Maternal Helminth Infections

  • Kathrin Straubinger
  • Clarissa Prazeres da CostaEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 828)


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.


Fetomaternal Maternal helminth infection Placenta Fetal imprinting Immune system development Germ-line In-utero Hematopoiesis 


  1. 1.
    Woodburn PW et al (2009) Risk factors for helminth, malaria, and HIV infection in pregnancy in Entebbe, Uganda. PLoS Negl Trop Dis 3:e473PubMedPubMedCentralGoogle Scholar
  2. 2.
    Adegnika AA et al (2010) Epidemiology of parasitic co-infections during pregnancy in Lambarene, Gabon. Trop Med Int Health 15:1204–1209PubMedGoogle Scholar
  3. 3.
    van Eijk AM et al (2009) Geohelminth Infections among pregnant women in rural western Kenya; a cross-sectional study. PLoS Negl Trop Dis 3:e370PubMedPubMedCentralGoogle Scholar
  4. 4.
    Hillier SD et al (2008) Plasmodium falciparum and helminth coinfection in a semi urban population of pregnant women in Uganda. J Infect Dis 198:920–927PubMedPubMedCentralGoogle Scholar
  5. 5.
    Kramer MS (2003) The epidemiology of adverse pregnancy outcomes: an overview. J Nutr 133:1592S–1596SPubMedGoogle Scholar
  6. 6.
    Steketee RW (2003) Pregnancy, nutrition and parasitic diseases. J Nutr 133:1661S−1667SGoogle Scholar
  7. 7.
    Barker DJ (2006) Adult consequences of fetal growth restriction. Clin Obstetr Gynecol 49:270–283Google Scholar
  8. 8.
    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 359:61–73PubMedPubMedCentralGoogle Scholar
  9. 9.
    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 50:531–540PubMedPubMedCentralGoogle Scholar
  10. 10.
    Navitsky RC et al (1998) Ancylostoma duodenale is responsible for hookworm infections among pregnant women in the rural plains of Nepal. J Parasitol 84:647–651PubMedGoogle Scholar
  11. 11.
    Brooker S, Hotez PJ, Bundy DA (2008) Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl Trop Dis 2:e291PubMedPubMedCentralGoogle Scholar
  12. 12.
    Christian P, Khatry SK, West KP Jr (2004) Antenatal antihelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364:981–983PubMedGoogle Scholar
  13. 13.
    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 11:1485–1495PubMedGoogle Scholar
  14. 14.
    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 88:48–53PubMedPubMedCentralGoogle Scholar
  15. 15.
    Yatich NJ et al (2010) The effect of malaria and intestinal helminth coinfection on birth outcomes in Kumasi, Ghana. Am J Trop Med Hyg 82:28–34PubMedPubMedCentralGoogle Scholar
  16. 16.
    Gallagher M et al (2005) The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS 19:1849–1855PubMedGoogle Scholar
  17. 17.
    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 71:6668–6671PubMedPubMedCentralGoogle Scholar
  18. 18.
    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)Google Scholar
  19. 19.
    Egwunyenga AO, Ajayi JA, Nmorsi OP, Duhlinska-Popova DD (2001) Plasmodium/intestinal helminth co-infections among pregnant Nigerian women. Mem Inst Oswaldo Cruz 96:1055–1059PubMedGoogle Scholar
  20. 20.
    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 45:57–64PubMedGoogle Scholar
  21. 21.
    Brair ME, Brabin BJ, Milligan P, Maxwell S, Hart CA (1994) Reduced transfer of tetanus antibodies with placental malaria. Lancet 343:208–209PubMedGoogle Scholar
  22. 22.
    Desai M et al (2007) Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7:93–104PubMedGoogle Scholar
  23. 23.
    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 184:627–632PubMedGoogle Scholar
  24. 24.
    Labeaud AD, Malhotra I, King MJ, King CL, King CH (2009) Do antenatal parasite infections devalue childhood vaccination? PLoS Negl Trop Dis 3:e442PubMedPubMedCentralGoogle Scholar
  25. 25.
