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Table of Contents
Vol. 66, No. 2, 2008
Issue release date: July 2008
Section title: Paper
Ann Nestlé [Engl] 2008;66:71–79
(DOI:10.1159/000129624)

Determinants of Responses to Oral Vaccines in Developing Countries

Sack D.A.a · Qadri F.b · Svennerholm A.-M.c
aDepartment of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Md., USA; bLaboratory Science Division, International Centre for Diarrhoeal Disease Research Bangladesh, Dhaka, Bangladesh; cDepartment of Microbiology and Immunology, University of Gothenburg, Gothenburg, Sweden
email Corresponding Author

Abstract

Oral vaccines which are intended for global use do not necessarily induce the same immune responses in all children worldwide. In fact, several vaccines often induce less frequent and lower mean antibody responses in children in developing countries, suggesting that the vaccines may be less protective among children in these areas. Though the reasons for this less vigorous response are not completely understood, it appears that nutrition-related factors, including both protein-calorie and micronutrient malnutrition, are important aspects in understanding the hyporesponsiveness seen in these children. Related issues including breastfeeding, interference from maternal placental antibodies, intestinal parasitic infections, intestinal mucosal damage and possibly maternal malnutrition during pregnancy also appear to be important. Vaccines designed for oral administration will need to be adjusted to these potential problems in order to maximize benefits for all children. Oral vaccines, when given to children in developing countries, may require higher doses of vaccine, booster doses, calorie, micronutrient and vitamin supplements, withdrawal of breast milk before vaccine administration, deworming medications or other measures to realize their full benefit.

© 2008 Nestec Ltd., Vevey/S. Karger AG, Basel


  

Key Words

  • Oral vaccines
  • Cholera
  • Rotavirus
  • Typhoid
  • Polio
  • Shigellosis
  • Immune response
  • Malnutrition
  • Zinc
  • Vitamin A
  • Breastfeeding

References

  1. Moore SE, Goldblatt D, Bates CJ, Prentice AM: Impact of nutritional status on antibody responses to different vaccines in undernourished Gambian children. Acta Paediatr 2003;92:170–176.
  2. Faden H: Results of a clinical study of polio vaccine: the Buffalo experience. Pediatr Infect Dis J 1991;10:973–975.
  3. Agarwal A, Sharma D, Kumari S, Khare S: Antibody response to three doses of standard and double dose of trivalent oral polio vaccine. Indian Pediatr 1991;28:1141–1145.
  4. Sabin AB: Vaccination against poliomyelitis in economically underdeveloped countries. Bull World Health Organ 1980;58:141–157.
  5. John TJ, Jayabal P: Oral polio vaccination of children in the tropics. 1. The poor seroconversion rates and the absence of viral interference. Am J Epidemiol 1972;96:263–269.
  6. Sutter RW, Suleiman AJ, Malankar P, et al: Trial of a supplemental dose of four poliovirus vaccines. N Engl J Med 2000;343:767–773.
  7. Triki H, Abdallah MV, Ben AR, et al: Influence of host related factors on the antibody response to trivalent oral polio vaccine in Tunisian infants. Vaccine 1997;15:1123–1129.
  8. Swartz TA, Skalska P, Gerichter CG, Cockburn WC: Routine administration of oral polio vaccine in a subtropical area. Factors possibly influencing seroconversion rates. J Hyg (Lond) 1972;70:719–726.
  9. Lepow ML, Warren RJ, Gray N, et al: Effect of Sabin type 1 poliomyelitis vaccine administered by mouth to newborn infants. N Engl J Med 1961;264:1071–1078.
  10. Plotkin SA, Katz M, Brown RE, Pagano JS: Oral poliovirus vaccination in newborn African infants. The inhibitory effect of breast feeding. Am J Dis Child 1966;111:27–30.
  11. Katz M, Plotkin SA: Oral polio immunization of the newborn infant; a possible method for overcoming interference by ingested antibodies. J Pediatr 1968;73:267–270.
  12. John TJ, Devarajan LV, Luther L, Vijayarathnam P: Effect of breast-feeding on seroresponse of infants to oral poliovirus vaccination. Pediatrics 1976;57:47–53.
  13. Myaux JA, Unicomb L, Besser RE, et al: Effect of diarrhea on the humoral response to oral polio vaccination. Pediatr Infect Dis J 1996;15:204–209.
  14. Bhaskaram P, Nair KM, Hemalatha P, et al: Systemic and mucosal immune response to polio vaccination with additional dose in newborn period. J Trop Pediatr 1997;43:232–234.
  15. Chopra K, Kundu S, Chowdhury DS: Antibody response of infants in tropics to five doses of oral polio vaccine. J Trop Pediatr 1989;35:19–23.
  16. Bahl R, Bhandari N, Wahed MA, et al: Vitamin A supplementation of women postpartum and of their infants at immunization alters breast milk retinol and infant vitamin A status. J Nutr 2002;132:3243–3248.
  17. Vesikari T, Isolauri E, d’Hondt E, et al: Protection of infants against rotavirus diarrhoea by RIT 4237 attenuated bovine rotavirus strain vaccine. Lancet 1984;i:977–981.

