Introduction
The issue of integration of HIV and reproductive health services has come to the forefront of policy discussions in recent years, particularly in Africa [1–5] . In Mwanza (northern Tanzania), women of reproductive age have high HIV prevalence (7% [6] ) and high unmet need for contraception (25% [7] ), so integrating family planning and HIV services would comprehensively address their sexual and reproductive health needs. Antenatal clinics (ANCs) are well attended in Tanzania (97% of women visit at least once during pregnancy [7] ), and therefore provide an opportunity to reach a large proportion of sexually active women of reproductive age, making them an obvious choice for delivery of integrated services.
With the advent of preventing mother-to-child transmission (PMTCT) treatment, the rationale for offering HIV testing in ANCs became even stronger, and Tanzania introduced an opt-out system whereby clinics with appropriate facilities offer HIV tests to all pregnant women on their first antenatal visit. The rationale for additionally integrating family planning into ANC services is strong, as HIV-positive and HIV-negative women may have different family planning needs [8] , which should be addressed during family planning counselling. Moreover, as pregnant women will naturally be thinking about family building, ANC services provide a timely opportunity for family planning counselling. For HIV-positive women, family planning information can help prevent future unwanted pregnancies and thereby reduce the number of HIV-infected babies born [9–11] . Although family planning is offered in other settings in Tanzania, many women do not use family planning services despite wanting to delay births, making ANCs a valuable opportunity to reach them with family planning information.
WHO issued a Call to Action recommending integration of family planning into antenatal PMTCT services [12] , which has yet to be implemented in many African countries [4] . Tanzanian guidelines for PMTCT counsellors suggest mentioning family planning only postpartum for HIV-positive women, and not at all for HIV-negative women [13] . Counsellors in Mwanza reported focusing on condoms during PMTCT counselling and referring women to a special clinic if they desired more information on family planning (personal communication).
Initiatives to integrate family planning into ANC services in Tanzania are at an early stage, so more evidence is required on the needs of pregnant women to develop appropriate integrated services. If family planning services are to be offered as a part of PMTCT counselling, the reproductive history and intentions of HIV-positive and HIV-negative pregnant women should be investigated and their specific needs identified.
This study reports findings from a survey of 5284 ANC attendees conducted in 15 clinics in Mwanza City and Magu district in northern Tanzania in 2007–2008. Reproductive and contraceptive history and intentions of HIV-positive and HIV-negative pregnant women are examined and recommendations drawn for the integration of family planning counselling into ANC services.
Methods
This ANC survey was the fourth of a series of HIV surveillance rounds in ANCs in Mwanza City and Magu District, conducted by the Tanzanian National Institute for Medical Research (NIMR) in collaboration with the London School of Hygiene and Tropical Medicine (LSHTM). All survey rounds collected information on HIV and sexual behaviour, but this round was the first to collect detailed information on family planning and reproductive behaviour. Findings from previous rounds are reported elsewhere [14] .
Between December 2007 and May 2008, all ANCs in the catchment area that offered HIV testing and counselling were surveyed. Nurses and counsellors in the clinics were trained to administer structured questionnaires to ANC clients before their HIV test. Questions covered socio-demographic background, sexual behaviour, reproductive history and intentions and contraceptive history and intentions. All pregnant women attending the clinics during the survey were invited to participate only once. An informed consent sheet was read to each participant; the interviewer recorded the woman's consent or refusal to participate and signed next to it.
On completion of the questionnaire, women were offered HIV testing and counselling and syphilis testing, and results were fed back the same day following standard national ANC protocols. If a participant consented to the researchers knowing the HIV result, a dried blood spot (DBS) was made using residual blood from the syphilis test. DBSs were subsequently collected from the clinics and analysed at the NIMR Laboratory, where HIV results were determined from two ELISA tests (Enzygnost; Dade Behring, Frankfurt, Germany and Uniform 2; Organon, Boxtel, The Netherlands).
Each participant was identified by an individual study number, which linked the questionnaire to the DBS HIV test, and no participant names were used. Data were double entered using Census and Survey Processing System (CSPro; U.S. Census Bureau, Wisconsin, USA), cleaned in Access (Microsoft Office Access Program; Microsoft, Denver, Colorado, USA) and exported to STATA version 10.1 (College Station, Texas, USA) for analysis.
