Promoting early HIV diagnosis and entry into care
Valdiserri, Ronald O.; Holtgrave, David R.; West, Gary R.
From the US Centers for Disease Control and Prevention, Atlanta, GA 30333, USA.
Correspondence to: Dr Ronald O. Valdiserri, Deputy Director, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road (MS E07), Atlanta, GA 30333, USA. Tel: +1 404 639 8002; fax: +1 404 639 8600
Received: 14 May 1999; revised: 16 August 1999; accepted: 27 September 1999.
Current antiretroviral therapeutic guidelines reflect the growing consensus that the early initiation of treatment for HIV is associated with virological, immunological, and clinical benefits. However, in the USA many persons with HIV are tested relatively late in the course of their infection, and then, often only because of the presentation of symptomatic disease. Similarly, a large proportion of HIV-infected Europeans are undiagnosed before the onset of AIDS. Even when individuals suspect that they may have been exposed to HIV, they often delay seeking testing, sometimes for periods longer than one year[4,5]. Nor does timely testing for HIV necessarily guarantee prompt entry into medical treatment. Delays between learning about a positive test result and seeking primary care have been reported in the range of 1-5 years[6,7].
Clearly, recent advances in the treatment of HIV disease are neither a cure nor a panacea. In fact, a minority opinion holds that the administration of highly active antiretroviral therapy (HAART) to persons who may have been infected with HIV for several months or longer could be detrimental, and that current regimens should be reserved until the onset of symptoms or laboratory evidence of reversible immune system damage.
We can expect to see HIV therapeutic options and approaches evolve over time. However, regardless of how recommendations to initiate antiretroviral therapy might change in the future, early diagnosis of HIV infection will remain preferable to late diagnosis. From a primary care perspective, the early diagnosis of HIV infection has the potential to facilitate entry into stable care systems, optimize clinical outcomes, and improve healthcare system planning capabilities.
In addition to the individual level, medical benefits of early diagnosis and treatment of HIV infection, there are also potentially significant public health benefits. Encouraging the early diagnosis and treatment of persons infected with HIV has the substantial possibility of reducing further the spread of the virus. Reports from both developing and industrialized countries [10,11] show that many persons will reduce sexual risk behaviors after a diagnosis of HIV infection, an important contribution towards reducing transmission. The concept of ‚early intervention‚ was elucidated during the first decade of the AIDS epidemic by Francis and colleagues, and has gained renewed momentum in recent years with the advent of HAART, which has been shown to reduce circulating levels of HIV RNA in plasma, lymphoid tissues, and semen. If treatment advances eventually reach a state at which they can render persons non-infectious, the public health benefits of early HIV diagnosis and treatment will become even more pronounced.
Although HIV prevention and treatment capacities vary across different socioeconomic and geopolitical settings, promoting the early diagnosis of HIV infection should be a component of all comprehensive approaches to addressing AIDS, for the reasons stated above. Even in countries where antiretroviral treatment options are severely limited, important contributions to health can be achieved through the diagnosis and treatment of sexually transmitted diseases (STD), tuberculosis (TB), and other opportunistic infections among HIV-infected persons.
This review will summarize what is known about variables that influence early HIV diagnosis and entry into care, and suggest facilitative strategies. Although a majority of the references reflect the US experience, they are probably relevant to the industrialized countries of western Europe. Also, several of the citations specifically address the unique issues of promoting voluntary HIV counselling and testing in developing world settings.
Trends in early HIV diagnosis in the USA
Testing for HIV antibodies takes place in a number of settings and under a variety of circumstances. HIV testing can be mandatory (e.g. military applicants and, in some countries, commercial sex workers) or voluntary. Testing can be conducted in publicly funded (e.g. government-supported clinics) or private settings (e.g. physicians‚ offices). The most recent permutation of HIV testing is the so-called ‚home‚ test kit, in which an individual purchases a kit, receives pre-test counselling by ‚phone or pamphlet, submits an oral fluid or dried blood spot sample by mail, and calls a toll-free telephone number to receive the results.
Surveys of American adults [17,18] indicate that, excluding blood donations, most voluntary testing takes place in medical care settings such as doctors‚ offices, managed care organizations, and hospitals. Typically, HIV testing in medical care settings, excluding blood banks, accounts for over half of all adult voluntary testing in the United States. A smaller percentage of HIV testing in the USA (some 2.6 million tests in 1996) takes place in publicly funded HIV counselling and testing sites, including clinics for the treatment of sexually transmitted diseases, family planning clinics, and drug treatment centers.
Although not extensively evaluated, it has been suggested that public and private sector testing may differ in terms of service quality, with higher rates of pre- and post-test counselling taking place in public sector settings. Furthermore, because of the venues in which publicly funded testing is offered in the USA (e.g. STD clinics and drug treatment centers) clients attending these sites are likely, on average, to be at higher risk from HIV compared with many of the patients receiving routine medical care services in the private sector. One study from Oregon, comparing public and private sector testing in the late 1980s and early 1990s, found that public clinics performed only 37% of all tests in that state, yet accounted for nearly two-thirds of all new HIV infections diagnosed in asymptomatic persons who self-initiated testing.
