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(A1) Identification of Oral Health Care Needs in Children and Adults, Management of Oral Diseases

T.A. Hodgson^1,*, S. Naidoo², M. Chidzonga³, F. Ramos-Gomez⁴ and C. Shiboski⁵

¹ Oral Medicine, Division of Maxillofacial Diagnostic, Medical and Surgical Sciences, UCL Eastman Dental Institute and UCLHT Eastman Dental Hospital, 256 Gray’s Inn Road, London, UK
² Department of Community Dentistry, Faculty of Dentistry, University of the Western Cape, Cape Town, South Africa
³ Department of Dentistry, College of Health Sciences, University of Zimbabwe, Avondale, Harare, Zimbabwe
⁴ Department of Growth and Development, University of California San Francisco, and Pediatric Dental Services, San Francisco General Hospital, USA; and
⁵ Oral Medicine Clinical Center, Department of Orofacial Sciences, University of California San Francisco, USA

Correspondence: ^* corresponding author, t.hodgson{at}eastman.ucl.ac.uk

	Abstract

TOP Abstract Introduction Conclusions and Suggestions for... References

 
The workshop considered five questions reviewing the identification of international oral health care needs of children and adults, and the management of oral diseases in resource-poor countries: (1) What is the role of the dental profession in the management of the HIV-infected individual? (2) Identifying health care needs-What are the epidemiology and disparities of HIV-associated oral lesions in children from different continents? (3) How effective is HIV treatment in controlling oral diseases? (4) Could we develop basic inexpensive oral and dental care protocols for economically deprived HIV-infected patients? and (5) What is the best method of arranging resources to meet the oral health care needs of people with HIV disease? The consensus of the workshop participants was that there is a need to re-target research efforts to non-established market economy countries and prioritize research in these regions to children with HIV disease. It will be important to assess commonalities and variations in oral health needs across geographical and cultural boundaries, and research efforts should be centralized in resource-poor countries to support multi-center longitudinal standardized studies. It is essential that oral health research be integrated into other health care research programs, to make these research priorities and public health initiatives feasible.

Key Words: Oral health • HIV • AIDS • international

	Introduction

TOP Abstract Introduction Conclusions and Suggestions for... References

 
This paper reports the debate and conclusions of a workshop on the identification of international oral health care needs of children and adults, and the management of oral diseases in resource-poor countries (Phuket, Thailand, July, 2004). A computer-assisted search of the English-language scientific literature conducted on MEDLINE was supplemented by references cited in the retrieved articles and presented by panel members to initiate discussion among the international participants in the workshop. The participants considered five questions:

• What is the role of the dental profession in the management of the HIV-infected individual?
  
• Identifying health care needs—What are the epidemiology and disparities of HIV-associated oral lesions in children from different continents?
  
• How effective is HIV treatment in controlling oral diseases?
  
• Could we develop basic inexpensive oral and dental care protocols for economically deprived HIV-infected patients?
  
• What is the best method of arranging resources to meet the oral health care needs of people with HIV disease?
  

Question 1: What is the role of the dental profession in the management of the HIV-infected individual? (Sudeshni Naidoo and Tim Hodgson)
The dental profession plays a multi-faceted role in the management of HIV-infected individuals:

• Orofacial lesions may identify adults with undiagnosed HIV infection.
  
• Orofacial disease may predict HIV disease progression in adults.
  
• In the diagnosis and management of HIV-associated orofacial lesions
  
• In maintaining quality of life
  
• In minimizing stigma and in the provision of non-discriminatory access to dental care
  
• In providing high-quality dental care
  
• In protecting others from harm (practicing universal infection control)
  

Orofacial lesions may identify adults with undiagnosed HIV infection.
During the routine dental examination of the asymptomatic individual or patient presenting with a specific oral mucosal complaint, oral health care professionals may detect signs consistent with underlying HIV infection. Many North American and European studies among adults have reported that the presence of oral candidosis (OC), oral hairy leukoplakia (OHL), and Kaposi’s sarcoma (KS) strongly suggests HIV infection in the absence of systemic immunosuppressive pharmacotherapy (Klein et al., 1984; Feigal et al., 1991; Ficarra et al., 1994; Shiboski et al., 1994; Greenspan, 1997; Greenspan and Greenspan, 2002). This led to the development of consensus guidelines defining oral lesions associated with HIV infection (EC-Clearinghouse, 1993).

