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Adv Dent Res 19:63-68, April, 2006
© 2006 International and American Associations for Dental Research

Oral Lesions in HIV Infection in Developing Countries: an Overview

Presented at the Fifth World Workshop on Oral Health and Disease in AIDS, Phuket, Thailand, July 6–9, 2004, sponsored by Prince of Songkla University, Thailand, the International Association for Dental Research, the World Health Organization, the NIDCR/National Institutes of Health, USA, and the University of California-San Francisco Oral AIDS Center.

K. Ranganathan1,*, and R. Hemalatha2

1 Department of Oral and Maxillofacial-Pathology, Ragas Dental College and Hospital, 2/102 East Coast Road, Uthandi, Chennai 600 119, India; and
2 Statistician, Ragas Dental College and Hospital, Chennai, India

Correspondence: * corresponding author, ran2{at}vsnl.com


   Abstract
TOP
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
HIV infection is a major global health problem affecting developing and developed countries alike. Oral lesions that are associated with this disease are important, since they affect the quality of life of the patient and are useful markers of disease progression and immunosuppression. Oral lesions in HIV infection have been well-documented in developed countries, but there are fewer reports on oral lesions from developing countries. Oral candidiasis is the most common opportunistic infection seen in all continents. Kaposi’s sarcoma has been reported only from Africa and Latin America, while histoplasmosis and penicilliosis were reported in patients with advanced disease from Thailand. HIV-associated salivary gland disease has a high prevalence in Africa and Latin America, especially in the pediatric group. It is clear that there are considerable regional variations in the oral manifestations of HIV infection, depending both on the populations studied and on the clinical expertise available, among other factors. Well-designed and -documented studies are necessary for the correct assessment of the nature and magnitude of the problem in developing countries, if oral health measures are to be effectively formulated for the HIV-infected.

KEY WORDS: Oral lesion • prevalence • HIV • candidiasis • India


   Introduction
TOP
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusions
 References
 
Human immunodeficiency virus (HIV) infection is a major global health problem. By the end of 2003, there were around 46 million HIV-infected people in the world (UNAIDS, 2004). More than 95% of the HIV-infected live in the developing countries. It is estimated that the number of people living with HIV infection in India alone is around 5 million (NACO, 2003), and this number is rapidly increasing. Given these figures, management of HIV infection has become one of the priority health issues in developing countries.

HIV-related oral lesions are frequent and often an early finding in HIV infection. They affect the quality of life of the patient and are useful markers of disease progression and immunosuppression, and their importance has been demonstrated in many studies (Greenspan, 1997; Margiotta et al., 1999; Patton et al., 1999).

A review of literature shows that the reports of oral lesions from developing countries are few when compared with those from developed countries. Also, the study designs and diagnostic criteria are varied. However, this is rapidly changing, as increasing numbers of investigators from different developing countries are publishing well-designed studies. This report summarizes the findings of these studies. The objective of this work was to ascertain the nature and prevalence of oral lesions in different regions, and to identify any gaps in ourunderstanding of these lesions in HIV disease.


   Methods
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 Abstract
 Introduction
 Methods
Results
 Discussion
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 References
 
We analyzed reports of oral lesions from developing countries over a period of 14 years (1990–2004), for both adult and pediatric cases. Reports in which the data collection and case-recording methods were well-described, the diagnostic criteria well-defined (EC Clearinghouse criteria, 1993), and the manuscript or at least a comprehensive abstract was available were chosen. Both cross-sectional and descriptive studies were included. Individual case reports were not included. The reports were then sub-grouped into four groups, based on the geographical region of the study: India, Thailand, Africa, and Latin America (Table 1Go).


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  		TABLE 1 - Regions reviewed
 

   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
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 References
 
Prevalence of any lesion
A detailed tabulation of the different studies, for both adult and pediatric patients, is given in Table 2Go. All the reports were cross-sectional, except for the cohort study on 1000 patients in Mexico (Ramirez-Amador et al., 2003) and a prospective study of 61 cases in Kenya (Butt et al,, 2001). The route of transmission in all adults was predominantly by sexual contact among heterosexuals, except in the report from Mexico (Ramirez-Amador et al., 2003), where 74% were MSM (men having sex with men), and the Thai cohort, where intravenous drug users constituted the majority (Nittayananta et al., 2001). In the pediatric group, HIV infection was acquired predominantly by vertical transmission, with a few cases due to blood transfusion.


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  		TABLE 2 - Oral Lesions in HIV-infected Adult and Pediatric Patients*
 
Males constituted the major percentage (> 50%) in most of the studies, except in the reports from Zaire (Tukutuku et al., 1990), Kenya (Butt et al., 2001), and Zambia (Hodgson, 1997), and in Thai cohorts, where women constituted more than 50% (Khongkunthian et al., 2001; Kerdpon et al., 2004). The percentage of adult patients with at least one oral lesion ranged from 21% (Wandzala and Pindborg, 1995; Itula et al., 1997) to 90% (Reichart et al., 2003) (Fig. 1Go). In the pediatric group, the percentage of those with one oral lesion ranged from 25% from India (Merchant et al., 2001) to a high of 63% from South Africa (Naidoo and Chikte, 2004).