The unmet need for family planning before pregnancy was calculated as the proportion of women who reported not wanting a child at the time of becoming pregnant but who were not using contraception at that time. Those who wanted a child later were classified as having an unmet need for spacing births, whereas those who did not want a child at all had an unmet need for limiting births. Women who were using contraception at the time of becoming pregnant and did not want a child then were classified as experiencing method failure. Future need for family planning was calculated as the sum of the proportion who did not want another child and the proportion who wanted to wait over 2 years until their next birth. As the mean length of postpartum amenorrhea in Tanzania is 12.7 months [7] , almost all women would experience the return of menses by 24 months, so that any woman expressing a desire to wait 2 years or more before the next child would have a need for family planning. In fact, 21% of women in our sample got pregnant within 15 months of their last birth, meaning that the 2-year cut-off point is likely to provide a lower end estimate of need for family planning after birth.
Results were adjusted for clustering at the clinic level. As all women attending the clinics in the survey period were interviewed, the number of participants in each clinic was proportional to its size, so the sample was self-weighting. Comparisons between means were made using the t -test adjusting for clinic effects. Direct age standardization was used, with the age distribution of all women as a standard. Comparisons between proportions were made using the Wald statistic (based on the F -test with adjusted degrees of freedom for several proportions and on the t -distribution for two proportions). Multivariate linear regression and logistic regression models were used to adjust for confounding. All statistical tests are reported at the 95% significance level.
Ethical approval for the study was obtained from the Tanzanian Medical Research Coordinating Committee and from the LSHTM Ethics Committee.
Results
Socio-demographic profile
Questionnaire response rates were high (99.6%). The mean age of women was 25 years, and the mean parity was 1.9. Residential distribution was 52% urban, 33% remote rural and 15% classified as rural roadside dwellers (living less than 1 km from the main road). Ninety percent of women were married, with 80% in their first marriage, and 8% were never married. The majority (77%) reported completing primary education, but only 7% had completed secondary and 11% had no formal education. Around 26.2% of women had ever used family planning.
Of the 5284 women interviewed, 5133 women (97.1%) were having an HIV test that day. HIV results were subsequently determined for 5121 women. HIV prevalence was 8.9% overall. HIV-positive women were on an average older than HIV-negative women by 1.7 years (Table 1 ) and more likely to be remarried (15.5 versus 9.9%). HIV-positive and HIV-negative participants did not differ in patterns of residence or educational attainment.
Table 1: Socio-demographic characteristics, reproductive history and intentions by HIV status.
Reproductive history and intentions by HIV status
Reproductive history differed by HIV status in several respects (Table 1 ). After age standardization, mean parity (calculated as number of live births) was 0.3 births lower in HIV-positive than HIV-negative women. After adjusting for age and parity, the proportion of children ever born who were still alive was significantly lower for HIV-positive women than HIV-negative women (88.9 versus 92.6%, P = 0.006), and the previous birth interval in HIV-positive women was 10.2 months longer than in HIV-negative women (P < 0.001). This association was not confounded by family planning use since last birth.
For reproductive intentions, significantly fewer HIV-positive women than HIV-negative women wanted another child after their current pregnancy (57.3 versus 66.1%); the difference remained significant after adjusting for age and parity (P = 0.007). For women who wanted another child, the mean ideal birth interval was 42.8 months and did not differ by HIV status.
In multivariate logistic regression analyses of reproductive correlates of HIV infection (Table 2 ), the odds of the last born child having died were significantly higher for HIV-positive than HIV-negative women [odds ratio (OR) 1.63, 95% confidence interval (CI) 1.12–2.35] after adjusting for age, parity, residence and education. Significantly more HIV-positive women had ever used family planning (35.5%) than HIV-negative women (25.3%) after adjusting for socio-demographic variables and time sexually active. The odds of having used family planning since the last birth were 1.87 times higher in HIV-positive than in HIV-negative women, after adjusting for all other factors including survival of the last child. Although overall only 0.5% of women did not intend to breastfeed, the adjusted odds of not wanting to breastfeed were 9.56 times higher in HIV-positive than in HIV-negative women (95% CI 3.86–23.66).
Table 2: Reproductive and sexual behaviour correlates of HIV infection.
