Periodontitis as an early presentation - Europe PMC

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May 15, 1991 - Outcome measures: Diagnosis of HIV infection: identification of ... the contention that RPP is one of the first signs of HIV infection or AIDS.


Periodontitis as an early presentation of HIV infection Howard C. Tenenbaum,*t§ DDS, PhD; David Mock,*t DDS, PhD, FRCDC; Andrew E. Simor4 MD, FRCPC Objective: To determine whether the presence of rapidly progressive periodontitis (RPP) in people at high risk for acquired immunodeficiency syndrome (AIDS) may be the first symptom of previously unrecognized human immunodeficiency virus (HIV) infection. Design: Case series. Setting: Dental clinic. Patients: Twenty patients who presented or were referred to the dental clinic over 6 months for the treatment of unexplained RPP and were at high risk for AIDS. Outcome measures: Diagnosis of HIV infection: identification of candidal organisms in cytologic smears, determination of complete and differential blood counts and of ratio between T4 (helper) and T8 (suppressor) lymphocytes, and performance of HIV antibody assays. Main results: All of the patients were men, although sex was not an inclusion criterion. Sixteen (80%) of the 20 patients were found to have HIV infection. Four had been aware that they were HIV positive: two admitted it only when their T4:T8 ratio was known and. the other two when the T4:T8 test was explained or requested. Fifteen of the patients were homosexual, three came from AIDS-endemic areas, and two had hemophilia. The RPP was responsible for alveolar bone loss in all of the patients. One patient lost bone in one site because of localized osteomyelitis. Only five patients had concurrent candidal overgrowth, and three had Kaposi's sarcoma. The mean T4:T8 ratio was 0.57 (standard deviation 0.52). Conclusions: These findings suggest that periodontal disease may be one of the first clinical presentations of previously undiagnosed HIV infection. Thus, patients at high risk for AIDS who present with aggressive periodontal disease should be investigated for possible HIV infection. However, further, prospective studies are required to confirm the contention that RPP is one of the first signs of HIV infection or AIDS.

Objectif: Determiner si la presence d'une desmodontite a evolution rapide (DER) chez les sujets qui presentent des risques eleves de syndrome immunodeficitaire acquis (SIDA) peut constituer le premier sympt6me d'une infection par virus immunodeficitaire humain (VIH) non decel&e auparavant. Conception: Serie de cas. Contexte: Clinique dentaire. Patients: Vingt patients qui se sont presentes ou ont ete envoyes a la clinique dentaire en 6 mois pour traitement d'une DER inexpliquee et qui presentaient un risque eleve de SIDA. From the departments of *Dentistry, tPathology, $Microbiology and $Internal Medicine and §the Samuel Lunenfeld Research Institute, Mount Sinai Hospital and University of Toronto, Toronto, Ont.

Reprint requests to: Dr. Howard C. Tenenbaum, Samuel Lunenfeld Research Institute, Rm. 984, Mount Sinai Hospital, 600 University Ave., Toronto, ONM5G IX5 MAY 15, 1991

CAN MED ASSOC J 1991; 144 (10)


Mesures des resultats: Diagnostic d'infection par VIH: depistage de la presence de Candida dans des frottis cytologiques, etablissement de la numeration globulaire et de la formule leucocytaire, et d'un ratio entre les lymphocytes T4 (amplificateur) et T8 (suppresseur), et execution d'essais aux anticorps du VIH. Principaux resultats: Tous les patients etaient des hommes, meme si le sexe n'etait pas un critere d'inclusion. Seize (80 %) des 20 patients etaient atteints d'infection a VIH. Quatre savaient qu'ils etaient seropositifs: deux ne l'ont admis qu'apres qu'on euit connu le ratio T4:T8 et les deux autres apres qu'on leur euit explique ou prescrit le test T4:T8. Quinze des patients etaient homosexuels, trois provenaient de zones endemiques a SIDA et deux etaient hemophiles. La DER etait a l'origine de deperdition d'os alveolaire chez tous les patients. Un patient a perdu du tissu osseux a un endroit a cause d'une osteomyelite localisee. Cinq patients seulement presentaient une proliferation de Candida simultanee et trois souffraient du sarcome de Kaposi. Le ratio T4:T8 moyen etait de 0,57 (ecart type de 0,52). Conclusions: Ces constatations laissent entendre que la maladie desmodontale peut etre une des premieres manifestations cliniques d'une infection a VIH non diagnostiquee auparavant. C'est pourquoi il faudrait soumettre a des tests de depistage d'infection a VIH les patients a risque eleve de SIDA et qui souffrent de desmodontite agressive. I1 faut toutefois proceder a des etudes prospectives pour confirmer l'hypothese selon laquelle la DER constitue une des premieres manifestations d'infection a VIH ou de SIDA.

