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Epidemiology and Social

Increasing HIV testing among male partners

Orne-Gliemann, Joannaa,b; Balestre, Erica,b; Tchendjou, Patricec,j; Miric, Marijad; Darak, Shrinivase,f; Butsashvili, Maiag; Perez-Then, Eddyd; Eboko, Fredh; Plazy, Melaniea,b; Kulkarni, Sanjeevanie; LoÛ, Annabel Desgrées dui; Dabis, Françoisa,b for the Prenahtest ANRS 12127 Study Group

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doi: 10.1097/QAD.0b013e32835f1d8c
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Abstract

Introduction

HIV testing is the cornerstone of HIV prevention [1]. HIV testing and more specifically knowledge of one's serostatus allows individuals to adopt safer behaviours that can reduce HIV transmission [2]. HIV testing is also a prerequisite for accessing care and treatment when HIV-infected. Antiretroviral treatment (ART) may also in turn contribute to overall HIV prevention [3]. Yet, although the expected benefits of HIV testing are well known, its coverage remains low worldwide. Population-based studies conducted between 2007 and 2009 in nine resource-limited countries estimated that only 34% of women and 17% of men were ever informed of their HIV status [4]. Further, HIV counselling and testing services have largely been organized on an individual and sex-specific basis. Women are often tested during pregnancy, for the prevention of mother-to-child transmission of HIV (PMTCT). The estimated coverage of prenatal HIV testing increased from 13% in 2004 to 21% in 2007 [4]. Whereas men usually access HIV testing in outpatient's consultations for sexually transmitted infections, at voluntary HIV counselling and testing centres, before a medical intervention, and more recently within male circumcision programmes. In the context of antenatal care (ANC), less than 20% of male partners of pregnant women themselves get tested for HIV [5–7].

Yet, male partner's HIV testing is consistently associated with the acceptability of PMTCT interventions by women at all levels [5,8,9]. A recent cohort study in Kenya suggests that a man's attendance to ANC visits with his female partner and being himself tested for HIV reduces the risk of HIV transmission to their infant and increases child survival [10]. Partner HIV testing is also key for the prevention of sexual transmission of HIV during pregnancy and after delivery [11,12], as it has been shown that a large proportion of new HIV infections occur within marriage and cohabitation [13]. These observational findings have rarely been corroborated by experiments data. Indeed, such data on interventions aiming at increasing HIV testing among male partners in the context of prenatal care are scarce [14].

The Prenahtest Study is a multicountry randomized intervention trial evaluating the efficacy of an innovative prenatal HIV counselling intervention called couple-oriented posttest HIV counselling (COC) [15]. The present analysis describes the primary study outcome, that is the impact of COC on partner HIV testing and investigates the socio-behavioural factors associated with partner HIV testing.

Methods

Ethics statement

The Prenahtest study protocol V4 – 18 December 2006 received ethical clearance from Comité National d’Ethique, 23 January 2007, in Cameroon; Comité de Etica Indepediente, Fundacion Dominica de Insectoligia, 9 April 2007, in Dominican Republic; IRB 00006752 of Maternal and Child Care Union, 13 November 2008 in Georgia; Independent Ethics Committee for Prayas Health Group, 27 March 2007, in India. The Prenahtest study was registered on ClinicalTrials.gov as NCT01494961.

Study setting

The study was carried out at four urban health centres catering mainly for underprivileged populations and located in four low/intermediate-resource countries with low/medium HIV prevalence: Centre Mère-Enfant de la Fondation Chantal Biya in Yaounde, Cameroon (national HIV prevalence in 2009 estimated at 5.3%), Hospital Materno-Infantil ‘San Lorenzo’ de los Mina in Santo Domingo, Dominican Republic (HIV prevalence: 0.9%), Sane Guruji Hospital in Pune, India (HIV prevalence: 0.3%) and Maternity Hospital N°5 in Tbilisi, Georgia (HIV prevalence: 0.1%) [16].

