Original Article
Neonatal Herpes Simplex Virus Infection in Relation to Asymptomatic Maternal Infection at the Time of Labor
N Engl J Med 1991; 324:1247-1252May 2, 1991
- Abstract
- Abstract
Background and Methods.
To define the risk factors associated with neonatal acquisition of herpes simplex virus (HSV) infection, we prospectively obtained HSV cultures from the cervix and external genitalia of 15,923 pregnant women in early labor who were without symptoms or signs of genital HSV infection. Follow-up of the women with positive cultures for HSV and their HSV-exposed infants included serologic tests and serial cultures for HSV.
Results.
HSV was isolated from 56 of the women (0.35 percent), 18 of whom (35 percent) had serologic evidence of a recently acquired, subclinical first episode of genital HSV infection, and 34 of whom (65 percent) had reactivation of HSV. Neonatal HSV developed in 6 of 18 infants (33 percent) born to the women with a first episode of genital HSV, and in 1 of 34 infants (3 percent) born to the women with reactivation of HSV (P<0.01); neonatal HSV also occurred in three of the infants born to the 15,867 women with negative cultures. Neonatal HSV-2 occurred in 1 of 4 infants born to mothers seronegative at delivery for both HSV-1 and HSV-2, in 4 of 12 infants exposed to HSV-2 whose mothers had only HSV-1 antibodies at delivery, and in none of the infants born to 31 women who were HSV-2-seropositive. An increased risk of neonatal HSV was associated with exposure to viral shedding from the cervix and the use of fetal-scalp electrodes.
Conclusions.
Of the asymptomatic women who shed HSV in early labor, about a third have recently acquired genital HSV, and their infants are 10 times more likely to have neonatal HSV than those of women with asymptomatic reactivation of HSV. The presence of maternal antibodies specific to HSV-2 but not HSV-1 appears to reduce the neonatal transmission of HSV-2. Further studies are necessary to determine whether screening and prophylactic treatment are warranted for infants of HSV-2-seronegative mothers who shed HSV-1 or HSV-2 in early labor. (N Engl J Med 1991; 324:1247–52.)
Article Activity
- Article
RECENT studies have indicated that most infants with neonatal herpes simplex virus (HSV) have mothers with subclinical genital HSV infection with asymptomatic shedding of the virus at the time of delivery.1 2 3 4 5 6 7 Not all infants exposed to HSV at the time of delivery acquire neonatal herpes.8 9 10 The design of a successful strategy to interrupt the maternal–neonatal transmission of the virus requires knowledge of the risk factors associated with such transmission and accurate identification of women with asymptomatic viral shedding at the time of delivery. We report the results of a prospective study of 15,923 women without clinical evidence of genital herpes on admission to the labor unit, designed to determine the proportion of women who shed HSV asymptomatically in early labor and to define the risk of neonatal HSV for their infants.
Methods
Selection and Recruitment of Patients
Between January 1984 and June 1989, all women without symptoms or lesions suggesting genital HSV who were evaluated in the labor admission rooms of the University of Washington or an associated private community hospital routinely had HSV cultures obtained from the labia and cervix. The external genital cultures were obtained by swabbing the labia majora and minora and the perianal and periclitoral areas. After insertion of a Graves speculum, a second swab was used to obtain cultures from the ectocervix, endocervix, and vaginal fornices. All personnel were instructed in these procedures, illustrative diagrams were posted in the labor admission rooms, and study personnel reviewed the culture techniques at both hospitals three times yearly.
