Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T05:58:36.630Z Has data issue: false hasContentIssue false
  • English
  • Français

Protozoan and helminth infections in pregnancy. Short-term and long-term implications of transmission of infection from mother to foetus

Published online by Cambridge University Press:  25 October 2007

ESKILD PETERSEN
ESKILD PETERSEN*
Affiliation:
Department of Infectious Diseases, Aarhus University Hospital, DK-8000 Aarhus, Denmark
*
*Corresponding author: Eskild Petersen, MD, DSc, DTM&H, Department of Infectious Diseases, Aarhus University Hospital, DK-8000 Aarhus, Denmark. Phone: +45 8949 8307. Fax: +45 8949 8310. E-mail: epf@sks.aaa.dk
Get access Rights & Permissions [Opens in a new window]

Summary

This review of protozoan and helminth infections in pregnancy focuses on the impact on the immune response in the newborn infant to maternal infection. Studies of protozoan and helminth infections in pregnant women and in their offspring have shown that children exposed to antigens or microorganisms during pregnancy often have a reduced immune response to these infections. The most common finding is a reduced IFNγ response to specific antigens regardless of specific infection studied. In some studies the impaired immune response disappeared before the age of one year, while in other studies the impaired immune response was present as much as two decades after birth. Data from chronic viral infections like Rubella, cytomegalovirus and hepatitis B also show that congenital or perinatal infections may result in a life-long inability to control the infections. Studies of both helminth and protozoan infections show that children exposed to antigens during gestation have a microorganism-specific impaired immune response which is characterized by reduced IFN-γ and stimulation of responses to specific antigens.

Keywords

Pregnancynewbornsprotective immunitytolerance protozoahelminth
Type
Research Article
Information
Parasitology , Volume 134 , Special Issue 13: PARASITES IN PREGNANCY , December 2007 , pp. 1855 - 1862
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abrams, E. T., Brown, H., Chensue, S. W., Turner, G. D. H., Tadesse, E., Lema, V. M., Molyneux, M. E., Rochford, R., Meshnick, S. R. and Rogerson, S. J. (2003). Host response to malaria during pregnancy: placental monocyte recruitment is associated with elevated β chemokine expression. Journal of Immunology 170, 2759–2764.CrossRefGoogle ScholarPubMed
Accapezzato, D., Francavilla, V., Paroli, M., Casciaro, M., Chircu, L. V., Cividini, A., Abrignani, S., Mondelli, M. U. and Barnaba, V. (2004). Hepatic expansion of a virus-specific regulatory CD8(+) T cell population in chronic hepatitis C virus infection. Journal of Clinical Investigation 113, 963–972.CrossRefGoogle ScholarPubMed
Adkins, B., Leclerc, C. and Marshall-Clarke, S. (2004). Neonatal adaptive immunity comes of age. Nature Reviews, Immunology 4, 553–564.CrossRefGoogle ScholarPubMed
Azogue, E., Fuente, C. LA and Darra, C. (1985). Congenital Chagas disease in Bolivia: epidemiological aspects and pathological findings. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 176–180.CrossRefGoogle ScholarPubMed
Baruch, D., Ma, X., Singh, H., Bi, X., Pasloske, B. and Howard, R. (1997). Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum-infected erythrocytes to CD36: conserved function with variant sequence. Blood 90, 3766–3775.CrossRefGoogle ScholarPubMed
Bittencourt, A. L. (1992). Possible risk factors for vertical transmission of Chagas disease. Revista Instituto Medicale Tropicale Sao Paulo 34, 403–408.CrossRefGoogle ScholarPubMed
