CLINICAL AND COMMUNITY STUDIES

ETUDES CLINIQUES ET COMMUNAUTAIRES

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 immunodefici-
taire 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) 1265
 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 mani-
festations 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 leuko-
plakia, 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 infec-
tion. 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 pa-
tients 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 AIDS-
endemic 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. Lym-
phadenopathy 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 suspect-
ed 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 perio-
LE 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 differen-
tial 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 im-
munosorbent 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
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
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 pa-
tients 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 dispropor-
tionate 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 exami-
nation with a periodontal probe (Fig. 2). In those
cases significant dental-alveolar bone loss was evi-
dent 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
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 unrec-
ognized 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 anoma-
lous 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) 1267
Discussion titis in a person who otherwise appears well should
prompt investigation into lifestyle and other factors
This case series illustrates that the development pertaining to the risk of HIV infection.
of RPP in a person at risk for HIV infection may be Our findings do not suggest that periodontitis is
an ominous event. Most of the patients were appar- one of the first signs of HIV infection. Certainly
ently completely unaware of their immunologic sta- HIV-associated periodontal disease and its manage-
tus. Indeed, it was the presence of aggressive perio- ment have been described elsewhere.2-6 However, it
dontitis that triggered further investigation, which is often considered as a later complication preceded
led to a diagnosis of HIV infection in 80% of the by, but not necessarily related to, the more common
patients. This highlights an important psychosocial oral symptoms of HIV infection: oral candidiasis
problem: a person, even one at high risk for AIDS, and white hairy leukoplakia. In our group of patients
who presents for treatment of periodontitis is unlike- the periodontal disease was often the first oral sign
ly to be emotionally prepared to hear that he or she and was frequently independent of other oral symp-
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. Further-
more, 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 tfc-
acquired immunodeficiency syndrome
Case Age, Candida Kaposi's TY4:T8 White hairy Previously unknow,
no. yr Sex Bone loss infection sarcoma ralbo leukoplakia HIV infection*
1 44 M 0. 43
2 46 M 0.21
3 38 M 0.27 1-
4 35 m 0.40
5 35 M 0.14
6 45 M 0.46 4-I
7
36 M 0.33
8 38 M 0.42 .+.t
9 45 M 0.50
10 37 M .T- 0.37 .4.
11 32 M NDt 0.10
12 29 m + ND§
13 38 M 0.52
14 39 M -t 0.04
15 43 M 0.58
16 52 M 0.12 NA
17 26 m 1.00 NA
18 40 m A- 1.90 NA
19 37 m 2.00 NA
20 39 m -t 1.14 NA
'HIV -- human immunodeficiency virus; NA = not applicable.
±ND - not determined.
-Bone loss was due to osteomyelitis at one site.
§Not determined because patient admitted to having HIV infectior

1268 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
Fig. 3: Panoramic radiograph, showing bone loss associated infection. Oral Surg Oral Med Oral Pathol 1989; 67: 292-295
with lesions shown in Figs. 1 (*) and 2 (+). Normal bone 4. Murray PA: Management of HIV-associated periodontal dis-
structure is visible elsewhere (arrows). eases. 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
toms of HIV infection. Even when the other symp- 6. Rosenstein DI, Eigner TL, Levin MP et al: Rapidly progressive
toms were present the gingival disease was the most periodontal disease associated with HIV infection: report of
obvious and, in fact, prompted the visit or referral to case. JAm Dent Assoc 1989; 118: 313-314
7. Klein RS, Harris CA, Small CB et al: Oral candidiasis in
the dental clinic. Nevertheless, it cannot be con- high-risk patients as the initial manifestation of the acquired
firmed from our findings whether RPP is indeed one immunodeficiency syndrome. N Engl J Med 1984; 311: 354-
of the first signs (oral or otherwise) of HIV infection, 358
even though this has been suggested by others.2 8. Chandrasekar PH, Molinari JA: Oral candidiasis: forerunner of
Our observations do provide a basis for prospec- acquired immunodeficiency syndrome. Oral Surg Oral Med
Oral Pathol 1985; 60: 532-534
tive controlled studies. Information regarding the 9. Jawetz E, Melnick JL, Adelberg EA: Review of Medical
positive predictive value of the diagnosis of RPP in Microbiology, 16th ed, Lange, Los Altos, Calif, 1984: 265-266

Canada's Fitweek, May 24 to June 2,

is the largest annual celebration of physical
activity in the world. Join the action and
| g g make physical activity regular of

| |{ > | ~~~~~~~your life.

with friends and
Participate on your own, or
family. Make your move toward active living.
It is fun and easy. Simply add a walk to your
C;
[ _ ^ _ | daily routine, a softball game to your weekend
plans or go dancing on a Saturday night. Or
choose to join one of over 14,000 Fitweek
events happening across the country.
Celebrate ng
My24-Jun 2 Condition
S e~~~~~~~~~~~~iness -ii
C~mda CAWcda
<_~~~~~~~~~~~~~~~~~~~~~Gvr~ s of C^ Couo~~ du Cmnd
Fk~w ~s AnUff~ Sport CondMon phya a 5~ws
pt

qCanada's Fitwe is a partnership of Fitness Canada, provincial and

teririal gorernosezas. and national nizatiom;
coordinatd by the Canada's Fitvek Seetariat.

MAY 15, 1991 CAN MED ASSOCJ 1991; 144 (10) 1269