    External Resources

  18. Hanlon P, Hanlon L, Marsh V, et al: Trial of an attenuated bovine rotavirus vaccine (RIT 4237) in Gambian infants. Lancet 1987;i: 1342–1345.

    External Resources

  19. Georges-Courbot MC, Monges J, Siopathis MR, et al: Evaluation of the efficacy of a low-passage bovine rotavirus (strain WC3) vaccine in children in Central Africa. Res Virol 1991;142:405–411.
  20. De Mol P, Zissis G, Butzler JP, et al: Failure of live, attenuated oral rotavirus vaccine. Lancet 1986;ii:108.

    External Resources

  21. Joensuu J, Koskenniemi E, Pang XL, Vesikari T: Randomised placebo-controlled trial of rhesus-human reassortant rotavirus vaccine for prevention of severe rotavirus gastroenteritis. Lancet 1997;350:1205–1209.
  22. Rennels MB, Glass RI, Dennehy PH, et al: Safety and efficacy of high-dose rhesus-human reassortant rotavirus vaccines – report of the National Multicenter Trial. United States Rotavirus Vaccine Efficacy Group. Pediatrics 1996;97:7–13.
  23. Lanata CF, Midthun K, Black RE, et al: Safety, immunogenicity, and protective efficacy of one and three doses of the tetravalent rhesus rotavirus vaccine in infants in Lima, Peru. J Infect Dis 1996;174:268–275.
  24. Linhares AC, Gabbay YB, Mascarenhas JD, et al: Immunogenicity, safety and efficacy of tetravalent rhesus-human, reassortant rotavirus vaccine in Belem, Brazil. Bull World Health Organ 1996;74:491–500.
  25. Perez-Schael I, Guntinas MJ, Perez M, et al: Efficacy of the rhesus rotavirus-based quadrivalent vaccine in infants and young children in Venezuela. N Engl J Med 1997;337:1181–1187.
  26. Linhares AC, Lanata CF, Hausdorff WP, et al: Reappraisal of the Peruvian and Brazilian lower titer tetravalent rhesus-human reassortant rotavirus vaccine efficacy trials: analysis by severity of diarrhea. Pediatr Infect Dis J 1999;18:1001–1006.
  27. Ruiz-Palacios GM, Perez-Schael I, Velazquez FR, et al: Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 2006;354:11–22.
  28. Vesikari T, Matson DO, Dennehy P, et al: Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 2006;354:23–33.
  29. Pichichero ME: Effect of breast-feeding on oral rhesus rotavirus vaccine seroconversion: a metaanalysis. J Infect Dis 1990;162:753–755.
  30. Rennels MB, Wasserman SS, Glass RI, Keane VA: Comparison of immunogenicity and efficacy of rhesus rotavirus reassortant vaccines in breastfed and nonbreastfed children. US Rotavirus Vaccine Efficacy Group. Pediatrics 1995;96:1132–1136.
  31. Linhares AC, Carmo KB, Oliveira KK, et al: Nutritional status in relation to the efficacy of the rhesus-human reassortant, tetravalent rotavirus vaccine (RRV-TV) in infants from Belem, Para state, Brazil. Rev Inst Med Trop Sao Paulo 2002;44:13–16.

