Radiographic Changes Associated with Tooth Resorption Type 2 in Cats
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1 Radiographic Changes Associated with Tooth Resorption Type 2 in Cats Susann-Yvonne Mihaljevic, Dr med vet; Alice Kernmaier, Dr med vet; Svea Mertens-Jentsch Summary: The aim of this retrospective study was to follow the progression of radiographic changes in intentionally retained roots of teeth affected with tooth resorption type 2 in cats. Emphasis was placed on assessment of degree of resorption as well as the occurrence of inflammatory changes in tooth roots. The results confirm that crown amputation is an adequate treatment in cats for teeth affected by type 2 resorption. J Vet Dent 29 (1); - &*. Introduction The term feline odontoclastic resorptive lesions or tooth resorption (TR) as currently recommended is defined as the destruction of hard dental tissue by activated odontoclastic cells in the cat. 1 The increase in activity of odontoclastic cells is related to mediators of inflammation and cytokines. The actual cause for this disease is still unknown. There is controversy concerning the pathogenesis of TR. Some authors argue that it is primarily a non-inflammatory disease whereas other sources interpret TR as an inflammatory disease. 2-5 These lesions that used to be called neck lesions (or feline caries, cervical neck lesions, cervical line erosions) in older literature are widely distributed in the whole cat population and are described as quite painful and one of the most frequently under diagnosed diseases in veterinary medicine. 6,7 The frequency of cats with TR varies according to the study protocol and has been reported between 28.5 % in a randomly selected cat population and 67 % in cats that were presented for dental problems. 8,9 Regardless of study design, dental radiographs are mandatory for making an accurate assessment for the presence of this disease in cats. 10 The distribution pattern of affected teeth is symmetrical in most cats. Frequently affected teeth include the third mandibular premolar as well as the first mandibular molar, the maxillary canine, and the maxillary fourth premolar. 1,6,11,12 There is a significantly higher number of cats > 10-years-old that have TR with dental calculus being a highly associated (75 %) clinical finding. 3,13,14 The actual degree of dental disease can be diagnosed only by thorough probing and dental radiographs without superimposition of other structures. 3 Examining the cervical area of affected teeth with a periodontal probe to detect periodontal pockets usually causes pain ( chattering ) probably due to exposed dentinal tubules that communicate with the pulp. 6 However, this clinical finding is not necessarily diagnostic since it can occur when probing visually unaffected teeth. Interpretation of dental radiographs is essential for the differentiation of TR type 1 and type 2 because the most distinctive changes can be seen in the area of the tooth roots with the crown potentially remaining clinically normal. 14 Ankylosis and osteoid remodelling that are characteristics of TR type 2 result from the degradation and modification of dentin and cementum into osteoid repair tissue (Fig. 1). The periodontal ligament space disappears whereas the physiological height of the alveolar crest generally remains unchanged. In cases of spontaneous crown fracture, the height of the alveolar crest may even be increased. With TR type 1, horizontal and vertical bone loss are common with exposure of the furcation. Periodontal ligament space and roots generally remain unchanged or show signs of periodontitis (Fig. 2). Recently, another definition was created by the American Veterinary Dental College (AVDC) Nomenclature Committee and termed TR type 3 that shows features of both type 1 and type 2 resorption in the same tooth. A tooth with this classification has areas of normal and narrow or lost periodontal ligament space, with focal or multifocal radiolucent areas in the tooth and decreased radiopacity in other areas of the tooth. The purpose of this study was to follow the progression of radiographic changes in intentionally retained roots of teeth affected with TR type 2. Materials and Methods Fifty-six cats were chosen from the dental patient population of the Small Animal Veterinary Clinic, Ravensburg. Cats of all ages and breeds were examined. The tooth status of these cats had been analyzed and classified at least once and as many as 4 times following the initial diagnosis using dental radiography with digital CCD-sensor-technology. The period of time between examinations varied from a minimum of 6-months to a maximum of 