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19 - Immune maladaptation in the etiology of pre-eclampsia; an updated epidemiological perspective

from Part II - Clinical Practice

Published online by Cambridge University Press:  03 September 2009

By
Gus Dekker  and
Pierre Yves Robillard
Edited by
Fiona Lyall  and
Michael Belfort
Fiona Lyall
Affiliation:
University of Glasgow
Michael Belfort
Affiliation:
University of Utah
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Summary

Introduction

Shallow, endovascular cytotrophoblast invasion in the spiral arteries and endothelial cell dysfunction are two key features in the pathophysiology of pre-eclampsia (Roberts and Redman, 1993). However, the cause of pre-eclampsia remains unknown. In humans, organ transplants will be rejected if there are differences between donor and recipient with respect to histocompatibility complex genes, i.e. human leukocyte antigens. The feto-placental unit contains paternal antigens that are foreign to its maternal host. The concept that pre-eclampsia may be an immunologic disorder dates back to the beginning of the century (McQuarrrie, 1923; Medawar, 1953; Scott and Beer, 1976; Veit, 1902). In the early 1950s, Medawar (1953) proposed the concept of the “fetus as an allograft.” Since then it has been assumed that implantation of the fetal placenta would be controlled by a maternal immune response mediated by T cells recognizing paternally derived allo-antigens expressed by the placenta. Ongoing research in the last decade has shown that implantation might predominantly involve a novel allogenetic recognition system based on natural killer cells rather than T cells. Dr. Ashley Moffett's chapter provides a detailed overview of our current understanding on the immune biology and immune pathology of placentation as it relates to pre-eclampsia, with a focus on the important role of NK-cells.

In this chapter we aim to provide an up-to-date review on epidemiologic studies corroborating or refuting the hypothesis that maladaptation between the maternal immune system and the feto-placental allograft is involved in the etiology of pre-eclampsia.

Type
Chapter
Information
Pre-eclampsia
Etiology and Clinical Practice
 , pp. 276 - 294
Publisher: Cambridge University Press
Print publication year: 2007

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References

Antinori, S., Versaci, C., Panci, C., Caffa, B. and Gholami, G. H. (1995). Fetal and maternal morbidity and mortality in menopausal women aged 45–63 years. Hum. Reprod., 10, 464–9.CrossRefGoogle ScholarPubMed
Atkins, D. C., Baucom, D. H. and Jacobson, N. S. (2001). Understanding infidelity: correlates in a national random sample. J. Fam. Psychol., 15, 735–49.CrossRefGoogle Scholar
Basso, O., Christensen, K. and Olsen, J. (2001). Higher risk of pre-eclampsia after change of partner. An effect of longer interpregnancy intervals. Epidemiology, 12, 624–9.CrossRefGoogle ScholarPubMed
Basso, O., Weinberg, C. R., Baird, D. D., Wilcox, A. J. and Olsen, J. (2003). Danish National Birth Cohort. Subfecundity as a correlate of preeclampsia: a study within the Danish National Birth Cohort. Am. J. Epidemiol., 157, 195–202.CrossRefGoogle ScholarPubMed
Beer, A. E. and Need, J. A. (1985). Immunological aspects of preeclampsia/eclampsia. In Birth Defects: Original Article Series, ed. Young, B.K., chapter 21, New York, March of Dimes Birth Defects, pp. 131–54.Google Scholar
Cepicky, P. and Podrouzek, P. (1990). Barrier contraception increases the risk of pre-eclampsia. Cesk. Gynekol., 55, 620–1 (Czech).Google ScholarPubMed
Chen, G., Wilson, R., Wang, S. H., Zheng, H. Z., Walker, J. J. and McKillop, J. H. (1996). Tumour necrosis factor-alpha (TNF-α) gene polymorphism and expression in preeclampsia. Clin. Exp. Immunol., 104, 154–9.CrossRefGoogle Scholar
Chesley, L. C. (1978). Hypertensive Disorders in Pregnancy. New York, Appleton-Century Crofts.