HIV seropositivity rates have decreased in publicly funded US sites in recent years. Whereas 4.4% of tests performed in publicly funded counselling and testing sites were positive in 1989, this number had dropped to 1.5% in 1996. This decrease reflects a significant increase in testing volume between 1989 and 1992, and a substantial number of high-risk seronegative persons who are being repeatedly tested in these settings.
A telephone survey of nearly 14 000 US adults conducted in the early 1990s  found that almost 60% of those at highest risk of HIV infection had not yet been tested. More recent data show an increase in HIV testing over time. In a population-based survey of American adults, trends in voluntary HIV testing were documented to have increased from 14 to 23% between 1993 and 1996. However, a greater increase in testing was seen among those who perceived themselves to be at low or no risk from HIV, compared with those who considered themselves to be at medium or high risk from HIV. Data continue to indicate the need for test promotion, with nearly half of US adults who report risk of HIV infection never having been tested.
It is estimated that between 650 000 and 900 000 persons in the United States are infected with HIV. Of those infected, as many as two-thirds may be aware of their positive serostatus. Conversely, as many as a third of HIV-infected persons may be unaware that they are infected; hence they are more likely to transmit virus because they are less likely to have adopted risk-reduction practices (e.g. consistent condom use). Nor are they able to take advantage of the potential benefits of early diagnosis and treatment. In a recent assessment of when (i.e. at what point in time) Europeans with AIDS learned that they were infected with HIV, it was demonstrated that a large proportion of HIV infections were undiagnosed before the onset of AIDS; this was especially pronounced for heterosexual men who were not injecting drug users (IDU). In a population-based sample of American adults with AIDS, only 22% met the criterion for early detection, which was defined as the recognition of HIV seropositivity more than 5 years before the diagnosis of AIDS.
Trends in early treatment for HIV disease in the USA
A national decline in AIDS deaths was first observed in the United States in 1996, as a result of improvements in medical care, the use of antiretroviral combination therapy, and increasing use of prophylactic drugs to prevent opportunistic infections. Similar declines have been reported in several western European countries, also attributed to the widespread use of combination antiretroviral therapies.
In the United States, diagnosed AIDS-defining opportunistic infections decreased 6% during 1996 compared with 1995, and deaths among persons reported with AIDS declined 23% in that same time period. However, these declines were not evenly distributed, either by sex or race/ethnicity; women and black people did not demonstrate declines in rates of opportunistic infections or death as marked as those observed for men and white people. This is probably partly due to differences in access to and usage of treatment for HIV.
Siegel and colleagues  found that nearly a quarter of the 84 seropositive women they studied in New York City waited more than 6 months after being informed of their HIV infection to seek medical care. Even more striking was the determination of Samet et al.  that 32% of 189 seropositive clients seeking primary care for the first time had waited more than 2 years after an initial positive serological test for HIV.
Variables influencing early HIV diagnosis and entry into care
Utilizing a framework first developed to classify barriers to prenatal care, it is possible to characterize the variables that influence early diagnosis and entry into care for HIV disease along three major axes: sociodemographic; attitudinal and behavioral; and systems-related. The majority of published studies tend to focus on HIV test-seeking behaviors rather than medical or help-seeking behaviors.
Findings related to sex, adolescence, race/ethnicity and socioeconomic status are presented below.
Researchers have noted that a substantial proportion of women at risk of HIV infection have either not been tested[26,34], delayed seeking testing[5,6,29,35], or have failed to obtain results if they were tested. However, Miller and colleagues  found that the majority (64%) of 470 Hispanic and African-American women attending an inner-city US family planning clinic accepted HIV testing, and that most of the women tested (87%) returned for their results. Their rates may have been higher than those found in other family planning settings because of the non-random nature of their client sampling.
In a cross-sectional study of HIV testing patterns among 131 low-income African-American mothers in Oakland, California, , 41% of the women reported that they had been tested for HIV, 18% more than once. No associations were found between reporting a past HIV test and a woman‚s marital status, level of education, type of health insurance, or primary source of healthcare. Women who had been tested were more likely to report a greater number of sexual partners within the past 5 years, and not having used a condom during their last episode of intercourse. Similarly, Heckman et al.  found that women who were more likely to have been tested for HIV in the past year were younger, perceived themselves to be at risk of HIV infection, reported more conversations with peers about AIDS concerns, and had condoms readily available.
In America, results from an annual national probability survey  revealed that from 1991 to 1993, the proportion of women aged 18-44 years who had ever been tested for HIV increased from 19 to 32%. In both 1991 and 1993, higher percentages of black and Hispanic women reported having been tested for HIV compared with white women. Trends suggest that the proportion of women being tested for HIV in the USA is increasing, but there still remain high-risk and infected women who are unaware of their serostatus.
