Zika virus prevention behaviors and knowledge among male partners of pregnant people, a cross-sectional analysis from the Zika en Embarazadas y Niños (ZEN) prospective cohort study, Colombia

doi:10.21203/rs.3.rs-3395311/v1

Background: Zika virus (ZIKV) infection in pregnancy can cause brain and eye abnormalities and neurodevelopmental sequelae. In the absence of medical countermeasures, behavioral interventions were recommended to prevent mosquito bites and sexual transmission of ZIKV.

Methods: We used self-reported data from the Zika en Embarazadas y Niños (ZEN) prospective cohort study in Colombia to describe the knowledge, attitudes, and behaviors related to ZIKV prevention in male partners compared to those of their pregnant partners at study enrollment during February 2017 – February 2018.

Results: Most male partners reported wearing protective clothing such as long pants (97.6%) and long sleeves (72.8%), as well as covering ankles and feet (89.1%) to prevent ZIKV infection. When comparing the preventive behavior of condom use between male and pregnant partners, 26 pairs (10.0%) both responded that they performed the behavior. Overall, 25.1% of male partners and 18.9% of pregnant people reported any condom use during the three months before enrolling in ZEN. When comparing other preventive behaviors between male and pregnant partners, the behavior which was most frequently reported by both partners was wearing long pants (85.4%), and the least frequently reported by both partners was using condoms after finding out about a partner’s pregnancy (3.4%).

Conclusions: These findings provide new information on the behaviors used by male partners to prevent ZIKV infection during the outbreak in Colombia and can be used to inform future ZIKV and other arbovirus prevention strategies that include both pregnant people and their partners.

Zika virus

knowledge

attitudes

behaviors

Colombia

pregnancy

prevention

The consequences of Zika virus (ZIKV) infection during pregnancy can be severe, including congenital Zika syndrome and possible neurodevelopmental abnormalities, especially if the infection occurs in early pregnancy (1-2). ZIKV transmission primarily occurs through the bite of an infected mosquito, in utero from mother to fetus, or through sexual transmission.

The Zika virus (ZIKV) outbreak in early 2015 in Brazil prompted Colombia to begin monitoring for Zika virus disease (ZVD) in August 2015, and the first outbreak was identified in Colombia in October 2015 (3,4). By April 2016, about 66 000 cases of ZVD were reported in Colombia, including just under 12 000 cases in pregnant people (3). By the end of July 2016, the estimated number of pregnant people affected by ZVD had grown to just over 18 000, as reported to Colombia’s national surveillance system (5). During the height of the epidemic, the prevalence of brain or eye defects in infants or fetuses was 13 per 10 000; prior to the epidemic and after the epidemic, the prevalence of brain or eye defects in Colombia was 8 and 11 per 10 000, respectively (5). Although the end of the Zika epidemic was declared in late July 2016 (6), monitoring for adverse pregnancy and infant outcomes continued.

The World Health Organization (WHO) recommends several methods for reducing the mosquito population and taking personal protection measures against mosquito bites, including application of repellents containing DEET to exposed skin and clothing, wearing protective clothing such as long-sleeved shirts and pants, using screens on windows and doors, using air conditioning, and using insecticidal-treated mosquito nets when sleeping (7). To prevent sexual transmission, the Colombian Ministry of Health and Social Protection recommended that couples or women of childbearing age delay pregnancy until the end of the ZIKV outbreak (8).

Previous studies have reported the knowledge, attitudes, and behaviors (KAB) of pregnant people towards the use of these behaviors to prevent ZIKV infection, but few studies have assessed these KAB among male partners of pregnant people in areas of active ZIKV transmission (9,10). However, several studies suggest that people, including pregnant people, were unaware that ZIKV could be sexually transmitted (11,12), leading to mixed perception of condom use during sex in both men and women, particularly around why it was necessary to use a condom when a person was already pregnant, and overcoming perceptions that condom use is an indicator of infidelity (10,13). Furthermore, ZIKV prevention messaging focused almost exclusively on mosquito bites or vector control instead of all modes of transmission (10,11).

This report describes the KAB around the prevention of ZIKV transmission among the male partners of pregnant people in an area where ZIKV was circulating. Because male partners infected with ZIKV can transmit the virus to their pregnant partners through sex, and because one partner’s attitudes toward prevention behaviors can shape the other partner’s actions, understanding male partners’ KAB can inform strategies to prevent ZIKV infection.

