Abstract
Effective interventions tailored to specific types of behaviors and contexts are needed for women at risk for HIV acquisition. Oral pre-exposure prophylaxis (PrEP) is an efficacious HIV prevention intervention that uses antiretroviral drugs to reduce the risk of acquiring HIV infection. In Mozambique, HIV remains a major public health concern, with a national prevalence of 13%. Studies have demonstrated that the migration of male miners between southern provinces of Mozambique and South Africa is contributing to the HIV epidemic in Mozambique. This increased risk is associated with the engagement of male miners, while separated from their partners, in sexual relationships with other women, including transactional sex workers, in a hyperendemic setting in South Africa. We conducted 25 in-depth interviews with a subset of female partners in a stable relationship with migrant miners participating in a prospective cohort study to assess the feasibility, acceptability, and adherence to daily oral short-term PrEP. Drug levels were available for the participants, as reported in an earlier study. Interviews were recorded, transcribed, and submitted for qualitative thematic analysis. The major themes identified were the benefits of taking PrEP, the ease of taking daily PrEP, the reluctance to disclose PrEP use to partners, the lack of changes in sexual behavior, and prevailing gender dynamics and how they impact women's ability to access PrEP and other HIV prevention interventions.
Introduction
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The compelling evidence for PrEP efficacy and acceptability led the World Health Organization (WHO) to recommend offering PrEP to all individuals at substantial risk of HIV infection. 4 Consequently, a number of PrEP demonstration projects have been implemented across different settings, including in several southern African countries. 5 However, evidence is still needed to inform optimal PrEP implementation strategies to maximize its use during periods of substantial risk, thereby increasing potential impact on HIV epidemic. 4
In Mozambique, where adult HIV prevalence is 15% for women and 10% for men, 6 heterosexual transmission accounts for ∼9 out of 10 new infections. 7 A study on the modes of HIV transmission reported that in 2013, most new HIV infections (40%) were found in the southern region of Mozambique, an area that accounts for only 24% of the adult population in the country. 8 Gaza Province, a southern province with the highest HIV prevalence at 24%, 6 serves as a source of migrant labor for the mines and industries in South Africa. Studies have demonstrated that many Mozambican miners who work in South Africa, separated from their families, solicit sex from sex workers, a high-risk activity in a hyperendemic environment. 9 –11 Previous studies have shown that migration between Gaza Province and South Africa is fueling the epidemic in southern Mozambique. 12,13 Moreover, data from a recent integrated biological and behavioral survey among Mozambicans working in mines in South Africa showed an HIV prevalence of 22%. 14 Approximately 80% of those surveyed had one wife in Mozambique and 38% reported at least one occasional sexual partner in the 12 months preceding the survey. Of these, approximately half reported using condoms consistently at last sex with casual partners, but only one in five reported using condoms at last time they had vaginal sex. 14 Many miners from Gaza return home during Christmas and Easter breaks. In fact, a seasonal pattern of births has been observed among female partners of migrant workers in Gaza Province, Mozambique, with a noticeable increase occurring in September, 9 months after the annual Christmas visits home. 15
Given the urgent need for effective HIV interventions in Gaza and the potential for PrEP as an effective prevention tool, ICAP at Columbia University in partnership with the Gaza Health Directorate and supported by WHO conducted an initial study to explore willingness of HIV-negative female partners of migrant miners in Gaza to consider short-term PrEP as a prevention option during periods of visits by their male partners. 16 Results from this study suggested high interest in short-term use of PrEP during periods of risk for HIV infection. Based on these findings, a prospective cohort study assessing the feasibility, acceptability, and adherence to daily short-term PrEP within the same population was conducted. 17 In this article, we describe the findings from a qualitative substudy, designed to elicit feedback from female partners of migrant miners on their experiences taking short-term daily oral PrEP.
Methods
Study design
During April 2016, we conducted in-depth interviews (IDIs) with a subset of female partners of migrant miners participating in a prospective cohort study. The parent study aimed to evaluate the feasibility, acceptability, and adherence with short-term daily oral PrEP among 74 HIV-negative female partners of male miners, in Chibuto and Xai-Xai, two districts of Gaza Province, Mozambique.
