Resumption of Sexual Intercourse Among Postnatal Women Enrolled on Lifelong Antiretroviral Therapy in Uganda

The postnatal period is critical to the delivery of interventions aimed at improving maternal health outcomes. This study examined the timing to resumption of sexual intercourse and associated factors among postnatal women living with HIV (WLWH) in Uganda. A sample of 385 women was drawn from a larger prospective cohort study conducted between 2013 and 2015. We used survival analysis to estimate the postpartum time periods during which women had a higher risk of sexual intercourse resumption within 6 months after childbirth. Cox proportional hazards regression was used to examine associated factors with sexual intercourse resumption. The cumulative probability of sexual intercourse resumption was lowest (6.2%) in the sub-acute postpartum period (1–45 days since delivery) and highest (88.2%) in the delayed postpartum period (151–183 days since delivery). Having a live-term baby (adjusted HR 0.52, 95% CI 0.31–0.85, p = 0.01) and an advanced education (adjusted HR 0.63, 95% CI 0.40–0.98, p = 0.04) were associated with a lower risk of sexual intercourse resumption. Desire for another child (adjusted HR 1.36, 95% CI 1.08–1.73, p = 0.01), having a sexual partner (adjusted HR 5.97, 95% CI 3.10–11.47, p < 0.001) and contraceptive use (adjusted HR 2.21, 95% CI 1.65–2.95, p < 0.001) were associated with a greater risk of sexual intercourse resumption. However, only 1 in 4 women who resumed sexual intercourse by the 90th day after childbirth, reported currently using contraception. HIV programs should focus on supporting postnatal women to align the timing of sexual intercourse resumption with their return to contraceptive use. Interventions aimed at improving contraceptive uptake among postnatal WLWH should target the delayed postpartum period.