Clark, D. A. (1993). Cytokines, decidua, and early pregnancy. Oxf. Rev. Reprod., 15, 83–111.Google ScholarPubMed
Clark, D. A. (1994). Does immunological intercourse prevent preeclampsia. Lancet, 344, 969–70.CrossRefGoogle Scholar
Conde-Agudelo, A. and Belizan, J. M. (2000). Maternal morbidity and mortality associated with interpregnancy interval: cross sectional study. Br. Med. J., 321, 1255–9.CrossRefGoogle ScholarPubMed
Dadelszen, P., Ornstein, M. P., Bull, S. B., Logan, A. G., Koren, G. and Magee, L. A. (2000). Fall in mean arterial pressure and fetal growth restriction in pregnancy hypertension: a meta-analysis. Lancet, 355, 87–92.CrossRefGoogle Scholar
Dekker, G. A. (1999). Risk factors for preeclampsia. Clin. Obstet. Gynecol., 42, 422–35.CrossRefGoogle ScholarPubMed
Dekker, G. A. (2002). The partner's role in the etiology of preeclampsia. J. Reprod. Immunol., 57, 203–15.CrossRefGoogle ScholarPubMed
Dekker, G. A. and Sibai, B. M. (1998). Etiology and pathogenesis of preeclampsia; current concepts. Am. J. Obstet. Gynecol., 179, 1359–75.CrossRefGoogle ScholarPubMed
Diekmann, W. J. (1952). The Toxemias of Pregnancy (2nd edn). St Louis, C. V. Mosby.Google Scholar
Einarsson, J. I., Sangi-Haghpeykar, H.. (2003). Sperm exposure and development of preeclampsia. Am. J. Obstet. Gynecol., 188, 1241–3.CrossRefGoogle ScholarPubMed
Eskenazia, B. and Harleyb, K. (2001). Perinatal epidemiology. Commentary: revisiting the primipaternity theory of pre-eclampsia. Int. J. Epidemiol., 30, 1323–4.CrossRefGoogle Scholar
Esplin, M. S., Fausett, M. B., Fraser, A., et al. (2001). Paternal and maternal components of the predisposition to preeclampsia. N. Engl. J. Med., 344, 867–72.CrossRefGoogle ScholarPubMed
Feeney, J. G. (1980). Pre-eclampsia and changing paternity. In Proceedings of the First Congress of the International Society for the Study of Hypertension in Pregnancy, ed. Bonnar, J., MacGillivray, I. and Symonds, M.. London: MTP Press Ltd, pp. 41–4.Google Scholar
Feeney, J. G. and Scott, J. S. (1980). Pre-eclampsia and changed paternity. Eur. J. Obstet. Gynecol. Reprod. Biol., 11, 35–8.CrossRefGoogle ScholarPubMed
Friedman, F. Jr., Copperman, A. B., Brodman, M. L., Shah, D., Sandler, B. and Grunfeld, L. (1996). Perinatal outcome after embryo transfer in ovum recipients: a comparison with standard in vitro fertilization. J. Reprod. Med. Obstet. Gynecol., 41, 640–4.Google ScholarPubMed
Goecke, C. and Schwabe, G. (1965). Vorschlag einer Stadien-Einteilung der Gestose. Zentralbl. Gynaekol., 87, 1439.Google Scholar
Grefenstette, I., Royere, D., Barthelemy, C. I., Tharanne, M. J. and Lansac, J. (1990). The outcome of 470 pregnancies obtained using AID with frozen semen. J. Gynecol. Obstet. Biol. Reprod., 19, 737–44.Google Scholar
Hall, G., Noble, W., Lindow, S. and Masson, E. (2001). Long-term sexual co-habitation offers no protection from hypertensive disease of pregnancy. Hum. Reprod., 16, 349–52.CrossRefGoogle ScholarPubMed
Hefler, L. A., Tempfer, C. B. and Gregg, A. R. (2001). Polymorphisms within the interleukin-1 beta gene cluster and preeclampsia. Obstet. Gynecol., 97, 664–8.Google ScholarPubMed
