Male partners’ involvement in prevention of mother-to-child HIV transmission in sub-Saharan Africa: A systematic review

Abstract In sub-Saharan Africa (SSA), male partners are rarely present during prevention of mother-to-child transmission (PMTCT) services. This systematic review aims to synthesize, from a male perspective, male partners’ perceived roles, barriers and enablers of their involvement in PMTCT, and highlights persisting gaps. We carried out a systematic search of papers published between 2002 and 2013 in English on Google Scholar and PubMed using the following terms: men, male partners, husbands, couples, involvement, participation, Antenatal Care (ANC), PMTCT, SSA countries, HIV Voluntary Counseling and Testing and disclosure. A total of 28 qualitative and quantitative original studies from 10 SSA countries were included. Men's perceived role was addressed in 28% (8/28) of the studies. Their role to provide money for ANC/PMTCT fees was stated in 62.5% (5/8) of the studies. For other men, the financial responsibilities seemed to be used as an excuse for not participating. Barriers were cited in 85.7% (24/28) of the studies and included socioeconomic factors, gender role, cultural beliefs, male unfriendly ANC/PMTCT services and providers’ abusive attitudes toward men. About 64% (18/28) of the studies reported enablers such as: older age, higher education, being employed, trustful monogamous marriages and providers’ politeness. In conclusion, comprehensive PMTCT policies that are socially and culturally sensitive to both women and men need to be developed.


Introduction
Every year, an estimated 1.5 million HIV-positive women become pregnant, and 90% of total HIV infections in children that are acquired through mother-to-child transmission (MTCT) during either pregnancy, labor or breastfeeding occur in sub-Saharan African (SSA) countries (UNAIDS 2013). A study carried out in Zambia shows that the majority of HIV transmission is reported to occur within stable couples (Dunkle, Stephenson, Karita, Chomba, Kayitenkore, Vwalika, et al. 2008), the highest risk being women with low control over their sexuality (Bhagwanjee, Govender, Reardon, Johnstone, George & Gordon 2013;Greiga, Peacock, Jewkes & Msimang 2008), low risk perception for HIV acquisition and whose male sexual partners have relatively high-risk sexual behaviors (Larsson, Thorson, Nsabagasani, Namusoko, Popenoe & Ekström 2010). In spite of remarkable achievements in the reduction of new HIV infections from 3.4 (3.1-3.7) million in 2001 to 2.3 (1.9-2.7) million in 2012, challenges remain. In the most affected SSA countries, HIV and AIDS-related diseases are still amongst the main causes of disease and death among women and children (UNAIDS 2013).
Programs to curtail mother-to-child HIV transmission (PMTCT) have been in place for almost 15 years worldwide. In most affected SSA countries, PMTCT is a component of antenatal care. Currently, there is increased access to free anti-retroviral drugs for PMTCT globally, which are also more effective, with simpler dosing and easy storage (WHO 2012). Taking advantage of anti-retroviral drugs availability, countries with a high HIV and AIDS burdens are escalating the provision of PMTCT interventions to respond to demands in underserved areas. The expansion needs innovation in order to strengthen the traditional PMTCT approach, which addresses only women and children, such as to include male partners. There is overwhelming evidence that male partners' participation in PMTCT is fundamental (Reece, Hollub, Nangami & Lane 2010;Semrau, Kuhn, Vwalika, Kasonde, Sinkala, Kankasa, et al. 2005;Theuring, Mbezi, Luvanda, Jordan-Harder, Kunz & Harms 2009), is strongly recommended by World Health Organization and has been contemplated in strategies of many MTCT control programs.
From a social perspective, traditional systems in both rural and urban settings in most SSA communities are deeply rooted in male authority over women's health, particularly in its sexual and reproductive aspects (Larsson et al. 2010;Orne-Gliemann et al. 2010)., Therefore, in these SSA settings, with the predominance of HIV heterosexual transmission, safeguarding current achievements and furthering PMTCT improvements demand combined actions that include women and their male partners as actors toward interruption of MTCT of HIV infection.

Review aims
This systematic review aims to identify and synthesize men's perceived role, barriers and enablers regarding their involvement in PMTCT in SSA countries and highlight persisting gaps.