Introduction
Pregnancy and childbirth-related complications are among the leading causes of maternal deaths in developing countries especially among women living with HIV [1]. In general, the process of pregnancy and childbirth is known to change women's physical and mental condition as well as their health-related quality of life [2][3][4][5]. Some of the factors found to affect the quality of life of postpartum women include depression, lactation problems, urinary complications and difficulties engaging in sexual intercourse after childbirth [6]. Although several studies in the past explored issues around sexuality during the postnatal period, the majority focused on women in the general population as opposed to those living with HIV [7][8][9][10]. Women living with HIV (WLWH) require special attention as they experience unique challenges with their health-related quality of life which are exacerbated by a compromised immunity [11,12].
Since the wake of the HIV pandemic in the early 1980s, several countries around the globe have made tremendous progress in the fight against HIV by integrating various interventions, including Prevention of Mother-To-Child Transmission (PMTCT) services for mothers and their infants [13]. In addition, guidelines for HIV prevention and treatment have been adopted by many countries based upon World Health Organization (WHO) guidelines on family planning use for national health systems [14]. These national guidelines put emphasis on dual contraception; which involves the use of both a hormonal method (oral contraceptives, long-acting reversible contraceptives, etc.) and a barrier method (condoms) as a component of the postnatal care (PNC) package. However, the guidelines are not accompanied with an appropriate message for WLWH to ensure that their timing of sexual intercourse resumption after childbirth coincides with the time to return of contraceptive use. As a result, we have postnatal women who resume sexual intercourse before they return to contraceptive use [15]. Whereas WHO recommends contact with the healthcare system during the postnatal period [16], findings from a systematic review involving 37 studies in rural Africa, showed that women preferred traditional postnatal services (involving traditional rituals and customs) over health facility-based postnatal care [17]. In most parts of rural Africa, majority of women believe in the traditional practices of postnatal care within their communities including initiation of sexual intercourse within 2-4 weeks after childbirth [18][19][20]. Others fear that their sexual partners would find sex elsewhere if they delayed resumption of sexual relations for too long [21].
Uganda is one of the countries in sub-Saharan Africa that tremendously contained the HIV pandemic in the early 1990s using messaging strategies such as the Abstain, no-sex Before marriage, use Condoms (ABC) strategy that brought down the HIV prevalence among adults aged 15-49 from a national average of 18.5% in 1992 to 6.3% in 2017 [13]. With the rollout of PMTCT and infant services, Uganda is increasingly registering success as WLWH continue to give birth to babies who are free of HIV [22,23]. The country has also registered high pregnancy intentions among postnatal WLWH [24,25]. In 2019, the World Bank put Uganda among the top 10 countries with the highest total fertility rate at 4.8 births per woman [26].
Although efforts to improve contraceptive uptake among women of child-bearing age have been stepped up, research in Uganda shows a delayed return to contraceptive use among postnatal women which does not coincide with their timing of sexual intercourse resumption following childbirth. A recent study in Uganda found a median time to contraceptive use following childbirth of 19 months [27]. This timing does not coincide with the 6 weeks to 6 months period within which the majority of postnatal women are likely to resume sexual intercourse [7,28]. Early resumption of sexual intercourse (before the end of the first six weeks of the postpartum period) is not generally recommended because of the increased risk of acquiring sexually transmitted infections due to vaginal lesions and complications following the delivery process [29,30]. Some of the factors found to be significantly associated with resumption of sexual intercourse before 6 weeks after childbirth include (1) socio-demographic factors such as younger age, lower education, occupation, urban resident, household income and family planning use; (2) physiological factors such as parity of one, vaginal delivery, no postpartum complications and; (3) socio-cultural factors such as husbands' demands, desire for another child, giving birth to a male child and fear of extra marital affairs due to prolonged postpartum abstinence [7,8,31,32]. Prior literature showed that women lack adequate health education and counselling (which should be provided during antenatal and postnatal care) on aligning the timing of sexual intercourse resumption after childbirth with their return to contraceptive use [33][34][35][36].
The Ugandan Ministry of Health (MoH) recommends at least six weeks of postpartum abstinence [33]. However, the extent to which postnatal WLWH adhere to the MoH guidelines for resumption of sexual intercourse remains low. Prior studies conducted in the Ugandan setting were not capable of estimating the time to resumption of sexual intercourse after delivery because of limitations with the study design [7]. This study used a prospective cohort design to estimate the postpartum time periods during which women had a higher risk of sexual intercourse resumption within 6 months after childbirth. The study also established average time to sexual intercourse resumption and associated factors among postnatal WLWH.

Study Sites
The study was conducted at three health facilities (Masaka Regional Referral Hospital, Mityana Hospital and Luwero Hospital) located respectively in Masaka, Mityana, and Luwero districts of Central Uganda. These facilities were among the first to provide lifelong ART in October 2012 shortly after MoH rolled out the national guidelines for implementation of lifelong ART for PMTCT in Uganda [37,38].

Study Design
The study used data from a larger prospective cohort study where women on lifelong ART were enrolled during pregnancy and followed up to 18 months between 2013 and 2015. Detailed information on the parent cohort study has been previously published [39][40][41][42].

Sample Size
This sub-study enrolled a sample of 385 postnatal women from the larger parent study and followed them up to 6 months to estimate the postpartum time periods during which women had a higher risk of sexual intercourse resumption after childbirth.

Inclusion Criteria
This study included 385 women who had completed at least one postnatal care (PNC) interview and had complete data on pregnancy outcomes for the first 90 days (3 months) after childbirth. A cut-off of 90 days (3 months) was used to cover the window period within which majority completed their 1st PNC interview so as to include as many women in the analysis as possible. This window period was given because of the difficulties associated with potential loss-to-follow up after childbirth in this study setting. Women who had no data on the outcome of interest (time to resumption of sexual intercourse) by the end of the study period were considered to be censored.

Sampling Procedure
On each clinic day, the attending nurses referred all WLWH to the study interviewer available on-site for eligibility screening and subsequent enrolment into the study [39,42]. Enrolment into the study was done consecutively until the required sample size was obtained.