During the study period, 18,630 women were in labor and subsequently delivered at the two study hospitals (Fig. 1Figure 1
Frequency of Neonatal Herpes Infection among Women with Asymptomatic Shedding of the Virus at the Time of Labor.). Genital HSV cultures were obtained within 48 hours of delivery for 15,923 of these women (85.5 percent). HSV cultures were not obtained in the remaining 2707 women for medical and obstetrical reasons, including the presence of advanced labor, precipitate delivery on admission to the labor unit, active vaginal bleeding, or the induction of labor with an interval of more than 48 hours between admission and delivery. Of the 2707 patients, 18 refused to have cultures performed, and the obstetrical staff neglected to perform them in 113. Women with clinically recognized active genital herpes infection were excluded from the study (accounting for approximately 1.2 percent of all deliveries during the study period), as were women admitted for cesarean section before the onset of labor.Follow-up of Mothers and Infants
Patients identified as shedding HSV at the time of admission to the labor unit were recalled and interviewed within 10 days of delivery (median, 7). HSV cultures were repeated, and an initial serum sample was obtained for HSV serologic testing. Subsequent HSV serologic testing was performed six to eight weeks later. The infants were also recalled and examined; HSV cultures were obtained from the nasopharynx, conjunctiva, umbilicus, and rectum and from any abrasions or suspicious lesions. The infants were then followed intensively for six weeks with serial HSV cultures and examinations. No antiviral chemotherapy was administered during this time, except that infants from whom HSV was isolated after more than 24 hours of life were considered to have neonatal HSV infection and were enrolled in the collaborative protocols for antiviral chemotherapy of the National Institute of Allergy and Infectious Diseases.7 To ensure complete ascertainment for neonatal HSV infection, we also reviewed all records from the virology laboratory, the records of the Children's Hospital Medical Center, University of Washington, and all cases of HSV infection reported to the state of Washington and the three counties (King, Snohomish, and Pierce) served by the University of Washington.1
Laboratory Methods
HSV was isolated and the isolates subtyped as described elsewhere.11 , 12 Serum samples were assayed for HSV antibodies by Western blot assay.13 , 14 The patients with HSV shedding were classified according to serologic status and viral-isolation data into three categories: those with primary genital herpes (women without antibodies to HSV-1 and HSV-2 in the initial serum sample who became seropositive for one of the virus types in the subsequent sample); those with a nonprimary first episode of genital herpes (women with HSV-1 antibodies in the initial serum sample from whom HSV-2 was isolated in early labor and who were seropositive for HSV-2 in the subsequent sample); those with reactivation of HSV (women with stable amounts of HSV antibodies in both the initial and the subsequent serum samples to the virus type isolated from their genital tract15 , 16). The criteria for defining the presence of antibodies specific to HSV-1 or HSV-2 in the initial serum sample as well as the occurrence of seroconversion to the heterologous type in the subsequent serum sample have been published previously.13 14 15 16 17 18 All paired serum samples were tested in parallel, and the serologic status of the mother was not known until three to four months after delivery. Asymptomatic HSV shedding was defined as being present when HSV could be isolated from the genitalia but the patient reported no symptoms and the attending clinician observed no signs of disease. Groups were compared by nonparametric tests in the case of continuous measurements. Categorical outcomes were assessed with the chi-square test or Fisher's exact test (two-sided).
Results
Study Population, Viral Type, and Serologic Status of Women with Asymptomatic HSV Shedding at the Onset of Labor
The median age of the women was 25. Of the 15,923 women evaluated, 11,341 (71 percent) delivered at University Hospital and 4582 (29 percent) at the community hospital. Of the women treated at University Hospital, 66.4 percent were white, 18.1 percent were black, 6.6 percent were Asian, 2.9 percent were Hispanic, and 2.3 percent were Native American. The corresponding figures for the community hospital were 92.4 percent, 6.2 percent, <1 percent, <1 percent, and <1 percent. Only 47.6 percent of the women who delivered at University Hospital were married, as compared with 80.6 percent at the community hospital.
HSV was isolated from the genital tract within 48 hours of delivery in 56 women (0.35 percent); 51 had HSV-2, and 5 HSV-1. The overall rates of asymptomatic shedding of HSV at delivery were 0.32 percent for HSV-2 and 0.03 percent for HSV-1. The rates of asymptomatic shedding were 0.36 percent at University Hospital and 0.32 percent at the community hospital. Serum samples for HSV-antibody testing were available from 52 of these 56 women (93 percent). Eighteen women (35 percent) had serologic evidence of having acquired a first episode of genital herpes near the onset of labor, and 34 (65 percent) had serologic evidence of asymptomatic reactivation of an already latent genital HSV infection. Of the 18 women with a first episode of disease, 5 (1 with HSV-1 and 4 with HSV-2) had virologic and serologic evidence of primary genital herpes. Of the 13 women with a nonprimary first episode of genital HSV in early labor, 12 had HSV-2 isolated at delivery, had only HSV-1 antibodies in the serum sample obtained on admission, and seroconverted to HSV-2 post partum, whereas 1 had HSV-1 isolated at delivery, had HSV-2 antibodies in the admission serum sample, and seroconverted to HSV-1 post partum. Among the 34 women with asymptomatic reactivation of HSV infection in early labor, 31 had reactivation of genital HSV-2 infection, and 3 of genital HSV-1. Of these 34 women, 21 (62 percent) reported a history of recurrent genital ulcerations but were without evidence of genital lesions or symptoms of HSV at the time of entry into the labor room, whereas 13 had no history of genital lesions but had HSV-2 antibodies in their initial serum sample and were shedding HSV-2 in early labor. HSV-2 was isolated from all four women for whom serum samples were not available; two of these four reported a history compatible with the presence of HSV. Thus, of the 54 women in whom both history and serologic results were obtained, 18 (33 percent) had a first episode and 36 a reactivation of HSV infection.