Study population and sampling

The study sample size was calculated so as to be able to measure in each study site a minimum improvement of 10% of the proportion of tested partners among women from the COC group (target: 15%) compared with women from the standard posttest HIV counselling group (baseline: under 5%), with an alpha type I error of 5% (two-sided test) and a β type II risk of 10% (power of 90%). Considering a proportion of 15% of women lost to follow-up and of noninterpretable observations, a minimum of 242 women in each group, that is 484 women per site were to be included. Inclusion criteria were: age at least 15 years, having a partner (defined as regular by the woman) on the day of enrolment, and accepting follow-up (including home visits if necessary) by the study team until 6 months postpartum. Exclusion criteria were: herself or her partner having been tested for HIV during her current pregnancy, having a partner who is absent for more than 6 months per year, being unwilling/unable to provide contact information and having a mental impairment at the moment of enrolment.

Enrolment and randomization

Between 26 February and 15 October 2009, all women attending their first prenatal care visit in the four study sites were informed about the study and, if interested to participate, screened for eligibility. Eligible women were offered participation and required to provide written informed consent. Women were enrolled before HIV testing, which was performed on the same day using rapid tests, except in Georgia where ELISA testing was used. Women were scheduled to receive posttest HIV counselling as per each site protocol, either on the same day of HIV testing (Dominican Republic), a few days later (India) or at the next ANC visit (Cameroon and Georgia). Women were individually randomized to receive either standard posttest HIV counselling or the COC intervention; women were blinded to the nature of the counselling. Randomization was performed centrally in Bordeaux and stratified according to trial centre. Blocked randomization was drawn by the trial statistician (in blocks of 10) to assign eligible women to one of the two counselling groups.

Posttest HIV counselling

Standard posttest HIV counselling

Standard posttest HIV counselling was delivered in each study site according to WHO [17] and local HIV counselling guidelines. Observations conducted during the pilot phase of the trial highlighted that the content and quality of sessions varied across sites and within sites; all sessions discussed HIV transmission and prevention and PMTCT, however most poorly addressed partner HIV testing and men's involvement within the prenatal HIV counselling and testing process [18].

Intervention: couple-oriented posttest HIV counselling

COC was designed as a strengthened posttest HIV counselling session, provided once to women and for 30 min on average. Through counselling, education and role-play, COC aims to develop women's communication skills and self-efficacy, so as to empower women to discuss HIV and sexual issues with their partner, including partner HIV testing and couple HIV counselling. The structure of the COC intervention was adapted from WHO [17] and was described in a COC manual, which was used to train the COC counsellors and could also be used during the counselling session [19]. COC counsellors did not provide standard posttest VIH counselling during the trial period. Tested during the pilot phase of the trial, COC was shown to be feasible and acceptable in the four study sites [18].

Data collection and follow-up

Three structured face-to-face quantitative questionnaires were administered to participants: at baseline prior to prenatal HIV testing (T0), 2–8 weeks after the posttest HIV counselling (T1) and 6 months postpartum (T2). Women were assigned identification numbers and all the questionnaires, process forms and laboratory samples were labelled with matching numbers to maintain confidentiality.

Adverse events, described as experience of violence or union break-ups occurring among study participants after randomization, were systematically documented and their relatedness to the study and/or intervention was assessed. Psychosocial services were available upon request.

Partner HIV counselling was provided as per each site protocol. All counsellors received refresher training on couple HIV counselling prior to the trial.

Women were provided incentives for follow-up: condoms, family planning visits, selected contraceptive methods and selected sexually transmitted infections screening were offered for free. Repeat HIV testing was offered to all HIV-negative women at T2. All women and partners tested HIV-positive within the study and their exposed infants were referred to a local HIV care and treatment programme.

