European Journal of Epidemiology

, Volume 34, Issue 10, pp 897–915 | Cite as

Measles, the need for a paradigm shift

  • Emilie JavelleEmail author
  • Philippe Colson
  • Philippe Parola
  • Didier Raoult


Measles vaccination schedules and targets of herd immunity have been designed according to the paradigm that the vaccine is as protective as natural infection, and the virus has remained of a single serotype over many decades. As a result, ongoing measles resurgence is mostly attributed to gaps in immunization. Using official data, we investigated the correlation between the rate of vaccine coverage reported and aggregated at the national level, and the incidence of cases. We discussed the limits of this indicator considered in isolation. We provide a literature overview of measles vaccine efficacy and failures. We questioned whether measles strains could escape the vaccine. Immunization tools and strategies for measles control deserve to be optimized in the current context.


Measles vaccine Efficacy Immunization Coverage Genotype 


Author contribution

All authors contributed to the review conception and design. Emilie Javelle made the literature search. Philippe Colson achieved virology laboratory testing presented in the article, and built some figures. Philippe Parola clinically managed the case of vaccine failure, helped in the study design and data collection. Didier Raoult had the idea for the article, reviewed data analyses and provided data interpretation. The first draft was written by Emilie Javelle and all authors commented on previous versions of the manuscript and critically revised the work. All authors read and approved the final manuscript.


This study was not funded.

Compliance with ethical standards

Conflict of interest

The authors declare that that they have no potential conflict of interest.

Supplementary material

10654_2019_569_MOESM1_ESM.pdf (570 kb)
Supplementary material 1 (PDF 569 kb)


