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DOI 10.1007/s10508-016-0818-z
ORIGINAL PAPER
Abstract Data suggest that pregnant women in some settings some high-risk sexual behaviors but increased the risk of sex
have high prevalence of HIV and other sexually transmitted without a condom.
infections (STI). We examined changes in sexual risk behaviors
and intravaginal practices during pregnancy that may contribute Keywords Sexual risk behaviors Pregnancy
to HIV and STI incidence using data from the Methods for Intravaginal practices
Improved Reproductive Health in Africa study conducted in
South Africa and Zimbabwe 20032006. We used a crossover
design and modified Poisson regression to compare behaviors Introduction
among HIV negative women 1845 years during pregnant and
non-pregnant periods. Among the 4802 women\45 years at Epidemiologic data suggest that pregnant women, particularly
enrollment, 483 (10.1 %) had a pregnancy and were included young pregnant women and those in resource-limited settings,
in the analysis. Compared to non-pregnant periods, pregnancy have high prevalence of sexually transmitted infections (STI),
was associated with fewer than 3 sex acts per week (adjusted risk including HIV (Berggren & Patchen, 2011; Chico et al., 2012;
ratio [ARR] 0.89; 95 % CI 0.790.99) but more sex acts without Kurewa et al., 2010; Moodley et al., 2015). STIs cause consid-
condoms (ARR 1.32; 95 % CI 1.151.51). Pregnancy was also erable morbidity in women, with infections potentially leading
associated with decreased reporting of other sexual risk behav- to infertility and other adverse health outcomes, including mor-
iors including any anal sex, multiple sexual partners, and/or tality in the case of HIV (Mullick, Watson-Jones, Beksinska, &
sex in exchange for drugs or money. Women also reported less Mabey, 2005; Paavonen & Eggert-Kruse, 1999). STIs can also
intravaginal wiping during pregnancy (ARR 0.84; 95 % CI cause complications during pregnancy includingpreterm deliv-
0.760.93). We found pregnancy decreased sexual activity and ery and premature rupture of membranes which can be life
threatening for both pregnant women and infants (Mullick et al.,
2005).In addition, certain infectionscan be transmittedto infants
causing congenital defects such as blindness and developmental
& Chloe A. Teasdale disabilities,andsomeinfectionscanbefatal(James& Kimberlin,
ct116@columbia.edu
2015; Mullick et al., 2005).
1
International Center for AIDS Care and Treatment Programs Sexual risk behaviors have been studied in order to identify
(ICAP), Mailman School of Public Health, Columbia which are most strongly associated with STI incidence and
University, 722 W 168th Street, Room 1319, New York, prevalence in women. Sexual risk behaviors found to be asso-
NY 10032, USA
ciated with STI transmission include sex without a condom
2
Department of Epidemiology, Mailman School of Public (unprotected sex), frequency of sex, concurrent sexual part-
Health, Columbia University, New York, NY, USA
nerships, number of lifetime sex partners, transactional orex-
3
Public Health Solutions, New York, NY, USA changesex (for shelter, money, or drugs), and unprotected anal
4
Ibis Reproductive Health, Cambridge, MA, USA sex (Chersich & Rees, 2008; Kaestle, Halpern, Miller, & Ford,
5
Department of Epidemiology, Hunter College, City University 2005; Mylonas, 2012; Op de Coul et al., 2011; Shain et al., 1999).
of New York School of Public Health, New York, NY, USA These data are important for understanding STI acquisition in
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Arch Sex Behav
women; however, there have been few examinations of whether intravaginal practices more often when they have transac-
sexual risk behaviors change during pregnancy, particularly in tional sex (Lees et al., 2014) which could increase STI risk if
low resource settings where STI prevalence is high. transactional sex partners are more likely to be infected with
Existing studies on sexual behaviors of pregnant women STIs or if transactional sex involves more risky behaviors.
have found that coital frequency tendsto decline over the course There are few studies describing intravaginal practices among
of pregnancy with the least amount of intercourse reported in pregnant women. In a cross-sectional study of pregnant women in
the third trimester generally (Bartellas, Crane, Daley, Bennett, Cote dIvoire, 97 % reported douching before antenatal medical
& Hutchens, 2000; Pauleta, Pereira, & Graca, 2010; Senkum- visits and 98 % reported douching as a common practice (La
wong, Chaovisitsaree, Rugpao, Chandrawongse, & Yanunto, Ruche et al., 1999). Data on other types of intravaginal practices
2006). Data from a cross-sectional survey of women in Malawi have not been reported among pregnant women. Given the lim-
found that pregnant women reported less sex than non-pregnant ited data on intravaginal practices during pregnancy and their
women and a decline in frequency of intercourse over the course potential as a risk factor for STI acquisition, it is critical to
of the pregnancy (Keating et al., 2012). A study from South describe the frequency of these behaviors among pregnant
Africa showed relatively high rates of sexual activity in late women and to document how intravaginal practices change
pregnancy but less frequent sex in the postpartum period. In during pregnancy.
the South African study, 67 % of women 2430 weeks gestation We conducted a secondary analysis of data from a randomized
reported sexual activity in the previous week, whereas only 49 % clinical trial to measure the association between pregnancy status
reported recent sexual activity at 3 months postpartum (Villar- and self-reported sexual behaviors and intravaginal practices
Loubet et al., 2013). among women with documented pregnancies during follow-up.