With regard to delays in seeking medical care after the diagnosis of HIV has been made, it has been suggested that women, as traditional care providers, may be faced with more pressing and immediate needs, including childcare, thus ignoring their own medical care. A review of health services use by urban American women  revealed that nearly 20% of HIV-infected women who had CD4 cell counts of less than 200 μl had never taken Pneumocystis carinii pneumonia (PCP) prophylaxis, thus reinforcing the notion of suboptimal HIV care among HIV-infected women. In a cohort study of 2864 HIV-infected US adults enrolled in medical care, women fared worse than men on most measures of medical service and pharmaceutical utilization. However, many of these effects were not independent of insurance status and race/ethnicity.
It is estimated that as many as one in four new HIV infections in the USA occur in those younger than 22 years of age. However, adolescent populations tend to be underserved by HIV counselling and testing services in venues that are designed primarily for adult populations, and many adolescents who are infected with HIV are identified late in the course of their infection, often when they become symptomatic. It has been shown, however, that adolescents who report a history of HIV testing are more likely to be at risk compared with those who have not been tested. A survey of 2548 Colorado students in grades 9-12  revealed that HIV tested adolescents were more than three times as likely to have injected drugs and twice as likely to have engaged in sexual intercourse compared with adolescents who had not been tested. However, more than a quarter of adolescents not tested reported at least one behavior that could put them at risk from HIV. Similarly, among 275 adolescent and young adult clients of an inpatient drug detoxification program in Massachusetts, over half (51%) had never been tested for HIV, despite high levels of risk behavior, including injecting drug use and sex with IDU.
When adolescents are tested for HIV, they may not return to learn their results. In a review of US publicly funded testing sites during 1990, persons aged 13-19 years old were half as likely to return for test results compared with clients who were aged 30-39 years. A review of the records of 4017 teenagers, attending publicly funded HIV counselling and testing clinics in Houston, Texas during the years 1990, 1991, and 1992, demonstrated that the majority (66%) failed to return to obtain their results and receive post-test counselling. Even after a diagnosis is made, HIV-infected youths often find themselves in unstable living situations, which contribute to difficulties in accessing primary care for HIV disease.
Race and ethnicity
Research studies on the associations between race/ethnicity and HIV testing and treatment-seeking behaviors have tended, in the USA, to focus primarily on African-American and Hispanic populations. National surveys conducted in the USA in the late 1980s and early-mid 1990s [17,26,50,51] showed that African-Americans and Hispanics were more likely to report having been tested for HIV compared with white people. However, in a population-based sample from Los Angeles County, Sorvillo and colleagues  documented that African-Americans and Latinos were less likely to have their HIV infections detected early, compared with white clients. Similarly, in the United Kingdom, among 4127 adults diagnosed with AIDS between 1989 and 1992, persons who were non-white (race/ethnicity not specified) were more likely than others to be unaware of their HIV infection before they were diagnosed with AIDS.
A nationally representative survey of 2717 heterosexual African-American adults conducted in late 1990-early 1991  revealed that whereas 22% reported some risk of HIV infection, of those, only 24% had been tested for HIV. Among attendees of US clinics for the treatment of STD, African-Americans have been reported to be more likely to refuse HIV testing, to report not having been tested in the past, and to fail to return for their test results if they are tested[48,56,57], when compared with white clients. Test refusal and failure to return for results has been associated with a number of factors, including previous testing episodes, fear of learning positive results, and perceptions of low risk[54,55]. In a study of 952 clients voluntarily entering public alcohol treatment centers in San Francisco in 1990-1991, African-American and Hispanic clients were significantly less likely to report previous HIV testing, when compared with whites. Taken in aggregate, these data suggest that whereas, on average, some racial/ethnic minority populations report more frequent testing than whites, there is also evidence that a substantial number of at-risk racial/ethnic minorities have not yet been tested for HIV, or test late, after the presentation of symptoms.
Although the majority of the studies cited treat racial/ethnic designations as if they were homogeneous, the reality is that they are not. In the USA, information about HIV testing and treatment-seeking behaviors among specific ethnic subgroups is less than adequate, but suggests that there may be distinct differences. For example, it has been reported that testing behavior varies among Hispanic subgroups, with Mexican-Americans and Cuban-Americans being less likely to be HIV tested compared with Puerto Ricans. In the USA, even after diagnosis and entry into care, African-Americans and Hispanics report more deficiencies in HIV care, compared with whites, although many of these disparities can be explained by differences in health insurance coverage.
Several studies [39,50,51] have demonstrated an inverse association between income and HIV testing in the USA, i.e. persons of lower income or at poverty level are more likely to have been tested for HIV. It should be noted, however, that higher income and educational levels have been associated with a history of earlier HIV diagnosis (i.e. recognition of seropositivity 5 years before the diagnosis of AIDS). Also, in an American survey of AIDS knowledge and attitudes, persons with higher educational levels were more likely to have knowledge of the antiretroviral agent zidovudine (AZT).