  1. 1.
    Hopkins DR, Hinman AR, Koplan JP, Lane JM. The case for global measles eradication. Lancet. 1982;1:1396–8.PubMedCrossRefGoogle Scholar
  2. 2.
    WHO. Global Vaccine Action Plan 2011–2020. Accessed 10 April 2019.
  3. 3.
    WHO. Data, statistics and graphics. Accessed 7 April 2019.
  4. 4.
    Ministerio de Salud activa protocolo ante caso sospechoso de sarampión. Accessed 10 April 2019.
  5. 5.
    Atrasheuskaya AV, Kulak MV, Neverov AA, Rubin S, Ignatyev GM. Measles cases in highly vaccinated population of Novosibirsk, Russia, 2000–2005. Vaccine. 2008;26:2111–8.PubMedCrossRefGoogle Scholar
  6. 6.
    Breakwell L, Moturi E, Helgenberger L, et al. Measles outbreak associated with vaccine failure in adults-Federated States Of Micronesia, February–August 2014. MMWR Morb Mortal Wkly Rep. 2015;64:1088–92.PubMedCrossRefGoogle Scholar
  7. 7.
    Rosenthal SR, Clements CJ. Two-dose measles vaccination schedules. Bull World Health Organ. 1993;71:421–8.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Hethcote HW. Measles and rubella in the United States. Am J Epidemiol. 1983;117:2–13.PubMedCrossRefGoogle Scholar
  9. 9.
    Funk S, Knapp JK, Lebo E, et al. Combining serological and contact data to derive target immunity levels for achieving and maintaining measles elimination. bioRxiv 2019;201574 (not peer reviewed).Google Scholar
  10. 10.
    Orsoo O, Saw YM, Sereenen E, et al. Epidemiological characteristics and trends of a Nationwide measles outbreak in Mongolia, 2015–2016. BMC Public Health. 2019;19:201.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    WHO. WHO/UNICEF Joint Reporting Process. Accessed 7 April 2019.
  12. 12.
    Irons B, Dobbins JG. Caribbean vaccine managers. The Caribbean experience in maintaining high measles vaccine coverage. J Infect Dis. 2011;204(Suppl 1):S284–8.PubMedCrossRefGoogle Scholar
  13. 13.
  14. 14.
  15. 15.
    Muscat M, Marinova L, Mankertz A, et al. The measles outbreak in Bulgaria, 2009–2011: an epidemiological assessment and lessons learnt. Euro Surveill. 2016;21:30152.PubMedCrossRefGoogle Scholar
  16. 16.
    George F, Valente J, Augusto GF, et al. Measles outbreak after 12 years without endemic transmission, Portugal, February to May 2017. Euro Surveill. 2017;22:30548.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Lancella L, Di Camillo C, Vittucci AC, Boccuzzi E, Bozzola E, Villani A. Measles lessons in an anti-vaccination era:public health is a social duty, not a political option. Ital J Pediatr. 2017;43:102.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Muscat M, Ben Mamou M, Singh S, et al. Elimination of measles in the WHO European region-challenges persist. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2019;62:440–9 [Article in German].PubMedCrossRefGoogle Scholar
  19. 19.
    Han K, Chen S, Tang C, et al. The epidemiological and serological characteristics of measles in Dongguan, China, 2005–2014. Hum Vaccines Immunother. 2016;12:2181–7.CrossRefGoogle Scholar
  20. 20.
    Pan American Health Organization/World Health Organization. Epidemiological update: measles. 4 March 2019. Accessed 28 April 2019.
  21. 21.
    WHO. Measles–Brazil. 11 June 2018. Accessed 28 April 2019.
  22. 22.
    Gastañaduy PA, Budd J, Fisher N, et al. A measles outbreak in an underimmunized Amish Community in Ohio. N Engl J Med. 2016;375:1343–54.PubMedCrossRefGoogle Scholar
  23. 23.
    Pager T, Mays JC. New York declares measles emergency, requiring vaccinations in parts of Brooklyn. N. Y. Times. 2019; published online April 10. Accessed 14 April 2019.
  24. 24.
    de Munter AC, Tostmann A, Hahné SJM, Spaan DH, van Ginkel R, Ruijs WLM. Risk factors for persisting measles susceptibility:a case-control study among unvaccinated orthodox Protestants. Eur J Public Health. 2018;28:922–7.PubMedCrossRefGoogle Scholar
  25. 25.
    Godefroy R, Chaud P, Ninove L, et al. Measles outbreak in a French Roma community in the Provence-Alpes-Côte d’Azur region, France, May to July 2017. Int J Infect Dis. 2018;76:97–101.PubMedCrossRefGoogle Scholar
  26. 26.
    Komitova R, Kevorkyan A, Boykinova O, et al. Difficulties in achieving and maintaining the goal of measles elimination in Bulgaria. Rev Epidemiol Sante Publique. 2019;67:155–62.PubMedCrossRefGoogle Scholar
  27. 27.
    Phadke VK, Bednarczyk RA, Salmon DA, Omer SB. Association between vaccine refusal and vaccine-preventable diseases in the United States: a review of measles and pertussis. JAMA. 2016;315:1149–58.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Wadman M. Measles cases have tripled in Europe, fueled by Ukrainian outbreak. Sci. AAAS. 2019; published online Feb 12. Accessed 15 May 2019.
  29. 29.
    Cousins S. Measles: a global resurgence. Lancet Infect Dis. 2019;19:362–3.PubMedCrossRefGoogle Scholar
  30. 30.