Figure 1
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  		Fig. 1 - Reported prevalence of any HIV-associated oral lesions from developing countries on three continents (adults).

 
Type of oral lesion reported
Oral candidiasis was the most commonly reported oral lesion. The occurrence ranged from 12% in Tanzania (Matee et al., 2000) to around 94% in Zaire (Tukutuku et al., 1990). In reports from Latin American countries, the prevalence was around 40%. Reports from India ranged from 21–81% (Anil and Challacombe, 1997; Ranganathan et al., 2000, 2004), while prevalence was 25–66% in reports from Thailand (Nittayananta et al., 2001; Kerdpon et al., 2004). The most common type of candidiasis in adults was the pseudomembranous type, with the percentages ranging from 1% in Kenya (Wanzala and Pindborg, 1995) to 70% in Peru (Gillespie and Marino, 1993), followed by erythematous candidiasis, the frequency of which ranged from 3% in India (Ranganathan et al., 2004) to 35% in Peru (Gillespie and Marino, 1993). In addition, a combination of pseudomembranous and erythematous types has been reported in 3% and 9% of patients in two cohorts from Thailand (Khongkunthian et al., 2001; Reichart et al., 2003). Angular cheilitis has been reported from all the regions, while hyperplastic candidiasis has been reported only from Africa and India (Tukutuku et al., 1990; Mugaruka et al., 1991; Wanzala and Pindborg, 1995; Ranganathan et al., 2004). Candidiasis in the pediatric group ranged from 11% in the Ugandan cohort (Bakaki et al., 2001) to 63% in the South African cohort (Naidoo and Chikte, 2004).

Oral hairy leukoplakia (OHL) has been reported from all regions. A prevalence of 43% was reported from Mexico (Gillespie and Marino, 1993). A high of 20% has been reported from Africa (Arendorf et al., 1998) and 36% from Thailand (Kerdpon et al., 2004). Reports from India indicate a lower frequency of around 2–7% (Anil and Challacombe, 1997; Ranganathan et al., 2000, 2004). In the pediatric group, the reported frequency for OHL was 1% from Brazil and South Africa (Santos et al., 2001; Naidoo and Chikte, 2004) to 7% from Thailand (Khongkunthian et al., 2001; Reichart et al., 2003).

Gingivitis and periodontitis associated with HIV infection—linear gingival erythema (Fig. 2Go), necrotizing ulcerative periodontitis (Fig. 3Go)—have been reported from the different regions, with frequencies ranging from 2–6% and 1–28%, respectively. Necrotizing ulceratve gingivitis (Fig. 4Go) has been reported only from Africa and Argentina. In the pediatric group, a frequency of 2% linear gingival erythema has been reported from Brazil (Fonseca et al., 2000).


Figure 2
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  		Fig. 2 - Prevalence of linear gingival erythema in adults reported from developing countries (percentage of HIV+ patients).

 

Figure 3
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  		Fig. 3 - Prevalence of necrotizing ulcerative periodontitis in adults reported from developing countries (percentage of HIV+ patients).

 

Figure 4
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  		Fig. 4 - Prevalence of necrotizing ulcerative gingivitis in adults reported from developing countries (percentage of HIV+ patients).

 
Oral ulcers (Table 2AGo) constitute a small percentage of reported oral lesions and include recurrent aphthae, viral and tuberculous ulcers, non-specific ulcers, and those that are neoplastic. Non-specific ulcers and recurrent aphthae constitute the majority. In most of the studies, a definitive diagnosis was not available. In the pediatric group, the reported frequency of mouth ulceration was 1% from Brazil (Santos et al., 2001) to 14% from South Africa (Naidoo and Chikte, 2004).

Oral Kaposi’s sarcoma (Fig. 5Go) was not reported from India or Thailand in the series reviewed here. In contrast, a frequency of 52% has been reported from Mexico (Ramirez-Amador et al., 1993) and 19% from Zimbabwe (Chidzonga, 2003).


Figure 5
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  		Fig. 5 - Prevalence of Kaposi’s sarcoma in adults reported from developing countries (percentage of HIV+ patients).

 
Oral hyperpigmentation has been reported from India, Africa, and Mexico. The highest prevalence of 26% was from India (Ranganathan et al., 2004).

Salivary gland disease was reported in the series from Africa and Thailand. These include xerostomia and enlargement of salivary glands. A surprisingly high frequency of around 47% has been reported from Tanzania in adults 27–45 years old (Matee et al., 2000). In the pediatric group, the occurrence of salivary gland disease was 7% in Ugandan children under 18 months of age (Bakaki et al., 2001) and 50% in the South African cohort (Naidoo and Chikte, 2004).

