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WHO guidelines for the prevention of sexual transmission of Zika virus [Internet]. Geneva: World Health Organization; 2020.

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WHO guidelines for the prevention of sexual transmission of Zika virus [Internet].

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Annex B2Evidence review, key question (2): Does consistent and correct condom use reduce transmission of Zika virus?

1. Background

Assuming correct usage and otherwise ideal circumstances, the efficacy of condoms as a barrier depends on their physical properties. The materials used to make condoms have different physical properties. Most male condoms are made from latex, which can be obtained from plants or produced synthetically (1, 2). Other materials used for male condoms are polyurethane (3) or membranes made from sheep intestines (4). The female condom is made out of polyurethane or nitrile (5). The diameter of the spherical Zika virus virions has been estimated by cryo-electron microscopy studies at 48 nm (6) and 50 nm (7). We applied a virion diameter of 48 nm. We refer to sheep intestine-based condoms as natural condoms and other condoms as non-natural condoms.

1.1. Assessment of condom properties

  • The International Organization for Standardization (ISO) defines the standards for the “freedom from holes” test, as well as physical properties of condoms – ISO 4074 for male latex condoms (8), ISO 23409 for synthetic male condoms (9), and ISO 25841 for female condoms (10) – manufacturing and testing (ISO 2859) (11). The WHO/United Nations Population Fund (UNFPA) procurement specifications for male latex condoms (12) and female condoms (13) are based on the ISO standards 4074 and 25841, respectively.
  • The mandatory freedom from holes test is either a water leak test where the condom is rolled and assessed for leakage, or a test where the flow of electric current through possible holes in condoms is assessed. For female condoms, only the water leak test is listed (10)H¿G . The ISO standards defines an acceptable quality level (AQL) of 0.25, meaning that the “great majority” of lots are accepted if at most 0.25% of condoms do not conform (11).

2. Systematic review methods

Table 1 shows our four questions about the efficacy and effectiveness of condoms to prevent sexual transmission of Zika virus. We anticipated the absence of direct evidence, so we searched for evidence about the properties of condoms to prevent leakage of particles of a given size, and the risk that leakage would pose. We combined this evidence to assess the hypothesis that condoms are an effective barrier method to prevent Zika virus infection. We used studies about HIV – diameter 145 nm (14) – to infer the effectiveness of condom use in the prevention of the sexual transmission of Zika virus, because the evidence base for condom effectiveness against HIV is larger than for condom effectiveness against other viruses.

Table 1Review questions for condom efficacy and effectiveness

Path of evidenceQuestion
Direct evidence1Does condom use reduce the sexual transmission of Zika virus, compared with non-use?
Indirect evidence2.1What are the physical properties of condoms to act as an effective barrier for viral particles?
2.2What is the minimal amount of leaked Zika virus necessary to cause an infection through sexual intercourse?
2.3What is the effectiveness of condoms to prevent the sexual transmission of other viral infections?

Table 1 shows the sources of information.

Table 2Overview of data sources for condom studies

Direct evidenceIndirect evidence
Question

1

Condom effectiveness against Zika virus

2.1

Physical properties of condoms

2.2

Minimal infectious dose of Zika virus

2.3

Condom effectiveness for other viral diseases

Search modesSystematic, Systematic handsearchForward backward, non-systematicSystematic, non-systematic, handsearchNon-systematic
Data sources systematicEmbase, Pubmed, LILACS, WHO, CDC, ECDC, PAHOPubmed, Embase
Data sources non-systematic(1, 3, 4, 15–22), Pubmed, Google, Google ScholarGoogle, Google Scholar, Health Canada, MedscapePubmed, Google, Google Scholar
Number of included studies01899

Abbreviations: Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS), World Health Organization (WHO), European Centre for Disease Prevention and Control (ECDC), Centers for Disease Control and Prevention (CDC), Pan American Health Organization (PAHO).

Risk of bias assessment

We assessed the quality of systematic reviews and reviews using risk of bias in systematic reviews (ROBIS) (23), and observational studies, with the quality appraisal checklist for quantitative studies reporting correlations and associations by NICE (24). For animal studies, we used the SYRCLE tool (25). For laboratory studies that assessed the physical properties of condoms, we informally appraised quality based on characteristics of the experiments. We could not find formal tools to assess the risk of bias in laboratory studies assessing the physical properties of condoms. We provide a narrative summary of the potential bias in these studies. We used GRADE (26) to assess the overall certainty of evidence for each outcome.

2.1. Direct evidence on the efficacy of condoms to prevent sexual transmission of Zika virus

We did not identify any direct evidence that assessed the condom effectiveness on the prevention of sexual transmission of Zika virus. None of 35 unique publications in Embase and PubMed met the eligibility criteria. None of 655 records on the websites of CDC, ECDC, PAHO and WHO met the eligibility criteria. See PRISMA flowchart in Fig. 1.

2.2. Indirect evidence, physical properties of condoms

  • We extracted data about condom leakage from 13 in vitro studies with condoms: 11 about male condoms published from 1984 to 1994, one about female condoms published in 1990 (28), and one about both male and female condoms in 2009 (5) (Fig. 2). We also included one in vitro study with latex and nitrile gloves (29), two reviews (30, 31), and one mathematical modelling study (32).
  • Leakage of condoms was tested using viral particles or proxies for viruses suspended in fluids. Five studies used the 27 nm bacteriophage φX174 for testing leakage (3, 5, 21, 22), five used HIV (140 nm) (19, 28, 33–35), four used herpes simplex virus (HSV1 and HSV2, 150–200 nm) (1, 35, 36). Single studies used cytomegalovirus (CMV, 150–200 nm), hepatitis B virus (HBV, 42 nm), polystyrene microspheres (PMS, 110 nm), poliovirus type 1 (PV1, 27 nm), the 100 nm bacteriophage T7 and a type of murine retrovirus with unknown size (xenophobic type C mouse retrovirus, XTCMR).
Fig. 1. PRISMA flowchart for direct evidence about the efficacy of condoms to prevent sexual transmission of Zika virus.

