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Implications of HIV Disease for Oral Health Services

P.G. Robinson

Dept. of Oral Health and Development, School of Clinical Dentistry, University of Sheffield, Claremont Crescent, Sheffield S10 2TA, UK; peter.g.robinson{at}sheffield.ac.uk

	Abstract

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This paper, by means of a quality framework, reviews health services research in relation to people with HIV infection. The relevance of oral health care services to people’s needs is considered in terms of the goal of health services to reduce the burden of disease on the everyday life of the population. Dental services may therefore have a role in primary prevention in the HIV epidemic, passing on information about HIV and promoting health through the early diagnosis and treatment of oral disease. Effectiveness research of oral health care in HIV assesses the usefulness of oral diagnosis, whether care is safe, and whether treatment is clinically effective. Few data are available on the efficiency of services. People with HIV still have problems accessing dental care, due to the volume of care available in relation to their need and acceptability of care. Access problems in the US are compounded by social inequality. Health services research data are particularly sparse in resource-poor countries, and there is a need to translate the available information into treatment guidelines appropriate to these settings. The research community and funding agencies should place greater emphasis on the quality of oral health services for people with HIV.

KEY WORDS: HIV • AIDS • health services research • oral health • dentistry

	Introduction

TOP Abstract Introduction Appropriateness of Health... Effectiveness of Health Care Efficiency Access Equity Acceptability Resource-poor Countries Conclusions and Recommendations References

 
The commissioning and administration of health services can be seen as a question of quality. Not only should the services be available and appropriate to the needs of the population, but they should also be effective in improving the health of the people under their care. We must always recognize that some procedures and services may be of no benefit or may be harmful, and that health resources are limited.

Decisions about health services should be derived from a combination of the values of the society in which they belong, the available resources, and the best evidence on their configuration, policies, and treatments. For these reasons, any appraisal of the quality of health care must consider not only the clinical, social, and economic impact of services, but also the impact of those services on the health system in which they operate. Health services research therefore requires not only data from rigorous randomized-controlled trials, but also data resulting from non-experimental and observational analysis (Jenkinson, 1997).

The quality of an object or service is its ’fitness for purpose’ (Juran and Godfrey, 2002). Within this definition, the quality of a complex item such as a health service can be considered in different dimensions. Maxwell (Table 1) provides a good framework for appraising oral health care for people with HIV, and these dimensions are compatible with similar approaches familiar to colleagues in the United States (Maxwell, 1984; Donabedian, 2003). Frameworks such as these have not often been used with respect to oral health services in HIV infection, but are perhaps reflected in Greenspan’s assertion that efficacy, safety, and cost-effectiveness must be considered when prescribing for the treatment of oral candidiasis (Greenspan, 1994).

	Appropriateness of Health Services

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What is ’health’? The World Health Organization (1946) definition is: ’A complete state of physical, mental and social well-being and not merely the absence of disease.’ The literature on the oral manifestations of HIV virtually ignores this definition, but focuses almost entirely on oral disease and its absence. This research community could do well to consider more the impact of oral disease on people with HIV.

Analysis of the preliminary data suggests that oral disease affects quality of life to a considerable extent in this group of already-sick people. Arendorf et al.(1998) found that more than one-quarter of South African people with HIV had oral discomfort necessitating treatment. In South Australia, patients with HIV experienced more social impact of oral disease than did a comparable sample of the general population (E Coates et al., 1996). More recently, Coulter and colleagues (Coulter et al., 2002) have studied oral-health-related quality of life in a representative sample of 2864 US adults. Their focus was on interference with social activities, food, swallowing, appearance, worry about the mouth, pain, and the use of medication. In multivariate analysis, interference with these activities was worse in people with oral symptoms, in drug users, and in people with less education. Of equal interest, oral health accounted for 1 to 2% of the variance in people’s general health. Very high levels of oral symptoms were also reported in North Carolina among a non-dental sample of 632 people with HIV (Patton et al., 2003).

This type of information has a multiplicity of uses (Robinson et al., 2003). One strategy in the debate of how dental services try to secure resources against competing demands will be to use these kinds of data to demonstrate the broader impacts of the mouth on everyday life. Put simply, your funding agency is more likely to give your clinic money if you can show that 5% of the population cannot eat than if you say that their volume of gingivo-crevicular fluid is elevated.