In patients undergoing oral examination in Tanzania, with the examiner unaware of their HIV status, oral mucosal lesions associated with HIV infection showed a high (85%) positive predictive value for underlying immunosuppression (Schiødt et al., 1990). In Zaire, OC was one of several clinical features related to HIV sero-conversion (Colebunders et al., 1991). A Nigerian study reported oral thrush as a presenting sign of HIV infection in 27% of cases (Akpede et al., 1997). In South Africa, necrotizing ulcerative gingivitis/periodontitis presenting in an otherwise systemically well individual had a positive predictive value of 69.6% for underlying HIV infection (Shangase et al., 2004). Clinical signs strongly indicative of HIV infection included OHL, KS, and OC in Uganda and Malawi (Mayanja et al., 1999; Lewis et al., 2003). In populations where the prevalence of HIV was low, clinical diagnoses of oral mucosal lesions alone were poor predictors of HIV infection (Robinson et al., 1998). The positive predictive values increased if used with a social history to identify risk factors for infection. In a resource-poor, high-HIV-prevalence setting, a study of similar design and adequate power has not been reported.

Orofacial disease may predict HIV disease progression in adults.
Oral lesions in adults have been shown to be associated with increased risk of progression of HIV disease, and the majority of longitudinal studies from North America have demonstrated an association between the presence of OC and OHL and a decreased CD4 lymphocyte count in HIV-infected adult subjects (Lifson et al., 1994; Begg et al., 1996, 1997; Hilton et al., 1997; Rabeneck et al., 1997; Schuman et al., 1998; Shiboski et al., 1999) and Europe (Moniaci et al., 1990; Plettenberg et al., 1990; Morfeldt-Manson et al., 1991; Husak et al., 1996; Ravina et al., 1996; Munoz-Perez et al., 1998). Cross-sectional studies have associated low CD4 lymphocyte counts with the presence of oral KS (Glick et al., 1994), non-Hodgkin’s lymphoma (Flaitz et al., 1996; Lozada-Nur et al., 1996), or necrotizing ulcerative periodontitis (Glick et al., 1994). Therefore, an oral health care professional diagnosing these lesions in a known HIV-infected client should be alerted to possible disease progression.

It has been proposed that oral lesions may be utilized as surrogate markers of disease progression in adults in the developing world, in the absence of laboratory markers (Shiboski, 2002). Only one longitudinal study from a resource-poor country showed a more rapid progression to AIDS in adults with OHL and/or OC (Ramírez-Amador et al., 1996). A second longitudinal study from Rwanda showed OC as an independent predictor of early mortality in a female adult cohort (Lindan et al., 1992). The presence of OC was highly predictive of a low CD4 count in Indian and Thai adults in cross-sectional studies (Ghate et al., 2000; Ranganathan et al., 2000; Kerdpon et al., 2004). In Tanzania, there appeared to be no specific oral lesions of prognostic value in HIV-infected adults (Matee et al., 2000); however, others have reported OC and HL as strong predictors for HIV infection (Miller et al., 1995). However, in Nigeria, OC was associated with advanced HIV infection (Anteyi et al., 2003), and in Zambia, erythematous candidosis was the only lesion significantly associated with CD4 lymphocyte counts of fewer than 200 cells/mm³ (Hodgson, 1997). Unfortunately, the use of OHL, which has been used to indicate disease progression in the developed world, is confounded by a decreased prevalence in many developing countries (Hodgson, 1997; Nittayananta et al., 1997; Kumarasamy et al., 2000; Ranganathan et al., 2004).

Diagnosis and management of HIV-associated orofacial lesions
HIV-associated orofacial lesions and iatrogenic oral disease secondary to anti-retroviral therapy result in considerable morbidity. They may alter facial appearance, impair speech, and cause difficulty with swallowing, which may lead to significant weight loss. The management of the oral manifestations of HIV infection in North America and Europe has been extensively reviewed (Greenspan and Shirlaw, 1997; Shirlaw et al., 2002). Protocols for the resource-poor setting are reviewed in Question 4 of this workshop.

Oral health and quality of life
It is assumed that oral disease significantly affects quality of life in patients with HIV infection, and that appropriate treatment results in a measurable improvement; however, the impact of oral disease on the HIV-infected individual is poorly documented. Oral soft tissue discomfort requiring treatment was experienced by more than a quarter, and was the presenting feature in 3.3%, of 600 HIV-infected individuals in South Africa (Arendorf et al., 1998). More recently, but also from South Africa, Yengopal and Naidoo (personal communication/in press), in a case-control study using the Oral Health Impact Profile, conclusively showed that patients who present with oral lesions associated with HIV infection had a significantly lower oral-health-related quality of life than did HIV-positive patients without oral lesions.

In South Australia, patients with HIV experienced more discomfort than a comparable sample of the general population, with 16.7% avoiding leaving their homes because of dental problems (Coates et al., 1996). In multivariate analyses, the presence of oral symptoms had a significant impact on health-related quality of life (Lorenz et al., 2001; Coulter et al., 2002). In addition, an improvement in oral health was significantly associated with improvements in both physical and mental health (Coulter et al., 2002). Therefore, it seems reasonable to conclude, on the basis of a few studies, that the oral health care professional can play a role in improving and maintaining health-related quality of life in HIV-infected patients.

