Abstract
Background: Dual method use, which combines condoms with a more effective modern contraceptive to optimize prevention of HIV and unplanned pregnancy, is underutilized in high-risk heterosexual couples.
Materials and Methods: Heterosexual HIV-discordant Zambian couples were enrolled from couples' voluntary HIV counseling and testing services into an open cohort with 3-monthly follow-up (1994–2012). Relative to dual method use, defined as consistent condom use plus modern contraception, we examine predictors of (1) condom-only use (suboptimal pregnancy prevention) or (2) modern contraceptive use with inconsistent condom use (effective pregnancy prevention and suboptimal HIV prevention).
Results: Among 3,049 couples, dual method use occurred in 28% of intervals in M+F− and 23% in M−F+, p < 0.01; condom-only use in 56% in M+F− and 61% in M−F+, p < 0.01; and modern contraceptive use with inconsistent condom use in 16% regardless of serostatus. Predictors (p < 0.05) of condom-only use included the man being HIV+ (adjusted hazard ratio, aHR = 1.15); baseline oral contraceptive pill (aHR = 0.76), injectable (aHR = 0.48), or implant (aHR = 0.60) use; woman's age (aHR = 1.04 per 5 years) and lifetime number of sex partners (aHR = 1.01); postpartum periods (aHR = 1.25); and HIV stage of the index partner III/IV versus I (aHR = 1.10). Predictors (p < 0.05) of modern contraceptive use with inconsistent condom use included woman's age (aHR = 0.94 per 5 years) and HIV+ male circumcision (aHR = 1.51), while time-varying implant use was associated with more consistent condom use (aHR = 0.80).
Conclusions: Three-quarters of follow-up intervals did not include dual method use. This highlights the need for counseling to reduce unintended pregnancy and HIV transmission and enable safer conception.
Keywords: : dual contraceptive method use, unintended pregnancy risk, HIV transmission risk, serodiscordant couples, Zambia
Introduction
Dual method use is defined as the use of condoms for HIV/sexually transmitted infection (STI) prevention plus use of an effective modern contraceptive method for unintended pregnancy prevention. A public health priority, dual method use increases prevention of (1) HIV/STI; (2) unintended pregnancy; and (3) mother-to-child transmission (PMTCT) when seroconversion is prevented in pregnant and breastfeeding women (Prong 1 of PMTCT) and pregnancies are prevented in HIV-positive women (Prong 2 of PMTCT).1–4 Condoms are the front-line prevention tool for HIV/STIs. However, condom use alone is not as effective as other modern contraceptive options in preventing unintended pregnancy.5,6 We previously published that the pregnancy rate among HIV-discordant couples using condoms alone in our cohort was 26.4/100 couple-years.7 This reinforces the benefits of dual method use for added protection against unplanned pregnancy. Additionally, given that HIV-discordant couples seeking to conceive are at increased risk of HIV transmission,8–10 safer conception options are needed for discordant couples who wish to conceive.
Despite the knowledge that dual method use benefits women and couples, and despite World Health Organization (WHO) guidelines recommending dual contraceptive method use,11 little is known about the factors associated with dual method use. More literature focusing on independent barriers to consistent condom or contraceptive use is needed to develop and target uptake and adherence strategies in high-risk couples. We have previously described factors associated with unprotected sex12 and contraceptive method uptake/continuation13 in such couples. The current analysis adds to a larger picture of dual prevention to optimize HIV and unintended pregnancy prevention.
We explore predictors of condom-only use (to explore unintended pregnancy-related risk factors) and modern contraceptive use with inconsistent condom use (to explore HIV transmission-related risk factors).
Materials and Methods
Ethics
This study was approved by the Office for Human Research Protections-registered Institutional Review Boards (IRBs) at Emory University and in Zambia. The University of Zambia Biomedical Research Ethics Committee (IORG0000774) has US Office of Human Research Protection registration and one IRB committee (IRB00001131) that reviews research protocols. Written informed consent was obtained jointly from participating couples.
Participants
Married/cohabiting HIV serodiscordant heterosexual couples living in Lusaka, Zambia, were identified between 1994 and 2012 and enrolled in an open cohort with 3-monthly longitudinal follow-up and free outpatient healthcare, including family planning at the research clinic. Couples were identified from couples' voluntary HIV counseling and testing (CVCT) services established by the Rwanda Zambia HIV Research Group (RZHRG). CVCT services include a group educational counseling session, on-site rapid HIV antibody testing, and joint post-HIV test counseling of the couple. CVCT promotional and recruitment strategies,14,15 enrollment procedures, retention and attrition,16 HIV testing and counseling procedures,16,17 and cohort demographics16,18 have been previously published.
Data collection
Demographic (including baseline age, years cohabiting, monthly income, literacy in Nyanja, religion, maternal language, and alcohol use), family planning and sexual history (including lifetime number of sexual partners, number of previous pregnancies, and fertility intentions), and clinical (including baseline HIV stage and viral load of the HIV-positive partners and male partner circumcision status) measures were collected at baseline. Fertility intentions were collected at enrollment from 2002 to 2011. Knowledge about and concerns with modern contraceptives were collected at baseline from 2002 to 2007.19 Condom use, contraceptive method use, and postpartum status were recorded during follow-up. Postpartum status was dichotomized in this analysis as being up to 6 months postpartum versus not pregnant/not postpartum.
Outcomes of interest
The first outcome of interest was time-varying condom-only use (consistent or inconsistent) without concurrent use of a modern contraceptive method (implant, injectables, copper intrauterine device [IUD], oral contraceptive pills [OCPs]) (Table 1). Indicators of unprotected sex with the study partner include self-reported condomless sex, sperm on a vaginal swab wet mount, incident pregnancy, or incident HIV seroconversion. This outcome was modeled to explore unintended pregnancy-related risk factors.
Table 1.
Nondual method use risk groups | Referent group | |
---|---|---|
Outcome 1 | Condom-only use: time-varying condom-only use (consistent or inconsistent) without modern contraceptive method use in the previous study interval | Consistent dual method use: time-varying modern contraceptive method use, with no indication of unprotected sex with the study partner in the previous study interval |
Outcome 2 | Modern contraceptive use with inconsistent condom use: time-varying modern contraceptive method use, with indication of condomless sex in the previous study interval |
The second outcome of interest was time-varying modern contraceptive use with inconsistent condom use, defined as intervals in which a modern contraceptive method (including surgical sterilization) was used, but condom use (defined using the above indicators of unprotected sex) was inconsistent. This outcome was modeled to explore HIV transmission-related risk factors.
Referent group
The time-varying dual method use was defined as having no indicator of unprotected sex with the study partner plus the use of a modern contraceptive method (implant, injectables, IUD, OCPs, and surgical sterilization) (Table 1).
