Introduction

After primary infection with human cytomegalovirus (CMV), CMV establishes life-long latency in the infected human [1]. Non-primary infection can occur in an individual with pre-existing immunity to CMV (being CMV seropositive) if there is reactivation of primary infection, or if re-infection occurs with a different CMV strain [1]. Primary or non-primary CMV infection can result in excretion of CMV in an infected individual’s bodily fluids, such as (but not limited to) saliva and urine [1, 2]. The presence of CMV in a bodily fluid, which may be detected by culture techniques or through CMV deoxyribonucleic acid detection by polymerase chain reaction, is known as shedding [2]. An individual can become infected with CMV through contact with bodily fluids of another individual who is shedding CMV [1, 3]. Young children may shed CMV for a prolonged period, making this age group an important source of CMV horizontal transmission to other children, adults, and importantly, pregnant women [1].

CMV infection is usually associated with no symptoms, or only mild symptoms, in most healthy individuals, including pregnant women [1, 3]. However, when CMV infection is contracted in a fetus before birth by vertical transmission from the mother, it can cause congenital CMV (cCMV) infection, which can be associated with severe disease in some infants [1, 3]. Up to 25% of children with cCMV infection will have life-long problems, such as sensorineural hearing loss (the most common adverse sequalae), neurodisability, and visual impairment [4–6]. Despite the burden of adverse health outcomes associated with cCMV infection, most pregnant women are not aware of CMV and cCMV infection, and advice about it is not routinely provided as part of antenatal care in the United Kingdom [7–9]. A pregnant woman may reduce her risk of acquiring CMV infection by the avoidance of direct mucosal contact with a young child’s saliva and urine, such as not kissing directly on the lips, not sharing food and drink with them and hand washing after contact with saliva or urine [10–13]. There is evidence to suggest that this might be achieved through educational interventions [14–17].

This study aimed to explore the experiences of those participating in a research study investigating CMV shedding during pregnancy in CMV seropositive women with young children, and the potential facilitators and barriers towards engaging pregnant women in CMV antenatal education and behavioural change measures.

Materials and methods

This qualitative interview study was nested within an observational study that was conducted to understand the feasibility of running an observational cohort study on CMV shedding during pregnancy in CMV seropositive pregnant women living with at least one child under the age of four years (Cytomegalovirus Shedding Characteristics in Pregnant Women (the cCHIPS study); Clinicaltrials.gov identifier NCT04021628). Eligible pregnant women were identified during routine antenatal appointments at a tertiary hospital in London, UK, and recruited between 9^th April 2019 and 30th December 2020. As part of the observational study, blood samples from all participating women were tested to determine their CMV serostatus. CMV seropositive women were enrolled, and serial saliva, urine, vaginal secretions, and blood samples were collected to assess for CMV shedding. A serial questionnaire was completed by the participating women to assess for hygiene-related behaviours. Women were aware that they were participating in a study about CMV, but were not given specific instructions about ways to reduce the risk of acquiring new CMV infection during pregnancy.

At the end of participation in the cCHIPS study, individual, semi-structured interviews were conducted to evaluate the participants’ experiences of study participation, on up to 20 participating women. The interview guide (Box 1) was developed collaboratively by the research team, consisting of open and closed questions with prompts. The series of questions were divided into two categories: the first was to explore the participants’ experiences of study participation (described as ‘direct’ experiences), and the second was to evaluate any subsequent non-specifically directed consequences of study participation (described as ‘indirect’ experiences).

The same interviewer conducted the interviews by phone, which were audio-recorded and transcribed verbatim. The transcribed interview data was analysed following the six phases of Thematic Analysis described by Braun and Clarke [18]. Where extracted quotes by the participants were included in the report, these are written in italic font and signified by the double quotation marks, and any omitted material are signified by the symbol ’…’.

The study was ethically approved by the National Health Service (NHS) Health Research Authority and London Brent Research Ethics Committee (19/LO/0161). Informed written consent was obtained from all participants. Authors SS and PH had access to information that could identify individual participants during or after data collection.

Results

Seventy-eight participating women were invited to take part in the interview via email, of which twenty responded and all agreed to it. Twenty pregnant women took part in the interviews, as described in the Methods section, with each interview lasting between 18 and 40 minutes. Each participating woman was interviewed once. Table 1 describes the demographic characteristics of women interviewed. The following two main themes were identified: 1) research participation is contingent on a balance of convenience and inconvenience, and benefits and risks, and 2) research participation in pregnancy is associated with subsequent non-specifically directed changes to usual behaviour influenced by awareness, knowledge, and support. The themes and subthemes that emerged from the 20 interviews are outlined in Table 2.