    Bassily S et al (1997) Immunogenicity of recombinant hepatitis B vaccine among infants of mothers with active schistosomiasis. Am J Trop Med Hyg 57:197–199PubMedGoogle Scholar
  26. 26.
    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 2:272PubMedGoogle Scholar
  27. 27.
    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 29:247–255PubMedPubMedCentralGoogle Scholar
  28. 28.
    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 377:52–62PubMedPubMedCentralGoogle Scholar
  29. 29.
    Harris NL et al (2006) Mechanisms of neonatal mucosal antibody protection. J Immunol 177:6256–6262PubMedGoogle Scholar
  30. 30.
    Levy O (2007) Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol 7:379–390PubMedGoogle Scholar
  31. 31.
    Marshall-Clarke S, Reen D, Tasker L, Hassan J (2000) Neonatal immunity: how well has it grown up? Immunol Today 21:35–41PubMedGoogle Scholar
  32. 32.
    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 189:1044–1051PubMedGoogle Scholar
  33. 33.
    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 23:424–430PubMedGoogle Scholar
  34. 34.
    Kane CM et al (2004) Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 173:7454–7461PubMedGoogle Scholar
  35. 35.
    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 107:20459–20464PubMedPubMedCentralGoogle Scholar
  36. 36.
    Hesse M et al (2004) The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol 172:3157–3166PubMedGoogle Scholar
  37. 37.
    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 207:2331–2341PubMedPubMedCentralGoogle Scholar
  38. 38.
    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 37:2174–2184PubMedGoogle Scholar
  39. 39.
    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 12:330–340PubMedGoogle Scholar
  40. 40.
    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, DCGoogle Scholar
  41. 41.
    Bethony J et al (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367:1521–1532PubMedGoogle Scholar
  42. 42.
    Guadalupe I et al (2009) Evidence for in utero sensitization to Ascaris lumbricoides in newborns of mothers with ascariasis. J Infect Dis 199:1846–1850PubMedPubMedCentralGoogle Scholar
  43. 43.
    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:e1753PubMedPubMedCentralGoogle Scholar
  44. 44.
    Larocque R, Gyorkos TW (2006) Should deworming be included in antenatal packages in hookworm-endemic areas of developing countries? Can J Public Health 97:222–224PubMedGoogle Scholar
  45. 45.
    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 11:184PubMedPubMedCentralGoogle Scholar
  46. 46.
    Elson LH et al (1996) In utero exposure to Onchocerca volvulus: relationship to subsequent infection intensity and cellular immune responsiveness. Infect Immun 64:5061–5065PubMedPubMedCentralGoogle Scholar
  47. 47.
    Das PK et al (1997) Wuchereria bancrofti microfilaraemia in children in relation to parental infection status. Trans R Soc Trop Med Hyg 91:677–679PubMedGoogle Scholar
  48. 48.
    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 99:1759–1766PubMedPubMedCentralGoogle Scholar
  49. 49.
    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 127:327–335PubMedGoogle Scholar
  50. 50.
    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 193:1005–1013PubMedGoogle Scholar
  51. 51.
    Malhotra I et al (2003) Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infect Immun 71:5231–5237PubMedPubMedCentralGoogle Scholar
  52. 52.
    Lammie PJ, Hitch WL, Walker Allen EM, Hightower W, Eberhard ML (1991) Maternal filarial infection as risk factor for infection in children. Lancet 337:1005–1006PubMedGoogle Scholar
  53. 53.
    Eberhard ML, Hitch WL, McNeeley DF, Lammie PJ (1993) Transplacental transmission of Wuchereria bancrofti in Haitian women. J Parasitol 79:62–66PubMedGoogle Scholar
  54. 54.
    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 55:732–739PubMedGoogle Scholar
  55. 55.
    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 117:130–137PubMedPubMedCentralGoogle Scholar
  56. 56.
