Abstract
Chronic helminth infections are highly prevalent in many parts of the world and a considerable infection rate during pregnancy has been reported. It is becoming clear that the development of the fetal immune system and the immune responses to homologous and possibly even heterologous antigens later in life is already determined in utero. The contributing factors and mechanisms are still under investigation. However, studies have demonstrated that maternal helminth infection can influence susceptibility to a homologous infection during childhood without previous fetomaternal transmission of the infectious agent itself during pregnancy. Whether this is caused e.g. by chronic maternal immune responses (cells or cytokines) such as immuneregulation or transmission of helminth derived antigen/proteins, and furthermore which developmental stage of the offspring’s immune system is affected by such factors e.g. in an epigenetic manner and finally, what clinical implications these results have regarding vaccination strategies, needs to be investigated in the future.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Woodburn PW et al (2009) Risk factors for helminth, malaria, and HIV infection in pregnancy in Entebbe, Uganda. PLoS Negl Trop Dis 3:e473
Adegnika AA et al (2010) Epidemiology of parasitic co-infections during pregnancy in Lambarene, Gabon. Trop Med Int Health 15:1204–1209
van Eijk AM et al (2009) Geohelminth Infections among pregnant women in rural western Kenya; a cross-sectional study. PLoS Negl Trop Dis 3:e370
Hillier SD et al (2008) Plasmodium falciparum and helminth coinfection in a semi urban population of pregnant women in Uganda. J Infect Dis 198:920–927
Kramer MS (2003) The epidemiology of adverse pregnancy outcomes: an overview. J Nutr 133:1592S–1596S
Steketee RW (2003) Pregnancy, nutrition and parasitic diseases. J Nutr 133:1661S−1667S
Barker DJ (2006) Adult consequences of fetal growth restriction. Clin Obstetr Gynecol 49:270–283
Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61–73
Ndibazza J et al (2010) Effects of deworming during pregnancy on maternal and perinatal outcomes in Entebbe, Uganda: a randomized controlled trial. Clin Infect Dis 50:531–540
Navitsky RC et al (1998) Ancylostoma duodenale is responsible for hookworm infections among pregnant women in the rural plains of Nepal. J Parasitol 84:647–651
Brooker S, Hotez PJ, Bundy DA (2008) Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl Trop Dis 2:e291
Christian P, Khatry SK, West KP Jr (2004) Antenatal antihelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364:981–983
Larocque R et al (2006) A double-blind randomized controlled trial of antenatal mebendazole to reduce low birthweight in a hookworm-endemic area of Peru. Trop Med Int Health 11:1485–1495
Fairley JK et al (2013) Birthweight in offspring of mothers with high prevalence of helminth and malaria infection in coastal Kenya. Am J Trop Med Hyg 88:48–53
Yatich NJ et al (2010) The effect of malaria and intestinal helminth coinfection on birth outcomes in Kumasi, Ghana. Am J Trop Med Hyg 82:28–34
Gallagher M et al (2005) The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS 19:1849–1855
Secor WE et al (2003) Increased density of human immunodeficiency virus type 1 coreceptors CCR5 and CXCR4 on the surfaces of CD4+ T cells and monocytes of patients with Schistosoma mansoni infection. Infect Immun 71:6668–6671
Gotuzzo E et al (2007) Frequent HTLV-1 infection in the offspring of Peruvian women with HTLV-1-associated myelopathy/tropical spastic paraparesis or strongyloidiasis. Rev Panam Salud Publica 22:223–230 (Pan Am J Public Health)
Egwunyenga AO, Ajayi JA, Nmorsi OP, Duhlinska-Popova DD (2001) Plasmodium/intestinal helminth co-infections among pregnant Nigerian women. Mem Inst Oswaldo Cruz 96:1055–1059
Chizzolini C, Trottein F, Bernard FX, Kaufmann MH (1991) Isotypic analysis, antigen specificity, and inhibitory function of maternally transmitted Plasmodium falciparum-specific antibodies in Gabonese newborns. Am J Trop Med Hyg 45:57–64
Brair ME, Brabin BJ, Milligan P, Maxwell S, Hart CA (1994) Reduced transfer of tetanus antibodies with placental malaria. Lancet 343:208–209
Desai M et al (2007) Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7:93–104
Okoko BJ et al (2001) The influence of placental malaria infection and maternal hypergammaglobulinemia on transplacental transfer of antibodies and IgG subclasses in a rural West African population. J Infect Dis 184:627–632