Regarding the treatment of HIV infection once a diagnosis has been made, lower socioeconomic status is widely perceived to be an important variable mediating access to healthcare and hence, survival. Not surprisingly, Shapiro et al.  found that HIV-infected American adults were more likely to report suboptimal care if they were uninsured or had Medicaid (medical care for those unable to afford regular medical services, financed through US state and federal governments) compared with those with private insurance. In America, declines in AIDS incidence and deaths have been greater for whites than African-Americans and Hispanics. This is interpreted, partly, as a manifestation of economic disadvantage among these populations, and as such, unequal access to healthcare services. Schwarcz and colleagues  found that non-white and uninsured HIV-infected persons in San Francisco were significantly less likely to have received primary PCP prophylaxis. In a ‚representative case method‚ sample of 84 HIV-infected women in New York City, Siegel et al.  reported significantly higher proportions of African-American and Puerto Rican individuals receiving Medicaid and a significantly higher proportion of whites in the study having private sources of medical coverage.
Shorter HIV survival in persons with lower incomes may not solely be a manifestation of access to medical care. Hogg and colleagues from Canada  showed that even in circumstances in which access to healthcare is not a significant discriminator (i.e. within a ‚universal healthcare system‚), lower socioeconomic status was associated with shorter survival after HIV infection.
Attitudinal and behavioral variables
Findings related to the perception of risk, the fear of learning positive serostatus, and behavioral risks are presented below.
Perception of risk/fear of learning positive serostatus
The perception of risk has been noted to have a bidirectional influence on HIV testing behaviors. Namely, the perception of risk can act either as a facilitator or a deterrent to HIV testing. Among US persons with a history of high-risk behaviors who delayed or did not seek HIV testing, a commonly cited reason is that they did not perceive that they were at risk of HIV infection[54,55,63,64], suggesting that accurately perceiving a risk for HIV may be a powerful testing motivator. An example of this presumption is an analysis of over 50 000 client visits to 25 STD clinics in the state of Illinois; clients who perceived themselves to be at risk from HIV were more likely than those who did not to accept pre-test counselling, to agree to be tested for HIV, and to return for the test results. Similarly, in a study of voluntary HIV test acceptability in rural Tanzania, the main reason stated for declining an HIV test was the perception of not being at risk from AIDS.
However, it has also been shown that when persons perceive that they may be at high risk of being infected with HIV, they may be hesitant to seek testing, often because they fear learning that they are infected with HIV[54,55,63,64]. In a rural southern state in the USA, this bidirectional influence varied by race; non-whites who perceived that they were at high risk from HIV reported less testing than non-whites with a low perceived risk of HIV infection. In the same study, whites who perceived that they were at high risk of HIV infection tested twice as often as white participants with a lower perceived risk.
In addition to its association with testing behavior, the perception of risk has also been reported to influence medical care seeking after a positive HIV diagnosis. Among 189 HIV-infected persons from the northeastern USA, being unaware of HIV risk at the time of a positive diagnosis was found to be one of three major client characteristics predicting delays in presentation to primary care.
Man to man sexual contact
Although it has been observed that gay men with high, self-reported sexual risk are more likely to be repeatedly tested for HIV[67,68], other members of this population may be unaware of their serostatus. In cross-sectional data collected in the United States and Canada, from both community-based and household venues[69,70], it was found that between 32 and 47% of gay men sampled did not know their current HIV serostatus. Among gay and bisexual men at risk of HIV infection, the fear of learning about a positive test is a commonly cited reason for delaying or avoiding HIV testing[64,69-71]. Other reasons for not testing include concerns about confidentiality/desire for anonymity[64,69,70,72], perceptions of being in good health and therefore not requiring the test[69,70], and a previous bad testing experience. Particularly interesting is the observation that gay men who have higher levels of socialization in gay identified venues, and those who are better integrated into the gay community  are more likely to be tested for HIV.
Information about treatment-seeking behaviors is less available. In 1992, Stall and colleagues  determined that among a cross-section of 2593 gay and bisexual men from the western and northwestern United States, 107 were known to be HIV positive but were not under treatment. However, lacking a healthcare provider accounted for only 22% of these 107 men. In that study, a major predictor of whether HIV-infected men were under treatment or not was beliefs about the efficacy of taking antiviral agents in promoting health. Concerns about the efficacy of antiviral medication may no longer have as substantial an impact on treatment-seeking behaviors as they did in 1992. An anonymous questionnaire completed by gay men in London in 1997  showed that nearly 70% of the 1800 respondents agreed that HIV treatments are ‚much better than they used to be‚. In fact, we can assume that the testing and treatment-seeking behaviors of other at-risk groups may also have been influenced by pervasive media accounts of advances in HIV therapies.
Injecting drug use
Among IDU in the USA and the UK, having been in drug treatment is a major predictor of HIV antibody testing[76-78]. A history of incarceration or treatment for a sexually transmitted disease also predicts HIV testing among IDU. Like many other groups, the presence of symptomatic HIV disease is strongly associated with HIV testing among IDU. In a review of over 72 000 testing episodes in US publicly funded sites, the highest rate of HIV infection among IDU was found among those clients being seen in physician office sites, perhaps reflecting persons who were seeking care for symptomatic HIV disease. Among 610 HIV-infected IDU in Baltimore, Maryland, the single most important predictor of healthcare utilization was the presence of two or more HIV-related symptoms.
Systems-related variables include an examination of the format and venue of HIV counselling and testing services; provider practices; policies that influence testing practices; mechanisms for client referral; and contextual issues.