    External Resources

  32. Perez-Schael I, Salinas B, Tomat M, et al: Efficacy of the human rotavirus vaccine RIX4414 in malnourished children. J Infect Dis 2007;196:537–540.
  33. Lin FY, Ho VA, Khiem HB, et al: The efficacy of a Salmonella typhi Vi conjugate vaccine in two-to-five-year-old children. N Engl J Med 2001;344:1263–1269.
  34. Murphy JR, Grez L, Schlesinger L, et al: Immunogenicity of Salmonella typhi Ty21a vaccine for young children. Infect Immun 1991;59:4291–4293.
  35. Cryz SJ Jr, Vanprapar N, Thisyakorn U, et al: Safety and immunogenicity of Salmonella typhi Ty21a vaccine in young Thai children. Infect Immun 1993;61:1149–1151.
  36. Cooper PJ, Chico M, Sandoval C, et al: Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect Immun 2001;69:1574–1580.
  37. Lagos R, Avendano A, Horwitz I, et al: Tolerance and immunogenicity of an oral dose of CVD 103-HgR, a live attenuated Vibrio cholerae 01 strain: a double-blind study of Chilean adults. Rev Med Chil 1993;121:857–863.
  38. Simanjuntak CH, O’Hanley P, Punjabi NH, et al: Safety, immunogenicity, and transmissibility of single-dose live oral cholera vaccine strain CVD 103-HgR in 24- to 59-month-old Indonesian children. J Infect Dis 1993;168:1169–1176.
  39. Suharyono, Simanjuntak C, Witham N, et al: Safety and immunogenicity of single-dose live oral cholera vaccine CVD 103-HgR in 5–9-year-old Indonesian children. Lancet 1992;340:689–694.
  40. Richie EE, Punjabi NH, Sidharta YY, et al: Efficacy trial of single-dose live oral cholera vaccine CVD 103-HgR in North Jakarta, Indonesia, a cholera-endemic area. Vaccine 2000;18:2399–2410.
  41. Lagos R, Fasano A, Wasserman SS, et al: Effect of small bowel bacterial overgrowth on the immunogenicity of single-dose live oral cholera vaccine CVD 103-HgR. J Infect Dis 1999;180:1709–1712.
  42. Sack DA, Sack RB, Shimko J, et al: Evaluation of Peru-15, a new live oral vaccine for cholera, in volunteers. J Infect Dis 1997;176:201–205.
  43. Cohen MB, Giannella RA, Bean J, et al: Randomized, controlled human challenge study of the safety, immunogenicity, and protective efficacy of a single dose of Peru-15, a live attenuated oral cholera vaccine. Infect Immun 2002;70:1965–1970.
  44. Kenner JR, Coster TS, Taylor DN, et al: Peru-15, an improved live attenuated oral vaccine candidate for Vibrio cholerae O1. J Infect Dis 1995;172:1126–1129.
  45. Qadri F, Chowdhury MI, Faruque SM, et al: Peru-15, a live attenuated oral cholera vaccine, is safe and immunogenic in Bangladeshi toddlers and infants. Vaccine 2007;25:231–238.
  46. Sack DA, Shimko J, Sack RB, et al: Comparison of alternative buffers for use with a new live oral cholera vaccine, Peru-15, in outpatient volunteers. Infect Immun 1997;65:2107–2111.
  47. Clemens JD, Sack DA, Harris JR, et al: Field trial of oral cholera vaccines in Bangladesh. Lancet 1986;ii:124–127.