All 56 culture-positive mothers were in labor at the time of entry, and 44 (79 percent) had evidence of ruptured membranes when the HSV cultures were obtained. Vaginal delivery proceeded in 43 of the mothers and cesarean delivery in 13 (23 percent); all the cesarean sections were for obstetrical indications. The frequency of cesarean section after the onset of spontaneous labor was 39 percent (7 of 18) in the women with a first episode of disease as compared with 16 percent (6 of 38) in those with a reactivation of genital herpes.
None of the 56 patients with asymptomatic HSV shedding reported symptoms suggestive of genital HSV or had lesions identified by the examining clinician on admission to the labor unit. Genital lesions were noted during delivery in eight patients, however. All eight of these women delivered their infants vaginally and had subsequent evidence of HSV-2 antibodies in the serum sample obtained at enrollment; none transmitted the infection to their newborns (see below). During the immediate postpartum period, an additional four women had genital lesions.
Incidence and Transmission Rate of Neonatal HSV Infection
Neonatal herpes developed in 10 infants for an overall incidence of 1 case per 18,630 live births. All 10 cases occurred in the infants of the 15,923 women for whom cultures were obtained — 8 at the university and 2 at the community hospital. The incidence of neonatal herpes at the two hospitals was 1 per 1418 live births and 1 per 2291 live births, respectively. Among the 56 women who shed virus asymptomatically on admission to the labor unit, 7 transmitted HSV to their infants (12.5 percent). Three infants in whom neonatal herpes subsequently developed were born to women who had negative HSV cultures on admission to the labor unit (Table 1Table 1
Characteristics of 10 Infants with Neonatal Herpes Infection, According to the Results of Maternal HSV Cultures in Early Labor and Other Variables.). All three of these mothers had histories consistent with symptomatic recurrent genital herpes antedating pregnancy — one with genital HSV-1 and two with genital HSV-2. The times between the initial culture and delivery were similar for the culture-negative and the culture-positive mothers. The transmission rate of neonatal HSV among infants born to mothers with negative HSV cultures on admission to the labor unit was 0.02 percent (3 of 15,867). The sensitivity of a positive maternal HSV culture on admission to the labor unit was 70 percent (7 of 10) for identifying the infants who subsequently had neonatal HSV; the specificity was 99.7 percent (15,867 ÷ 15,913). The positive predictive value was 12.5 percent (7 of 56), and the negative predictive value 99.9 percent (15,864 ÷ 15,867).Frequency of HSV Transmission to Infants from Mothers with a Recent First Episode of Subclinical Genital Herpes
Neonatal HSV infection developed in 6 of the 18 infants (33 percent) born to mothers with serologic evidence of a first episode of genital HSV at term, as compared with 1 of 34 infants (3 percent) born to women who had subclinical reactivation of genital HSV at delivery (P<0.01) (Fig. 1). Neonatal herpes developed in 2 of the 5 HSV-exposed infants (40 percent) born to mothers with primary genital HSV, in 4 of the 13 such infants (31 percent) born to mothers with a nonprimary first episode of genital herpes, in 1 of the 21 infants (4.8 percent) of mothers with a history of recurrent symptomatic genital HSV, and in none of the 13 infants born to HSV-2—seropositive mothers with subclinical genital herpes. When only neonatal HSV-2 infections were evaluated, they were found in 5 of 16 infants (31 percent) of mothers with a first episode of HSV-2, as compared with none of 31 infants of mothers with a reactivation of HSV-2 (P<0.01). Among women with a first episode of genital HSV-2, the rate of transmission to the infant was similar between those with primary and those with nonprimary infection (1 of 4 vs. 4 of 12, respectively). Of the 31 women with a reactivation of HSV-2 at delivery, none transmitted infections to their infants. Fifteen of these women had only HSV-2 antibodies in their enrollment serum sample, whereas 16 had antibodies to both HSV-1 and HSV-2.