Hendler, I., Dulitzky, M., Soriano, D., et al. (1997). Pregnancy outcome after oocyte donation. Am. J. Obstet. Gynecol., 176, S133.CrossRefGoogle Scholar
Hernandez-Valencia, M., Saldana Quezada, L., Alvarez Munoz, M. and Valdez Martinez, E. (2000). Barrier family planning methods as risk factor which predisposes to preeclampsia. Ginecol. Obstet. Mex., 68, 333–8 (in Spanish).Google ScholarPubMed
Hiby, S. E., King, A., Sharkey, A.. (1999). Molecular studies of trophoblast HLA-G: polymorphisms, isoforms, imprinting and expression in preimplantation embryo. Tissue Antigens, 53, 1–13.CrossRefGoogle ScholarPubMed
Ikedife, D. (1980). Eclampsia in multiparae. Br. Med. J., 280, 985–6.CrossRefGoogle Scholar
Jivraj, S., Anstie, B., Cheong, Y. C., Fairlie, F. M., Laird, S. M. and Li, T. C. (2001). Obstetric and neonatal outcome in women with a history of recurrent miscarriage: a cohort study. Hum. Reprod., 16, 102–6.CrossRefGoogle ScholarPubMed
Koelman, C. A., Coumans, A. B., Nijman, H. W., Doxiadis, I. I. N., Dekker, G. A. and Claas, F. H. J. (2000). Correlation between oral sex and a low incidence of preeclampsia: a role for soluble HLA in seminal fluid? (Hypothesis.)J. Reprod. Med., 46, 155–66.Google Scholar
Khong, T. Y., Adema, E. D. and Erwich, J. J. (2003). On an anatomical basis for the increase in birth weight in second and subsequent born children. Placenta, 24, 348–53.CrossRefGoogle ScholarPubMed
Klonoff Cohen, H. S., Savitz, D. A., Cefalo, R. C. and McCann, M. F. (1989). An epidemiologic study of contraception and preeclampsia. J. Am. Med. Assoc., 262, 3143–7.CrossRefGoogle ScholarPubMed
Lachmeijer, A. M., Crusius, J. B., Pals, G., Dekker, G. A., Arngrímsson, R. and ten Kate, L. P. (2001). Polymorphisms in the tumor necrosis factor and lymphotoxin-alpha gene region and preeclampsia. Obstet. Gynecol., 98, 612–19.Google ScholarPubMed
Li, D.K. and Wi, S. (2000). Changing paternity and the risk of preeclampsia/eclampsia in the subsequent pregnancy. Am. J. Epidemiol., 151, 57–62.CrossRefGoogle ScholarPubMed
Lie, R. T., Rasmussen, S., Brunborg, H., Gjessing, H. K., Lie-Nielsen, E. and Irgens, L. M. (1998). Fetal and maternal contributions to risk of pre-eclampsia: a population based study. Br. Med. J., 316, 1343–7.CrossRefGoogle Scholar
Lucassen, A. and Parker, M. (2001). Revealing false paternity: some ethical considerations. Lancet, 357, 1033–5.CrossRefGoogle Scholar
Marti, J. J. and Herrmann, U. (1977). Immunogestosis: a new etiologic concept of “essential” EPH gestosis, with special consideration of the primigravid patient. Am. J. Obstet. Gynecol., 128, 489–93.CrossRefGoogle ScholarPubMed
Martin, R. D. (1996). Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol. Sci., 11, 149–56.Google Scholar
Marzi, M., Vigano, A., Trabattoni, D., et al. (1996). Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin. Exp. Immunol., 106, 127–33.CrossRefGoogle ScholarPubMed
McQuarrie, I. (1923). Isoagglutination in the new born infants and their mother: a possible relationship between interagglutination and the toxemias of pregnancy. Johns Hopkins Hosp. Bull., 34, 51–4.Google Scholar
