Oral

OralDiseases
lesion prevalence
(2002) 8 (Suppl.
and classification
2), 98109
2002 Blackwell Munksgaard All rights reserved
LL Patton
16015665
et al

98 www.blackwellmunksgaard.dk

Prevalence and classification of HIV-associated

oral lesions
LL Patton1, JA Phelan2, FJ Ramos-Gomez3, W Nittayananta4, CH Shiboski5, TL Mbuguye6
1
Department of Dental Ecology, School of Dentistry, University of North Carolina, Chapel Hill, NC, USA; 2Department of Oral
Pathology, New York University College of Dentistry, New York, NY, USA; 3Department of Growth and Development, Division of
Paediatric Dentistry, University of California San Francisco, San Francisco, CA, USA; 4Department of Stomatology, Faculty of
Dentistry, Prince of Songkla University, Haadyai, Songkhla, Thailand; 5Department of Stomatology, School of Dentistry,
University of California, San Francisco, CA, USA; 6Department of Community Health, Medical School, Parktown,
University of the Witwatersrand, South Africa

OBJECTIVES: An International Workshop ad- Introduction

dressed the prevalence and classification of HIV/
As we draw near the close of the second decade of global
AIDS associated oral lesions.
experience with AIDS, we were asked to explore the vari-
DESIGN: Five questions provided the framework
ability in reported prevalence of opportunistic infections
for discussion and literature review. What is the
and neoplasms that arise in the oral cavity in response to
prevalence of oral lesions in children and adults?
HIV infection and its accompanying immune deciency.
Should the accepted classification of HIV-related
Our understanding of the prevalence of oral manifestations
oral lesions be modified in the light of recent find-
of HIV is inuenced by a number of factors, including the
ings? Why is there a gender difference in the preval-
following: early studies were done before HIV testing was
ence of oral lesions in developed and developing
available; some studies used subjects with a diagnosis of
countries? Are there unusual lesions present in de-
AIDS, whereas others used all those who were HIV-
veloping countries? Is there any association between
infected; medical and immunological status has been incon-
modes of transmission and the prevalence of oral
sistent across reports; AIDS denition has changed over
lesions?
time; most early studies were done in Europe and the US;
RESULTS: Workshop discussion emphasized the
most subjects in early studies were homosexual men; in the
urgent need for assistance in the development of
past few years there has been an emergence and increased
expertise to obtain accurate global prevalence data
availability in developed nations of antiretroviral therapy,
for HIV-associated oral lesions. Oral candidiasis has
including more effective viral suppression with protease
been consistently reported as the most prevalent
inhibitors; medications to treat or prevent opportunistic in-
HIV-associated oral lesion in all ages. Penicilliosis
fections have become more widely available; study designs
marneffei, a newly described fungal infection, has
have varied from cross-sectional to longitudinal and may or
emerged in South-east Asia. Oral hairy leukoplakia
may not include HIV-uninfected controls from the popula-
and Kaposis sarcoma appear to be associated with
tion at risk; subject selection criteria have varied from those
male gender and male-to-male HIV transmission
identied in dental clinic populations, medical clinics, and
risk behaviours. These lesions occur only rarely in
other research studies, and have varying distributions of
children.
gender, race, and HIV transmission risks.
CONCLUSIONS: Additional prevalence data are
Despite the differences in methods and the shortcomings
needed from developing countries prior to substan-
of existing studies, the two oral lesions that appear cur-
tially altering the 1993 ECC/WHO Classification of
rently as the most prevalent are oral candidiasis and hairy
oral lesions associated with adult HIV infection. The
leukoplakia. The EC-Clearinghouse on Oral Problems
workshop confirmed current oral disease diagnostic
Related to HIV Infection and WHO Collaborating Centre
criteria.
on Oral Manifestations of the Immunodeciency Virus last
Keywords: HIV; oral mucosa; oral candidiasis; oral hairy revised their consensus classication of the oral manifesta-
leukoplakia; Kaposis sarcoma; epidemiology tions of HIV infection and their presumptive and denitive
diagnostic criteria for oral lesions in September 1992 (EC-
Clearinghouse, 1993). This scheme, most applicable to
patients in Europe and the US, groups lesions into three
categories according to strength of association with HIV
Correspondence: Lauren L. Patton, Department of Dental Ecology, CB
#7450, School of Dentistry, University of North Carolina, Chapel Hill, NC infection (Table 1). In March 1994 and May 1995, the
275997450, USA. Tel.: +1 919 9662792, Fax: +1 919 9666761, E-mail: Collaborative Workgroup on the Oral Manifestations of
Lauren_Patton@dentistry.unc.edu Paediatric HIV Infection met and developed a consensus

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 Oral lesion prevalence and classification
LL Patton et al

99
Table 1 September 1992 Consensus Classication of Oral Lesions Asso- Table 2 Consensus Classication of Orofacial Lesions Associated with
ciated with Adult HIV Infection (EC-Clearinghouse, 1993) Paediatric HIV Infection (Ramos-Gomez et al, 1999)