Assessment of the problems that cause most bother within a community can also be used to plan and configure oral health services. For example, if almost 60% of people with HIV in a community have symptoms of hot and cold sensitivity(Patton et al., 2003), then the most pressing need is for general dental care, whereas the HIV research community (myself included) has focused more on unusual conditions seen in the disease. Information on the health needs of people can also be used to evaluate health services. We should not claim that the management of oral disease in HIV-infected individuals is important to self-esteem, quality of life, and the maintenance of adequate nutritional intake without evidence to that effect. These types of patient-centered outcomes have been used in the evaluation of treatments for HIV disease, but not in relation to oral care (Alston et al., 1999; Miles et al., 2002). More research is needed on the oral-health-related quality of life in people with HIV, and on the effect of oral health care on patients’ experience of disease.

The concept of need is also elusive in relation to the oral health care of people with HIV. What do we really mean when we refer to an individual’s or community’s ’need’ for care? One useful definition of health care need is ’the ability to benefit from health care’ (Culyer, 1995). It follows from this definition that a health care need can exist only when there is an underlying health care problem for which an effective treatment is available.

Based on these points, oral health services might have three roles in the promotion of health in relation to HIV disease: primary prevention in the HIV epidemic, passing on information about HIV and finally, and promoting health through the early diagnosis and treatment of oral disease (this would include providing necessary dental care).

Dental services in the primary prevention of HIV transmission
The role of dental services in reducing the incidence of HIV is largely ignored in the dental literature. We should remember that people with HIV are important partners in prevention; The virus can be transmitted only through them. If they feel abandoned by care services, they are less likely to understand the need for prevention and to be motivated to protect others (MacNeil and Anderson, 1998). This is important in social intervention approaches to HIV prevention, to avoid discrimination against people infected with HIV (Mann and Tarantola, 1996; WHO, 1998).

Choi and Coates (1994) have argued that medical, social, and mental health services for people with HIV are a validated strategy for reducing HIV transmission. Moreover, this approach has greater impact when applied across a community in a variety of services. Colleagues will not need reminding that to develop these community-wide services requires pre-existing organization, the presence of directly affected individuals in academia and public health, and open-mindedness (TJ Coates et al., 1996). This argument has been repeated by Shriver et al.(2000), who talks about access to primary care as a structural factor in HIV prevention not only to reduce infectivity (i.e., viral load), but also to reduce morbidity.

There is one other area of primary prevention of HIV transmission for which dentistry can be congratulated. Despite the millions of surgical interventions undertaken by dentists globally, every day, only a very few clusters of cases are possibly associated with dentistry (Bautista and Orostegui, 1997; Ciesielski et al., 1992). It is not difficult to prevent transmission of HIV in dentistry; nonetheless, we have risen to the challenge on a scale unmatched by colleagues in other branches of health care.

Dental services in passing on information
Twenty-five years into the HIV epidemic, there are still misunderstanding and ignorance about the disease in both developed and developing countries (Stadler, 2003). Dental health workers are well-placed to pass on information about HIV. We have long known that patients see dental practices as a place where they can discuss and receive valuable and trusted information about HIV. The public is willing to discuss AIDS with dentists and will read information we supply. Given the continued epidemic, it is increasingly important for dentists to educate a receptive public about AIDS. This type of information-giving can be effective even if it only increases awareness by passing on information in posters in waiting rooms (Ward and Hawthorne, 1994)

	Effectiveness of Health Care

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The technical aspects of care can be considered in three ways: whether care is safe, whether the diagnoses are useful, and whether the treatment achieves its aim (clinical effectiveness).

Safety of dental treatment
There is a small body of research on the safety of specific treatments in people with HIV that has been systematically reviewed (Bonito et al., 2002; Patton et al., 2002a). Analysis of the available data suggests that complication rates associated with dental treatment in people with HIV are similar to those in HIV-negative people. None of the primary authors called for special precautions in HIV-positive patients who did not have some other indication for doing so. The reviewed data were limited to a small range of treatments (endodontic and exodontic). The consistent indication provided by these data-that care could be provided safely-may have prevented subsequent researchers from studying this topic. While it is impossible to conclude that there is no greater risk of complication after invasive dental procedures, analysis of the data does not provide a rationale for antibiotic prophylaxis or any other special precautions. We must remember the evidence-based mantra that we should not provide an intervention (in this case special precautions) without clear evidence for doing so.

Diagnosis of oral disease
Naturally, oral and dental treatment should be based on accurate diagnosis. In addition to the difficulties of recognizing conventional oral diseases, one also may need to diagnose the diseases associated with HIV. Fortunately, with the exception of periodontal diseases (Robinson, 1998), the clinical diagnosis of oral diseases strongly associated with HIV is relatively straightforward and can be supplemented with laboratory tests.