M any systemic diseases and disorders (e.g., diabetes mellitus and blood dyscrasia) can have oral signs and symptoms.' Moreover, many of these manifestations present mainly as aggressive gingivitis or periodontitis unresponsive to conventional therapy; often minimal local etiologic factors such as dental debris, calculus and plaque can be found.2-6 There are many established oral manifestations of human immunodeficiency virus (HIV) infection and acquired immunodeficiency syndrome (AIDS), such as candidiasis, Kaposi's sarcoma, white hairy leukoplakia and periodontal disease.2 Although it is generally assumed that the first oral signs of HIV infection are candidiasis or white hairy leukoplakia, gingival and periodontal changes may be earlier manifestations.2 Both the physician and the dentist must be well aware of the characteristics and presentation of such manifestations of HIV infection. However, it is not known whether the presence of HIV-related periodontitis is the first sign that HIV infection is progressing to AIDS. We assembled this case series to demonstrate a link between rapidly progressive periodontitis (RPP) and previously unrecognized HIV infection in patients who are at high risk for HIV infection.

Methods Patient selection We selected the charts of 20 patients who had presented or had been referred to the dental clinic over 6 months because of RPP. The patients were asked if they were a member of a group at high risk for AIDS if clinical findings and a history of RPP warranted it. The specific risk groups were (a) male 1266

CAN MED ASSOC J 1991; 144 (10)

homosexual, (b) previous inhabitant of an AIDSendemic area, (c) patient with hemophilia and (d) intravenous drug abuser. None of the patients had been investigated for other nondental problems associated with HIV infection.

Patient management After the history was obtained routine oral examination, including simple visual inspection, was performed. A periodontal probe was used to assess any loss of attachment between the gingival tissue and the teeth and to measure gingival recession. Recession of 5 mm or more was considered to be a significant loss of gingival tissue. Features such as pain or bleeding on probing were recorded. The level of oral cleanliness was estimated visually. Lymphadenopathy was assessed by means of palpation. Panoramic or intraoral radiographs were obtained to determine whether bone loss had occurred around affected teeth.

Diagnostic tests If a patient did not admit to having HIV infection and if HIV infection or AIDS was suspected on the basis of the history and clinical findings, a series of diagnostic tests was performed. Since the proliferation of candidal organisms has been clearly associated with the development of immunodeficiency7,8 superficial exfoliative samples were obtained from the mouth to detect these organisms regardless of whether clinical signs of candidiasis were present. One sample was taken from the dorsal surface of the tongue with a sterile stainless-steel spatula and the other from the perioLE 15 MAI 1991

dontal sites with a stainless-steel periodontal probe. The two samples were smeared on glass slides and fixed in 100% ethanol in preparation for routine Papanicolaou staining and examination. Culture was not done, since positive results would probably be obtained in many otherwise healthy patients.9 If Kaposi's sarcoma was suspected routine methods for excisional or incisional biopsy were followed. Since other systemic diseases can produce changes in the periodontium complete and differential blood counts were done in addition to routine blood tests for such elements as glucose, calcium, phosphate and alkaline phosphatase. Finally, one of the most useful indicators of immunodeficiency, the ratio between T4 (helper) and T8 (suppressor) lymphocytes, was calculated. Although a normal ratio does not preclude HIV infection one that is below normal in a patient with other signs or symptoms suggestive of AIDS points very strongly to HIV infection.2,5 HIV antibody titres were determined by means of enzyme-linked immunosorbent assay (ELISA) and confirmed by means of the Western blot technique. All of the patients were counselled and gave informed consent before the HIV testing.