Labeaud AD, Malhotra I, King MJ, King CL, King CH (2009) Do antenatal parasite infections devalue childhood vaccination? PLoS Negl Trop Dis 3:e442
Bassily S et al (1997) Immunogenicity of recombinant hepatitis B vaccine among infants of mothers with active schistosomiasis. Am J Trop Med Hyg 57:197–199
Ghaffar YA, Kamel M, el-Sobky M, Bahnasy R, Strickland GT (1989) Response to hepatitis B vaccine in infants born to mothers with schistosomiasis. Lancet 2:272
Elliott AM et al (2010) Effects of maternal and infant co-infections, and of maternal immunisation, on the infant response to BCG and tetanus immunisation. Vaccine 29:247–255
Webb EL et al (2011) Effect of single-dose antihelmintic treatment during pregnancy on an infant’s response to immunisation and on susceptibility to infectious diseases in infancy: a randomised, double-blind, placebo-controlled trial. Lancet 377:52–62
Harris NL et al (2006) Mechanisms of neonatal mucosal antibody protection. J Immunol 177:6256–6262
Levy O (2007) Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol 7:379–390
Marshall-Clarke S, Reen D, Tasker L, Hassan J (2000) Neonatal immunity: how well has it grown up? Immunol Today 21:35–41
van der Kleij D et al (2004) Responses to Toll-like receptor ligands in children living in areas where schistosome infections are endemic. J Infect Dis 189:1044–1051
Yamaguchi T, Wing JB, Sakaguchi S (2011) Two modes of immune suppression by Foxp3+ regulatory T cells under inflammatory or non-inflammatory conditions. Semin Immunol 23:424–430
Kane CM et al (2004) Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 173:7454–7461
Ritter M et al (2010) Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc Natl Acad Sci U S A 107:20459–20464
Hesse M et al (2004) The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol 172:3157–3166
Grainger JR et al (2010) Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J Exp Med 207:2331–2341
Layland LE, Rad R, Wagner H, da Costa CU (2007) Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur J Immunol 37:2174–2184
Dauby N, Goetghebuer T, Kollmann TR, Levy J, Marchant A (2012) Uninfected but not unaffected: chronic maternal infections during pregnancy, fetal immunity, and susceptibility to postnatal infections. Lancet Infect Dis 12:330–340
Hotez PJ et al. (2006) Helminth infections: soil-transmitted helminth infections and schistosomiasis. In: Jamison DT et al (eds) Disease control priorities in developing countries. World Bank, Washington, DC
Bethony J et al (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367:1521–1532
Guadalupe I et al (2009) Evidence for in utero sensitization to Ascaris lumbricoides in newborns of mothers with ascariasis. J Infect Dis 199:1846–1850
Mehta RS et al (2012) Maternal geohelminth infections are associated with an increased susceptibility to geohelminth infection in children: a case-control study. PLoS Negl Trop Dis 6:e1753
Larocque R, Gyorkos TW (2006) Should deworming be included in antenatal packages in hookworm-endemic areas of developing countries? Can J Public Health 97:222–224
Cooper PJ et al (2011) Impact of early life exposures to geohelminth infections on the development of vaccine immunity, allergic sensitization, and allergic inflammatory diseases in children living in tropical Ecuador: the ECUAVIDA birth cohort study. BMC Infect Dis 11:184
Elson LH et al (1996) In utero exposure to Onchocerca volvulus: relationship to subsequent infection intensity and cellular immune responsiveness. Infect Immun 64:5061–5065
Das PK et al (1997) Wuchereria bancrofti microfilaraemia in children in relation to parental infection status. Trans R Soc Trop Med Hyg 91:677–679
Malhotra I et al (1997) In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. J Clin Invest 99:1759–1766
Kirch AK et al (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
Malhotra I et al (2006) Prenatal T cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood. J Infect Dis 193:1005–1013
Malhotra I et al (2003) Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infect Immun 71:5231–5237
Lammie PJ, Hitch WL, Walker Allen EM, Hightower W, Eberhard ML (1991) Maternal filarial infection as risk factor for infection in children. Lancet 337:1005–1006
Eberhard ML, Hitch WL, McNeeley DF, Lammie PJ (1993) Transplacental transmission of Wuchereria bancrofti in Haitian women. J Parasitol 79:62–66
Pit DS, Polderman AM, Schulz-Key H, Soboslay PT (2000) Prenatal immune priming with helminth infections: parasite-specific cellular reactivity and Th1 and Th2 cytokine responses in neonates. Allergy 55:732–739
