FELINE DENTISTRY

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GINGIVITIS/STOMATITIS IN CATS Charles A. Williams, DVM, and Mary Suzanne Aller, DVM

DESCRIPTION AND ETIOPATHOGENESIS

Chronic inflammatory conditions affecting the gingiva and oral mucosa of domestic cats have been variously termed feline plasma cell gingivitis-pharyngitis, feline gingivitis-stomatitis, plasmacytic stomatitis-pharyngitis, and feline lymphocyticplasmacytic gingivitis, depending on the distribution of lesions and based on histopathology. 10• 53• 59• 68 • 115• 121 Feline oral inflammatory disease may range from simple gingivitis, in which the only tissue affected is the gingiva itself exhibiting hyperemia, edema, and bleeding, to varying degrees of stomatitis, in which the grossly obvious inflammation extends beyond the mucogingival junction into the oral mucosa 53 (Figs. 1 and Color Plate 1, * Figure 2). Cats with chronic inflammation of the gingivae and oral mucosa frequently exhibit ulceration and extensive proliferation of granulation tissue, with lesions extending well onto the palatoglossal folds and fauces (Color Plate 1, Figure 3). Presenting signs usually include halitosis, ptyalism, dysphagia, inappetance, and weight loss. 121 The most consistent hematologic abnormality reported has been a polyclonal hypergammaglobulinemia. 68• 121, 163 There may be evidence of external root resorption or retention of root tips or bony sequestrae in edentulous areas. 58• 59 • 114 The exact cause is unknown, but the condition has been characterized based on the frequent histologic finding in gingival biopsies of a heavy infiltrate of inflammatory cells predominantly of the lymphocytic and plasmacytic types 68 • 85 (Fig. 2). Although these findings are suggestive of an immunologic basis for the condition, a number of studies have also implicated oral bacteria, particularly the gram~negative anaerobe black-pigmented Bacteroides species. 82 • 90• 106• 132 Others report a high incidence of calicivirus in cases of stomatitis, 27• 48• 147• 159 and oral infections are reported to be a common clinical sign associated with the acquired feline immunodeficiency diseases of feline leukemia virus (FeL V) and feline immunodeficiency virus (FIV). 35· 56 • 160• 162 In fact, any compromise of the body's ability to resist and repair is likely to result in the exacerbation of oral disease, with similar gross clinical signs in which infection or inflammation is chronic. 47• 56 *See color section in the beginning of this issue. From the Blue Cross Animal Hospital, Fairfax, Virginia

VETERINARY CLINICS OF NORTH AMERICA: SMALL ANIMAL PRACTICE VOLUME 22 • NUMBER 6 • NOVEMBER 1992

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Figure 1. A and B, Simple gingivitis in two 10-month-old cats. There is hyperemia and edema of the gingiva, especially of the upper premolars.

Regretfully therefore any form of gingivitis or stomatitis that is nonresponsive to treatment is likely to be lumped into a single category regardless of cause. This is especially true when biopsy reports consistently come back reporting gingivae infiltrated with inflammatory cells predominantly of the lymphocytic and plasmacytic types. These histologic features, however, are to be expected with chronic infiltration of bacteria or other antigenic or mitogenic stimuli.53· 89 Recently there have been some attempts to classify feline oral disease in stages based on the amount or degree of inflammation as seen on gross examination, but it is not known if the wide range of clinical presentations are due to separate diseases or if they simply represent stages of the same disease. 41 • 53 There has been speculation that studying the responses of oral tissue to oral flora may be more meaningful than the search for a specific etiologic agent. 53 It is along this line that we would like to proceed with this article because there are a number of mechanisms by which the host response, which is normally protective, can result irt tissue destruction and chronic inflammation. We begin with a review of the normal host defenses to oral

Figure 2. Photomicrograph of a feline gingival biopsy specimen exhibiting lymphocyticplasmacytic infiltration. (Courtesy of K. Lyon, Mesa, AZ.)

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disease, then cite evidence of a number of pathways of destructive host responses. We conclude by discussing some common clinical presentations, showing how the information helps us to devise treatment strategies. For the detailed description of specific treatment techniques, the reader is directed to the cited references. In all species, the gingival tissue is continually subjected to both mechanical wear and plaque bacterial exposure. The primary defense against oral disease is provided by the epithelial surface, the saliva, and the initial inflammatory response. Healthy epithelium provides an effective protective barrier, although some endotoxins are able to diffuse through mucosal membranes and alter permeability, allowing penetration of additional antigens. Saliva exerts a major influence on plaque by mechanically cleansing oral surfaces,· buffering acids, and controlling bacterial activity. The major antibacterial factors in saliva include enzymes, leukocytes, and antibodies. The initial protective inflammatory response involves phagocytosis by polymorphonuclear leukocytes and is characterized histologically as a widening of small capillaries with adherence of neutrophils to the vessel walls. Leukocytes can be seen migrating through capillary walls, with increasing numbers found in the connective tissue, junctional epithelium, and the gingival sulcus. 11 Once past this initial defense, foreign materials are processed by macrophages, which incur secondary responses via both humoral and cellular pathways. 55 • 148 The differentiation of lymphocytes then results in the production of immunoglobulins by plasmocytes (humoral) and the interaction of T lymphocyte populations (cellular). Thus periodontal lesions begin with acute inflammation dominated by an infiltration of polymorphonuclear leukocytes. This acute response gives way to a T lymphocyte-dominated lesion and finally converts to a B cell-plasma cell dominated lesion. 146 During these processes, a much more severe inflammatory response may ensue, which potentiates pathways for host tissue damage. 28 • 124 Inflammatory mediators produced by the host can induce a series of complex changes that results in gingival pocket formation, gingival recession, and bone and tooth resorption. 21 • 60 · 101 • 124 Therefore the maintenance of healthy gingiva is based on an equilibrium between the bacterial challenge and the host defenses. Disease will occur when the balance is broken either by increased amount or virulence of the bacteria or by altered defense mechanisms of the tissue. 101 The accumulation of plaque bacteria can contribute to the production of gingivitis or periodontal disease either by direct pathogenic effects or by inciting a destructive inflammatory process. 60 • 106 Because plaque bacteria can actually adhere to many oral surfaces, such as teeth, gingiva, mucosa, calculus, and other plaque formations, it would appear that animals have little hope of completely eliminating the inciting organisms. 20• 39 Protective inflammatory and immune responses reduce bacterial numbers, and there may be a period of remission. As the organisms recolonize and proliferate, however, there is a return of inflammation, and the characteristic waxing and waning of inflammation seen in chronic periodontal disease can be observed. 106 Other forms of gingivitis-stomatitis or periodontal disease can be explained on the basis of immunodeficiency, hypersensitivity, or other compromise in the host's ability to resist and repair.