Data Collection Methods
Written informed consent was obtained from all eligible study participants who accepted to participate. A structured questionnaire with pre-coded responses was administered by a trained and experienced study interviewer who was stationed at the facility for the duration of the study period. During the 6-month follow-up period, face-to-face interviews were conducted at different time intervals defined as number of days since delivery: 1-45, 46-90, 91-120, 121-150 and 151-183. These time intervals were selected based on the three phases of the postpartum period, which can be distinct but also continuous namely: the initial or acute phase which involves the first 6-12 h after childbirth; sub-acute postpartum period which lasts 2-6 weeks, and the delayed postpartum period, which can last up to 6 months.
For ethical reasons, interviews could not be conducted during the initial or acute phase (6-12 h after childbirth). We selected the time interval of 1-45 days since delivery, to represent the sub-acute postpartum period within which sexual intercourse resumption is not recommended based on current Ugandan MoH guidelines. The time interval of 46-90 days since delivery represents the delayed postpartum period up to 6 months which is a time of gradual restoration of muscle tone and connective tissue to the pre-pregnant state. All follow-up interviews were, as much as possible, tied to the schedule of postnatal clinic visits for the women and their infants. The data collection tool used was a structured questionnaire which was translated into Luganda, the commonly spoken native language in the study area.

Study Measures
At the initial visit, data were collected on women's sociodemographic characteristics included: age, marital status, education level, religion and primary occupation. At subsequent visits, women were asked about the outcome of their latest pregnancy, HIV positive status disclosure to at least someone, currently having a sexual partner, partner HIV testing (for those who reported having sexual partners) and current contraceptive use which we defined as condom use combined with or without other contraceptive methods. To capture data on current contraceptive use we asked; are you or your spouse currently using any family planning method? Those who said, 'yes' to this question were additionally asked to select one or more options from a pre-coded list of contraceptive methods. We also asked about women's desire for another child and resumption of sexual intercourse after childbirth. The primary outcome variable was the 'time to resumption of sexual intercourse after childbirth'. To obtain data on this variable, women were asked to self-report how soon they resumed sexual intercourse after delivery: 'Since you delivered your child, have you resumed sexual intercourse with your partner?' Those who said, 'yes' to this question, were asked: how soon after delivery did you and your sexual partner resume sexual intercourse? Women chose from 3 options: (1) within 6 weeks; (2) after 6 weeks; (3) I don't remember. Those who chose the third option were assumed to have resumed sexual intercourse within 6 weeks and were likely not to have attended their 6-week postpartum clinic visit based upon findings from prior studies.
For instance, a cohort study involving women who had not attended the 6-week postpartum clinic visit showed that reasons for non-attendance included: having a normal vaginal delivery, no postpartum complications and a feeling of general well-being [31]. The same factors were found to be significantly associated with resumption of sexual intercourse before the end of the first 6 weeks postpartum [9,32,43].

Study Variables by Specific Objective
This study used three interviewer-administered questionnaires: (1) the baseline questionnaire administered at the time of study enrolment; (2) the PNC-1st interview questionnaire administered during the first postnatal visit following childbirth and; (3) the PNC-subsequent questionnaire administered at all subsequent postnatal interviews ( Table 1). The PNC-subsequent questionnaire did not include some questions from the PNC-1st postnatal interview (e.g. questions on pregnancy outcome) as they did not need to be repeated.

Data Management
At the end of each day's work, all completed questionnaires were reviewed and checked for completeness under the supervision of the study coordinator. Each questionnaire was independently entered twice by two data entrants who conducted all the data capture into the computer using CSPro version 5. The data manager compared the two data entries to identify and edit any inconsistencies.