Blacklock, B. and Gordon, R. M. (1925). Malaria infection as it occurs in late pregnancy, its relationship to labor and early infancy. Annals of Tropical Medicine and Parasitology 19, 327–365.CrossRefGoogle Scholar
Boutlis, C. S., Yeo, T. W. and Anstey, N. M. (2006). Malaria tolerance – for whom the cells toll? Trends in Parasitology 22, 371–377.CrossRefGoogle Scholar
Buimovici, E. and Cooper, L. Z. (1985). Cell-mediated response in Rubella infections. Reviews of Infectious Diseases 7 (Suppl. 1), S123–S128.CrossRefGoogle Scholar
Brabin, B. J. (1983). An analysis of malaria in pregnancy in Africa. Bulletin of the World Health Organization 61, 1005–1016.Google ScholarPubMed
Brabin, B. J., Brabin, L. R., Sapau, J. and Alpers, M. P. (1988). A longitudinal study of splenomegaly in pregnancy in a malaria endemic area in papua New Guinea. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 677–681.CrossRefGoogle Scholar
Brabin, B. J., Ginny, M., Sapau, J., Galme, K. and Paino, J. (1990). Consequences of maternal anaemia on outcome of pregnancy in a malaria endemic area in Papua New Guinea. Annals of Tropical Medicine and Parasitology 84, 11–24.CrossRefGoogle Scholar
Brake, D. A. (2003). Parasite and immune response. DNA and Cell Biology 22, 405–419.CrossRefGoogle Scholar
Bray, R. S. and Anderson, M. J. (1979). Falciparum malaria and pregnancy. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 427–431.CrossRefGoogle ScholarPubMed
Broen, K., Brustoski, K., Engelmann, I. and Luty, A. J. (2007). Placental Plasmodium falciparum infection: causes and consequences of in utero sensitization to parasite antigens. Molecular and Biochemical Parasitology 151, 1–8.CrossRefGoogle ScholarPubMed
Bruce-Chwatt, L. J. (1983). Malaria and pregnancy. British Medical Journal 286, 1457–1458.CrossRefGoogle ScholarPubMed
Brustoski, K., Moller, U., Kramer, M., Petelski, A., Brenner, S., Palmer, D. R., Bongartz, M., Kremsner, P. G., Luty, A. J. and Krzych, U. (2005). IFN-gamma and IL-10 mediate parasite-specific immune responses of cord blood cells induced by pregnancy-associated Plasmodium falciparum malaria. Journal of Immunology 174, 1738–1745.CrossRefGoogle ScholarPubMed
Brustoski, K., Moller, U., Kramer, M., Hartgers, F. C., Kremsner, P. G., Krzych, U. and Luty, A. J. (2006). Reduced cord blood immune effector-cell responsiveness mediated by CD4+ cells induced in utero as a consequence of placental Plasmodium falciparum infection. Journal of Infectious Diseases 193, 146–154.CrossRefGoogle ScholarPubMed
Buimovici-Klein, E. and Cooper, L. Z. (1985). Cell-mediated immune response in Rubella infections. Reviews of Infectious Diseases 7 (Suppl. 1), S123–S128.CrossRefGoogle ScholarPubMed
Cannon, D. S. H. (1958). Malaria and prematurity in the western region of Nigeria. British Medical Journal 2, 877–888.CrossRefGoogle ScholarPubMed
Clark, D. A. (1994). Microfilaria, tolerance, and T cells. Lancet 343, 868–869.CrossRefGoogle ScholarPubMed
Covell, G. (1950). Congenital malaria. Tropical Diseases Bulletin 47, 121–125.Google ScholarPubMed
Craig, A. and Scherf, A. (2001). Molecules on the surface of the Plasmodium falciparum-infected erythrocyte and their role in malaria pathogenesis and immune evasion. Molecular and Biochemical Parasitology 115, 129–143.CrossRefGoogle ScholarPubMed
Deloron, P., Dubois, B., Le Hasran, J. Y., Richie, D., Fievet, N., Cornet, M., Ringwald, P. and Cot, M. (1997). Isotypic analysis of maternally transmitted Plasmodium falciparum-specific antibodies in Cameroon, and relationship with risk of P. falciparum infection. Clinical and Experimental Immunology 110, 212–218.CrossRefGoogle ScholarPubMed