Test characteristics: systems and site
Although research in this area is not extensive, the characteristics of a testing system (e.g. the process one goes through to acquire testing services, the type of diagnostic test used, the process required to receive test results) as well as where the test is offered can influence HIV test-seeking behaviors and test-receiving outcomes.
Failure to return for HIV test results has been documented in both industrialized  and developing world  settings. In a population-based, probability sample of US households, it was estimated that more than one in 10 persons tested for HIV in 1994 did not receive their results. However, when a rapid HIV test  is substituted for the standard enzyme immunoassay test, the majority of clients can receive final results during their initial visit[11,83]. In an African study of voluntary counselling and testing for married couples, the use of rapid HIV testing increased the number of persons who learned their test results, and was associated with less fear, compared with couples who received HIV results in a subsequent, post-test counselling visit.
Recently, another major change has been made in HIV testing systems in the United States with the introduction of home collection testing, in which an individual purchases a test kit, self-collects and mails a finger-stick specimen for testing, and calls a toll-free number in a week or so, to learn the results of the test. Evaluations to date indicate that the actual number of persons using home collection testing in the USA has been lower than expected[85,86]. This may be because of the high price of the test (US$40-50), aversion to finger stick, or the 3-7 day wait for results.
The use of oral mucosal transudate for HIV antibody screening and confirmatory testing has been shown to be an accurate alternative to serum testing, and increases the possibilities for expanding the availability of HIV testing beyond traditional facility-based sites into community venues, thus potentially increasing the acceptability to clients who would not access these services in clinic-based settings. When pilot tested in a US gay bar setting, it was found that 22% of the men who accepted the oral fluid testing had not previously been tested for HIV. Earlier testing systems that screened for IgG-specific antibodies in the saliva of STD clients and commercial sex workers in Zaire found that study participants preferred saliva collection to venipuncture.
A number of reports [90-92] show that the subject of AIDS, including HIV testing, is not always adequately discussed during encounters between healthcare providers and patients. In the USA, more recent medical graduates, who have learned about HIV/AIDS during their training, appear more likely to discuss these issues with their patients. Clients in a variety of healthcare settings are more likely to accept HIV testing if it is offered by providers who have a ‚pro-testing‚ attitude, and stress the potential benefit of testing for the welfare of clients, their partners, and offspring. This has been repeatedly documented in perinatal care settings in the United States[94-96], where provider attitudes and women‚s perceptions of how strongly their providers encourage HIV testing have emerged as significant predictors of perinatal testing. However, in other perinatal settings, both in the US  and in England[98,99], patients‚ fear and low perception of risk continue to impede the acceptance of HIV testing.
Although the quality of a provider‚s pretest counselling may influence a client‚s willingness to accept HIV testing, few studies have explicitly examined this relationship. One that did so studied African-American women who received AIDS information specifically framed in a culturally relevant videotape; they were more likely to accept HIV testing compared with those who received a standard public health message.
Provider characteristics may also influence care-seeking behaviors. Even when controlling for age, sex, mode of HIV transmission, type of health insurance, income, education, and place of residence, race has been shown to be strongly associated with the receipt of drug therapy for HIV disease. The reasons for these racial differences are not entirely clear, and may partly reflect provider characteristics and biases. A recent qualitative study of American adolescents  found that teenagers‚ impressions of their providers‚ ‚attitudes‚ were major factors in bringing young people into or deterring them from healthcare; this was especially true for sexual healthcare, including HIV testing.
Policy level characteristics
In addition to the physical attributes of a testing system and the practices of the providers who offer HIV testing, a number of policy considerations can influence both HIV test-seeking and care-seeking behaviors. Among the most salient of policies affecting HIV testing is the availability of anonymous testing.
Anonymous testing is offered as a means of encouraging HIV testing in both industrialized and developing world settings[11,20,103]. Persons who are tested anonymously are not required to provide their names. In Uganda‚s voluntary HIV counselling and testing program, anonymity is cited as a critical component for establishing trust and ensuring client demand for services. Studies from the industrialized world [69,104,105] suggest that men who have sex with men (MSM) are more likely to seek HIV testing when it is offered anonymously. When persons seeking anonymous testing in California were surveyed, 40% reported that they would have avoided HIV testing had it not been available anonymously. A national sample of Americans reporting HIV risks  indicated that persons with less education and lower incomes were more likely to be willing to be tested for HIV if the results could be known only to them.
In South Carolina, where anonymous HIV testing is not available, a small proportion of residents sought testing in neighboring states, where anonymous services can be found. Although only 75 residents were tested out-of-state during the study period, compared with the 57 137 who were tested in-state, they were significantly more likely to be HIV positive (12 versus 3%).
Two American studies [109,110] considered the impact of restricting the availability of anonymous HIV testing services in North Carolina to 18 out of 100 counties. Kassler and colleagues  found that eliminating anonymous testing in 82 North Carolina counties caused a small decrease in testing among some ‚possibly high-risk men‚. Picciotto-Hertz et al.  found that testing increased throughout North Carolina in the 16 months after restriction. However, overall testing increased 64% in those counties retaining anonymous testing options compared with 44% increases in those counties that had eliminated the anonymous option.
