Knowledge of cytomegalovirus and available prevention strategies in pregnancy: a cross-sectional study in Portugal

Abstract Objective Maternal and fetal congenital infection by cytomegalovirus (CMV) during pregnancy is the leading infectious cause of neurologic impairment and hearing loss. Efforts at limiting CMV exposure are based on hygienic measures. This study assessed the relationship between CMV knowledge and pregnant women’s time perspective as per the Zimbardo Time Perspective Inventory (ZTPI) scale. Methods We conducted a prospective descriptive study at a secondary-care Portuguese hospital between October to November 2021. All consecutive pregnant women in antenatal third-trimester appointments were included. The questionnaire included: sociodemographic data, knowledge about CMV, and the ZTPI scale, validated to our population. The number of correct answers in the knowledge section of the questionnaire was tallied to determine the individual knowledge score (KS). We investigated patients subjective perceptions of CMV infection during pregnancy, CMV knowledge, and CMV serologic status of pregnant women. Results We enrolled 96 pregnant women. 81.0% had not previously heard about CMV and only 8.8% had heard about it through their obstetrician. No significant association between awareness of CMV and education level was detected. 16.0% of pregnant women declared that they were aware of the hygienic measures for CMV. The CMV serology was performed in 21.3% of those enrolled in the preconception assessment, and 13.8% proved to be immune. From the time perspective, half of the women displayed a future-oriented attitude. Future-oriented women had significantly higher KS. No significant association was found between KS and education level, age, or previous pregnancy. There was a significant association between KS and women that work in health care. Conclusions Most patients had no knowledge of CMV. Being a medical professional and having a future-oriented outlook increases knowledge about CMV. Primary health care and obstetrics doctors may play a crucial role in informing pregnant women of antenatal appointments. The CMV serology coverage is scarce in this sample. This study constitutes a first step toward raising the awareness of the general population about CMV.


Introduction
Cytomegalovirus (CMV) is the most common congenital infection (0.5-2% of all live births) and the main cause of congenital sensorineural hearing loss. It is a contributing cause of up to 10% of all cases of cerebral palsy. Congenital infection can occur after maternal primary infection or nonprimary infection [1,2] CMV seroprevalence in patients of child-bearing age, defined as evidence of previous CMV infection (positive CMV immunoglobulin G (IgG)), is estimated to be between 50% to 85% in Europe and the United States [3]. However, data about the Portuguese context are scarce [4]. Guidelines and practices regarding CMV serological screening in pregnancy are very heterogeneous. Most North American and European guidelines do not recommend routine screening for CMV infection during pregnancy [5]. However, without any recommendations for systematic screening of maternal CMV infections, maternal seroconversion is sometimes diagnosed when serology is electively performed in pregnancy after symptoms [6]. The prevalence of congenital infection correlates with seroprevalence of the mother. Prevention research such as vaccine and hygiene studies should target not only seronegative but also seropositive pregnant women [1,7,8]. Educational interventions to promote simple hygienic measures, such as hand hygiene, may reduce primary CMV infection and reinfection during pregnancy. As these education and hygienic interventions are inexpensive and straightforward, they should be considered for all pregnant women, regardless of serologic status [6]. Despite the absence of randomized trials demonstrating the efficacy of maternal hygiene education, the only way to prevent maternal CMV infection is by limiting exposure to the virus [9].
Awareness and knowledge of congenital infection are low and this raises the risk of maternal infection. It is estimated that only 15% to 25% of pregnant women report awareness of CMV and its implications for pregnancy but, once informed, more than 70% want CMV screening [10,11].
Time perspective is one of the factors that most significantly shape how human beings behave, inflecting the way individuals partition the flow of personal and social experiences into distinct temporal categories. This affects decision-making by locating the primary set of psychological influences within the temporal frames of present, past, or future [12]. Zimbardo and Boyd (1999) identified five types of time perspectives: the past-positive (PP) perspectivea tendency to focus on the positively evaluated past; the past-negative (PN) perspectivea tendency to focus on negative events in the past; the future (F) perspectivecharacterized by planning for and achieving future goals; the present-hedonistic (PH) perspectivea tendency to seize the "here and now" at all costs; and the present-fatalistic (PF) perspective the belief that the future is predestined, which leads to a tendency to live the present in a passive manner [13].
Zimbardo Time Perspective Inventory (ZTPI) is one of the most well-known and widely used measures of time perspectives and has been extensively used in research in the fields of psychiatry, psychology, and human behavior. The research has revealed that it is an important psychological variable associated with many areas of human functioning, such as well-being, health behaviors, risky behaviors, tendency to become addicted, etc [14]. The studies describe the relationship between health and risk behaviors and sometimes perspective types. For example, individuals with a present-oriented time perspective (PF or PH) are associated with higher-risk health behaviors, and individuals with a stronger future time perspective tend to report less-risk health behaviors [15]. The authors did not find any study about time perspectives that focuses on pregnant women.
The first aim of this study was to determine the awareness and knowledge of CMV among pregnant women; secondly, to establish a time perspective relation to knowledge about CMV, and finally determine factors that may influence CMV knowledge and awareness.