73-months. Radiographic changes of TR type 2 root remnants (TR Stage 5) were classified as follows: a) root not visible, complete resorption; b) root or root remnants partially visible (in resorption) without radiographic evidence of inflammation; c) root remnant visible without radiographic evidence of resorption or inflammation, ankylosis possible; d) root remnants visible with radiographic evidence of inflammation. Radiographic evidence of inflammation included radiolucency of the bone, a wider than normal periodontal space, lytic lesions of tooth root and the periradicular area, or complete bone loss (Table 1). Only the mandibular premolar and molar teeth were examined with the teeth being assessed individually. Dental radiographs were obtained using a parallel intraoral technique. In order to correctly represent the apical aspect of the mandibular third premolar tooth; a slightly modified parallel technique was performed (Fig. 3). The cat is placed in lateral recumbency with the teeth that are to be examined toward the x-ray beam. The sensor is then placed intraorally between 20 J VET DENT Vol. 29 No. 1 Spring 2011
2 Table 1 Nomenclature for tooth resorption as recommended by the American Veterinary Dental College. Stage 1 (TR1): Stage 2 (TR2): Stage 3 (TR3): Stage 4 (TR4): Stage 5 (TR5): Mild dental hard tissue loss (cementum or cementum and enamel) Moderate dental hard tissue loss (cementum or cementum and enamel with loss of dentin that does not extend to the pulp cavity) Deep dental hard tissue loss (cementum or cementum and enamel with loss of dentin that extends to the pulp cavity); most of the tooth retains its integrity Extensive dental hard tissue loss (cementum or cementum and enamel with loss of dentin that extends to the pulp cavity); most of the tooth has lost its integrity (TR 4a) crown and root are equally affected (TR 4b) the crown is more severely affected than the root (TR 4c) the root is more severely affected than the crown remnants of hard dental tissue are visible only as irregular radiopacities and gingival covering is complete the mandibles as far ventral as possible and parallel to the mandible. The X-ray tube is moved in a slight ventrodorsal direction from the correct 90 position to the mandible and sensor. This positioning is aided by cat placement on a special foam mattress a with a concave shape. With this technique, it is possible to achieve a complete image of all mandibular roots without appreciable root elongation or foreshortening. Figure 1 Intraoral radiograph of the lateral left mandible showing the third premolar tooth with tooth resorption (stage 4a-type 2). There is marked loss of dentin in the area of the crown as well as the root extending into the pulp without any radiographic evidence of inflammation. Note the maintained height of the alveolar crest and root replacement by bone. In particularly narrow small oral cavities, the ventral sublingual edge of the sensor can be inclined towards the symphysis with the dorsal palatal edge adjacent to the crowns of the maxillary teeth as a further modification. Radiographs were taken using a CCD-sensor b. Exposure settings used for these intraoral radiographs were 60 kv, 7mA, 0.05s. The images were saved using digital software c. Figure 2 Intraoral radiograph of the lateral left mandible showing tooth resorption of the third (TR-S3-T1) and fourth (TR-S1-T1) premolar teeth. Note the maintained periodontal ligament space and horizontal bone loss. The image contrast was enhanced to make the distal root remnant of the first molar tooth with an apical radiolucency more visible. J VET DENT Vol. 29 No. 1 Spring
3 Figure 3 Photograph showing the classical intraoral parallel technique (A) to image the feline mandibular premolar and molar teeth. The anatomy of the osseous symphysis and narrowing of the rostral mandible make it difficult to position the sensor/film to image the entire third premolar tooth including the root apices. Modification of the parallel technique places the sensor/film more ventral and adjusting the x-ray tube in a ventrodorsal direction provides an approximate 65 degree angle to the parallel teeth/sensor-axis (B). An additional modification includes tipping the sensor/film diagonally with the ventral edge of the sensor/film next to the opposite arcade of mandibular teeth (arrowhead) and the dorsal edge placed buccally along the ipsilateral maxillary arcade (arrow). The X-ray tube is adjusted to a 90 angle towards the sensor/film (C). Crown amputation with intentional root retention was performed as described previously. 