Statistical analysis

All partner HIV testing events were computed from the day the woman received posttest HIV counselling to 6 months postpartum. Partner HIV testing rates were measured using three indicators: tests notified within site laboratory logbooks, tests self-reported by women within the questionnaires (reports of tests having occurred on site or elsewhere) and tests notified by laboratory logbooks or reported by women (combined indicator). To estimate the effect of COC on these outcomes, an intention-to-treat analysis was conducted on all randomized women. In case of a missing value on our main outcome, we considered that the partner was not tested for HIV. As the four study sites present different epidemiological, socio-demographic and cultural contexts, the data were not pooled a priori and all statistical analysis were stratified according to study site. Odds ratios (OR) and confidence intervals at 95% (CI) were estimated and Wald tests were used. To estimate socio-behavioural factors associated with the combined indicator for partner HIV testing, we first conducted nonadjusted logistic regressions. Variables that were statistically significant at 0.25 in univariable analysis were included in the multivariable models. To select the final adjusted models, a descending manual method was performed and confounders were verified. The goodness of fit of the final adjusted models was checked with the Hosmer and Lemeshow test and the accuracy was checked with the area under curve statistic. Data were processed and analysed with the use of SAS software (version 9.2; SAS Institute, Cary, North Carolina, USA).

Results

Recruitment and retention

Among the 4249 pregnant women informed about the Prenahtest Study, 3366 (79.2%) were screened for eligibility. One thousand and thirty-eight women (30.8%) did not meet eligibility criteria, mainly because women were not available for the planned follow-up period (42.0%) or they had already been tested for HIV during their current pregnancy (25.8%). Of the 2328 eligible women, 1943 (83.5%) consented to participate and were randomized (484 in Cameroon, Dominican Republic and India, respectively, and 491 in Georgia). One thousand nine hundred and twenty-two women (98.9%) completed the baseline T0 questionnaire and of these, 1726 (89.8%) completed either the T1 or T2 questionnaire (Fig. 1). Overall lost to follow-up rates after randimization were comparable between women from standard posttest HIV counselling and COC groups (11.0% in standard posttest HIV counselling and 11.3% in COC in Cameroon, 6.9 and 6.1% in Georgia and 9.1 and 11.9% in India), except in Dominican Republic (12.8% in standard posttest HIV counselling and 20.3% in COC group, P = 0.04).

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Fig. 1:
Trial profile. Prenahtest ANRS 12127 trial (2009–2011).DR, Dominican Republic.

Participant characteristics

Women's characteristics at enrolment and during follow-up are presented in Table 1. We found no baseline differences between women assigned to standard posttest HIV counselling or COC and very little differences between women followed-up and those lost-to-follow-up. Women's median age at baseline varied between 21 in Dominican Republic and 27 years in Cameroon. Women were more likely to be primiparous in Georgia and India (52.5 and 41.9%, respectively) than in Cameroon or Dominican Republic (<30%). All or almost all women were married in India (99.0%) and Georgia (83.7%), whereas in Cameroon only 37.8% were formally married; in Dominican Republic women were mostly in free union (83.1%). More than 40% of women in Georgia and India had been accompanied by their partner to their ANC visit, much less so in the two other sites (18.4% in Cameroun and 25.4% in Dominican Republic). Women in Cameroon reported a history of couple communication on HIV (87.8%), whereas HIV had been little discussed within couples in India (45.7%) and Georgia (42.8%). Most women in Cameroon reported a history of HIV testing (84.3%) compared with 38.3% in Georgia and 36.4% in India. Women reported that their partner had been previously tested for HIV in 69.6% of cases in Cameroon, 38.6% in Dominican Republic, 12.0% in Georgia and 9.1% in India.

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Table 1-a:
Characteristics of participating pregnant women. Prenahtest ANRS 12127 trial (2009–2011).
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Table 1-b:
Characteristics of participating pregnant women. Prenahtest ANRS 12127 trial (2009–2011).

HIV prevalence in the study sample was 11.6% in Cameroon and below 1% in the three other sites. More than 95% of women disclosed their HIV status to their partner, with comparable rates in both study groups, except in Georgia where disclosure was significantly more likely within the COC group (94.8 versus 78.5%, P < 0.0001). In Georgia, couple communication regarding HIV and condoms during the follow-up period was poor among women from standard posttest HIV counselling group (<40%) and significantly higher among women from COC group (>70%, P < 0.0001). Women in Dominican Republic and Georgia were significantly more likely to have suggested HIV testing to their partner than women from standard posttest HIV counselling group; no difference according to group was observed in Cameroon and India.