Methods
To be well informed on the subject of this study, we carried out a systematic search in English on Google Scholar, and PubMed. Additional searches were carried out on WHO, UNAIDS, UNICEF, UNFPA publications and local gray literature. However, the systematic presentations here were limited to published articles in peer-reviewed journals, between January 2002 and December 2013. The terms used in the search included: men, male, husbands, couples involvement, participation Antenatal Care (ANC), PMTCT, SSA countries, HIV Voluntary Counseling and Testing (VCT), VCT, HIV Testing, HIV Disclosure, in different combinations accordingly. Published articles reporting on male involvement with PMTCT, HIV counseling and testing and sero-status disclosure were sought after. Specifically, the main outcomes sought were men's perceived role, barriers, obstacles, facilitators, predictors and enablers to PMTCT. Studies were identified through their titles, retrieved and screened abstracts and full texts, and lastly, the articles were assessed for eligibility and inclusion in this systematic review. Duplicated studies were eliminated. To be eligible for this review, the study was required to be an original qualitative or quantitative study carried out in SSA, addressing men's involvement in PMTCT, HIV counseling and testing and sero-status disclosure from a male perspective. Studies were excluded if not carried out in SSA, not related to PMTCT, reported women's perspectives, and did not include meńs perspectives. Each abstract and/or full paper selected was read several times, data were extracted regarding, country, authors, study aim, study site and population, male partner PMTCT attendance, HIV counseling and testing, sero-status disclosure, perceived male role, barriers (obstacles, hindrances) and enablers (predictors, facilitators). RM analyzed and summarized the data. MS and OD reviewed the processes of studies selection and data extraction analyses (Fig. 1).
(1) Male partners' perceived roles on PMTCT were cited in (28%) 8/28 studies. We identified men's perceived direct and indirect roles. The direct role most frequently stated was financial support (Byamugisha, Tumwine, Semiyaga, & Tylleskär 2010;Kwambai et al. 2013;Larsson et al. 2010;Nkuoh et al. 2010;Theuring et al. 2009), followed respectively by decision-making, responsibility over women's health (Koo, Makin, & Forsyth 2013a;Kwambai et al. 2013;Larsson et al. 2010; Theuring et al.   (Kwambai et al. 2013;Nkuoh et al. 2010;Theuring et al. 2009). One study referred to indirect support through improvement of communication between couples (Aarnio, Aarnio, Olsson, Chimbiri & Kulmala 2009), faithfulness during pregnancy and support to HIV-positive women (Aarnio et al. 2009). Financial support was stated in 62.5% (5/8) of the studies (Tables 1 and 2). Most men reported believing that their main role was that of a breadwinner (Larsson et al. 2010;Musheke, Bond & Merten 2013) and provider of money for health expenses, ANC/PMTCT clinic fees, food and family well-being (Larsson et al. 2010;Nkuoh et al. 2010;Theuring et al. 2009). Nevertheless, the meńs role of guaranteeing family income and having to work is often used as an excuse to not accompany their wives to ANC/ PMTCT clinics (Kwambai et al. 2013;Larsson et al. 2010;Musheke et al. 2013). According to some men's statements, as part of their responsibility (Aarnio et al. 2009;Theuring et al. 2009) and in spite of their awareness of women's financial dependence, they assume that women need their permission to go to ANC/PMTCT sessions because only male partners can decide

Original Article
Journal of Social Aspects of HIV/AIDS VOL. 12 NO. 1 2015 which clinic to attend and which ANC/PMTCT care they can afford (Kwambai et al. 2013;Theuring et al. 2009). Other men perceive that they have to persuade women and sometimes obligate them to attend ANC/PMTCT clinics or see a traditional birth attendant in reaction to women's careless health conduct, ignorance or laziness (Kwambai et al. 2013). Few men see their role as extending to sharing responsibility during pregnancy, childbirth and child care (Nkuoh et al. 2010), as well as helping with cooking and housework (Kwambai et al. 2013;Nkuoh et al. 2010;Theuring et al. 2009) and improving women's diets (Kwambai et al. 2013).
(2) Perceived barriers for male partners involvement in PMTCT were present in 85% (24/28) of the studies, and comprised socioeconomic constraints, health system factors, cultural beliefs, gender inequity, limited knowledge of ANC/PMTCT, mistrustful marriages and inadequate couples' communication patterns.
(2.1) Socioeconomic barriers cited in 39.2% (11/28) of the studies consisted of: (2.1.2) Work commitments: Overlap of clinic appointment schedules and working hours (Duff et al. 2012;Koo et al. 2013a;Orne-Gliemann et al. 2010;Reece et al. 2010;Theuring et al. 2009;Tweheyo et al. 2010), sporadic jobs and casual labor, jobs with little control of assignments (Reece et al. 2010) were frequently cited. The belief that ANC/PMTCT was only for women and children had negative impact at meńs workplace leading them not to request leave to attend PMTCT clinics (Theuring et al. 2009). Accompanying women to PMTCT was a stigma for men, as they feared not being authorized by their employers to attend PMTCT with their spouses, and worried with confidentiality issues linked to HIV/PMTCT (Reece et al. 2010).
