causing pain and suffering for the animal.
In addition, our study is the first using oral radiography to explore the dentition of Swedish free ranging red foxes. Studies based on cadaver examination and radiology enables increased detection of oral pathology compared to ocular evaluation of dry skull specimens.
Absence of teeth
In this study tooth absence was a common finding, as 17 out of 55 (30.9%) foxes were missing one or more teeth. The number of congenitally absent teeth in our study were almost the same in the adult group as in the young adult group (8 and 9 teeth respectively). In young animals, congenital tooth absence is supposedly more common than acquired tooth absence. Acquired tooth absence is more likely to be observed in older animals which was found in our study, where 21 teeth were lost in the adult group, compared to 3 in the young adult group and 1 in the juvenile group, which confirms this assumption.
Previous studies have shown a prevalence of tooth absence between 7.2% and 16.5% in the red fox [8, 5, 13], while a prevalence of 19.8% was found in the grey fox [5]. Reason for tooth absence was not included. The most common teeth to be absent were the mandibular third molar and the first maxillary premolar teeth.
Genetic variation between species can explain different prevalences of congenital tooth absence [8, 9, 16]. The grey fox is smaller than the red fox, and relative jaw and muzzle length may have some influence on tooth absence. Reduction in relative jaw and muzzle length can lead to crowding and rotation of teeth and in the end a selection for individuals missing the third mandibular molar and the first maxillary premolar tooth, teeth with weak genetic control and little significance in feeding [5, 8, 9, 16].
The fact that few other studies included acquired tooth loss may contribute to a higher prevalence of tooth absence in our study. Looking specifically at the frequency of tooth absence of the third mandibular molar tooth supposedly congenitally missing, a more concordant result between our study and other studies was evident [8, 10, 11, 13].
The most common teeth to be missing due to trauma in our study were the incisors and the mandibular first premolar teeth, followed by maxillary canines. Our result corresponded well with the result in a study from North America of the Grey fox (Urocyon cinereoargenteus) (1.1% compared to 0,8%) even though radiographic examination was not included in that study [7].
Tooth morphology
Tooth crowns are generally slender and more pointed in the red fox than in domesticated dogs. Studies of red foxes have shown that tooth morphology differ geographically [18, 19]. This biologic variation is caused either by genetic differences; genotypic variation (mutations), or by the effect of environmental factors (climate, food supply, other predators etc.) on the expression of the genetic potentials; phenotypic variation [19]. Further, gender differences in tooth morphology also occur, called sexual dimorphism [19]. The term anomaly characterizes an abnormality, deviation from or divergence from the established norm [11]. The same feature may be considered an anomaly by some and an expression of natural variation by others.
In our study, radicular developmental grooves were seen in almost all (92.7%) of the foxes. Domesticated dogs also have radicular developmental grooves, most prominent in the mesial root of the mandibular first molar tooth [4, 14, 15]. The same kind of grooves seem to be common in the Swedish red fox but not just in the mandibular first molar, but also in other teeth. Frequent appearance of these developmental grooves in the Swedish red fox, suggests a variation of tooth morphology rather than an anomaly.
Another finding was the root morphotype dilaceration. Dilaceration was more often present in the maxilla rather than in the mandible. No other study has investigated the prevalence of dilaceration in the red fox, however other root morphotype like fused roots is mentioned in some studies [11].
One further finding was supernumerary roots. The cause of supernumerary roots is not fully understood [20]. Trauma or infection during odontogenesis and root formation may be a possible explanation for supernumerary roots [21]. In the domestic dog the most common tooth to have supernumerary roots are the second and third maxillary and mandibular premolars [20].
Supernumerary roots were found in 9% of the Swedish foxes, primarily in the maxillary and mandibular first premolar teeth. Another study reported a prevalence of 5.7% supernumerary roots in the specimen, not only the first premolar teeth but also the first maxillary molar teeth [11]. In Poland, the frequency of teeth with supernumerary roots were 2% and the most common tooth to be affected was the third maxillary premolar tooth [8]. In two different studies from north America the prevalence of supernumerary roots was 2.3% in the red fox and 10.7% in the grey fox, the later which corresponds well with the result in our study [6, 7]. In dogs both genetic and environmental factors are supposed to play a role in the development of supernumerary roots [20]. Presumable the same applies to foxes and may explain the differences in results between studies.
Anomalies in the crown is unusual and has not always been included in other studies. In our study malformed tooth crowns, like microdontia, macrodontia, gemination and supernumerary cusps were identified in 27.2% of the foxes but only1% of examined teeth. In two studies 0.8% respective 1.6% of the specimen were presented with malformed crowns [8, 6]. In one study from Poland 18.4% of the examined skulls had deviations from the typical shape of the tooth. The deviations were reported as a change of the crown outline, faulty formation of the occlusal surface, additional and incorrect structures, and reduction in tooth shape and not specified as microdontia, gemination etc. [8, 9, 18, 19]. Variations and details in classification of crown morphology differ between studies making comparisons difficult and may partly explain differences in results between studies. Besides inclusion criteria and a subjective classification, genetic variations between populations in different regions of the world, presumably explain the different prevalence of malformations/variations in tooth and root-morphology.