One US study  suggested that anonymous testing may even contribute to early HIV medical care. In a probability sample of 835 new AIDS cases reported to US health departments between May 1995 and December 1996, it was shown that persons tested anonymously experienced a longer period of time in HIV-related care before an AIDS diagnosis (918 days) when compared with those tested confidentially (531 days). This association remained significant even after adjusting for age, sex, race/ethnicity, education, income, insurance statues, HIV exposure group, and whether the respondent had a regular source of care, or symptoms, at the time of the HIV test.
Closely aligned to the subject of the availability of anonymous HIV testing is the issue of name reporting of HIV-seropositive individuals to governmental health authorities. In the USA, various surveys have assessed the willingness of high-risk clients to seek HIV antibody testing in situations of mandatory HIV reporting. (As of August 1999, 33 out of 50 states in the USA legislate name reporting for HIV.) Samples of MSM[112,113], racial/ethnic minority clients (especially African-Americans and Hispanics) and others whose behaviors place them at high risk of HIV infection  have indicated an unwillingness to seek testing under these circumstances.
However, in an analysis of testing patterns in six American states, 12 months before and after the implementation of name HIV reporting, there were no significant declines in the total number of HIV tests performed at publicly funded HIV counselling and testing sites in any state, other than those expected from trends present before reporting began. Another American study, a cross-sectional survey of 556 untested persons, revealed that whereas 19% stated that name reporting was one of the factors in their decision to avoid testing and was the main factor for 2%; the fear of learning about a positive result and low perception of risk were the most common deterrents to testing in all risk groups. However, untested MSM who lived in states with name-based reporting identified concerns about reporting as a reason for not testing more often than untested MSM living in states without name-based reporting (35 versus 11%). Concerns about government HIV reporting policies clearly factor into some individuals‚ decision-making about HIV testing. What is less clear is how this particular variable is mediated by other salient variables, including perceptions of increasing benefit associated with the HIV test, in the light of HIV treatment advances.
Client referral mechanisms
Without doubt, the reasons for delay in medical care-seeking are multi-factorial. This fact has been well established by ongoing studies of other disease conditions, including cancer. However, the attributes of a referral system (i.e. by what means formal linkages are made between screening activities/facilities and treatment activities/facilities) are among the important determinants of whether care will be promptly accessed and received after a diagnosis of HIV infection has been made. Referral systems and processes are especially critical if screening activities (i.e. voluntary HIV testing) occur in locales other than primary care settings.
In the domain of HIV prevention and treatment, referral can have three distinct meanings: the referral of high-risk persons to a facility or provider where they can receive HIV counselling and testing; the referral of seronegative persons who are at high ongoing risk of HIV infection to needed services (e.g. long-term risk reduction counselling, drug treatment, etc.); and the referral of HIV-seropositive clients for treatment of their HIV infection.
In 1993, when a group of external experts evaluated publicly funded HIV counselling and testing activities in the United States, they noted that whereas referral to care services for HIV-infected persons was ‚more successful‚ than the referral of high-risk uninfected persons to needed prevention services (e.g. drug treatment for IDU), they were still ‚not always adequate‚. A 1995 study of 142 HIV-infected men and women diagnosed in STD clinics some 6-24 months previously, revealed that 25% had never received medical care. Although many of those who had not received care cited psychological denial or lack of interest as the reason, there were some who stated that they had never been referred for care. In the USA, case management (i.e. individually linking clients with needed services) has been advocated by many as a means of improving the referral of HIV-seropositive persons into needed medical, psychological, and social services[121-123]. Referral is an essential program component even in developing world settings where antiretroviral therapy is limited, e.g. HIV-infected persons with TB symptoms can be referred for TB testing and treatment.
Another system-wide influence on the early diagnosis and treatment of HIV infection pertains to the role of HIV counselling and testing in a nation‚s overall HIV prevention strategy. In the United States, voluntary HIV counselling and testing is a cornerstone of national HIV prevention efforts, with substantial public resources provided to support no or low-cost HIV counselling and testing for persons at risk from HIV. In the USA, the importance of keeping HIV counselling and testing both voluntary and confidential have been of paramount public health importance since the antibody test first became available. Furthermore, the Centers for Disease Control and Prevention, the US governmental agency responsible for national HIV prevention efforts, continues to support the importance of providing anonymous HIV counselling and testing for at-risk persons who may be unwilling to access confidential testing.
A policy analysis of three European nations (Britain, Sweden, and Hungary), found distinct differences in the role that HIV testing played in national HIV prevention efforts. Danziger  opined that some countries he studied had policies that were more overtly supportive of HIV testing as a prevention tool (e.g. Sweden), whereas others tended to regard HIV testing primarily as a diagnostic test, with ‚relatively little‚ emphasis placed on the preventative role of testing (e.g. Britain).
