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Prolonged Preterm Rupture of Fetal Membranes, a Consequence of an Increased Maternal Anti-Fetal T Cell Responsiveness

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Prolonged Preterm Rupture of Fetal Membranes, a Consequence of an Increased Maternal Anti-Fetal T Cell Responsiveness 0031-3998/05/5804-0648 PEDIATRIC RESEARCH Vol. 58, No. 4, 2005 Copyright © 2005 International Pediatric Research Foundation, Inc. Printed in U.S.A. Prolonged Preterm Rupture of Fetal Membranes, a Consequence of an Increased Maternal Anti-fetal T Cell Responsiveness ANDREA STEINBORN, EDGAR SCHMITT, YVONNE STEIN, ANDREAS KLEE, MARKUS GONSER, ERHARD SEIFRIED, AND CHRISTIAN SEIDL Department of Obstetrics and Gynecology [A.S., Y.S.], University of Frankfurt, 60590 Frankfurt/Main, Germany; Institute of Immunology [E.Sc.], University of Mainz, 55131 Mainz, Germany; Department of Obstetrics and Gynecology [A.K., M.G.], Dr. Horst-Schmidt Hospital, 65199 Wiesbaden, Germany; and Institute of Transfusion Medicine and Immunohaematology [E.Se., C.S.], Blood Transfusion Center of the German Red Cross, 60528 Frankfurt, Germany ABSTRACT A fetus, although semi-allogeneic, is usually accepted by the with women with uncontrollable preterm labor. Our results re- maternal immune system. However, complications, including vealed a strongly reduced allogeneic T cell response of PBMCs alloresponsive mechanisms, are thought to be potentially detri- from pregnant women that was further down-regulated when mental for a successful pregnancy. Therefore, we compared PBMCs from their own fetus were used as stimulators. By allogeneic T cell responses of nonpregnant women with the contrast, data from women with PPROM suggest an increased response of healthy pregnant women and pregnant women who maternal T cell response specifically toward the fetal HLA have various gestation-associated diseases. Peripheral blood antigens.(Pediatr Res 58: 648–653, 2005) mononuclear cells (PBMCs) of all three groups were stimulated with PBMCs from unrelated volunteers. Pregnant women had Abbreviations significantly reduced stimulation indices (SIs) compared with CTG, cardiotocogram nonpregnant women. Exposing PBMCs from pregnant women to HELLP, hemolysis, elevated liver enzymes, low platelet count PBMCs of their own fetus led to a further significant decrease of IUGR, intrauterine growth restriction SIs. Among the two groups of pregnant individuals, SIs of MLC, mixed lymphocyte culture women with prolonged preterm rupture of fetal membranes MMP, matrix metalloprotease (PPROM) were significantly higher when the maternal PBMCs PBMC, peripheral blood mononuclear cells were stimulated with PBMCs of their own fetus. This phenom- PL, preterm labor enon could not be observed after stimulation with PBMCs from PPROM, prolonged preterm rupture of fetal membranes unrelated volunteers. In addition, an increased humoral immune SI, stimulation index response was assessed for women with PPROM in comparison TNF, tumor necrosis factor During pregnancy the maternal immune system is con- nisms that act at the maternal–fetal interface to protect the fetus fronted with paternal allo-antigens expressed by the fetal tis- from maternal immune attack are known (1). In addition, sues. Therefore, maternal immune rejection processes toward mechanisms that induce peripheral immune tolerance to the fetal HLA antigens may represent a major cause of complica- fetus seem to be of equal if not of greater importance for tions, such as uncontrollable preterm labor (PL), prolonged successful course of pregnancy. preterm rupture of fetal membranes (PPROM), pregnancy- One such mechanism is most possibly the induction of induced hypertensive diseases [preeclampsia; hemolysis, ele- CD25ϩCD4ϩ T regulatory cells, a specialized T cell popula- vated liver enzymes, low platelets (HELLP) syndrome] or tion that was shown not only to suppress autoaggressive im- intrauterine growth restriction (IUGR). Several local mecha- mune responses (2) but also to prevent graft rejection as a result of induction of transplantation tolerance (3). Pregnancy- Received November 17, 2004; accepted February 11, 2005. induced expansion of these regulatory T cells occurs in both Correspondence: Andrea Steinborn, Ph.D., Department of Obstetrics and Gynecology, mice (4) and humans (5). These cells were able to suppress the University of Heidelberg Vo␤trasse 9, 69115 Heidelberg, Germany; e-mail: [email protected]. allogeneic T cell response directed against the fetus (4). Re- DOI: 10.1203/01.PDR.0000180541.03425.76 cently, it was reported that normal human pregnancy also is 648 MATERNAL T CELL RESPONSE AND PPROM 649 associated with an increased number of regulatory T cells in METHODS the maternal circulation (5). Other mediators that influence peripheral immune tolerance Participants in the mixed lymphocyte culture reaction study. This study are soluble HLA (sHLA) class I molecules. Soluble forms