Enamel defects
Local enamel defects were found in 52.7% of the skulls in our study and in 2.2% of examined teeth although histologic examination was not performed. The most affected teeth were the maxillary and mandibular canines followed by mandibular premolars and maxillary incisors. Enamel hypoplasia with a prevalence of 2.5% has previously been reported as the third most common finding in the Polish red fox population [8]. In another study 6.9% of the skulls presented enamel defects most frequently presented in the canine teeth, like in our study [6]. The reason for higher prevalence of enamel defects in our study compared to others is unclear. The fact that staining was a common finding in our study may have been a confounding factor.
Attrition / abrasion
Dental wear commonly occurs in free ranging carnivores. In our study, in total 149 teeth (6.5% of examined teeth, 25% of the foxes) were affected by attrition or abrasion. One earlier study reported a prevalence of 3,5% attrition/abrasion in the skulls another 1% of examined teeth [13, 7], which is considerably lower than in our study. In contrast, one study reported so-called stage 1 attrition/abrasion in 94% of the specimens, however, as stages of attrition were not specified in our study, comparison is difficult [6]. Further, in another study, most of the grey foxes (85.6%) exhibited some degree of attrition and abrasion, affecting 47.1% of the teeth present for examination [7]. The fourth premolar teeth and the first and second molar teeth in all quadrants were the most affected teeth, unlike in our study, where the upper and lower incisors and the upper canines were the most affected teeth. The difference in abrasion pattern may indicate a different dietary habit, suggesting that the grey fox ingest a higher proportion of plant material [22]. Age of the animal is also a significant factor to consider when assessing attrition and abrasion. The older the specimen, the more likely to find attrition and abrasion.
Dental fractures
In our study 80% of the foxes, or 8.7% of examined teeth presented with some type of dental fracture. The rostral and exposed position of the canine and incisor teeth and their role in defense and hunting may contribute to these teeth´s susceptibility for fracturing. Dental fractures were noted in 78.4% of foxes and 15.4% of examined teeth in the grey fox from California, USA, although radiography was not included in this study [7]. This is consistent with our results, except that the prevalence of enamel fractures was higher in our study. As in our study the canine teeth were the most frequently affected teeth. Another recent study of the red fox, although not including radiography, reported tooth fractures in 51% of the skulls or 3,1% of examined teeth [6]. Root fractures were most common especially in the incisors, followed by complicated crown fracturs and complicated crown root fractures. Diet, age and the size of the prey for different species, may affect the type of tooth fracture and most affected teeth in the oral cavity.
Periapical radiolucency, indicating endodontic disease, was present in 38.2% of the foxes and often seen together with root resorption. In our study endodontic disease was noted primarily together with complicated crown fractures which were present in 20% of the foxes. Other trauma like uncomplicated crown fractures, attrition/abrasion, as well as periodontal disease can cause endodontic disease and may explain the presence of periapical radiolucency seen in teeth without complicated crown fractures. Endodontic disease can be highly painful, implying that a considerable number of foxes may experience oral pain. [4].
Periodontitis
Horizontal and vertical bone loss are indications of periodontitis [23]. In our study 29% of the foxes showed localized horizontal bone loss and 20% showed vertical bone loss. No classification of the periodontal disease into different stages was performed in our study [4]. The most affected teeth, especially with horizontal bone loss, were the mandibular third and fourth premolars and the mandibular molar teeth. This aligns well with the study of grey foxes, where about half of the specimens displayed some degree of bony changes consistent with periodontitis [5]. Like in our study, premolar teeth were most affected. Early onset and high prevalence of periodontitis is described in other canids such as the domestic dog [24].
Methodological considerations
Prevalence of absent teeth are frequently included in studies on dental variations and anomalies in wild animals [5–8, 10, 11, 13]. Museum specimens are commonly used when analyzing oral and dental anomalies and pathology [5–8, 11–13]. In a dry museum specimen, true congenital tooth absence has been described as presenting with a flat and straight bony ridge, in contrast to traumatic tooth loss where a scar like, small elevation or pocket at the original location of the tooth may be seen. Identification of missing teeth in museum specimens usually rely solely on macroscopic findings while dental radiography is seldom used. Hence it can be difficult to determine if a tooth is missing congenitally or as consequence of trauma. The criteria for tooth absence are conclusive for assessment of the result and the possibility to compare results between studies.
Dental radiography is thus crucial in identification of tooth absence. Tooth root remnants and a visible alveolus are signs that confirm acquired tooth absence. Morphologic normal bone together with absence of alveolus and tooth at the site is characteristic of a congenital tooth absence, however, if an old individual has lost a tooth early in life, the bone will show a similar appearance as with congenital tooth absence making it difficult to determine the etiology behind tooth absence in elderly animals [17]. Hereby, age becomes another factor influencing the determination of the etiology behind missing teeth and may implicate a negligible risk of misjudgment in our study.
The composition and the ratio between young and old individuals in a study group must be considered when comparing results of different studies. Age can be estimated in various ways, e.g. based on tooth eruption and the development of the cranial sutures or examination of the cementum annuli [25, 26, 27]. In our study the width of the pulp was used to estimate the age of the foxes [3]. Similar to our study, many studies divided their study population into groups based on age: adult or young adult [5, 6, 7, 13]. With respect to age, our study population was comparable to these studies provided that our juvenile group was counted as young adults. Foxes with deciduous teeth were excluded in all studies.
One limitation of this study was the relatively low number of examined specimens. Further, all specimens were collected from a limited geographic area of Sweden. Further studies on a larger population of foxes with known sex, more exact age determination and from different regions of Sweden would give an even more accurate depiction of the dental anomalies, variations and pathology existing in the Swedish red fox.