RESEARCH

From caution to urgency: the evolution of HIV testing and counselling in Africa

De la prudence à l'urgence: l'évolution des activités de conseil et de dépistage du VIH en Afrique

De la cautela a la urgencia: La evolución de las pruebas de detección del VIH y el asesoramiento en África

R Baggaley^I; B Hensen^II,*; O Ajose^III; KL Grabbe^IV; VJ Wong^V; A Schilsky^IV; Y-R Lo^I; F Lule^VI; R Granich^I; J Hargreaves^II

^IHIV/AIDS Department, World Health Organization, Geneva, Switzerland
^IIDepartment of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, England
^IIIClinton Health Access Initiative, Dar es Salaam, United Republic of Tanzania
^IVDivision of Global HIV/AIDS, Centers for Disease Control and Prevention, Atlanta, United States of America (USA)
^VOffice of HIV/AIDS, United States Agency for International Development, Washington, USA
^VICommunicable Diseases, World Health Organization Regional Office for Africa, Brazzaville, Congo

ABSTRACT

OBJECTIVE: To describe recent changes in policy on provider-initiated testing and counselling (PITC) for human immunodeficiency virus (HIV) infection in African countries and to investigate patients' experiences of and views about PITC.
METHODS: A review of the published literature and of national HIV testing policies, strategic frameworks, plans and other relevant documents was carried out.
FINDINGS: Of the African countries reviewed, 42 (79.2%) had adopted a PITC policy. Of the 42, all recommended PITC for the prevention of mother-to-child HIV transmission, 66.7% recommended it for tuberculosis clinics and patients, and 45.2% for sexually transmitted infection clinics. Moreover, 43.6% adopted PITC in 2005 or 2006. The literature search identified 11 studies on patients' experiences of and views about PITC in clinical settings in Africa. The clear majority regarded PITC as acceptable. However, women in antenatal clinics were not always aware that they had the right to decline an HIV test.
CONCLUSION: Policy and practice on HIV testing and counselling in Africa has shifted from a cautious approach that emphasizes confidentiality to greater acceptance of the routine offer of HIV testing. The introduction of PITC in clinical settings has contributed to increased HIV testing in several of these settings. Most patients regard PITC as acceptable. However, other approaches are needed to reach people who do not consult health-care services.

RÉSUMÉ

OBJECTIF: Décrire les changements récents dans la politique d'activités de conseil et de dépistage à l'initiative du fournisseur (PITC), du virus de l'immunodéficience humaine (VIH) dans les pays africains, et enquêter sur les expériences et opinions des patients relatives à la PITC.
MÉTHODES: Les publications, ainsi que les politiques nationales, les cadres stratégiques, les plans et autres documents pertinents relatifs au dépistage du VIH ont été étudiés.
RÉSULTATS: Sur les pays africains passés en revue, 42 d'entre eux (79.2%) avaient adopté une PITC. Sur ces 42 pays, tous recommandaient la PITC pour la prévention de la transmission mère-enfant du VIH, 66,7% pour les cliniques soignant la tuberculose et les patients affectés par cette maladie, et 45,2%, pour les cliniques soignant les infections sexuellement transmissibles. En outre, 43,6% des pays avaient adopté la PITC en 2005 ou 2006. L'examen des publications a permis d'identifier 11 études sur les expériences des patients et leur opinion relatives à la PITC dans les environnements cliniques en Afrique. La grande majorité considérait la PITC comme étant acceptable. Cependant, les femmes en consultations prénatales n'étaient pas toujours conscientes du fait qu'elles avaient le droit de refuser un dépistage du VIH.
CONCLUSION: La politique et la pratique relatives aux activités de conseil et de dépistage du VIH en Afrique sont passées d'une approche prudente, mettant l'accent sur la confidentialité, à une plus grande acceptation de l'offre systématique de dépistage du VIH. L'introduction de la PITC dans les milieux cliniques a contribué à augmenter le dépistage du VIH dans plusieurs de ces environnements. La plupart des patients considèrent la PITC comme étant acceptable. Toutefois, d'autres approches sont nécessaires pour atteindre les personnes qui ne font pas appel aux services de santé.