    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 343:890–893PubMedGoogle Scholar
  57. 57.
    Haque A, Capron A (1982) Transplacental transfer of rodent microfilariae induces antigen-specific tolerance in rats. Nature 299:361–363PubMedGoogle Scholar
  58. 58.
    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)Google Scholar
  59. 59.
    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 74:271–282PubMedGoogle Scholar
  60. 60.
    King CL et al (1998) B cell sensitization to helminthic infection develops in utero in humans. J Immunol 160:3578–3584PubMedGoogle Scholar
  61. 61.
    Rook GA (2009) Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 126:3–11PubMedPubMedCentralGoogle Scholar
  62. 62.
    Carvalho L et al (2009) Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126:28–34PubMedPubMedCentralGoogle Scholar
  63. 63.
    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 126:18–27PubMedPubMedCentralGoogle Scholar
  64. 64.
    Cooke A (2009) Review series on helminths, immune modulation and the hygiene hypothesis: how might infection modulate the onset of type 1 diabetes? Immunology 126:12–17PubMedPubMedCentralGoogle Scholar
  65. 65.
    van den Biggelaar AH et al (2000) Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356:1723–1727PubMedGoogle Scholar
  66. 66.
    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 173:269–272PubMedGoogle Scholar
  67. 67.
    Camus D et al (1976) Sensitization to Schistosoma mansoni antigen in uninfected children born to infected mothers. J Infect Dis 134:405–408PubMedGoogle Scholar
  68. 68.
    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 35:429–437PubMedGoogle Scholar
  69. 69.
    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 68:647–651PubMedGoogle Scholar
  70. 70.
    Kurtis JD et al (2011) Maternal Schistosomiasis japonica is associated with maternal, placental, and fetal inflammation. Infect Immun 79:1254–1261PubMedPubMedCentralGoogle Scholar
  71. 71.
    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 5:115PubMedPubMedCentralGoogle Scholar
  72. 72.
    Malhotra I et al (1999) Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol 162:6843–6848PubMedGoogle Scholar
  73. 73.
    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 92:20–26PubMedGoogle Scholar
  74. 74.
    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)Google Scholar
  75. 75.
    Elliott AM et al (2005) Helminth infection during pregnancy and development of infantile eczema. JAMA 294:2032–2034PubMedGoogle Scholar
  76. 76.
    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 99:137–145PubMedGoogle Scholar
  77. 77.
    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 215:101–112PubMedGoogle Scholar
  78. 78.
    Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology 20:180–193PubMedGoogle Scholar
  79. 79.
    Maltepe E, Bakardjiev AI, Fisher SJ (2010) The placenta: transcriptional, epigenetic, and physiological integration during development. J Clin Invest 120:1016–1025PubMedPubMedCentralGoogle Scholar
  80. 80.
    Li L, Kang J, Lei W (2010) Role of Toll-like receptor 4 in inflammation-induced preterm delivery. Mol Hum Reprod 16:267–272PubMedGoogle Scholar
  81. 81.
    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 138:177–184PubMedGoogle Scholar
  82. 82.
    Redman CW, Sargent IL (2009) Placental stress and pre-eclampsia: a revised view. Placenta 30(Suppl A):S38–S42PubMedGoogle Scholar
  83. 83.
    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 109:8–15Google Scholar
  84. 84.
    Moormann AM et al (1999) Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. J Infect Dis 180:1987–1993PubMedGoogle Scholar
  85. 85.
    Zaretsky MV, Alexander JM, Byrd W, Bawdon RE (2004) Transfer of inflammatory cytokines across the placenta. Obstet Gynecol 103:546–550PubMedGoogle Scholar
  86. 86.
    Aaltonen R, Heikkinen T, Hakala K, Laine K, Alanen A (2005) Transfer of proinflammatory cytokines across term placenta. Obstet Gynecol 106:802–807PubMedGoogle Scholar
  87. 87.
    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 85:140–148PubMedPubMedCentralGoogle Scholar
  88. 88.