Analysis methods
Couples were censored if the partner who was HIV negative (HIV−) at enrollment seroconverted; if the partner who was HIV positive (HIV+) at enrollment initiated antiretroviral treatment (ART, which became available in government clinics in 2007); and if either partner died or if the couple separated, relocated, or were otherwise lost to follow-up. Additionally, we exclude 8% of study intervals during which couples are not at risk for dual method use due to pregnancy or lack of sexual activity. In the model of condom use only, couples who are sterilized (n = 40 couples) were excluded from the analysis as they were not at risk for method uptake.
The distributions of dual method use, condom-only use, and modern contraceptive use with inconsistent condom use were calculated over all study intervals. Differences between M+F− and M−F+ couples were quantified using p-values from McNemar's tests for correlated proportions. The distributions of exposure covariates were calculated (means and standard deviations [SDs] for normal continuous variables; medians and interquartile ranges for non-normal continuous variables; and counts and percentages for categorical variables) stratified by the outcomes of interest. We present baseline (cross-sectional) cohort demographics in the text; longitudinal (time on study weighted-average) measures of frequency are given in the tables.
In univariable and multivariable analyses, repeated outcomes survival analysis models (Andersen–Gill models) explored factors associated with the two outcomes of interest. Andersen–Gill models are a counting process extension of Cox survival models that accommodate longitudinal data with nonindependent repeated outcomes. As we had no primary exposure of interest, multivariable models comprised all covariates that were significantly (p < 0.05) associated with the outcome of interest in univariable analyses in our primary analysis models. Subanalysis models were run, including variables associated with the outcome of interest in univariable models that were not collected over all study follow-up intervals (e.g., fertility intentions, collected from 2002 to 2011; and contraceptive method knowledge and concerns, collected from 2002 to 2007). We explored the potential for interaction by the gender of the HIV-positive partner, but did not find major differences—thus, couple serostatus is considered as a covariate in the models.
Data analysis was conducted with SAS, v9.4 (Cary, NC).
Results
Distribution of outcomes and cohort demographics
Among 3,049 discordant couples (N = 1,393 M+F−, N = 1,656 M−F+) followed for an average of roughly 2 years, dual method use was recorded in 26% of intervals (28% in M+F− and 23% in M−F+, p < 0.01), condom-only use in 59% of intervals (56% in M+F− and 61% in M−F+, p < 0.01), and modern contraceptive use with inconsistent condom use (16% regardless of couple serostatus) (Table 2). M+F− couples were more likely (p < 0.01) to have any intervals, including IUD and implant use (12% of overall study intervals), compared with M−F+ couples (8% of overall study intervals). Of intervals reporting condom-only (consistent or inconsistent) use without modern contraception, 37% (32% in M+F− and 40% in M−F+, p < 0.01) had an indication of unprotected sex.
Table 2.
All couples | M + F− | M−F+ | |||||
---|---|---|---|---|---|---|---|
N intervals | % | N intervals | % | N intervals | % | p | |
Dual method use | 6,096 | 26 | 3,343 | 28 | 2,753 | 23 | * |
Condoms only | 14,015 | 59 | 6,675 | 56 | 7,340 | 61 | * |
Modern contraceptive use with inconsistent condom use | 3,723 | 16 | 1,854 | 16 | 1,869 | 16 | |
Contraceptive method use | |||||||
Implant | 1,684 | 7 | 968 | 8 | 716 | 6 | * |
Injectables | 3,601 | 15 | 1,815 | 15 | 1,786 | 15 | |
IUD | 630 | 3 | 432 | 4 | 198 | 2 | * |
OCP | 3,557 | 15 | 1,798 | 15 | 1,759 | 15 | |
Permanent method | 347 | 1 | 184 | 2 | 163 | 1 | |
Unprotected sex | |||||||
Yes | 8,848 | 37 | 4,022 | 34 | 4,826 | 40 | * |
No | 14,986 | 63 | 7,850 | 66 | 7,136 | 60 |
Distributions are calculated across all study intervals.
p (two-tailed) <0.001.
IUD, intrauterine device; OCP, oral contraceptive pill.
At baseline, the average age of men in the cohort was 35.3 (SD = 8.0) years, the average age of women was 28.6 (SD = 6.7) years, the average time cohabiting was 7.2 (SD = 6.2) years, the average number of couples' previous pregnancies was 3.6 (SD = 2.4), and 49.6% of men and 57.6% of women stated they did not want more children.
Condom-only use
Univariable analysis results are presented for condom-only versus dual method use (Tables 3 and 4). Condom-only use was more likely among M+F− compared with M−F+ couples and older women. There were no differences by years cohabiting, literacy, religious affiliation, or maternal language/tribal group. Not surprisingly, baseline OCP and injectable contraceptive use were associated with less condom-only use during follow-up, as were baseline implant (p = 0.065) and IUD use (p = 0.098), although the hazard ratios (HRs) were not significant likely due to small numbers. Condom-only use was associated with HIV disease stages III–IV and with higher viral load of the HIV+ partner (p = 0.089). Man's age, number of lifetime partners, and circumcision status were not associated with condom-only use. Women's higher number of lifetime sex partners was significantly associated with condom-only use (HR = 1.00, p < 0.0001). Both men and women wanting a pregnancy in the next year were associated with condom-only use, as were being in the postpartum period during follow-up. Knowledge of and concerns about contraceptive methods were not predictive.
Table 3.