HIV testing has both preventative (e.g. decreasing transmission once persons learn they are infected) and diagnostic functions. However, countries whose national policies characterize HIV testing as primarily a diagnostic procedure may inadvertently discourage asymptomatic infected persons who perceive themselves as being at low risk from seeking testing. Furthermore, in developing world settings, where antiretroviral treatments are scarce, promoting HIV testing as mainly diagnostic may dissuade at-risk persons from seeking testing because of the misperception that little can be done after a positive diagnosis is received.
Questions have been raised about the programmatic role of HIV counselling and testing in the developing world, especially given the ‚severe financial strain‚ of providing antiretroviral combination therapy to seropositive individuals, and the competition for scarce prevention resources. Clearly, the economic realities faced by developing nations put the early diagnosis of HIV infection in a different context compared with the wealthier nations of the industrialized world. Nevertheless, initiatives have been undertaken to improve access to antiretroviral therapies, and HIV counselling and testing has the potential to play an important role in both HIV prevention and care efforts[11,127], even in financially poor countries.
Social marketing of early HIV diagnosis and entry into care
A recent US review  suggested that most HIV-infected adults who are not receiving regular care are those with early or unrecognized HIV infection. Findings in Europe are consistent with this, in that a significant proportion of HIV infections remain undiagnosed before the onset of AIDS. The discipline of social marketing provides a useful model for identifying a comprehensive array of strategies to promote early HIV diagnosis and entry into care. Social marketing is ‚a research-driven and consumer-centered process‚ that intends to change individual behaviors using commercial marketing techniques. Social marketing strategies have been successfully applied to a number of HIV prevention efforts in both industrialized and developing world settings. Others have suggested that social marketing might be used to promote HIV counselling and testing.
Although many mistakenly equate social marketing as being synonymous with media campaigns, the discipline encompasses much more than mass communication and advertising. Audience segmentation (i.e. the identification of one or more homogeneous subaudiences within a population) and the purposeful design of a social product (e.g. promoting the value of the early diagnosis of HIV infection) giving explicit consideration to product, price, place, and promotion, are important attributes that characterize social marketing efforts.
Audience segmentation is an especially important consideration when attempting to promote early HIV diagnosis for infected persons who are unaware of their status. Cost efficiency and program effectiveness are both improved when broad-target populations are divided into smaller, more homogenous market segments. Although HIV prevention mass media campaigns have been shown to result in increased HIV testing[133-135], these increases have often been among the ‚worried well‚[133,135]. Such findings do not mean that mass media is an ineffective source of information about HIV testing. Rather, that messages encouraging early HIV diagnosis require adequate formative research and development to ensure that they have been appropriately targeted to reach subaudiences of high-risk and undiagnosed persons. For instance, broadcast media may be an effective means of reaching IDU with HIV prevention and primary care messages, as long as these are targeted and aired at appropriate times. The use of census track and commercial marketing databases, in concert with HIV/AIDS surveillance data, enables highly specific targeting of HIV prevention messages, and can be used to focus campaigns finely to reach persons who may be infected yet unaware of their positive serostatus (M. Shepherd, CDC, personal communication).
HIV diagnosis as a consumer product
A number of basic strategies exist that might improve the way potential consumers view the product of early HIV diagnosis. Modalities such as rapid testing, which can increase client and provider convenience by negating the need for a follow-up visit, have been successfully implemented in developing world settings. Rapid testing will probably increase the uptake of HIV testing, at least among some individuals. With the licensure of testing systems that rely on oral specimen collection, rather than venipuncture, more individuals are likely to find testing acceptable.
Because some high-risk persons may avoid HIV testing because of previous bad testing experiences, providers are urged to tailor the counselling provided, whether brief or long, to meet the special needs of the person being served. This means that counselling must extend beyond ‚advice giving‚. For some clients, especially those who are mistrustful of testing systems or fearful of learning about a positive result, counselling may take the form of ‚trust-building‚. Moreover, the manner in which information is provided, including the notification of a positive HIV diagnosis, may influence future treatment compliance and the continuation of contact with medical services.
To make HIV counselling and testing services more attractive, they should be packaged to meet the needs of specific client groups. Low-income women, for example, may require HIV testing services that are configured with readily available child care. Transgendered clients are more likely to utilize HIV testing services in which providers are sensitive to their unique psychological and primary care needs (K. Clements, San Francisco DOH, personal communication). American teenagers report that they are more likely to seek/agree to HIV testing in youth-oriented healthcare facilities, including school-based clinics.
The price of HIV diagnosis
Health services can be conceptualized as an exchange, where clients, as consumers, will exchange their resources for perceived benefits, including intangibles such as improved health or peace of mind. Money, time, physical and cognitive effort, lifestyle changes, and psychological factors such as stress and anxiety can all be viewed as comprising the price that consumers might pay for health services, including HIV diagnostic and care services.
As the economic construct of ‚price elasticity of demand‚ tells us, demand will increase as the price drops. Therefore, the HIV testing ‚price‚ for some clients can be decreased (and demand increased) by offering testing services in accessible locations and by reducing waiting times and other barriers to testing. In Uganda, where clients pay fees for HIV testing, ‚Free Days‚ are routinely advertised as a way to attract young people, women, and couples into testing.