Fig. 1PRISMA flowchart for direct evidence about the efficacy of condoms to prevent sexual transmission of Zika virus

Source: adapted from (27).

The proportion of condoms that leaked varied between studies. In two of six studies that used particles smaller than Zika virus, none of the condoms leaked but sample sizes were small; poliovirus, 0/70 and 0/28 (37); and HBV, 0/15 (1). The largest study (n=546) found leakage in 3% (95% CI: 2–5) (3). Proportions of leaking condoms were highest in the study by Voeller et al., but condoms in this study were five years old (22).

Risk of bias assessment

We assessed a high risk of bias for lacking power size considerations (all included studies), manually performed experiments (1, 19, 28, 33–37), lack of reporting detail (19, 33, 39), old condoms (22), or lack of control experiments (1, 19, 33).

2.3. Indirect evidence, minimal infectious dose of Zika virus

See PRISMA flowchart (Fig. 3).

  • We identified 16 unique publications in a search for studies about the minimal infectious dose of Zika virus in bodily fluids relevant to sexual transmission, but none provided any data.
  • We identified 23 unique publications in a search for studies about the minimal infectious dose for sexual transmission of other viruses in humans. We included 13 after screening titles and abstracts but retained none after full text assessments. All studies were animal experiments.
  • We included nine publications identified in the systematic review for review question 1 (Annex B1), which reported on the intravaginal or intrarectal dose of Zika virus in animal models. Seven studies used mouse models (40–46) and two used non-human primate models (47, 48). All six studies that assessed Zika virus infection through intravaginal inoculation in mice used hormone treatment to induce diestrus (40–42, 44, 45, 47). In non-human primates, a dose of log 4 to log 6 plaque forming units (PFU) (47) and log 7 PFU (48) led to successful intravaginal inoculation. The smallest dosages used to successfully infect immunodeficient diestrus mice were 1000 PFU (43) and 750 PFU (45).

Risk of bias assessment

Reporting in all studies (1, 19, 33–36) was too poor to allow an assessment of the risk of bias using the SYRCLE tool.

2.4. Indirect evidence, condom effectiveness for prevention of non-Zika viral STIs

  • We included five studies, all of which reported on the effectiveness of condoms to prevent HIV infection in “always” or “consistent” condom users compared with “never” users; one study pooled data from two cohort studies (49), three conducted a meta-analysis (15, 16, 50), and one narrative review (51).
  • In MSM serodiscordant couples, Smith et al. reported on prevention of HIV transmission among MSM, pooling data from two cohort studies based on participants in RCTs (49). Condom effectiveness was 70.5% (95% CI: 58.2–79.2). A WHO meta-analysis estimated condom effectiveness against the sexual transmission of HIV in MSM at 64% (95% CI: 33–80, 5 studies, I2 0%) (50).
  • In heterosexual serodiscordant couples: Giannou et al. estimated the effectiveness of male condoms at 71% (95% CI: 63–80, 17 studies, I2 39%)(16). Weller et al. estimated the effectiveness of male condoms at 80.2% (95% CI: 56.3–91.0). Three of five cohorts used to calculate the incidence among “never” condom users were also included in the calculation by Giannou et al. (16). These estimates aggregate condom effectiveness over both vaginal and anal sex.
  • Holmes et al. concluded in a narrative review that condoms are effective in protecting against HIV transmission (51).

Risk of bias assessment

Using the ROBIS tool (23), all systematic reviews were at high risk of bias because none assessed the risk of bias in individual studies. The study by Smith et al. (49) was limited by the representativeness of the study population, as it pooled data of RCT for an HIV vaccine and an HIV-behavioural intervention.

Fig. 2. Fraction of leaking condoms, stratified by particle size, and sorted from lowest to highest.

Fig. 2Fraction of leaking condoms, stratified by particle size, and sorted from lowest to highest

Text at the top right position indicates the fraction of leaking condoms followed by Clopper–Pearson CIs (38), the particle assessed, the number of condoms (N) tested, and the materials of the tested condoms. We report results stratified by brand for Voeller et al. (22) because the fraction of leaking condoms showed large heterogeneity between brands. * Indicates leakage results of female condoms. All other results refer to male condoms. We excluded results from tests with spermicide-treated condoms. Abbreviations used: bacteriophage T7 (T7), bacteriophage φX174 (φX174), cytomegalovirus (CMV), herpes simplex type 2 (HSV2), HIV, hepatitis B virus (HBV), herpes simplex (HSV, type 1 and 2), polystyrene microspheres (PMS), poliovirus type 1 (PV1). We calculated confidence intervals for the leakage studies using Clopper–Pearson’s exact method with the R package PropCIs (38).

Fig. 3. PRISMA flow chart for indirect evidence, minimal infectious dose of Zika virus.

Fig. 3PRISMA flow chart for indirect evidence, minimal infectious dose of Zika virus

Search strategy A was on Zika virus in bodily fluids, and search strategy B on other viruses in bodily fluids relevant to sexual transmission.

Source: adapted from (27).

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