DEFICIENT HOST RESPONSE

In 1982, Perryman109 listed five mechanisms for naturally occurring immune incompetence in animals: (1) failure to acquire passive immunity, (2) inherited

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deficiency of the complement system, (3) inherited deficiency of the neutrophil or neutrophil function, (4) inherited deficiencies of lymphocytic function, and (5) absence of hormone or cofactors required for lymphocytic differentiation and function. In addition, inherited monocyte dysfunction is known to play a role in the development of gingival disease. 106 Although one cannot be certain that all of these mechanisms result in oral disease, there are some well-documented conditions that do tend to support this concept. In humans, there is evidence that early-onset periodontitis is familial and is due to an autosomal recessive trait. 146 In most cases of juvenile periodontitis in humans, neutrophil dysfunction is suspected or documented as one underlying cause. 106 Likewise in Chediak-Higashi syndrome, an inherited neutrophil and monocyte dysfunction documented in humans, cattle, Persian cats, and mink, there is early-onset oral disease leading to rapid tooth loss.47· 57· 106 Further, gingival disease is reported to be a prominent feature of cyclic neutropenia, which is known to occur in humans and dogs (Gray Collie syndrome). 95 Cyclic or chronic neutropenias have also been associated with oral inflammation in the catY· 140· 141 ' 156 Staphylococcus aureus is known to produce a leukotoxin that causes a granulocytopenia. 66 Staphylococcus species have been associated with chronic osteomyelitis of dental origin in cats/0 This leads to the hypothesis that any quantitative or qualitative neutrophil dysfunction can predispose to oral disease by compromising the body's first line of defense. Acquired immune deficiency has been associated with feline dental disease.36 Early reports have shown FeLV infections to be a cause of immune deficiency with stomatitis as a prevalent sign. 27· 62· 88 Although later studies indicate the percent of feline stomatitis cases caused by FeLV is low, it is reported that FeL V is capable of inducing FIV. 74· 128 FIV-infected cats are characterized by a reduction in lymphocytes and neutrophils, reduced T cell blastogenic response, and impaired antibody production. 128· 149 The most commonly reported clinical sign associated with cats infected with FIV is gingivitisstomatitis/· 34• 35· 49· 103· 131 · 158· 160· 162 In a survey of 78 British and 18 North American cats with chronic stomatitis, the reported prevalence of FeLV was low, but the incidence of both FIV and feline calicivirus (FCV) were very high when compared with controls. 74 The high incidence of FCV is not clearly understood, and there are conflicting reports regarding its significance in chronic stomatitis. 54· 75 Hematologic abnormalities, immunodeficiency, and oral disease in cats infected with FIV, however, are quite comparable to what is well documented in humans infected with the human immunodeficiency virus (HIV). 2· 108· 129 Human HIV patients experience T cell deficiency and immune system malfunction. Clinically they exhibit many oral symptoms including hairy leukoplakia, candidiasis, aphthous stomatitis, and rapidly progressive periodontal diseases. 3· 42• 50· 51 · 81 Certain periopathogenic bacteria are also known to induce temporary immune dysfunction through endotoxin production, perpetuating gingival disease. 106 Many chemicals also have a marked effect on the immune system. Both cytotoxic drugs and corticosteroids are known to inhibit both humoral and cellular immunity. These drugs tend to inhibit the initial production of immunoglobulin more readily than the anamnestic response. 76 Griseofulvin has been shown to cause a neutropenia. 130 Although the mechanism is not always clear, stress in and of itself or the stress of concurrent disease will also reduce a patient's ability to prevent dental disease, and therefore gingivitis-stomatitis can appear as a clinical sign. 27· 71 Likewise, nutritional deficiencies, endocrine dysfunctions, or metabolic diseases will alter the host response with similar results. 5· 13 Acute necrotizing ulcerative

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gingivitis (ANUG), also known as trench mouth or Vincent's stomatitis, is an example of a condition in which organisms usually considered to be nOrJ;Ilal oral inhabitants are incriminated in a disease process. 22 ANUG is an acute infection associated with spirochetes and fusiform bacillus and brought on by stress. 26' 71 Cases of ANUG have been reported in both dogs and cats.n, 83 In cats, it has also been reported to be associated with FIV infection."' Attempts were made to induce the condition experimentally by innoculating healthy Beagles with plaque from an ANUG patient-73 The only individuals that developed the condition were those dogs given corticosteroids, alluding to the fact that individuals exposed to the organisms do not become diseased unless immunocompromised.

