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Risk Factors for Congenital Cytomegalovirus Infection in the Offspring of Young Women: Exposure to Young Children and Recent Onset of Sexual Activity

^a Departments of Pediatrics, Epidemiology, and Maternal and Child Health
^b Pediatrics and Microbiology, University of Alabama, Birmingham, Alabama

	ABSTRACT

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OBJECTIVE. Two recognized sources of maternal cytomegalovirus infection are young children and sexual activity. Previous studies evaluated either maternal exposures to young children or sexual activity, but these studies did not evaluate whether both of these maternal cytomegalovirus sources contribute to increases in congenital cytomegalovirus infections within populations with a high prevalence of infection among women of childbearing age. Our objective with this study was to investigate whether maternal cytomegalovirus exposure through young children and by sexual activity increases the risk for congenital cytomegalovirus infection in their offspring.

METHODS. A case-control study of 519 women from a delivery population in Birmingham, AL, between December 1992 and July 1998 was undertaken to measure the association between maternal cytomegalovirus exposures and an increased risk for congenital cytomegalovirus infection in their infants. Routine newborn cytomegalovirus screening at the hospital identified infants with congenital cytomegalovirus infection. The cases (n = 150) were women who delivered an infant with congenital cytomegalovirus infection, and the control subjects (n = 369) were randomly selected from the delivery population of women whose newborns were uninfected. Investigation of exposures included using a standardized maternal interview, prenatal and medical chart abstraction, and laboratory confirmation of cytomegalovirus infection.

RESULTS. Significant associations between congenital cytomegalovirus infection and caring for preschool children in the year before delivery, onset of sexual activity <2 years before delivery, sexually transmitted diseases during pregnancy, household size >3 people, and maternal age <25 years were identified. Women who cared for preschool children in the year before delivery and also became sexually active within the 2 years before delivery were at greatest risk for delivering an infant with congenital cytomegalovirus infection.

CONCLUSIONS. Caring for young children and recent onset of sexual activity contribute to an increased risk for congenital cytomegalovirus infection in the offspring of young women.

Key Words: case-control study • cytomegalovirus • sexual activity • pregnancy • child care

Abbreviations: CMV—cytomegalovirus • STD—sexually transmitted disease • OR—odds ratio • aOR—adjusted odds ratio • CI—confidence interval

Congenital cytomegalovirus (CMV) infection remains the most common intrauterine infection in the United States and is a leading cause of sensorineural hearing loss in children. These fetal infections are a result of a maternal CMV infection that occurs either before or during the pregnancy. Two recognized sources of maternal CMV infection are young children and sexual activity.

Evidence for young children as a source of CMV infection for women of childbearing age includes studies of children in child care centers and their parents.^1–6 Studies have demonstrated that parents have an increased risk for CMV infection when the child attends a child care where CMV infection is prevalent.^2,4,7 Also, CMV seroconversion in parents has been associated with CMV excretion in their child.^4,8 In 1 study, the same CMV strain was identified in an older sibling, the mother, and subsequently in the infant with congenital CMV infection.⁵ Other studies also identified the same CMV strain in children and their parents or other adult family members.^5,9,10

Studies in sexually transmitted disease (STD) clinics and adolescent populations have indicated that sexual transmission is another important source of CMV infection in young urban women.^11–14 High rates of CMV infection have been observed in both STD clinic populations and adolescent populations.^14–16 Also, similar CMV strains have been found in the sexual partners of those who were infected recently with CMV.¹⁷ Sexually transmitted infections during pregnancy also have been associated with delivering an infant with congenital CMV infection.¹⁸

Although young children and sexual activity are recognized as sources of CMV infection, previous studies did not evaluate whether these exposures both singly and together contribute to increases in maternal infections that then may lead to congenital CMV infections. Rates of congenital CMV infection are highest in urban, low-income, predominantly black populations in which the CMV seroprevalence rates among women of childbearing age are high, suggesting that CMV exposures are occurring frequently in these populations.¹⁹ We undertook a case-control study in an urban delivery population to investigate whether maternal CMV exposure through young children and by sexual activity increases the risk for congenital CMV infection in offspring.

	METHODS

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Study Population
We conducted a case-control study in the delivery population of University Hospital (Birmingham, AL) between December 1992 and July 1998. During this time, all newborns who were delivered at University Hospital were screened for congenital CMV infection by detection of virus in saliva using a rapid-culture method as previously described.^20,21 This screening method has a documented 100% sensitivity and 100% specificity.²⁰ More than 88% of all newborns who were delivered at the hospital were screened for congenital CMV infection, and 155 infants were identified with congenital CMV infection during the study period. All positive results on the newborn screening test were confirmed by isolation of virus from urine and/or saliva at a 3- or 4-week postnatal follow-up clinic visit.