In 2017, Colombia’s Instituto Nacional de Salud (INS) and the U.S. Centers for Disease Control and Prevention (CDC) launched a prospective pregnancy cohort study Zika en Embarazadas y Niños (ZEN) in three departments of Colombia with high numbers of ZIKV cases reported during the ZIKV outbreak (Atlántico, Santander, and Valle de Cauca). One of the objectives of this study was to understand ZIKV prevention behaviors used by pregnant people in these areas. Unique to this cohort, male partners were also enrolled.

Pregnant people in their first trimester were recruited from 13 public and private prenatal clinics based on study inclusion criteria (14). At their study enrollment visit, pregnant people were asked if a male partner lived with them and, if so, whether study staff could contact him. Male partners were included if they were 18 years or older, if their pregnant partner was 18 years or older, spoke Spanish, lived in the same household as their pregnant partner who was enrolled in the study, and the pregnant partner agreed that their male partner could be asked to participate in the study (14). Pregnant people and male partners were excluded if they were incarcerated, unable or unwilling to consent to participate in study activities, or if they were physically or psychologically unable to participate, based on the judgment of clinical or study staff (14). Male partners were enrolled between February 2017 and February 2018 and visited the prenatal clinics to complete an interviewer-administered enrollment questionnaire. Questions included behaviors to prevent ZIKV infection performed in the past seven days: wearing long pants, wearing long sleeves, covering ankles and feet, using mosquito repellent; using condoms during sex, and if the frequency of condom use changed after finding out their partner was pregnant. Further details on the ZEN cohort methods and objectives are described elsewhere (14).

Analyses were conducted in SAS 9.4 (Cary, NC). With the exception of change in condom use, variables with more than two response options were dichotomized; for example, if responses could be ‘always’, ‘sometimes’, ‘never’, or ‘don’t know’, ‘always’ and ‘sometimes’ were grouped and ‘never’ and ‘don’t know’ were grouped. For the question about change in condom use after finding out a partner was pregnant, response options were dichotomized as ‘any change in condom use’ (where condom use was reported more often or where condom use was reported less often) and ‘no change in condom use’ (where no change in condom use, do not use condoms, or don’t know were reported). A sensitivity analysis was performed with ‘always’ and ‘sometimes’ grouped, and ‘never’ alone, excluding ‘don’t know’. Frequencies, number and percent where both the male and pregnant partner reported engaging in a behavior, and simple Kappa coefficients that account for agreement among male and pregnant partners, excluding agreement by chance, were used to describe KAB among male partners and pregnant people enrolled in ZEN. Kappa coefficients were considered as: poor agreement (≤ 0.4), moderate agreement (0.41 – 0.75), and good agreement (> 0.75). A negative Kappa coefficient was considered as a response disagreement.

Enrollment of pregnant people occurred between three and 16 weeks of gestation, with the median enrolled at 9 weeks (interquartile range: 7, 12 weeks). Of the 1 519 pregnant people enrolled in ZEN, 1 399 met the study criteria for having a male partner included in the study, and 779 gave permission to contact their male partner (14). Among the 656 male partners that were reachable and screened for participation, 33 did not meet inclusion criteria, and 336 were eligible but declined to participate (14).

Data from 287 pregnant people and their male partners enrolled in ZEN were used in this analysis. Of 287 male partners that participated, 56.1% were 28 years or older, 35.5% completed technical school or university, 67.6% had public or private health insurance compared to none or unknown insurance status, 98.3% were married or in a free union, and 79.1% had low socioeconomic status (SES) as defined by the Colombian government (15). SES strata are based on residences that should receive public services, and those of higher SES strata pay more for public services and help to subsidize those of lower strata (15).

A higher proportion of males responded that someone in their community could be infected with ZIKV (75.4% vs. 67.6%), and when asked about the likelihood of a baby having intrauterine growth restriction (IUGR) if the pregnant person has ZIKV (81.8% vs. 73.7%) compared to their pregnant partners. Males and pregnant partners responded similarly in that they were very or somewhat worried about contracting ZIKV (84.4% vs. 89.9%), that it was very or somewhat likely that a baby could be born with microcephaly if the pregnant person has ZIKV (87.6% vs. 86.6%), that it was very or somewhat likely a baby could be born with other congenital anomalies if the pregnant person has ZIKV (87.2% vs. 83.0%), and that it was very or somewhat likely that a pregnant person with ZIKV could have a pregnancy loss or stillbirth (78.23% vs. 80.4%) (Table).