Desowitz, R. S. (1988). Prenatal immune priming in malaria: antigen-specific blastogenesis of cord blood lymphocytes from neonates born in a setting of holoendemic malaria. Annals of Tropical Medicine and Parasitology 82, 121–125.CrossRefGoogle Scholar
Desowitz, R. S. (1992). Placental Plasmodium falciparum parasitemia in East Sepik (Papua New Guinea) women of different parity: the apparent absence of acute effects on mother and foetus. Annals of Tropical Medicine and Parasitology 86, 95–102.CrossRefGoogle ScholarPubMed
Druilhe, P., Monjour, L. and Gentilini, M. (1976). Passage transplacentaire des antigènes solubles plasmodiaux. Induction d'une tolérance immuitaire spécifique. Presse Medicale 5, 1430–1431.Google Scholar
Dunn, D., Wallon, M., Peyron, F., Petersen, E., Peckham, C. and Gilbert, R. (1999). Mother-to-child transmission of toxoplasmosis: risk estimates for clinical counselling. Lancet 353, 1829–1833.CrossRefGoogle ScholarPubMed
Elson, L. H., Days, A., Calvopina, M., Paredes, W., Araujo, E., Guderian, R. H., Bradley, J. E. and Nutman, T. B. (1996). In utero exposure to Onchocerca volvulus: relationship to subsequent infection intensity and cellular immune responsiveness. Infection and Immunity 64, 5061–5065.CrossRefGoogle ScholarPubMed
Eynon, E. E. and Parker, D. C. (1993). Parameters of tolerance induction by antigen targeted to B lymphocytes. Journal of Immunology 151, 2958–2964.CrossRefGoogle ScholarPubMed
Fievet, N., Ringwald, P., Bickii, J., Dubois, B., Maubert, B., Hesran, J. Y. LE, Cot, M. and Deloron, P. (1996). Malaria cellular immune response in neonates from Cameroun. Parasite Immunology 18, 483–490.CrossRefGoogle Scholar
Fried, M., Nosten, F., Brockman, A., Brabin, B. J. and Duffy, P. E. (1998). Maternal antibodies block malaria. Nature 395, 851–852.CrossRefGoogle ScholarPubMed
Fried, M., Muga, R. O., Misore, A. O. and Duffy, P. E. (1998). Malaria elicts type 1 cytokines in the human placenta: IFN-γ and TNF-α associated with pregnancy outcomes. Journal of Immunology 160, 2523–2530.CrossRefGoogle Scholar
Ganem, D. and Prince, A. M. (2004). Hepatitis B virus infection – natural history and clinical consequences. New England Journal of Medicine 350, 1118–1129.CrossRefGoogle ScholarPubMed
Garweg, J. G., Scherrer, J., Wallon, M., Kodjikian, L. and Peyron, F. (2005). Reactivation of ocular toxoplasmosis during pregnancy. British Journal of Obstetrics and Gynaecology 112, 241–242.CrossRefGoogle ScholarPubMed
Gilles, H. M., Lawson, J. B., Sibelas, M., Voller, A. and Allan, N. (1969). Malaria, anemia and pregnancy. Annals of Tropical Medicine and Parasitology 63, 245–263.CrossRefGoogle Scholar
Gras, L., Wallon, M., Pollak, A., Cortina-Borja, M., Evengard, B., Hayde, M., Petersen, E. and Gilbert, R. for the European Multicenter Study on Congenital Toxoplasmosis (2005). Association between prenatal treatment and clinical manifestations of congenital toxoplasmosis in infancy: a cohort study in 13 European centres. Acta Paediatrica 94, 1721–1731.CrossRefGoogle ScholarPubMed
Gürtler, R. E., Segura, E. L. and Cohen, J. E. (2003). Congenital transmission of Trypanosoma cruzi infection in Argentina. Emerging Infectious Diseases 9, 29–32.CrossRefGoogle ScholarPubMed
Guglietta, S., Beghetto, E., Spadoni, A., Buffolano, W., del Porto, P. and Gargano, N. (2007). Age-dependent impairment of functional helper T cell responses to immunodominant epitopes of Toxoplasma gondii antigens in congenitally infected individuals. Microbes and Infection 9, 127–133.Google ScholarPubMed
Hang, L. M., Boros, D. L. and Warren, K. S. (1974). Induction of immunological hyporesponsiveness to granulomatous hypersensitivity in Schistosoma mansoni infection. Journal of Infectious Diseases 130, 515–522.CrossRefGoogle ScholarPubMed