Soboslay PT et al (1999) Prenatal immune priming in onchocerciasis-Onchocerca volvulus-specific cellular responsiveness and cytokine production in newborns from infected mothers. Clin Exp Immunol 117:130–137
Steel C, Guinea A, McCarthy JS, Ottesen EA (1994) Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigens. Lancet 343:890–893
Haque A, Capron A (1982) Transplacental transfer of rodent microfilariae induces antigen-specific tolerance in rats. Nature 299:361–363
Storey N, Kee JC, Behnke JM, Wakelin D (1988) Prenatal sensitisation in experimental filariasis: observations on Acanthocheilonema viteae infections in mice. Trop Med Parasitol 39:299–303 (official organ of Deutsche Tropenmedizinische Gesellschaft and of Deutsche Gesellschaft fur Technische Zusammenarbeit)
Bosshardt SC, McVay CS, Coleman SU, Klei TR (1992) Brugia pahangi: effects of maternal filariasis on the responses of their progeny to homologous challenge infection. Exp Parasitol 74:271–282
King CL et al (1998) B cell sensitization to helminthic infection develops in utero in humans. J Immunol 160:3578–3584
Rook GA (2009) Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 126:3–11
Carvalho L et al (2009) Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126:28–34
Jackson JA, Friberg IM, Little S, Bradley JE (2009) Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology 126:18–27
Cooke A (2009) Review series on helminths, immune modulation and the hygiene hypothesis: how might infection modulate the onset of type 1 diabetes? Immunology 126:12–17
van den Biggelaar AH et al (2000) Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356:1723–1727
Sabin EA, Araujo MI, Carvalho EM, Pearce EJ (1996) Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J Infect Dis 173:269–272
Camus D et al (1976) Sensitization to Schistosoma mansoni antigen in uninfected children born to infected mothers. J Infect Dis 134:405–408
Novato-Silva E, Gazzinelli G, Colley DG (1992) Immune responses during human schistosomiasis mansoni. XVIII. Immunologic status of pregnant women and their neonates. Scand J Immunol 35:429–437
Attallah AM, Ghanem GE, Ismail H, El Waseef AM (2003) Placental and oral delivery of Schistosoma mansoni antigen from infected mothers to their newborns and children. Am J Trop Med Hyg 68:647–651
Kurtis JD et al (2011) Maternal Schistosomiasis japonica is associated with maternal, placental, and fetal inflammation. Infect Immun 79:1254–1261
Elliott AM et al (2005) A randomised controlled trial of the effects of albendazole in pregnancy on maternal responses to mycobacterial antigens and infant responses to Bacille Calmette-Guerin (BCG) immunisation [ISRCTN32849447]. BMC Infect Dis 5:115
Malhotra I et al (1999) Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol 162:6843–6848
Ghaffar YA, elSobky MK, Raouf AA, Dorgham LS (1989) Mother-to-child transmission of hepatitis B virus in a semirural population in Egypt. J Trop Med Hyg 92:20–26
Mpairwe H et al (2011) Antihelminthic treatment during pregnancy is associated with increased risk of infantile eczema: randomised-controlled trial results. Pediatr Allergy Immunol 22:305–312 (official publication of the European Society of Pediatric Allergy and Immunology)
Elliott AM et al (2005) Helminth infection during pregnancy and development of infantile eczema. JAMA 294:2032–2034
Attallah AM, Abbas AT, Dessouky MI, El-emshaty HM, Elsheikha HM (2006) Susceptibility of neonate mice born to Schistosoma mansoni-infected and noninfected mothers to subsequent S. mansoni infection. Parasitol Res 99:137–145
Othman AA, Shoheib ZS, Saied EM, Soliman RH (2010) Congenital exposure to Schistosoma mansoni infection: impact on the future immune response and the disease outcome. Immunobiology 215:101–112
Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology 20:180–193
Maltepe E, Bakardjiev AI, Fisher SJ (2010) The placenta: transcriptional, epigenetic, and physiological integration during development. J Clin Invest 120:1016–1025
Li L, Kang J, Lei W (2010) Role of Toll-like receptor 4 in inflammation-induced preterm delivery. Mol Hum Reprod 16:267–272
Williams PJ, Bulmer JN, Searle RF, Innes BA, Robson SC (2009) Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy. Reproduction 138:177–184
Redman CW, Sargent IL (2009) Placental stress and pre-eclampsia: a revised view. Placenta 30(Suppl A):S38–S42