Minimize stigma—provide non-discriminatory access to dental care.
Although access to dental treatment has significantly improved for HIV-infected patients in North America and Europe, some oral health care practitioners remain unwilling to accept this patient group, and HIV-infected individuals continue to experience discrimination by health care professionals (HIV patients seek better dental care, 2002) (Table 1). While in the United States of America, the number of dentists willing to treat HIV-infected patients has nearly doubled to 83% from 1984 to 2003 (Gerbert, 1987; Seacat and Inglehart, 2003), a trend mirrored in many European countries (Angelillo et al., 1994; Scheutz and Langebaek, 1995), a recent study from central England would suggest that only 55% of dentists would accept HIV-infected patients for treatment without hesitation (Crossley, 2004). One of the few resource-poor countries to give insight into the willingness of dentists to provide care to HIV-infected patients is Brazil, where, despite there being an increase in dentists willing to treat HIV-infected patients, 60% remained concerned about providing care (Sposto et al., 1994; Jorge et al., 1996; Daniel et al., 2004). In South Africa, only 42% of dentists were willing to treat patients who were HIV-infected (Naidoo, 1997). In contrast, in Kenya, 87% were willing to treat this group (Gachigo and Naidoo, 2001). In Chennai, India, only 22% of dentists would willingly treat HIV-infected patients, and this was despite having appropriate levels of knowledge and infection control procedures (Balasundarum, 2004). It is difficult to compare studies from different continents directly, since not only are the geographical locations disparate, but also the samples selected are not comparable, and the response rates are variable.

Protect others from harm—practice universal infection control.
In North America and Europe, the risk of contracting HIV during dentistry is considered low, due to universal cross-infection implementation (McCarthy et al., 2002). The risk of transmission increases proportionally with the prevalence of HIV. In Africa, the number of patients presenting to dental clinics with undiagnosed HIV infection is significant. Recent estimates suggest 2.3% in Nigeria (Arotiba et al., 2003) and 10.9% in Tanzania (Matee et al., 1999). While the treatment needs of this patient group are the same as for those who are not HIV-infected, greater compliance with universally accepted cross-infection practices suitable for the resource-poor setting is required (Gachigo and Naidoo, 2001). In Mexico, 51% of dentists considered the risk of patient-to-patient transmission as considerable, despite improved levels of cross-infection control from 1992 to 1999 (Maupome et al., 2000, 2002).

Question 2: Identifying health care needs—What are the epidemiology and disparities of HIV-associated oral lesions in children from different continents? (Francisco Ramos-Gomez)
A literature review on the epidemiology of HIV-associated oral lesions in children worldwide retrieved 28 articles that may be grouped as (1) prevalence studies, (2) studies suggesting that orofacial lesions may contribute to identifying children with HIV infection, and (3) studies of the prognostic value of orofacial lesions among HIV-infected children. Table 3 summarizes those studies discussed in the workshop.

1. those commonly associated with pediatric HIV infection,
   
2. those less commonly associated with pediatric HIV infection, and
   
3. those strongly associated with HIV infection but rare in children.
   

Orofacial lesions commonly associated with pediatric HIV infection in North America and Europe include OC, herpes simplex infection, linear gingival erythema, parotid enlargement (PE), and recurrent oral ulceration. In contrast, orofacial lesions strongly associated with HIV infection, but rare in children, include KS, non-Hodgkin’s lymphoma, and OHL. Prevalence studies in North America and Europe consistently find OC to be the most frequently reported dental health condition (as high as 67%) among pediatric HIV patients (Ramos-Gomez et al., 1999; Chen et al., 2003), followed by PE, periodontal and gingival disease, and herpes simplex.

In Thailand, 48.9% of 45 HIV-infected children examined had one or more HIV-related oral lesions, and in this population, erythematous candidosis was most commonly identified (Reichart et al., 2003). In 169 South African HIV-infected children, 63% of those visiting the hospital outpatient department had orofacial lesions associated with HIV disease. In this sample, pseudomembranous candidosis was most commonly identified, and 9% of the sample had oral ulceration. However, only 1% of the sample had OHL, and none oral KS (Naidoo and Chikte, 2004). Almost 50% of the institutionalized sample had evidence of, predominantly unilateral, PE (Naidoo and Chikte, 2004). This study reinforces the need for careful definition of the setting from which the sample is recruited, since differences in prevalence may be a result of variable sample characteristics in the same geographical location. The prevalence of pediatric oral KS and ranula, however, appears to be increasing in HIV-infected children in Zimbabwe (Chidzonga and Rusakaniko, 2004). Several reports have suggested that an increasing number of HIV-infected children may present with cancrum oris, and cases have been reported from Zimbabwe, Lesotho, and South Africa (Chidzonga, 1996; Adedoja et al., 2002; Naidoo and Chikte, 2004). In Mexican and Indian children, OC is the most frequently detected HIV-related oral lesion (Gaitan-Cepeda et al., 2002; Madhivanan et al., 2002).