Daily oral PrEP [tenofovir/emtricitabine (TDF/FTC 200 mg/300 mg)] was offered for a 6-week period to prevent HIV acquisition during partners' return home from the mines in South Africa, for Easter break in March/April 2016. Eligible women who consented were enrolled and initiated into PrEP 2 weeks before their husband's arrival, were offered PrEP for 2 weeks while their partner was at home and for 2 weeks after their partner had returned to the mines. At week 4 and week 6 after PrEP initiation, a follow-up visit was conducted where sociodemographic data were collected alongside adherence levels measured by self-report, pill count, and dry blood spot cards for testing of ARV drug levels. A final follow-up visit was conducted 2 weeks after PrEP discontinuation at week 8. During all follow-up visits, blood specimens were collected for hepatic alanine aminotransferase (ALT) levels, HIV testing, and preparation of dried blood spots for drug levels.
Substudy design
Between weeks 6 and 8, of the 74 women enrolled in the study of short-term PrEP use, a subset of women was invited to participate in a single IDI. We purposively included women who were available to be interviewed and who had higher and lower self-reported levels of PrEP adherence.
Data collection
We used a semistructured IDI guide to explore women's experiences as study participants, including main positive and negative outcomes, facilitators, and challenges while taking daily PrEP, disclosure of study participation, willingness to continue taking PrEP, and willingness to recommend PrEP to others.
Data analysis
All IDIs were conducted in Portuguese or Changana, audiorecorded, and transcribed verbatim. The transcripts were then translated into English. A qualitative researcher reviewed the interviews using a thematic analysis approach to identify codes and broad analytic thematic categories. A structured coding scheme was developed and the data were then entered and analyzed using Atlas.ti Version 1.0.37. Theme descriptions were formed to explain specific findings from the analysis and illustrated with quotes. Approximately 30% of the initial transcripts were double-coded by an independent qualitative researcher to check intercoder reliability on selected codes.
In addition, participant demographic, behavioral, and biomedical variables were summarized as percentages to allow comparison between the subgroup of women participating in IDIs and the rest of participants from the cohort study. These analyses were performed using Stata 14.1.
Ethics
The study was approved by the World Health Organization Ethics Review Board, the Mozambique National Bioethics Committee for Health (CNBS), and the Columbia University Medical Center Institutional Review Board.
Results
Participants' characteristics
A purposeful sample of 25 women participated in the IDIs. Participants' demographic and behavioral characteristics for this subset were similar to all participants (Table 1). The majority of women were aged between 36 and 49 years, were in a long-term stable relationship with a migrant miner (mean time in relationship, 19 years), and never or rarely used condoms with their partner (76%). Approximately one-third had never been tested for HIV before study participation and less than half knew their partner's HIV status.
IDI, in-depth interview; IQR, interquartile range.
At the week 4 follow-up visit, levels of detectable drug among the subset of participants interviewed were similar to all study participants (Table 2). Among those interviewed, self-reported adherence was 88%, adherence measured by pill count was 96%, and 76% had detectable drug levels for PrEP.
Tenofovir diphosphate levels in dried blood spots.
The total does not equal 100% because it was a multiple choice question.
Everything these pills brought me were good things
Overall, participants reported that being part of the study was a positive experience because it made them feel good for a number of reasons. The main reason they cited was the additional protection from being infected with HIV regardless of their partner's sexual behavior while working in the mines in South Africa and their refusal to use condoms when back home. Even for the three participants who knew that their husbands were on ART, having access to PrEP was seen as something good to “double” their protection.
The good things it [PrEP] brought for me was to give me more hope in life, because without protection I could even die of HIV, but now that I found these drugs I am confident that I will not die because of HIV.