15 Lingual and buccal gingival flaps were prepared. The crown was amputated with a small round bur at the height of the alveolar crest and remaining root tissue carefully removed to a depth of 1 to 2-mm. One pellet containing 10.0 mg framycetin (neomycin B) and 2.0 mg lidocaine hydrochloride d was placed in the wound. The gingiva was apposed with absorbable suture material in a simple interrupted pattern. Results Of the 56 cats examined, 67.8 % were diagnosed with continued resorption that showed a partially visible root remnant(s) in resorption without radiographic evidence of inflammation (Group b) [Fig. 4]. Cats (14.3 %) also showed continued signs of TR type 2 (Group a) with a completely resorbed root(s) [Fig. 5]. Additionally, 14.3 % of cats showed a non-resorbed root remnant(s) (Group c) with possible progression of ankylosis without radiographic evidence of inflammation (Fig. 6). The smallest group of cats (3.6 %) constituted those that showed signs of unchanged TR type 2 with evidence of an inflamed root remnant(s) suggestive of TR type 3 (Group d) [Fig. 7]. The graphical representation of the distribution of changes in teeth affected by tooth resorption 2 is shown in Fig. 8. The interval between initial diagnosis and follow-up radiographic examination ranged from 6 to 73-months (Fig. 9). Most cats were presented within the first (27.1 %) or second (23.7 %) year following initial diagnosis. Discussion The results of this retrospective study confirm that crown amputation is an adequate treatment for teeth affected by TR type 2. It also reinforces that proper classification of this disease is required for successful treatment and outcome. Teeth of the lateral mandible were chosen for evaluation since the third premolar and first molar are commonly affected by TR. 16 Other authors have shown that there is a high statistical correlation between the TR of the third mandibular premolar tooth and TR status of the whole dentition. 17 Further, dental radiographs of these teeth are taken using a parallel technique making comparison of dental radiographs at different points in time more accurate. Teeth of the maxilla are more difficult to evaluate due to superimposition of the zygomatic process, and the use of the bisecting angle teeth that may be more cumbersome and require more re-takes for comparable radiographs over time. With the radiographic classification of tooth resorption, various factors can lead to misinterpretation. Older cats, for example, often show signs of hypercementosis or periradicular ostitis which can be superimposed on the periodontal ligament and be confused with ankylosis. The presence of mixed TR types may complicate classification especially when involving the same tooth. Radiographic evaluation of bone loss is a relatively insensitive diagnostic tool making bone loss early in the disease process difficult to determine. By comparing radiographs and histological specimens, other authors were 22 J VET DENT Vol. 29 No. 1 Spring 2011
4 Figure 4 Radiograph of the left mandible before (A) crown amputation of the fourth premolar (308) tooth (TR-S4a-T2) showing a ghost root (Group b). Vaguely visible are root remnants of the first molar (309) tooth (Group a) and third premolar (307) tooth (TR-S5-T2, Group b). The 2-year postoperative radiograph (B) shows progressive resorption of 308 (TR-S5-T2, Group b) with only apical root remnants visible. The roots of 307 and 309 continue to be resorbed, however there are a few noticeable radiolucent areas at the alveolar crest of 309. Areas such as these should receive continued radiographic monitoring when associated with gingival inflammation is present. Figure 5 Radiograph of the right mandible before (A) crown amputation of the third premolar (407) tooth (TR-S4c-T2; Group b). Crown and root remnants of 407 are in resorption without radiographic evidence of inflammatory changes. There appears to be incipient ankylosis of the fourth premolar tooth (408). The 2-year postoperative radiograph (B) shows complete resorption of 407 (TR-S5-T2, Group a) tooth roots. Note the progressive ankylosis and apical resorption of 408 as well as incipient resorptions at the cementoenamel junction of both 408 and the first molar tooth (409). The 6-year postoperative radiograph (C) shows complete resorption of 407 (TR-S5-T2, Group a) with completely remodelled roots that remain free of radiographic evidence of inflammatory changes. The 408 and 409 show progressive TR type 2. Although the mesial root of 409 shows typical changes of type 1 TR such as horizontal bone loss and hypercementosis of the lamina dura, this cat was included only to document the progression of 407 pathology. Editor s Note: suboptimal positioning of images in this figure was obtained before the authors developed alternative techniques to view the entire 307/407. J VET DENT Vol. 29 No. 1 Spring
