Volume 79, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


In Mozambique, as in many sub-Saharan countries, measles remains a public health problem. We conducted cross-sectional surveys in which we assessed measles-specific antibodies in serum and breast milk by plaque reduction neutralization (PRN) assay and measles secretory IgA in breast milk by enzyme-linked immunosorbent assay. A total of 151 persons < 1 month to 23 years of age were surveyed; 81 (53.6%) of 151 had PRN titers equal to or above the protective level (≥ 200 mIU/mL). We found many serosusceptible persons, including 20.5% in whom no PRN antibody was detected. Almost all (96%) infants 6–8 months of age had non-protective PRN titers. Overall, 20.7% (6 of 29) of persons known to have received measles vaccine had non-protective titers. The geometric mean titer (GMT) of breast milk PRN antibodies was 41.6 mIU/mL (95% confidence interval [CI] = 34.0–51.0 mIU/mL) and the secretory IgA GMT was 227.6 (EU/mL) (95% CI = 179.1–289.1 EU/mL). The PRN titers of breast milk tended to increase with age. A notable proportion of the population in Manhiça, Mozambique apparently remains susceptible to clinical measles despite recent mass vaccination campaigns.


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  1. Bryce J, Boschi-Pinto C, Shibuya K, Black RE, and the WHO Child Health Epidemiology Refrence Group, 2005. WHO estimates of the causes of death in children. Lancet 365 : 1147–1152.
  2. Cutts F, Monteiro O, Tabard P, Cliff J, 1994. Measles control in Mapuo, Mozambique using a single dose of Schwarz vaccine at age 9 months. Bull World Health Organ 72 : 227–231.
  3. Krugman S, 1983. Further-attenuated measles vaccine: characteristics and use. Rev Infect Dis 5 : 477–481.
  4. Tiulchinsky TH, Ginsberg GM, Abed Y, Angeles MT, Akukwe C, Bonn J, 1993. Measles control in developing and developed countries: the case for a two-dose policy. Bull World Health Organ 71 : 93–103.
  5. Godoy P, Domínguez A, Salleras L, 1999. Measles: effect of a two-dose vaccination programme in Catalonia, Spain. Bull World Health Organ 77 : 132–137.
  6. Renegar KB, Jackson GD, Mestecky J, 1998. In vitro comparison of the biologic activities of monoclonal monomeric IgA, polymeric IgA, and secretory IgA. J Immunol 160 : 1219–1223.
  7. de Francisco A, Hall AJ, Unicomb L, Chakraborty L, Yunus M, Sack RB, 1998. Maternal measles antibody decay in rural Bangladeshi infants: implications for vaccination schedules. Vaccine 16 : 564–568.
  8. Tapia MD, Sow SO, Medina-Moreno S, Lim Y, Pasetti MF, Kotloff K, Levine MM, 2005. A serosurvey to identify the window of vulnerability to wild-type measles among infants in rural Mali. Am J Trop Med Hyg 73 : 26–31.
  9. Mossong J, O’Callaghan C, Ratham S, 2001. Modelling antibody response to measles vaccine and subsequent waning of immunity in a low exposure population. Vaccine 19 : 523–529.
  10. Lee MS, Chien LJ, Yueh YY, Lu CF, 2001. Measles seroepidemiology and decay rate of vaccine-induced measles IgG titers in Taiwan, 1995–1999. Vaccine 19 : 4644–4651.
  11. Tipples GA, Hamkar R, Mohktari-Azad T, Gray M, Parkyn G, Head C, Ratnam S, 2003. Assessment of immunoglobulin M enzyme immunoassays for diagnosis of measles. J Clin Microbiol 41 : 4790–4792.
  12. Weaver LT, Arthur HM, Bunn JE, Thomas JE, 1998. Human milk IgA concentrations during the first year of lactation. Arch Dis Child 78 : 235–239.
  13. Chen RT, Markowitz LE, Albrecht P, Stewart JA, Mofenson LM, Preblud SR, Orenstein WA, 1990. Measles antibody: reevaluation of protective titer. J Infect Dis 162 : 1036–1042.
  14. Ratnam S, Gadag V, West R, Burris J, Oates E, Stead F, Bouilianne N, 1995. Comparison of commercial enzyme immunoassays kits with plaque reduction neutralization test for detection of measles virus antibody. J Clin Microbiol 33 : 811–815.
  15. Cohen BJ, Audet S, Andrews N, Beeler J, 2007. Plaque reduction neutralization test for measles antibodies: description of a standardized laboratory method for use in immunogenicity studies of aerosol vaccination. Vaccine 26 : 59–66.
  16. Cutts F, 1993. Module 7. Measles, The Immunological Basis for Immunization Series. Geneva. World Health Organization.
  17. Hanson LA, Hahn-Zoric M, Berndes M, Ashraf R, Herias V, Jalil F, Butta TI, Laeeg A, Mattsby-Baltzer I, 1994. Breast feeding: overview and breast milk immunology. Acta Paediatr Jpn 36 : 557–561.