I felt quite comfortable with taking these drugs, they are very important in my life to prevent many diseases (…) In case my partner would be infected (with HIV), I will not get it. I want to prevent myself because my husband stays a long time away from home and when he comes back, he can infect me with HIV through unprotected sex. To make matters worse he does not accept to use a condom with me.
Having the opportunity to get HIV tested and being relieved to find out that they were HIV negative were also reported as a very positive experience by the participants. Knowing that after testing they would have access to a new HIV prevention method also motivated women to take the test and to be part of the study.
Participating in the study made me feel more reassured and pleased, to know that really I am negative, it gives me more strength to continue living without HIV, and also happy to know what to do, not to become infected with HIV.
PrEP brought me something good because I had doubts about my HIV status, because my husband is infected and I wondered how it could be that I don't have this disease, that's why I was very worried and when they told me about PrEP, I went to see if I could get these pills to prevent myself.
Another positive factor noted by a few women was the transport reimbursement they received for every follow-up visit, which made participants feel supported and removed a significant barrier to study participation.
Other positive thing was that we had a transport allowance. As I live far away, imagine if I had to come using my money I wouldn't have been able to come and participate in this study, maybe I would give up. I felt a lot of joy in joining the study mainly knowing that through it, I will be prevented for a long time.
Nevertheless, a few participants mentioned that the strongest discomfort they felt was drawing blood at every visit to assess adherence to PrEP by measuring drug levels in blood. Participants felt anxious and feared becoming weak due to this blood draw.
For me all this was easy from the beginning, the only difficult thing was to get blood taken almost periodically. In my life this thing of taking blood has not happened to me before, I just received blood because of the lack of it in my body, while there were no vitamins, or food to replace that blood that they draw from us many times. So the extraction of blood was the thing that almost made me give up this study.
PrEP was good because it did not cause me any harm
Taking PrEP was also framed as a positive experience in view of the absence of adverse events experienced by the participants. Half of the participants said that contrary to their initial fears, taking PrEP did not produce negative changes in their bodies and also did not affect their daily routines.
I just felt good because I didn't have any negative reaction, I feel just like I felt before taking (PrEP).
Because I didn't spend anything, I feel my life was renewed, and I complied taking it (PrEP). I didn't feel any pain, and not even side effects, I took [the pills] till I finished all, I first took 30 and then 15 tablets, I didn't get sick, I didn't get pains in the eyes or ears or not even the stomach.
Taking PrEP daily was easy
We explored how women experienced the daily intake of PrEP. In general, participants felt that it was easy and noted the variety of strategies they used to help them remember to take pills as prescribed on a daily basis and uphold their daily intake of pills.
Always taking the pills at the same time
Being consistent with the time to take the pills and specially taking them at the end of the day was a strategy used by the majority of the participants. This allowed them to take the pills during a quiet time of the day after finishing all daily duties. This also allowed the participants to have more privacy to take the pills without their partners being aware of it.
Maybe it was [easier] for choosing a time when I am not moving around anymore and I always took that time when watching the news on TV. I thought it was the most peaceful time for me, when I no longer move around and have to go out.
That time [at night] is quieter, and even my husband at that time he may be resting. Also because I didn't tell him anything and it is the right time for me to take while he sleeps or is watching TV, I get up and take my medication.
Using the cell phone as a reminder
Using the cell phone to set an alarm as a reminder to take the pills was another strategy used by the majority of participants. The cell phone was chosen because it was an object that they always kept handy.
I chose the alarm because I may forget to take, think that the time is right while it passed or still early. Now this alarm I put on my phone gives me the right time of taking without any failures, as soon as it rings I get up, get the pills and take them. The phone is easier because anywhere I go, I always have my phone.
Normalization of adverse events
Another strategy that improved motivation for pill taking by the majority of participants was the normalization of potential adverse events. Although most women reported having some adverse effects during the initial days of PrEP use, these effects did not discourage participants from taking the pills because they saw them as a “normal” reaction. Participants had been advised by the study nurses about potential minor discomfort and that they should allow some time for their body to get used to this new drug, while at the same time counseling them on the need to report severe effects or discomforts. This “normalization” motivated women to continue taking PrEP despite initial minor side effects.