MacGillivray, I. (1983). Pre-Eclampsia: The Hypertensive Disease of Pregnancy. London, Saunders.Google Scholar
Medawar, P. B. (1953). Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. In: Evolution 7. Society for Experimental Biology. New York: Academic Press, pp. 320–38.Google Scholar
Michalas, S., Loutradis, D., Drakakis, P., et al. (1996). Oocyte donation to women over 40 years of age: pregnancy complications. Eur. J. Obstet. Gynecol. Reprod. Biol., 64, 175–8.CrossRefGoogle ScholarPubMed
Mills, J. L., Klebanoff, M. A., Graubard, B. I., Carey, J. C. and Berendes, H. W. (1991). Barrier contraceptive methods and preeclampsia. J. Am. Med. Assoc., 265, 70–3.CrossRefGoogle ScholarPubMed
Moore, M. P. and Redman, C. W. (1983). Case-control study of severe pre-eclampsia of early onset. Br. Med. J. (Clin. Res. Ed.), 287, 580–3.CrossRefGoogle ScholarPubMed
Morcos, C. C., Bourguet, P. S. G., Prabcharan, O., et al. (2000). Pregnancy-induced hypertension and duration of sexual cohabitation. J. Reprod. Med., 45, 207–12.Google ScholarPubMed
Mosher, W. D. and Pratt, W. F. (1990). Contraceptive use in the United States, 1973–1988. Adv. Data, 182, 1–10.Google Scholar
Mosmann, T. R., Cherwinski, H. and Bond, M. W. (1986). Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol., 136, 2348–57.Google ScholarPubMed
Mosmann, T. R. and Moore, K. W. (1991). The role of Il-10 in cross-regulation of TH1 and TH2 responses. Immunol. Today, 12, 49.CrossRefGoogle Scholar
Mostello, D., Catlin, T. K., Roman, L., Holcomb, Jr. W. L. and Leet, T. (2002). Preeclampsia in the parous woman: who is at risk. Am. J. Obstet. Gynecol., 187, 425–9.CrossRefGoogle ScholarPubMed
Need, J. A. (1975). Pre-eclampsia in pregnancies by different fathers. Br. Med. J., ii, 548–9.CrossRef
Need, J. A., Bell, B., Meffin, E. and Jones, W. R. (1983). Pre-eclampsia in pregnancies from donor inseminations. J. Reprod. Immunol., 5, 329–38.CrossRefGoogle ScholarPubMed
Pados, G., Camus, M., Steirteghem, A., Bonduelle, M. and Devroey, P. (1994). The evolution and outcome of pregnancies from oocyte donation. Hum. Reprod., 9, 538–42.CrossRefGoogle ScholarPubMed
Pandian, Z., Bhattacharya, S. and Templeton, A. (2001). Review of unexplained infertility and obstetric outcome: a 10 year review. Hum. Reprod., 16, 2593–7.CrossRefGoogle ScholarPubMed
Perkins, R. P. (1993). Pregnancy following donor insemination: implications for preeclampsia. J. Matern. Fetal. Med., 2, 52–4.CrossRefGoogle Scholar
Roberts, J. M. and Redman, C. W. G. (1993). Pre-eclampsia: more than pregnancy-induced hypertension. Lancet, 341, 1447–51.CrossRefGoogle ScholarPubMed
Robertson, S. A. (2002). Transforming growth factor beta – a mediator of immune deviation in seminal plasma. J. Reprod. Immunol., 57, 109–28.CrossRefGoogle ScholarPubMed
Robertson, S. A., Bromfield, J. J. and Tremellen, K. P. (2003). Seminal ‘priming’ for protection from pre-eclampsia – a unifying hypothesis. J. Reprod. Immunol., 59, 253–65.CrossRefGoogle ScholarPubMed