Materials and methods
We conducted a monocentric prospective descriptive/observational study at a secondary-care Portuguese hospital. We included all consecutive pregnant women from antenatal third-trimester appointments between October to November 2021. The study was carried out by obstetricians working at the Department of Obstetrics of Centro Hospitalar do M edio Ave. After informed consent, participants were invited to read and answer a questionnaire. It consisted of 16 questions assessing baseline sociodemographic information, 12 questions assessing awareness about CMV and toxoplasmosis, serologic screening of CMV, and knowledge about CMV, including 10 true/false items ( Table 1). The number of correct answers was tallied to determine a knowledge score (KS) [16], and, to assess the time perspective of pregnant women, according to the validated ZPTI version translated to Portuguese [13].  6, 9, 10, 13, 18, 21, 24, 30, 40, 43, 45, 51 and 56). Each one of the five factors was measured, and the type of time perspective was identified based on the factor in which the pregnant women scored the highest.
The KS scores were categorized into 3 levels according to the number of correct answers: low level of KS (0-3 correct items), medium level (4-7 correct items), and high level (8-10 correct items).
Demographics information such as age, ethnicity, education was collected from the questionnaire. Some clinical information, like parity, medical and surgical history, previous history of congenital infection and toxoplasmosis screening serology was collected from hospital records.

Statistical analysis
For the statistical analysis, we used SPSS V R -Software, Version 26. Means or medians were calculated for continuous variables and frequencies or proportions for categorical variables. This study was approved by the local ethics committee of the Centro Hospitalar M edio Ave. All participants signed a consent form based on the latest version of the Helsinki Declaration.
The required sample size of 78 cases, was calculated using the statistical Excel V R -Software and taking into account that the prevalence of pregnant women of low risk corresponds to 60% of the total pregnancies attending our hospital by year (n ¼ 700), with a confidence level of 95%.
Analyses were performed using the Mann-Whitney test, Fisher's exact test, and the chi-square test to investigate the association between ZPTI/KS and each demographic characteristic using a p-value of <.05.

Results
A total of 96 pregnant women were recruited over the 2-month study period. Sixteen participants were excluded from the analysis because they did not appropriately answer the questionnaire (above 20%). The median age of the participants was 31.1 (SD, 5.027). 33.8% (n ¼ 27) had a college degree, 45,0% (n ¼ 36) had a high school diploma, and 18,8% (n ¼ 15) had only completed elementary school, see Table 1. Among the participants, 81,0% were unaware of CMV or any risks of congenital infection. The primary setting in which some participants had previously heard of CMV was through their obstetrician (8.8%). No significant association was found between awareness of CMV and education level (Fisher's exact test, p ¼ .710).
The pregnancy was not planned in 27,5% of cases. 36 pregnant women had children at home, but only 6 of them were awareness about CMV (chi-square, p ¼ 0,639). Only 16,0% (n ¼ 13) of pregnant women declared to know the hygienic measures for CMV prevention and 5.0% know how to apply it. In comparison, 93.8% of pregnant women reported being aware of toxoplasmosis and preventive measures.
The CMV screening was carried out in 21.3% (n ¼ 17 cases) of the preconception assessment and in 43.8% (n ¼ 35 cases) in the first trimester. About the seroprevalence, 13.8% (n ¼ 11 cases) of preconception and 33.8% (n ¼ 27 cases) in first trimester were IgGþ/IgM-, see Table 2.
On KS, 56,3% had low level (n ¼ 45 cases), 38.8% had medium (n ¼ 31 cases), and 5,0% had high level (n ¼ 4 cases). The hit rates for each question can be seen in Table 3. There was no significant association between KS and education level (Mann-Witney U test, p ¼ .757), employment (Fisher's exact test, p ¼ .532), marital status (Fisher's exact test, p ¼ .617), age (Mann-Witney U test, p ¼ .697) or previous pregnancy (Mann-Witney U test, p ¼ .899). A significant association between KS and women being health care professionals was found (Fisher's exact test, p < .01).
Regarding the Time Perspective, Table 4 shows the absolute and relative frequency of women by their time perspective result on the ZPTI scale and the analysis of the score on the CMV knowledge scale concerning the mean value of correct answers, median, minimum value, maximum value, and dispersion of results, represented by the associated standard error. Half of the women (n ¼ 40) were future-oriented. About the other half, 26.3% (n ¼ 21) were present-oriented, of which 2 participants scored higher in Present Fatalist items and 19 women scored higher in Present Hedonist items; and 23.8% (n ¼ 19) were pastoriented, with 9 participants scoring higher in Past Positive items and 10 women scoring higher in Past Negative items. Figure 1 shows a diagram of extremes and quartiles for each of the five possible time perspectives of pregnant women and their results on the CMV knowledge    scale. It is possible to visually observe a trend toward greater knowledge about CMV in the group of futureoriented women, which is proven in the statistical tests. Future-oriented women showed a significantly higher CMV KS (Mann-Witney U test, p ¼ .012), with a mean of 3.88 correct answers in the future-oriented group (n ¼ 40) and a mean of 2.60 correct answers for the non-future-oriented women (n ¼ 40). There was no association between a nonplanned pregnancy and being present-oriented (Fisher's exact test, p ¼ .320) or future-oriented (Fisher's exact test, p ¼ .622).

