AMERICAN JOURNAL OF REPRODUCTIVE IMMUNOLOGY 2:217-221 (19821
0271-7352/82/0204-0217$02.00 © 1982 ALAN R. LISS, INC.
Epstein-Barr Virus in Normal Pregnant Women*
KIYOSHI SAKAMOTO, JOHN GREALLY, ROBERT F. GILFILLAN, JULIANNE SEXTON, VANESSA BARNABEI, JOANNE YETZ,
THOMAS BECHTOLD, JANET K. SEELEY, EAMON O'DWYER, AND DAVID T. PURTILO
Departments of Pathology, University of Massachusetts, Worcester (K.S., J.S., VB., J.Y., T B., JK.S., D.T P.) and University of Nebraska Medical
Center, Omaha (K.S., J.Y., T B., D.T P.); Department of Pathology and Obstetrics and Gynecology, Galway Medical College, Republic of Ireland
(J.G., E.O'D.); Virology Laboratory, Massachusetts Department of Public Health, Boston (RF.G.); and Department of Pediatrics, University of
Connecticut Health Center, Farmington (J K.S.)
ABSTRACT: Acquired immune suppression accom-
panying normal pregnancy may be associated with
reactivation of Epstein-Barr virus (EBV). Pregnant
women with reactivated EBV having anti-EA anti-
bodies show high titers of antiviral capsid antigen
(VCA) geometric mean titers (GMT) of 522 versus 170
in those lacking anti--early antigen (EA). Among
twenty-seven seropositive women at parturition, 17
(63%) had generated antibody to EA, and all 27 (100%)
demonstrated significant increases in antibody to VCA
(p < 0.01). In contrast, antibody titers to cytomega-
lovirus, herpes hominis, varicella-zoster, and rubella
viruses in the pregnant women were comparable to
those found in nonpregnant controls. (Am J Reprod
Immunol. 1982; 2:217-221.)
Key words: Epstein-Barr virus, reactivation, pregnancy,
immune suppression.
INTRODUCTION
Cellular immunity in pregnant women is depressed as
is manifested by impaired lymphocyte responses to plant
mitogens and most microorganisms.
1
Multiple mecha-
nisms prevent rejection of the conceptus by the mother.l-"
Among these adaptive mechanisms, immune suppression
is a two-edged sword, protecting the fetus from immune
rejection but occasionally rendering the pregnant woman
vulnerable to infection. An increased morbidity and mor-
tality is observed in normal pregnant women to primary
infection by many viruses." Cytomegalovirus (CMV) and
herpes hominis can be associated with birth defects when
pregnant women become infected.v" The extent of another
herpesvirus, the ubiquitous Epstein-Barr virus (EBV) has
not been thoroughly studied during pregnancy.
EBV can: 1) infect and transform human B cells; 2)
induce lymphoma and mononucleosis in cotton-topped
marmosets; 3) cause infectious mononucleosis (1M)in hu-
mans; 4) persist in a chronically infected host in a latent
state; 5) produce life-threatening lymphoproliferative dis-
eases in immune--compromised patients; and 6) be asso-
ciated with Burkitt lymphoma and nasopharyngeal car-
cinoma (NPC).7-12 Our laboratory has demonstrated how
inherited and acquired immunodeficiency renders individ-
uals vulnerable to EBV-induced diseases.9-12 In a contin-
Submitted for publication February 11, 1982; accepted May 15, 1982.
"This work was supported in part by grant CA 23561 from the National Institutes
of Health, by the Lymphoproliferative Research Fund, and by a Burroughs-Wellcome
Travelling Grant.
Address reprint requests to David T. Purtilo, MD, Department of Pathology and
Laboratory Medicine, University of Nebraska Medical Center, 42nd and Dewey Avenue,
Omaha, NE 68105.
uation of these studies, we investigated the virus-host
interaction in apparently healthy pregnant women. In
studies described here, we provide evidence for reactiva-
tion of EBV during pregnancy by demonstration of anti-
body to early antigen (EA).
MATERIALS AND METHODS
To test the hypothesis that the immune suppression of
pregnancy can reactivate latent EBV infection in normal
pregnant women, we obtained with informed consent 15
ml of peripheral venous blood from 28 Irish women at
parturition and 5 to 10 ml of blood from the corresponding
umbilical cord of 27 of their newborns. Frozen sera ( - 20°C)
from 14 nonpregnant females of from 17 to 32 years of age
and 17 healthy males 19 to 41 years of age were assessed
for EBV antibody titers while 40 premarital women from
Massachusetts, ages 18 to 25, were used as controls for
antibody titers against cytomegalovirus, herpes hominis,
varicella-zoster, and rubella. Samplesfrom pregnant women
were frozen at -70°C until tested for EBV-specific anti-
bodies to EA, EB nuclear-associated antigen (EBNA), and
viral capsid antigen (VCA).
EBV-Specific Serology
Antibody titers of IgG anti-VCA,13 IgM anti-VCA,14
IgA anti-VCA,15 and anti-EA,16 including diffuse (D) and
restricted (R) components."? were determined by indirect
immunofluorescence. For detection of antibodies to VCA,
the P3HR-l cell line was maintained at 33°C for two weeks
in RPMI medium with 10% fetal calf serum (Microbiol-
ogical Associates, Bethesda, Md), 100 IUlml penicillin, and
100 umg/ml streptomycin (GlBCO, Grand Island, NY);
harvested; and fixed in acetone." Smears of these cultures
contained about 10% VCA-positive cells. Fluores-
cein--conjugated (FITC) antihuman IgG, IgA, and IgM
(heavy chain-specific) were obtained from Hyland Diag-
nostic Laboratories (Costa Mesa, Calif). Raji cells, exposed
to a high multiplicity of infection with P3HR-I-EBV, were
used for the anti-EA determinations: The virus concen-
tration was adjusted to yield 10% antigen-positive cells
after 48 h at 37°C in the presence or 20 ug/ml cytosine
arabinoside (Sigma, St. Louis, Mo), Raji cells, grown at
37°Cfor 3 to 4 days, were harvested and used for anti-EBNA
assays." FITC--conjugated caprine'antibody to human B1a/
B
1c
globulin (Hyland Laboratories) was used as a second
antibody and diluted 1:40 before use.
Viral Cultures of Throat Washings
A deep throat gargle was obtained from each mother,
who each gargled with 35 ml of RPMI-1640 for 3 min. The