Orofacial lesions may identify children with HIV infection.
Oral lesions have also been shown to be the presenting symptoms and signs in HIV-infected children in North America and Europe (Katz et al., 1993; Moniaci et al., 1993; Howell et al., 1996; Ramos-Gomez et al., 1996, 2000; Nicolatou et al., 1999). It is suggested that erythematous candidosis is associated with an earlier stage of HIV disease in children, and is therefore an important early diagnostic indicator (Moniaci et al., 1993; Nicolatou et al., 1999); however, other longitudinal studies would suggest the pseudomembranous form to be the first oral sign (Ramos-Gomez et al., 2000). Oropharyngeal candidosis, PE, and orofacial herpes simplex infection are the most consistent markers of underlying HIV infection in children (Ramos-Gomez et al., 1996).

Orofacial disease may predict HIV disease progression in children.
The majority of studies reporting the prognostic value of oral lesions in children infected with HIV originate in the developed world (Tovo et al., 1992; Katz et al., 1993; Chan et al., 1994; Del Toro et al., 1996; Howell et al., 1996; Ramos-Gomez et al., 1996; Nicolatou et al., 1999; Kozinetz et al., 2000). In a Californian cohort, the presence of oropharyngeal candidiasis was significantly associated with all progression markers examined: failure to thrive, use of anti-retroviral agents, lower CD4 counts, and development of acquired immunodeficiency syndrome (AIDS) (Ramos-Gomez et al., 2000). The presence of OC and cervical lymphadenopathy suggests disease progression (Nicolatou et al., 1999), but these are poor predictors of the serious consequences of AIDS (Fine et al., 2003) or mortality (Barasch et al., 2000). A further North American study suggests that an increase in the number of oral lesions in known HIV-infected children is associated with a decreased CD4 count, but not HIV viral load (Flanagan et al., 2000). PE has been recognized as a distinct feature of HIV infection in children since the first descriptions of the disease. This manifestation has been reported in 10–30% of children with symptomatic HIV infection (Pahwa et al., 1986). The presence of PE is a predictor of positive prognosis and long-term survival in HIV-infected children (Katz et al., 1993). The prevalence of oral lesions in children on anti-retroviral therapy is significantly less than that in untreated controls; however, a low CD4 count remained significantly associated with a greater number of oral lesions (Okunseri et al., 2003a). A correlation between delayed tooth eruption and the progression of pediatric HIV to AIDS has been demonstrated (Hauk et al., 2001). Caries experience in HIV-infected children is considerably greater than that for the general US pediatric population (Hicks et al., 2000), and this was also reported in Romania (Chen et al., 2003). Caries experience appears to increase with a decreasing CD4 count and moderate to severe immune suppression (Hicks et al., 2000).

In Thai children, the prevalence of mucocutaneous disease increased with lower CD4 counts (Wananakul et al., 2003). However, in Brazil, although one study agrees with the Thai findings (Santos et al., 2001), another provides conflicting evidence with a correlation between the prevalence of pediatric oral lesions and the HIV viral load, but not the CD4 count (Grando et al., 2002). In a Mexican sample of 48 HIV-infected children, no association between the prevalence of HIV-related oral lesions and immunological status or viral load was observed (Gaitan-Cepeda et al., 2002). Analysis of the limited cross-sectional data from resource-poor countries therefore suggests that an increased frequency of oral lesions in children is associated with HIV disease progression, and, at the present time, the development of oral lesions strongly associated with HIV infection should alert the pediatrician and other health care workers in the developing world to possible disease progression.

Question 3: How effective is HIV treatment in controlling oral diseases? (Caroline Shiboski)
The results of the literature review on the effectiveness of HIV treatment in controlling oral diseases are summarized and presented according to the following outline: (1) Study design and population (Table 4); (2) Variables, measures, and statistics (Table 4); and (3) Study results and summary (Table 5).