(2.1.3) Time constraints: Time away from job including the waiting time at the clinic (Byamugisha et al. 2010;Duff et al. 2012;Nkuoh et al. 2010;Theuring et al. 2009;Tweheyo et al. 2010) as well as the time needed for HIV testing, including receiving counseling, testing and returning for results were seen as barriers (Koo et al. 2013a;Reece et al. 2010). Some men said that they were unable to spend the entire day alongside their partners at clinics (Koo et al. 2013a) and that all of the procedures were time consuming (Koo et al. 2013a) and a nuisance for them (Tweheyo et al. 2010).
(2.2) Health systems related barriers found in 39% (11/28) studies were as follows: (2.2.1) PMTCT targets and scope: Men perceive ANC/PMTCT clinics as unfriendly (Koo et al. 2013a;Kwambai et al. 2013;Larsson et al. 2010;Orne-Gliemann et al. 2010), dominated by women as both clients and care providers (Koo et al. 2013a) and they feel totally ignored (Kwambai et al. 2013). ANC/ PMTCT interventions were focused on HIV and neglected general wellness, fatherhood and father's roles, a common unmet need particularly expressed by young fathers (Koo et al. 2013a;Larsson et al. 2010;Theuring et al. 2009). HIV testing was not mandatory for male partners within PMTCT (Koo et al. 2013a). The few accompanying male partners were frequently asked to wait outside the room (Byamugisha et al. 2010;Orne-Gliemann et al. 2010;Theuring et al. 2009). In this regard, male partners wonder why they should accompany their partners to ANC/PMTCT visits (Byamugisha et al. 2010;Theuring et al. 2009).    the results, could lead to domestic violence (Aarnio et al. 2009;Duff et al. 2012;Falnes et al. 2011;Mlay, Lugina & Becker 2008). Cases of sero-discordance, involving positive woman can culminate in divorce. If the man is positive, the consequences are lighter often involving quarrels and denial (Kiarie et al. 2006;Larsson et al. 2010).
(2.4) Men's inadequate knowledge stated in 50% (14/28) of the studies included: Some men believing their HIV status would always be the same as that of their wives (Falnes et al. 2011;Katz, Kiarie, John-Stewart, Richardson, John & Farquhar 2009;Koo et al. 2013a), but MTCT as only the mother's responsibility (Koo et al. 2013a). Others were unaware of the availability of ANC HIV testing and counseling (Aarnio et al. 2009), felt insufficiently involved (Duff et al. 2012;Kwambai et al. 2013), unclear on the concept of the father's involvement in ANC/PMTCT (Theuring et al. 2009) and felt that there was a lack of opportunity to learn about HIV/AIDS and Highly Active Antiretroviral Therapy (HAART) (Chinkonde, Sundby & Martinson 2009;Duff et al. 2012). Some could repeat broadcasted HIV testing messages while still not going for HIV testing (Larsson et al. 2010). Some did not understand the role of ANC/PMTCT if the mother and baby were well (Mohlala et al. 2012) or see the advantages of testing where there were no symptoms (Auvinen, Kylmä, Välimäki, Bweupe & Suominen 2013;Larsson et al. 2010;Theuring et al. 2009).
(2.6) Distrustful marriages and couples' communication patterns: Some men described their marriages as unstable and distrustful (Auvinen et al. 2013;Larsson et al. 2010;Reece et al. 2010;Walcott et al. 2013) with mutual suspicions of extra-marital relationships, but particularly among men (Koo et al. 2013a;Larsson et al. 2010). On the other hand, some traditional norms prohibit women to initiate HIV and reproductive health conversations (Larsson et al. 2010), others intentionally neglect information provided by wives (Larsson et al. 2010). These situations contribute to turning communication around HIV infection into a sensitive and intricate subject, told in the third person (Koo et al. 2013a;Larsson et al. 2010;Orne-Gliemann et al. 2010;Reece et al. 2010). Other men suspect that their wives have either distorted or withheld some information (Chinkonde et al. 2009;Musheke et al. 2013) and feel forced into getting tested by their partners, with the collusion of health workers (-Musheke et al. 2013), some have never been requested to attend ANC/PMTCT sessions and thought they were not needed (Mohlala et al. 2012).