Group 1: Lesions strongly associated with HIV infection Group 1: Lesions commonly associated with paediatric HIV infection.
Candidiasis Candidiasis
Erythematous Erythematous
Pseudomembraneous Pseudomembraneous
Hairy leukoplakia Angular cheilitis
Kaposis sarcoma Herpes simplex virus infection
Non-Hodgkins lymphoma Linear gingival erythema
Periodontal disease Parotid enlargement
Linear gingival erythema Recurrent aphthous ulcers
Necrotizing (ulcerative) gingivitis Minor
Necrotizing (ulcerative) periodontitis Major
Group 2: Lesions less commonly associated with HIV infection Herpetiform
Bacterial infections Group 2: Lesions less commonly associated with paediatric HIV
Mycobacterium avium-intracellularae infection.
Mycobacterium tuberculosis Bacterial infections of oral tissues
Melanotic hyperpigmentation Periodontal diseases
Necrotizing (ulcerative) stomatitis Necrotizing (ulcerative) gingivitis
Salivary gland disease Necrotizing (ulcerative) periodontitis
Dry mouth due to decreased salivary ow rate Necrotizing (ulcerative) stomatitis
Unilateral or bilateral swelling of major salivary glands Seborrheic dermatitis
Thrombocytopenia purpura Viral infections
Ulceration NOS (not otherwise specied) Cytomegalovirus
Viral infections Human papillomavirus
Herpes simplex virus Molluscum contagiosum
Human papillomavirus (warty-like) lesions Varicella-zoster virus
Condyloma acuminatum Herpes-zoster
Focal epithelial hyperplasia Varicella
Verruca vulgaris Xerostomia
Varicella-zoster virus Group 3: Lesions strongly associated with HIV infection but rare in
Herpes zoster children.
Varicella Neoplasms
Group 3: Lesions seen in HIV infection Kaposis sarcoma and non-Hodgkins lymphoma
Bacterial infections Oral hairy leukoplakia
Actinomyces israelii Tuberculosis-related ulcers
Escherichia coli
Klebsiella pneumonia
Cat-scratch disease
Drug reactions (ulcerative, erythema multiforme, lichenoid, toxic
epidermolysis) and Chungpanich, 1997; Ranganathan et al, 2000) to 0
Epithelioid (bacillary) angiomatosis
Fungal infection other than candidiasis
94% in Africa (Tukutuku et al, 1990; Itula et al, 1997) and
Cryptococcus neoformans 592% in the US (Klein et al, 1991; Melnick et al, 1991;
Geotrichum candidum Lamster et al, 1994; Little et al, 1994), largely depending
Histoplasma capsulatum on the prevalence of AIDS diagnoses or individuals with
Mucoraceae (mucormycosis zygomycosis) low CD4 counts among those studied.
Aspergillus flavus
Neurological disturbances The second most common oral lesion appears to be oral
Facial palsy hairy leukoplakia, with reported prevalence from 0% to
Trigeminal neuralgia 20% in Africa (Mugaruka et al, 1991; Arendorf et al, 1998),
Recurrent aphthous stomatitis 313% in Asia (Nittayananta and Chungpanich 1997;
Viral infections
Cytomegalovirus
Ranganathan et al, 2000), up to 43% in Mexico (Gillispie
Molluscum contagiosum and Marino 1993), and from 7% to 30% in the US and
Europe (Lamster et al, 1994; Palmer et al, 1996; Schmidt-
Westhausen et al, 1997; Schuman et al, 1998), with lower
prevalence among women than men.
classication for oral lesions in children using the frame- Prevalence of the other strongly HIV-associated lesions
work of the EC-Clearinghouse and WHO (Ramos-Gomez varies according to region of the world and cohort examined.
et al, 1999) (Table 2). Prevalence of Kaposis sarcoma (KS) varies from 0% to
12% in Africa (Tukutuku et al, 1990; Arendorf et al, 1997;
1 What is the prevalence of oral lesions Matee et al, 2000) and from 0% to 38% in the US and
Europe (Roberts et al, 1988; Swango et al, 1991; Ficarra
in children and adults? et al, 1994; Little et al, 1994; Schmidt-Westhausen et al,
Among adults, oral candidiasis appears to be the most com- 1997; Schuman et al, 1998; Margiotta et al, 1999), where
monly reported lesion across the world. Table 3 illustrates greater proportions of the study populations tend to be men
prevalence of oral lesions in studies of adults by region of who have sex with men. Of interest, KS has never been
the world. Prevalence of oral candidiasis varies from 56% reported from Asia, where heterosexual sex is the main
to 81% in Asia (Anil and Challacombe, 1997; Nittayananta HIV transmission risk behaviour, as in Africa.

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Table 3 Prevalence of oral lesions among HIV-infected people in developing and developed nations

Reference Country/ AIDS status* No. subjects Any oral OC OHL Ulcers Neoplasms HIV Perio Others
Region (% men) lesion Dz

ASIA
Ranganathan et al (2000) India 37% AIDS 300 72% 56% OC 3% 3% 0% 16% LGE 23% hyperpigmentation;
(68%) 33% PC 2% oral submucous brosis

100
14% EC
8% AC
1% HYP
Anil and Challacombe India 44% AIDS 96 N/A 81% OC 7% 6% APHTH 4% SCCa 23% NUP 4% non-healing extraction wound
(1997) (59%) 64% PC 3% TB ulcer
21% EC
13% AC
Nittayananta and Thailand 100% AIDS 124 82% 66% OC 13% 11% Atypical 5% 7% 4% HIS
Chungpanich (1997) (73%) 54% PC 5% HSV NHL 2% PEN
25% EC 63% XEROS
6% AC
AFRICA
Matee et al (2000) Tanzania 65% AIDS 192 N/A 12% OC 6% 4% APHTH 0% 0% 47% HIVSGD
(N/A) 12% PC 2% HSV 1% CA
0% EC 7% Other
0% AC
Oral lesion prevalence and classification
LL Patton et al

Arendorf et al (1998) South Africa 20% CDC1 600 60% 38% OC 20% 3% 2% KS 4% LGE 1% HIVSGD
24% CDC2 (63%) 16% PC 1% HSV 1% NHL 1% NUG 1% hyper-pigmentation
35% CDC3 16% EC 3% NUP
20% CDC4 7% AC
Arendorf et al (1997) South Africa N/A 485 56% 35% OC 19% 3% 0% 4% LGE 18% other
(65%) 13% PC 2% NUG
16% EC 4% NUP
6% AC
Itula et al (1997) Namibia N/A 29 21% 0% 3% 3% HSV 3% KS 3% LGE 3% leukoplakia of buccal mucosa
(55%) of face 3% NUG
Hodgson (1997) Zambia 48% AIDS 107 N/A 25% OC 5% 0% 8% KS 4% 5% HIVSGD
(42%) 19% PC 3% NUG 4% Zoster