Cases were mothers of newborns who were identified with congenital CMV infections during the study period. A total of 150 of 155 mothers of infants with congenital CMV infection are included in the study. Reasons for not participating included the following: not approached after the death of infant (n = 1), unavailable because of lack of infant custody (n = 2), and declined participation (n = 2).

Control subjects were randomly selected from the mothers of uninfected newborns who were delivered during the study period and frequency-matched by ±3 weeks of birth and race to cases in a 2:1 ratio. Eligible mothers of uninfected infants were randomly selected from the delivery population weekly and invited to participate in our study by a letter and telephone calls. Control subjects who participated in our study did not differ with respect to age, race, the source of prenatal care, or number of pregnancies from the potentially eligible mothers who did not participate. The study was approved by the University of Alabama Institutional Review Board, and all participants provided informed consent.

A structured interview using a standard maternal questionnaire was administered by trained interviewers with the mothers at their first visit, usually 3 or 4 weeks after their delivery. Questions were asked about the following: maternal demographic characteristics; household information, such as number, age, and gender of members in the household; care for young children either as a family member and baby-sitter or volunteer at a church nursery. Information about sexual history; sexually transmitted infections; gynecologic and medical history; medications and drug use during pregnancy; complications during pregnancy; and employment history, specifically whether job duties involved the care of young children, also were collected.

Maternal prenatal and delivery records were abstracted for the following: maternal and demographic factors, laboratory confirmation of sexually transmitted infections, medical conditions, and obstetric history. Standardized prenatal summaries (obstetric automated record) were available for women who received prenatal care from the county health department clinics, 95% of the study population.²² These standardized prenatal summaries contained summary information on each prenatal visit, all laboratory test results, and medical and obstetric history. Records were abstracted 2 to 3 months after delivery. Good agreement (based on statistics) was observed between the questionnaire and the prenatal record for demographics, prenatal visits, and sexually transmitted infections.²³

Data Analysis
For assessment of risk factors for congenital CMV infection, characteristics of case patients and control subjects were examined using the ² test for categorical variables and the 2-tailed t test for continuous variables. Also, univariate odds ratios (ORs) and 95% confidence intervals (CIs) using the exact method were calculated. Multivariate unconditional logistic regression using backward stepwise selection with P < .10 was used as a cutoff for retention in the model to assess whether putative risk factors were independently associated with delivering an infant with congenital CMV infection. Potential confounders that were found to be associated with congenital CMV infection on univariate analysis were included in the multivariate model, as were risk factors that were considered a priori to be potential confounders. All data analyses were performed using SAS 8 statistical software (SAS Institute, Inc, Cary, NC).

	RESULTS

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Study population characteristics are shown in Table 1. Both case patients and control subjects are predominantly single, black women. The source of prenatal care was similar for both case patients and control subjects: 95% received prenatal care from the county health department. More than two thirds of the case patients and control subjects enrolled in prenatal care in the first trimester of their pregnancy. The case patients were significantly less likely to have a previous pregnancy and also were younger at delivery than the control subjects. Household size was slightly larger for the case patients than for the control subjects. However, the number of children who were younger than 6 years and residing in the household was similar for both the case patients (median: 0; range: 0–4 children) and the control subjects (median: 1; range: 0–5 children). Only 3 (2.0%) of the case patients and 7 (1.9%) of the control subjects reported ever having been employed as a child care or nursery worker.

View larger version (16K): [in this window] [in a new window]   FIGURE 1 Comparison of the proportion of case mothers with control subjects who cared directly for preschool children in the 12 months before delivery according to age groups (months).