    Vince GS, Johnson PM (2000) Leucocyte populations and cytokine regulation in human uteroplacental tissues. Biochem Soc Trans 28:191–195PubMedGoogle Scholar
  89. 89.
    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 7:132PubMedPubMedCentralGoogle Scholar
  90. 90.
    Mold JE et al (2008) Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322:1562–1565PubMedPubMedCentralGoogle Scholar
  91. 91.
    Guleria I, Sayegh MH (2007) Maternal acceptance of the fetus: true human tolerance. J Immunol 178:3345–3351PubMedGoogle Scholar
  92. 92.
    Allen JE, Maizels RM (2011) Diversity and dialogue in immunity to helminths. Nat Rev Immunol 11:375–388PubMedGoogle Scholar
  93. 93.
    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–1790SGoogle Scholar
  94. 94.
    Shimamura M, Huang YY, Goji H (2003) Antibody production in early life supported by maternal lymphocyte factors. Biochim Biophys Acta 1637:55–58PubMedGoogle Scholar
  95. 95.
    Kovar MG, Serdula MK, Marks JS, Fraser DW (1984) Review of the epidemiologic evidence for an association between infant feeding and infant health. Pediatrics 74:615–638PubMedGoogle Scholar
  96. 96.
    Frank AL et al (1982) Breast-feeding and respiratory virus infection. Pediatrics 70:239–245PubMedGoogle Scholar
  97. 97.
    Duncan B et al (1993) Exclusive breast-feeding for at least 4 months protects against otitis media. Pediatrics 91:867–872PubMedGoogle Scholar
  98. 98.
    Cochi SL et al (1986) Primary invasive Haemophilus influenzae type b disease: a population-based assessment of risk factors. J Pediatr 108:887–896PubMedGoogle Scholar
  99. 99.
    Arnon SS (1984) Breast feeding and toxigenic intestinal infections: missing links in crib death? Rev Infect Dis 6(Suppl 1):193–201Google Scholar
  100. 100.
    Lucas A, Cole TJ (1990) Breast milk and neonatal necrotising enterocolitis. Lancet 336:1519–1523PubMedGoogle Scholar
  101. 101.
    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 300:837–840PubMedPubMedCentralGoogle Scholar
  102. 102.
    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–S20PubMedGoogle Scholar
  103. 103.
    Zaccone P et al (2009) Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice. Eur J Immunol 39:1098–1107PubMedGoogle Scholar
  104. 104.
    Wilson MS et al (2005) Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 202:1199–1212PubMedPubMedCentralGoogle Scholar
  105. 105.
    Korten S et al (2009) The nematode parasite Onchocerca volvulus generates the transforming growth factor-beta (TGF-beta). Parasitol Res 105:731–741PubMedGoogle Scholar
  106. 106.
    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 12:555–564PubMedGoogle Scholar
  107. 107.
    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 2012:721085PubMedPubMedCentralGoogle Scholar
  108. 108.
    Wright AL, Holberg CJ, Taussig LM, Martinez FD (2001) Factors influencing the relation of infant feeding to asthma and recurrent wheeze in childhood. Thorax 56:192–197PubMedPubMedCentralGoogle Scholar
  109. 109.
    Bottcher MF, Jenmalm MC, Garofalo RP, Bjorksten B (2000) Cytokines in breast milk from allergic and nonallergic mothers. Pediatr Res 47:157–162PubMedGoogle Scholar
  110. 110.
    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 14:35–41PubMedGoogle Scholar
  111. 111.
    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 28:539–550PubMedGoogle Scholar
  112. 112.
    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):257–267PubMedGoogle Scholar
  113. 113.
    Santos P et al (2010) Influence of maternal schistosomiasis on the immunity of adult offspring mice. Parasitol Res 107:95–102PubMedGoogle Scholar
  114. 114.
    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 38:372–379PubMedGoogle Scholar
  115. 115.
    Landreth KS (2002) Critical windows in development of the rodent immune system. Hum Exp Toxicol 21:493–498PubMedGoogle Scholar
  116. 116.