Condom-only using intervals | Dual method using intervals | |||||||
---|---|---|---|---|---|---|---|---|
N intervals/means | %/SD | N intervals/means | %/SD | HR | 95% CI | p-Value (two-tail) | ||
Couple serostatus | ||||||||
M+F− (N = 1,393) | 6,675 | 48% | 3,316 | 55% | 1.13 | 1.07 | 1.20 | <0.0001 |
M−F+ (N = 1,656) | 7,340 | 52% | 2,740 | 45% | Ref. | |||
Man's age in years (mean, SD) (HR per 5-year increase) | 35.69 | 8.34 | 35.24 | 7.46 | 1.01 | 0.995 | 1.03 | 0.189 |
Woman's age in years (mean, SD) (HR per 5-year increase) | 29.03 | 7.01 | 28.42 | 6.24 | 1.02 | 1.01 | 1.04 | 0.014 |
Household Income in USD (median, IQR) (HR per 20 USD increase) | 57.50 | 71.80 | 55.20 | 71.70 | 1.00 | 0.99 | 1.01 | 0.857 |
Years cohabiting (mean, SD) (HR per 5-year increase) | 7.09 | 6.58 | 7.60 | 5.80 | 0.99 | 0.97 | 1.02 | 0.552 |
Woman reads Nyanja | ||||||||
Yes, easily | 3,312 | 24% | 1,389 | 24% | Ref. | |||
With difficulty/not at all | 10,647 | 76% | 4,453 | 76% | 1.02 | 0.96 | 1.08 | 0.586 |
Man reads Nyanja | ||||||||
Yes, easily | 4,647 | 43% | 2,042 | 45% | Ref. | |||
With difficulty/not at all | 6,235 | 57% | 2,496 | 55% | 1.02 | 0.95 | 1.09 | 0.612 |
Man's religion (2002–2012) | ||||||||
Catholic | 1,251 | 28% | 883 | 29% | 0.95 | 0.81 | 1.11 | 0.509 |
Other Christian | 2,297 | 52% | 1,582 | 52% | 0.95 | 0.83 | 1.10 | 0.498 |
Other/none | 910 | 20% | 603 | 20% | Ref. | |||
Woman's religion (2002–2012) | ||||||||
Catholic | 1,743 | 23% | 1,025 | 24% | 1.02 | 0.90 | 1.15 | 0.775 |
Other Christian | 4,670 | 62% | 2,673 | 61% | 1.03 | 0.92 | 1.14 | 0.637 |
Other/none | 1,085 | 14% | 662 | 15% | Ref. | |||
Baseline contraceptive method used | ||||||||
None/condoms alone | 12,298 | 88% | 4,253 | 71% | Ref. | |||
OCP | 1,128 | 8% | 916 | 15% | 0.78 | 0.68 | 0.90 | 0.001 |
Injectable | 331 | 2% | 615 | 10% | 0.51 | 0.41 | 0.64 | <0.0001 |
Implant | 81 | 1% | 115 | 2% | 0.59 | 0.34 | 1.03 | 0.065 |
IUD | 59 | 0% | 124 | 2% | 0.50 | 0.22 | 1.14 | 0.098 |
Number of previous pregnancies (mean, SD) (HR per pregnancy increase) | 3.49 | 2.49 | 3.76 | 2.22 | 0.99 | 0.98 | 1.00 | 0.125 |
HIV stage of HIV+ partner | ||||||||
Stage I | 4,818 | 34% | 2,156 | 36% | Ref. | |||
Stage II | 4,684 | 33% | 2,117 | 35% | 1.04 | 0.97 | 1.11 | 0.315 |
Stage III | 3573.00 | 25% | 1,403 | 23% | 1.12 | 1.05 | 1.21 | 0.002 |
Stage IV | 940 | 7% | 380 | 6% | 1.16 | 1.04 | 1.29 | 0.007 |
Log viral load of HIV+ partner (mean, SD) (HR per log vial load increase) | 4.53 | 0.89 | 4.39 | 93% | 1.04 | 0.99 | 1.09 | 0.089 |
Circumcision status (male partner) | ||||||||
Yes | 1,874 | 13% | 773 | 13% | Ref. | |||
No | 12,134 | 87% | 5,256 | 87% | 1.03 | 0.95 | 1.12 | 0.448 |
Man lifetime sex partners (mean, SD) (HR per partner increase) | 10.78 | 14.46 | 11.64 | 14.64 | 1.00 | 1.00 | 1.00 | 0.942 |
Woman lifetime sex partners (mean, SD) (HR per partner increase) | 3.53 | 8.46 | 2.97 | 5.45 | 1.00 | 1.00 | 1.01 | <0.0001 |
Postpartum status (time varying)a | ||||||||
Not pregnant/not postpartum | 11,363 | 96% | 5,202 | 99% | Ref. | |||
Postpartum (up to 6 months) | 477 | 4% | 73 | 1% | 1.25 | 1.18 | 1.34 | <0.0001 |
Fertility intentions of man (2002–2011) | ||||||||
Yes, next year | 973 | 22% | 237 | 8% | 1.50 | 1.32 | 1.70 | <0.0001 |
Yes, but not next year | 1,478 | 33% | 1,113 | 36% | 1.11 | 0.97 | 1.27 | 0.126 |
Don't know/no | 2,007 | 45% | 1,718 | 56% | Ref. | |||
Fertility intentions of woman (2002–2011) | ||||||||
Yes, next year | 1,479 | 29% | 349 | 10% | 1.48 | 1.32 | 1.65 | <0.0001 |
Yes, but not next year | 1,051 | 21% | 757 | 22% | 1.12 | 0.98 | 1.29 | 0.102 |
Don't know/no | 2,517 | 50% | 2,259 | 67% | Ref. |
Analysis excludes n = 40 women who were sterilized at baseline (not at risk for the outcome of interest).
Time-varying variable.
CI, confidence interval; HR, hazard ratio; IQR, interquartile range; SD, standard deviation; USD, United States Dollar.
Table 4.
Primary analysis (1994–2012) | Subanalysis (2002–2011) | |||||||
---|---|---|---|---|---|---|---|---|
aHR | 95% CI | p-Value (two-tail) | aHR | 95% CI | p-Value (two-tail) | |||
Couple serostatus | ||||||||
M+F− | 1.15 | 1.09 | 1.22 | <0.0001 | 1.14 | 1.02 | 1.27 | 0.021 |
M−F+ | Ref. | Ref. | ||||||
Woman's age in years (aHR per 5-year increase) | 1.04 | 1.02 | 1.06 | <0.001 | 1.06 | 1.02 | 1.11 | 0.003 |
Baseline contraceptive method used | ||||||||
None/condoms alone | Ref. | Ref. | ||||||
OCP | 0.76 | 0.20 | 0.87 | <0.0001 | 0.56 | 0.43 | 0.73 | <0.0001 |
Injectable | 0.48 | 0.38 | 0.60 | <0.0001 | 0.39 | 0.28 | 0.56 | <0.0001 |
Implant | 0.60 | 0.36 | 0.995 | 0.048 | 1.18 | 0.90 | 1.55 | 0.239 |
IUD | 0.52 | 0.24 | 1.13 | 0.096 | n/a | |||
HIV stage of HIV+ partner | ||||||||
Stage I | Ref. | Ref. | ||||||
Stage II | 1.01 | 0.94 | 1.08 | 0.789 | 1.00 | 0.88 | 1.14 | 0.988 |
Stage III or IV | 1.10 | 1.03 | 1.17 | 0.005 | 1.11 | 0.98 | 1.26 | 0.106 |
Woman lifetime number of sex partners (aHR per partner increase) | 1.01 | 1.00 | 1.01 | <0.0001 | 1.01 | 1.01 | 1.01 | <0.0001 |
Postpartum status (time varying)a | ||||||||
Not pregnant/not postpartum | Ref. | Ref. | ||||||
Postpartum (up to 6 months) | 1.25 | 1.17 | 1.34 | <0.0001 | 1.37 | 1.22 | 1.54 | <0.0001 |
Fertility intentions of woman (2002–2011) | ||||||||
Yes, next year | 1.39 | 1.25 | 1.55 | <0.0001 | ||||
Yes, but not next year | 1.20 | 1.03 | 1.39 | 0.017 | ||||
Don't know/no | Ref. |
Analysis excludes n = 40 women who were sterilized at baseline (not at risk for the outcome of interest).
Time-varying variable.
aHR, adjusted hazard ratio.