Robillard, P. Y., Hulsey, T. C., Alexander, G. R., Keenan, A., Caunes, F. and Papiernik, E. (1993). Paternity patterns and risk of preeclampsia in the last pregnancy in multiparae. J. Reprod. Immunol., 24, 1–12.CrossRefGoogle ScholarPubMed
Robillard, P. Y., Hulsey, T. C., Perianin, J., Janky, E., Miri, E. H. and Papiernik, E. (1994). Association of pregnancy-induced hypertension with duration of sexual cohabitation before conception. Lancet, 344, 973–5.CrossRefGoogle ScholarPubMed
Robillard, P. Y., Dekker, G. A. and Hulsey, T. C. (1999). Revisiting the epidemiological standard of preeclampsia: primigravidity or primipaternity?Eur. J. Obstet. Gynecol. Reprod. Biol., 84, 37–41.CrossRefGoogle ScholarPubMed
Robillard, P. Y., Dekker, G. A. and Hulsey, T. C. (2002). Evolutionary adaptations to pre-eclampsia/eclampsia in humans: low fecundability rate, loss of oestrus, prohibitions of incest and systematic polyandry. Am. J. Reprod. Immunol., 47, 104–11.CrossRefGoogle ScholarPubMed
Robillard, P. Y., Hulsey, T. C., Dekker, G. A. and Chaouat, G. (2003). Preeclampsia and human reproduction. An essay of a long term reflection. J. Reprod. Immunol., 59, 93–100.CrossRefGoogle ScholarPubMed
Saftlas, A. F., Levine, R. J., Klebanoff, M. A., et al. (2003). Abortion, changed paternity, and risk of preeclampsia in nulliparous women. Am. J. Epidemiol., 157, 1108–14.CrossRefGoogle ScholarPubMed
Salha, O., Sharma, V., Dada, T., et al. (1999). The influence of donated gametes on the incidence of hypertensive disorders of pregnancy. Hum. Reprod., 14, 2268–73.CrossRefGoogle ScholarPubMed
Schenker, J. G. and Ezra, Y. (1994). Complications of assisted reproductive techniques. Fertil. Steril., 61, 411–22.CrossRefGoogle ScholarPubMed
Scott, J. R. and Beer, A. A. (1976). Immunologic aspects of pre-eclampsia. Am. J. Obstet. Gynecol., 125, 418–27.CrossRefGoogle ScholarPubMed
Serfaty, D. (1992). Medical aspects of oral contraceptive discontinuation. Adv. Contracept., 8, 21–33.CrossRefGoogle ScholarPubMed
Serhal, P. F. and Craft, I. (1987). Immune basis for pre-eclampsia: evidence from oocyte recipients. Lancet, ii, 744.CrossRefGoogle Scholar
Serhal, P. F. and Craft, I. L. (1989). Oocyte donation in 61 patients. Lancet, I, 1185–7.CrossRefGoogle Scholar
Skjaerven, R., Wilcox, A. J. and Lie, R. T. (2002). The interval between pregnancies and the risk of preeclampsia. New. Engl. J. Med., 346, 33–8.CrossRefGoogle ScholarPubMed
Smarason, A. K., Sargent, I. L., Starkey, P. M. and Redman, C. W. G. (1993). The effect of placental syncytiotrophoblast microvillous membranes from normal and pre-eclamptic women on the growth of endothelial cells in vivo. Br. J. Obstet. Gynaecol., 100, 943–9.CrossRefGoogle Scholar
Smith, G. N., Walker, M., Tessier, J. L. and Millar, K. G. (1997). Increased incidence of preeclampsia in women conceiving by intrauterine insemination with donor versus partner sperm for treatment of primary infertility. Am. J. Obstet. Gynecol., 177, 455–8.CrossRefGoogle ScholarPubMed
Soderstrom Anttila, V. and Hovatta, O. (1995). An oocyte donation program with goserelin down-regulation of voluntary donors. Acta Obstet. Gynecol. Scand., 74, 288–92.CrossRefGoogle ScholarPubMed