6/12/02, 9:42
6% EC 1% NUP
Wanzala and Pindborg Kenya N/A 337 21% 13% EC 3% 2% APHTH 1% KS N/A N/A
(1995) (0%) 1% PC 1% HSV
1% AC
2% HYP
Mugaruka et al (1991) Zaire 95% AIDS 103 N/A 62% OC 0% 6% APHTH; 5% KS 4% NUG 13% HIVSGD
(Democratic Republic (N/A) 31% PC 1% HSV 12% non- 1% HPV
of the Congo) 29% EC necrotizing
3% AC gingivitis
2% HYP
Tukutuku et al (1990) Zaire 100% AIDS 83 N/A 94% OC 14% 12% APHTH 12% KS 16% NUG 2% HIVSGD
(Democratic Republic 32% PC 4% HSV 17% NUP 8% leukoplakia
of the Congo) (45%) 23% EC
33% AC
6% HYP
ODIC20
Wanzala et al (1989) Kenya N/A 269 13% 13% OC 2% 1% APHTH 0% N/A N/A
(0%) 11% EC 1% HSV
1% AC
1% HYP

LATIN AND SOUTH AMERICA

Ramirez-Amador Mexico 79% AIDS 436 71% 39% OC 30% 8% 2% KS 3% NUG 6% exfoliative chelitis;
et al (1998) (87%) 18% PC 3% HSV 2% NUP 5% hyperpigmentation;
26% EC 3% XEROS
11% AC
Ramirez-Amador Mexico 100%AIDS 42 N/A 36% PC 33% 0% 52% KS 9% LGE 26% exfoliative chelitis

101
et al (1993) with cancer (95%) 12% EC 14% oral hyperpigmentation
5% AC 9% XEROS
Gillispie and Marino Argentina N/A 125 N/A 40% OC 3% 2% 3% KS 0% LGE
(1993) (77%) 6% AC 12% HSV 24% NUG
10% NUP
Brazil N/A 269 (85%) N/A 42% PC 11% 5% 8% KS 2% LGE
12% EC 1% HSV 1% NUG
5% NUP
Chile N/A 15 N/A 47% OC 20% 7% 13% KS 0%
(93%) 27% PC 0% HSV
20% EC
Mexico N/A 125 N/A 51% OC 43% 4% 3% KS 4% LGE 5% oral erythema
(88%) 16% PC 3% HSV 0% NUG
35% EC 4% NUP
16% AC
Peru N/A 20 (100%) N/A 70% PC 25% 30% 5% KS 0% 25% oral erythema
25% EC 0% HSV
55% AC

EUROPE
Margiotta et al (1999) Italy 35% AIDS 104 36% 6% PC 10% 4% APHTH 0% 3% LGE/ 7% hyperpigmentation
LL Patton et al

(64%) 4% EC NUG/NUP 1% HPV

Schmidt-Westhausen Germany 30% AIDS 70 43% 31% OC 7% 3% 0% KS 0% 3% HIVSGD
et al (1997) (0%) 24% PC 1% HSV 0% NHL
6% EC
4% AC
Ceballos-Salobrena Spain 42% AIDS 396 99% 66% OC 16% 1% 3% KS 5% NUG 1% other
et al (1996) (74%) 38% PC 5% HSV

6/12/02, 9:42
24% EC
23% AC
Oral lesion prevalence and classification

7% HYP
Palmer et al (1996) UK 42% AIDS 456 59% 24% EC 30% 6% 4% KS 8% NUP 2% XEROS
(95%) 14% PC 2% HSV 2% petechiae
6% AC 1% HIVSGD
1% HPV
Ficarra et al (1994) Italy 22% AIDS 36 50% 39% OC 17% 14% HSV 0% 6% NUG 3% Zoster
(100%)
Laskaris et al (1992) Greece 23% AIDS 160 91% 61% OC 24% 8% 12% KS 4% LGE 4% HPV
(N/A) 31% PC 3% HSV 1% NHL 11% NUG 26%XEROS
16% EC 1% SCC 19% NUP 4% exfoliative chelitis
11% AC 1% HL 2% hyperpigmentation
4% HYP
101

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Table 3 (contd)

Reference Country/ AIDS status* No. subjects Any oral OC OHL Ulcers Neoplasms HIV Perio Others
Region (% men) lesion

102
Dz

Barone et al (1990) Italy 9% AIDS 217 41% 31% OC 19% 1% HSV 3% KS 0% 3% hyperpigmentation
(79%) 18% EC 1% HPV
9% PC 1% other
4% AC
1% HYP
Moniaci et al (1990) Italy N/A 737 40% 24% OC 10% 3% 2% KS 1% NUG 2% XEROS
(73%) 11% EC 1% HSV 4% other
7% PC
2% AC
1% HYP
Porter et al (1989) 9% AIDS 44 N/A 25% PC 16% 7% HSV 2% KS 9% LGE 5% furred tongue
(98%) 2% EC 11% NUG 2% XEROS
7% AC 11% NUP 2% hyperpigmentation
2% HYP
Oral lesion prevalence and classification
LL Patton et al

Schulten et al (1989) Netherlands 44% AIDS 75 76% 52% OC 16% 4% 4% KS 5% NUG 5% petechiae
(92%) 35% PC 1% HSV 5% XEROS
13% EC 4% brown hairy tongue
12% AC 4% HPV
3% HYP 3% other