Other oral lesions that have been reported include histoplasmosis (Nittayananta and Chungpanich, 1997; Kerdpon et al., 2004), penicilliosis (Nittayananta and Chungpanich, 1997), lymphoma (Nittayananta and Chungpanich, 1997; Arendorf et al., 1998; Kamiru and Naidoo, 2002; Ramirez-Amador et al., 2003), and oral squamous cell carcinoma (Anil and Challacombe, 1997). In the pediatric group, Molluscum contagiosum was seen in 21% of 71 children from South Africa (Naidoo and Chikte, 2004).

The individual oral lesions are listed by geographical location in Table 3Go. The range of prevalence from different regions is shown.


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  		TABLE 3 - Average Prevalence by Region
 

   Discussion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusions
 References
 
A comprehensive review of the literature of oral lesions in HIV infection, reported from developing countries over the last decade and half, reveals that although there are numerous case reports and cross-sectional/descriptive studies, prospective/longitudinal studies are lacking. The UNAIDS global HIV infection statistics (UNAIDS, 2004) state that almost 50% of those affected are women. Interestingly, except in a few studies (Tukutuku et al., 1990; Hodgson, 1997; Butt et al., 2001; Khongkunthian et al., 2001; Kerdpon et al., 2004), males constituted more than 50% of the cohort, even though the major risk was by sexual contact among heterosexuals. One reason we have encountered is that men have better access to these health centers than do women. Larger population-based studies in women and spouses of infected men are needed to improve out understanding of, and address, this discrepancy. Not surprisingly, studies reported in children are fewer than those in adults. However, given the fact that there are around 2.9 million children with HIV infection (UNAIDS, 2004), and since there are indications that the distribution of lesions in children may differ from that in adults, more studies are needed.

Oral candidiasis is the most common opportunistic infection encountered in both adult and pediatric populations in different regions. At present, it is usually effectively managed by antifungal medication. However, given its prevalence, it may not be too far in the future that we may encounter development of strains resistant to existing anti-fungal medications. Further research is needed to ascertain the strains in resource-poor countries, as well as drug sensitivity, and differences in the organisms, if any, from those in developed countries.

Among resource-poor continents, KS has been reported only from Africa and Latin America, due to the endemic presence of HHV-8. In Asian countries, particularly India, KS has not been reported, since HHV-8 is not endemic in this population.

Oral submucous fibrosis (OSMF) reported from India was due to the habit of areca nut chewing, a common habit in this part of the world, but it is not clear whether the frequency of OSMF is actually raised with HIV infection.

HIV salivary gland disease in adults (Tukutuku et al., 1990; Mugaruka et al., 1991; Hodgson, 1997; Arendorf et al., 1998; Matee et al., 2000; Chidzonga, 2003) and children (Bakaki et al., 2001; Naidoo and Chikte, 2004) has been reported from Africa. Though the reason for the high prevalence is not known, it has been suggested that this could be due to the presence of HLA-DR5 and untreated advanced-stage disease in Africans (McArthur et al., 2003).

The highest prevalence of xerostomia (63%) has been reported from Thailand (Nittayananta and Chungpanich, 1997), but it is highly likely that this was because all the patients were hospitalized and in the advanced stage of the disease, rather than being attributable to a direct association with salivary gland disease.

Histoplasmosis (Nittayananta and Chungpanich, 1997; Kerdpon et al., 2004) and penicilliosis caused by Penicillium marneffei (Nittayananta and Chungpanich, 1997) are endemic to Southeast Asia and are associated with severe immunosuppression. In both these studies, all the patients were in the advanced stage of the disease.

Periodontal lesions and gingivitis were more prevalent in Africa and India, due to poor nutrition and inadequate oral hygiene practices. However, there was much variation in the diagnostic criteria used. Consequently, there is a need for standardization of diagnostic criteria and assessment of outcome measures that can be easily taught, implemented, and reproduced in the resource-constrained setting of developing countries.

The variations reported in prevalence studies summarized here could be due to various factors that include race, gender, age, risk behaviors, geographical location, socio-economic and immune status, duration of HIV infection, medication, method of subject selection, number of subjects examined, diagnostic criteria used, and timing of evaluation of subjects (Patton et al., 2000).


   Conclusions
TOP
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
References
 
Oral candidiasis is the most common opportunistic infection seen in both adult and pediatric populations of the developing countries. Histoplasmosis and penicilliosis have been reported only from Thailand. Latin American countries report KS and salivary gland disease, the latter being more common in the pediatric group than in adults. An association of HIV with oral pigmentation and OSMF has been reported from India. A high prevalence of periodontitis and gingivitis has been reported from India and Africa, in association with HIV. Most of the reports cited here are descriptive and help us understand the nature of HIV disease and its distribution in the different regions of the world. Analysis of these data should serve as a nidus for well-designed prospective studies with well-defined diagnostic criteria and outcome measures, in both adult and pediatric groups. Future research should focus on the more frequent opportunistic infection, such as candidiasis, and address lesions with unique geographical distribution, such as Kaposi’s sarcoma.


   References
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 Methods
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 Discussion
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 References
 
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