Variables, measures, and statistics
The prevalence of OC was the main outcome in all studies (Table 5). Some studies also explored the prevalence of OHL, KS, and recurrent ulcers. The retrospective study of clinic records also included oral warts among the outcome measures. In the prospective studies, participants were followed over time from before HAART was initiated to several months/years after (Arribas et al., 2000; Schmidt-Westhausen et al., 2000; Ramírez-Amador et al., 2003; Greenspan et al., 2004; Nicolatou-Galitis et al., 2004). The cross-sectional studies compared several groups of participants on various treatment regimens (with or without protease inhibitors) with an untreated control group (Patton et al., 2000; Tappuni and Fleming, 2001). The case-control study compared 56 HIV-positive patients having clinically diagnosed oral warts with 168 HIV-positive controls with respect to specific immunologic factors, such as CD4 count and viral load (King et al., 2002). Prevalence was the most common measure of disease frequency reported, but incidence was estimated and explored over time in one recent study among adult women in the US (Greenspan et al., 2004).

Study results and summary
All the prospective studies and the retrospective study showed a significant decrease of OC over time (before and after the initiation of HAART) (Arribas et al., 2000; Schmidt-Westhausen et al., 2000; Greenspan et al., 2001, 2004; Ramírez-Amador et al., 2003; Nicolatou-Galitis et al., 2004), and one cross-sectional study found a much higher prevalence of OC among adults who were not on any anti-retroviral medication than in those on HAART (Tappuni and Fleming, 2001) (Table 5). Ramírez-Amador and her colleagues, who followed the largest sample over 12 years, found that OC decreased by half (from 44% to 20%) (Ramírez-Amador et al., 2003). Greenspan and colleagues (2004) reported that the incidence of OC fell from 7.4% to 3.4%, and estimated that the relative risk of having OC was half among women on HAART compared with untreated HIV-positive women (Greenspan et al., 2004). Only two prospective studies reported a decreased prevalence of HL over time (Schmidt-Westhausen et al., 2000; Ramírez-Amador et al., 2003). Similarly, one cross-sectional study found a significantly lower prevalence of HL in the group which included 42% participants on protease inhibitors, compared with the group recruited earlier, and among whom only 8% were taking PIs (Patton et al., 2000). One prospective study also reported a significant decrease in the prevalence of KS, from 9% to 1%, after the initiation of HAART (Schmidt-Westhausen et al., 2000). One intriguing finding was reported by Greenspan and colleagues, who conducted a retrospective analysis among adults followed in an Oral Medicine clinic: They found a statistically significantly higher prevalence of warts among those on HAART than among those who were not taking HAART (Greenspan et al., 2001). Furthermore, King and colleagues (2002) found that the risk of oral warts was associated with a 1-Log₁₀ decrease in HIV RNA level in the 6 months before diagnosis of oral warts (odds ratio, 2.35; 95% confidence interval, 1.08, 5.11).

This review reveals a very strong role played by HAART in controlling the occurrence of OC. The effect of HAART on other oral lesions does not appear to be as strong, probably because of the overall low background prevalence for most lesions other than OC. In populations that had a high baseline prevalence of HL, there was a significant decrease observed over time after the initiation of HAART.

Question 4: Could we develop basic inexpensive oral and dental care protocols for economically deprived HIV-infected patients? (Midion Chidzonga and Sudeshni Naidoo)
In HIV-infected individuals, oral management strategies aimed at improving quality of life need to be directed not only at those presenting with oral lesions associated with HIV infection, but also at the prevention of dental disease. The resultant improved oral-health-related quality of life in these populations would occur even in those who have no access to anti-retroviral therapy. Recently, a proposal for basic oral health care has been presented for under-served communities (van Palenstein Helderman and Mikx, 2002). The leading principle of the basic package of oral health care (BPOC) is that it should be available for all, with the emphasis on prevention, and has been defined as: (i) emergency care (oral urgent treatment), (ii) exposure to appropriate fluoride (affordable fluoride toothpaste), and (iii) appropriate treatment technology (atraumatic restorative treatment).

This can be extended to regions with high HIV prevalence with the added proviso of basic training in the diagnosis and management of the common HIV/AIDS oral lesions. This relies heavily on a community-oriented promotion of oral health and is meant to be affordable and effective, although the effectiveness, acceptance, and sustainability have yet to be adequately evaluated (van Palenstein Helderman et al., 2003). The package needs adaptation to each environment according to the prevailing disease pattern, infrastructure, and oral health level of development, as well as community attitudes, perceptions and practices, and available finance. The strategies for the prevention and control of HIV-related common orofacial disease are poorly documented in resource-poor countries, where expensive pharmacotherapy is unavailable.

OC is a significant cause of morbidity in HIV disease. Dysphagia in malnourished HIV-infected subjects may result in rapid clinical deterioration. There is no antifungal medication widely available for the majority of HIV-infected Africans. Even the use of topical antiseptic agents, such as gentian violet mouthrinse, is limited (Hodgson, 1997). The in vitro effect of gentian violet has been documented for many years (Simon and Tabrizi, 1967). The interim results of a randomized controlled study in Malawi, comparing gentian violet with nystatin suspension in children with OC, suggests that the much cheaper alternative is equally effective for management in this environment (Hodgson, personal communication).