Table 2 includes potential risk factors that were associated with delivering an infant with congenital CMV infection. Maternal age <25 years at delivery and being primiparous both were associated with delivering an infant with congenital CMV infection. Having 3 or more people living in the household during the year before delivery slightly increased the risk for delivering a child with congenital CMV infection, although this factor was of borderline significance. Direct care of both children who were younger than 3 years and children who were younger than 6 years was associated with an increased risk for congenital CMV infection, although having children who were younger than 6 years residing in the household was not associated with an increased risk for congenital CMV infection. Recent onset of sexual activity (<2 years) was associated with an increased risk for delivering an infant with congenital CMV infection, although sexual debut at an early age (<16) and the number of lifetime sexual partners (>3) did not increase the risk for delivering an infant with congenital CMV infection. Control subjects were more likely to have a history of sexually transmitted infections than the case patients. Case patients reported higher percentages of gonorrhea, chlamydia, genital warts, syphilis, and trichomoniasis during pregnancy than the control subjects, but these differences were not statistically significant. However, when sexually transmitted infections during pregnancy were combined, women with any sexually transmitted infection (gonorrhea, chlamydia, genital warts, syphilis, genital herpes, or trichomoniasis) during pregnancy had an increased risk for delivering an infant with congenital CMV infection compared with women who had no identified sexually transmitted infections. Bacterial vaginosis during pregnancy also was associated with delivery of an infant with congenital CMV infection but was of borderline significance.

View larger version (17K): [in this window] [in a new window]   FIGURE 2 Distribution of 2 factors (caring for children who were younger than 6 years in the year before delivery and recent onset of sexual activity <2 years before delivery) in the case patients and control subjects.

	DISCUSSION

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Our results indicate that young children and sexual transmission both contribute to congenital CMV infections in this young urban population. Providing direct care of young children in the year before delivery seems to be an important source of maternal CMV infections and increases the risk for delivering a newborn with congenital CMV infection in this population. The recent onset of sexual activity and the presence of sexually transmitted infections during pregnancy indicate that young women in the population are acquiring CMV infections through sexual exposures to CMV, which in turn can lead to in utero CMV infections. Women who both care for young children and have recent onset of sexual activity have the greatest risk for delivering an infant with congenital CMV infection (OR: 7.2). Maternal age <25 years at delivery and living in a household with 3 or more people in the year before delivery also contribute to congenital CMV infections in this population.

More than 76% of the case mothers cared for young children either in their household or in a friend's household. It is interesting that because case patients are more likely to be primiparous, their exposures to CMV by young children are occurring not as they care for their own children but when they care for a relative's or a friend's child. Previous studies have shown that children who excrete CMV may spread infection to a parent and to other adults in the household.^4,5,8 Other studies have demonstrated that having children in child care centers with high rates of CMV infection correlates with an increased risk for CMV infection in the parents of these children.^2,4,7 Possibly young children in these households were acquiring CMV infection in child care centers, resulting in CMV exposure for other household members. However, in both the case patients and control subjects, fewer than one third of the young children who resided in the homes were in any type of group child care, suggesting that child care centers are not an important source of CMV infection for mothers in this urban population. Also, possible occupational exposure to CMV while working in a child care facility or nursery did not account for the observed increased risk for congenital CMV infection, because only 3 case patients (2.0%) and 7 (1.9%) control subjects listed any employment as child care or nursery workers.^24–26

Recent onset of sexual activity (<2 years) in young women increased the risk for congenital CMV infection in their offspring. This finding suggests that recent sexual exposure to CMV resulted in maternal CMV infections that may have occurred in the months or year before conception and also during pregnancy. Previous work suggested that the risk for congenital CMV infection remains elevated even when primary maternal infection occurs months before conception.²⁷

Although individual sexually transmitted infections were not independently associated with delivering infants with congenital CMV infection, the case patients had higher percentages of gonorrhea, chlamydia, genital warts, syphilis, and trichomoniasis than the control patients. The association with sexually transmitted infections during pregnancy may be only an indicator of recent sexual activity and recently acquired CMV infections. However, a study of women who attended an STD clinic found that CMV was isolated from the cervix 6.5 times more often when other sexually transmitted infections were present.¹³ It is possible that other sexually transmitted infections during pregnancy may enhance the transmission of CMV from mother to fetus. A prospective study that captures the temporal relationship between CMV infection²⁸ and other sexually transmitted infections is needed to clarify the role of concomitant infections on in utero transmission of CMV.