Where both male and pregnant partners responded ‘yes’ or that it was ‘very or somewhat likely’ to the same knowledge or attitude question, the percentage was highest for being somewhat or very worried about contracting ZIKV (76.1%) and lowest for whether someone in the community could have ZIKV (50.7%) (Table). All Kappa coefficients fell in the poor agreement to disagreement categories, with the highest Kappa coefficient at 0.0388 for the question about the likelihood of pregnancy loss or stillbirth if the pregnant person has ZIKV.

Male partners were more likely than pregnant people to report engaging in Zika preventive behaviors in the last seven days, including wearing long pants (97.6% vs. 87.8%) and long sleeves that cover their arms (72.8% vs. 65.2%), to report covering their feet and ankles (89.1% vs. 58.3%), and using mosquito repellent (18.7% vs. 17.6%) (Table). In the three months prior to enrolling in ZEN, 25.1% of male partners reported condom use during sex, whereas 18.9% of pregnant people reported that their male partner used a condom. Of the male partners with reported condom use in the three months prior to enrolling in ZEN (25.1%), 82.6% answered the question around the frequency of use after finding out about their partner’s pregnancy and 3.4% (8/237) reported any change in frequency of condom use. Of the pregnant people who reported that their male partner used a condom after finding out about the pregnancy, 11.0% (26/237) said that there was a change in the frequency of condom use during sex.

The percentage of couples where both male partners and pregnant partners reported engaging in a behavior to prevent ZIKV (i.e., responding ‘always/sometimes’ or ‘more frequently’) was highest for wearing long pants that cover legs (85.4%) and lowest for change in condom use after finding out about a partner’s pregnancy (3.4%) (Table). Kappa coefficients ranged from disagreement to moderate agreement, with the highest Kappa coefficient at 0.5657 for not abstaining from vaginal sex in the three months prior to enrolling in the study and the lowest at -0.0474 for whether covering feet and ankles in the seven days to prevent mosquito bites prior to enrolling in ZEN.

The third lowest preventive behavior reported by males and pregnant partners was for condom use, where 10.0% of males and pregnant partners both responded ‘always/sometimes’ to using condoms in the three months prior to enrollment. (Table). Condom use after finding out a partner was pregnant changed in eight couples where each partner responded to this question (Table). While 74.9% of male partners reported no condom use, 18.6% of male partners reported condom use when pregnant partners indicated no condom use, and 11.9% of pregnant partners reported condom use when male partners did not indicate condom use (data not shown). The Kappa coefficient for using condoms was considered to have a poor agreement, at 0.3065.

Results were not meaningfully different in the sensitivity analysis where ‘don’t know’ was excluded from the Kappa coefficients (data not shown).

Despite Colombian Ministry of Health and Social Protection and WHO recommendations to prevent ZIKV in areas with high transmission rates, ZIKV prevention behaviors were inconsistent between pregnant people and their male partners in this cohort study. Cultural norms or routine practice may play a role in behaviors that prevent or facilitate ZIKV infection. For example, one study found that women may prefer to wear skirts, shorts, and short sleeves that are less protective against mosquito bites as opposed to long pants or long sleeves to keep cool during warmer parts of the day (16). Furthermore, use of mosquito repellent to prevent ZIKV infection was infrequently reported by both pregnant people and male partners. Other qualitative studies in Colombia found that pregnant people considered Zika to be a concern, but were hesitant to purchase mosquito repellent due to the high cost and potential allergic reactions to chemicals found in repellents (16,17). In one of the same studies, male partners did not consider Zika to be major concern, and expressed similar concerns around using mosquito repellents (16).

Condom use was low among pregnant people and their male partners (10.0%) in this cohort study. Promoting condom use to prevent ZIKV transmission while considering gender norms and cultural context is a complex issue. In qualitative studies on gender and ZIKV prevention behaviors in Latin America and the Caribbean, women are perceived as the home’s caretakers while men are perceived as the breadwinners and protectors of their families (10,13). Condom use or abstinence in a relationship lead to suspicion of infidelity and lack of trust (10,13). Considering condom use as a prevention measure for ZIKV and other arboviruses from both men’s and women’s perspectives in culturally relevant ZIKV and arbovirus prevention messaging may help increase the frequency of ZIKV preventive behaviors. For example, messaging that emphasizes condom use as a means of protecting one’s family from ZIKV and its impacts could appeal to men and may help strategic communications campaigns and other public health prevention activities focusing on men.