Wilczynski JR et al (2003) Lymphocyte subset distribution and cytokine secretion in third trimester decidua in normal pregnancy and preeclampsia. Eur J Obstetr Gynecol Reprod Biol 109:8–15
Moormann AM et al (1999) Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. J Infect Dis 180:1987–1993
Zaretsky MV, Alexander JM, Byrd W, Bawdon RE (2004) Transfer of inflammatory cytokines across the placenta. Obstet Gynecol 103:546–550
Aaltonen R, Heikkinen T, Hakala K, Laine K, Alanen A (2005) Transfer of proinflammatory cytokines across term placenta. Obstet Gynecol 106:802–807
Bobetsis YA, Barros SP, Lin DM, Arce RM, Offenbacher S (2010) Altered gene expression in murine placentas in an infection-induced intrauterine growth restriction model: a microarray analysis. J Reprod Immunol 85:140–148
Vince GS, Johnson PM (2000) Leucocyte populations and cytokine regulation in human uteroplacental tissues. Biochem Soc Trans 28:191–195
Rieger L et al (2009) Specific subsets of immune cells in human decidua differ between normal pregnancy and preeclampsia-a prospective observational study. Reprod Biol Endocrinol 7:132
Mold JE et al (2008) Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322:1562–1565
Guleria I, Sayegh MH (2007) Maternal acceptance of the fetus: true human tolerance. J Immunol 178:3345–3351
Allen JE, Maizels RM (2011) Diversity and dialogue in immunity to helminths. Nat Rev Immunol 11:375–388
M’Rabet L, Vos AP, Boehm G, Garssen J (2008) Breast-feeding and its role in early development of the immune system in infants: consequences for health later in life. J Nutr 138:1782S–1790S
Shimamura M, Huang YY, Goji H (2003) Antibody production in early life supported by maternal lymphocyte factors. Biochim Biophys Acta 1637:55–58
Kovar MG, Serdula MK, Marks JS, Fraser DW (1984) Review of the epidemiologic evidence for an association between infant feeding and infant health. Pediatrics 74:615–638
Frank AL et al (1982) Breast-feeding and respiratory virus infection. Pediatrics 70:239–245
Duncan B et al (1993) Exclusive breast-feeding for at least 4 months protects against otitis media. Pediatrics 91:867–872
Cochi SL et al (1986) Primary invasive Haemophilus influenzae type b disease: a population-based assessment of risk factors. J Pediatr 108:887–896
Arnon SS (1984) Breast feeding and toxigenic intestinal infections: missing links in crib death? Rev Infect Dis 6(Suppl 1):193–201
Lucas A, Cole TJ (1990) Breast milk and neonatal necrotising enterocolitis. Lancet 336:1519–1523
Lucas A, Brooke OG, Morley R, Cole TJ, Bamford MF (1990) Early diet of preterm infants and development of allergic or atopic disease: randomised prospective study. BMJ 300:837–840
Verhasselt V (2010) Neonatal tolerance under breastfeeding influence: the presence of allergen and transforming growth factor-beta in breast milk protects the progeny from allergic asthma. J Pediatr 156:S16–S20
Zaccone P et al (2009) Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice. Eur J Immunol 39:1098–1107
Wilson MS et al (2005) Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 202:1199–1212
Korten S et al (2009) The nematode parasite Onchocerca volvulus generates the transforming growth factor-beta (TGF-beta). Parasitol Res 105:731–741
Korten S, Kaifi JT, Buttner DW, Hoerauf A (2010) Transforming growth factor-beta expression by host cells is elicited locally by the filarial nematode Onchocerca volvulus in hyporeactive patients independently from Wolbachia. Microbes Infect 12:555–564
Yamamoto T, Tsubota Y, Kodama T, Kageyama-Yahara N, Kadowaki M (2012) Oral tolerance induced by transfer of food antigens via breast milk of allergic mothers prevents offspring from developing allergic symptoms in a mouse food allergy model. Clin Dev Immunol 2012:721085
Wright AL, Holberg CJ, Taussig LM, Martinez FD (2001) Factors influencing the relation of infant feeding to asthma and recurrent wheeze in childhood. Thorax 56:192–197
Bottcher MF, Jenmalm MC, Garofalo RP, Bjorksten B (2000) Cytokines in breast milk from allergic and nonallergic mothers. Pediatr Res 47:157–162
Bottcher MF, Jenmalm MC, Bjorksten B (2003) Cytokine, chemokine and secretory IgA levels in human milk in relation to atopic disease and IgA production in infants. Pediatr Allergy Immunol 14:35–41
Noureldin MS, Shaltout AA (1998) Anti-schistosomal IgE and its relation to gastrointestinal allergy in breast-fed infants of Schistosoma mansoni infected mothers. J Egypt Soc Parasitol 28:539–550