(3.2) Male-friendly PMTCT services were dependent on availability of specific information on ANC/PMTCT directed toward men (Aarnio et al. 2009;Byamugisha et al. 2010;Mohlala et al. 2012;Reece et al. 2010;Theuring et al. 2009), understanding of the value of the services offered, and the kindness and politeness of health workers (Reece et al. 2010;Theuring et al. 2009). Men were also keen to receive invitation letters, health information addressed directly to them from health workers and those other than their partners (Byamugisha et al. 2010;Mohlala et al. 2012;Reece et al. 2010;Theuring et al. 2009), and clinic hours during non-work period such as weekends, appointments outside ANC/PMTCT clinics, for example, at their homes or work places (Larsson et al. 2010;Reece et al. 2010). Men were also in favor of learning more about fatherhood issues, couples' VCT, existence of health products, drugs and promotion of refresher courses and customer care skills for healthcare providers (Byamugisha et al. 2010).
(3.4) Education: In South Africa (Koo et al. 2013a), men with higher levels of education were 5.8 times more likely to attend ANC clinics, and 2.7 times more likely to be tested for HIV in Ivory Coast (Brou et al. 2007

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Journal of Social Aspects of HIV/AIDS VOL. 12 NO. 1 2015 (3.5) Employment: Most men who participated in the studies included in this review were employed (Msuya et al. 2008). For 58 (47%) men, it was important to receive an official letter to present to their employers for permission to attend ANC/ PMTCT clinics (Reece et al. 2010).
(3.6) Men's empowerment: Promotion of couple-and family-centered PMTCT interventions (Koo et al. 2013a) and mobilization of men for PMTCT using male peers, churches and mosques were found to be effective (Byamugisha et al. 2010). Encouraging initiatives exclusively for men, led by men, promoting men's psychosocial support groups, community education through men's support groups as peer educators are all approaches that support men to attend PMTCT sessions as well as to continue sensitizing and educating other men in their communities (Mohlala et al. 2012;Reece et al. 2010). It is important that the role of men is clearly defined to better support women at PMTCT (Koo et al. 2013a;Mohlala et al. 2012).

Discussion
This review reiterates the low level of male partners' involvement in PMTCT. Fig. 2 summarizes multiple factors that influence men's involvement in PMTCT. The need and demand for men involvement at PMTCT clinics are influenced by the prevailing understanding of PMTCT not being a men's role, but rather a women's issue (Aarnio et al. 2009;Duff et al. 2012;Larsson et al. 2010;Nkuoh et al. 2010;Theuring et al. 2009;Tweheyo et al. 2010). The role of men is perceived rather to be as provider of money for family sustenance and payment of eventual costs for care related to delivery or baby care (Falnes et al. 2011;Larsson et al. 2010;Mohlala et al. 2012;Nkuoh et al. 2010;Orne-Gliemann et al. 2010;Reece et al. 2010;Theuring et al. 2009). Traditional cultural concepts about gender roles (Falnes et al. 2011;Reece et al. 2010;Theuring et al. 2009) and social constructions (Tweheyo et al. 2010) favoring male partner superiority may inhibit them to assume a more active role in PMTCT. On the other hand, the perceived inferiority of women (Duff et al. 2012;Falnes et al. 2011;Larsson et al. 2010) and their greater responsibility over pregnancy and childbearing (Falnes et al. 2011;Larsson et al. 2010;Theuring et al. 2009) contribute for their greater role and eventually lonesome involvement in PMTCT.
Some men miss opportunities to participate in PMTCT because they neglect information given by their female partners (Duff et al. 2012;Falnes et al. 2011;Larsson et al. 2010). Nevertheless, some men express lack of knowledge and awareness for their insufficient involvement with their spouses' pregnancy and PMTCT process (Duff et al. 2012;Kwambai et al. 2013;Larsson et al. 2010). Men were not concerned with getting tested or with prevention of HIV infection from mother to their child even though they were able to repeat the broadcasted HIV prevention messages (Larsson et al. 2010). These attitudes and behaviors highlight the need for urgent improvement of men's involvement through multi-sectoral approaches, including those aimed at communities, in order to produce behavior change, decrease negative beliefs and cultural practices.