Hara, T., Ohashi, S., Yamashita, Y., Abe, T., Hisaeda, H., Himemo, K., Good, R. A. and Takeshita, K. (1996). Human Vδ2+ γδ T-cell tolerance to foreign antigens of Toxoplasma gondii. Proceedings of the National Academy of Sciences, USA 93, 5136–5140.CrossRefGoogle ScholarPubMed
Hermann, E., Truyens, C., Alonso-Vega, C., Even, J., Rodriguez, P., Berthe, A., Gonzalez-Merino, E., Torrico, F. and Carlier, Y. (2002). Human fetuses are able to mount an adultlike CD8 T-cell response. Blood 100, 2153–2158.CrossRefGoogle ScholarPubMed
Hermann, E., Alonso-Vega, C., Berthe, A., Truyens, C., Flores, A., Cordova, M., Moretta, L., Torrico, F., Braud, V. and Carlier, Y. (2006). Human congenital infection with Trypanosoma cruzi induces phenotypic and functional modifications of cord blood NK cells. Pediatric Research 60, 38–43.CrossRefGoogle ScholarPubMed
Hohlfeld, P., Forestier, F., Marion, S., Thulliez, P., Marcon, P. and Daffos, F. (1990). Toxoplasma gondii infection during pregnancy: T lymphocyte subpopulations in mothers and fetuses. Pediatric Infectious Diseases Journal 9, 878–881.CrossRefGoogle ScholarPubMed
Hui, C.-K. and Lau, G. K. K. (2005). Immune system and hepatitis B virus infection. Journal of Clinical Virology 34 (Suppl. 1), S44–S48.CrossRefGoogle ScholarPubMed
Ismaili, J., van der Sande, M., Holland, M. J., Sambou, I., Keita, S., Allsopp, C., Ota, M. O., McAdam, K. P. and Pinder, M. (2003). Plasmodium falciparum infection of the placenta affects newborn immune responses. Clinical and Experimental Immunology 133, 414–421.CrossRefGoogle ScholarPubMed
King, C. L., Malhotra, I., Wamachi, A., Kioko, J., Mungai, P., Wahab, S. A., Koech, D., Zimmerman, P., Ouma, J. and Kazura, J. W. (2002). Acquired immune responses to Plasmodium falciparum merozoite surface protein-1 in the human fetus. Journal of Immunology 168, 356–364.CrossRefGoogle ScholarPubMed
Kirch, A. K., Duerr, H. P., Boatin, B., Alley, W. S., Hoffmann, W. H., Schulz-Key, H. and Soboslay, P. T. (2003). Impact of parental onchocerciasis and intensity of transmission on development and persistence of Onchocerca volvulus infection in offspring: an 18 year follow-up study. Parasitology 127, 327–335.CrossRefGoogle ScholarPubMed
Lammie, P. J., Hitch, W. L., Allen, E. M. W., Hightower, W. and Eberhard, M. L. (1991). Maternal filarial infection as risk factor for infection in children. Lancet 337, 1005–1006.CrossRefGoogle ScholarPubMed
Larkin, G. L. and Thuma, P. E. (1991). Congenital malaria in a hyperendemic area. American Journal of Tropical Medicine and Hygiene 45, 587–592.CrossRefGoogle Scholar
Le Hasran, J. Y., Cot, M., Personne, P., Fievet, N., Dubois, B., Beyemé, M., Boudin, C. and Deloron, P. (1997). Maternal placental infection with Plasmodium falciparum and malaria morbidity during the first 2 years of life. American Journal of Epidemiology 146, 826–831.CrossRefGoogle Scholar
Lewert, R. E. and Mandlowitz, S. (1969). Schistosmiasis. Prenatal induction of tolerance to antigens. Nature 224, 1029–1030.CrossRefGoogle Scholar
Lok, A. S., McMahon, B. J. and the Practice Guidelines Committee, American Association for the Study of Liver Diseases (2001). Chronic hepatitis B. Hepatology 34, 1225–1241.CrossRefGoogle ScholarPubMed
Maizels, R. M. and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733–744.CrossRefGoogle ScholarPubMed
Malhotra, I., Mungai, P., Wamachi, A., Kioko, J., Ouma, J. H., Kazura, J. W. and King, C. L. (1999). Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. Journal of Immunology 162, 6843–6848.CrossRefGoogle ScholarPubMed