RESUMEN

OBJETIVO: Describir los cambios recientes en la estrategia sobre la realización de pruebas de detección del virus de la inmunodeficiencia humana (VIH) y el asesoramiento emprendidos por los proveedores (PITC) en países africanos e investigar las experiencias de los pacientes y sus opiniones acerca de la PITC.
MÉTODOS: Se llevó a cabo un examen de las publicaciones y de estrategias de detección del VIH nacionales, convenios estratégicos, planes y otros documentos importantes.
RESULTADOS: De los países africanos examinados, 42 (79,2%) había adoptado la estrategia PITC. De esos 42, todos recomendaban la PITC para prevenir la transmisión maternoinfantil del VIH, el 66,7% la recomendaba a las clínicas y pacientes con tuberculosis y el 42,5% a las clínicas de tratamiento de infecciones de transmisión sexual. Además, el 43,6% adoptó la PITC en el año 2005 o 2006. La búsqueda bibliográfica identificó 11 estudios sobre las experiencias de los pacientes y sus opiniones acerca de la PITC en entornos clínicos de África. Una mayoría clara consideró la PICT aceptable. Sin embargo, las mujeres en las clínicas de atención prenatal no siempre fueron conscientes de que tenían el derecho a rechazar las pruebas de detección del VIH.
CONCLUSIÓN: La estrategia y práctica de las pruebas de detección del VIH y el asesoramiento en África han cambiado desde un enfoque cauteloso que enfatiza la confidencialidad a una mayor aceptación de la oferta sistemática de pruebas de detección del VIH. La introducción de la PITC en los entornos clínicos ha contribuido a incrementar el número de pruebas de detección del VIH en muchos de esos entornos. La mayoría de pacientes considera la PTIC aceptable. No obstante, se necesitan otros enfoques para llegar a aquellas personas que no acuden a los servicios sanitarios.

Background

Since the first antibody tests for human immunodeficiency virus (HIV) infection became available, public health organizations and human rights activists have debated the best approach to HIV testing and counselling (HTC).¹ At a time when there was no effective treatment and HIV-infected individuals faced widespread discrimination and stigmatization,¹ many argued that HTC was inappropriate because it provided little benefit to the individual.^1,2 Conversely, others believed that testing was the key to promoting a change in behaviour.^1,3 These two concerns framed early debates about HTC.⁴

Initially, there was general support for a cautious response to HTC and HIV infection, although this was considered "exceptional" compared with responses to other infectious diseases.^1,5 For example, in 1987, the World Health Organization (WHO) emphasized caution in extending routine HIV testing beyond blood donors.¹ At that time, standards for HTC, which were based on an international consensus reached by WHO and other stakeholders, emphasized voluntarism and gave rise to the adoption of voluntary counselling and testing.¹ This approach consisted of three primary components: counselling before and after an HIV test, which included an individualized risk-reduction plan based on the test results; informed written consent; and confidentiality.¹

As evidence emerged that antiretroviral therapy (ART) could significantly reduce mother-to-child HIV transmission and "alter the clinical course" of HIV infection, the HTC debate changed.^1,3,6 Clinicians and public health professionals now argued that an exceptional approach to HTC was no longer appropriate. The view was that HTC should be standard clinical practice in settings where patients present with symptoms of an HIV infection and where ART is available.^1,2

At first, however, ART was not universally available. In 2003, only 1% of individuals in need of ART had access to treatment and WHO declared a global health emergency.⁷ This declaration gave rise to a series of initiatives for expanding access to ART in developing countries, including the 2003 WHO 3-by-5 initiative and The World Bank's Multi-Country HIV/AIDS Program.^7–9 In the same year, increased funding for extending treatment became available through the United States President's Emergency Plan for AIDS Relief and the Global Fund to Fight AIDS, Tuberculosis and Malaria. In addition, the political climate changed and increased access to prevention and treatment of HIV infection was endorsed. These developments profoundly influenced the debate on HTC at a time when fewer than 10% of those infected with HIV were aware of their status¹⁰ and most were diagnosed at the end stage of the disease, when immune suppression made ART less effective.^11,12 Consequently, voluntary counselling and testing was no longer seen as sufficient for enabling people to become aware of their HIV status. In the era of ART, alternative approaches to HTC were required.^1,2