Results Patient characteristics All of the 20 patients were men, although sex was not used as an inclusion criterion. Fifteen of the patients were homosexual, three were originally from endemic areas, and two had hemophilia. The ages were from 26 to 52 years; the mean age was 39 (standard deviation [SD] 5.7) years. All of the patients presented because of pain in the gingival

and associated tissues or obvious tissue loss around the teeth (Fig. 1). Eighteen of the patients reported having bleeding gums. In all cases the patient or his dentist reported rapid development of the gingival problem within 6 months; this was confirmed on examination by a loss of 5 mm or more of gingival attachment. In all, 16 (80%) of the patients were found to be positive for HIV antibody. Four (20%) of the patients had been aware of their HIV seropositivity before the testing (Table 1). Two admitted it only when the T4:T8 ratios were presented to them and the other two when the T4:T8 test was explained or requested. None of the four suspected that the periodontitis was related to the HIV infection. The periodontal disease was often disproportionate to the amount of dental debris or bacterial plaque (Fig. 1); in fact, the oral hygiene was generally quite good, with minimal deposits of bacterial plaque, calculus and debris. There was often marked erythema and edema of the gingival tissue. Obvious tissue loss (5 mm or more), leaving exposed root surfaces, was observed and was usually localized (Fig. 1). More acute conditions were characterized by significant and painful tissue necrosis presenting as white plaques on inflamed and ulcerated gingival tissue. In some cases localized and painless tissue destruction was seen without obvious inflammation. Occasionally the extent of disease was less obvious and could only be detected through specific examination with a periodontal probe (Fig. 2). In those cases significant dental-alveolar bone loss was evident on radiographs (Table 1, Fig. 3), but the loss of gingival attachment to the roots was masked by overlying gingival tissue that appeared normal on visual inspection. In one patient a single site had worsened over a number of days, and osteomyelitis was diagnosed. Lymphadenopathy was detected in 1 (55%) of the patients. There was marked bleeding after gentle periodontal probing in all of the patients. Our study design did not permit identification of previous possible HIV-associated diagnoses.

Test results

Fig. 1: Locally aggressive periodontal disease characterized by inflammation and marked recession of gingival tissue in man with previously undiagnosed human immunodeficiency virus infection; root surface (*) is relatively clean. Adjacent gingival tissue (arrows) is less inflamed and may appear normal on casual inspection. MAY 15, 1991

The results of the diagnostic testing are shown in Table 1. Candidal organisms were detected in only five (25%) of the patients, none of whom had overt clinical signs of candidiasis. Previously unrecognized Kaposi's sarcoma was identified in three (15%) of the patients; the incidence was higher among those who knew their HIV antibody status. The biochemical tests did not reveal any anomalous results. However, six (30%) of the patients had a leukocyte count below normal. The T4:T8 ratio varied from 0.04 to 2.0 (normally > 0.8); the mean ratio was 0.57 (SD 0.52). CAN MED ASSOC J 1991; 144 (10)



titis in a person who otherwise appears well should prompt investigation into lifestyle and other factors pertaining to the risk of HIV infection. Our findings do not suggest that periodontitis is one of the first signs of HIV infection. Certainly HIV-associated periodontal disease and its management have been described elsewhere.2-6 However, it is often considered as a later complication preceded by, but not necessarily related to, the more common oral symptoms of HIV infection: oral candidiasis and white hairy leukoplakia. In our group of patients the periodontal disease was often the first oral sign and was frequently independent of other oral symp-