5 Figure 6 Radiograph of the left mandible (A) showing TR-S5-T2, Group c of the fourth premolar tooth (308) and TR-S5-T2, Group b of the third premolar tooth (407). There was spontaneous crown fracture of 307 whereas the crown of 308 had received crown amputation. There is an apical radiolucency at the mesial root of the 308 that required radiographic monitoring. Note the area of increased radiolucency that could indicate early resorption of the distal aspect of the dentinoenamel junction of 309. The 2-year follow-up radiograph (B) shows progressive resorption of 307 with only very slight signs of remodelling of 308 (TR-S5c-T2, group c). The apical radiolucency of the mesial root of the 408 had not progressed. Further monitoring was recommended for this tooth and the expanding TR lesion at the distal dentinoenamel junction of 309. The 6-year follow-up radiograph (C) shows continued resorption of 307 and no substantial changes of 308 since the previous radiographic examination. When comparing with the previous examination radiograph, there is increased radioopacity of the roots of 308 in comparison with true ghost roots of 307. There is progressive ankylosis of the roots of 309 with only very slight expansion of the lesion at the dentinoenamel junction. Figure 7 Radiograph of the right mandible (A) before crown amputation of the fourth premolar tooth (408) showing TR-S4c-T2, group b resorption at the dentinoenamel junction and of the mesial and distal roots with increased radioopacity of the apical parts of the roots. The right mandibular third premolar (407) and molar (409) teeth are missing and there is increased radioopacity in the apical part of the nearly completely resorbed distal root of 407. Note small radiolucent areas demarcated with a radioopaque line in the region of the completely resorbed mesial root of 409. The 2-year follow-up radiograph (B) shows even more radioopacity of the root remnants of 408, with little progression in resorption and some radiolucent areas in the apical area and near the alveolar crest (group d). Note a radioopaque area at the apical part of the resorbed distal root of 407. The 6-year follow-up radiograph (C) shows no further resorption of the 408 root remnants. Note the 3 radiolucent areas (two near the alveolar crest and one apically near the distal root remnant). 24 J VET DENT Vol. 29 No. 1 Spring 2011
6 able to show that primary changes of TR cannot be diagnosed radiographically. 18 Likewise the often described burn-out artifact with a radiolucency in the area of the dentinoenamel junction can cause misinterpretation especially in the area of the furcation. 7,19 Finally, the clinician should always understand that the 2-dimensional image represents a 3-dimensional structure and therein lies reason for difficult or incorrect interpretation. The resorption process of the teeth of this study occurred at varying speeds without radiographic evidence of inflammation which confirms the results of other authors. 2,3 Speed of resorption may certainly be influenced by the degree of resorption at the time of diagnosis. For example, if ghost roots are present to a certain degree at the first radiographic examination, end-stage TR is already present. Therefore, resorption would seemingly take place more quickly between the first and second examinations. Also, the technique for crown amputation and the amount of superficial root and bone removal may also affect resorption rate. Thorough superficial root and bone removal of infected tissue will lead to better healing of the wound with complete resorption and remodelling of bone without any evidence of inflammation. In contrast, an iatrogenic wound infection due to poor technique and /or an insufficient wound closure can lead to a prolonged or inappropriate healing including faster resorption and delayed remodelling of bone. Therapeutically, if a definite classification of TR type 2 is not possible or if there is marked gingivitis, the treatment of choice should be complete extraction of all affected teeth and dental remnants. Crown amputation and intentional root retention is an established procedure for clearly diagnosed TR type 2. This technique should be used when the root(s) is in an advanced stage of resorption and it is not possible to remove the root without causing excessive trauma to the bone substance. After performing crown amputation, radiographic examinations should be performed regularly to monitor root status. The results of our study are in agreement with previous studies that evaluated the