Assessment of knowledge and attitudes about Zika were fairly consistent between pregnant people and their male partners, in that most responses where both the pregnant person and male partner responded positively (“Yes”, “Very/Somewhat”) were not significantly different than one another. Although there was no significant difference in how worried pregnant people and male partners were about contracting ZIKV, there was a significant difference in responses about whether someone in their community could get ZIKV and whether a baby could have IUGR if the pregnant person is infected with ZIKV. Contrarily, there was no significant difference in positive responses regarding the likelihood a baby could be born with microcephaly or congenital anomalies, or the likelihood of a pregnancy loss or stillbirth if a mother was infected with ZIKV during pregnancy. Other reports have shown similar findings, where attitudes about ZIKV and degree of knowledge about possible outcomes related to ZIKV infection during pregnancy differ by pregnant person and male partner (16,18).

This analysis is subject to several limitations. First, these data are self-reported, and participants received information about the consequences of ZIKV infection during the enrollment process, potentially introducing social desirability bias, with participants more likely to report preventive behaviors. Second, only 20.5% (287/1 399) of eligible male partners agreed to participate. There are observed differences in characteristics between pregnant people whose male partner enrolled in ZEN and those who did not enroll; those who enrolled had a higher level of education, were more likely to have private insurance, and be married (14). Third, the condom use questions did not specifically ask about sex with the pregnant partner; some men reported having vaginal sex with more than one partner in the three months prior to enrolling in the study, meaning reported condom use may have been to prevent another sexually transmitted infection or to prevent pregnancy in a different partner and not necessarily to prevent ZIKV infection in the pregnant person. Additionally, condom use may have been low among males and their partners because they were actively trying to get pregnant, despite public health recommendations to delay pregnancy during the ZIKV epidemic. Fourth, as participants were asked about their condom use in the three months before enrolling in ZEN, the time of conception overlapped with the time period condom use was assessed in ~59% of pregnancies (data not shown). This study did not assess partner behaviors at follow-up visits in relation to reduced burden of ZIKV transmission. Because this cohort was enrolled when the ZIKV outbreak was already waning in Colombia, it is unclear whether the pattern and frequency of preventive behaviors were similar during the height of the outbreak. Finally, as there is no comparable comparison group, we cannot be certain whether male partners or pregnant people changed ZIKV prevention behaviors due to pregnancy.

These findings provide an understanding of the knowledge, attitudes, and preventive behaviors male partners had concerning ZIKV after the large outbreak in Colombia. Comparing responses to questions around condom use between male partners and pregnant people can provide information for public health practitioners about the extent of condom use as a ZIKV prevention behavior in the population. It may be feasible to use pregnant people’s responses as a proxy for their male partners given that responses to behavior-related questions were fairly consistent between male and pregnant partners and the challenges in recruiting male partners to participate fully in health-related studies. The results from this study can be used to inform future public health campaigns to expand knowledge about and methods to prevent sexual transmission of ZIKV. Culturally appropriate campaigns could focus on including the roles that both men and pregnant people have in preventing the sexual transmission of ZIKV.

CDC – U.S. Centers for Disease Control and Prevention

INS – Instituto Nacional de Salud (National Institute of Health)

IUGR – Intrauterine growth restriction

KAB – Knowledge, Attitudes, Behaviors

SES – Socioeconomic status

WHO – World Health Organization

ZEN – Zika en Embarazadas y Niños (Zika in Pregnant People and Children)

ZIKV – Zika virus

ZVD – Zika virus disease

Ethics Approval and Consent: The study was approved by the INS Ethics and Methods Committee and the CDC Institutional Review Board. All participants provided informed consent. Participation was voluntary, and they could opt out of study activities or withdraw at any time.

Consent for Publication: All authors have given consent to publish.

Availability of Data and Materials: The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request.

Competing Interests: The authors declare that they have no competing interests.

Funding: This work was supported by the Centers for Disease Control and Prevention (CDC), the Instituto Nacional de Salud, and the Office of Infectious Disease, Bureau for Global Health, U.S. Agency for International Development (USAID), under the terms of an Interagency Agreement with CDC. The work was implemented through Vysnova Partners, Inc., with contract numbers 200-2016-91589 and 200-2017-95780.

Author Contributions: CS analyzed and interpreted the data and wrote the first and subsequent drafts of the manuscript. AT performed the analytic replication. SA performed a literature search on background information to support development of the manuscript. SG, MG, DV, VT, and MO conceived the original study. AT, SA, VB, JC, SN, SG, MG, DV, VT, and MO edited the manuscript for content and accuracy. All authors read and approved the final manuscript.

Acknowledgements: The authors acknowledge the many project staff for their immense support and contributions to this project: INS staff; Colombia’s Ministry of Health and Social Protection; Secretaries of Health and all field staff in each of the study sites; CDC staff Margaret A Honein and Candice Y Johnson; and the study participants and their families.