One development was the emergence of provider-initiated HIV testing and counselling (PITC).¹ In 2003, only 52% of pregnant women in Botswana knew their HIV status.¹³ To increase the knowledge of HIV status, the government instituted a policy of "routine" PITC in various clinical settings in 2004.¹⁴ Similarly, Uganda implemented PITC in referral hospitals in 2005 and Zambia implemented it in tuberculosis clinics in 2004.^15,16 In 2006, the United States Centers for Disease Control and Prevention recommended that PITC be offered to adults aged 13 to 64 years in all health-care settings, with consent being assumed unless the patient explicitly declined.^1,17 As treatment was scaled up, routine HTC gained traction and several countries introduced PITC in clinical settings. Early results demonstrated an increase in HTC uptake.^18–20 With the implementation of PITC expanding globally, WHO recognized the need for guidance. In 2007, WHO and the United Nations Programme on HIV/AIDS issued a document on PITC in health-care facilities. The final document was an extensive revision of an initial 2006 draft and took into account concerns about coercion, human rights and the definition of the word "routine".^1,7

The primary aim of this study was to review how policy in African countries has changed in response to the growing recognition that health-care providers should offer more HTC. The rationale for focusing on HTC policy in Africa was, first, that 68% of the estimated 34 million people with HIV infections worldwide at the end of 2010 resided in sub-Saharan Africa, a region with only 12% of the global population,²¹ and, second, that it was important to examine policy responses in settings where there was an urgent need to address low HTC coverage, for example, to prevent mother-to-child HIV transmission or to identify individuals with HIV infections who could benefit from ART. Additional aims were to investigate patients' perceptions of PITC and their experience of the process of PITC, with particular reference to informed consent and counselling.

Methods

National policy documents, strategies, plans, frameworks, guidelines and reports on HIV testing or HIV prevention and treatment were identified by searching the WHO Library Information System, Google Scholar and the knowledge base repositories of organizations and institutions, including the International Labour Organization, the United States Agency for International Development (the AIDSTAR One project), the University of California in San Francisco (the HIVInSite knowledge base) and Harvard University. The Evidence to Action HIV and AIDS Data Hub was also searched. Where information was not readily available or further clarification was required, WHO country representatives were contacted. In addition, the review also considered documents that did not focus on HIV prevention alone but covered relevant broad issues, such as maternal and child health, human rights, tuberculosis and opportunistic infections.

Identified documents were grouped into three categories according to their overall objectives:

• guidelines, manuals, protocols, legislation and policy;

• national strategic plans, strategic frameworks and multisectoral frameworks;

• other literature, including published and unpublished reviews.

The date assumed for the adoption of a policy depended largely on the type of documents identified and the strength of the evidence available, with further confirmation being obtained from WHO country representatives. Since the date of publication of legislation, policy, guidelines, manuals and protocols (i.e. the first document category) explicitly indicated the date on which a policy was adopted, this date was used in preference to the dates of other documents. When these documents were not available, the publication date of a strategic plan (i.e. the second document category) was used. However, when the only documents identified belonged to the third category, the date on which a policy was adopted was determined by consultation with WHO country representatives.

To obtain information on patients' experiences of and views about PITC, we searched the MEDLINE, EMBASE, International Bibliography of the Social Sciences, PsychINFO and Global Health databases for relevant documents published in 2000 or later using the following terms: provider-initiated, routine, diagnostic, opt-out, HIV, human immunodeficiency virus, AIDS, acquired immune deficiency syndrome, counselling, testing, screening, experience, personal experience, opinion, attitude, acceptability and informed consent. We considered publications from a range of disciplines, with a focus on quantitative and qualitative studies of PITC. Reports of studies were reviewed if the studies: (i) involved the routine offer of HTC in an African country; (ii) were conducted in a clinical setting after HTC had been offered to patients or involved patients who were recruited in a clinical setting and had experience of PITC in that clinical setting; or (iii) assessed the acceptability of PITC to patients or their experience with components of the PITC process, particularly the acquisition of informed consent; and (iv) were published in English. Data on the acceptability of PITC and on patients' experiences of PITC were extracted separately.