The topical disinfectant chlorhexidine has been shown to be a promising agent to prevent OC in HIV-infected children (Barasch et al., 2004). The significant results of this study were not reproduced in HIV-infected adults in Thailand (Nittayananta et al., 2006).

Extracts of traditionally used East African medicinal plants—Entada abyssinica, Terminalia spinosa, Harrisonia abyssinica, Ximenia caffra, Azadirachta indica, and Zahna africana—showed in vitro activity against various Candida species, the minimum inhibitory concentrations ranging from 0.006 to greater than 8 mg/mL, and the minimum fungicidal concentrations from 0.06 to greater than 8 mg/mL (Fabry et al., 1996). Preliminary results suggest that Dodonaea angustifolia, a traditional South African medicinal plant, has in vitro antifungal activity (Patel and Coogan, 2006). The in vitro antifungal activity of 0.5% potassium Lawsone methyl ether (extract from Impatiens balsamina and Gentianaceae family) appears as effective as 0.12% and 0.2% chlorhexidine (Prasirst et al., 2006). The use of traditional antifungal agents in the resource-poor setting warrants further investigation. If a consistent clinical response in adequately powered trials, without reported adverse effects, is published, their use should be advocated in preference to more expensive antifungal preparations.

The essential oil of Melaleuca alternifolia (tea tree oil) has the ability to disrupt the permeability barrier of cell membrane structures, and the accompanying loss of chemiosmotic control is the most likely source of its lethal action on Candida species at minimum inhibitory levels (Hammer et al., 2003, 2004; Oliva et al., 2003). The equal efficacy of alcohol-based and alcohol-free melaleuca oral solutions for the treatment of fluconazole-refractory oropharyngeal candidiasis in patients with AIDS may provide a cheap alternative regimen for patients with AIDS and suffering from oropharyngeal candidosis refractory to fluconazole (Vazquez and Zawawi, 2002).

Important advances in the treatment of KS in North America and Europe, including the use of liposomal anthracyclines and paclitaxel (Cheung et al., 1999; Tulpule et al., 2002), have been superseded by the effect of highly active anti-retroviral therapy (Cattelan et al., 2004). However, the use of chemotherapeutic agents is not curative and is associated with cumulative toxicity, including bone marrow suppression; further, these agents are unavailable to the majority of resource-poor environments. Single-agent chemotherapy is intermittently available and may palliate Kaposi’s sarcoma in this setting (Olweny et al., 2005). Thalidomide may also be a potentially efficacious and cheap palliative therapy for mucocutaneous pediatric Kaposi’s sarcoma in the resource-poor setting (Hodgson et al., 2006).

Question 5: What is the best method of arranging resources to meet the oral health care needs of people with HIV disease? (Sudeshni Naidoo and Tim Hodgson)
Prior to the development of an oral health care program, a local needs assessment, combined with knowledge of the resources available to institute the proposed outcome, is required. Even in North America and Europe, many would argue that access to dental care is far from acceptable for many individuals with HIV infection. In the United States, while public policy suggests that HIV-infected individuals should be able to go to any dentist with whom they feel comfortable, and where they will receive the best possible care (Barnes et al., 1996), many individuals in Canada received hospital care regardless of disease stage (McCarthy et al., 1996), with access to other clinics limited by economic factors. A continuing level of dissatisfaction with the availability of oral health care has been reported in the United Kingdom (Croucher et al., 1997), and 40% of the people living with HIV had experienced discrimination at the hands of health care professionals (HIV patients seek better dental care, 2002). In Europe, the most appropriate setting for oral care delivery to HIV-infected individuals from a consumer’s perspective remains controversial (Scheutz, 1990; Gallagher et al., 1998). The factors supporting the need for dedicated clinics have previously been reviewed and, in many settings, remain unresolved (Abel et al., 1995; Glick and Sciubba, 1995; Rogers, 1995).