However, oral diagnosis has wider implications than in the management of local disease. Oral examination has gained greater importance as an indicator of HIV infection with the onset of effective treatments for the underlying disease, especially to those who could benefit from treatment but who do not suspect that they are infected. Early detection of HIV infection improves prognosis and reduces transmission, but, in the US, 30%–40% of cases are diagnosed late (Klein et al., 2003). In some settings, effective risk assessment coupled with clinical examination could increase early detection of the infection.

There are systematic reviews on the specific topics of oral conditions as indicators of seroconversion and of severe immunosuppression (Bonito et al., 2002). Evidence for selected oral lesions as markers for seroconversion is limited to a single study of candidiasis. The low prevalence of oral disease in very early HIV disease effectively rules out their use as markers for seroconversion. Data from ten articles were included in the review on whether oral conditions indicate severe immunosuppression. In summary, oral examination is not a good replacement for serology to detect HIV progression to the next stage of disease, and is of little benefit in a clinical setting in anything other than opportunistic assessment.

However, the value of any diagnostic test is dependent on the purpose to which the test is put, the prevalence of the disease in the population, and the resources and an infrastructure to act on the information. In some respects, then, the use of oral examination to detect or ’stage’ HIV disease may be of less value in developed countries where these resources are available, because these same countries can also have serological assessments that may be more valid and precise.

It is therefore in the developing world that oral examination may provide more benefits as a screening tool for HIV infection (Robinson et al., 1998). Ninety percent of HIV-positive women in developing countries do not know their HIV status (Phoolcharoen and Detels, 2002), and yet targeting antiretroviral therapy in pregnancy may increase its cost-effectiveness. However, only limited data are available on the predictive value of oral disease in developing countries (Muzyka et al., 2001; Adurogbangba et al., 2004). These data and those collected in developed countries are not readily generalizable to other settings.

Given the potential impact on the health care and quality of life in patients with HIV, attempts to provide adequate training for primary care physicians in this area seem wise (Patton et al., 2002b). Sifri and colleagues developed a core curriculum on oral health in HIV disease that is organized in a manner that is clinically relevant for primary care physicians (Sifri et al., 1998), and a structured risk assessment algorithm has been devised to encourage dentists who notice specific conditions or become aware of risky behaviors to talk with their patients about HIV/AIDS (Mulligan and Lemme, 2001).

However, we should not underestimate either the skill or the application required to diagnose oral diseases in a busy clinic after a modicum of training. In a recent study of doctors in Uganda, the doctors could diagnose oral disease with a sensitivity of 0.61 when compared with dental students. However, over the following three months, doctors failed to diagnose a single case of HIV-associated oral disease in a series of 259 patients. Health care workers in developing countries can be trained in the diagnosis of oral manifestations of HIV, but diagnostic validity decreases with time from training. Sustained diagnostic validity may be possible with more effective training, and if oral diagnosis formed an integral part of patients’ health care, rather than part of a research project (Vernazza and Young, 2004).

Clinical effectiveness
Concerns about the harm and effectiveness of treatment have driven the move toward evidence-based care. Evidence-based dentistry provides us with explicit algorithms for searching and appraising evidence on the effectiveness of care. Unfortunately, a simple search for systematic reviews and randomized controlled trials of oral care in HIV infection reveals how, as a research community, we have let down our clinical colleagues. Treatments for oral diseases seen in HIV infection remain largely untested, and the robust data that evaluate oral care in HIV disease can be summarized in a few short paragraphs (Table 2).

Even in South Africa, a country most severely affected by HIV, 16 of 20 senior officers for HIV/AIDS programs and/or oral health organizations reported that there were no existing oral health policies on HIV/AIDS in their health care institutions or organizations. None of the interviewees knew of any specific protocols on oral care in HIV/AIDS (Ogunbodede and Rudolph, 2002).

	Efficiency

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My searches have been unable to locate data on the cost-effectiveness of oral treatment. Again, this finding is in contrast to the growing body of economic data in the medical care of HIV disease (Holtgrave, 2002; Yazdanpanah et al., 2003).

The comparison with medicine is particularly important because, as we know, dentistry must compete with HIV prevention and treatment programs for the scarce resources that are available. For example, a systematic review of the cost-effectiveness of HIV/AIDS interventions in Africa estimated that a case of HIV/AIDS could be prevented for $11 by targeted condom distribution with treatment of sexually transmitted diseases. Single-dose nevirapine and short-course zidovudine for prevention of mother-to-child transmission, voluntary counselling and testing, and tuberculosis treatment cost under $75 per disability-adjusted life year (DALY) gained (Table 3) (Creese et al., 2002). In industrialized countries, the cost of preventing one previously unknown HIV infection is between US$460 and US$1.2 million, strongly depending on prevalence (Schrappe and Lauterbach, 1998).