Available data are inconsistent with regard to how pregnancy
impacts sexual risk behaviors known to be associated with STI
acquisition. Sex without a condom was more frequently repor- Method
ted by pregnant women compared to non-pregnant women in
several studies (Gray et al., 2005; Morrison et al., 2007; Mugo Participants
et al., 2011; Reid et al., 2010); however, other risk behaviors
associated with STI transmission appear less common among We examined the association between pregnancy and sexual
pregnant women including concurrent sexual partnerships and risk behaviors and vaginal practices using a crossover design
transactional sex (Gray et al., 2005; Morrison et al., 2007; Reid comparing self-reported data by the same group of women prior
et al., 2010). There are few data on the sexual risk behaviors of to and during pregnancy. The data come from the Methods for
male partners of pregnant women which is also a critical fac- Improved Reproductive Health in Africa (MIRA) study, an
tor in womens STI acquisition. Pregnant women in Malawi open-label randomized controlled trial of the diaphragm and
reported greater fear of male partner infidelity compared to lubricant gel for prevention of HIV infection in women which
non-pregnant women (Keating et al., 2012). However, in studies has been previously described (Padian et al., 2007). The MIRA
with data collected from male partners, men in South Africa and trial was approved by institutional review boards in the U.S.,
Uganda were not more likely to report additional sex partners South Africa, and Zimbabwe (ClinicalTrials.gov: NCT00121
when their female partners were pregnant (Gray et al., 2005; 459), and the current analysis was exempt from additional ethics
Villar-Loubet et al., 2013). review as a secondary analysis of de-identified data.
Inadditiontosexualriskbehaviors,intravaginalpracticeshave During MIRA study follow-up, which ranged from 12 to 24
been identified as a potentially important mechanism for STI months, participants attended quarterly visits and received rou-
acquisition. Intravaginal practices include a broad array of tine STI and HIV testing, and risk reduction counseling includ-
behaviors such as douching or cleaning the vagina which may ing unlimited condoms. At each visit, participants reported sex-
be done for hygienic reasons or for pregnancy prevention, as ual activity, contraceptive and condom use, and intravaginal
well as practices aimed at altering the vagina, such as inserting practices in the previous 3 months through clinician-adminis-
absorbent materials to tighten or dry the vagina (Lees et al., tered interviews and audio computer-assisted self-interview-
2014; Myer, Kuhn, Stein, Wright, & Denny, 2005). Intravagi- ing (ACASI). Women who became pregnant during follow-up
nal practices have been studied as a potential causal factor in continued in the study during and after pregnancy.
womens STI risk, most notably HIV (Joesoef et al., 1996; Lees Pregnancy status was assessed at all quarterly study visits
et al., 2014; Low et al., 2011; Myer et al., 2005; Scholes et al., through laboratory (urine) pregnancy testing. Knowledge of
1998). It is not fully understood how intravaginal practices pregnancy was assessed at each quarterly follow-up visit through
increase STI risk; it may be through abrasions to vaginal tissue a clinical questionnaire which included asking women whether
or through alteration of the vaginal pH level which causes bac- they had been pregnant at any time prior to the visit and on what
terial vaginosis (Low et al., 2011; Rottingen, Cameron, & Gar- date they knew of the pregnancy. Women who became pregnant
nett, 2001). Some studies have shown that women engage in reported the date when they first knew of the pregnancy and
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resolution of pregnancies, including deliveries, miscarriages, included frequency of vaginal sex acts per week with/without
and terminations. To examine whether sexual risk behaviors a condom, number of vaginal sex partners, transactional sex,
and vaginal practices changed in response to pregnancy, only and any anal intercourse. In addition to examining the individual
follow-up time after the date a woman knew of a pregnancy measures, a dichotomoushigh-risk sexvariable was created
was considered as pregnant follow-up time for the analysis. indicating any report of the following: vaginal sex without a con-
For the analysis, a woman was considered pregnant in the inter- dom, exchange sex, anal sex (with or without condoms), two or
val preceding a visit if she had a positive urine pregnancy test at more sex partners, and having had a new sex partner. Women
the visit and had knowledge of the pregnancy prior to the visit. also reported on male sexual partner behaviors at enrollment,
In addition, women were also considered pregnant at a visit if it including HIV-positive status, partners away from home for
occurred within 6 weeks of a reported birth as women were preg- more than month, suspecting or knowing a partner had other
nant for the majority of that visit interval. sex partners, and use of alcohol or drugs before sex. A variable
Visit intervals with women who had negative pregnancy tests was created indicating male partners who werehigh riskat
were considered non-pregnant, including those with reports of enrollment using these variables. At follow-up visits, women
miscarriages and terminations since the last visit. Visit intervals reported whether they knew or suspected male partners of having
were also considered non-pregnant for women who had posi- other partners and abuse by partners.