Discussion
It has been shown in the past that simple hygiene advice can reduce the incidence of CMV primary infections in pregnancy. This study tried to determine if Portuguese pregnant women were aware of CMV and the adequate hygienic measures to adopt [17].
The present study is innovative. The authors have no knowledge of other studies that assess the time perspective of pregnant women and CMV awareness in Portuguese pregnant women.
The fact that future-oriented women scored higher on CMV KS, showing higher knowledge about the risks of CMV for the fetus, is congruent with the literature reporting less health-endangering behaviors in futureoriented people [18].
Healthcare practitioners should therefore include in their counseling CMV infection risk factors, screening, and hygiene measures to prevent CMV infection. At the same time, this study raises awareness of the potentially serious fetal complications caused by this virus. In the past, it has been suggested for mandatory prenatal CMV serological screening has been recommended to ensure that obstetricians properly counsel their patients [19]. However, we know that fewer than half (44%) of obstetricians advise their patients about how to prevent CMV [20]. Our study emphasizes the need for a better understanding of the reasons why physician knowledge of CMV transmission might not result in pregnancy counseling. Some previous studies have shown that knowledge about CMV infection amongst health professionals is low, lacking, or inadequate, with regard to: how common congenital CMV infection is, how to interpret CMV serology, symptoms in mothers, long-term effects in neonates, and inadequate knowledge about prevention strategies [21]. Additionally, a lack of confidence in discussing CMV and lack of clinical guidelines have been reported. However, strategies such as meetings, conferences, and eLearning increase health professionals' awareness and knowledge. No specific study for Portugal has yet addressed the reasons for the lack of CMV knowledge among health professionals. However, adequately informed health professionals advise women on CMV hygiene precautions most frequently [22,23].
Cytomegalovirus screening is not routinely recommended during pregnancy in Portugal, but is recommended preconceptionally in some cases [24]. However, universal education about prevention strategies should be implemented. Some brochures or websites for patients may be used for improving awareness of pregnant women [21,22].
Communication during CMV screening in pregnancy should focus on risk and severity perception. This should be the model to consider when we plan the implementation of a universal antenatal CMV serological screening policy [25]. Those who were screened for CMV did not show higher KS (Mann Whitney U test, p ¼ 0.278). Additionally, being aware of CMV did not correlate with higher knowledge (Fisher's exact test, p ¼ 0.723). It is important to reinforce the need to explain to pregnant women the effects of maternal CMV primary or nonprimary infection as well as the hygienic measures that need to be taken to reduce the risk of infection during pregnancy.
The strengths of the study were a high participation rate and the use of instruments that had already been validated or previously known to successfully assess the awareness, knowledge, and time perspective of pregnant women. Our sample population limits how generalizable the data may be given that the period of recruitment was relatively short. In addition, although all women were asked to complete the questionnaire after their appointment during the study period, only women who chose to complete the study could be included and, therefore, we have an inherent response bias with our sample of convenience. The external validity of this study is limited since it was a monocentric study on a secondary hospital.
Future questionnaires should attempt to identify other factors associated with providing CMV knowledge and assess the impact of education on the time perspective of pregnant women.

Conclusion
Many women are unaware of congenital CMV and require more education from their medical service providers. Additionally, most patients had no knowledge of CMV. Health professionals and a future-oriented stance may increase one's knowledge about CMV.
Future surveys should attempt to identify factors associated with the lack of hygienic/sanitary measures and information on CMV in prenatal care. Primary health care and obstetricians may play a crucial role in informing pregnant women. This study constitutes a first step toward raising awareness about CMV among pregnant women in Portugal.

Disclosure statement
No potential conflict of interest was reported by the author(s). The authors alone are responsible for the content and for writing this article.

Funding
The author(s) reported there is no funding associated with the work featured in this article.