HIV-positive women were twice as likely as HIV-negative women to want to use a condom if their partner had sex with another woman (OR 0.43, 95% CI 0.19–0.95). The odds of not wanting to disclose their upcoming HIV test result to their partner were 2.35 times higher for HIV-positive women, after controlling for other factors including marital status.
Unmet need for family planning
Prior to this pregnancy, 28% of women reported an unmet need for family planning: 20.5% for spacing and 7.5% for limiting births (Table 1 ). No significant differences by HIV status were detected at the 95% level. A higher proportion of HIV-positive than HIV-negative women reported wanting their child immediately as opposed to later (P = 0.037), but the difference became nonsignificant after adjusting for age and parity. Unmet need (for spacing and limiting) shows a steady increase with age (Fig. 1 ) and is nonsignificantly lower in HIV-positive than in HIV-negative women at all ages apart from the oldest age group.
Fig. 1: Percentage of women with an unmet need for family planning before pregnancy and future need for family planning by age and HIV status. FP, family planning; HIV+, HIV positive; HIV−, HIV negative.
Future need for family planning was extremely high in our ANC population, with 83.8% of women reporting they wanted to wait over 2 years until the next birth. Future need for family planning was not significantly different between HIV-positive and HIV-negative women but increased with age in both groups (Fig. 1 ). Ninety-five percent of women with previous unmet need had future need for family planning. Future need in these women may be more likely to go unmet than in women with no past unmet need. Therefore, the unmet need estimates in Fig. 1 (lower curves) also represent a rough estimate of future unmet need out of total future need for family planning (upper curves).
Family planning ever use of antenatal clinic clients
Having identified past use of family planning as a strong correlate of HIV infection, we examined the methods used. Overall, hormonal methods were more popular than barrier methods. Female condoms, foam, jelly, withdrawal, abstinence and ‘other/traditional methods’ had each been used by less than 1% of past family planning users. The most popular method was injectable contraception, used by 70.9% of HIV-negative and 75.9% of HIV-positive past family planning users, followed by the pill used by 40.2 and 37.3%, respectively. Past condom use was 3.3% in HIV-negative and 2.5% in HIV-positive women. Differences in method distribution between HIV-positive and HIV-negative past users of family planning were nonsignificant, although given higher rates of past use in HIV-positive women, ever use of pills and injectables among all women was significantly higher in HIV positive than in HIV negative (Fig. 2 ).
Fig. 2: Percentage of ever use of the six most popular family planning methods by the total antenatal clinic population. HIV+, HIV positive; HIV−, HIV negative; IUD, intrauterine contraceptive device.
Figure 2 shows the six most popular family planning methods in terms of past use and intention to use. Intention to use did not significantly differ by HIV status (77.5% of HIV negative versus 80.5% of HIV positive, P = 0.165). Intention to use each method was higher than past use, but method distribution was similar, with injectables being the most popular method followed by pills. Intention to use condoms (4.6% of HIV-negative women and 3.7% of HIV-positive women) was low compared with the injectable or pill.
To describe past family planning use by socio-demographic background (Table 3 ), we grouped methods into hormonal (pill, injectable and implant) and barrier (male and female condoms, foam and jelly). Overall family planning use increased with age, particularly between those less than 20 and those 20–24 years of age in whom the odds of having ever used family planning increased 2.75 times after controlling for marital status, parity and residence. Ever use of hormonal methods displayed a similar pattern. Odds of having ever used barrier methods showed a less significant increase with age (possibly due to smaller sample size). No significant age trend was apparent in past condom use.
Table 3: Predictors of family planning ever use by method type.
The odds of family planning ever use were lower in roadside and rural areas compared with urban areas (OR 0.47 and 0.37, respectively) but were not significantly different between roadside and rural areas. Ever use of hormonal methods displayed the same pattern, but ever use of barrier methods did not differ by area of residence.
A strong association between parity and ever use of family planning was evident even after controlling for other factors, with odds of family planning ever use in women of parity 1 being 11 times higher than for women of parity 0. Odds did not differ significantly between women of parity 1 and above, pointing to the first birth as the main trigger for family planning use. The same pattern was apparent for ever use of hormonal method, but there was no apparent trend for ever use of barrier methods. After adjusting for parity, there was no association between marital status and past family planning use, regardless of method type.