NORTH AMERICA
Patton et al (2000) North Carolina 33% AIDS 299 38% 17% OC 11% 3% APHTH 0% KS 2% NUG/ 5% HIVSGD
(73%) 2% HSV 0% NHL NUP/NUS 4% HPV
Patton et al (1998) North Carolina 50% AIDS 238 48% 20% OC 26% 4% APHTH 2% KS 4% LGE 2% HIVSGD;
(76%) 15% PC 1% NOS 1% NHL 1% NUG 2% HPV
4% EC 2% HSV 5% NUP

6/12/02, 9:42
3% AC
Schuman et al (1998) US multicentre 17% AIDS 867 40% 15% OC 7% 3% 0% KS 14% LGE 1% HPV
(0%) 12% PC 11% NUG
3% EC
4% AC
Begg et al (1996) New York 10% AIDS 164 (83%) N/A 31% OC 16% 16% 2% KS 21% LGE N/A
Little et al (1994) Minnesota 0% AIDS 106 28% 5% OC 9% 8% 0% KS 0% LGE 1% HPV
(N/A) 6% HSV 2% NUP
5% NUS
Glick et al (1994) Philadelphia, PA N/A 454 N/A 54% OC 17% 3% APHTH 7% KS 9% NUP 8% XEROS
(89%) 5% HSV 3% HIVSGD
Lamster et al (1994) New York 10% AIDS 160 N/A 30% OC 29% 11% 2% KS 22% LGE 1% HPV
(83%) 6% NUG
Shiboski et al (1994) San Francisco, CA 0% AIDS 176 22% 14% OC 10% 3% 0% KS N/A 0% HPV
(0%) 11% PC 0% NHL 0% HIVSGD
4% EC
2% AC
ODIC20
Barr et al (1992) New York 29% AIDS 102 (100%) 36% 17% OC 20% 4% APHTH 2% KS N/A N/A
9% PC 3% HSV
6% EC
2% AC
Thompson, et al US Military N/A 390 (97%) N/A 9% OC 9% N/A N/A 7% NUG N/A
(1992) 8% PC
1% EC
Klein et al (1991) New York 100% AIDS 181 (57%) 92% 92% OC 19% 10% 4% KS N/A N/A
Melnick et al (1991) Minnesota 0% AIDS 106 (98%) 25% 5% OC 9% 8% APHTH N/A N/A 1% HPV
6% HSV
Feigal et al (1991) San Francisco, CA N/A 737 N/A 6% PC 20% 2% 2% KS N/A N/A

103
(100%) 1% EC
1% AC
Swango et al (1991) US Military 6% AIDS 230 (90%) 30% 16% OC 14% 2% AHPTH 0% KS N/A N/A
11% PC
6% EC
3% AC
Melnick et al (1989) Washington State N/A 141 (N/A) 30% 12% OC 13% 2% APHTH 1% KS 4% NUG 0% HPV
0% HSV
Roberts et al (1988) US NIH referral 100% AIDS 84 (92%) N/A 29% OC 4% 2% APHTH 38% KS 7% NUG 7% XEROS
Phelan et al (1987) New York 100% AIDS 103 N/A 88% OC 5% 3% 4% KS N/A 9% XEROS
(77%) 88% PC 9% HSV 9% exfoliative chelitis
6% patchy depapillated tongue
3% other
Silverman et al (1986) San Francisco, CA 91% AIDS 164 (100%) N/A 87% OC 21% 7% APHTH 32% KS 19% NUP 13% XEROS
10% HSV 2% NHL 1% HPV
Barr and Torosian (1986) New York 66% AIDS 122 (100%) 84% 83% OC 0% 5% 11% KS N/A N/A
5% HSV
AUSTRALIA AND PACIFIC ISLANDS
None

Key: OC = oral candidiasis; PC = pseudomembraneous candidiasis; EC = erythematous candidiasis; AC = angular cheilitis; HYP = hyperplastic candidiasis; OHL = oral hairy leukoplakia; HSV = herpes
LL Patton et al

simplex virus; KS = Kaposis sarcoma; NHL = non-Hodgkins lymphoma; LGE = linear gingival erythema or HIV-gingivitis; NUG = necrotizing ulcerative gingivitis; NUP = necrotizing ulcerative
periodontitis or HIV-periodontitis; NUS = necrotizing ulcerative stomatitis; HIV SGD = HIV salivary gland disease (or enlarged parotid and/or submandibular glands); XEROS = xerostomia; APHTH =
aphthous ulcers, HIS = histoplasmosis; PEN = penicilliosis; HPV = human papilloma virus infection; CA = carcinoma; HL = Hodgkins lymphoma; NOS = not otherwise specied.
*AIDS status = AIDS by CDC case denition (USDHHS, 1992), by clinical AIDS dening illness, or by CD4 nadir <200 cells mm3.