Malhotra, I., Mungai, P., Muchiri, E., Ouma, J., Sharma, S., Kazura, J. W. and King, C. L. (2005 a). Distinct Th1- and Th2-Type prenatal cytokine responses to Plasmodium falciparum erythrocyte invasion ligands. Infection and Immunity 73, 3462–3470.CrossRefGoogle ScholarPubMed
Malhotra, I., Ouma, J. H., Wamachi, A., Kioko, J., Mungai, P., Njzovu, M., Kazura, J. W. and King, C. L. (2005 b). Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infection and Immunity 71, 5231–5237.CrossRefGoogle Scholar
Malhotra, I., Mungai, P. L., Wamachi, A. N., Tisch, D., Kioko, J. M., Ouma, J. H., Muchiri, E., Kazura, J. W. and King, C. L. (2006). Prenatal T cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood. Journal of Infectious Diseases 193, 1005–1013.CrossRefGoogle ScholarPubMed
Marchant, A., Appay, V., Sande M., VAN DER, Dulphy, N., Liesnard, C. and Kidd, M. (2003). Mature CD8+ T lymphocyte response to viral infection during fetal life. Journal of Clinical Investigation 111, 1747–1755.CrossRefGoogle ScholarPubMed
McDermott, J. M., Wirima, J. J., Steketee, R. W., Breman, J. G. and Heymann, D. L. (1996). The effect of placental malaria infection on perinatal mortality in rural Malawi. American Journal of Tropical Medicine and Hygiene 55 (Suppl. 1), 61–65.CrossRefGoogle ScholarPubMed
McGregor, I. A. (1984). Epidemiology, malaria and pregnancy. American Journal of Tropical Medicine and Hygiene 33, 517–525.CrossRefGoogle ScholarPubMed
McLeod, R., Beem, O. M. and Estes, R. G. (1985). Lymphocyte anergy specific to Toxoplasma gondii in a baby with congenital toxoplasmosis. Journal of Clinical Laboratory Immunology 17, 149–153.Google Scholar
Menendez, C., Ordi, J., Ismail, M. R., Ventura, P. J., Aponte, J. J., Kahigwa, E., Font, F. and Alonso, P. L. (2000). The impact of placental malaria on gestational age and birth weight. Journal of Infectious Diseases 181, 1740–1745.CrossRefGoogle ScholarPubMed
Miller, M. J. (1958). Observations of the natural history of malaria in the semi-resistant west African. Transactions of the Royal Society of Tropical Medicine and Hygiene 52, 152–168.CrossRefGoogle ScholarPubMed
Mora, M. C., Sanchez-Negrette, O., Marco, D., Barrio, A., Ciaccio, M., Segura, M. A. and Basombrio, M. A. (2005). Early diagnosis of congenital Trypanosoma cruzi infection using PCR, hemoculture, and capillary concentration, as compared with delayed serology. Journal of Parasitology 91, 1468–1473.CrossRefGoogle ScholarPubMed
Moormann, A. M., Sullivan, A. D., Rochford, R. A., Chensue, P. J., Bock, P. J., Nyirenda, T. and Meshnik, S. R. (1999). Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. Journal of Infectious Diseases 180, 1987–1993.CrossRefGoogle ScholarPubMed
Mutabingwa, T. K., Bolla, M. C., Li, J. L., Domingo, G. J., Li, X., Fried, M. and Duffy, P. E. (2005). Maternal malaria and gravidity interact to modify infant susceptibility to malaria. Public Library of Science Medicine 2, 1260–1268.Google ScholarPubMed
Negrette, O. S., Mora, M. C. and Basombrio, M. A. (2005). High prevalence of congenital Trypanosoma cruzi infection and family clustering in Salta, Argentina. Pediatrics 115, e668–672.CrossRefGoogle Scholar
Neves, S. F., Eloi-Santos, S., Ramos, R., Rigueirinho, S., Gazzinelli, G. and Correa-Oliveira, R. (1999). In utero sensitization in Chagas' disease leads to altered lymphocyte phenotypic patterns in the newborn cord blood mononuclear cells. Parasite Immunology 21, 631–639.CrossRefGoogle ScholarPubMed
Nossal, G. J. V., Karvelas, M. and Pulendran, B. (1993). Soluble antigen profoundly reduces memory B-cell numbers even when given after challenge immunization. Proceedings of the National Academy of Sciences, USA 90, 3088–3092.CrossRefGoogle ScholarPubMed