    Weissman IL (2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157–168PubMedGoogle Scholar
  117. 117.
    Bradley TR, Metcalf D (1966) The growth of mouse bone marrow cells in vitro. Austr J Exp Biol Med Sci 44:287–299Google Scholar
  118. 118.
    Tavassoli M (1991) Embryonic and fetal hemopoiesis: an overview. Blood Cells 17:269–281 (discussion 282–266)Google Scholar
  119. 119.
    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):463–473PubMedPubMedCentralGoogle Scholar
  120. 120.
    Pardoll DM et al (1987) Differential expression of two distinct T-cell receptors during thymocyte development. Nature 326:79–81PubMedGoogle Scholar
  121. 121.
    Ceredig R, MacDonald HR, Jenkinson EJ (1983) Flow microfluorometric analysis of mouse thymus development in vivo and in vitro. Eur J Immunol 13:185–190PubMedGoogle Scholar
  122. 122.
    Reece P et al (2011) Maternal allergy modulates cord blood hematopoietic progenitor Toll-like receptor expression and function. J Allergy Clin Immunol 127:447–453PubMedGoogle Scholar
  123. 123.
    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 139:256–264PubMedPubMedCentralGoogle Scholar
  124. 124.
    Astori M, Finke D, Karapetian O, Acha-Orbea H (1999) Development of T-B cell collaboration in neonatal mice. Int Immunol 11:445–451PubMedGoogle Scholar
  125. 125.
    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 151:6617–6626PubMedGoogle Scholar
  126. 126.
    Forsthuber T, Yip HC, Lehmann PV (1996) Induction of TH1 and TH2 immunity in neonatal mice. Science 271:1728–1730PubMedGoogle Scholar
  127. 127.
    Ridge JP, Fuchs EJ, Matzinger P (1996) Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science 271:1723–1726PubMedGoogle Scholar
  128. 128.
    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 139:261–266PubMedGoogle Scholar
  129. 129.
    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 277:48122–48129PubMedGoogle Scholar
  130. 130.
    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 171:5837–5841PubMedGoogle Scholar
  131. 131.
    Aksoy E et al (2005) Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J Biol Chem 280:277–283PubMedGoogle Scholar
  132. 132.
    Conrad ML et al (2009) Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78. J Exp Med 206:2869–2877PubMedPubMedCentralGoogle Scholar
  133. 133.
    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 188:282–285PubMedGoogle Scholar
  134. 134.
    de Silva NR, Sirisena JL, Gunasekera DP, Ismail MM, de Silva HJ (1999) Effect of mebendazole therapy during pregnancy on birth outcome. Lancet 353:1145–1149PubMedGoogle Scholar
  135. 135.
    Torlesse H, Hodges M (2000) Antihelminthic treatment and haemoglobin concentrations during pregnancy. Lancet 356:1083PubMedGoogle Scholar
  136. 136.
    Torlesse H, Hodges M (2001) Albendazole therapy and reduced decline in haemoglobin concentration during pregnancy (Sierra Leone). Trans R Soc Trop Med Hyg 95:195–201PubMedGoogle Scholar
  137. 137.
    Haider BA, Humayun Q, Bhutta ZA (2009) Effect of administration of antihelminthics for soil transmitted helminths during pregnancy. Cochrane Database Syst Rev CD005547Google Scholar
  138. 138.
    Yazdanbakhsh M, Rodrigues LC (2001) Allergy and the hygiene hypothesis: the Th1/Th2 counterregulation can not provide an explanation. Wien Klin Wochenschr 113:899–902PubMedGoogle Scholar
  139. 139.
    Bach JF (2002) The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 347:911–920PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Kathrin Straubinger
    • 1
  • Clarissa Prazeres da Costa
    • 1
    Email author
  1. 1.Department of Parasitology, Institute of Medical Microbiology, Immunology and Hygiene Technische Universität MünchenMunichGermany

Personalised recommendations