In the primary multivariable model (Table 4), predictors of condom-only use versus dual method use during follow-up intervals (p < 0.05) included the man being the HIV+ partner (adjusted hazard ratio, aHR = 1.15); baseline OCP (aHR = 0.76), injectable (aHR = 0.48), or implant (aHR = 0.60) use; increasing woman's age (aHR = 1.01) and lifetime number of sex partners (aHR = 1.01); postpartum periods (aHR = 1.25); and stage III–IV versus I HIV disease of the index partner (aHR = 1.10). In subanalyses, including fertility intentions, wanting to have a child either in the text year (aHR = 1.39) or later (aHR = 1.20) was also predictive.
Modern contraceptive use with inconsistent condom use
Univariable analysis results are presented for modern contraceptive use with inconsistent condom use versus dual method use (Tables 5 and 6). Younger ages of men and women were associated with inconsistent condom use among modern contraceptive users, as was use of injectables and implants at baseline. However, over follow-up intervals, time-varying implant use and surgical sterilization (adopted by 68 women after enrollment) were associated with consistent condom use. Women wanting a pregnancy, but not in the next year, were associated with modern contraceptive use with inconsistent condom use, and an interaction between HIV status and circumcision was discovered (with HIV+ circumcised men with wives using modern contraception being at increased hazard for inconsistent condom use). Knowledge of and concerns about contraceptive methods were not predictive.
Table 5.
Method using intervals | Dual method using intervals | |||||||
---|---|---|---|---|---|---|---|---|
N intervals | % | N intervals | % | HR | 95% CI | p-Value (two-tail) | ||
Couple serostatus | ||||||||
M+F− | 1,854 | 50% | 3,343 | 55% | 1.06 | 0.94 | 1.18 | 0.343 |
M−F+ | 1,869 | 50% | 2,753 | 45% | Ref. | |||
Man's age in years (mean, SD) (HR per 5-year increase) | 33.92 | 7.52 | 35.30 | 7.48 | 0.95 | 0.91 | 0.99 | 0.010 |
Woman's age in years (mean, SD) (HR per 5-year increase) | 27.22 | 6.03 | 28.48 | 6.27 | 0.95 | 0.90 | 0.99 | 0.013 |
Household income in USD (median, IQR) (HR per 20 USD increase) | 49.56 | 64.03 | 55.00 | 71.40 | 0.99 | 0.98 | 1.01 | 0.467 |
Years cohabiting (mean, SD) (HR per 5-year increase) | 6.85 | 5.38 | 7.65 | 5.81 | 0.97 | 0.92 | 1.02 | 0.219 |
Woman reads Nyanja | ||||||||
Yes, easily | 879 | 24% | 1,407 | 24% | Ref. | |||
With difficulty/not at all | 2,709 | 76% | 4,475 | 76% | 0.97 | 0.84 | 1.12 | 0.669 |
Man reads Nyanja | ||||||||
Yes, easily | 1,381 | 45% | 2,073 | 45% | ||||
With difficulty/not at all | 1,688 | 55% | 2,497 | 55% | 0.98 | 0.86 | 1.11 | 0.721 |
Man's religion (2002–2012) | ||||||||
Catholic | 444 | 26% | 900 | 29% | 0.87 | 0.68 | 1.10 | 0.247 |
Other Christian | 893 | 53% | 1,585 | 51% | 0.99 | 0.80 | 1.21 | 0.923 |
Other/none | 349 | 21% | 615 | 20% | Ref. | |||
Woman's religion (2002–2012) | ||||||||
Catholic | 449 | 20% | 1,032 | 23% | 0.88 | 0.70 | 1.11 | 0.273 |
Other Christian | 1,393 | 64% | 2,686 | 61% | 1.02 | 0.83 | 1.25 | 0.847 |
Other/none | 349 | 16% | 682 | 16% | Ref. | |||
Baseline contraceptive method used | ||||||||
None/condoms alone | 2,455 | 66% | 4,253 | 70% | Ref. | |||
OCP | 614 | 17% | 916 | 15% | 1.11 | 0.94 | 1.32 | 0.205 |
Injectable | 433 | 12% | 615 | 10% | 1.25 | 1.05 | 1.50 | 0.015 |
Implant | 95 | 3% | 115 | 2% | 1.44 | 1.02 | 2.03 | <0.001 |
IUD | 87 | 2% | 124 | 2% | 1.14 | 0.72 | 1.79 | 0.574 |
Sterilization | 19 | 1% | 40 | 1% | 0.93 | 0.37 | 2.33 | 0.883 |
Time-varying contraceptive method use | ||||||||
OCP | 1,491 | 40% | 2,023 | 34% | Ref. | |||
Injectable | 1,446 | 39% | 2,107 | 35% | 1.04 | 0.93 | 1.16 | 0.501 |
Implant | 449 | 12% | 1,220 | 20% | 0.81 | 0.66 | 1.00 | 0.055 |
IUD | 231 | 6% | 392 | 7% | 1.09 | 0.82 | 1.45 | 0.558 |
Sterilization | 87 | 2% | 259 | 4% | 0.65 | 0.44 | 0.98 | 0.040 |
Number of previous pregnancies (mean, SD) (HR per pregnancy increase) | 3.68 | 2.09 | 3.77 | 2.22 | 1.00 | 0.97 | 1.02 | 0.823 |
HIV stage of HIV+ partner | ||||||||
Stage I | 1,333 | 36% | 2,164 | 35% | Ref. | |||
Stage II | 1,306 | 35% | 2,120 | 35% | 0.91 | 0.79 | 1.05 | 0.196 |
Stage III | 876 | 24% | 1,428 | 23% | 0.92 | 0.79 | 1.07 | 0.263 |
Stage IV | 208 | 6% | 384 | 6% | 0.90 | 0.72 | 1.12 | 0.340 |
Log viral load of HIV+ partner (mean, SD) (HR per log viral load increase) | 4.49 | 0.93 | 4.39 | 93% | 1.03 | 0.94 | 1.13 | 0.489 |
Circumcision status (male partner) | ||||||||
Yes | 543 | 15% | 773 | 13% | Ref. | |||
No | 3,170 | 85% | 5,296 | 87% | 0.88 | 0.75 | 1.04 | 0.140 |
Man lifetime sex partners (mean, SD) (HR per partner increase) | 11.41 | 14.94 | 11.66 | 18.44 | 1.00 | 1.00 | 1.00 | 0.615 |
Woman lifetime sex partners (mean, SD) (HR per partner increase) | 3.03 | 2.58 | 2.97 | 5.44 | 1.00 | 0.99 | 1.01 | 0.945 |
Postpartum status (time-varying) | ||||||||
Not pregnant/not postpartum | 4,504 | 98% | 4,059 | 98% | Ref. | |||
Postpartum (up to 6 months) | 70 | 2% | 63 | 2% | 1.14 | 0.90 | 1.43 | 0.286 |
Fertility intentions of man (2002–2011) | ||||||||
Yes, next year | 164 | 10% | 237 | 8% | 1.19 | 0.93 | 1.52 | 0.171 |
Yes, but not next year | 697 | 41% | 1,113 | 36% | 1.17 | 0.97 | 1.41 | 0.108 |
Don't know/no | 825 | 49% | 1,750 | 56% | Ref. | |||
Fertility intentions of woman (2002–2011) | ||||||||
Yes, next year | 178 | 10% | 349 | 10% | 0.97 | 0.74 | 1.29 | 0.854 |
Yes, but not next year | 545 | 30% | 757 | 22% | 1.25 | 1.04 | 1.49 | 0.015 |
Don't know/no | 1,105 | 60% | 2,291 | 67% | Ref. | |||
Circumcision × serostatus | ||||||||
M+F− | ||||||||
Yes | 253 | 7% | 306 | 5% | 1.55 | 1.19 | 2.01 | 0.001 |
No | 1,594 | 43% | 3,028 | 50% | 0.99 | 0.87 | 1.11 | 0.815 |
M−F+ | ||||||||
Yes | 290 | 8% | 467 | 8% | 0.91 | 0.76 | 1.08 | 0.289 |
No | 1,576 | 42% | 2,268 | 37% | Ref. |
Table 6.