HYPERSENSITIVITY, POLYREACTIVITY, AND AUTOIMMUNITY

In addition to immunosuppression as a factor in oral disease, many immune-mediated pathways of host tissue destruction have been described. 38 ' 63 ' 64' 106 Lymphocytic transformation studies have shown that cell-mediated immunity against gram-negative microorganisms plays an important role in the pathogenesis of periodontal disease in humans. 65 There is a significant blastogenic response of human lymphocytes to sonicates of oral bacteria that is due to specific antigens and is not mitogenic in nature. 107' 112 It appears that both immediate and delayed hypersensitivities can be involved in the production of oral disease. 63 In humans, gamma immunoglobulin E (IgE)-containing plasma cells found in gingival tissue are suggestive of an immediate hypersensitivity reaction to oral bacteria. When the IgE antibody combines with antigen, there is a release of histamines, slow reactive substance of anaphylaxis (SRS-A), bradykinins, and serotonin, which can result in host self-destruction. 102 The cell-mediated immune response known as the delayed hypersensitivity reaction causes host tissue destruction by lymphokines, which target epithelial cells and fibroblasts. 23 Thus the host response determines the degree of tissue breakdown, and the continued presence of the antigenic stimulus is the driving force for the persistence of inflammation. 124, 142 In 1980, Smith et al 134 hypothesized that severe periodontitis was the consequence of B cell hyperactivity. There are certain inbred strains of mice that hyperrespond to B cell mitogens, and this hyperresponsiveness is genetically determined. 146 There is evidence that B cell-produced interleukin is an important factor in bone resorption and that polyclonal B cell activation may lead to production of autoantibody, such as antitype I and antitype III collagens, with destruction of tissue through antibody-dependent, cell-mediated cytotoxicity reactions, immune complex formation, and complement activation. 146 In human periodontal disease, antibody to collagen can be found in gingival crevicular fluid. 113 With an increase in plasma cells in the gingiva, there is increased destruction of collagen attributed to autoantibody. 67 There are four factors required to incite maximum plasma cell response. They include (1) recent antigen-induced activation of antigen specific T and B cells, which have increased sensitivity to nonspecific activators; (2) specific antigen at the local site; (3) nonspecific activators at the local site; and (4) the local milieu of chronic inflammation. 89 Research suggests that autoreactivity is a consequence of polyreactivity. 52 ' 150 Many cases of chronic feline gingivitis-stomatitis may satisfy these criteria for polyclonal B cell activation as a cause of chronic oral inflammation. A common laboratory feature of severe gingivitis-stomatitis in cats is

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polyclonal hypergammaglobulinemia, and the immunohistology of feline gingival biopsies suggests that the histologic lesion of lymphocytic-plasmacytic gingivitis is due to polyclonal B cell activation. 78 The gram-negative anaerobe Bacteroides species, known to be a component of feline oral flora, have been shown to be potent polyclonal B cell activators. 112 There are reports of autoimmune-mediated oral lesions in the cat. 1· 91 Because autoreactivity can be a consequence of polyreactivity, one should question a diagnosis of primary autoimmunity based solely on oral immunofluorescence. The possibility exists that such a cat is actually suffering from autoimmunity induced by polyclonal B cell activation in dental disease. In our practice, we have seen a number of chronic stomatitis cases in cats that were positive for autoantibody as detected by immunofluorescence of gingival biopsies at the time of active clinical signs· yet were found to be negative when subsequently tested following successful treatment of dental disease and remission of signs. There are other autoimmune disorders, however, that have been documented as a cause of oral lesions. In pemphigus vulgaris, oral lesions are eventually found in approximately 90% of human and canine patients. 9 ' Likewise, oral lesions are common in bullous pemphigoid cases. I. 92 In pemphigus, the production of autoantibody is directed against antigen associated with the epidermal cell membranes, as opposed to pemphigoid, in which the antigen is found in the lamina Iucida of the basement membrane. 28

ROOT RESORPTION

In addition to soft tissue inflammation, the teeth and surrounding bone commonly develop resorptive lesions. 36· 53 · 114 When gingivitis, periodontitis, or chronic periodontal disease is present, horizontal and vertical bone loss occurs as a result of interleukin-induced bone resorption during the inflammatory process. 124 Subsequently external root resorption of the teeth at the cementoenamel junctions and furcations may occur. The lesions may not be visible during the oral examination because the crown will often be concealed by hyperplastic gingiva or granulation tissue (Fig. 3; and Color Plate 1, Figures 4-

Figure 3. A, A resorptive lesion on the canine exhibiting soft tissue filling in the defect. 8,

radiograph demonstrating the root resorption and ankylosis of a canine with a resorptive lesion. Reparative bone has filled the root defect, resulting in loss of normal root and periodontal structures. A premolar is also missing.