Data Analysis
Analysis for this study included 732 repeated observations contributed by the 385 women for whom data were collected on pregnancy outcomes for the first 90 days (3 months) after childbirth. We used descriptive statistics, survival analysis and Cox proportional regression models to analyse the data. Descriptive analyses were conducted to describe women's characteristics using frequencies and proportions, means, and standard deviation. Survival analysis was used because of the nature of our primary outcome variable, 'time to resumption of sexual intercourse within 6 months after childbirth', which is a time variable. The probability of sexual intercourse resumption was assessed by fixed covariates such as age, marital status, education at enrolment and by time-varying covariates such as HIV partner testing and disclosure of HIV positive status.
Due to the discrete nature of the timing of follow-up, data from visits were ascribed to the time of follow-up from date of delivery to self-report of first sexual intercourse. For the continuous predictors, we used a univariate Cox proportional model. We also used a life-table approach to obtain hazards of sexual intercourse resumption by categories of time from delivery to resumption of sexual intercourse. In order to determine independent factors associated with time-to-sexual intercourse resumption, we conducted semi-parametric Cox proportional hazards regression analyses. We obtained adjusted hazard ratios (HR) as a measure of association with corresponding 95% confidence intervals (CI) at 5% level of statistical significance. All data analyses were performed   Table 2).

Participant Characteristics at the First Postnatal Visit (90 Days Since Delivery)
Of all women (N = 385), 87% (n = 335) reported having a sexual partner. Of those who had sexual partners, 46.8% (n = 180) did not know if their partner ever tested for HIV and 53.5% (n = 83) of those whose partners ever tested for HIV, reported a positive partner HIV status. By the 90th day (3 months) since delivery, 84.4% (n = 325) had disclosed their HIV positive status to at least one person (Table 3). Of all women (N = 385), 46.2% (n = 178) reported wanting more children, and 90.1% (n = 347) wanted to delay having children for a period of two years. By the 90th day (3 months) since delivery, 26% (n = 100) had resumed sexual intercourse and 6.5% (n = 25) of those who resumed, reported currently using contraception (Table 3). Of the 100 women, who had resumed sexual intercourse by the 90th day since delivery, 77% (n = 77) reported resuming sexual intercourse after 6 weeks following childbirth (Table 3).

Cumulative Probability of Sexual Intercourse Resumption Within 6 Months After Childbirth Among Women Enrolled on Lifelong ART in Uganda
The study enrolled 385 women who were followed up for 6 months to estimate the postpartum time-periods in which women had a higher risk of sexual intercourse resumption after childbirth. During the initial interval period (1-45 days since delivery), out of the 385 women enrolled, 24 reported resuming sexual intercourse during that interval period and 16 were lost-to-follow up, leaving 345 women in active follow-up. By the second visit (46-90 days since delivery), out of 345 women, 77 had the outcome of interest (i.e. resumed sexual intercourse) and 46 were lost-to-follow up during that interval period, leaving 222 women in active follow-up ( Table 4). The cumulative probability of sexual intercourse resumption was lowest (6.2%) in the sub-acute postpartum period (1-45 days since delivery) and highest (88.2%) in the delayed postpartum period (151-183 days since delivery) ( Table 4).

Adjusted Analysis of Factors Associated with Time to Sexual Intercourse Resumption Within 6 Months After Childbirth Among Women Enrolled on Lifelong ART in Uganda
This study found five independent factors which were significantly associated with the risk of sexual intercourse resumption within 6 months after childbirth. These were: (1) pregnancy outcome (having a live-term baby), (2) education level (advanced secondary/university), (3) currently having a sexual partner, (4) desire for another child and (5) current contraceptive use. Women who reported having a live-term baby had a 48% lower risk of resuming sexual intercourse within 6 months after childbirth compared to those who had a premature, still birth or miscarriage (adjusted HR 0.52, 95% CI 0.31-0.85, p = 0.01). Similarly; women who had completed advanced secondary/university education had a 37% lower risk of resuming sexual intercourse within 6 months after childbirth compared to those who had completed under 7 years of school (adjusted HR 0.63, 95% CI 0.40-0.98, p = 0.04) ( Table 6). Women who reported currently having a sexual partner were almost 6 times more likely to resume sexual intercourse within 6 months after childbirth compared to those who did not have sexual partners (adjusted HR 5.97, 95% CI 3.10-11.47, p < 0.001). Women who reported wanting another child had a 36% higher risk of resuming sexual intercourse within 6 months after childbirth compared to those who did not want another child (adjusted HR 1.36, 95% CI 1.08-1.73, p = 0.01). Women who reported currently using contraception (condoms/ other modern family planning methods) were 2.21 times more likely to resume sexual intercourse within 6 months after childbirth compared to those who reported not currently using contraception (adjusted HR 2.21, 95% CI 1.65-2.95, p < 0.001) ( Table 6).