Side effects were not negative because whatever the drug, it has its effects, hence I didn't consider it as negative, it was something that worried me but I can't say that it worried me a lot, it was not something that could made me give up the drugs.
I felt good, I liked the treatment; Only at the beginning, I felt a bit of headache, some dizziness but then it passed and I felt normal again, also it wasn't such a serious thing, it was a passing thing.
Keeping in mind that PrEP is protection
Half the participants said that being aware that PrEP increased their protection from HIV infection and that this extra protection was directly related to the correct intake of pills motivated them to take the pills. It also increased women's tolerance to the initial side effects.
What was easy for me was the time of taking them [the pills] and the fact that I put in my mind that the PrEP drugs will make me be prevented and live for a long time without getting infected with HIV. I would take them every day knowing that they are to save my life.
I felt dizziness but I understood that it was the way my body reacted to the tablets. I felt it was not bad, because soon I realized they were the side effects of the pills…because these tablets have a lot of value, the hospital staff gives us these drugs so that we are saved from the disease.
Carrying the pills
Carrying the pills with them whenever they left their homes was also noted as a facilitator for some women because they avoided missing pills due to social events.
I go to church, I do my things normally but I don't forget to take every day. When I want to leave early, I put my little bottle in my bag and go to church. When it's time to take, I take without any problems.
Forgetting a few PrEP doses
Although none of the participants reported discontinuing PrEP during study participation, four participants reported missing a few doses of PrEP. This was due to forgetting, getting sick with malaria, or being away from home and not having the pills with them.
There were two days that I forgot, but they were not consecutive days, once I forgot to take because I was at a funeral, I forgot to take them with me.
Reluctance to disclosing taking PrEP to partner
The majority of the participants chose not to disclose study participation to their partners. Participants indicated that they were afraid that their partners would not understand why they wanted to take a pill to prevent them from getting HIV. They feared that their partners might think they were taking PrEP to prevent getting HIV from other sexual partners. Also, some women were afraid that their partners might think they were hiding the fact that they were HIV positive and the pills were antiretroviral treatment. To minimize the risk of conflicts such as verbal or physical violence, often they preferred to hide the fact that they were taking PrEP.
You know how men are, they are not open with us women, when I try to talk to him, he becomes emotional from everything I talk about, and my words have no value. I even joined this study to fight for myself, because if you want to talk about prevention for both, he assaults me with words and I get shy, I end up not saying anything and I leave him like that. When it's the time to take medication, you just go to your corner and take it in secret.
I didn't tell him because my husband is annoying, I was afraid because he would think that the pills I'm taking are for treating HIV, he would think that I am HIV-positive, I saw that if I told him, he would create major problems.
However, some women reported that they had decided to inform their partners. Women explained that they preferred to be open about the motives that made them want to take PrEP, that is, to protect them from an HIV infection. After disclosing study participation, none of the participants reported a negative reaction from their partners. On the contrary, some women said that their partners were supportive and even reminded them of the importance of taking the pills every day.
Nothing negative [happened], I think everything went well. Even my husband, I had not told him anything for fear that he might forbid me to take, but as soon as he returned [home] to spend Easter, I informed him and he had no problem; on the contrary he supported me.
Independent of disclosure to their male miner partner, all but one participant reported having disclosed study participation to a family member or a friend. None of the participants reported negative reactions after this type of disclosure, and in fact some female friends and family members volunteered for participation in the study once they learned of it.
My mother is my confidant; she knows many of my secrets. I told her that we were invited to be part of a study and that there were PrEP pills to take and avoid getting HIV, and that I was taking them because I don't trust my relationship a lot.
I even mobilized the other mothers, I even found one who might come here next week to do the PrEP treatment.