Other potential costs, including stigma, job loss, and denial of healthcare  are far more difficult to address and may require more fundamental solutions, including anti-discrimination legislation[143,144]. As is the case in Switzerland, many nations have explicitly identified the reduction in discrimination as a tenet of their HIV/AIDS policies. The use of mass communication strategies, which have been important in promoting anti-discrimination efforts, may be helpful in promoting the early diagnosis of HIV, by destigmatizing HIV testing and increasing knowledge of the benefits of early testing. Maintaining anonymous testing opportunities is an especially important means of reducing the ‚price‚ of HIV testing for many stigmatized populations.
Price may also be seen from the perspective of the provider. In the USA, some providers perceive recommended pretest counselling as ‚too onerous‚ and a deterrent to offering testing to their clients. A hospital in San Francisco ‚uncoupled‚ prevention counselling from diagnostic testing, resulting in improved rates of earlier testing for high-risk patients. An expert panel of the US Institute of Medicine recently recommended that pretest counselling in prenatal settings consist ‚primarily of notification that HIV testing is a regular part of prenatal care for everyone and that women have a right to refuse it‚. This, they believe, will speed the implementation of universal HIV testing for all pregnant women. Although there is no consensus in the public health community that such ‚uncoupling‚ efforts will result in uniform benefit, one can expect to hear continued discussions about the ‚price‚ of HIV testing from both the client and provider perspective.
The placement of HIV diagnostic services
The importance of place in social marketing recognizes that consumers are not homogeneous when it comes to their preferences or their abilities to access health and social services. For instance, late testing for HIV infection has been found to be associated with lower self-reported access to outpatient medical care. Given this finding, some have advocated that emergency rooms and other acute care facilities may serve as an appropriate locale for HIV testing and counselling among populations who are underserved in other primary care settings.
An important strategy for improving the placement of HIV testing is to ensure that it is available in settings where high-risk and undiagnosed seropositive clients are served, including drug treatment facilities, TB clinics, reproductive health clinics, and STD clinics. However, the placement of HIV counselling and testing should not be limited to medical facilities. Correctional settings, social service organizations, and community-based organizations all provide organizational venues where high-risk and seropositive clients may learn their serostatus. For some vulnerable populations, like adolescents, transportation logistics may impede the receipt of HIV testing. Therefore, it has been suggested that school and student health clinics in the USA ensure that confidential HIV and STD testing services are available on site. Another means of overcoming transportation and other access barriers to early diagnosis is to bring HIV counselling and testing services to clients through community and street outreach activities. Expanding testing beyond organizational venues (medical or otherwise) is well served by advances in HIV testing technologies[15,16,88]. Well-targeted, peer delivered, HIV counselling and testing programs could encompass locales as diverse as bars, bathhouses, street corners where drug injectors congregate, and commercial sex environments.
Promoting the early diagnosis of HIV
The promotion of early HIV diagnosis has evolved over time and with advances in available antiretroviral and opportunistic therapies. Campaigns increasingly underscore the individual health benefits of early diagnosis and treatment. However, for some populations, it may be necessary to promote more than the potential medical benefits of early HIV diagnosis. For example, a study of IDU found that viewing HIV treatment as a source of personal control and hope may help to motivate positive behaviors for HIV treatment. In developing world settings, where access to antiretroviral agents is severely limited, HIV testing might be promoted for ‚social reasons‚, such as planning for the future.
As with all aspects of social marketing, formative research is critical to understanding what particular motivators may be especially important for specific populations. Formative research among substance-using HIV-positive youths found that care providers may at times ignore or under-emphasize the substance abuse treatment needs of youths, thus forcing patients to become ‚HIV-positive persons‚, when substance abuse issues may be of more immediate concern to the youth.
For some infected clients, promotion may need to emphasize access and ease of referral to other needed medical and psychosocial services, rather than knowledge of HIV serostatus, per se. An excellent example of this circumstance comes from Canada, where a national consultation on HIV prevention and gay youth  found that ‚leading‚ with HIV/AIDS as the primary issue was a mistake. Instead, gay youth were most immediately interested in ‚safe zones‚ where they could discuss ‚coming out‚ issues with their peers. Into that broader context it was then possible to promote a specific HIV and STD prevention agenda.
Knowledge of HIV serostatus has been an important element in HIV prevention and treatment efforts since antibody testing first became available. Improvements in HIV therapeutics further strengthen the rationale for early HIV diagnosis and entry into care. Benefits will accrue at both an individual and societal level, with outcomes of improved health and productivity, reduced hospitalization costs, and decreased transmission from unsuspecting HIV-seropositive individuals. Using a social marketing approach that embraces audience segmentation, a strong consumer perspective, and adequate formative research in advance of message development will help to ensure the success of these efforts. However, the reader is cautioned to remember that testing, despite its importance, cannot on its own be considered an adequate HIV prevention or treatment response. Rather, HIV testing is an essential linchpin, linking prevention to care, for the benefit of the individual and society.
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HIV testing; early intervention; social marketing
© 1999 Lippincott Williams & Wilkins, Inc.
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