Volume 86, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



This study investigated priming as a consequence of maternal parasitic infections. Cord blood plasma samples of 63 African newborns were assessed by enzyme-linked immunosorbent assay for their content of total and schistosome-specific or filaria-specific IgE and IgG4. The frequencies of lymphocyte phenotypes in cord blood were also determined by using flow cytometry, and were compared with those of European newborns. We found significantly increased schistosome soluble egg antigen (SEA)–specific IgE in cord plasma of those born to mothers with schistosome infections and correlations between fetal and maternal SEA-specific and filaria antigen–specific IgE. These data are evidence for priming of the fetal immune system to maternal helminth infections. Furthermore, we show significantly enhanced percentages of CD5– B cells in African newborns cord blood compared with Europeans, which is consistent with earlier maturation of the African fetal immune system.


Article metrics loading...

Loading full text...

Full text loading...



  1. Loke YW, , 1982. Transmission of parasites across the placenta. Adv Parasitol 21: 155228.[Crossref]
  2. 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: 137145.[Crossref]
  3. King CL, Malhotra I, Mungai P, Wamachi A, Kioko J, Ouma JH, Kazura JW, , 1998. B cell sensitization to helminthic infection develops in utero in humans. J Immunol 160: 35783584.
  4. Malhotra I, Mungai P, Wamachi A, Kioko J, Ouma JH, Kazura JW, King CL, , 1999. Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol 162: 68436848.
  5. 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: 101112.[Crossref]
  6. Soboslay PT, Geiger SM, Drabner B, Banla M, Batchassi E, Kowu LA, Stadler A, Schulz-Key H, , 1999. Prenatal immune priming in onchocerciasis: Onchocerca volvulus-specific cellular responsiveness and cytokine production in newborns from infected mothers. Clin Exp Immunol 117: 130137.[Crossref]
  7. Weil GJ, Hussain R, Kumaraswami V, Tripathy SP, Phillips KS, Ottesen EA, , 1983. Prenatal allergic sensitization to helminth antigens in offspring of parasite-infected mothers. J Clin Invest 71: 11241129.[Crossref]
  8. Malhotra I, Mungai PL, Wamachi AN, Tisch D, Kioko JM, Ouma JH, Muchiri E, Kazura JW, King CL, , 2006. Prenatal T cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood. J Infect Dis 193: 10051013.[Crossref]
  9. 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: 539550.
  10. Hitch WL, Eberhard ML, Lammie PJ, , 1997. Investigation of the influence of maternal infection with Wuchereria bancrofti on the humoral and cellular responses of neonates to filarial antigens. Ann Trop Med Parasitol 91: 461469.[Crossref]
  11. Lewert RM, Mandlowitz S, , 1969. Schistosomiasis: prenatal induction of tolerance to antigens. Nature 224: 10291030.[Crossref]
  12. Malhotra I, Ouma J, Wamachi A, Kioko J, Mungai P, Omollo A, Elson L, Koech D, Kazura JW, King CL, , 1997. In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. J Clin Invest 99: 17591766.[Crossref]
  13. Schwarz NG, Adegnika AA, Breitling LP, Gabor J, Agnandji ST, Newman RD, Lell B, Issifou S, Yazdanbakhsh M, Luty AJ, Kremsner PG, Grobusch MP, , 2008. Placental malaria increases malaria risk in the first 30 months of life. Clin Infect Dis 47: 10171025.[Crossref]
  14. Carlier Y, Nzeyimana H, Bout D, Capron A, , 1980. Evaluation of circulating antigens by a sandwich radioimmunoassay, and of antibodies and immune complexes, in Schistosoma mansoni-infected African parturients and their newborn children. Am J Trop Med Hyg 29: 7481.
  15. Hassan MM, Hassounah OA, Hegab M, Salah K, el-Mahrouky L, Galal N, , 1997. Transmission of circulating schistosomal antigens from infected mothers to their newborns. J Egypt Soc Parasitol 27: 773780.
  16. Avrech OM, Samra Z, Lazarovich Z, Caspi E, Jacobovich A, Sompolinsky D, , 1994. Efficacy of the placental barrier for immunoglobulins: correlations between maternal, paternal and fetal immunoglobulin levels. Int Arch Allergy Immunol 103: 160165.[Crossref]