    External Resources

  48. Holmgren J, Clemens J, Sack DA, Svennerholm AM: New cholera vaccines. Vaccine 1989;7:94–96.
  49. Trach DD, Clemens JD, Ke NT, et al: Field trial of a locally produced, killed, oral cholera vaccine in Vietnam. Lancet 1997;349:231–235.
  50. Clemens JD, Sack DA, Harris JR, et al: Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 1990;335:270–273.
  51. Concha A, Giraldo A, Castaneda E, et al: Safety and immunogenicity of oral killed whole cell recombinant B subunit cholera vaccine in Barranquilla, Colombia. Bull Pan Am Health Organ 1995;29:312–321.
  52. Sanchez JL, Vasquez B, Begue RE, et al: Protective efficacy of oral whole-cell/recombinant-B-subunit cholera vaccine in Peruvian military recruits. Lancet 1994;344:1273–1276.
  53. Taylor DN, Cardenas V, Sanchez JL, et al: Two-year study of the protective efficacy of the oral whole cell plus recombinant B subunit cholera vaccine in Peru. J Infect Dis 2000;181:1667–1673.
  54. Lucas ME, Deen JL, von Seidlein L, et al: Effectiveness of mass oral cholera vaccination in Beira, Mozambique. N Engl J Med 2005;352:757–767.
  55. Taylor DN, Cardenas V, Perez J, et al: Safety, immunogenicity, and lot stability of the whole cell/recombinant B subunit (WC/rCTB) cholera vaccine in Peruvian adults and children. Am J Trop Med Hyg 1999;61:869–873.
  56. Clemens JD, Stanton BF, Chakraborty J, et al: B subunit whole-cell and whole-cell only oral vaccines against cholera: studies on reactogenicity and immunogenicity. J Infect Dis 1987;155:79–85.
  57. Sack DA, Clemens JD, Huda S, et al: Antibody responses after immunization with killed oral cholera vaccines during the 1985 vaccine field trial in Bangladesh. J Infect Dis 1991;164:407–411.
  58. Hallander HO, Paniagua M, Espinoza F, et al: Calibrated serological techniques demonstrate significant different serum response rates to an oral killed cholera vaccine between Swedish and Nicaraguan children. Vaccine 2002;21:138–145.
  59. Glass RI, Svennerholm AM, Stoll BJ, et al: Effects of undernutrition on infection with Vibrio cholerae O1 and on response to oral cholera vaccine. Pediatr Infect Dis J 1989;8:105–109.
  60. Albert MJ, Qadri F, Wahed MA, et al: Supplementation with zinc, but not vitamin A, improves seroconversion to vibriocidal antibody in children given an oral cholera vaccine. J Infect Dis 2003;187:909–913.
  61. Qadri F, Ahmed T, Wahed MA, et al: Suppressive effect of zinc on antibody response to cholera toxin in children given the killed, B subunit-whole cell, oral cholera vaccine. Vaccine 2004;22:416–421.
  62. Glass RI, Stoll BJ: The protective effect of human milk against diarrhea. A review of studies from Bangladesh. Acta Paediatr Scand Suppl 1989;351:131–136.
  63. Trach DD, Cam PD, Ke NT, et al: Investigations into the safety and immunogenicity of a killed oral cholera vaccine developed in Viet Nam. Bull World Health Organ 2002;80:2–8.
  64. Svennerholm AM, Steele D: Microbial-gut interactions in health and disease. Progress in enteric vaccine development. Best Pract Res Clin Gastroenterol 2004;18:421–445.
  65. Savarino SJ, Hall ER, Bassily S, et al: Introductory evaluation of an oral, killed whole cell enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine in Egyptian infants. Pediatr Infect Dis J 2002;21:322–330.
  66. Qadri F, Ahmed T, Ahmed F, et al: Reduced doses of oral killed enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine is safe and immunogenic in Bangladeshi infants 6–17 months of age: dosing studies in different age groups. Vaccine 2006;24:1726–1733.
  67. Walker RI, Steele D, Aguado T: Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease. Vaccine 2007;25:2545–2566.
  68. Sack DA, Shimko J, Torres O, et al: Randomised, double-blind, safety and efficacy of a killed oral vaccine for enterotoxigenic E. coli diarrhoea of travellers to Guatemala and Mexico. Vaccine 2007;25:4392–4400.
  69. Coster TS, Hoge CW, VanDeVerg LL, et al: Vaccination against shigellosis with attenuated Shigella flexneri 2a strain SC602. Infect Immun 1999;67:3437–3443.
  70. Anonymous: Future needs and directions for Shigella vaccines. Wkly Epidemiol Rec 2006;81:51–58.
  71. Cohen D, Ashkenazi S, Green MS, et al: Double-blind vaccine-controlled randomised efficacy trial of an investigational Shigella sonnei conjugate vaccine in young adults. Lancet 1997;349:155–159.
  72. Wellinghausen N: Immunobiology of gestational zinc deficiency. Br J Nutr 2001;85 (suppl 2):S81–S86.
  73. Golden MH, Jackson AA, Golden BE: Effect of zinc on thymus of recently malnourished children. Lancet 1977;ii:1057–1059.