Besides work commitments (Theuring et al. 2009) and alleged lack of time (Aarnio et al. 2009;Byamugisha et al. 2010;Falnes et al. 2011;Larsson et al. 2010;Mulongo et al. 2010;Nkuoh et al. 2010;Theuring et al. 2009) reported in reviewed studies, there is also a lack of legislation ensuring fathers' greater participation at PMTCT (Orne-Gliemann et al. 2010;Tweheyo et al. 2010). This legislative gap is even worse when employers also understand PMTCT as women issue (Nkuoh et al. 2010;Reece et al. 2010) and hinder their male employees from attending PMTCT services (Larsson et al. 2010). Additionally, men fear to be asked by their employers to disclose their HIV status, which may also prevent them from asking permission to attend PMTCT sessions with their spouses (Reece et al. 2010). Money constraints may also be a real barrier for male partner PMTCT attendance (Byamugisha et al. 2010;Duff et al. 2012;Reece et al. 2010;Tweheyo et al. 2010). However, reviewed studies make no mention of increasing male partner attendance even if PMTCT services are free of charge.
For the most conservative communities among the sub-SSA Countries included in this study, pregnancy and childbearing are female responsibility (Larsson et al. 2010;Reece et al. 2010;Theuring et al. 2009) and family provision, more a male duty. There is no culturally perceived role for male partners at PMTCT (Byamugisha et al. 2010;Koo et al. 2013a). Also, women are prohibited from discussing sexual and reproductive issues with their male partners (Koo et al. 2013a;Larsson et al. 2010), restricting therefore sharing of information and appeal for their male partners involvement at PMTCT (Duff et al. 2012). So, an important role has to be played by the less traditionalist community members (open-minded or unprejudiced), civil society faith-based organizations, traditional healers and traditional birth attendants in promoting reforms of community norms and taboos (Byamugisha et al. 2010;Larsson et al. 2010;Mohlala et al. 2012) to enhance men understanding of their parenthood role and need for their involvement in PMTCT.
Even though men acknowledge the (Koo et al. 2013a;Kwambai et al. 2013) challenges women face in directing conversations, most of them still are not receptive to discuss HIV-related issues which contributes to couples' communication gaps and misunderstandings (Larsson et al. 2010;Orne-Gliemann et al. 2010;Reece et al. 2010;Villar-Loubet, Bruscantini, Shikwane, Weiss, Peltzer & Jones 2013). Having monogamic families (Brou et al. 2007), having children (Katz et al. 2009), stable and faithful relationships (Koo et al. 2013b) were all identified as enabling factors. However, polygamy and extra-marital relationships are relatively common in these settings and may interfere in males' involvement in PMTCT.
Globally and at country level, the PMTCT policies have been conceived to promote female reproductive and sexual rights.
However, in more traditional settings in SSA Countries, the political focus on HIV epidemic feminization, PMTCT (Falnes et al. 2011) and the greater emphasis on mother and child health may reinforce some men's cultural background which tends to confer on women all responsibility for pregnancy, blame for eventual HIV infection and transmission to the child (Falnes et al. 2011). This seems to be one of the reasons why MCH nurses often feel not prepared to address health, sexual and reproductive needs of men (Koo et al. 2013a;Larsson et al. 2010).
We can conclude that the relationship of men with their community's cultural beliefs, social norms, work commitments, local health policies and healthcare delivery systems are some important factors influencing men's involvement in PMTCT. At global and local levels, reproductive and sexual health approaches should be revised to address men's, women's and community's roles in reproductive health and childbirth. Thus, there is a need for greater education, health and labor sector reforms that contribute to improve national policies and strategies for men's involvement in PMTCT. Innovative multi-sectoral reforms aimed at men's involvement in PMTCT should also promote free health services to diminish the financial pressure on the financially more vulnerable men. Due to the urgency of improving men's involvement in PMTCT, feasible low-cost enablers should be better explored and implemented, for instance, the involvement of male community leaders and faith-based organizations, employers, training of health workers to improve understanding of male health and reproductive needs. Innovative strategies should also see opportunities for scheduling men or couples for weekday afternoon PMTCT services.
Although the findings of this review present valuable evidence about the roles, barriers and enablers of men's involvement with PMTCT, there are some limitations to consider. The review analyzed only reported evidence from published studies retrieved from PubMED and Google Scholar, which might exclude some studies and/or evidence such as existing gray literature in SSA Countries. On the other, the SSA Countries are very diverse in terms of ethno-cultural background and thus the evidence produced in this study might not be generalizable to all diverse settings (urban, rural, etc.) and contexts in these countries.

Funding
This work was supported by Scholarship provided jointly by University Eduardo Mondlane (UEM) and Flemish International University Coopreation (IUC).