Earlier sexual debut (<16 years of age), multiple sexual partners (>3), and history of sexually transmitted infections were not associated with increases in congenital CMV infection in our population. However, early sexual debut, multiple sexual partners, and history of sexually transmitted infections have been reported to be associated with CMV seropositivity in other populations.^14,15,29 These factors may be indicative of earlier CMV exposures, resulting in women's becoming CMV seropositive before pregnancy and therefore decreasing their risk for delivering newborns with congenital CMV infection. We previously reported that maternal immunity to CMV years before pregnancy is protective for offspring in future pregnancies.³⁰

Young maternal age as a risk factor for congenital CMV infection has been observed in previous reports.^19,30,31 This study also found that women aged 25 years or less at delivery were more likely to have an infant with congenital CMV infection than women who were older. Young maternal age may be a marker of recent exposure to CMV, although it also may be indicative of a biological effect of age on maternal infection. Possibly the combination of an age-related factor with recent exposure to the virus in young women enhances CMV infection during pregnancy and increases the risk for transmission to the fetus.¹⁹

Another risk factor for congenital CMV infection that was identified in our study was residing in a household with 3 or more people. This risk factor was independent of young children's living in the household. Our study did not collect information on the number of rooms in the house, so we were not able to assess crowding or other living conditions that may have contributed to CMV infections and subsequent transmission to the fetus. However, the case patients (69%) were more likely to live in households where their parents or grandparents were the heads of household compared with the control mothers (54%). In many of these parental households, other siblings and their children also were living in the house, resulting in larger households and more opportunities for exposures to CMV among the case mothers.

This study may have underestimated the number of individual sexually transmitted infections in the population because the study relied primarily on maternal recall to document the presence of infections during pregnancy. Underestimation may be attributable to a lack of understanding by the participant or an unwillingness of the participant to reveal previous sexually transmitted infections. We attempted to minimize the possible underestimation of exposures by interviewing the women without other family members present, using a standardized questionnaire, and carefully reviewing the prenatal records for laboratory culture and identification dates of sexually transmitted infections during pregnancy. The combination of using both the questionnaire and the prenatal summaries allowed us to capture most reported and documented sexually transmitted infections. Overall, in both the case patients and control subjects, the estimates of sexually transmitted infections are similar to previous reports of STDs in young women within the population.^18,32

To minimize further the possibility of differential maternal recall between the case patients and control subjects, we used similar interview methods and collection of prenatal summaries for both groups. Besides using a standard interview, the interval between delivery and interview was the same for both case patients and control subjects. Also, because >95% of the case patients and control subjects received their prenatal care within the same system, it is unlikely that collection of exposure information differed between the groups.

Our study findings describe maternal CMV exposures that result in congenital CMV infections in a predominantly unmarried, low-income, black delivery population. Although these young women's CMV exposure opportunities may have been more frequent, there is no evidence to suggest that if women in other populations are caring for young children or have recently become sexually active, then they would not have a similar risk for congenital CMV infection in their offspring. It is likely that predominantly married, middle to upper income, white delivery populations also are being exposed to CMV while caring for young children.

For prevention of congenital CMV infection, young women of childbearing age should be informed about CMV transmission routes.³³ Young women who are considering pregnancy or who are already pregnant should be instructed to practice good hygiene (ie, hand-washing) when caring for young children.³⁴ Adolescents and young women should be advised to avoid salivary and genital contact with others. However, changing behavior through health communication is challenging. A randomized, clinical trial that provided information on CMV and the importance of hand-washing failed to show a decrease in CMV acquisition by women of childbearing age, demonstrating the difficulty in changing behaviors,³⁵ yet successes have been observed in lowering the risk for HIV infection in black adolescents through health education interventions.^36–38 Even if behavioral changes through health communication decreases some congenital CMV infections, more likely an effective vaccine that is given to children or young teens and could prevent congenital infection would be more successful in preventing congenital CMV infection in most populations.

	ACKNOWLEDGMENTS

 
This study was supported in part by grants from the National Institutes of Health, the National Institute of Child Health and Human Development (P01 HD 10699), the National Institute of Allergy and Infectious Diseases (P01 AI43681), the National Institute on Deafness and Other Communication Disorders (R01 DC02139), and the General Clinical Research Center (M01 R00032).

	FOOTNOTES

 
Accepted Feb 15, 2006.

Address correspondence to Karen B. Fowler, DrPH, Department of Pediatrics, 1600 7th Ave S, CHB 306, Birmingham, AL 35233-1711. E-mail: kfowler{at}uab.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.

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This Article Abstract Full Text (PDF) P3Rs: Submit a response Alert me when this article is cited Alert me when P3Rs are posted Alert me if a correction is posted Citation Map Services E-mail this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to My File Cabinet Download to citation manager Citing Articles Citing Articles via CrossRef Citing Articles via Google Scholar Google Scholar Articles by Fowler, K. B. Articles by Pass, R. F. Search for Related Content PubMed PubMed Citation Articles by Fowler, K. B. Articles by Pass, R. F. Related Collections Infectious Disease & Immunity

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