CDC Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official positions of the CDC, USAID, or INS.

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Table. Comparison of ZIKV Knowledge, Attitudes, and Behaviors between Male Partners and their Pregnant Partners Enrolled in ZEN

	Male Partners n (%)	Pregnant Partners n (%)	Both Reported ‘Yes’, ‘Very/Somewhat’, or Performed a Behavior n (%)	Simple Kappa Coefficient (95% confidence interval)
Knowledge and Attitudes
Someone in community can be infected with Zika? (N=284)
Yes	214 (75.4)	192 (67.6)	144 (50.7)	-0.0116 (-0.1252, 0.1020)
No/Don’t Know	70 (24.7)	92 (32.4)
Level of worry about getting Zika (N=276)
Very/Somewhat Worried	233 (84.4)	248 (89.9)	210 (76.1)	0.0205 (-0.0997, 0.1407)
Not Worried/Don’t Know	43 (15.6)	28 (10.1)
Likelihood a baby is born with microcephaly if mother infected with Zika? (N=283)
Very/Somewhat Likely	248 (87.6)	245 (86.6)	214 (75.6)	-0.0220 (-0.1317, 0.0877)
Not Likely/Don’t Know	35 (12.4)	38 (13.4)
Likelihood a baby is born with other congenital anomalies if mother infected with Zika? (N=282)
Very/Somewhat Likely	246 (87.2)	234 (83.0)	205 (72.7)	0.0243 (-0.0960, 0.1446)
Not Likely/Don’t Know	36 (12.8)	48 (17.0)
Likelihood a baby has intrauterine growth restriction if mother infected with Zika? (N=285)
Very/Somewhat Likely	233 (81.8)	210 (73.7)	172 (60.4)	0.0063 (-0.1073, 0.1199)
Not Likely/Don’t Know	52 (18.3)	75 (26.3)
Likelihood of pregnancy loss/stillbirth if mother infected with Zika? (N=285)
Very/Somewhat Likely	223 (78.3)	229 (80.4)	181 (63.5)	0.0388 (-0.0813, 0.1590)
Not Likely/Don’t Know	62 (21.8)	56 (19.7)
Behaviors
Long pants covering legs^a (N=287)
Always/Sometimes	280 (97.6)	252 (87.8)	245 (85.4)	-0.0424 (-0.0693, -0.0155)
Never	7 (2.4)	35 (12.2)
Long sleeves covering arms^a (N=287)
Always/Sometimes	209 (72.8)	187 (65.2)	143 (49.8)	0.1104 (-0.0063, 0.2270)
Never	78 (27.2)	100 (34.8)
Feet and ankles covered^a (N=285)
Always/Sometimes	254 (89.1)	166 (58.3)	145 (50.9)	-0.0474 (-0.1267, 0.0318)
Never	31 (10.9)	119 (41.8)
Mosquito repellent^a (N=284)
Always/Sometimes	53 (18.7)	50 (17.6)	17 (6.0)	0.1819 (0.0475, 0.3163)
Never	231 (81.3)	234 (82.4)
Vaginal sex ^b (N=261)
Did not abstain	258 (98.9)	257 (98.5)	256 (98.1)	0.5657 (0.1237, 1.0000)
Abstained	3 (1.2)	4 (1.5)
Condom use^c (N=259)
Always/Sometimes	65 (25.1)	49 (18.9)	26 (10.0)	0.3065 (0.1731, 0.4399)
Never	194 (74.9)	210 (81.1)
Condom use changed after finding out partner was pregnant ^d (N=237)
Any change in frequency of condom use	40 (16.9)	26 (11.0)	8 (3.4)	0.1262 (-0.0227, 0.2751)
No change in frequency of condom use	197 (83.1)	211 (89.0)

^aResponses indicate whether the person performed the behavior in the seven days prior to enrollment.

^bResponses indicate whether the person abstained from vaginal sex in the three months prior to enrollment.

^cResponses indicate whether the person used a condom during sex in the three months prior to enrollment.

^dWhere respondents reported always or sometimes using a condom with their partner in the three months prior to enrollment.

No competing interests reported.

Zika virus prevention behaviors and knowledge among male partners of pregnant people, a cross-sectional analysis from the Zika en Embarazadas y Niños (ZEN) prospective cohort study, Colombia

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Abstract

Background

Methods

Results

Discussion

Conclusions

List of Abbreviations

Declarations

References

Table

Additional Declarations

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