Discussion
This study used a prospective cohort design to estimate the risk of sexual intercourse resumption and associated factors among postnatal WLWH in Uganda. The cumulative probability of sexual intercourse resumption was lowest (26.2%) in the sub-acute postpartum period and highest (88.2%) in the delayed postpartum period. Of the 100 women who reported resuming sexual intercourse by the 90th day since delivery, majority (77%) resumed after 6 weeks following childbirth. This is good news for HIV programs in Uganda as it aligns well with the MoH recommendation of 6 weeks of postpartum abstinence for all women irrespective of HIV status. Similar findings in Nigeria and Australia showed a gradual increase in the risk of post-delivery sexual intercourse resumption of up to 94% by the 6th month [8,10]. The low resumption of sexual intercourse in the sub-acute postpartum phase may be explained by the fact this phase is a critical period of physical and emotional restoration for the mother while the delayed postpartum phase is a period when the health-related quality of life should have normally improved for most women [5]. This study found that having a live-term baby was associated with a lower risk of sexual intercourse resumption. Prior studies elsewhere found similar results. A study that explored women's postpartum sexual experiences in the United States found a lower risk of sexual intercourse resumption when a mother had a live-term baby [44]. Another study that examined the prevalence of women's postpartum health problems cited exhaustion, backache and lack of sleep due to the baby crying [45]. Such issues could potentially shift the attention of the mother away from her sexual partner, as more time is spent caring for the baby as opposed to attending to the sexual needs of her partner. This argument was further supported by a study that examined postpartum sexuality experiences among black African couples, which found a reduced frequency of sexual intercourse in 75% of the couples [46]. Having a live-term baby will potentially reduce the risk of early sexual intercourse resumption in the postpartum period as more time is spent with the baby. Findings from this study also showed that higher education was associated with a lower risk of sexual intercourse resumption. Similar results were found in Nigeria where women with a higher education had a longer median time to end of postpartum abstinence [8]. Education improves women's autonomy in health decision-making for fertility control, including access to family planning services [47][48][49]. Therefore, advancing women's education is one way to reduce the risk of early sexual intercourse resumption after childbirth.
Findings from this study further showed that women's desire for another child, having a sexual partner and contraceptive use, increased the risk of sexual intercourse resumption. Prior literature showed high fertility desires and pregnancy intentions among WLWH in Uganda [24]. Studies in Nigeria, Cameroon and Ethiopia also found that contraceptive use, women's desire for another child coupled with pressure from the husband to initiate sexual intercourse significantly increased the risk of sexual intercourse resumption [8,9,32,50]. Much as having a sexual partner and desiring another child increased the risk of sexual intercourse resumption, an early and timely return to contraceptive use in the postpartum period would help minimize the risk of multiple pregnancies and associated adverse outcomes for mothers and their infants.
By the 90th day (3 months) after childbirth, 26.2% of women in our study had resumed sexual intercourse but only 6.5% of those who resumed, reported currently using contraception. In other words, only 1 in 4 women who resumed sexual intercourse by the 90th day after childbirth, reported currently using contraception. This finding points to a gap that needs to be addressed by HIV programs. Literature shows that women with short inter-pregnancy intervals of 5 months or less have higher risk for maternal death, third trimester bleeding, premature rupture of membranes and anaemia compared to women with inter-pregnancy intervals of 18 to 23 months [51]. This finding explains the 2-year child-spacing period recommended by WHO [14]. HIV programs should therefore focus on supporting postnatal women to align the timing of sexual intercourse resumption with their return to contraceptive use. One way to achieve this, is by integrating HIV services with postpartum family planning services. This strategy was found to reduce the incidence of unwanted pregnancies among postnatal WLWH [52]. In addition, health providers need to provide health education and counselling on contraception and resumption of sexual intercourse after childbirth during antenatal and postnatal care. Women who receive postpartum family planning counselling during antenatal and postnatal care were found to more likely to use contraception than those who do not receive any counselling [36]. Another strategy is by increasing male involvement in maternal health care services. Male involvement in maternal health services was found to be a significant predictor of postpartum family planning utilization, as it enhances joint healthcare decisionmaking between the woman and her partner [53]. As such, the woman and her partner can make a joint decision on uptake of family planning services and timing for resumption of sexual intercourse after childbirth. Strengthening efforts in postpartum family planning will help accelerate the achievement of the 3 rd Sustainable Development Goal (SDG) of ensuring good health and well-being for all by 2030.