Results

The policies, guidelines or strategic plans on PITC from 52 African countries were reviewed. Documents for one country could not be retrieved and Western Sahara was not included in the review. There was evidence that a policy had been adopted by 42 (79.2%) of 53 countries (Table 1), whereas 10 (18.9%) had not adopted a policy: Algeria, Angola, Chad, Egypt, Libya, Morocco, the Niger, Sao Tome and Principe and Tunisia (Fig. 1). Documents could not be retrieved for the Gambia. A large proportion of countries (n = 17; 43.6%) adopted a PITC policy between 2005 and 2006, whereas 10 (25.6%) adopted a policy between 2003 and 2004 and 10 (25.6%), including the Comoros, the Congo, the Democratic Republic of the Congo and South Africa, adopted a policy between 2007 and 2008. The Central African Republic and Equatorial Guinea were the last of the 42 countries to adopt PITC, in 2009 and 2010, respectively (Table 1).

Clinical settings and target populations

All 42 countries that adopted a PITC policy recommended that pregnant women should be covered either in antenatal clinics or in services provided for the prevention of mother-to-child HIV transmission. In addition, 73.8% of the 42 countries adopted a policy of universal PITC, which was defined as offering HTC to all patients or adults visiting a health-care facility. Documents for 66.7% of countries recommended PITC for either tuberculosis patients or clinics, 45.2% recommended it for patients with sexually transmitted infections, 14.3% for family planning clinics, 7.1% for most-at-risk populations and 7.1% for individuals attending out-patient departments (Table 1).

Patient's perspectives and experience

The literature search identified over 2000 publications, of which 11 were considered eligible for inclusion in the review (Table 2 and Table 3, available at: http://www.who.int/bulletin/volumes/90/9/11-100818). The majority were observational studies; 8 investigated the acceptability of PITC to women or their experiences of it in antenatal clinics, whereas the remaining 3 involved tuberculosis patients, women attending immunization clinics with their infants and patients attending a medical emergency unit.

Overall, the large majority of individuals who received PITC found it acceptable (Table 2). For example, in Uganda 98.5% of women who were attending an antenatal clinic for the first time considered the routine offer of HTC during pregnancy "good" or "very good".²⁶ In South Africa, 93% of women offered HTC while attending midwife obstetric units agreed that all pregnant women should be tested for HIV.²² Among pregnant women who opted for HTC in a study from Zimbabwe, 89% stated that the routine offer of HTC was helpful and empowering and enabled women to make an informed decision about the prevention of mother-to-child HIV transmission and infant feeding.²⁴

In addition, experience of PITC was generally regarded as good (Table 3). For example, in Zimbabwe, 98% of pregnant women stated they were satisfied with the information they received on routine HTC.²⁴ In South Africa, 52% of pregnant women who had been tested for HIV felt they had made an informed choice and had a positive experience, whereas 28% felt that their choice had been "less clear" and 20% that their voluntariness had been compromised.³¹

Discussion

This review of HTC policy in Africa illustrates the changing response to HTC that has taken place in the last decade. Before WHO issued guidance on PITC in 2007, approximately 50% of African countries had adopted PITC in health-care facilities.^3,33,34 Subsequently, the number of countries that included PITC in their HIV policies or strategies increased and, by the time of writing, 42 African countries had elected to recommend PITC in health-care facilities, with a large proportion adopting such a policy between 2005 and 2006. With evidence that ART can reduce mother-to-child HIV transmission, all these countries recommended PITC in antenatal clinics. In addition, more than half recommended universal coverage for all adults and coverage for tuberculosis clinics and patients.

Previous studies of the acceptability of PITC have used the uptake of testing as an indicator of acceptability.^35,36 Although they provided evidence of the feasibility of PITC, these studies did not reflect patients' experiences of or views about PITC. Our review of the published literature suggests that PITC is generally acceptable to patients. Studies reported that more than 75% regarded PITC as acceptable, particularly in antenatal clinics.²² However, findings from studies of pregnant women may not be generalizable to other population groups since these women may be more willing to undergo HIV testing because they believe it will benefit their children.³⁷ Patients in other clinical settings may find PITC less acceptable, perhaps because of their perceived risk of infection or fear.³⁷ In our review, evidence from four studies, the majority involving small groups of pregnant women, indicated that patients were not always aware they had the right to decline HTC in antenatal clinics, perhaps because of the power balance between patients and health-care providers.^29,31 However, studies in other regions suggest that women may find the routine offer of HTC acceptable because it "normalizes" the process of HTC.³⁸