HIV infection remained strongly associated with past family planning use after controlling for all other factors, with HIV-positive women displaying 1.28 times higher odds of past use than HIV-negative women (Table 3 ). Odds of past use of hormonal method remained significantly higher in HIV-positive compared with HIV-negative attendees (OR 1.32, 95% CI 1.10–1.57), but ever use of barrier methods showed no association with HIV infection (OR 1.08, 95% CI 0.34–3.45).
Discussion
The higher proportion of remarried HIV-positive women compared with HIV-negative women comes as no surprise, given that marital instability is a risk factor for HIV. The lower parity observed in HIV-positive participants supports previous findings of lower fertility in HIV-infected women [15–18] due to biological effects of infection, such as lower fecundity and higher rates of foetal loss [15,16,19,20] , and behavioral factors, such as higher prevalence of widowhood and reduced sexual activity, in symptomatic HIV-positive women [20,21] . Biological explanations find some support in the longer birth intervals displayed by our HIV-positive sample. Higher family planning use in HIV-positive women may also contribute to lower fertility, although past family planning use was also associated with older age and higher parity.
The lower fertility of HIV-positive women has certain implications for family planning service provision to HIV-positive pregnant women, especially those starting an antiretroviral therapy [22] . If HIV-positive women who had low fecundity in the past want more children, they may opt not to use family planning postpartum to increase their chances of conception. Higher mortality of children of HIV-positive mothers may lead HIV-positive women to want to ‘replace’ children who have died to achieve a culturally acceptable family size. Although some women may prefer to delay or stop childbearing if they know they are HIV positive, as reported in other studies [23–25] , family planning counselling should devote particular attention to those women who desire another child to ensure they are aware of the risks of MTCT and are offered the possibility of spacing their births to reduce the risks of adverse pregnancy outcomes.
The death of a baby can also lead to shorter birth intervals through biological mechanisms, as the mother stops breastfeeding and resumes menstruation sooner. HIV-positive women are likely to be in this situation more often than HIV-negative women. Moreover, some HIV-positive women will not breastfeed at all. Family planning counselling for HIV-positive women should highlight the increased risk of pregnancy in the absence of breastfeeding, even in the first few months postpartum, and recommend the use of family planning if the client does not want a child in the next 2 years (which was the case for 87% of HIV-positive women in our sample).
The reluctance of many HIV-positive women to disclose their status to their partner suggests that some women know or suspect they are HIV positive and fear their partner's reaction. This has obvious implications not only for HIV prevention but also for family planning counselling. Having a child is a heavy commitment, and it is important that partners are aware of women's HIV status before deciding to have another child. Family planning counselling should highlight the importance of partner disclosure for future pregnancy decisions and choice of appropriate family planning methods (particularly as condom use is likely to be controlled by the partner). Couple counselling after status disclosure would also provide an opportunity for more nuanced advice on family planning, according to whether the couple is seroconcordant or discordant and for promotion of the more popular hormonal methods if appropriate.
The distribution of family planning methods can inform the design of family planning counselling guidelines for ANCs. The popularity of the injectable and the pill testify to women's need for a method that is discreet and simple to use. Injectables, in particular, give women the opportunity to use contraception without telling their partner, a valued advantage in a society in which men want more children than women [7] . Family planning counselling should evaluate each woman's medical and social circumstances in order to offer methods adapted to the woman's needs. This will help reduce the family planning discontinuation rate that is currently 38% within the first year in Tanzania [7] . There is an urgent need to address the widespread reluctance to use condoms. Ours is not the first study to point out disappointingly low rates of condom use among childbearing women in high HIV prevalence settings [26] . However, family planning counselling in ANCs can work towards increasing their acceptability by challenging their widespread association with infidelity in this population (internal document from Tazama Project, NIMR) and encouraging women to start to see them as a means of preventing pregnancy, while continuing to emphasize their use in sexually transmitted infections (STIs) and HIV prevention. Although use of condoms for dual protection has not been highly successful in the past when most of the STIs that posed a danger were curable, in the era of HIV, attitudes to dual protection may change, and ANC/Voluntary Counselling and Testing for HIV (VCT) settings are an opportunity to discuss these evolving circumstances.