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103

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 Oral lesion prevalence and classification
LL Patton et al
104
Non-Hodgkins lymphoma is reported to be present in up
to 5% of HIV-infected adults in Africa and Asia (Nittayananta
and Chungpanich, 1997) and up to 2% of individuals in the
US (Silverman et al, 1986). Linear gingival erythema is
present in up to 16% of patients in developing nations
(Ranganathan et al, 2000) and 22% in the US (Lamster
et al, 1994). Necrotizing (ulcerative) gingivitis and necrot-
izing (ulcerative) periodontitis are reported to be present
in up to 16% and 17% of patients in Africa, respectively
(Tukutuku et al, 1990), and a 23% prevalence of necrotiz-
ing ulcerative periodontitis has been reported in India (Anil
and Challacombe, 1997). In contrast, in the US and Europe,
necrotizing (ulcerative) gingivitis and necrotizing (ulcerat-
ive) periodontitis are reported in up to 11% and 19% of
HIV-infected subjects, respectively (Silverman et al, 1986;
Laskaris et al, 1992; Porter et al, 1989; Schuman et al, 1998).
At the Workshop, an overview of the new classication
of oral lesions associated with paediatric AIDS was given
by Dr Francisco J. Ramos-Gomez. Oral candidiasis is the
most commonly reported lesion in children infected with
HIV and may be the rst clinically visible manifestation
of the disease (Ramos-Gomez et al, 1999). Its prevalence
varies from 18% to 72% (Ketchem et al, 1990; Katz et al,
1993; Moniaci et al, 1993; Chan et al, 1994; Valdez et al,
1994; Del Toro et al, 1996; Howell et al, 1996; Ramos-
Gomez et al, 1996). Among a study group of 91 perinatally
exposed HIV-positive children (median age 20 months, range
1 month7 years) in Northern California, 67% had orop-
haryngeal candidiasis present for 2 months or recurrent de-
spite topical therapy, compared to 8% of 185 non-infected
children born to HIV-positive mothers, resulting in a 25-
fold higher risk of oral candidiasis among those with HIV
(Ramos-Gomez et al, 1996). As is the case with adults, oral
candidiasis may have value in predicting progression to
AIDS in children (Katz et al, 1993; Ramos-Gomez et al,
1996).
HSV infections are common in childhood both as primary
gingivostomatitis and recurrent HSV infection and are re-
ported in 1.724% of HIV-infected children (Katz et al, 1993;
Moniaci et al, 1993; Ramos-Gomez et al, 1996). Linear
gingival erythema is the most common HIV-associated
periodontal disease in children and is reported to vary widely
in frequency from 0% to 48% (Chan et al, 1994; Howell
et al, 1996; Ramos-Gomez et al, 1999). Parotid enlargement
or glandular swelling occurs in 350% of HIV-infected chil-
dren, later in the disease course and may be associated with
slower progression of HIV disease (Katz et al, 1993; Moniaci
et al, 1993; Chan et al, 1994; Valdez et al, 1994; Del Toro
et al, 1996; Ramos-Gomez et al, 1999). Recurrent aphthous
ulcers are also moderately common in children with HIV,
occurring in 57% of children (Moniaci et al, 1993; del
Toro et al, 1996). Other lesions strongly associated with
HIV in adults, such as oral hairy leukoplakia and KS, are
rare in children (Ramos-Gomez et al, 1999).
2 Should the accepted classification
of oral lesions in relation to HIV be
modified in the light of recent findings?
The classication system for oral lesions as proposed by
the EC-Clearinghouse and WHO in 1992 (EC-Clearinghouse
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ODIC20 104
1993) was not substantially challenged at this time. Peni-
cilliosis marneffei (Nittayananta, 1999; see section 4 below)
was recognized as a potential Group 3 Fungal infection
other than candidiasis lesion, as this disease had dramati-
cally increased recently with the explosive epidemic of HIV
in South-east Asia. KS, a Group 1 lesion, has also not been
reported in Asian countries. More urgently, assistance is
needed in developing and supporting the research infra-
structure and clinical expertise required to facilitate more
widespread documentation of oral lesion prevalence among
populations infected with HIV in developing countries, prior
to considering modication of the consensus classication
system. To date, there is a paucity of prevalence data from
developing countries when compared to that from Europe
and the US (see Table 3). Differences between prevalence
data reported from developed and developing countries
may be due to factors such as transmission risk behaviours,
geographical location, gender, ethnicity, malnutrition, and
endemic diseases.
Reporting on the status of research into the prevalence of
oral lesions in the current Democratic Republic of the Congo,
Dr Theophile Mbuguye pointed out that the only studies
from his country indicating a high prevalence of oral can-
didiasis are now a decade old (see Table 3, Tukutuku et al,
1990; Mugaruka et al, 1991). They were conducted prior
to the 1997 war that resulted in the change of his large
central African countrys name from Zaire to the Democratic
Republic of the Congo. The 1998 war and its consequences
have increased the poverty and worsened sexual behaviour
of the population, thus increasing the prevalence of sexu-
ally transmitted diseases and transmission of HIV. Dentists
in the Democratic Republic of the Congo are not effectively
involved in programmes dealing with the HIV pandemic.
As the HIV situation in African countries appears to be
similar, with increasing incidence of HIV resulting from
heterosexual transmission and limited resources for treat-
ment, the prevalence of oral manifestations of HIV is also
likely to be increasing, but the changing epidemiology
of oral disease has not been documented. There is an
urgent need to implement a network for Oral HIV/AIDS
in African countries to exchange information, expertise
and strategies for prevention and care. Then the recent
ndings from developing countries may justify modica-
tion of the current classication of oral lesions related to
HIV infection.
3 Why is there a gender difference in the
prevalence of oral lesions in developed
and developing countries?
Relationships between oral lesions and gender have been
reported in several studies. A low prevalence of oral lesions
among women sex workers in Kenya was initially reported
by Wanzala et al, (1989) and was thought to be a result of
relatively recent acquisition of HIV-1 infection by these
women. This indeed may have been the case because when
a sample from this population of women was examined 3
years later, the overall lesion prevalence had increased from
15% to 41%, with the relative risk signicantly increasing
as women in this later cohort progressed toward ARC/AIDS
from other stages (Wanzala and Pindborg, 1995).
6/12/02, 9:42