Study Limitations
This study did not collect data on 'mode of delivery' despite extensive published literature on the relationship between duration of postpartum abstinence and timing of sexual intercourse resumption [7,10]. However, some published studies showed that mode of delivery did not reach statistical significance in the association with time to sexual intercourse resumption [44,50,[54][55][56]. Additional evidence from a systematic review showed inconsistencies in reported associations between mode of delivery and sexual intercourse resumption [57]. This implies that not having data on 'mode of delivery' would not have changed the direction of our study findings. This study did not allow for comparison of factors between WLWH and those not living with HIV since initial enrolment of participants in the parent cohort study was restricted to WLWH. Without this comparison, it may be difficult to contextualize the results as being significant to WLWH.

Conclusion
The majority of postnatal WLWH resumed sexual intercourse after six weeks post-delivery which aligns well with the Ugandan MoH 6-week recommendation on postpartum abstinence for all women irrespective of HIV status. The cumulative probability of sexual intercourse resumption was highest in the delayed postpartum period. However, only 1 in 4 women who resumed sexual intercourse by the 90th day after childbirth, reported currently using contraception. Resumption of sexual intercourse, if not matched with a timely return to contraceptive use, may result into multiple pregnancies and adverse maternal health outcomes for WLWH exacerbated by a compromised immunity. Interventions aimed at improving postpartum contraceptive uptake among WLWH should target the delayed postpartum period.
Author Contributions All authors supervised data collection including recruitment and follow up of study participants. RN conceptualized the research question and wrote the first draft of the paper. FM led the analysis and interpretation of data. AM and EB revised the draft manuscript to strengthen its intellectual content. RKW conceived and led the design of the larger study protocol, reviewed and revised the paper for substantial intellectual content. SK contributed to revising the manuscript and helped to strengthen the global health component of the manuscript. JA and JM provided technical oversight and supervision of study implementation activities on behalf of the Ugandan Ministry of Health. All authors reviewed and approved the final version of the manuscript.
Funding This study was funded by Global Fund through the Ugandan Ministry of Health under Grant Number: UGD-708-G07-H. The content is solely the responsibility of the authors and does not necessarily represent the official views of Global Fund.

Data Availability
The datasets analyzed for this study are available from the corresponding author if requested.

Conflict of interest
The authors have no competing interests to declare.
Ethical Approval Ethical approval was obtained from Makerere University School of Public Health Higher Degrees Research and Ethics Committee (Protocol number 064) and the Uganda National Council for Science and Technology (Registration number SS3153).

Informed Consent
Potentially eligible study participants were read an informed consent form and asked if they were willing to participate in the study. Consenting participants signed two copies of a written informed consent form and retained a copy for their future reference.