This case series illustrates that the development of RPP in a person at risk for HIV infection may be an ominous event. Most of the patients were apparently completely unaware of their immunologic status. Indeed, it was the presence of aggressive periodontitis that triggered further investigation, which led to a diagnosis of HIV infection in 80% of the patients. This highlights an important psychosocial problem: a person, even one at high risk for AIDS, who presents for treatment of periodontitis is unlikely to be emotionally prepared to hear that he or she has signs or symptoms of HIV infection. Certainly this has an impact on dentists, who are not as prepared as physicians to discuss such potentially devastating health problems with patients. Furthermore, there are people who are apparently aware of their HIV antibody status but for various reasons do not inform dental caregivers of it. This could have implications for the design of effective treatment of their periodontal condition. Therefore, although this subgroup did not represent most of the cases in our series it is important to recognize that it exists and that reliance on history alone may not identify patients at risk for HIV infection. The cases presented here should alert medical and dental practitioners to the possibility of aggres- Fig. 2: Deep penetration (50% of periodontal probe) into sive periodontitis in patients at risk for AIDS. pocket. Area may not be recognized with simple visual Similarly, the development of unexplained periodon- inspection. Table 1: Clinical and diagnostic features of patients with apidly progressive periodontitis who were at high risk tfcacquired immunodeficiency syndrome



Age, yr




2 3

46 38 35 35 45 36 38




5 6 7

8 9 13

45 37 32 29 38

14 15 16 17 18 19 20

39 43 52 26 40 37 39

10 11


m M M M M M M M m M M M M m m m m

Bone loss

Kaposi's sarcoma

TY4:T8 ralbo 0. 43 0.21 0.27 0.40 0.14


NDt +


-t =

Previously unknow, HIV infection*



0.33 0.42


0.37 0.10 ND§ 0.52 0.04 0.58 0.12 1.00

1.90 2.00 1.14


White hairy leukoplakia

0.46 0.50

'HIV -- human immunodeficiency virus; NA

±ND - not determined.





not applicable.

-Bone loss was due to osteomyelitis at one site. §Not determined because patient admitted to having HIV infectior


CAN MED ASSOC J 1991; 144 (10)

LE 15 MAI 1991

people at high risk for AIDS could be very important in recognizing HIV infection early. Moreover, since most of the patients described here appeared to have significant immunodeficiency, as demonstrated by the mean T4:T8 ratio, the prognostic value of periodontitis with respect to the development of AIDS in previously unidentified or known HIV carriers remains to be seen. We thank Dr. A. Ross Kerr, Department of Dentistry, Mount Sinai Hospital, for assisting with the preparation of the manuscript.

References 1. Rose LF, Kaye D (eds): Internal Medicine for Dentistry, 2nd ed, Mosby, Toronto, 1990: 1153 2. Robertson PB, Greenspan JS: Oral Manifestations of AIDS: Diagnosis and Management of HIV-Associated Infections, PSG Pub, Littleton, Mass, 1988: 49-70 3. Pindborg JJ: Classification of oral lesions associated with HIV infection. Oral Surg Oral Med Oral Pathol 1989; 67: 292-295 4. Murray PA: Management of HIV-associated periodontal diseases. Dent Teamwork 1989; 2: 96-99 5. Greenspan D, Greenspan JS: The oral clinical features of HIV infection. Gastroenterol Clin North Am 1988; 17: 535-543 6. Rosenstein DI, Eigner TL, Levin MP et al: Rapidly progressive periodontal disease associated with HIV infection: report of case. JAm Dent Assoc 1989; 118: 313-314 7. Klein RS, Harris CA, Small CB et al: Oral candidiasis in high-risk patients as the initial manifestation of the acquired immunodeficiency syndrome. N Engl J Med 1984; 311: 354358 8. Chandrasekar PH, Molinari JA: Oral candidiasis: forerunner of acquired immunodeficiency syndrome. Oral Surg Oral Med Oral Pathol 1985; 60: 532-534 9. Jawetz E, Melnick JL, Adelberg EA: Review of Medical Microbiology, 16th ed, Lange, Los Altos, Calif, 1984: 265-266

Fig. 3: Panoramic radiograph, showing bone loss associated with lesions shown in Figs. 1 (*) and 2 (+). Normal bone structure is visible elsewhere (arrows).

toms of HIV infection. Even when the other symptoms were present the gingival disease was the most obvious and, in fact, prompted the visit or referral to the dental clinic. Nevertheless, it cannot be confirmed from our findings whether RPP is indeed one of the first signs (oral or otherwise) of HIV infection, even though this has been suggested by others.2 Our observations do provide a basis for prospective controlled studies. Information regarding the positive predictive value of the diagnosis of RPP in

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