Primary analysis (1994–2012) | Subanalysis (2002–2011) | |||||||
---|---|---|---|---|---|---|---|---|
aHR | 95% CI | p-Value (two-tail) | aHR | 95% CI | p-Value (two-tail) | |||
Woman's age in years (aHR per 5-year increase) | 0.94 | 0.90 | 0.98 | 0.024 | 0.98 | 0.92 | 1.04 | 0.766 |
Baseline contraceptive method used | ||||||||
None/condoms alone | Ref. | Ref. | ||||||
OCP | 1.07 | 0.91 | 1.27 | 0.406 | 0.96 | 0.77 | 1.19 | 0.703 |
Injectable | 1.24 | 1.04 | 1.49 | 0.017 | 1.32 | 1.07 | 1.62 | 0.008 |
Implant | 1.66 | 1.16 | 2.38 | 0.006 | 1.98 | 1.31 | 2.99 | 0.001 |
IUD | 1.07 | 0.64 | 1.77 | 0.802 | 0.61 | 0.37 | 0.99 | 0.048 |
Sterilization | 1.47 | 0.54 | 4.01 | 0.453 | 1.13 | 0.45 | 2.83 | 0.788 |
Time-varying contraceptive method use | ||||||||
OCP | Ref. | Ref. | ||||||
Injectable | 1.03 | 0.92 | 1.15 | 0.634 | 1.05 | 0.89 | 1.23 | 0.569 |
Implant | 0.80 | 0.64 | 0.99 | 0.042 | 0.79 | 0.62 | 1.03 | 0.086 |
IUD | 1.12 | 0.83 | 1.53 | 0.461 | 1.59 | 1.76 | 2.38 | 0.023 |
Sterilization | 0.71 | 0.44 | 1.15 | 0.161 | 1.01 | 0.65 | 1.56 | 0.980 |
Fertility intentions of woman (2002–2011) | ||||||||
Yes, next year | 1.07 | 0.81 | 1.41 | 0.647 | ||||
Yes, but not next year | 1.25 | 1.05 | 1.49 | 0.012 | ||||
Don't know/no | Ref. | |||||||
Circumcision × serostatus | ||||||||
M+F− | ||||||||
Yes | 1.51 | 1.14 | 1.99 | 0.004 | 1.59 | 1.07 | 2.35 | 0.022 |
No | 0.97 | 0.86 | 1.10 | 0.645 | 0.82 | 0.70 | 0.97 | 0.019 |
M−F+ | ||||||||
Yes | 0.93 | 0.78 | 1.12 | 0.446 | 0.85 | 0.63 | 1.15 | 0.289 |
No | Ref. | Ref. |
In the primary multivariable model (Table 6), predictors (p < 0.05) of modern contraceptive use with inconsistent condom use versus dual method use included woman's decreasing age (aHR = 0.99) and HIV+ male circumcision (aHR = 1.51) while time-varying implant use (aHR = 0.80). In subanalyses, women desiring more children, but not in the next year (aHR = 1.25), and time-varying IUD use (aHR = 1.6) were predictive of the outcome, while baseline IUD use (aHR = 0.61) and HIV+ men not being circumcised (aHR = 0.82) were protective.
Discussion
In this study, we explore unintended pregnancy-related risk factors and HIV transmission-related risk factors. In our cohort, the use of both condoms and contraceptive methods increased drastically from baseline method use (Table 3) to time-varying use after the couple was jointly counseled about their serodiscordant status (Table 5). However, among condom-only using intervals, almost 37% had an indication of unprotected sex, indicating risk of both HIV and unplanned pregnancy for these couples. Among modern contraceptive using intervals, 38% included an indication of inconsistent condom use, and although risk of unplanned pregnancy was reduced, the risk of HIV transmission remained. Dual method use—combining a modern contraceptive method with consistent condom use in this cohort of HIV serodiscordant couples—was noted in only 23%–28% of follow-up intervals. We describe the profile of Zambian discordant couples who may require increased fertility goal-based dual method counseling to prevent both HIV/STI and unintended pregnancy.
At least half of couples in our cohort did not want more children, yet 59% of follow-up intervals included only condom use despite the availability of the full range of modern contraceptive options offered at the research clinic. A study among HIV+ women in care and treatment in Swaziland similarly found that most women rely on condoms alone and hypothesized that this is related to a long history of HIV programs focusing solely on condoms for HIV+ people.20 Additionally, 16% of follow-up intervals were among modern method users who were using condoms inconsistently (although as we have reported previously, follow-up intervals with long-acting reversible contraception [LARC] use include significantly fewer intervals with unprotected sex relative to condom use alone21,22). A study in South Africa similarly found that among younger men and women (ages 18–24), dual method use was rare (15.4%) and was associated with higher sexual frequency and men's knowledge of contraceptive methods.23 Studies among younger populations in sub-Saharan Africa have noted that concerns about possible perceptions of infidelity may be a barrier to condom negotiation.24–26 Although we did not find that couples' contraceptive knowledge predicted either outcome, the importance of involving men in informative conversations about contraceptive methods is indicated.