The goal of dental public health programs is to provide the greatest improvement in oral health to the greatest number of people at the lowest cost (Weintraub, 1998). Implicit in this statement is the argument that when any program is planned for a community, there is a broad range of factors that must be considered to ensure that maximum benefit is achieved by the targeted population. Data from Yengopal and Naidoo (personal communication) show that patients are affected by oral diseases in key performance areas of their lives. Clinicians, policy makers, and health managers who continue to ignore the patient’s views/feelings about how oral disease affects their quality of life stand the risk of developing or running oral health programs that are not relevant to the needs of the communities that they are designed to serve. Due to insufficient financial resource, limited dental workforce, and lack of infrastructure in non-established market economy countries, the solution of the oral health problem does not lie in extending traditional Western dental services (van Palenstein Helderman et al., 1999). To evaluate an approach to oral health care for a given target population, a small-scale demonstration project to evaluate effectiveness, efficiency, and sustainability should be completed before larger programs are attempted (van Palenstein Helderman et al., 2003). The Dakar Report, a regional oral health strategy for African countries, recognizes the significant burden of disease and disability caused by the oral manifestations of HIV (WHO, 1998; Hobdell et al., 2004). Prior to the issue of the report, previous approaches to oral health in Africa failed to recognize the epidemiological priorities of the region, or to identify reliable and appropriate strategies to achieve them. Although dental caries and periodontal disease have historically been considered the most important oral health problems around the world, in African countries they are neither as common (but are subject to regional variation) nor of the same order of severity as in the developed world (Manji et al., 1991; Baelum and Scheutz, 2002), and priority problems identified include cancrum oris, acute necrotizing ulcerative gingivitis, oral precancer and cancer, and the oral manifestations of HIV (WHO, 1998).

In the United States, the unmet oral health care needs of many HIV-infected individuals suggest that resources need review. To improve access to care in New York, mobile clinics have brought dentistry into the communities where there is the greatest need (Zabos and Trinh, 2001). These target African-Americans, Hispanics, low-income women and children, the homeless, and other risk groups previously receiving only emergency episodic dental care. To serve these diverse HIV-infected populations, greater co-ordination of services is needed, and state insurance programs should consider expanding the benefits structure to include dental care (Heslin et al., 2001). The success of the Minnesota access to dental care program was attributed to the removal of financial barriers and the mainstreaming of HIV-infected patients into primary dental health care (Hastreiter and Jiang, 2002).

Despite available services, 18.7% of HIV-infected patients in Argentina abandoned oral health care programs, the failure being dependent on proximity to clinics, and life-related and other epidemiological factors, including date of initial HIV diagnosis (Squassi et al., 1998). Episodic problem-oriented oral health care is more common among black than white HIV-infected individuals in North Carolina, with cost the most common barrier to accessing services (Patton et al., 2003). However, the decision to access dental services for any individual is multifactorial, and many lacked a perceived benefit of preventive health care and failed to access discretionary services because of a feeling of disenfranchisement from and distrust of health care providers.

Studies in sub-Saharan Africa reveal a limited access to and utilization of dental care among the black population, especially in rural areas and areas of extreme poverty (Westaway et al., 1999). Educating non-dental health care professionals to routinely and effectively examine the oral cavity in each patient seen, and to identify sentinel lesions, has been advocated in these regions (Shiboski, 2002).

In North America, access to dental care for HIV-infected children remains difficult in some areas. In the United States of America, 38% of HIV-infected children never visited the dentist, despite receiving consistent medical care and being on public insurance programs (Okunseri et al., 2003b). This percentage varied with ethnicity, half the white children in this cohort never having attended. Similarly, in Spain, few HIV-infected children receive dental care (Munoz-Munoz et al., 2002). In the United States of America, HIV-infected children also have a significantly lower compliance with oral health care programs than do non-HIV-infected children (Broder et al., 1996), with personal and family factors, as well as access to health care delivery systems, acting as barriers (Broder et al., 1999). Perceived barriers to dental treatment among female caregivers of HIV-infected children include poor interpersonal communication, shame and anger, other concurrent family illness, their own dental fear, and the fact that dental care is given low priority (Broder et al., 2002). Facilitators to improve access to dental care include good communication between caregiver and dentist, transportation assistance, and the coordination of visits with medical appointments.

A collaborative workgroup on oral manifestations of pediatric HIV infection has provided standardized management regimens and treatment recommendations for some of the more common HIV-related orofacial manifestations in North America and Europe (Ramos-Gomez et al., 1999). In addition to proposing a three-tiered classification model of pediatric orofacial manifestations (see answer to question 2), a comprehensive, anticipatory infant oral care program utilizing (1) oral health risk assessment at regularly scheduled dental visits, (2) early regular dental assessments, (3) counseling sessions with parents during either regular dental visits or additional visits scheduled if a child is deemed at risk, (4) preventive treatment such as the application of fluoride varnish or sealants, and (5) outreach and incentives to reinforce attendance and oral health education and disease prevention has been suggested (Ramos Gomez et al., 2002). Facilitating access to early and regular dental care is clearly a crucial part of any effective intervention strategy, and intervention techniques should be tailored to the community being served.