  18. Gordon AE, Saadi AT, MacKenzie DA, Molony N, James VS, Weir DM, Busuttil A, Blackwell CC, 1999. The protective effect of breast feeding in relation to sudden infant death syndrome (SIDS): III. Detection of IgA antibodies in human milk that bind to bacterial toxins implicated in SIDS. FEMS Immunol Med Microbiol 25 : 175–182.
  19. Thomas JE, Austin S, Dale A, McClean P, Harding M, Coward WA, Weaver LT, 1993. Protection by human milk IgA against Helicobacter pylori infection in infancy. Lancet 342 : 121.
  20. Brandtzaeg P, 2007. Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25 : 5467–5484.
  21. Oddy WH, 2004. A review of the effects of breastfeeding on respiratory infections, atopy, and childhood asthma. J Asthma 41 : 605–621.
  22. Cushing AH, Samet JM, Lambert WE, Skipper BJ, Hunt WC, Young SA, McLaren LC, 1998. Breastfeeding reduces risk of respiratory illness in infants. Am J Epidemiol 147 : 863–870.
  23. Ahmed F, Clements JD, Rao MR, Sack DA, Khan MR, Haque E, 1992. Community-based evaluation of the effect of breast-feeding on the risk of microbiologically confirmed or clinically presumptive shigellosis in Bangladeshi children. Pediat 90 : 406–411.
  24. Elahi S, Buchanan RM, Babiuk LA, Gerdts V, 2006. Maternal immunity provides protection against pertussis in newborn piglets. Infect Immun 74 : 2619–2627.
  25. Oyedele OO, Odemuyiwa SO, Ammerlaan W, Muller CP, Adu FD, 2004. Passive immunity of measles in the breastmilk and cord blood of some Nigerian subjects. J Trop Pediatr 51 : 45–48.
  26. Alonso PL, 2002. Manhiça DSS, Mozambique. Indepth Network 1 : 189–195.
  27. Novela M, 2006. Incidência de Sarampo em Moçambique. Reunião Nacional de Doenças Preveníveis por Cacinas e PAV. Maputo, Mozambique 28–30 Junho 2006.
  28. Relatório de Actividades da Direcção Distrital de Saúde da Manhiça. 2002. Manhiça, Mozambique.
  29. Arguelles MH, Orellana ML, Castello AA, Villegas GA, Masini M, Belizan AL, Gonzalez Ayala S, Vera OD, Glikmann G, 2006. Measles virus-specific antibodies levels in individuals in Argentina who received a one-dose vaccine. J Clin Microbiol 44 : 2733–2738.
  30. Nates SV, Giordano MO, Medeot SI, Martinez LC, Baudagna AM, Naretto E, Garrido P, De Wolff CD, 1998. Loss of maternally derived measles immunity in Argentinian infantis. Pediatr Infec Dis J 17 : 313–316.
  31. Scott S, Cumberland P, Shulman CE, Cousens S, Cohen BJ, Brown DW, Bulmer JN, Dorman EK, Kawuondo K, Marsh K, Cutts F, 2005. Neonatal measles immunity in rural Kenya: the influence of HIV and placental malaria infections on placental transfer of antibodies and levels of antibody in maternal and cord serum samples. J Infect Dis 191 : 1854–1860.
  32. Abanamy AK, Salman H, Abdulazeem M, 1991. Follow-up study for measles maternal antibodies and seroconversion after measles vaccination. Ann Saudi Med 11 : 51–53.
  33. Gans HA, Arvin AM, Galinus J, Logan L, DeHovitz R, Maldonado Y, 1998. Deficiency of the humoral immune response to measles vaccine in infants immunized at age 6 months. JAMA 280 : 527–532.
  34. Good RA, Zak S, 1956. Disturbances in gamma globulin synthesis as experiments of nature. Pediatrics 18 : 109–149.
  35. Burnet FM, 1968. Measles as an index of immunological function. Lancet 2 : 610–613.
  36. Davidkin I, Valle M, 1998. Vaccine-induced measles virus antibodies after two doses of combined measles, mumps and rubella vaccine: a 12-year follow-up in two cohorts. Vaccine 16 : 2052–2057.
  37. El Mubarak HS, Ibrahim SA, Vos HW, Mukhtar MM, Mustafa OA, Wild TF, Osterhaus AD, de Swart RL, 2004. Measles virus protein-specific IgM, IgA, and IgG subclass responses during the acute and convalescent phase of infection. J Med Virol 72 : 290–298.
  38. Audet S, Virata-Theimer ML, Beeler JA, Scott DE, Frazier DJ, Mikolajczyk MG, Eller N, Chen FM, My Yu, 2006. Measles-virus-neutralizing antibodies in intravenous immunoglobulins. J Infect Dis 194 : 781–789.
  39. Asensi MT, Martinez-Costa C, Buesa J, 2006. Anti-rotavirus antibodies in human milk: quantification and neutralizing activity. J Peadiatr Gastr Nutr 40 : 560–567.
  40. Atkinson WL, Orenstein WA, Krugman S, 1992. The ressurgence of measles in the United States, 1989–1990. Annu Rev Med 43 : 451–463.

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  • Received : 05 Mar 2008
  • Accepted : 06 Jul 2008

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