    External Resources

  74. Walker CF, Black RE: Zinc and the risk for infectious disease. Annu Rev Nutr 2004;24:255–275.

  

Author Contacts

David A. Sack
Department of International Health
Johns Hopkins Bloomberg School of Public Health
615 N Wolfe Street, Baltimore MD 21205 (USA)
Tel. +1 443 287 8795, Fax +1 410 502 6733, E-Mail dsack@jhsph.edu

  

Article Information

Published online: July 14, 2008
Number of Print Pages : 9
Number of Figures : 0, Number of Tables : 0, Number of References : 74

  

Publication Details

Annales Nestlé (English ed.)

Vol. 66, No. 2, Year 2008 (Cover Date: July 2008)

ISSN: 0517–8606 (Print), eISSN: 1661–4011 (Online)

For additional information: http://www.karger.com/ANE


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Oral vaccines which are intended for global use do not necessarily induce the same immune responses in all children worldwide. In fact, several vaccines often induce less frequent and lower mean antibody responses in children in developing countries, suggesting that the vaccines may be less protective among children in these areas. Though the reasons for this less vigorous response are not completely understood, it appears that nutrition-related factors, including both protein-calorie and micronutrient malnutrition, are important aspects in understanding the hyporesponsiveness seen in these children. Related issues including breastfeeding, interference from maternal placental antibodies, intestinal parasitic infections, intestinal mucosal damage and possibly maternal malnutrition during pregnancy also appear to be important. Vaccines designed for oral administration will need to be adjusted to these potential problems in order to maximize benefits for all children. Oral vaccines, when given to children in developing countries, may require higher doses of vaccine, booster doses, calorie, micronutrient and vitamin supplements, withdrawal of breast milk before vaccine administration, deworming medications or other measures to realize their full benefit.

© 2008 Nestec Ltd., Vevey/S. Karger AG, Basel


  

Author Contacts

David A. Sack
Department of International Health
Johns Hopkins Bloomberg School of Public Health
615 N Wolfe Street, Baltimore MD 21205 (USA)
Tel. +1 443 287 8795, Fax +1 410 502 6733, E-Mail dsack@jhsph.edu

  

Article Information

Published online: July 14, 2008
Number of Print Pages : 9
Number of Figures : 0, Number of Tables : 0, Number of References : 74

  

Publication Details

Annales Nestlé (English ed.)