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5). These defects, however, can be detected tactilely with an explorer and appear painful. Deep lesions may actually reach the pulp chamber, and the granulation tissue may originate from the pulp, producing a pulpal polyp. (Figure 4, and Color Plate 2, Figure 5) As resorption progresses and extends apically, repair with new bone formation ensues, causing ankylosis of the root to the surrounding bone. (Fig. 3B) Radiographically early lesions are difficult to detect but may be discernible as minute radiolucent defects of the tooth usually at the furcation and cementoenamel junction but sometimes apically or coronally18 (Figs. 3B, 5B and 6). Advanced lesions will appear radiographically as large radiolucent cavitations within the crown or the root and in fact may be more properly termed internal resorption at this stage 21 (Figure 6, Color Plate 1, Figure 4). Root resorption that occurs within the bone and undergoes repair will appear radiographically as a defect in the contour of the root anatomy but with obliteration of the periodontal ligament space and lamina dura by reparative bone 21 (Fig. 7). The resorption may ultimately cause loss of most of the crown with retention of root and crown fragments. Even though the gingiva appears to heal, a persistent inflammatory response both in the bone and in the gingiva may follow and is associated with these retained root and crown fragments 70 (Fig. 8). These fragments may act as sequestra and form discrete fistulas. Thus even a cat that is edentulous can still experience gingivostomatitis of dental origin. Radiographically tooth fragments with various types of bony lesions will be discernible. Periosteal new bone formation, sclerosis, lysis, and cystic lesions can all be associated with the resorbing tooth fragments in the bone 122 (Figs. 8-10). Histologically this resorptive process entails features of inflammatory resorption and reparative resorption. 6• 21 Osteoclasts, which are derived from the monocyte line, are activated during the inflammatory process and are capable of resorbing both bone and dental tissues. 119• 126 During repair, osteoblasts are activated, and reparative bone can be formed in the defect. 6• 21 If inflammation is established within the bone, chronic osteomyelitis can be diagnosed histologically in later stages. 70• 122 The bone may actually be infected with oral bacteria or be chronically inflamed because the retained root fragments are colonized with oral bacteria and are a source of inflammatory mediators. 136• 152 The cause of this resorptive process in the cat is unknown at this time but appears to be often associated with chronic inflammation. 36• 125• 143 Both periodontal and endodontic disease or injury may play a role and induce external or internal inflammatory resorption of teeth. 6 · 21 • 77• 99 • 110• 135• 161 Experimentally external root resorption in the cat can be induced and detected histologically in 10 days from the onset of an inciting inflammatory event but may not be detected radiographically for 14 or more days. 157 The association of external root resorption in the cat with chronic inflammation and the predilection for certain furcation sites of the teeth may be a reflection of the anatomy of cat teeth. The short neck of many feline teeth will predispose to furcation exposure of plaque bacteria, toxins, and inflammatory metabolites early on in the development of periodontal disease even with mild gingival and bone recession. The concavity of the furcation anatomy potentiates gingival pocket formation, which would serve as a reservoir of plaque organisms. In addition, cats may have a higher incidence of accessory canals especially in furcation areas, complicating the pathologic process by involving pulp exposure to plaque bacteria. 30• 157 Another contributing factor may be chronic vomiting from any cause, such as hairballs. A certain percentage of humans suffering from anorexia/bulimia, a disease in which chronic vomiting is a feature, exhibit cementoenamel erosions. The low pH of gastric fluids deposited around the

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A

B

Figure 4. A, Resorptive lesions are present on all three cheek teeth. 8 , Resorptive lesions at the furcations, with severe loss of molar structure.

Figure 5. A, Bone loss at the furcation of both premolars and a resotptive lesion of the third premolar furcation. 8 , Resorptive lesions are present on all three cheek teeth.

Figure 6. Resorption appears to be occurring within the root canal of the third premolar.

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Figure 7. A, Defects in the contour of the root surface can be seen in both premolars. Note the relatively short caudal root of the molar. B, Resorption and bony repair of roots of both teeth are resulting in ankylosis.

Figure 8. A fragment of the mesial molar root associated with a bone defect and osteosclerosis.

Figure 9. Resorption of the canine root is incomplete, and bone lysis is associated with the unresorbed apical fragment.

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Figure 10. Bone defects are present at the alveolar site of the molar; there is external root resorption of the remaining molar and periosteal new bone formation at the site of the preexisting third premolar.

gingival margin after vomiting is thought to damage enamel and also may stimulate osteoclast activity. 69 • 118 • 11 9 Dietary risk factors are also suspected as another possible cause in the development of external root resorption. Surveys of cat skulls collected before circa 1960 show a low incidence of external root resorption, yet since 1960 the incidence has apparently increased. This suggests that the increased incidence of external root resorption is not due to our improved diagnostic ability but rather may be associated with some aspect of domestication such as changing feeding practices.36 • 53 There are no doubt multiple causes for external root resorption in the cat, and this problem bears further investigation. CLINICAL SYNDROMES

In view of the multifactorial nature of gingival disease, diagnosis and treatment of any condition predisposing a cat to oral inflammation should be attempted. Once oral inflammation is established, however, most cases of feline gingivitis-stomatitis require treatment for dental disease regardless of underlying cause. 46 In the practice setting, for treatment purposes it is useful to separate feline gingivitis-stomatitis into clinical syndromes based on the age of onset and clinical course. Certain lines of pure-bred cats, especially Abbysinians and Persians, are predisposed to an early-onset hyperplastic gingivitis. 105 Several causes of gingival hyperplasia have been studied; nevertheless, there is a distinct syndrome in which young individuals are afflicted with a hyperemic proliferative gingivitis. 12· 29 • 105 Frequently these individuals are initially affected just before or at the time of adult teeth eruption. A thin film of plaque may be discernible, but there is an absence of obvious calculus. The gingival hyperplasia may progress, so proliferative gum tissue completely covers the crowns of the premolars and molars before the age of 1 year (Fig. 11). There may be resorptive lesions of the teeth concealed by the gingiva but tactilely or radiographically detectable. This condition of early-onset proliferative gingivitis is designated in our hospital as

feline juvenile hyperplastic gingivitis.