Association between Cervical HSV Shedding and Transmission to the Infant
Among the 56 women with asymptomatic HSV shedding, the virus was isolated only from the cervix in 10, from both the cervix and the labia in 12, and only from the labia in 34 (Table 2Table 2
Incidence of Neonatal HSV in the Infants of 56 Infected Mothers, According to Viral Type and Anatomical Site of Asymptomatic Viral Shedding in Early Labor.). Neonatal HSV occurred in 2 of 10 infants born to mothers who had shedding only from the cervix, in 4 of 12 infants of mothers who had shedding from both the cervix and the labia, and in 1 of 34 infants of mothers who had shedding only from the labia (P<0.01 for the comparison of transmission rates between mothers with shedding only from the cervix and those with shedding only from the labia). Overall, HSV was isolated from the cervix of six of the seven mothers with documented HSV shedding in early labor who gave birth to an infected infant. The seventh infant was born to a mother with a serologically documented nonprimary first episode of HSV-2 who had HSV-2 isolated from her cervix four days post partum, although only the cultures from the labia were positive at the time of admission. Of the 22 mothers with HSV isolated from the cervix, 5 had serologic evidence of a primary first infection, 7 had a nonprimary first episode, and 10 had a reactivation of disease.Association between Fetal-Scalp Electrodes and Acquisition of Neonatal HSV Infection
Fetal-scalp electrodes were applied to 8 of the 10 infants who had neonatal herpes. Among the infants whose mothers had HSV shedding at delivery, fetal scalp electrodes were used in all 7 in whom neonatal HSV developed, as compared with 23 of the 49 infants (47 percent) exposed to HSV-infected secretions during delivery but without neonatal herpes (P<0.01). When only infants with neonatal HSV-2 infection were considered, the corresponding figures were 5 of 5 as compared with 20 of 45 (P = 0.05). The duration of ruptured membranes was similar in the 6 infants in whom fetal-scalp monitors were used and in whom neonatal HSV subsequently developed and the 22 infants who were exposed but remained uninfected (8.9 and 10.3 hours, respectively). Six of the seven infants born to mothers who were culture-positive at delivery were also exposed to cervical HSV infection. Because of the association between such exposure and the use of fetal-scalp electrodes, the relative independence of these two risk factors for the acquisition of neonatal HSV could not be assessed. Of the four infants with neonatal HSV who subsequently had skin lesions, lesions on the scalp were noted in one.
Outcomes in Infants with Neonatal HSV Infection
All infants with neonatal HSV infection were treated.7 Of the seven neonates with HSV-2 infection, one had disseminated disease and died, five had encephalitis with or without the involvement of skin, eyes, or mucous membranes (only one of the five was normal, and four had moderate or severe developmental delays), and one had localized conjunctival infection and was developmentally normal. Thus, only two of the seven neonates with HSV-2 were developmentally normal (Table 1). All three infants with neonatal HSV-1 infection are alive at this writing and neurodevelopmentally intact, including one born to a mother with an asymptomatic primary genital HSV-1 infection. Overall, of the 10 infants with neonatal herpes, 5 are neurodevelopmentally normal at this writing, and 5 have died or are disabled.
Discussion
Our study provides several new observations about the transmission rates and risk factors associated with the acquisition of neonatal HSV infection. The HSV viral type, the mother's clinical stage of infection, the anatomical site of viral shedding, the use of fetal-scalp electrodes, and the specificity of passively transferred HSV antibodies from mother to infant all appeared to influence the transmission of HSV infection to the newborn. Overall, 0.35 percent of women who delivered live-born infants at our hospitals and had no signs or symptoms of HSV at that time shed HSV asymptomatically at the onset of labor, and approximately 1 in every 2000 live-born infants at these two hospitals had neonatal herpes. The overall transmission rate for HSV infection was 12.5 percent among the 56 women asymptomatically shedding HSV at term. Surprisingly, 35 percent of these women had serologic evidence of a recent subclinical first episode of genital HSV infection near the time of delivery. The rate of transmission of neonatal herpes was 10 times higher (33 percent) among the infants of women with recently acquired first episodes of genital infection than among those with reactivations of genital herpes (3 percent).
The passive transfer of maternal antibodies to HSV-2 but not to HSV-1 appeared to reduce the subsequent transmission of neonatal HSV-2 infection. None of the 31 infants born to mothers with reactivation of HSV-2 infection in early labor subsequently had neonatal herpes; these data are similar to those reported by Prober et al.19 In contrast, the rate of transmission of neonatal HSV-2 infection was 31 percent (5 of 16) among the women who shed HSV-2 at delivery but did not have HSV-2—specific antibodies in their initial serum samples. Others have suggested that the first episode of genital HSV infection in the mother near the time of delivery is associated with a higher rate of transmission of genital herpes.2 , 19 Our data show this conclusively. The rates of transmission of neonatal HSV were similar, however, in formerly seronegative women who had a subclinical first episode of primary HSV-2 (1 of 4) and in women who already had HSV-1 antibodies and had a subclinical first episode of nonprimary genital HSV-2 (4 of 13, or 31 percent). Investigations of male-to-female transmission of genital HSV-2 have suggested that previous HSV-1 infection appears to reduce the relative risk of HSV-2 infection by about half.10 In this study, however, we were unable to demonstrate a protective effect of the presence of HSV-1—specific antibodies. Whether these differences in the role of previous HSV-1 infection in horizontal as compared with vertical transmission are related to cross-protective cellular immune responses, differences in viral titers at exposed surfaces, or other factors requires further study. The passive transfer of antibodies to type-specific epitopes appears, however, to be the chief determinant of protection against the acquisition of neonatal disease. Passive immunization with HSV-2-specific antibodies or active immunization of the mother with an HSV-2—specific immunogen may be a potential therapeutic strategy to interrupt neonatal HSV infection.