	Access

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If we assume that dental care delivers benefits to patients, it seems likely that regular visits are required for the best effect. Regular dental attenders with HIV receive more diagnostic and preventive care and less restorative and surgical treatment than do irregular attenders (Hastreiter and Jiang, 2002). This finding is consistent with our knowledge of the general population, but indicates the value of patients’ ability to access dental services.

The concept of access to care encompasses the volume of care available in relation to the volume of need in the population, the affordability and acceptability of care, and the way services are located and organized to receive patients (Penchansky and Thomas, 1981). Many countries have determined that most care of people with HIV should be provided within mainstream services, and so estimates of dental treatment need and availability have not been regarded as a priority. Most studies of the nature and volume of dental care required by people with HIV have been crude estimates of the proportion of people with HIV who perceive a need for care, and have not linked population needs to the supply of services.

While crucial for the planning and evaluation of services, this type of information is parochial, insofar as the realistic and perceived needs of a community will be determined by local factors, such as background levels of health, expectations about health and services, and the availability of resources. Such research is therefore rarely generalizable.

Planning models have estimated that patients with HIV living in the US require 1.9 to 3.4 dental visits/year (Lenker et al., 1993), but there have been long-standing problems with access to dental care in several countries. These problems persist even in industrialized countries. Only about 40% of people with HIV in the US had seen a dentist in the preceding six months (Coulter et al., 2000). In Southern Europe and the US, a similar proportion, 40%, of people with HIV have unmet dental treatment needs (Marx et al., 1997; Baratta et al., 2000). In Patton’s study of 632 HIV-infected adults who visited a medical clinic, 65% had unmet dental needs in the preceding three years (Patton et al., 2003).

The response of dentists to patients with HIV has been reviewed recently (Hodgson et al., 2006) and varies with geographical location. There appears to be a trend toward greater acceptance of infected patients with time. For example, the proportion of Danish dentists willing to treat patients with HIV rose from 56% to 79% between 1986 and 1992 (Scheutz and Langebaek, 1995). Correspondingly, younger dentists are more likely to accept patients with HIV than are older dentists, and a recent study of US dental students found 83% willing to treat (Seacat and Inglehart, 2003; Crossley, 2004). Problems persist, however: Only 45% of respondents to a survey in northwest England would accept HIV+ patients without hesitation (Crossley, 2004).

There is still work to be done on the attitudes and behavior of dentists toward people with HIV. But this is not a simple educational task. A significant body of research consistently shows that non-professional attitudes, the perceived norms of colleagues, low optimism scores, and low levels of comfort with homosexuality were the best predictors of refusal of treatment to HIV-infected patients (Kunzel and Sadowsky, 1991; Bennett et al., 1993; Sadowsky and Kunzel, 1996). Dentists are still worried about personal danger. In Mexico City, as recently as 1999, 79% of dentists perceived the risk of HIV infection as "considerable" to "very strong" (Maupome et al., 2002). In addition, dentists are concerned about loss of staff and other patients (Crossley, 2004).

In the past, there has been an over-reliance on naïve Knowledge-Attitudes-Behaviors models of education. Such models that assume that providing dentists with knowledge will change their attitudes and their behaviors will inevitably follow. In reality, attitudes to death, to sex, and to risk are deeply held views that are immune to dry facts. If teaching about HIV is to modify the attitudes and behaviors of dentists, it requires careful planning and consideration of all the factors that shape the way dentists feel and act. Learning should be interactive and discursive. It should consider ethics and attitudes toward patients and should involve both patients and counselors (Carter et al., 1997).

	Equity

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In most of the world, particularly Africa, AIDS has always been a disease of poverty; it has become so in the United States and is moving that way in Europe. In addition, HIV disease both reduces and makes demands on income. It is essential, then, that the availability of oral care for people with HIV be fair—that is, equitable. Unfortunately, that is not the case. All the available data are from the US and consistently indicate greater need and less service use among the most disadvantaged (Table 4) (Marx et al., 1997; Shiboski et al., 1999; Coulter et al., 2000; Duran et al., 2000; Heslin et al., 2001; Ramos-Gomez, 2002; Menke et al., 2003; Patton et al., 2003). This situation is exacerbated by advanced disease (Dobalian et al., 2003; Patton et al., 2003).