of was approved by the Regional Ethics Committee. Informed consent was obtained from all participants. From June 2002 until February 2003, EDTA HLA-A, -B, -C, and -G were shown to inhibit cytotoxic T cell plasma samples were collected from 96 healthy male or female volunteers, activity through CD8 ligation, leading to increased apoptosis who constituted the nonpregnant control group, and from 137 pregnant women by Fas/Fas-ligand interaction of these cells (6–8). Thus, in- in the third trimester. All pregnant women were classified into five different groups according to pregnancy complications and outcome. From these preg- creased availability of sHLA class I molecules may have strong nant women, both maternal and cord blood samples were consecutively immune-suppressive effects and affect potentially maternal collected immediately after delivery. Clinical characteristics of all of these immune homeostasis. Besides these nonspecific effects on the patients are detailed below and summarized in Table 1. As sufficient volumes of both maternal and fetal blood samples were necessary for the mixed immune response, sHLA class I molecules have specific effects lymphocyte culture (MLC) reaction studies, a period of 9 mo was needed to get on the allogeneic T cell response. These molecules induce the at least 10 patients per group. This study represents an explorative pilot study for which no previous knowledge exists. All experiments were done for the apoptosis of cytotoxic T lymphocytes through binding to their first time. Therefore, we were not able to do a sample size calculation to corresponding T cell receptors (9–11). Therefore, maternal calculate the expected number of patients that would be necessary to test for alloreactive T cells could be blocked by fetally derived sHLA the assessment of significant differences between groups. We finished our study after having recruited at least 10 patients per group and checked our class I molecules. By this way, the maternal T cell response results for significant differences of the patient groups as described below. directed specifically against the fetal HLA class I antigens is Group 1 consisted of 68 healthy women who delivered term neonates suppressed, whereas the T cell response against other unrelated (38–42 wk gestation) with normal birth weight, after the onset of spontaneous term labor (n ϭ 42) or elective cesarean section because of cephalopelvic allogeneic donors is not influenced. disproportion, breech presentation, repeated cesarean section, or fear of vaginal We show here that the alloreactive immune response toward birth (n ϭ 26). Group 2 consisted of 15 women who delivered preterm (25–37 wk gestation) because of uncontrollable PL associated with progressive dila- peripheral blood mononuclear cells (PBMCs) from healthy tion of the os uteri or fetal heart rate patterns necessitating immediate delivery adults was considerably reduced in pregnant compared with [pathologic cardiotocogram (CTG)]. For all of these women, rupture of fetal nonpregnant women. This alleviated response was further membranes occurred after the onset of labor, and latency from membrane rupture to delivery was Ͻ24 h in all cases. Depending on gestational age and strongly diminished when PBMCs that were isolated from the clinical symptoms, pregnancy was interrupted by cesarean section (n ϭ 7) or individual fetus were the targets. The same finding could be spontaneous delivery (n ϭ 8). observed in pregnant women who experience various gesta- Group 3 consisted of 20 women who delivered preterm (25–37 wk gesta- tion) with diagnosis of PPROM. This diagnosis was defined as spontaneous tion-associated diseases. An exception were women who had membrane rupture that occurred before the onset of labor. For all women in PPROM and exhibited a comparatively high alloresponse, this group, rupture of fetal membranes occurred at least 24 h before the onset of labor. Five of these women received labor-promoting drugs because fetal suggesting an increased anti-fetal reaction under these lung maturity was attained. Six patients delivered by cesarean section, and 14 conditions. women delivered spontaneously after the onset of labor. Table 1. Clinical characteristics and stimulation index (SI) of patients participating in the mixed lymphocyte culture (MLC) reaction study 1 4 Normal Term 2 3 Preeclampsia 5 Delivery PL PPROM HELLP IUGR n ϭ 68 n ϭ 15 n ϭ 20 n ϭ 22 n ϭ 12 Patient Group 38–42 weeks 28–37 weeks 30–37 weeks 25–41 weeks 38–42 weeks Preterm Labor 3/68 15/15 14/20 3/22 0/12 Prolonged rupture of 9/68 0/15 20/20 0/22 0/12 membranes Increased leukocyte count* 13/68 7/15 12/20 11/22 2/12 Increased CRP levels† 7/68 2/15 4/20 11/22 2/12 IUGR‡ 0/68 2/15 4/20 7/22 12/12 Hypertension§ 1/68 0/15 1/20 22/22 0/12 Proteinuria࿣ 0/68 1/15 1/20 22/22 0/12 Elevated liver enzymes¶ 0/68 0/15 0/20 6/22 0/12 Low platelet count** 2/68 1/15 0/20 7/22 1/12 SI (Control)
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