Partner HIV testing rates and effect of couple-oriented posttest HIV counselling

Overall, COC resulted in an absolute gain in partner HIV testing rates, which varied between study sites. According to the combined indicator integrating both laboratory and woman's self-reported data on partner HIV testing, 59 partners (24.7%) in Cameroon were tested for HIV in COC group versus 35 (14.3%) in standard posttest HIV counselling group [OR = 1.97; CI = (1.24–3.13)]; in Dominican Republic, 56 partners (23.1%) versus 49 (20.3%) [OR = 1.19; CI = (0.77–1.83)]; in Georgia, 66 partners (26.8%) versus three (1.2%) [OR = 29.57; CI = (9.15–95.56)]; and in India, 86 partners (35.4%) versus 64 (26.6%) [OR = 1.51; CI = (1.03–2.23)] (Table 2).

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Table 2:
Effect of prenatal couple-oriented HIV counselling on partner HIV testing rates (n = 1943). Prenahtest ANRS 12127 trial (2009–2011).

When looking only at the data notified by the laboratory, the effect of COC on partner HIV testing rates remained highly significant in Cameroon, Georgia and in India (P < 0.01) and became significant in Dominican Republic, with a significantly higher proportion of partners tested from COC group compared with standard posttest HIV counselling group [8.3 versus 2.5%, OR = 3.54; CI = (1.40–8.98)].

Adverse events

In total, 77 women reported separating from their partner during the follow-up period, most in Dominican Republic (n = 51). There was no significant difference in union break-ups between women from standard posttest HIV counselling and COC groups in all sites (Table 3). Less than 16% of women reported emotional violence from their partner during the follow-up period. Verbal violence was very rarely reported in Georgia (<3%), however, it was more frequent in Dominican Republic (>17%). Physical violence was reported by less than 7% of women overall. Women from COC group were less likely to report emotional violence than women from standard posttest HIV counselling group in Georgia and India (3.5 versus 11.8% and 9.4 versus 16.0%, respectively), and less likely to report physical violence in Cameroon and India (1.9 versus 6.4% and 6.5 versus 12.8%, respectively) (Table 3).

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Table 3:
Conjugal violence and union break-ups reported during the follow-up period (n = 1726). Prenahtest ANRS 12127 trial (2009–2011).

Factors associated with partner HIV testing

Factors associated with partner HIV testing were documented among women followed-up at least once and for whom all variables of interest were documented (n = 1607). The adjusted models are presented Table 4. In Cameroon, among the factors significantly associated with partner HIV testing (combined indicator) was the fact that the woman had received COC [Adjusted OR (AOR) = 2.4; CI = (1.4–4.0), P < 0.01], was HIV-infected [AOR = 2.4; CI = (1.1–5.0), P = 0.02], reported having ever discussed condoms with her partner [AOR = 2.4; CI = (1.1–5.3), P = 0.03] and that her partner had been previously tested for HIV [AOR = 2.3; CI = (1.3–4.2), P < 0.01]. In Dominican Republic, partners were more likely to have been tested for HIV when the woman perceived her partner as very involved in her pregnancy [AOR = 2.3; CI = (1.3–4.1), P = 0.02, compared with normally involved] and when her partner had been previously tested for HIV [AOR = 3.8; CI = (2.1–7.2), P < 0.01]. In Georgia, partner HIV testing was more likely when the woman had received COC [AOR = 20.5; CI = (5.9–70.5), P < 0.01], when her partner had been previously tested for HIV [AOR = 4.2; CI = (1.4–13.2), P = 0.03] and when she wished to suggest HIV testing to her partner [AOR = 1.9; CI = (1.1–3.7), P = 0.03]. Finally in India, among the factors significantly associated with partner HIV testing were that the woman had received COC [AOR = 1.7; CI = (1.1–2.5), P = 0.01], had been accompanied by her partner to ANC [AOR = 2.0; CI = (1.3–3.1), P < 0.01] and had suggested HIV testing to her partner [AOR = 2.3; CI = (1.1–5.1), P = 0.03].