Women disempowerment
A theme that emerged through all interviews and linked to the motivation for PrEP uptake and to the decision to disclose study participation was the prevailing sense of disempowerment that the women perceived within their relationships. Women described their partners as being the ones with the decision-making authority within the couple. This partially related to the fact that men provided for the family and women consequently depended financially on them. Also, as described above, women reported having fear of their partners' reaction if they did something that was socially prohibited or incorrect. They indicated that these negative reactions could be physical or verbal violence or “being sent away from home.” Therefore, for fear of the consequences this might bring on themselves and the family, women were afraid of taking the initiative to discuss sensitive topics, such as the importance of getting HIV tested, and had limited options but to accept that their partners had other sexual partners or did not want to use condoms.
I don't know the HIV status of my husband. You know how these husbands of ours are, who work in the mines in South Africa, I can't even ask anything about the test, because we argue a lot at home. I can't take the initiative to ask things like that. Only he can. To avoid noise I prefer to remain silent.
It's not me who decides, when he wants he uses a condom. I just see that he has used a condom after sex, because I can't negotiate condom use with him for fear of aggression by words. Still I am safe because I know I am protected with PrEP, even if he refuses to use condoms I trust I will not get it [HIV].
I didn't tell anyone [I was taking PrEP] because it is a new drug, I did not want to rush and tell people. And as I have not told my husband, if I told others, that information would reach my husband's ears. My husband is very annoying when you do things he does not allow…he argues with me and sometimes he beats me.
Sexual behavior—everything exactly the same as before
The majority of the participants reported no changes in sexual behavior with PrEP use, mainly since they were not using condoms before taking PrEP and they continued not using condoms while taking PrEP. Some participants also indicated that because they were afraid that their partners might find out they were taking PrEP they made an effort to do everything exactly the same as before. Similarly, they also reported not having other sexual partners prior or during PrEP use.
Nothing has changed because I did not tell him I was taking PrEP… and my husband does not even want to see a condom; he doesn't want us to use a condom.
Nothing has changed because I did not talk about this issue of taking PrEP with my husband; even if I wanted to change, he would ask the reason for this change and so I preferred to stay quiet to avoid noise and aggression by words.
Three women, however, did report changes in sexual behavior. For one participant this involved a decrease in condom use associated with less fear of being infected with HIV. For the others, even though they were not using condoms before or while taking PrEP, taking the pills made them feel less anxious during sexual intercourse.
It changed because before I forced him to use a condom, but now I say we will do it anyway without a condom, as I'm prevented.
I can say something has changed because I felt more comfortable with him, because as he is infected with HIV, I did not feel at ease and neither did he, but since I started taking (PrEP), we both feel at ease. Before, I was afraid, scared to have sex with my husband, now I am more secure.
PrEP should continue
All participants indicated that they would be willing to take PrEP again, to protect themselves from HIV infection through their partner's sexual behavior. Some participants, using the opportunity to make closing remarks, mentioned their concern about future access to PrEP, for them and also for other women in a similar situation.
I would just like to thank you for the opportunity that the Government created to give us these drugs, we were prevented for a long period, but they should continue with the medication to help others to save themselves from HIV, even for us, we would like to take again because imagine if our husbands come back [from the mines] without protection, we run the same risks as before.
Discussion
This is the first qualitative study exploring the perspectives of female sexual partners of male migrants receiving short-term oral PrEP for prevention of HIV acquisition. The major themes identified were the ease of taking daily PrEP, the challenges of revealing study participation to partner, lack of changes in sexual behavior while on PrEP, and prevailing gender dynamics and how they affect women's access to HIV prevention interventions.