Vol. 66, No. 2, Year 2008 (Cover Date: July 2008)

ISSN: 0517–8606 (Print), eISSN: 1661–4011 (Online)

For additional information: http://www.karger.com/ANE


Article / Publication Details

First-Page Preview
Abstract of Paper

Published online: 7/14/2008
Issue release date: July 2008

Number of Print Pages: 9
Number of Figures: 0
Number of Tables: 0

ISSN: 0517-8606 (Print)
eISSN: 1661-4011 (Online)

For additional information: http://www.karger.com/ANE


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Moore SE, Goldblatt D, Bates CJ, Prentice AM: Impact of nutritional status on antibody responses to different vaccines in undernourished Gambian children. Acta Paediatr 2003;92:170–176.
  2. Faden H: Results of a clinical study of polio vaccine: the Buffalo experience. Pediatr Infect Dis J 1991;10:973–975.
  3. Agarwal A, Sharma D, Kumari S, Khare S: Antibody response to three doses of standard and double dose of trivalent oral polio vaccine. Indian Pediatr 1991;28:1141–1145.
  4. Sabin AB: Vaccination against poliomyelitis in economically underdeveloped countries. Bull World Health Organ 1980;58:141–157.
  5. John TJ, Jayabal P: Oral polio vaccination of children in the tropics. 1. The poor seroconversion rates and the absence of viral interference. Am J Epidemiol 1972;96:263–269.
  6. Sutter RW, Suleiman AJ, Malankar P, et al: Trial of a supplemental dose of four poliovirus vaccines. N Engl J Med 2000;343:767–773.
  7. Triki H, Abdallah MV, Ben AR, et al: Influence of host related factors on the antibody response to trivalent oral polio vaccine in Tunisian infants. Vaccine 1997;15:1123–1129.
  8. Swartz TA, Skalska P, Gerichter CG, Cockburn WC: Routine administration of oral polio vaccine in a subtropical area. Factors possibly influencing seroconversion rates. J Hyg (Lond) 1972;70:719–726.
  9. Lepow ML, Warren RJ, Gray N, et al: Effect of Sabin type 1 poliomyelitis vaccine administered by mouth to newborn infants. N Engl J Med 1961;264:1071–1078.
  10. Plotkin SA, Katz M, Brown RE, Pagano JS: Oral poliovirus vaccination in newborn African infants. The inhibitory effect of breast feeding. Am J Dis Child 1966;111:27–30.
  11. Katz M, Plotkin SA: Oral polio immunization of the newborn infant; a possible method for overcoming interference by ingested antibodies. J Pediatr 1968;73:267–270.
  12. John TJ, Devarajan LV, Luther L, Vijayarathnam P: Effect of breast-feeding on seroresponse of infants to oral poliovirus vaccination. Pediatrics 1976;57:47–53.
  13. Myaux JA, Unicomb L, Besser RE, et al: Effect of diarrhea on the humoral response to oral polio vaccination. Pediatr Infect Dis J 1996;15:204–209.
  14. Bhaskaram P, Nair KM, Hemalatha P, et al: Systemic and mucosal immune response to polio vaccination with additional dose in newborn period. J Trop Pediatr 1997;43:232–234.
  15. Chopra K, Kundu S, Chowdhury DS: Antibody response of infants in tropics to five doses of oral polio vaccine. J Trop Pediatr 1989;35:19–23.
  16. Bahl R, Bhandari N, Wahed MA, et al: Vitamin A supplementation of women postpartum and of their infants at immunization alters breast milk retinol and infant vitamin A status. J Nutr 2002;132:3243–3248.
  17. Vesikari T, Isolauri E, d’Hondt E, et al: Protection of infants against rotavirus diarrhoea by RIT 4237 attenuated bovine rotavirus strain vaccine. Lancet 1984;i:977–981.

    External Resources

  18. Hanlon P, Hanlon L, Marsh V, et al: Trial of an attenuated bovine rotavirus vaccine (RIT 4237) in Gambian infants. Lancet 1987;i: 1342–1345.

    External Resources

  19. Georges-Courbot MC, Monges J, Siopathis MR, et al: Evaluation of the efficacy of a low-passage bovine rotavirus (strain WC3) vaccine in children in Central Africa. Res Virol 1991;142:405–411.
  20. De Mol P, Zissis G, Butzler JP, et al: Failure of live, attenuated oral rotavirus vaccine. Lancet 1986;ii:108.