Strickland, D. M., Guzick, D. S., Cox, K., et al. (1986). The relationship between abortion in the first pregnancy and development of pregnancy-induced hypertension in the subsequent pregnancy. Am. J. Obstet. Gynecol., 154, 146–8.CrossRefGoogle ScholarPubMed
Tremellen, K. P., Seamark, R. F. and Robertson, S. A. (1998). Seminal transforming growth factor 1 stimulates granulocyte–macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol. Reprod., 58, 1217–25.CrossRefGoogle Scholar
Trogstad, L. I., Eskild, A., Magnus, P., Samuelsen, S. O. and Nesheim, B. I. (2001). Changing paternity and time since last pregnancy; the impact on pre-eclampsia risk. A study of 547238 women with and without previous pre-eclampsia. Int. J. Epidemiol., 30, 1317–22.CrossRefGoogle Scholar
Trupin, L. S., Simon, L. P. and Eskenazi, B. (1996). Change in paternity: a risk factor for preeclampsia in multiparas. Epidemiology, 7, 240–4.CrossRefGoogle ScholarPubMed
Tubbergen, A. M., Lachmeijer, S. M., Althuisius, M. E., Vlak, H. P., Geijn, H. and Dekker, G. A. (1999). Change in paternity: a risk factor for preeclampsia in multiparous women?J. Reprod. Immunol., 45, 81–8.CrossRefGoogle ScholarPubMed
Veit, J. (1902). Über Albuminurie in der Schwangerschaft. Ein Beitrag zur Physiologie der Schwangerschaft. Berliner Klin. Wchschr., 3, 513–16.Google Scholar
Verwoerd, G. R., Hall, D. R., Grove, D., Maritz, J. S. and Odendaal, H. J. (2002). Primipaternity and duration of exposure to sperm antigens as risk factors for pre-eclampsia. Int. J. Gynaecol. Obstet., 78, 121–6.CrossRefGoogle ScholarPubMed
Vries, M. J., Dekker, G. A. and Schoemaker, J. (1998). Higher risk of preeclampsia in the polycystic ovary syndrome. A case control study. Eur. J. Obstet. Gynecol. Reprod. Biol., 76, 91–5.CrossRef
Wang, J. X., Knottnerus, A. M., Schuit, G., Norman, R. J., Chan, A. and Dekker, G. A. (2002). Surgically obtained sperm, and risk of gestational hypertension and pre-eclampsia. Lancet, 359, 673–4.CrossRefGoogle ScholarPubMed
Watson, J. G., Carroll, J. and Chaykin, S. (1983). Reproduction in mice: the fate of spermatozoa not involved in fertilization. Gamete Res., 7, 75–84.CrossRefGoogle Scholar
Wegmann, T. G., Lin, H., Guilbert, L. and Mosmann, T. R. (1993). Bidirectional cytokine interactions in the maternal–fetal relationship: is successful pregnancy a Th2 phenomenon?Immunol. Today, 15, 353–6.CrossRefGoogle Scholar
Weiner, H. L., Friedman, A., Miller, A., et al. (1994). Oral tolerance: immunologic mechanisms and treatment of animal and human-organ specific autoimmune diseases by oral administration of autoantigens. Ann. Rev. Immunol., 12, 809–37.CrossRefGoogle ScholarPubMed
Westendorp, R. G. J., Langermans, J. A. M., Huizinga, T. W. J., et al. (1997). Genetic influence on cytokine production and fatal meningococcal disease. Lancet, 349, 170–3.CrossRefGoogle ScholarPubMed
Zavazava, N. and Kronke, M. (1996). sHLA class I molecules induce apoptosis in alloreactive cytotoxic T cells. Nat. Med., 2, 1005–11.CrossRefGoogle Scholar

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