Our review has several limitations. It was difficult to retrieve all the documents required to understand national PITC policy fully. Although we contacted WHO country offices, it was not possible to obtain information for some countries and, for others, the date on which policy was adopted was unknown. In addition, the ambiguous language of some documents made it difficult to determine when and in which settings policies were adopted. Consequently, our data on the years in which PITC policies were adopted may be inaccurate. We minimized this inaccuracy by asking two reviewers to determine independently the date of policy adoption using the available evidence. Our review of patients' experiences of and views about PITC also has several limitations and the findings must be interpreted with caution. First, our review was subject to a language bias and a publication bias. Second, the majority of studies included took place in antenatal clinics and there may be studies from other clinical settings that we did not identify. Some studies that reported on the acceptability of PITC included only small samples of women and did not involve interviews with women who declined an offer of HTC.^28,31,32 In addition, the studies included in our review are subject to their own limitations: the majority were nonrandomized studies and the difficulty of reporting and synthesizing evidence from nonrandomized studies is well documented.³⁹ Moreover, studies were subject to acquiescence bias⁴⁰ and, as the questions posed to patients were different in each study, it was difficult to compare their findings.

In general, the evidence suggests that the introduction of PITC in antenatal clinics has been associated with an increase in HIV testing rates. A 2010 WHO report on universal access stated that the testing rate in eastern and southern Africa rose from 48% in 2008 to 50% in 2009.¹⁰ Moreover, with the increased uptake of HTC and the better access to ART that followed from the introduction of PITC,¹³ mother-to-child HIV transmission has been virtually eliminated in some countries:^13,24 in 2009, four of the 25 countries with the highest HIV disease burden achieved the target set by the United Nations General Assembly Special Session on HIV/AIDS of providing at least 80% of HIV-infected pregnant women with ART.¹⁰ In addition, one literature review found that the introduction of PITC in antenatal clinics contributed to the achievement of universal HTC in pregnant women.⁴¹ Moreover, the results of the seven African-based studies included in our review indicate that implementation of PITC led to an increase in the uptake of HTC by pregnant women that ranged from 9.9% in Malawi to 65.6% in Uganda, with more than 75% of women accepting PITC across all seven studies.⁴¹

The implementation of PITC has also led to a high rate of HIV testing among individuals visiting tuberculosis and sexually transmitted infection clinics.^15,42–44 A cluster randomized trial conducted in tuberculosis clinics in South Africa in 2005 found that the introduction of opt-out PITC increased the uptake of HIV testing by 13.7%, from 6.5% when HIV testing was carried out on an opt-in basis to 20.2% with opt-out PITC.⁴⁵ The 2011 WHO report on global tuberculosis control stated that HTC is now standard for tuberculosis patients in many countries, especially in Africa. In 2010, more than 75% of tuberculosis patients knew their HIV status in 68 countries and territories, including 22 countries in the WHO African Region.⁴⁶ Further efforts are still needed globally, however, since only 34% of 6.2 million tuberculosis patients were aware of their HIV status in 2010.

Despite the availability of effective therapy and the increase in HIV testing, population-based surveys conducted between 2007 and 2009 in 10 sub-Saharan African countries indicated that the median proportion of people with an HIV infection who are aware of their status was under 40%.^10,47 Moreover, although PITC can contribute to increased testing in clinical settings,⁴¹ the adoption of PITC alone will not achieve universal access to HTC. Other approaches that enable people not attending health-care services to access HIV testing should be developed in parallel to ensure that access to testing is equitable and that individuals with HIV infections are diagnosed before they become symptomatic. In 2011, the HIV Prevention Trials Network study 52 (HPTN052) confirmed that ART was effective for preventing the transmission of HIV in serodiscordant couples.⁴⁸ There is a rationale, therefore, for considering and evaluating household or community-based testing in addition to expanding PITC.⁴⁹ Data on these alternative approaches would help identify the most effective and appropriate way of implementing HIV testing in specific local contexts, while taking into account the resources available and social constraints.

Acknowledgements

We would like to thank Chris Grundy for Fig. 1.

Competing interests: None declared.

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(Submitted: 5 December 2011 – Revised version received: 9 May 2012 – Accepted: 11 May 2012 – Published online: 27 June 2012)

* Correspondence to B Hensen (e-mail: bernadette.hensen@lshtm.ac.uk).