Overall, this study found a high acceptability of short-term PrEP as demonstrated by participants' positive experiences with study participation. This result is consistent with results from a previous qualitative study that assessed hypothetical willingness to use short-term PrEP in the same population. 16 The study showed that female partners of migrant miners were willing to take PrEP because they perceived themselves at a high risk of HIV infection and lacking access to other feasible prevention strategies. Our study found that due to prevailing gender inequalities, including financial dependence and fear of gender-based violence, participants have limited ability to access HIV prevention methods, particularly in view of the need to negotiate regarding condom use, thus placing them at high risk for HIV infection. In these contexts, PrEP could expand women's HIV prevention options, returning decision-making power and control around this issue to the women. 18 –20
Similar to findings in other PrEP studies, 21,22 one of the main positive outcomes of study participation was the additional sense of being protected from getting HIV infection that participants felt while taking PrEP. PrEP was something that increased the individual woman's control as she could take it discretely, without knowledge of the partner, and at a convenient time. The need for additional protection from HIV derived from the perception that male partners have multiple sex partners while away working in the mines in South Africa and the extremely low rate of condom use reported among this population. Both these findings are consistent with previous studies conducted in Mozambique. 16,17
Our study found that the majority of women preferred not to disclose study participation to their partners for fear that they might not allow them to take the pills and for fear of other social harms. This is somehow contradictory with results from the previous acceptability study that assessed hypothetical acceptability of PrEP in the same population where most of the women indicated that they would feel morally obliged to discuss everything with the partner and anticipated the need to ask for permission before PrEP uptake. 16 However, although partner engagement has been found to be an important support for adherence, 22 –24 this fact might need to be counterbalanced by the potential for partners to discourage or prohibit use of preventive methods such as PrEP by women at risk for HIV. Thus, offering PrEP to at-risk women should be tailored to their needs and these women should not be required to disclose PrEP use to their partners. However, women in this study who did disclose to partners found this beneficial, and hence, for women who seek disclosure, support should be provided to ensure safe disclosure to partners. In addition, only one participant reported changes in sexual behaviors due to the use of PrEP, which is consistent with other study results. 25 However, it should be noted that our study was of short duration.
It is important to highlight as well that, for several participants, the opportunity to access HIV testing was also a positive by-product from study participation. Coverage by HIV testing in Mozambique remains low with the most recent data showing that only 61% of women and 38% of men age 15–49 have ever been tested. 6 For women who participated in our study, knowing that after being tested they could access a novel HIV prevention method might have increased motivation for test uptake. This finding suggests that PrEP availability may also contribute to increased acceptability and coverage of HIV testing for vulnerable and hard-to-reach populations. This highlights the potential of using PrEP services to increase demand for HIV testing in unreached populations at substantial HIV risk and the need for further research on how best to integrate PrEP services with health services in the country. 26
In our study, both self-reported adherence and detectable drug levels were high and participants offered some of their strategies that enabled them to accomplish this. They reported use of mobiles phone alarms and daily routines such as TV programs for maintaining the same time for taking the pills. Although side effects were experienced, these were anticipated and the women taking PrEP coped well with these, highlighting the importance of the counseling they received in terms of anticipation of certain side effects. These strategies have been reported in other implementation studies and highlight the importance of adequate counseling and support. 22,27
This study provided support for transport to PrEP services, which lessened the burden of clinic attendance. Ways to decrease cost for women in low-income settings may need to be considered.
The results of this study have to be interpreted in the light of some limitations. The study included a limited number of participants. Data on sensitive behavioral topics such as sexual behavior and adherence were collected using interviewer-administered surveys, a method acknowledged to be prone to social desirability bias. 28
In conclusion, our study found that there is high acceptance of and interest in short-term daily PrEP among female partners of migrant workers and found the opportunity to test and consider PrEP for HIV prevention empowering. It highlighted that with effective counseling, side effects can be successfully managed and women were able to develop individual strategies to support adherence and make decisions on disclosure of PrEP use. This study demonstrates the potential role of PrEP as an additional acceptable and feasible HIV prevention strategy in contexts of high HIV vulnerability and who may be unable to negotiate condom use with their partners.
Footnotes
Acknowledgments
This study was supported by the WHO through funding provided by the Bill and Melinda Gates Foundation (Grant OPP1032248). We thank all the study participants for their time and cooperation. We acknowledge the study nurses and interviewers for their work and dedication. We thank the WHO and the Provincial Health Directorate of Gaza for their continuous support during the study implementation.
Author Disclosure Statement
No competing financial interests exist.