Figure 11. The hyperplastic gingiva is not attached to the crown and can be retracted to examine for resorptive lesions and to perform gingivectomy.

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Figure 12. There is a saucer-shaped bone defect and a wide periodontal space around the distal root of the molar, consistent with periodontitis. Note the relatively short roots of the molar.

We term another clinical syndrome occurring in cats before 9 months of age feline juvenile-onset gingivitis-periodontitis. There appears to be a predilection for Siamese, Maine Coon, and the domestic short-hair cats. Many of these individuals are of small stature and have a history of being "sickly" as kittens, often with chronic upper respiratory disease. Initial oral signs occur just before or at the time of eruption of adult teeth. Retention of deciduous teeth if present produces crowding and enhances plaque accumulation. The small gingival pocket that is normally found around the adult teeth as they erupt through the gingiva may form an early reservoir for plaque bacteria in these susceptible individuals.15• 61 Abundant accumulations of plaque and calculus develop rapidly. Gingival recession, pocketing, bone loss, and furcation exposures are common. Gingival swelling is usually due to edema and inflammation rather than hyperplasia. Lesions may be localized or generalized and often are first seen in the central lower incisor area (Color Plate 2, Fig. 6). Radiographically root length may appear shorter than normal (Fig. 12). Root length may be shortened owing to apical root resorption associated with apical periodontitis. If the root length is blunted developmentally, there is reduced root surface area available for periodontal support. A slight attachment loss would then have more clinical significance for the congenitally shorter root than for a root of normal length. Obviously increased mobility and exfoliation can occur more quickly when the roots are shorter than usual. 14 In addition, there may be radiographic evidence of periodontitis and horizontal and vertical bone loss (Fig. 13). Resorptive lesions of the teeth neck and roots often develop. Adult-onset periodontal disease is usually seen as the consequence of years of plaque accumulation without the benefit of oral hygiene treatments or any home care other than self-cleaning from chewing activities (Fig. 14). These cases are u sually the easiest to control because the host response is of a more typical and predictable nature, characterized by chronic inflammation with periods of quiescence and exacerbation. When the plaque and calculus are removed, these p atients will respond with remission of signs, although gross anatomic changes such as gingival recession, pocketing, bone loss, and furcation

Figure 13. Bone loss and resorptive lesions are present on all three teeth, with radiographic evidence of apical periodontitis of the molar roots and the mesial ·oot of the fourth premolar. The apex of the distal ."'lolar root is undergoing resorption.

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Figure 14. A and 8, Chronic periodontal disease. Gingivitis and recession is associated with calculus and plaque accumulations in this adult cat.

exposure may predispose them to more rapid return of signs because of enhanced plaque accumulation (Figs . 15 and 16). Gingivostomatitis in adult cats appears to be the culmination of chronic immune-mediated processes resulting from immune suppression or hyperresponsiveness to a chronic antigenic stimulus or both. Unlike the juvenile form and contrary to some reports, in our practice, the adult form has no breed predilection.53 The underlying condition may have been present before adulthood but because of neglect or lack of awareness is ignored or not detected until clinical signs are advanced in the adult. These cats may appear suddenly painful to the owner, who interprets this as an acute condition. The chronicity is evident, however, because of the presence of exuberant granulation tissue and missing teeth (see Color Plate 1, Figure 3) . Commonly there are excessive accumulations of plaque and calculus and radiographic lesions of external root resorption and retained root tips (see Figs. 7-10, 13, 18). The laboratory values in these cats can vary, as one would expect because they are a heterogeneous group. Some cats have hemograms revealing a chronic or cyclic leukopenia or have serum globulins in the low to normal range in spite of plaque accumulations, exudation, and dramatic gingival and oral mucosal inflammation. Other cats have a more extensive and greater degree of inflammation involving gingiva, oral mucosa, and the pharynx and have high serum proteins owing to polyclonal hypergammaglobulinemia. Gingival biopsy reveals a similar lymphocytic and plasmocytic infiltrate in both cases, making differentiation difficult. Some exhibit positive immunofluorescence on gingival biopsy despite the absence of dermatologic signs.