It is important to note that the concept of dual method use has been complicated among target audiences, providers, and national and international health agencies due to confusion between the related terms dual protection and dual method use (with dual protection defined as simultaneous protection against unintended pregnancy and HIV/STIs [possibly with condoms alone] and dual method use defined as the simultaneous use of condoms with a more efficacious contraceptive method).27,28 Another point of confusion is that different studies of dual method use apply differing definitions, with dual method use sometimes defined as either consistent dual method use over time or at a specific interval (the definition we and others have used),29,30 while some typically cross-sectional studies define dual method use as women ever having used both condoms (consistently or inconsistently) plus a modern method within some previous time frame.23,31,32
In our study, older women were more likely to use condoms only (putting them at risk for unintended pregnancy), while younger women using modern methods were more likely to report inconsistent condom use (putting couples at risk for HIV transmission). Older couples may perceive themselves to be at lower risk for pregnancy and thus less likely to adopt modern methods along with their condom use. Conversely, although younger couples seem to be more successfully accessing contraception, they struggle with consistent condom use, possibly due to challenges posed by condom negotiation or gender norms.33 Among those using condoms only during follow-up, only 12% were using a modern contraceptive method at baseline. Although access to the full range of methods was provided at the research clinic, lack of familiarity may have been an obstacle,13,34 independent of age.
We also see that couples who are postpartum may be at increased risk of using condoms only, putting them at risk for unintended pregnancy. We have previously shown that while Zambian women in postpartum periods are reporting less sex in general,21 we show here that postpartum periods are characterized by both occasional unprotected sex and slow adoption of contraception. Poor postpartum dual method use could be due to low-risk perception among couples due to having less sex and lactational amenorrhea. Interestingly, a study among 821 South African women showed that although still suboptimal, the postpartum dual method use was higher among HIV-positive relative to HIV-negative women, and the authors conclude that HIV positivity may motivate women to adopt dual methods.35 We, however, see similar patterns of poor postpartum dual method use regardless of discordant couple serostatus (M+F− or M+F−) indicating a need for risk, contraception, and condom counseling postpartum among all discordant couples. Scale up of postpartum long-acting contraceptive method (IUDs and implant insertion) may be highly beneficial.
Other significant predictors of dual method use may be related to risk perception. Couples with more clinically advanced HIV+ partners were at increased risk of using condoms only without use of a modern contraceptive method, putting them at risk for unintended pregnancy. It is possible that couples with index partners having more clinically advanced HIV disease may not perceive themselves at high risk of pregnancy. Among couples using modern contraception, those with circumcised HIV+ men were more likely to have unprotected sex, while those with uncircumcised HIV+ men were less likely to have unprotected sex relative to HIV− uncircumcised referent group. This is an unexpected and concerning finding. It has been noted that messages regarding the protective effect of circumcision may be misinterpreted at times as being protective for male to female transmission.36,37 While some studies have not observed disinhibition38 related to male circumcision, others have seen decreased condom use in circumcised men, although HIV prevalence is still significantly lower in circumcised versus uncircumcised men, regardless of any behavioral disinhibition observed.39,40
The finding that couples with HIV+ uncircumcised men were more likely to use dual methods than contraception alone, but the highest risk group of HIV− uncircumcised men were not, was also surprising and warrants exploration.
As expected, increased fertility intentions are associated with any form of nondual method use, and expanded promotion of safe conception approaches is urgently needed for discordant couples. Targeting prevention efforts to discordant couples desiring pregnancy and discussing safe conception strategies (including intravaginal insemination; low-cost sperm washing; ART for prevention in the index partner; and pre-exposure prophylaxis in the HIV− partner41) are imperative.
When holistically considering the dual method-associated predictors that emerged in this study (whether risk perception possibly related to age, stage of disease, postpartum periods, circumcision status, or fertility intentions), improving dual method use can be achieved by integrating CVCT with couples' family planning services. We have previously shown that for couples who want to delay fertility, integrated couples' HIV and family planning counseling that provided access to LARC methods as well as reinforced dual-method use counseling led to increased uptake of IUDs and implants and reduced unprotected sex among HIV-discordant couples in Lusaka, Zambia, and Kigali, Rwanda.42
We have also recently reported on the sustained protective behavior changes that couples practice after CVCT, namely decreases in self-reported unprotected sex with the study partner, self-reported sex with outside partners, sperm on a vaginal swab wet prep, and incident STIs.43 Furthermore, regarding issues with contraceptive method education and concerns, we have shown that a video-based intervention providing information to couples on contraceptive methods can significantly increase contraceptive method uptake and decrease unintended pregnancy incidence among contraceptive experienced women.7,44 However, over time, method discontinuation and switching13,34 confirm the need not only for strong promotion but also support with method adherence and side effect management.
The importance of targeting couples to promote dual method use not only for family planning counseling but also importantly for facilitated HIV serostatus disclosure cannot be understated. In a cross-sectional study of 658 HIV+ women in Nigeria, the nondual method use was significantly associated with nondisclosure of HIV status with sexual partners.32 Similarly, a study in Botswana showed that discussing HIV and contraception with one's sexual partner was associated with dual method use,45 a nationally representative sample of young women in South Africa showed that strong communication about condoms and modern contraception with one's sexual partner was associated with dual method use,30 and a study of HIV+ adults in 18 HIV clinics in Kenya, Namibia, and Tanzania also showed that condom and contraception communication were associated with dual method use.46 Although we did not specifically measure couple-level communication factors in our study, the CVCT model with integrated family planning counseling provides couples with the tools to facilitate such critical conversations.47
A systematic review of the effectiveness of family planning counseling interventions for HIV+ African women (1990–2011) provides an overview of intervention impact on contraceptive uptake and pregnancy incidence and echoes our conclusion that CVCT and couples' family planning counseling should be integrated. This review concluded that successful interventions were focused on integrated family planning counseling and HIV prevention services with a focus on identifying fertility intentions and increasing contraceptive knowledge.48 Family planning and HIV prevention programs should integrate counseling on dual method use, and combining condoms for HIV/STI prevention with a long-acting contraceptive for added protection against unintended pregnancy warrants repetition.19,49
Limitations to our study include the potential for misclassification of the outcomes. Such misclassification is more of a concern with measures of unprotected sex and OCP use, compared with injectable contraceptives, implants, and IUD, which were administered/inserted at the research clinic. However, we would not expect such misclassification to be differential by the covariates of interest, and we used multiple measures of unprotected sex (self-report and biological) to mitigate possible misclassification. Self-selection into the cohort likely creates a bias for more health-motivated couples, possibly with more stable long-term relationships, and therefore limits generalizability. From the data, we cannot discern whether women are exclusively breastfeeding during postpartum intervals in the 3 months between study visits; although exclusive breastfeeding can be effective at preventing pregnancy, this method should not be relied on to prevent pregnancy as the ability to exclusively breastfeed may change.