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Table 1. Participant demographics.

https://doi.org/10.1371/journal.pone.0292134.t001

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Table 2. Themes and sub-themes emerged from interviews with pregnant women.

https://doi.org/10.1371/journal.pone.0292134.t002

Discussion

This qualitative study sought to explore the experiences of pregnant women taking part in an observational research study about CMV shedding in pregnancy and to identify the potential facilitators and barriers towards engaging pregnant women with CMV risk-reduction measures.

Our findings that convenience of participation is a key reason for pregnant mothers, especially those with young children to minimise any potential impact on childcare, to take part and remain in a study have reaffirmed that convenience should be at the core of study design. Paradoxically, low-intensity study involvement reduces engagement between the participant and the study team, which could impact on study compliance and retention. In future studies, ensuring that the design involves regular contacts, monitoring and reminders, whilst still maintaining convenience of study participation, would be beneficial to both the participants and research team.

A collaboration between the research and clinical teams is essential to ensure that research procedures and clinical appointments can run in synchrony, as also shown in previous research [19]. The timing of research involvement is another key consideration when designing a maternal study. It is important to weigh up the benefits for a pregnant woman to complete a study procedure around the time of birth against the risks of poor study compliance.

Antenatal screening for CMV infection and neonatal screening for cCMV infection are not part of routine maternity care in the UK. The fact that pregnant women valued the ability to know their own and their newborns’ CMV status without inducing unintended anxiety or concerns, is reassuring not only for future studies, but also for the potential implementation of routine antenatal and neonatal CMV screening. The concern of inducing anxiety in pregnant women through the acquisition of information on CMV without being able to provide solutions to treat it, has been recognised to be a factor in the reluctance of health care professionals to include CMV in routine antenatal education [8]. However, in line with our findings, the same research also found that pregnant women were keen to acquire knowledge about CMV and were motivated to reduce risks of CMV to their unborn child [8].

This was a non-interventional study, where no recommendations to perform hygiene-based behaviours were made, nor was information provided of any hygiene-based behaviours that could promote the risk of CMV infection to them or their unborn child. However, the serial questionnaires to assess the pregnant women’s hygiene-based behaviours used induced the reflection of and heightened awareness into their own behaviour, some enough to have resulted in a change to their behaviours during study participation. Our findings are in line with previous research that has highlighted that trial participation had an impact on the participants’ thinking about their own behaviour, with a possibility to influence change [20]. The potential for subsequent non-specifically directed changes of behaviour through study participation should be evaluated when designing a trial to consider its influence on the study results.

Knowledge of CMV serostatus empowered women participating in the study to make informed decisions on their behaviour. Most pregnant women modified their behaviour to reduce contact with saliva and urine of their young child, with the aim of reducing the risk of a new CMV infection which could be passed on to their unborn child. However, some did not adapt their behaviours because of the perception that the risk of vertical transmission was significantly reduced, as they already had CMV immunity. The ability of the knowledge of maternal CMV serostatus to have an impact on the perceptions to risk that may result in a behavioural change, may be an important consideration in the evaluation of antenatal CMV screening.

Our findings have highlighted that behavioural change messages about CMV in pregnancy should be framed as a short-term measure instead of a long-term measure to make it more attainable, and, in line with previous research [8], as a risk-reduction measure. We have also shown that behavioural change messages about CMV should be framed in the context of advice about other infections, to make behavioural change measures during pregnancy more achievable, relatable, and practical for women. Our study has also identified the value of involving partners in antenatal education on CMV, especially on the continual support they are able to provide to the pregnant women in implementing behavioural measures to reduce the risks of CMV. Moreover, our study has shown that continual prompts is a key factor to sustain behavioural change measures throughout pregnancy, which can be provided by their partners. Research also supports the inclusion of partners for behavioural change [8, 21].

Although the study was limited to 20 participating pregnant women, thematic saturation was achieved it provided rich data highlighting the experiences of participating women and reveals the potential facilitators and barriers towards engaging pregnant women in CMV antenatal education and risk-reduction measures. The lack of ethnic diversity may have had an impact on the findings and therefore warrants further investigation.

Finally, while the behavioural modification identified in our study was specific to pregnant women with existing children, most of the themes and subthemes identified from our study can be applied in most context of maternal research. We recommend for research involving pregnant women, especially in those with existing children, to be centred around convenience of participation. We also recommend it to be informative, empowering, holistic, and supportive.

This qualitative study provided a richer understanding of the pregnant mothers’ experiences and perspectives on participation in research. It showed that study participation during pregnancy in women with young children is feasible. It provided us with lessons to be learnt and a better understanding of the potential facilitators and barriers towards engaging pregnant women in CMV antenatal education and risk-reduction measures, which can be applied in other contexts of maternal research.

Acknowledgments

We would like to thank the women who participated in this study.