  17. el-Nahal HM, Kaddah MA, Hassan SI, Abdel Ghany A, Ibrahim AM, Ramzy RM, Mostafa EA, , 1998. Effect of Schistosoma mansoni infection on offsprings born from infected mothers. J Egypt Soc Parasitol 28: 523538.
  18. 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: 429437.[Crossref]
  19. Romia SA, Handoussa AE, Youseff SA, el Zayat MM, , 1992. Transplacental transfer of schistosomal antigens and antibodies. J Egypt Soc Parasitol 22: 575582.
  20. Malek A, Sager R, Kuhn P, Nicolaides KH, Schneider H, , 1996. Evolution of maternofetal transport of immunoglobulins during human pregnancy. Am J Reprod Immunol 36: 248255.[Crossref]
  21. Pitcher-Wilmott RW, Hindocha P, Wood CB, , 1980. The placental transfer of IgG subclasses in human pregnancy. Clin Exp Immunol 41: 303308.
  22. Kohler C, Adegnika AA, Van der Linden R, Agnandji ST, Chai SK, Luty AJ, Szepfalusi Z, Kremsner PG, Yazdanbakhsh M, , 2008. Comparison of immunological status of African and European cord blood mononuclear cells. Pediatr Res 64: 631636.[Crossref]
  23. van den Biggelaar AH, Prescott SL, Roponen M, Nadal-Sims MA, Devitt CJ, Phuanukoonnon S, Pomat W, Tulic MK, Lehmann D, Siba PM, Richmond PC, Holt PG, , 2009. Neonatal innate cytokine responses to BCG controlling T-cell development vary between populations. J Allergy Clin Immunol 124: 544550.[Crossref]
  24. Kremsner PG, Enyong P, Krijger FW, De Jonge N, Zotter GM, Thalhammer F, Muhlschlegel F, Bienzle U, Feldmeier H, Deelder AM, , 1994. Circulating anodic and cathodic antigen in serum and urine from Schistosoma haematobium-infected Cameroonian children receiving praziquantel: a longitudinal study. Clin Infect Dis 18: 408413.[Crossref]
  25. Gabriel S, De Bont J, Phiri IK, Masuku M, Riveau G, Schacht AM, Deelder AM, Van Dam GJ, Vercruysse J, , 2002. Transplacental transfer of schistosomal circulating anodic antigens in cows. Parasite Immunol 24: 521525.[Crossref]
  26. Naus CW, van Dam GJ, Kremsner PG, Krijger FW, Deelder AM, , 1998. Human IgE, IgG subclass, and IgM responses to worm and egg antigens in schistosomiasis haematobium: a 12-month study of reinfection in Cameroonian children. Clin Infect Dis 26: 11421147.[Crossref]
  27. Qian ZL, Deelder AM, , 1982. Circulating antigens in Schistosoma infections. Acta Leiden 49: 7180.
  28. Grogan JL, Kremsner PG, van Dam GJ, Metzger W, Mordmuller B, Deelder AM, Yazdanbakhsh M, , 1996. Antischistosome IgG4 and IgE responses are affected differentially by chemotherapy in children versus adults. J Infect Dis 173: 12421247.[Crossref]
  29. Haarbrink M, Terhell AJ, Abadi K, Asri M, de Medeiros F, Yazdanbakhsh M, , 1999. Anti-filarial IgG4 in men and women living in Brugia malayi-endemic areas. Trop Med Int Health 4: 9397.[Crossref]
  30. Butterworth AE, Bensted-Smith R, Capron A, Capron M, Dalton PR, Dunne DW, Grzych JM, Kariuki HC, Khalife J, Koech D, , 1987. Immunity in human schistosomiasis mansoni: prevention by blocking antibodies of the expression of immunity in young children. Parasitology 94: 281300.[Crossref]
  31. El Ridi R, Ismail S, Gaafar T, El Demellawy M, , 1997. Differential responsiveness of humans with early-stage schistosomiasis haematobium to Schistosoma haematobium soluble adult-worm and egg antigens. Parasitol Res 83: 471477.[Crossref]
  32. Hillyer GV, Pacheco E, , 1986. Isolation and characterization of Schistosoma haematobium egg antigens. Am J Trop Med Hyg 35: 777785.
  33. Iskander R, Das PK, Aalberse RC, , 1981. IgG4 antibodies in Egyptian patients with schistosomiasis. Int Arch Allergy Appl Immunol 66: 200207.[Crossref]
  34. Harnett W, Kusel JR, Barrowman MM, , 1985. The use of aldehydes to show a relationship between host and parasite antigens at the surface of adult male Schistosoma mansoni . Parasite Immunol 7: 415428.[Crossref]
  35. Saunders N, Wilson RA, Coulson PS, , 1987. The outer bilayer of the adult schistosome tegument surface has a low turnover rate in vitro and in vivo . Mol Biochem Parasitol 25: 123131.[Crossref]
  36. Snary D, Smith MA, Clegg JA, , 1980. Surface proteins of Schistosoma mansoni and their expression during morphogenesis. Eur J Immunol 10: 573575.[Crossref]
  37. Deelder AM, Klappe HT, van den Aardweg GJ, van Meerbeke EH, , 1976. Schistosoma mansoni: demonstration of two circulating antigens in infected hamsters. Exp Parasitol 40: 189197.