tive pregnancy tests but no knowledge of the pregnancy. Visits Self-reported data on intravaginal practices were also col-
that occurred more than 6 weeks after a reported delivery were lected at all quarterly follow-up visits and were classified into
excluded from the analysis as data suggest that sexual behav- three categories: intravaginal washing (inside the vagina),wip-
iorsmaychangeinthepostpartumperiod(DeSchachtetal.,2014). ing, or insertion of products not related to menstruation. Fre-
Visits that occurred during a pregnancy were further classified quency of the three types of intravaginal practices was assessed
according to the estimated gestational age of the fetus at the visit using categories for reported daily, weekly, monthly, or none,
based on the first date women reported knowing of a pregnancy, and a summary variable was created indicating any of the three
first positive pregnancy test, or the delivery date (last menstrual intravaginal practices.
period date was not available). Given that we did not have precise
gestational age measuresandthatpreviousstudieshavesuggested Statistical Analysis
that sexual behaviors change in the third trimester (Bartellas et al.,
2000; Pauletaet al., 2010), gestational age was estimated in weeks Descriptive statistics (chi-squared tests for categorical variables
and then visits were grouped by trimester with visits in the first and Wilcoxon tests for continuous variables) were used to com-
28 weeks of pregnancy considered to be first/second trimester pare demographic characteristics and frequency of reported sex-
and visits after 28 weeks and up to 6 weeks postpartum as third ual behaviors and intravaginal practices at enrollment comparing
trimester. women included in the analysis who had pregnancies to women
We restricted the analysis to women 1845 years of age who who did not have a pregnancy during follow-up. Next, the fre-
had at least one visit with a laboratory positive pregnancy test with quency of sexual behaviors and intravaginal practices reported at
prior knowledge of the pregnancy and then examined non-preg- study visits prior to and during pregnancies among women
nant visits prior to the pregnancy and visits during pregnancy. To included in the analysis was examined. To compare the fre-
be included, women had to have at least one non-pregnant visit at quency of reported sexual risk behaviors and intravaginal prac-
most 6 months prior to the first pregnant visit. Only scheduled tices, logistic regression models fitted with generalized estimat-
quarterly follow-up visits with both pregnancy testing and self- ing equations (GEE) with an exchangeable correlation matrix
reported behavior data were examined. Visits after HIV diagnosis were used to estimate robust standard errors (for continuous vari-
for women who seroconverted and visits more than 6 months ables, linear regression with GEE was used). The same analysis
apart were excluded (follow-up time was truncated at the last was conducted to examine the association between sexual behav-
visit before a 6-month gap) in order to ensure comparisons iors and intravaginal practices according to gestational age. A
between pregnant and non-pregnant visits were in close prox- further analysis measured change across two visits for each
imity. For women with two pregnancies during follow-up, only woman, the visit just prior to the pregnancy, and the first visit
visits prior to and during the first pregnancy were included. during the pregnancy, using McNemars test for paired cate-
gorical data. Finally, modified Poisson regression models (to
Measures correct variance estimates for repeated measures per partic-
ipant) were fitted to estimate the risk ratio of sexual risk behav-
Sexual Risk Behaviors and Intravaginal Practices iors and intravaginal practices at pregnant and non-pregnant
visits (Zou, 2004). Multivariable models were adjusted for age,
Women were asked via ACASI about their sexual behavior in the study randomization arm, and location. All statistical proce-
previous 3 months at enrollment and quarterly visits. Reports dures were conducted using SAS 9.3 (SAS Institute, Cary, NC).