Conclusions
These results highlight the risk profile of Zambian discordant couples who may require dual contraceptive method promotion. Importantly, these are well-counseled couples who receive family planning and condom use counseling, as well as access to contraception, at regular intervals. Our study participants know their joint HIV status and serodiscordancy compared with other settings where testing and disclosure of status are not common. Thus, this study represents a near-ideal world among couples and highlights persistent gaps in consistent condom and family planning uptake. As ART services are expanded and more serodiscordant couples are becoming virally suppressed, prevention of HIV transmission within discordant couples and safe conception strategies will increasingly rely on ART. However, given that many ART-eligible Africans are still not accessing treatment50 and ART adherence in Zambia remains imperfect,51,52 it remains important to promote low-cost prevention options in cases where virologic suppression for the positive partner is not achieved. Our results highlight the need for counseling to prevent unintended pregnancy and HIV transmission and enable safer conception. This can best be achieved by integrating CVCT with couples' family planning services.
Acknowledgments
This study was supported by the National Institute of Child Health and Development (NICHD R01 HD40125); National Institute of Mental Health (NIMH R01 66767); the AIDS International Training and Research Program Fogarty International Center (D43 TW001042); the Emory Center for AIDS Research (P30 AI050409); National Institute of Allergy and Infectious Diseases (NIAID R01 AI51231; NIAID R01 AI040951; NIAID R01 AI023980; NIAID R01 AI64060; NIAID R37 AI51231); the US Centers for Disease Control and Prevention (5U2GPS000758); and the International AIDS Vaccine Initiative. This study was made possible by the generous support of the American people through the US Agency for International Development (USAID). The contents do not necessarily reflect the views of USAID or the US Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author Disclosure Statement
No competing financial interests exist.
References
- 1.PEPFAR. Prevention of mother-to-child transmission of HIV: Expert panel report and recommendations to the U.S. congress and U.S. global AIDS coordinator 2010. Available at: www.pepfar.gov/documents/organization/135465.pdf Accessed September1, 2016
- 2.Cates W, Jr., Steiner MJ. Dual protection against unintended pregnancy and sexually transmitted infections: What is the best contraceptive approach? Sex Transm Dis 2002;29:168–174 [DOI] [PubMed] [Google Scholar]
- 3.Woodsong C, Koo HP. Two good reasons: Women's and men's perspectives on dual contraceptive use. Soc Sci Med 1999;49:567–580 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Berer M. Dual protection: Making sex safer for women. London: Reproductive Health Matters, 1997 [Google Scholar]
- 5.Raifman J, Chetty T, Tanser F, et al. Preventing unintended pregnancy and HIV transmission: Effects of the HIV treatment cascade on contraceptive use and choice in rural KwaZulu-Natal. J Acquir Immune Defic Syndr (1999) 2014;67 Suppl 4:S218–S227 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Polis CB, Bradley SE, Bankole A, Onda T, Croft T, Singh S. Typical-use contraceptive failure rates in 43 countries with Demographic and Health Survey data: Summary of a detailed report. Contraception 2016;94:11–17 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Wall KM, Haddad L, Vwalika B, et al. Unintended pregnancy among HIV positive couples receiving integrated HIV counseling, testing, and family planning services in Zambia. PLoS One 2013;8:e75353. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Nakayiwa S, Abang B, Packel L, et al. Desire for children and pregnancy risk behavior among HIV-infected men and women in Uganda. AIDS Behav 2006;10(4 Suppl):S95–S104 [DOI] [PubMed] [Google Scholar]
- 9.Myer L, Morroni C, Rebe K. Prevalence and determinants of fertility intentions of HIV-infected women and men receiving antiretroviral therapy in South Africa. AIDS Patient Care STDs 2007;21:278–285 [DOI] [PubMed] [Google Scholar]
- 10.Beyeza-Kashesya J, Ekstrom AM, Kaharuza F, Mirembe F, Neema S, Kulane A. My partner wants a child: A cross-sectional study of the determinants of the desire for children among mutually disclosed sero-discordant couples receiving care in Uganda. BMC Public Health 2010;10:247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.World Health Organization. Medical eligibility criteria for contraceptive use, 5th ed. Geneva, Switzerland: WHO Press, 2015 [PubMed] [Google Scholar]
- 12.Wall KM, Kilembe W, Vwalika B, et al. Sustained effect of couples' HIV counselling and testing on reducing unprotected sex among HIV serodiscordant couples Paper presented at: AIDS 2016; Durban, South Africa [Google Scholar]
- 13.Haddad L, Wall KM, Vwalika B, et al. Contraceptive discontinuation and switching among couples receiving integrated HIV and family planning services in Lusaka, Zambia. AIDS 2013;27 Suppl 1:S93–S103 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Wall KM, Kilembe W, Nizam A, et al. Promotion of couples' voluntary HIV counselling and testing in Lusaka, Zambia by influence network leaders and agents. BMJ Open. 2012. September 6;2(5). pii: [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Mark KE, Meinzen-Derr J, Stephenson R, et al. Contraception among HIV concordant and discordant couples in Zambia: A randomized controlled trial. J Women's Health (Larchmt) 2007;16:1200–1210 [DOI] [PubMed] [Google Scholar]
- 16.Kempf MC, Allen S, Zulu I, et al. Enrollment and retention of HIV discordant couples in Lusaka, Zambia. J Acquir Immune Defic Syndr (1999) 2008;47:116–125 [DOI] [PubMed] [Google Scholar]
- 17.Boeras DI, Luisi N, Karita E, et al. Indeterminate and discrepant rapid HIV test results in couples' HIV testing and counselling centres in Africa. J Int AIDS Soc 2011;14:18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Dunkle KL, Greenberg L, Lanterman A, Stephenson R, Allen S. Source of new infections in generalised HIV epidemics—Authors' reply. Lancet 2008;372:1300–1301 [DOI] [PubMed] [Google Scholar]
- 19.Grabbe K, Stephenson R, Vwalika B, et al. Knowledge, use, and concerns about contraceptive methods among sero-discordant couples in Rwanda and Zambia. J Women's Health (Larchmt) 2009;18:1449–1456 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Church K, Wringe A, Fakudze P, et al. Reliance on condoms for contraceptive protection among HIV care and treatment clients: A mixed methods study on contraceptive choice and motivation within a generalised epidemic. Sex Transm Infect 2014;90:394–400 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Wall KM, Kilembe W, Vwalika B, et al. Hormonal contraception does not increase women's HIV acquisition risk in Zambian discordant couples, 1994–2012. Contraception 2015;91:480–487 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Wall KM, Kilembe W, Vwalika B, et al. Hormonal contraceptive use among HIV-positive women and HIV transmission risk to male partners, Zambia, 1994–2012. J Infect Dis 2016;214:1063–1071 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Seutlwadi L, Peltzer K. The use of dual or two methods for pregnancy and HIV prevention amongst 18–24-year-olds in a cross-sectional study conducted in South Africa. Contraception 2013;87:782–789 [DOI] [PubMed] [Google Scholar]