When assessing gender-oral lesion associations, work-
shop participants felt that it was important to acknowledge
possible strong confounding by transmission risk behavi-
ours, as is the case in cohort comparisons between homo-
sexual men and female injecting drug users (see section 5
below). For example, in a mixed gender, mixed transmis-
sion risk group population of 238 HIV-infected subjects
from North Carolina, analysis showed that for oral hairy
leukoplakia (63 cases), males had a bivariate odds ratio of
4.9 (95% CI 1.9, 12.9) and homosexual men had a bivari-
ate Odds ratio of 2.5 (95% CI 1.3, 5.0), whereas using a
multivariable approach the homosexual men risk behaviour
lost explanatory power, leaving male gender to be signic-
ant with an Odds ratio of 4.45 (95% CI 1.6, 11.96) (Patton
et al, 1998).
In a cross-sectional analysis conducted in Mexico City
involving 379 men and 57 women with HIV infection,
Ramirez-Amador et al (1998) reported that oral ulcers, KS
and necrotizing periodontal disease were present only in men,
whereas the other lesions studied, including hairy leukoplakia
and oral candidiasis, had no signicant gender predilection.
Arendorf et al (1997) reported that among HIV-infected
heterosexuals in South Africa, 160 males had a higher pre-
valence of oral lesions combined (candidiasis, oral hairy
leukoplakia, HIV-associated periodontal disease and other
oral lesions) than did 115 females (P = 0.054). Males
(11.9%) had a signicantly (P = 0.025) higher rate of HIV-
associated periodontal disease than females (6.1%). No
difference was found in oral hairy leukoplakia rates (23%
for men and 22% for women), whereas candidosis was
slightly more prevalent in women (46%) compared to men
(37%). In Maryland, among 444 men and 118 women who
are HIV-infected AIDS-free injecting drug users, Vlahov
et al (1994) found that the frequency of self-reported oral
candidiasis did not vary by sex overall or within levels of
CD4 cell count.
Two longitudinal studies presented at the workshop by
Dr Caroline H. Shiboski, gave further insight into the clini-
cal and statistical associations and possible causal relation-
ships between gender and various oral lesions, the strongest
evidence in developed nations being between male gender
and oral hairy leukoplakia and KS. Melnick et al (1994),
using a multicentre urban community cohort in the US,
reported that compared with 768 women, the 3779 men
were at increased risk over time for development of KS
(Relative Risk (RR), 6.25; 95% CI, 1.5425.0) and oral
hairy leukoplakia (RR, 1.85; 95% CI, 1.063.23). These
risks were obtained by a proportional hazards model with
stratication by centre and by covariates corresponding to
CD4 count, age, race, history of injection drug use, Karnofsky
score, disease progression history, and the use of antire-
troviral therapy and PCP prophylaxis. More women than men
experienced oropharyngeal pseudomembranous candidiasis,
but gender differences were not statistically signicant. These
authors suggested that gender differences in this cohort may
reect differential access to health care and standard treat-
ments or different socioeconomic status and social support
for women compared with men.
In a San Francisco, California-based cohort described
by Shiboski et al (1996), of 200 men and 218 women with
HIV infection, a regression model for longitudinal data
ODIC20 105
Oral lesion prevalence and classification
LL Patton et al
105
demonstrated that the odds of having hairy leukoplakia were
2.50 times (95% CI, 1.344.76) greater for men (22% preva-
lence) than women (9% prevalence), controlling for CD4
cell count, race and injection drug use. A weaker associa-
tion was found between the occurrence of oral candidiasis
and gender, favouring men (24%) versus women (13%)
(adjusted Odds ratio 1.85, 95% CI 1.03.43). These authors
suggest that the gender difference in prevalence and incid-
ence of oral hairy leukoplakia may result from a difference
in the mode of expression of the aetiological agent, Epstein
Barr virus (EBV) in the oral epithelium. A second possible
explanation was proposed that the gender difference may be
explained by the confounding effect of unknown variables,
such as history of medication use, smoking, and alcohol
intake. Thirdly, time since seroconversion is another un-
known variable that may have confounded the hairy
leukoplakiagender relationship, as the duration of HIV in-
fection may have been longer for men than women in this
group, such that controlling for CD4 cell count may not
reect the actual disease burden.
Since the development and widespread use in developed
nations of quantitative measurements of plasma HIV RNA
(viral load tests) to monitor viral response to antiretroviral
therapy (see review Patton and Shugars, 1999), additional
information has become available that suggests a lesser, but
supplemental, role for viral burden in the strong relation-
ship between CD4 cell count and expression of many of the
strongly associated oral manifestations of HIV. Patton et al
(1999), in a medically treated cohort of 250 HIV-infected
subjects in North Carolina, described individuals presenting
with oral hairy leukoplakia having a two-fold increased risk
(OR 2.08, 95% CI 1.03, 4.21) of having a relatively high
viral load (above 20 000 copies ml1) in a multivariable
logistic regression model controlling for CD4 count and
antiretroviral therapy. Additionally, Margiotta et al (1999)
in a cohort of 104 medically treated Italians with HIV,
found that individuals with oral lesions considered to be
strongly associated with HIV (including hairy leukoplakia),
had a median viral load of 17 900 copies ml1 compared to
1795 copies ml1 for those without oral lesions. Perhaps the
association of male gender with oral hairy leukoplakia in
the Shiboski et al (1996) and Melnick et al (1994) studies
could be partially explained by higher viral loads among
men who were infected earlier in the HIV epidemic and had
undergone greater disease progression at the time of inclu-
sion in these studies.
4 Are there unusual lesions that are
present in developing countries?
Unusual lesions are appearing in HIV-infected individuals in
developing countries. A relatively newly described lesion
resulting from infection with the fungus, Penicillium marne-
ffei, which displays orofacial manifestations, was reviewed
by Dr Wipawee Nittayananta (Nittayananta, 1999). This
facultative intracellular pathogen was uncommon before
AIDS and is now the third most common opportunistic in-
fection after tuberculosis and cryptococcosis in patients with
HIV/AIDS in certain parts of South-east Asia where it is
endemic (Duong, 1996). Penicilliosis marneffei accounts for
14% of initial clinical presentations of patients with AIDS
Oral Diseases