	Conclusions and Suggestions for Future Research

TOP Abstract Introduction Conclusions and Suggestions for... References

 
Five questions were explored through comprehensive literature reviews, and were discussed as part of this workshop. Review and discussion of the first question on the role of the dental profession in the management of HIV-infected people led to the following conclusions:

• Specific orofacial lesions may play an important role in identifying HIV-infected persons, which is particularly relevant and applicable to resource-poor countries. Thus, it is important to train health care professionals in the recognition of orofacial lesions in these settings.
  
• Prognostic significance of HIV-related orofacial lesions has been well-described in industrialized countries, but the concept is most applicable to the resource-poor setting.
  
• Early diagnosis of orofacial lesions is essential for optimal treatment, particularly periodontal lesions, which have a higher prevalence in resource-poor countries and may lead to cancrum oris.
  
• The dental profession also plays an important role with respect to the provision of routine dental care and to diet counseling for HIV-positive patients in maintaining a healthy oral cavity, which affects quality of life.
  
• There is still much work to be done with respect to minimizing stigma and decreasing discrimination to treat among dentists in both industrialized and resource-poor countries.
  
• The role of the dentist still needs to be emphasized with respect to universal infection control and protecting patients from HIV transmission.
  

Review and discussion of the second question on the epidemiology of HIV-associated oral lesions in children from different continents concluded that:

• OC is the most common lesion in children, but there is still a lack of data from resource-poor countries.
  
• Cancrum oris and possibly other orofacial lesions are seen in resource-poor countries but may be underreported.
  
• Specific orofacial lesions such as OC have been shown to be strongly associated with HIV disease progression in North America and Europe, and can play an important role as prognostic markers in resource-poor countries.
  
• There is a high prevalence of concomitant dental diseases in HIV-infected children around the world (due to frequency of cariogenic medication intake in industrialized countries, and to poor diet and access to care in resource-poor countries).
  

There is a need to:

• update and revise the Classification Criteria for Diagnosis for Oral Manifestations in Pediatric HIV Infection to include data from Asia, India, and Africa; and
  
• assess the prognostic implications of oral lesions for short-and long-term survival in resource-poor countries.
  

Review and discussion of the third question on the effectiveness of HIV treatment in controlling oral disease concluded that:

• HIV anti-retroviral treatment is very effective in reducing the occurrence of OC, but there is little evidence of change in HL prevalence.
  
• It has been suggested that there is an increase in the prevalence of oral warts in patients on protease inhibitors, although this conclusion was drawn from a study based in a clinic population. This may also suggest that an increase in oral wart prevalence is associated with immune reconstitution, as hypothesized by investigators who found increased risk of oral warts in patients with decreasing HIV RNA within 6 months before wart diagnosis.
  

Research should be conducted on the effect of HIV oral disease treatment on general HIV disease.

Review and discussion of the fourth question on the potential development of basic inexpensive oral and dental care protocols for resource-poor countries suggested the following:

• Reports have been published on the use of inexpensive remedies, such as gentian violet and oil of melaleuca, in the treatment of oral candidosis. Chlorhexidine could also be used in the prevention and treatment of oral candidosis.
  
• Other plant extracts have been studied in vitro, but there is a great need for randomized controlled trials on inexpensive local remedies of HIV-related orofacial lesions in resource-poor settings.
  

Review and discussion of the fifth and final question on optimal methods of arranging resources to meet oral health care needs of people with HIV disease led to the following recommendations:

• Local needs assessment and knowledge of local settings are of paramount importance prior to any protocol development
  
• It is also essential to: (1) integrate oral health skills into curricula of a wide range of health personnel, including recognition of HIV-related orofacial lesions, oral health home-based care, and the importance of enlisting community participation; and (2) integrate oral health care into other health-related programs, to improve patient oral health awareness, alleviate patient distrust in oral health care in many settings, and to educate parents/guardians regarding oral health care of their children.
  

The consensus at the end of the workshop was that there is a need to re-target research efforts to resource-poor countries and to prioritize research efforts on children with HIV disease in this setting. It will be important to assess commonalities and variations in oral health needs across geographical and cultural boundaries (for example, organization of regional meetings; creation of regional research centers). We should centralize research efforts in resource-poor countries to support multi-center longitudinal standardized studies to:

• explore the use of OL as a surrogate marker for the initiation of anti-retroviral therapy and prophylaxis of opportunistic diseases—for example, tuberculosis;
  
• identify alternative therapies for OC and other opportunistic infections; and
  
• assess the impact of oral disease on quality of life, and on access to oral care.
  

Finally, it will be essential to integrate oral health research into other health care research programs, to make these research priorities and public health initiatives feasible.

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Advances in Dental Research, Vol. 19, No. 1, 106-117 (2006)
DOI: 10.1177/154407370601900121


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