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Table 4:
Factors associated with partner HIV testing (combined indicator) in Cameroon, Dominican Republic, Georgia and India (n = 1607). Prenahtest ANRS 12127 trial (2009–2011).

Discussion

Our primary result is that, as hypothesized, a behavioural intervention delivered to pregnant women, which takes into account their couple relationship, can increase the uptake of HIV testing among men in the context of ANC. In the context of increased investments towards the elimination of mother-to-child transmission of HIV, COC, integrated within ANC and PMTCT services in replacement of standard posttest HIV counselling, could contribute to improve the coverage of men's HIV testing worldwide. In low HIV prevalence settings, valorising such a beneficial effect of prenatal HIV counselling and testing is all the more so relevant that the number of paediatric HIV infections avoided by PTMCT are a priori limited.

We observed different effects of COC across study sites, rather limited in Dominican Republic and very important in Georgia. This suggests that the level of HIV prevalence may not be a key determinant of the acceptability of partner HIV testing. The analysis of the socio-behavioural factors associated with partner HIV testing provides further insight on why and how COC may have influenced women's attitudes and their partner's behaviour. In India and Georgia, men's presence in ANC is relatively frequent and in our study was used as an opportunity for partner HIV testing (significant association in Georgia in univariate analysis only). However, partner HIV testing in ANC may be challenging in certain settings [20]. Qualitative results from our pretrial pilot study [18] showed that, in the Cameroon and Dominican Republic study sites, the attitudes of healthcare workers towards men were often harsh, ANC wards were too crowded, and thus men felt ill-at-place, as reported by others in Uganda [21]. Partners in these two sites may have preferred to be tested for HIV in non-ANC laboratories or free-standing HIV counselling and testing centres. And this is why, although the laboratory logbooks provide verifiable data, they may also underestimate the rates of partner HIV testing. Further, the fact that overall fewer partner HIV tests were performed at the site laboratories, as compared to those self-reported by women, may to some extent reflect a social desirability bias, whereby women over-reported partner HIV testing to please the interviewer, which could also explain the absence of difference in self-reported partner HIV testing rates among women from standard posttest HIV counselling and COC groups.

We observed that in Cameroon, Dominican Republic and Georgia, men were more likely to be tested for HIV during their partner's pregnancy when they had already been tested once. Understanding men's motivation and perceptions of the benefits of HIV testing, both as individuals and within their couple, is thus crucial to further improve uptake [22–26]. In addition, partners were more likely to have been tested when women had suggested HIV testing to their partner in Cameroon and India. Partner HIV testing was not associated with verbal couple communication on HIV in Dominican Republic where local gender roles may not place women as the best initiators of partner HIV testing. A ‘medical prescription’ from health workers could be helpful to encourage partners to be tested [27], however, the efficacy of such a strategy was not confirmed in a recent trial [14]; invitations distributed by influential people may be another intervention successful in prompting couples to seek joint HIV testing as shown in Rwanda [28]. Finally in Cameroon, partner HIV testing was associated with couple communication on condom. These results suggest that COC may have supported women who had already initiated a conjugal discussion around HIV prevention to suggest HIV testing to their partner. They also confirm that HIV testing remains a key entry point for the prevention of sexual risks within the couple.

Another important result of our trial is that not only was COC shown to be safe but it also seemed to have potential benefits in reducing partner violence in Georgia and India. The counselling, education and role play activities conducted during COC are likely to have helped women in finding the right moment and the right words to discuss sensitive topics with their partner, such as HIV prevention and specifically partner HIV testing.