Three of the 10 cases of neonatal HSV infection that we studied occurred among women who had negative HSV cultures at delivery. These false negative results were not due to a delay before the inoculation of the culture. All three cases involved women with a reactivation of infection who were likely to shed low titers of HSV. Whether improper sampling or improper storage occurred cannot be determined. These data indicate, however, that viral isolation has a sensitivity of only 70 percent for the identification of infants at risk of acquiring neonatal herpes. The overall negative predictive value of a viral culture is 99.9 percent, but it is not absolute. The development of a more rapid and specific technique of detecting asymptomatic cervical HSV secretion during labor would help in the overall clinical care of infants exposed to HSV infection at delivery.
Our study shows the complex epidemiology of neonatal herpes. Although the incidence of neonatal HSV in our study was 2 to 10 times higher than that estimated by others,5 , 20 , 21 the rate of asymptomatic shedding of HSV among the women entering our delivery rooms (0.35 percent) for whom cultures were obtained was essentially identical to the rates reported by others.22 23 24 The relatively high efficiency of HSV transmission to the infants in our study was due to the high proportion of women shedding HSV after a subclinical first episode of genital herpes at or near term. Other populations in which HSV shedding at delivery may be associated with a higher proportion of women with asymptomatic reactivation of latent HSV-2 may have similar or even higher rates of maternal shedding at the onset of labor but a lower subsequent incidence of neonatal HSV. Our data also suggest that strategies for preventing neonatal herpes are likely to vary according to the local epidemiology of genital herpes. It is interesting that despite demographic and socioeconomic differences between the two study hospitals, the frequency of asymptomatic shedding, the incidence of neonatal HSV, and the relative proportion of women with HSV shedding at labor who had a first episode of infection were relatively similar. In our area, where the rate of asymptomatic first-episode HSV infection in pregnancy is high, a strategy to identify mothers at risk of such infection during pregnancy appears necessary.25 One such approach involves assessing the HSV serologic status of pregnant women and their sexual partners early in the course of pregnancy. Women who are either HSV-seronegative or HSV-1—seropositive with HSV-2—seropositive partners could then be counseled about the need to avoid unprotected exposure in the latter half of pregnancy. In populations with a high rate of HSV-2 seroprevalance, screening pregnant women for HSV-2 and identifying those with reactivations of HSV-2 at delivery may be more useful.
In summary, the 31 percent rate of transmission of HSV-2 among exposed infants whose mothers do not have type-specific antibodies to HSV-2 suggests that these infants should be considered for prophylaxis with antiviral chemotherapy, passive immunoprophylaxis, or both. The rapid typing and serologic methods now available allow the identification of infants born to mothers who are HSV-seronegative and shedding either HSV-1 or HSV-2 in early labor or to mothers who shed HSV-2 and have only HSV-1 antibodies, or the reverse. The importance of preventing neonatal herpes is underscored by the fact that despite early identification and the prompt initiation of therapy, over half our infants with neonatal HSV-2 infection had severe neurologic disability or died. Since break-through infection has occurred in infants even after acyclovir prophylaxis, however, we believe that this area should be investigated actively before such a routine is initiated.26 , 27
Supported by a grant (AI-20381 ) from the National Institutes of Health and a grant from the March of Dimes Birth Defects Foundation.
We are indebted to Kathey Mohan, M.S.N., and Dana Griffin, B.S., for their help in following the mothers and HSV-exposed infants; to Ms. Joan Dragavon for her supervision of the large number of viral cultures required in the conduct of this trial; and to Samuel Ajl, Ph.D., and the March of Dimes Birth Defects Foundation for their continuing support of these studies.
Source Information
From the Departments of Obstetrics and Gynecology (Z.A.B., S. Berry, L.A.V.), Laboratory Medicine (R.A., S.S., L.C.), Medicine (L.C.), Pediatrics (S. Burchett), and Biostatistics (J.B.), University of Washington, and the Children's Hospital Medical Center, Seattle. Address reprint requests to Dr. Brown at RH-20, University of Washington, Seattle, WA 98195.
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