TREATMENT REGIMENS

The basic treatment for all forms of feline gingivitis-stomatitis is to control plaque bacteria through a dental prophylaxis followed by home care for the maintenance of oral hygiene .• An adequately equipped dental operatory is of paramount importance in the proper delivery of the various required treatments. The complete dental prophylaxis should be performed under general anesthesia and include crown scaling, subgingival scaling, root planing, gingival curettage, polishing, sulcular irrigation, and fluoride treatment. Home care goals are aimed at plaque reduction through mechanical and chemical means. If possible, brushing, swabbing, or wiping the eat's teeth with a veterinary oral hygiene product daily or every other day may effectively reduce plaque. 116 The main obstacle to effective home care is compliance. Our experience is that

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Figure 15. A and 8, A 5-mL pocket has formed around this premolar despite excellent home care. C, Radiograph shows a combined endo-periodontallesion of the fourth premolar. Note the furcation bone loss of the third premolar.

training a cat to accept the brief restraint required for home care often requires months of patience and perseverance on the part of the owner, even when training is begun with a kitten who has no painful oral condition. If home care is attempted, choose products that have an acceptable taste. Products that we have found helpful are chlorhexidine gel (CHX gel, Veterinary Prescription), CET enzymatic paste (Veterinary Prescription), and unflavored stannous fluoride gels (OmniGel, Dunhall; GelKam, Scherer; SF04, Veterinary Prescription). All of these products exhibit antiplaque properties and help reduce gingivitis.• Although the effect of fluoride on gingivitis has been equivical, the rationale for its use in feline dental disease is based on research indicating that in the presence of fluoride, root sensitivity is diminished, remineralization of demineralized enamel is favored, and osteoclast activity is inhibited. 4• 16• 25• 80• 94• 96• 104• m , 137• 144• 145 Thus fluoride applications may have benefits for those cases exhibiting external root resorption. Because fluoride has potential toxic effects both acute and chronic, its use should be monitored to avoid overdosage. 19• 79• 100• 153 The cat appears to be one of the least susceptible to fluoride toxicity of those species studied, and plasma clearance by the kidneys is rapid. 154• 155 Therefore fluoride should probably be avoided in those individuals with renal disease in which fluoride clearance may be impaired. Likewise, using an anesthetic such as

Figure 16. Generalized horizontal bone loss, leaving very little bone support for these teeth.

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methoxyflurane that produces fluoride metabolites may potentiate fluoride toxicity during the fluoride treatment of prophylaxis. 155 Whatever product is used by the owner should be used in very scant amounts (pea-sized or less), comparable to a similar dose for a small child who does not expectorate and ultimately ingests much of the product applied. 79' wo, 153 Antibiotics are a useful adjunct to treatment but should not be used as a replacement for those procedures designed to improve oral hygiene. 133 Antibiotics that have been suggested as effective against periodontal pathogens are amoxicillin, metronidazole, tetracycline, and clindamycin. 9 ' 53' 87 Supportive care also includes maintaining an adequate level of nutrition with supplementation as indicated to correct imbalances that may have an immunomodulating effect. 24' 32 ' 98 , 138 Underlying predisposing conditions should be diagnosed by appropriate laboratory tests. 46 Baseline data should include complete blood count, chemistry panel, and FeLV and FIV testing. We do not routinely recommend feline infectious peritonitis (FIP) testing because we have often found results to be erroneous. Serial blood counts may be indicated to document cyclic hematopoiesis. Radiographic studies to monitor bone loss and root resorption should be performed at the time of dental prophylaxis. External root resorption that is very shallow can be planed, polished, and sealed with a fluoride varnish (Copal with fluoride Cavity Varnish, Schein). 84 Restoration of deeper resorptive lesions using a glass ionomer may be an option for select cases. 31 ' 40' 86' 151 Deep lesions involving the pulp should be treated endodontically using calcium hydroxide as an obturating material before the glass ionomer restorative is placed. 31 ' 33' m, 120 Owing to the small nature of feline root canals, this particular technique is probably limited to the canine teeth in most cases. If the root structure is severely compromised, extraction is indicated. Additional testing such as gingival biopsy for histopathology or immunofluorescence may be warranted. The overall treatment plan and follow-up will vary according to the prevailing syndrome. In feline juvenile hyperplastic gingivitis, it is necessary to perform gingivectomy to eliminate the pseudopockets formed as the result of gingival hyperplasia. 31 ' 44' 45 Practitioners are often reluctant to do prophylaxis on these patients because they are so young and usually have no visible calculus. Nevertheless, thorough plaque removal and the reestablishment of normal sulcus depth (0 to 1 mm) is important and must be followed by diligent plaque control through aggressive home care and professional prophylaxis as frequently as every 2 to 3 months. By providing diligent care during the first 1 to 2 years of life, permanent anatomic changes are avoided. As these individuals mature, many often revert to a more normal status, requiring less and less frequent treatments. Patients with juvenile-onset gingivitis-periodontitis, adultonset periodontal disease, and gingivostomatitis should have a thorough dental prophylaxis every 4 to 9 months and be maintained via a program of aggressive home care. Anatomically compromised teeth should be extracted when home care and professionally provided dental prophylaxis can no longer maintain a quiescent state. Extraction technique may differ according to radiographic findings. Sclerotic bone has poor vascularity, and if in addition there is ankylosis of the root to the sclerotic bone, poor healing is very possible with sequela such as sequestra formation and persistent alveolar and root fragments. 127 To prevent postextraction alveolar osteitis owing to infection and formation of devitalized bone and tooth fragments, a few recommendations can be made. Traumatic extraction technique should be avoided. Root atomization with a small round bur may be preferable to elevation with a dental elevator, which may fracture the alveolus or tooth. Reduce preoperative and postoperative bacterial contamination of the alveolar socket. Introducing debris into the

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Figure 17. Healed extraction site of the lower molar. There is smooth cortical bone at the former alveolar crest, and the alveolar socket has been remodeled to blend with the surrounding trabecular bone.