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 Oral lesion prevalence and classification
LL Patton et al
106
(Clezy et al 1994). The reservoir in nature and mode of
exposure is unknown. However, inhalation of spores from
contaminated soil is the most likely route of transmission
(Nittayananta, 1999).
Clinical presentation can take the form of a focal
penicilliosis or a fatal, progressive, disseminated infection
(Nittayananta, 1999). Signs and symptoms are varied, includ-
ing a chronic productive cough, generalized lymphadeno-
pathy, septicaemia, hepatosplenomegaly, anaemia, leukocy-
tosis, intermittent fever with or without chills, weight loss,
osteoarticular lesions, pericarditis, multiple subcutaneous
abscesses, and papule-like ulcers (Nittayananta, 1999).
Cutaneous lesions on the face, upper trunk and extremities
resemble the nodular or papular necrotic lesions of mol-
luscum contagiosum (Nittayananta, 1999). Oral lesions may
occur as shiny papules, erosions or shallow ulcers of vary-
ing sizes covered with whitish yellow, necrotic slough on
the palate, gingiva, labial mucosa, tongue and oropharynx
(Nittayananta, 1999). A study of oral lesions in a group of
124 Thai adults with AIDS, conducted by Nittayananta and
Chungpanich (1997), revealed oral lesions of penicilliosis
to be relatively rare, with a prevalence of 2%, both cases
being found in women. Serological tests for both antigens
and antibodies are used for rapid presumptive diagnosis,
although positive culture on Sabourauds dextrose agar at
25C and biopsy are required for denitive diagnosis
(Nittayananta, 1999). Treatment of mild to moderately severe
penicilliosis marneffei is accomplished with itraconazole
or ketoconazole, whereas parenteral amphotericin B may be
required for serious infection (Nittayananta, 1999). Early
treatment improves prognosis.
A review of the literature revealed that another lesion
seen in HIV-infected children and young adults in Africa
is noma or cancrum oris. This may resemble necrotizing
ulcerative stomatitis in HIV-infected adults in developed
countries. Chidzonga (1996) described eight cases of this
gangrenous infection of the oral cavity, which is common
in malnourished children or those with predisposing debil-
itating disease or immune suppression. Noma may begin as
a small ulcer of the buccal or gingival mucosa that rapidly
progresses to extensive necrosis, creating deep perforated
wounds. Management includes treatment of predisposing
disease, local debridement and wound irrigation with saline
and hydrogen peroxide, systemic antibiotics (penicillin, strep-
tomycin or metronidazole) and nutritional support. The acute
destructive process may be arrested by conservative treat-
ment; however, long-term consequences of noma in African
AIDS patients are unknown because patient survival rate
from HIV is so poor.
Unusual lesions in HIV-infected patients may indeed be
newly described opportunistic infections presenting in the
oral cavity or merely existing oral disease conditions that
are exacerbated by the underlying immune deciency, asso-
ciated nutritional deciency, and general disease state. Tu-
berculosis ulcers of the tongue and squamous cell cancers
of the oral cavity may be on the rise as the HIV epidemic
grows in Asia, where tuberculosis is a common opportunis-
tic infection and betel nut chewing is a strong risk factor
for oral cancer (Anil and Challacombe, 1997). Unusual com-
plications of common oral disease may also occur in an
immune suppressed patient, such as non-healing extraction
Oral Diseases
ODIC20 106
wounds (Anil and Challacombe, 1997). Other oral lesions
not currently included in the accepted Classication scheme
for Oral Manifestations of HIV (EC-Clearinghouse, 1993)
have been reported, including: exfoliative cheilitis (Phelan
et al, 1987; Laskaris et al, 1992; Ramirez-Amador et al,
1993; Ramirez-Amador et al, 1998), submucous brosis
(Ranganathan et al, 2000), brown hairy tongue (Schulten
et al, 1989), petechiae (Schulten et al, 1989; Palmer et al,
1996) and oral erythema (Gillispie and Marino, 1993).
5 Is there any association between modes
of transmission and the prevalence of
oral lesions?
Certain oral lesions have been associated with specic modes
of HIV transmission in several populations. Evidence points
to a homosexual male bias for KS and oral hairy leukoplakia.
In a New York City prevalence survey, KS and hairy
leukoplakia were seen exclusively in homosexual men
(Phelan et al, 1987). In a North Carolina cohort, KS was
signicantly associated with homosexual men (P = 0.048)
who were at a 2.5-fold higher risk of hairy leukoplakia than
individuals with other risk behaviours (95% CI 1.3, 5.0)
(Patton et al, 1998). Among a group of 737 HIV-infected
Italians in Turin, most being injecting drug users, hairy
leukoplakia and KS were clearly more prevalent in homo-
sexual men than in other risk groups (Moniaci et al, 1990).
In Florence, Italy, 217 HIV-infected patients (65% inject-
ing drug users) were examined for oral lesions and all pati-
ents with KS were homosexual or bisexual men (Barone
et al, 1990). Similarly, in the New York cohort of Lamster
et al, (1994), KS occurred only among homosexual men.
Even among HIV-infected women, Shiboski et al (1994)
observed a sexual transmission risk association. Of those
who became infected through high-risk sexual activity, 22%
had hairy leukoplakia, whereas of injection drug users only
5% were diagnosed with this lesion (P = 0.01).
Comparing oral lesion prevalence among 79 HIV-infected
injection drug users and 81 HIV-infected homosexual men
in New York City, Lamster et al (1994) reported that the
percentage of subjects with oral lesions did not differ by
risk cohort, yet the types of lesions did differ by group.
Injecting drug users had a much higher prevalence of oral
candidiasis than homosexual men (43% versus 17%), possi-
bly due to a greater underlying burden of dental disease and
greater baseline carriage of oral Candida. In San Francisco,
oral candidiasis was less frequently observed among women
who acquired HIV heterosexually than for women who were
injection drug users at all CD4 levels, although this associa-
tion was statistically signicant only for women with CD4
cell count nadirs <200 cells mm3 (P = 0.003) (Shiboski
et al, 1994).
In an HIV-infected population in South Africa, Arendorf
et al, (1997) reported that 88 homosexual males had a higher
prevalence of oral candidiasis (49%) than 115 heterosexual
males (37%; P = 0.063). These authors propose that the
increased practice of oro-genital sex among homosexuals
(89%) compared to heterosexuals (34%) may contribute to
the increased prevalence of oral candidiasis seen among
homosexuals. In the Mexico City cohort of Ramirez-Amador
et al (1998), erythematous candidiasis was more likely
6/12/02, 9:42