Nosten, F., ter-Kuile, F., Maelankirri, L., Decludt, B. and White, N. J. (1991). Malaria during pregnancy in an area of unstable endemicity. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 424–429.CrossRefGoogle Scholar
Ordi, J., Ismail, M. R., Ventura, P. J., Kahigwa, E., Hirt, R., Cardesa, A., Alonso, P. L. and Menendez, C. (1998). Massive chronic intervillositis of the placenta associated with malaria infection. American Journal of Surgery and Pathology 22, 1006–1011.CrossRefGoogle ScholarPubMed
Ou, D., Chong, P., Tingle, A. J. and Gillam, S. (1993). Mapping T-cell epitopes of Rubella virus structural proteins E1, E2 and C recognized by T-cell lines and clones derived from infected and immunized populations. Journal of Medical Virology 40, 175–183.CrossRefGoogle Scholar
Petersen, E., Høgh, B., Marbiah, N. T., David, K. and Hanson, A. P. (1991). Development of immunity against Plasmodium falciparum malaria: Clinical and parasitological malaria can not be separated. Journal of Infectious Diseases 164, 149–153.CrossRefGoogle Scholar
Pouvelle, B., Buffet, P. A., Lepolard, C., Scherf, A. and Gysin, J. (2000). Cytoadherence of Plasmodium falciparum ring-stage-infected erythrocytes. Nature Medicine 6, 1264–1268.CrossRefGoogle Scholar
Ridge, J. P., Fuchs, E. J. and Matzinger, P. (1996). Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science 271, 1723–1726.CrossRefGoogle ScholarPubMed
Riecke, C. H., Staalsoe, T., Koram, K., Akanmori, B. D., Riley, E. M., Theander, T. G. and Hviid, L. (2000). Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulphate A. Journal of Immunology 163, 3309–3316.CrossRefGoogle Scholar
Rogerson, S. J., Pollina, E., Getachew, A., Tadesse, E., Lema, V. M. and Molyneux, M. E. (2003). Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. American Journal of Tropical Medicine and Hygiene 68, 115–119.CrossRefGoogle ScholarPubMed
Schenone, H., Gaggero, M., Sapunar, J., Contreras M. C., DEL and Rojas, A. (2001). Congenital Chagas disease of second generation in Santiago, Chile. Report of two cases. Revista Instituto Medicale e Tropicale Sao Paulo 43, 231–232.CrossRefGoogle ScholarPubMed
Schleiss, M. R. (2006). The role of the placenta in the pathogenesis of congenital cytomegalovirus infection: is the benefit of cytomegalovirus immune globulin for the newborn mediated through improved placental health and function? Clinical Infectious Diseases 43, 1001–1003.Google ScholarPubMed
Soboslay, P. T., Geiger, S. M., Drabner, B., Banla, M., Batchassi, E., Kowu, L. A., Stadler, A. and Schulz-Key, H. (1999). Prenatal immune priming in onchocerciasis-Onchocerca volvulus-specific cellular responsiveness and cytokine production in newborns from infected mothers. Clinical and Experimental Immunology 117, 130–137.CrossRefGoogle ScholarPubMed
Stagno, S., Pass, R. F., Dworsky, M. E. and Alford, C. A. Jr (1982). Maternal cytomegalovirus infection and perinatal transmission. Clinical Obstetrics and Gynecology 25, 563–576.CrossRefGoogle ScholarPubMed
Steel, C., Guinea, A., McCarthy, J. and Ottesen, E. A. (1994). Long-term effect of prenatal exposure to maternal microfilaremia on immune responsiveness to filarial parasite antigens. Lancet 343, 890–893.CrossRefGoogle Scholar
Stekete, R. W., Wirima, J. J., Hightower, A. W., Slutsker, L., Heymann, D. L. and Breman, J. G. (1996). The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity and interuterine growth retardation in rural Malawi. American Journal of Tropical Medicine and Hygiene 55, 33–41.CrossRefGoogle Scholar