  38. el-Raziky EH, Shaker ZA, Abbassy AF, Aboul-Ezz FM, Naguib YA, , 1978. A preliminary report on materno-foetal immunological changes in schistosomiasis. II. Circulating antigens and antibodies. Egypt J Bilharz 5: 7784.
  39. Dunne DW, Bickle QD, , 1987. Identification and characterization of a polysaccharide-containing antigen from Schistosoma mansoni eggs which cross-reacts with the surface of schistosomula. Parasitology 94: 255268.[Crossref]
  40. Harn DA, Mitsuyama M, David JR, , 1984. Schistosoma mansoni. Anti-egg monoclonal antibodies protect against cercarial challenge in vivo . J Exp Med 159: 13711387.[Crossref]
  41. Capron A, Dessaint JP, , 1992. Immunologic aspects of schistosomiasis. Annu Rev Med 43: 209218.[Crossref]
  42. Knopf PM, Coghlan RL, , 1989. Maternal transfer of resistance to Schistosoma mansoni . J Parasitol 75: 398404.[Crossref]
  43. Ford MJ, Dissous C, Pierce RJ, Taylor MG, Bickle QD, Capron A, , 1987. The isotypes of antibody responsible for the ‘late’ passive transfer of immunity in rats vaccinated with highly irradiated cercariae. Parasitology 94: 509522.[Crossref]
  44. Hagan P, , 1993. IgE and protective immunity to helminth infections. Parasite Immunol 15: 14.[Crossref]
  45. Berry SM, Fine N, Bichalski JA, Cotton DB, Dombrowski MP, Kaplan J, , 1992. Circulating lymphocyte subsets in second- and third-trimester fetuses: comparison with newborns and adults. Am J Obstet Gynecol 167: 895900.[Crossref]
  46. Bhat NM, Kantor AB, Bieber MM, Stall AM, Herzenberg LA, Teng NN, , 1992. The ontogeny and functional characteristics of human B-1 (CD5+ B) cells. Int Immunol 4: 243252.[Crossref]
  47. de Vries E, de Bruin-Versteeg S, Comans-Bitter WM, de Groot R, Hop WC, Boerma GJ, Lotgering FK, van Dongen JJ, , 2000. Longitudinal survey of lymphocyte subpopulations in the first year of life. Pediatr Res 47: 528537.[Crossref]
  48. Casali P, Burastero SE, Nakamura M, Inghirami G, Notkins AL, , 1987. Human lymphocytes making rheumatoid factor and antibody to ssDNA belong to Leu-1+ B-cell subset. Science 236: 7781.[Crossref]
  49. Casali P, Notkins AL, , 1989. CD5+ B lymphocytes, polyreactive antibodies and the human B-cell repertoire. Immunol Today 10: 364368.[Crossref]
  50. Hardy RR, Hayakawa K, Shimizu M, Yamasaki K, Kishimoto T, , 1987. Rheumatoid factor secretion from human Leu-1+ B cells. Science 236: 8183.[Crossref]
  51. Herzenberg LA, Kantor AB, , 1992. Layered evolution in the immune system. A model for the ontogeny and development of multiple lymphocyte lineages. Ann N Y Acad Sci 651: 19.[Crossref]
  52. Erkeller-Yuksel FM, Deneys V, Yuksel B, Hannet I, Hulstaert F, Hamilton C, Mackinnon H, Stokes LT, Munhyeshuli V, Vanlangendonck F, , 1992. Age-related changes in human blood lymphocyte subpopulations. J Pediatr 120: 216222.[Crossref]
  53. Kotiranta-Ainamo A, Apajasalo M, Pohjavuori M, Rautonen N, Rautonen J, , 1999. Mononuclear cell subpopulations in preterm and full-term neonates: independent effects of gestational age, neonatal infection, maternal pre-eclampsia, maternal betamethason therapy, and mode of delivery. Clin Exp Immunol 115: 309314.[Crossref]
  54. O'Gorman MR, Millard DD, Lowder JN, Yogev R, , 1998. Lymphocyte subpopulations in healthy 1–3-day-old infants. Cytometry 34: 235241.[Crossref]
  55. Rabian-Herzog C, Lesage S, Gluckman E, , 1992. Characterization of lymphocyte subpopulations in cord blood. Bone Marrow Transplant 9 (Suppl 1): 6467.
  56. Lalor MK, Floyd S, Gorak-Stolinska P, Ben-Smith A, Weir RE, Smith SG, Newport MJ, Blitz R, Mvula H, Branson K, McGrath N, Crampin AC, Fine PE, Dockrell HM, , 2011. BCG vaccination induces different cytokine profiles following infant BCG vaccination in the UK and Malawi. J Infect Dis 204: 10751085.[Crossref]
  57. Lalor MK, Smith SG, Floyd S, Gorak-Stolinska P, Weir RE, Blitz R, Branson K, Fine PE, Dockrell HM, , 2010. Complex cytokine profiles induced by BCG vaccination in UK infants. Vaccine 28: 16351641.[Crossref]

Data & Media loading...

  • Received : 15 Jul 2011
  • Accepted : 26 Dec 2011

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error