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Table 1 continued
Characteristics at enrollment Total Women with no pregnancies Women in analysis p value
N % N % N %
Table 2 Risk behaviors reported at 2540 follow-up visits and association with pregnancy status, N = 483 women (unadjusted odds ratios)
Reported behaviors at follow-up Frequency of report Frequency of report Frequency of report Odds ratio pregnant versus
at all visits at non-pregnant at pregnant visits non-pregnant periods
visits
N % N % N % OR 95 % CI p value
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Fig. 1 Risk behaviors reported at two follow-up visits for each woman: last non-pregnant and first pregnant visit, N = 483
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Table 3 Association between pregnancy status and reported risk behaviors and intravaginal practices at follow-up visits, N = 483 women, 2540 visits
(modified Poisson risk regression)
Risk behavior Univariable Adjusted
RR 95 % CI p value RR 95 % CI p value
Any vaginal sex since last visit 0.80 0.641.00 0.05 0.84 0.671.05 .12
Vaginal sex C3 times per week 0.88 0.800.99 0.03 0.89 0.790.99 .04
Condom use (male or female) at last sex 0.85 0.750.96 0.01 0.82 0.720.93 \.01
Unprotected sex (any report) 1.30 1.141.49 \0.01 1.32 1.151.51 \.001
Anal sex since last visit 0.68 0.510.90 0.01 0.67 0.510.89 .01
Sex in exchange for money or drugs 0.84 0.611.17 0.30 0.83 0.601.15 .27
C2 male sex partners since last visit 0.55 0.390.77 \0.01 0.47 0.320.69 \.01
New sex partner 0.84 0.691.02 0.07 0.81 0.670.98 .03
Suspects/knows male partner concurrency 0.92 0.801.06 0.21 0.89 0.781.02 .10
High-risk sexa 0.75 0.640.88 \0.01 0.74 0.630.86 \.01
Intravaginal washing
Daily 0.94 0.81.1 0.29 0.94 0.841.06 .32
Weekly 0.92 0.81.1 0.36 0.91 0.751.10 .33
Monthly or less 0.73 0.60.9 0.01 0.74 0.580.94 \.01
None (ref) 1.00 1.00
Any 0.92 0.81.0 0.14 0.92 0.821.03 .15
Intravaginal wiping
Daily 0.85 0.80.9 \0.01 0.85 0.760.95 .01
Weekly 0.76 0.61.0 0.04 0.76 0.590.99 .04
Monthly or less 0.80 0.61.1 0.13 0.81 0.611.07 .14
None (ref) 1.00 1.00
Any 0.92 0.80.9 \0.01 0.84 0.760.93 \.01
Intravaginal insertion (non-menstruation related)
Daily 0.93 0.81.2 0.52 0.93 0.751.15 .49
Weekly 0.87 0.51.4 0.57 0.87 0.541.40 .57
Monthly or less 0.79 0.61.1 0.12 0.78 0.581.06 .12
None (ref) 1.00 1.00
Any 0.87 0.71.0 0.12 0.87 0.731.04 0.11
a
High-risk sex: (any of the following) C2 partners, exchange sex, anal sex, and use of alcohol and/or drugs before sex
sexual partner in the past 3 months (Table 2). Overall, during preg- Comparingsexual riskbehaviorsreportedbywomenatthelast
nancy, women were less likely to report high-risk sex (OR = 0.59, non-pregnant visit and the first pregnant visit, 15.7 % of women
95 % CI [0.47, 0.72]) and were significantly less likely to report who reported sex without a condom at the pregnant visit had not
intravaginalwashing,wiping,orinsertionofproducts;oddsofdaily reportedsexwithoutacondomattheprecedingnon-pregnantvisit
intravaginal wiping during pregnancy were 30 % lower (OR = (p\.05, Fig. 1). A significant proportion of women also changed
0.66, 95 % CI [0.590.75]) compared to non-pregnant periods. from reporting some high-risk sex prior to pregnancy, but none
Of the 904 pregnant visits included in the analysis, 492 (54.4 %) once they were pregnant (p\.01). Women also appeared to
were estimated to have occurred during the first/second trimester decrease intravaginal wiping (p = .05) once they were preg-
and 412 (45.6 %) occurred during the third trimester (data not nant with a significant proportion changing from reporting this
shown). Compared to visits earlier in pregnancy, during the third behavior prior to pregnancy but not reporting it at the first preg-
trimester women reported less sex between visits, OR 0.39, 95 % nant visit.
CI[0.220.72],andfewerreportedthree ormore sexactsperweek, In multivariable Poisson models, pregnancy was associated with
OR = 0.59, 95 % CI [0.47, 0.73]. During the third trimester, less frequent sex, adjusted risk ratio (ARR) sex C3 times per week
women were more likely to report sex without a condom com- 0.89, 95 % CI [0.790.99], less reported condom use at last sex,
paredto visitsearlierinpregnancy. Nodifferenceswereobserved ARR = 0.82, 95 % CI [0.72, 0.93], and more reported unprotected
in sexual risk behaviors between early and late pregnancy, nor for sex,ARR = 1.32,95 %CI[1.15,1.51](Table 3).Overallpregnancy
intravaginal practices. was also associated with less high-risk sex, ARR = 0.74, 95 % CI
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