progression of TR and root replacement after crown amputation in cats. 15,20 In order to radiographically evaluate intentionally retained root remnants, we suggest an additional classification depending on the degree of resorption (no resorption, in resorption, completely resorbed) and presence or absence of radiographic Figure 8 Graphical representation of the distribution of changes in teeth affected by tooth resorption type 2. Root Remnants Visible with Radiographic Evidence of Inflammation Root Remnant Visible without Radiographic Evidence of Resorption or Inflammation, Ankylosis Possible 14.3 % 3.6 % 14.3 % Root Not Visible, Complete Resorption 67.8 % Root or Root Remnants Partially Visible (in Resorption) without Radiographic Evidence of Inflammation J VET DENT Vol. 29 No. 1 Spring
7 Figure 9 Graphical representation of the period of time between the first and last radiographic examination of teeth with tooth resorption type 2. Time (months) Percent of Animals 15.3 % 27.1 % 23.7 % 15.3 % 10.2 % 6.8 % 1.7 % 30 % 25 % 20 % 15 % 10 % 5 % 0 % Time (months) inflammatory signs such as radiolucency, widened periodontal space, lytic lesions of tooth root and the periradicular area, or complete bone loss. This could provide a comprehensible documentation of the course of disease and should be discussed further. a Dento-Dorm, Dento-Dorm GbR, Ravensburg, Germany b c d Heliodent DS, Bensheim, Germany Sidexis, Bensheim, Germany Leukasekegel, Dermapharm AG, Grünwald, Germany Author Information From the Clinic for Small Animal Medicine in Ravensburg (Mihaljevic), Eywiesenstr. 4, Ravensburg, Germany; Eckenerstr. 95/1 (Kernmaier), Friedrichshafen, Germany; Hahnstr. 8/2 (Mertens-Jentsch), Markdorf, Germany. s.mihaljevic@tierlinik-rv.de References 1. Gorell C. Feline odontolastic resorptive lesions. Proceedings of the 28th World Congress. XXVIII. WSAVA, Bangkok (2003). 2. Gorell C, Larsson A. Feline odontolastic resorptive lesions: unveiling the early lesion. J Small Anim Pract 2002; 11: Roes F. Pathogenese, Diagnostik und Therapie bei neck lesions der Katze unter Verwendung von GLAS-IONOMER-ZEMENTEN. Berlin, Freie Universität, Fachbereich Veterinärmedizin, Dissertation (1996). 4. Roes F. Pathohistologie der Zahnhartsubstanzzerstörung bei der Katze. Prakt Tierarzt 2004; 3: Möllenbeck S. Histologische Untersuchungen zu Frühveränderungen der Felinen 26 J VET DENT Vol. 29 No. 1 Spring 2011 Odontoklastischen Resorptiven Läsionen (FORL) an klinisch gesunden Zähnen. Prakt Tierarzt 2004; 3: Eickhoff M. 14 Katze Spezial, 14.1 Feline odontoklastische resorptive Läsionen (FORL). In: Eickhoff M Zahn-, Mund- und Kieferheilkunde bei Klein- und Heimtieren. Stuttgart: Enke Verlag, 2005; Mulligan TW. Classification of feline cervical line lesions. Proceedings of the Annual Veterinary Dental Forum. Las Vegas; Schlup VD. Epidemiologische und morphologische Untersuchungen am Katzengebiss. Kleintierpraxis 1982; 27: Van Wessum R, Harvey CE, et al. Feline dental resorptive lesion prevalence patterns. Vet Clin North Am Small Animal Pract 1992; 22: Verstraete F, Kass PH, et al. Diagnostic value of full-mouth radiography in cats. Am J Vet Res 1998; 6: Harvey CE, Orsini P et al. Mapping of the radiographic central point of feline dental resorptive lesions. J Vet Dent 2004; 1: Ingham KE, Gorell C, et al. Prevalence of odontoclastic resorptive lesions in a population of clinically healthy cats. J Small Anim Pract 2001; 9: Pettersson A, Mannerfelt T. Prevalence of dental resorptive lesions in Swedish cats. J Vet Dent 2003; 3: DuPont GA. Tooth resorption. In: Atlas of dental radiography in dogs and cats. Saunders Elsevier:St. Louis, 2009; DuPont GA. Crown amputation with intentional root retention for advanced feline resorptive lesions - a clinical study. J Vet Dent 1995; 1: Ingham KE, Gorell C, et al. Prevalence of the feline odontoclastic resorptive lesions in a cat population. Proceedings of the 9th Annual Meeting of the European Veterinary Dental Society, Copenhagen; Heaton M, Wilkinson J et al. A rapid screening technique for feline odontclastic resorptive lesions. J Small Anim Pract 2004; 12: Roes F, Möllenbeck S. Untersuchungen zur Pathogenese der felinen odontoklastischen resorptiven Läsion (FORL). Kleintierpraxis 2003; 11: Mulligan TW, Aller MS et al. Acquired defects: caries and regressive changes. In: Atlas of Canine and Feline Dental Radiography. Yardley, PA: Veterinary Learning Systems, 1998; Gengler W, Dubielzig R, et al. Physical examination and radiographic analysis to detect dental and mandibular bone resorption in cats: a study of 81 cases from necropsy. J Vet Dent 1995; 3:
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