    External Resources

  21. Joensuu J, Koskenniemi E, Pang XL, Vesikari T: Randomised placebo-controlled trial of rhesus-human reassortant rotavirus vaccine for prevention of severe rotavirus gastroenteritis. Lancet 1997;350:1205–1209.
  22. Rennels MB, Glass RI, Dennehy PH, et al: Safety and efficacy of high-dose rhesus-human reassortant rotavirus vaccines – report of the National Multicenter Trial. United States Rotavirus Vaccine Efficacy Group. Pediatrics 1996;97:7–13.
  23. Lanata CF, Midthun K, Black RE, et al: Safety, immunogenicity, and protective efficacy of one and three doses of the tetravalent rhesus rotavirus vaccine in infants in Lima, Peru. J Infect Dis 1996;174:268–275.
  24. Linhares AC, Gabbay YB, Mascarenhas JD, et al: Immunogenicity, safety and efficacy of tetravalent rhesus-human, reassortant rotavirus vaccine in Belem, Brazil. Bull World Health Organ 1996;74:491–500.
  25. Perez-Schael I, Guntinas MJ, Perez M, et al: Efficacy of the rhesus rotavirus-based quadrivalent vaccine in infants and young children in Venezuela. N Engl J Med 1997;337:1181–1187.
  26. Linhares AC, Lanata CF, Hausdorff WP, et al: Reappraisal of the Peruvian and Brazilian lower titer tetravalent rhesus-human reassortant rotavirus vaccine efficacy trials: analysis by severity of diarrhea. Pediatr Infect Dis J 1999;18:1001–1006.
  27. Ruiz-Palacios GM, Perez-Schael I, Velazquez FR, et al: Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 2006;354:11–22.
  28. Vesikari T, Matson DO, Dennehy P, et al: Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 2006;354:23–33.
  29. Pichichero ME: Effect of breast-feeding on oral rhesus rotavirus vaccine seroconversion: a metaanalysis. J Infect Dis 1990;162:753–755.
  30. Rennels MB, Wasserman SS, Glass RI, Keane VA: Comparison of immunogenicity and efficacy of rhesus rotavirus reassortant vaccines in breastfed and nonbreastfed children. US Rotavirus Vaccine Efficacy Group. Pediatrics 1995;96:1132–1136.
  31. Linhares AC, Carmo KB, Oliveira KK, et al: Nutritional status in relation to the efficacy of the rhesus-human reassortant, tetravalent rotavirus vaccine (RRV-TV) in infants from Belem, Para state, Brazil. Rev Inst Med Trop Sao Paulo 2002;44:13–16.

    External Resources

  32. Perez-Schael I, Salinas B, Tomat M, et al: Efficacy of the human rotavirus vaccine RIX4414 in malnourished children. J Infect Dis 2007;196:537–540.
  33. Lin FY, Ho VA, Khiem HB, et al: The efficacy of a Salmonella typhi Vi conjugate vaccine in two-to-five-year-old children. N Engl J Med 2001;344:1263–1269.
  34. Murphy JR, Grez L, Schlesinger L, et al: Immunogenicity of Salmonella typhi Ty21a vaccine for young children. Infect Immun 1991;59:4291–4293.
  35. Cryz SJ Jr, Vanprapar N, Thisyakorn U, et al: Safety and immunogenicity of Salmonella typhi Ty21a vaccine in young Thai children. Infect Immun 1993;61:1149–1151.
  36. Cooper PJ, Chico M, Sandoval C, et al: Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect Immun 2001;69:1574–1580.
  37. Lagos R, Avendano A, Horwitz I, et al: Tolerance and immunogenicity of an oral dose of CVD 103-HgR, a live attenuated Vibrio cholerae 01 strain: a double-blind study of Chilean adults. Rev Med Chil 1993;121:857–863.
  38. Simanjuntak CH, O’Hanley P, Punjabi NH, et al: Safety, immunogenicity, and transmissibility of single-dose live oral cholera vaccine strain CVD 103-HgR in 24- to 59-month-old Indonesian children. J Infect Dis 1993;168:1169–1176.
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