Lenzi JA, Sobral AC, Araripe JR, Grimaldi Filho G, Lenzi HL (1987) Congenital and nursing effects on the evolution of Schistosoma mansoni infection in mice. Mem Inst Oswaldo Cruz 82(Suppl 4):257–267
Santos P et al (2010) Influence of maternal schistosomiasis on the immunity of adult offspring mice. Parasitol Res 107:95–102
Petralanda I, Yarzabal L, Piessens WF (1988) Parasite antigens are present in breast milk of women infected with Onchocerca volvulus. Am J Trop Med Hyg 38:372–379
Landreth KS (2002) Critical windows in development of the rodent immune system. Hum Exp Toxicol 21:493–498
Weissman IL (2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157–168
Bradley TR, Metcalf D (1966) The growth of mouse bone marrow cells in vitro. Austr J Exp Biol Med Sci 44:287–299
Tavassoli M (1991) Embryonic and fetal hemopoiesis: an overview. Blood Cells 17:269–281 (discussion 282–266)
Holladay SD, Smialowicz RJ (2000) Development of the murine and human immune system: differential effects of immunotoxicants depend on time of exposure. Environ Health Perspect 108(Suppl 3):463–473
Pardoll DM et al (1987) Differential expression of two distinct T-cell receptors during thymocyte development. Nature 326:79–81
Ceredig R, MacDonald HR, Jenkinson EJ (1983) Flow microfluorometric analysis of mouse thymus development in vivo and in vitro. Eur J Immunol 13:185–190
Reece P et al (2011) Maternal allergy modulates cord blood hematopoietic progenitor Toll-like receptor expression and function. J Allergy Clin Immunol 127:447–453
Reece P, Baatjes AJ, Cyr MM, Sehmi R, Denburg JA (2013) Toll-like receptor-mediated eosinophil-basophil differentiation: autocrine signalling by granulocyte-macrophage colony-stimulating factor in cord blood haematopoietic progenitors. Immunology 139:256–264
Astori M, Finke D, Karapetian O, Acha-Orbea H (1999) Development of T-B cell collaboration in neonatal mice. Int Immunol 11:445–451
Adkins B, Ghanei A, Hamilton K (1993) Developmental regulation of IL-4, IL-2, and IFN-gamma production by murine peripheral T lymphocytes. J Immunol 151:6617–6626
Forsthuber T, Yip HC, Lehmann PV (1996) Induction of TH1 and TH2 immunity in neonatal mice. Science 271:1728–1730
Ridge JP, Fuchs EJ, Matzinger P (1996) Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science 271:1723–1726
Gdalevich M, Mimouni D, Mimouni M (2001) Breast-feeding and the risk of bronchial asthma in childhood: a systematic review with meta-analysis of prospective studies. J Pediatr 139:261–266
van der Kleij D et al (2002) A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J Biol Chem 277:48122–48129
Thomas PG et al (2003) Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J Immunol 171:5837–5841
Aksoy E et al (2005) Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J Biol Chem 280:277–283
Conrad ML et al (2009) Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78. J Exp Med 206:2869–2877
Diav-Citrin O, Shechtman S, Arnon J, Lubart I, Ornoy A (2003) Pregnancy outcome after gestational exposure to mebendazole: a prospective controlled cohort study. Am J Obstet Gynecol 188:282–285
de Silva NR, Sirisena JL, Gunasekera DP, Ismail MM, de Silva HJ (1999) Effect of mebendazole therapy during pregnancy on birth outcome. Lancet 353:1145–1149
Torlesse H, Hodges M (2000) Antihelminthic treatment and haemoglobin concentrations during pregnancy. Lancet 356:1083
Torlesse H, Hodges M (2001) Albendazole therapy and reduced decline in haemoglobin concentration during pregnancy (Sierra Leone). Trans R Soc Trop Med Hyg 95:195–201
Haider BA, Humayun Q, Bhutta ZA (2009) Effect of administration of antihelminthics for soil transmitted helminths during pregnancy. Cochrane Database Syst Rev CD005547
Yazdanbakhsh M, Rodrigues LC (2001) Allergy and the hygiene hypothesis: the Th1/Th2 counterregulation can not provide an explanation. Wien Klin Wochenschr 113:899–902
Bach JF (2002) The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 347:911–920
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media New York
About this chapter
Cite this chapter
Straubinger, K., Prazeres da Costa, C. (2014). Maternal Helminth Infections. In: Horsnell, W. (eds) How Helminths Alter Immunity to Infection. Advances in Experimental Medicine and Biology, vol 828. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1489-0_2
Download citation
DOI: https://doi.org/10.1007/978-1-4939-1489-0_2
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4939-1488-3
Online ISBN: 978-1-4939-1489-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)