Su, X. Z., Heatwole, V. M., Wertheimer, S. P., Guinet, F., Herrfeldt, J. A., Peterson, D. S., Ravetch, J. A. and Wellems, T. E. (1995). The large diverse family of var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected eythrocytes. Cell 82, 89–100.CrossRefGoogle Scholar
Tachon, P. and Borojevic, R. (1978). Mother-child relation in human schistosomiasis mansoni: skin test and cord blood reactivity to schistosomal antigens. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 605–609.CrossRefGoogle ScholarPubMed
Tobian, A. A., Mehlotra, R. K., Malhotra, I., Wamachi, A., Mungai, P., Koech, D., Ouma, J., Zimmerman, P. and King, C. L. (2000). Frequent umbilical cord-blood and maternal-blood infections with Plasmodium falciparum, P. malariae, and P. ovale in Kenya. Journal of Infectious Diseases 182, 558–563.CrossRefGoogle ScholarPubMed
Torre, R. L., Nigro, G., Mazzocco, M., Best, A. M. and Adler, S. P. (2006). Placental enlargement in women with primary maternal cytomegalovirus infection is associated with fetal and neonatal disease. Clinical Infectious Diseases 43, 994–1000.CrossRefGoogle ScholarPubMed
Torrico, F., Vega, C. A., Suarez, E., Tellez, T., Brutus, L., Rodriguez, P., Torrico, M. C., Schneider, D., Truyens, C. and Carlier, Y. (2006). Are maternal re-infections with Trypanosoma cruzi associated with higher morbidity and mortality of congenital Chagas disease? Tropical Medicine and International Health 11, 628–635.Google ScholarPubMed
Urban, B. C., Ferguson, D. J., Pain, A., Willcox, N., Plebanski, M., Austyn, J. M. and Roberts, D. J. (1999). Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400, 73–77.CrossRefGoogle ScholarPubMed
Vekemans, J., Truyens, C., Torrico, F., Solano, M., Torrico, M. C., Rodriguez, P., Alonso-Vega, C. and Carlier, Y. (2000). Maternal Trypanosoma cruzi infection upregulates capacity of uninfected neonate cells to produce pro- and anti-inflammatory cytokines. Infection and Immunity 68, 5430–5434.Google ScholarPubMed
Wallon, M., Kodjikian, L., Binquet, C., Garweg, J., Fleury, J., Quantin, C. and Peyron, F. (2004). Long-term ocular prognosis in 327 children with congenital toxoplasmosis. Pediatrics 113, 1567–1572.CrossRefGoogle ScholarPubMed
Weil, G. J., Hussain, R., Kumaraswami, V., Phillips, K. S. and Ottesen, E. A. (1983). Prenatal allergic sensitization to helminth antigens in offspring of parasite-infected mothers. Journal of Clinical Investigation 71, 1124–1129.CrossRefGoogle ScholarPubMed
Wilson, M. S. and Maizels, R. M. (2006). Regulatory T cells induced by parasites and the modulation of allergic responses. In Parasites and Allergy (ed. Capron, M. & Trottein, F.), pp. 176–195. Karger, Basel.Google Scholar
Yamada, M., Stekete, R., Abramowsky, C., Kida, M., Wirima, J., Heymann, D., Rabbege, J., Breman, J. and Aitkawa, M. (1989). Plasmodium falciparum-associated placental pathology: a light and electron microscopic and immunohistologic study. American Journal of Tropical Medicine and Hygiene 41, 161–168.CrossRefGoogle Scholar
Yamamoto, J. H., Vallochi, A. L., Silveira, C., Filho, J. K., Nussenblatt, R. B., Cunha-Neto, E., Gazzinelli, R. T., Belfort, R. Jr and Rizzo, L. V. (2000). Discrimination between patients with acquired toxoplasmosis and congenital toxoplasmosis on the basis of the immune response to parasite antigens. Journal of Infectious Diseases 181, 2018–2022.CrossRefGoogle ScholarPubMed
Xi, G., Leke, R. G., Thuita, L. W., Zhou, A., Leke, R. J., Mbu, R. and Taylor, D. W. (2003). Congenital exposure to Plasmodium falciparum antigens: prevalence and antigenic specificity of in utero-produced antimalarial immunoglobulin M antibodies. Infection and Immunity 71, 1242–1246.CrossRefGoogle ScholarPubMed