In spite of the positive impact of COC, partner HIV testing rates remained low in the four study sites, with overall less that a third of men tested for HIV during their partner's pregnancy. With the scaling-up of treatment programmes, HIV testing will be increasingly available in primary healthcare centres, within mobile clinics, through door-to-door programmes or even maybe within community sites such as bars [29]. Multiplying HIV testing options for men and mainstreaming HIV counselling and testing services in community development and health programmes will be critical to promote partner HIV testing as a culturally acceptable behaviour and increase the acceptability of HIV prevention initiatives targeting couples.

This study has certain limitations. First, COC is a brief, single-session counselling intervention and, as such, was certainly limited in the amount of individualized skill building it could provide. Second, because of the large socio-cultural differences and variations in participant characteristics according to the country, we conducted four separate explanatory models to assess the factors associated with partner HIV testing, which means that we could not directly compare results across sites. Finally, because a large proportion of men tested for HIV in Cameroon were tested outside the study site, their HIV status could not be confirmed, and thus we were unable to investigate sero-discordance as an explanatory variable.

Overall, however, this trial is the first to show the efficacy of a counselling intervention in increasing partner HIV testing rates in low-resource settings. Further, the multisite design allowed documenting the impact of COC according to diverse socio-cultural backgrounds and in different epidemiological contexts. Investing in couple-oriented prenatal HIV counselling and integrating a couple approach to HIV prevention within routine mother and child health services, at the health centre level as well as within the community, could be a simple public health strategy contributing to the elimination of mother-to-child transmission of HIV and to improve the management of sexual risks in a conjugal context.

Acknowledgements

We thank our fieldwork team for their efforts and the counsellors dedicated to providing women with the best service possible. Special thanks to Brigitte Bazin, Claire Rekacewicz and Laurence Quinty (ANRS), and Catherine Wilfert (EGPAF) for encouraging the study team throughout the trial. We would like to thank also Karen Malateste for her involvement in the early stages of the analysis.

J.O.G. wrote the study proposal, was the overall trial coordinator and led the process of data analysis, interpretation, and paper writing. All authors participated in designing the study and the questionnaires. P.T., M.M., E.P-T, S.D., M.B. were the local site coordinators, provided advice during study design and managed the fieldwork. F.D., P.T. and A.D.L. were the study investigators and provided advice during study design and fieldwork. All authors cointerpreted the data and co-wrote the article. E.B. and M.P. conducted the statistical analysis. S.K. and F.E. provided advice during fieldwork, data analysis, data interpretation, and writing.

This research was sponsored and primarily funded by the Agence Nationale de Recherches sur le SIDA et les hépatites virales (French Nationale Agency on AIDS Research) (grant ANRS 12127). Complementary funding was provided by the Elizabeth Glaser Pediatric AIDS Foundation (Sub-agreement 354–07).

No funding bodies had any role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

ClinicalTrials.gov: NCT01494961.

Members of the Prenahtest ANRS 12127 Study Group

Principal investigators: François Dabis, Patrice Tchendjou

Trial coordinator: Joanna Orne-Gliemann

Site coordinators: Maia Butsashvili (Georgia), Shrinivas Darak (India), Marija Miric (Dominican Republic), Eddy Perez-Then (Dominican Republic - Investigator), Patrice Tchendjou (Cameroon)

Methodology, biostatistics, data management (Bordeaux): Eric Balestre, Karen Malateste, Mélanie Plazy

Data collection: Denise Amassana (Cameroun), Tatiana Etounou (Cameroon), Mukta Gadgil (India), Maia Kajaia (Georgia), Maitreyi Kulkarni (India), Mildred Martinez (Dominican Republic), Angeline Ngo Essounga (Cameroon), Laura Nunez (Dominican Republic), Lucia Santos (Dominican Republic), Marina Topuridze (Georgia)

Social sciences expertise: Annabel Desgrées du LoÛ, Fred Eboko

Public health expertise: Sanjeevani Kulkarni, Vinay Kulkarni, Eddy Perez-Then

Conflicts of interest

There are no conflicts of interest.

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Keywords:

counselling; HIV; male; testing; trial; women

© 2013 Lippincott Williams & Wilkins, Inc.