- 24.Parker L, Pettifor A, Maman S, Sibeko J, MacPhail C. Concerns about partner infidelity are a barrier to adoption of HIV-prevention strategies among young South African couples. Cult Health Sex 2014;16:792–805 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Harrington EK, Dworkin S, Withers M, Onono M, Kwena Z, Newmann SJ. Gendered power dynamics and women's negotiation of family planning in a high HIV prevalence setting: A qualitative study of couples in western Kenya. Cult Health Sex 2016;18:453–469 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.MacPhail C, Terris-Prestholt F, Kumaranayake L, Ngoako P, Watts C, Rees H. Managing men: Women's dilemmas about overt and covert use of barrier methods for HIV prevention. Cult Health Sex 2009;11:485–497 [DOI] [PubMed] [Google Scholar]
- 27.Morroni C, Myer L, Mlobeli R, Gutin S, Grimsrud A. Dual protection among South African women and men: Perspectives from HIV care, family planning and sexually transmitted infection services 2007. Available at: http://pdf.usaid.gov/pdf_docs/PNADT165.pdf Accessed September2, 2016
- 28.UNFPA. Recommendations on Integration of Reproductive Health & HIV/AIDS 2004. Available at: www.appg-popdevrh.org.uk/Publications/Linking SexRH and HIVAIDS Hearings/Presentations/PDF/1 UNFPA Hearings Briefing.pdf Accessed September2, 2016
- 29.Yam EA, Mnisi Z, Mabuza X, et al. Use of dual protection among female sex workers in Swaziland. Int Perspect Sex Reprod Health 2013;39:69–78 [DOI] [PubMed] [Google Scholar]
- 30.MacPhail C, Pettifor A, Pascoe S, Rees H. Predictors of dual method use for pregnancy and HIV prevention among adolescent South African women. Contraception 2007;75:383–389 [DOI] [PubMed] [Google Scholar]
- 31.Chibwesha CJ, Li MS, Matoba CK, et al. Modern contraceptive and dual method use among HIV-infected women in Lusaka, Zambia. Infect Dis Obstet Gynecol 2011;2011:261453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Lawani LO, Onyebuchi AK, Iyoke CA. Dual method use for protection of pregnancy and disease prevention among HIV-infected women in South East Nigeria. BMC Women's Health 2014;14:39. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Fladseth K, Gafos M, Newell ML, McGrath N. The impact of gender norms on condom use among HIV-positive adults in KwaZulu-Natal, South Africa. PLoS One 2015;10:e0122671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Wall KM, Vwalika B, Haddad L, et al. Impact of long-term contraceptive promotion on incident pregnancy: A randomized controlled trial among HIV-positive couples in Lusaka, Zambia. J Acquir Immune Defic Syndr (1999) 2013;63:86–95 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Marlow HM, Maman S, Moodley D, Curtis S, McNaughton Reyes L. HIV status and postpartum contraceptive use in an antenatal population in Durban, South Africa. Contraception 2015;91:39–43 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Maughan-Brown B, Godlonton S, Thornton R, Venkataramani AS. What do people actually learn from public health campaigns? Incorrect inferences about male circumcision and female HIV infection risk among men and women in Malawi. AIDS Behav 2015;19:1170–1177 [DOI] [PubMed] [Google Scholar]
- 37.Layer EH, Beckham SW, Mgeni L, Shembilu C, Momburi RB, Kennedy CE. “After my husband's circumcision, I know that I am safe from diseases”: Women's attitudes and risk perceptions towards male circumcision in Iringa, Tanzania. PLoS One 2013;8:e74391. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Agot KE, Kiarie JN, Nguyen HQ, Odhiambo JO, Onyango TM, Weiss NS. Male circumcision in Siaya and Bondo Districts, Kenya: Prospective cohort study to assess behavioral disinhibition following circumcision. J Acquir Immune Defic Syndr (1999) 2007;44:66–70 [DOI] [PubMed] [Google Scholar]
- 39.Kibira SP, Nansubuga E, Tumwesigye NM, Atuyambe LM, Makumbi F. Differences in risky sexual behaviors and HIV prevalence of circumcised and uncircumcised men in Uganda: Evidence from a 2011 cross-sectional national survey. Reprod Health 2014;11:25. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Kibira SP, Sandoy IF, Daniel M, Atuyambe LM, Makumbi FE. A comparison of sexual risk behaviours and HIV seroprevalence among circumcised and uncircumcised men before and after implementation of the safe male circumcision programme in Uganda. BMC Public Health 2016;16:7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Ciaranello AL, Matthews LT. Safer conception strategies for HIV-serodiscordant couples: How safe is safe enough? J Infect Dis 2015;212:1525–1528 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Khu NH, Vwalika B, Karita E, et al. Fertility goal-based counseling increases contraceptive implant and IUD use in HIV-discordant couples in Rwanda and Zambia. Contraception 2013;88:74–82 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Wall KM, Kilembe W, Vwalika B, et al. Sustained effect of couples' HIV counselling and testing on risk reduction among Zambian HIV serodiscordant couples. Sex Transm Infect 2017;93:259–266 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Stephenson R, Vwalika B, Greenberg L, et al. A randomized controlled trial to promote long-term contraceptive use among HIV-serodiscordant and concordant positive couples in Zambia. J Women's Health (Larchmt) 2011;20:567–574 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Kraft JM, Galavotti C, Carter M, et al. Use of dual protection in Botswana. Stud Fam Plann 2009;40:319–328 [DOI] [PubMed] [Google Scholar]
- 46.Antelman G, Medley A, Mbatia R, et al. Pregnancy desire and dual method contraceptive use among people living with HIV attending clinical care in Kenya, Namibia and Tanzania. J Fam Plann Reprod Health Care 2015;41:e1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Hageman KM, Karita E, Kayitenkore K, et al. What the better half is thinking: A comparison of men's and women's responses and agreement between spouses regarding reported sexual and reproductive behaviors in Rwanda. Psychol Res Behav Manage 2009;2:47–58 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.O'Reilly KR, Kennedy CE, Fonner VA, Sweat MD. Family planning counseling for women living with HIV: A systematic review of the evidence of effectiveness on contraceptive uptake and pregnancy incidence, 1990 to 2011. BMC Public Health 2013;13:935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.World Health Organization. Exploring common ground: Building a better understanding and a closer alliance between family planning and STI/HIV prevention activities. 1999. https://core.ac.uk/download/pdf/23798004.pdf Accessed September8, 2016
- 50.UNAIDS. Treatment 2015. 2012. Available at: www.unaids.org/sites/default/files/media_asset/JC2484_treatment-2015_en_1.pdf Accessed April20, 2016
- 51.Scott CA, Iyer HS, McCoy K, et al. Retention in care, resource utilization, and costs for adults receiving antiretroviral therapy in Zambia: A retrospective cohort study. BMC Public Health 2014;14:296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Czaicki NL, Holmes CB, Sikazwe I, et al. Nonadherence to antiretroviral therapy among HIV-infected patients in Zambia is concentrated among a minority of patients and is highly variable across clinics. AIDS 2017;31:689–696 [DOI] [PubMed] [Google Scholar]