	Acceptability

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Given the stigma of HIV and its impact on the lives of those affected, the acceptability of services would seem to be important. Yet the acceptability of care to patients with HIV infection can compound other access difficulties (Robinson and Croucher, 1993). There are several ways of assessing acceptability. Perhaps the most obvious is measurement of satisfaction, although this has been reported only occasionally (Robinson and Croucher, 1994; Croucher et al., 1997). In addition, patient satisfaction surveys may under-represent the views of the most dissatisfied patients, who do not attend subsequent appointments.

Other indicators of the acceptability of care include non-attendance at appointments and disclosure of HIV status (Robinson et al., 1994). Charbonneau and colleagues (1999) found that although 83% of people with HIV preferred their dentist to be aware of their status, 25% had never disclosed it to a dentist. Common reasons for failure to disclose include fear of refusal or some other negative attitude, and concerns about confidentiality. These findings are compatible with those of the review of access and indicate that more attention should be paid to the professionalism of dentists.

One response to access problems has been the development of clinics dedicated to patients with HIV. This notion is popular among dentists, perhaps because the existence of such allows them to avoid their ethical responsibilities to patients, although it may add to the stigmatization of patients. Patients with HIV are divided about preferences for dedicated or mainstream care. In the UK, 45% preferred general practice compared with 48% in favor of specialist clinics (Gallagher et al., 1998). In the US, a telephone survey of predominantly urban gay men found that two-thirds of those who had seen a dentist had attended mainstream facilities. It may be that, in this population, there was a well-established network of ’HIV-friendly’ dentists (Barnes et al., 1996). Analysis of these data, cumulatively, supports policies encouraging people with HIV to go to the dentist with whom they feel most comfortable (Barnes et al., 1996). However, many health care systems may not be able to afford dedicated clinics.

	Resource-poor Countries

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Most of the research referred to in this presentation has been carried out in the developed world. While there is little information available in these settings, still less is useful for the countries that bear the greatest burden of HIV and AIDS in the developing world. Measures need to be tailored for the poor countries, to make them relevant in places with a high frequency of HIV infection and minimal resources (Matee et al., 1999).

It must be possible to develop treatment guidelines that are consistent with the highest standards of quality of care, but that have the added advantage of using technologies and resources appropriate to resource-poor settings. For example, we know that necrotizing gingivitis has an incidence of around 2% in HIV-infected people and can be debilitatingly painful. The standard of care in the UK is for a dentist to debride the lesions and prescribe metronidazole. There is common anecdotal evidence that patients can self-treat this disease by cleaning with wooden interdental sticks in the absence of antibiotics and dentists. Could this much simpler regimen be translated, tested, and disseminated for wider use?

Approaches such as these should have the advantage of facilitating much more effective use of clinical and non-clinical staff. The WHO has suggested that physicians can supervise clinical teams but delegate day-to-day management and adherence support tasks to other workers (World Health Organization, 2004). Could not a similar approach be tested in dentistry, particularly to a disease like NUG, which responds so readily to treatment? Guidelines developed from this more appropriate research would fill the gaps in availability and access, allowing for a shift toward care and support for those living with HIV/AIDS (Ogunbodede and Rudolph, 2002).

	Conclusions and Recommendations

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This paper has considered the oral health service implications of HIV disease. A great deal is known about the pathology of oral disease in HIV infection, and we can all take pride in the way dentistry has risen to the challenge of this disease. Despite that, more consideration is needed of the purpose of dental services in HIV infection and in general. This will affect our judgments of their quality.

The research community, funding agencies, and service providers must place more emphasis on the appropriateness, effectiveness, efficiency, accessibility, acceptability, and equity of dental services. This work needs much more effort and much more resources. This work is neither sexy, expensive, nor ’high-tech’ laboratory science. Moreover, much of it will not be generalizable from one setting to another. Inevitably, then, there will be some duplication of effort if, for example, the solutions to oral care problems differ in affluent and resource-poor countries.

Research on the value of oral conditions as markers of HIV infection should continue, but its real value may lie in areas that lack the resources and infrastructure for frequent serological assessment. Since the usefulness of tests depends very much on the prevalence of disease in the community and other local factors, this research is probably of more value if carried out in these environments.

	Acknowledgments

 
I thank Drs. Tim Hodgson, Sue Naidoo, and Lauren Patton for kindly sharing material for this review. Drs. Barry Gibson and Zoe Marshman reviewed early drafts of the manuscript.

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