The fact that 77% of women want to use family planning testifies to its relative acceptability in this population, although the possibility of courtesy bias from respondents cannot be ruled out. The large gap between intention to use and past use suggests that the willingness to use family planning may not always be translated into action (either because of specific barriers to use or because some women may plan to use family planning only after reaching their desired family size). Seventy-three percent of never users reported intending to use family planning in the future. For these women, family planning counselling can help remove barriers to family planning use that may have been encountered in the past. For women who do not intend to use family planning, counselling can discuss reasons for their decision, identify barriers to use and highlight the importance of birth spacing. In our population, unmet need for spacing births was higher than unmet need for limiting births; counselling could thus emphasize the role of family planning for birth spacing and promote reversible family planning methods. Higher past family planning use in HIV-positive women should not lead to the assumption that HIV-positive women are less in need of family planning counselling: unmet need for family planning in HIV-positive women was as high as in HIV-negative women, stressing the need for comprehensive counselling, regardless of HIV status. Our estimate of unmet need for family planning (28%) is close to the Demographic and Health Survey (DHS) 2005 estimate for Mwanza region (25% [7] ), suggesting that it is realistic.
Significantly fewer HIV-positive women than HIV-negative women wanted another child after their current pregnancy, suggesting a high future need for family planning in HIV-positive women. Meeting the future needs of HIV-positive women to prevent unwanted pregnancies is particularly important: it will reduce orphanhood and has been shown to be a cost-effective way to reduce MTCT [11,27,28] . However, insofar, as unmet need and future need for family planning were also very high in HIV-negative women, and given that most women do not know their HIV status, reducing unmet need in all women should remain the primary goal of family planning counselling services.
The increase in use of hormonal methods with age and from parity 0 to 1 should act as a reminder that young women with no previous children are less likely to have used family planning. Yet unmet need was still 16% in 15–19-year olds of parity 0. Family planning counselling should ensure that teenagers receive adequate information and access to family planning. The lower prevalence of past family planning use in rural and roadside areas compared with urban areas underscores the need to increase family planning access in nonurban areas, especially as the unmet need for family planning is as high as in urban areas. Integration of family planning counselling into ANC services may therefore be of highest priority in rural areas where sources of family planning information are likely to be fewer.
HIV counselling as a part of ANC services in Tanzania provides women with a chance to reflect on future childbearing in the light of their HIV status, and is thus a valuable opportunity to reach women with family planning information and provide truly comprehensive reproductive and sexual health services for HIV-positive and HIV-negative women. To maximize its effectiveness, this type of counselling could be reinforced closer to the time of family planning use, for example, during postnatal maternal child health (MCH) and vaccination clinics, which argues for further service integration.
Conclusion
Our study showed that among women in ANCs, only a minority of women have ever used family planning, and unmet need before pregnancy was high, but the reported future need for family planning was very high. Family planning counselling as a part of ANC services can fill the gaps between past use, intentions and needs by providing tailored information to every pregnant woman, HIV positive or HIV negative, so that the woman can make an informed decision about her future reproductive career. The public health importance of preventing unwanted pregnancies and MTCT should act as a strong incentive to integrate these services. If HIV-positive women become effective users of family planning, the need for costly PMTCT services will be reduced.
In order to design effective family planning counselling tailored to the needs of the clinic population, more research is needed to examine socio-demographic and reproductive profiles of ANC attendees in other settings. The success in integrating a family planning programme into ANC is likely to be dependent on its suitability to the particular social and cultural context.
Acknowledgements
This work was funded by the Global Fund for AIDS, Tuberculosis and Malaria.
Sarah Keogh was involved in the design of the survey and questionnaire and the training of interviewers. She carried out the data analysis and was responsible for writing of the manuscript.
Mark Urassa was the principal investigator for the study. He was involved in the survey design and was responsible for all survey logistics. He oversaw the recruitment and training of interviewers and the smooth running of the survey from start to finish.
Yusufu Kumogola was the field supervisor for the survey and was responsible for overseeing daily data collection activities, for ongoing and refresher training of the interviewers and quality control of questionnaires.
Julius Mngara was the senior laboratory technician responsible for HIV testing of DBS.
Basia Zaba was involved in the design of the survey and the questionnaire and contributed ideas to the data analysis.
Conflicts of interest: None.
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