among patients who contracted HIV via blood transfusion
as opposed to those who acquired HIV through sexual
transmission.
In Lamster et al (1994), oral ulcers were found in 13.6%
of homosexual men in New York compared to 7.6% of
injection drug users. Ramirez-Amador et al (1998) reported
that in Mexico City oral ulcers were found only in indi-
viduals who contracted HIV through sexual transmission. It
thus appears that individuals acquiring HIV through sexual
transmission, who are becoming an increasing proportion of
world AIDS cases, may be at greatest risk of oral disease.
In many of these cases, there may be sexual transmission of
known (e.g. KS-associated human herpes virus or human
herpes virus 8; Di Alberti et al 1996) and yet to be known
viral cofactors.
Future research agenda
The future research agenda for this area must be cognizant
of differences in resources between developed and develop-
ing nations. This must include the extent of existing research
infrastructure and potential for its expansion in developing
nations. Collaboration or partnering between developing and
developed nations to accomplish this agenda was considered
important by workshop attendees.
All studies are strengthened by use of rigour in study
design, use of the best trained and experienced examiners,
specic documented subject inclusion criteria, and docu-
mented use of standard presumptive or denitive oral lesion
diagnostic criteria as may be appropriate for study design.
Developing nations
Identication and documentation of the prevalence of oral
lesions among HIV-infected children (including neonates)
and adults as compared to HIV-negative individuals is needed
to allow distinction between unusual presentations of preva-
lent endemic oral disease and unusual new HIV-associated
diseases. Consideration in these studies should be given
to cofactors such as transmission risk behaviours, gender,
ethnicity, co-infections (sexually transmitted diseases, oral
infections, tuberculosis, etc.), malnutrition, tobacco smok-
ing, and other oral habits.
Developed nations
Prevalence studies in developed nations should allow inclu-
sion of factors similar to those in developing nations, sup-
plemented by laboratory analyses such as CD4 cell counts,
quantication of plasma HIV RNA, and use of antiretroviral
and other medications to treat HIV and its opportunistic
infections. Large or multicentre cohorts will be needed to
assess the impact of the evolution of HIV disease and its
management on oral lesion prevalence and incidence as
new technologies (e.g. therapeutic HIV vaccines) or evolu-
tion of antiretroviral drug resistance leads to renewed
viraemia or failure of HAART therapy in some individuals.
Currently observed gender differences with respect to hairy
leukoplakia in US populations may merit further investiga-
tion in conjunction with investigations of gender differences
in KS prevalence after controlling for variables such as
ODIC20 107
Oral lesion prevalence and classification
LL Patton et al
107
viral load, smoking, socio-economic status, and medication
intake.
Additional research is needed to help identify the (1).
prevalence of oral lesions among HIV-infected adults and
children more broadly among nations and regions of the
world; (2). prevalence and diagnostic/prognostic importance
of oral lesions during acute or primary HIV infection; and
(3). impact on oral lesion prevalence of systemic and local
innate resistance and acquired immunity (humoral and
cell-mediated immune response). If an accepted method of
quantifying oral lesions that includes extent and severity of
symptoms is developed, it would be important to include
this assessment in future studies to help gain a broader
sense of the impact of oral lesions on quality of life.
Once oral lesions among HIV-infected individuals have
been documented more extensively in developing nations,
the more global experience may suggest the need to re-
evaluate the EC-Clearinghouse and WHO classication
system of oral manifestations of HIV (EC-Clearinghouse,
1993). Future changes are likely in the Group 3 (seen in
HIV), Group 2 (less commonly associated with HIV), and
possibly Group 1 (strongly associated with HIV) oral lesions.
Although the classication system for orofacial manifesta-
tions of HIV-infected paediatric patients is relatively new
(Ramos-Gomez et al, 1999), inclusion of clinical experience
and future studies from African nations may suggest a need
to include additional lesions endemic to these countries in
some categories for children as well.
Conclusions
In the epidemiology of oral diseases, descriptive data must
rst be employed to document the variety and distribution
of oral conditions. From prevalence studies, new and emerg-
ing oral disease conditions, such as penicilliosis marneffei,
may be recognized as part of the oral disease burden of
HIV infection. Descriptive documentation must be followed
by analytic analyses where resources are available for the
application of good epidemiological science. In an ana-
lytical approach, predisposing and confounding factors, such
as the contribution of transmission risks to varying oral
disease presentations, must be acknowledged. Finally, the
interrelationship of oral disease to the entire biologic and
social environment in varying populations must be con-
sidered to allow us to predict infection and disease progres-
sion and to design strategies to prevent or treat the varied
oral consequences of HIV/AIDS within the limitations of
our knowledge and resources.
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