alveolar socket during extraction should be avoided by first removing calculus from the tooth to be removed. After removal of a tooth or root, any possible residual fragments or material may be removed with a small excavator (#17, Milltex) and with copious flushing using saline or chlorhexidine (Nolvadent, Fort Dodge). Gingiva should be sutured using 4-0 chromic surgical gut to prevent exposure of denuded bone. "· 122• 139 Complete healing will take several weeks, but if there is persistent inflammation at the operative site, radiographs should be retaken to rule out alveolar fragments, sequestra, retained roots, and chronic osteomyelitis93 · 122 (Figs. 17 and 18). For those cases in which continuing treatment is not feasible or effective, the only hope for successful control is by the extraction of all the teeth caudal to the canines. If signs persist, the canines and incisors should also be extracted. Nonhealing extraction or operative sites

Figure 18. Examples of poorly healed extraction sites found in cats exhibiting gingivostomatitis. A, The contour of the former alveolar crest is rough and irregular. There are sequestra, alveolar fragments, sclerotic plaques, a retained root fragment, and periosteal new bone formation. 8, Sclerotic plaques present at the preexisting molar site. C, Generalized sclerosis of the trabecular bone. The alveolus of the fourth lower premolar has not remodeled ; thus, there is a defect in the contour of the cortical bone at the alveolar crest. Remnants of root apex structures are present in the alveoli. 0, Multiple retained root fragments present in the maxilla. Lysis is present around the mesial root of the no longer present third premolar.

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Figure 19. Some remodeling of the alveoli has occurred, but there is an irregular contour of the cortical bone. A tooth fragment is present in the alveolus of the fourth lower premolar mesial root. Sclerosis and periosteal new bone formation are present at the site of the no longer present third lower premolar.

need to be reexplored and debrided . In a small percentage of cases, several ' separate procedures are required before remission of signs is accomplished. Retained root tips or bony sequestrae should be retrieved and the underlying bone curetted if the radiographic lesions are associated with gingival inflammation.136· 152 Some of the bony sequestra are quite small and may be difficult to appreciate unless the radiograph is examined with a magnifying glass. The lack of smooth cortical bone at the former alveolar crest with sclerosis of the surrounding trabecular bone or if there has been poor remodeling (continued radiographic visibility of the alveolar socket) suggests that healing has not occurred and that chronic osteitis or osteomyelitis is established 17• 72 • 123 (Fig. 19). The recommended treatment in these cases is surgical exploration and debridement of the bone Y An incision is made over the alveolar crest and the gingiva reflected with a periosteal elevator (ST7, Schein) to expose the bone. Often a large defect or numerous small defects in the cortical bone can be seen and may involve the entire alveolar crest (Fig. 20) . The bone is curetted and debrided back to fresh bleeding bone on either side of the defect, and the defect is carefully debrided using an excavator or a small round bur, followed by generous flushing with saline or chlorhexidine. Care should be exercised whenever using power equipment to debride the mandible owing to the close proximity of the mandibular canal, which houses the mandibular artery, vein, and alveolar nerve. The gingiva should be sutured over the bone and antibiotics administered postoperatively. Histopathology or culture and sensitivity of the bone is of interest but often is not financially feasible for many owners, who at this point have already made a considerable investment in the treatment of a chronic problem. Anti-inflammatory doses of corticosteroids may be indicated anytime there is chronic inflammation, especially if it extends beyond the mucogingival line and concurrent disease has been ruled out. 46 In addition, steroids may be indicated as an adjunct if autoimmunity is a factor. Some cases of FeLVassociated neutropenia have also responded to corticosteroid treatment,l 7• 141 · 156

Figure 20. The gingiva has been reflected from the crestal bone to reveal the unhealed bone defects in the mandible that can be 'present in feline gingivostomatitis.

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although one case of chronic cyclic neutropenia did not respond favorably. 140 The hyperresponsive patients are especially plaque intolerant and in adqition to aggressive professional dental treatment and meticulous horne care need treatment for hypersensitivity. Therefore the concurrent use of coricosteroids is almost always necessary, although they should not be used as a substitute for proper dental treatment. Corticosteroid administration is discontinued once the cat' s lesions are in remission. SUMMARY

Any alteration in the balance of bacterial challenge versus the h~st's ability to resist and repair will result in oral lesions that are similar in appearance. The bacterial cause of gingivitis and periodontitis in humans and in all other animals in which it has been studied is firmly established, and specific species of predominantly gram-negative anaerobes have been implicated. 82 • 90 ; 106• I:l2 Naturally occurring or acquired immunopathologies are likely to result in premature dental disease. 106· 124 When oral disease is associated with the accumulation of plaque, a positive response can be achieved by reducing the bacterial challenge to the host through the maintenance of oral hygiene by timely professional dental prophylaxis and horne care. Disease that is the result of atypical immune responses, however, can be much more difficult to manage. Such oral disease can occur with either immune deficiencies or exaggerated immune responses, and it is likely that multiple mechanisms are active concurrently. In any case, gram-negative anaerobes present in plaque are likely to be a major contributing factor. Therefore patients with chronic refractory gingivitisstomatitis must be considered to be plaque intolerant. Only with a freq'!lent regimen of aggressive and thorough professional dental treatment plus meticulous oral home care on a daily basis can one expect to keei} these cases in remission. Because this is often unrealistic, the only other way to keep these patients free of disease is by total dental extraction. The tissues that are colonized by the causative organisms must be eliminated. All root tips and bony sequestra must be removed and healing with intact epithelium accomplished before these cases will go into remission. Edentulous feline patients that continue to have signs of gingivostomatitis have been found to have an area of nonhealed bony sequestrum and chronic osteomyelitis. Once effective debridement has been accomplished and epithelial healing completed, nonresponsive cases can be expected to go into remission (Color Plate 2, Figure 7). It is hoped that as more is learned about this frustrating problem, the many factors influencing feline oral disease will be scientifically documented. In the future, actual diagnoses can be systematically made early on in disease, and treatment will be more than just symptomatic.

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33. Foreman PC, Barnes IE: A review of calcium hydroxide. Int Endo J23:283-297, 1990 34. Forsyth K, Reed RE: Feline immunodeficiency virus and cancer. J Am Assoc Feline Pract 1(2):5-9, 1989 35. Friend SCE, Birch CJ, Lording PM, et al: Feline immunodeficiency virus: Prevalence, disease associations and isolation. Aust Vet J67(6):237-243, 1990 36. Frost P, Williams CA: Feline dental disease. Vet Clin North Am Small Anim Pract 16(5):851-873, 1986 37. Gabbert NH: Cyclic neutropenia in a feline leukemia-positive cat: A case.report. J Am Anim Hosp Assoc 20:343-347, 1984 38. Genco RJ, Mashimo PA, Krygier G, et al: Antibody-mediated effects on the periodontium. J Periodontal 45(5):330-337, 1974 39. Gibbons RJ: Bacterial adhesion to oral tissues: A model for infectious diseases. J Dent Res 68(5):750-760, 1989 40. Golden AL: Restoration of cat neck lesions using glass ionomer. Proceedings Veterinary Dentistry 1989, AVO, AVDC, New Orleans, 1989, p 39 41. Goldstein GS, King G, Venner M: Radiation as adjunct therapy in treating plasmacytic lymphocytic stomatitis in cats. Second World Veterinary Dental Congress, Vienna, 1991 42. Greenspan D: Oral viral leukplakia: A new oral lesion in association with AIDS. Compend Contin Educ Dent 6(8):484, 1990 43. Grime PD, Bowerman TE, Weller PT, et al: Gentamicin impregnated polymethylmethacrylate beads in the treatment of primary chronic osteomyelitis of the mandible. Br J Oral Maxillofac Surg 28:367-374, 1990 44. Grove TK: Problems associated with the management of periodontal disease in clinic practice. Probl Vet Med Dent 2(1):124, 1990 45. Grove K: Peridontal therapy. Compend Contin Educ Vet Med 5(8):660-665, 1983 46. Gruffydd-Jones TJ: Gingivitis and stomatitis. In August JR (ed): Consultations in Feline Internal Medicine. Philadelphia, WB Saunders, 1991, pp 397-402 47. Guilford GW: Primary Immunodeficiency Diseases of Dogs and Cats. Friskies Research Digest (Carnation Company, Pico Rivera, CA) 24(1):1-5, 1988 48. Harbour DA, Howard PE, Gaskell RM: Isolation of feline calicivirus and feline herpesvirus from domestic cats 1980 to 1989. Vet Rec 128:77-80, 1991 49. Hardy WD: Feline T-lymphotropic lentivirus: Retrovirus-induced immunosuppression in cats. JAm Anim Hosp Assoc 24:241-243, 1988 50. Haring JI: Oral manifestations of HIV infection. Part 1. Compend Contin Educ Dent 6(3):150-154, 1990 51. Haring JI: Oral manifestations of HIV infection. Part 2. Oral infections and neoplastic lesions. Compend Contin Educ Dent 6(4):236-243, 1990 52. Hartman AB, Mallett CP, Srinivasappa J, et al: Organ reactive autoantibodies from non-immunized adult BALB/c mice are polyreactive and express non-biased VH gene usage. Molec Immunol 26(4):359-370, 1989 53. Harvey CE: Oral inflammatory diseases in cats. J Am Anim Hosp Assoc 27(6):585591, 1991 54. Harvey CE: Feline gingivitis-stomatitis. Abstract from Proceedings of the Academy of Veterinary Dentistry Annual Meeting, New Orleans, 1988 55. Harvey CE, O'Brian ET: Oral, dental, pharyngeal, and salivary gland disorders. In Ettinger SJ (ed): Textbook of Veterinary Medicine. Philadelphia, WB Saunders, 1983, pp 1152-1163 56. Harvey CE: Oral, dental, pharyngeal, and salivary gland disorders. In Ettinger SJ (ed): Textbook of Veterinary Internal Medicine. Philadelphia, WB Saunders, 1989, pp 1226-1229 57. Harvey CE: Oral and dental disease of the cat. Proceedings from American Association of Feline Practitioners, Boston, 1988 58. Harvey CE, Shofer F, Venner M, et al: Results following conservative treatment of gingivitis/stomatitis in cats. Philadelphia, University of Pennsylvania, 1988 59. Harvey CE, Shofer F, Venner M: Clinical features and periodontal indices in cats with chronic gingivitis-stomatitis. Philadelphia, University of Pennsylvania, 1989 60. Hausmann E: Potential pathways for bone resorption in human periodontal disease. J Periodontal 45(5, part II):338-343, 1974

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stomatitis in cats.

Any alteration in the balance of bacterial challenge versus the host's ability to resist and repair will result in oral lesions that are similar in ap...
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