    Obradovic Z, Balta S, Obradovic A, Mesic S. The impact of war on vaccine preventable diseases. Mater Socio-Medica. 2014;26:382–4.CrossRefGoogle Scholar
  31. 31.
    El Bcheraoui C, Jumaan AO, Collison ML, Daoud F, Mokdad AH. Health in Yemen: losing ground in war time. Glob Health. 2018;14:42.CrossRefGoogle Scholar
  32. 32.
    Paniz-Mondolfi AE, Tami A, Grillet ME, et al. Resurgence of vaccine-preventable diseases in Venezuela as a regional public health threat in the Americas. Emerg Infect Dis. 2019;25:625–32.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Lee AD, Clemmons NS, Patel M, Gastañaduy PA. International importations of measles virus into the United States during the Post-Elimination Era, 2001‒2016. J Infect Dis. 2018;219:1616–23.CrossRefGoogle Scholar
  34. 34.
    Rovida F, Brianese N, Piralla A, et al. Outbreak of measles genotype H1 in Northern Italy originated from a case imported from Southeast Asia, 2017. Clin Microbiol Infect. 2019;25:526–8.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Plans-Rubió P. Evaluation of the establishment of herd immunity in the population by means of serological surveys and vaccination coverage. Hum Vaccines Immunother. 2012;8:184–8.CrossRefGoogle Scholar
  36. 36.
    Leong WY. Measles cases hit record high in Europe in 2018. J Travel Med. 2018. Scholar
  37. 37.
    Enders JF, Peebles TC. Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proc Soc Exp Biol Med. 1954;86:277–86.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Katz SL, Kempe CH, Black FL, et al. Studies on an attenuated measles-virus vaccine. N Engl J Med. 1960;263:180–4.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    WHO. Immunological basis for immunization: measles (Update 2009). Accessed 10 April 2019.
  40. 40.
    de Swart RL, Yüksel S, Osterhaus ADME. Relative contributions of measles virus hemagglutinin- and fusion protein-specific serum antibodies to virus neutralization. J Virol. 2005;79:11547–51.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Bellini WJ, Rota PA. Biological feasibility of measles eradication. Virus Res. 2011;162:72–9.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Fulton BO, Sachs D, Beaty SM, et al. Mutational analysis of measles virus suggests constraints on antigenic variation of the glycoproteins. Cell Rep. 2015;11:1331–8.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Tahara M, Bürckert J-P, Kanou K, Maenaka K, Muller CP, Takeda M. Measles virus hemagglutinin protein epitopes: the basis of antigenic stability. Viruses. 2016;8:216.PubMedCentralCrossRefGoogle Scholar
  44. 44.
    Tamin A, Rota PA, Wang ZD, Heath JL, Anderson LJ, Bellini WJ. Antigenic analysis of current wild type and vaccine strains of measles virus. J Infect Dis. 1994;170:795–801.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Lech PJ, Tobin GJ, Bushnell R, et al. Epitope dampening monotypic measles virus hemagglutinin glycoprotein results in resistance to cocktail of monoclonal antibodies. PLoS ONE. 2013;8:e52306.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Rota WJB, Rota PA. Genetic diversity of wild-type measles viruses: implications for global measles elimination programs. Emerg Infect Dis. 1998;4:29–34.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    WHO. Nomenclature for describing the genetic characteristics of wild-type measles viruses (update). Part I. Wkly Epidemiol Rec. 2001;76:242–7.Google Scholar
  48. 48.
    CDC. Measles. Genetic analysis of measles virus. Lab Tools. 2019; published online Feb 26. Accessed 10 April 2019.
  49. 49.
    Bankamp B, Lopareva EN, Kremer JR, et al. Genetic variability and mRNA editing frequencies of the phosphoprotein genes of wild-type measles viruses. Virus Res. 2008;135:298–306.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Rota JS, Zhong-De W, Rota PA, Bellini WJ. Comparison of sequences of the H, F, and N coding genes of measles virus vaccine strains. Virus Res. 1994;31:317–30.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Demicheli V, Rivetti A, Debalini MG, Di Pietrantonj C. Vaccines for measles, mumps and rubella in children. Cochrane Database Syst Rev 2012;15:Cd004407.Google Scholar
  52. 52.
    Advisory Committee on Immunization Practices, Centers for Disease Control and Prevention (CDC). Immunization of health-care personnel: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR. 2011;60:1–45.Google Scholar
  53. 53.
    Uzicanin A, Zimmerman L. Field effectiveness of live attenuated measles-containing vaccines: a review of published literature. J Infect Dis. 2011;204(Suppl 1):S133–48.PubMedCrossRefGoogle Scholar
  54. 54.
    Yeung LF, Lurie P, Dayan G, et al. A limited measles outbreak in a highly vaccinated US boarding school. Pediatrics. 2005;116:1287–91.PubMedCrossRefGoogle Scholar
  55. 55.
    Lee MS, Lee LL, Chen HY, Wu YC, Horng CB. Post mass-immunization measles outbreak in Taoyuan County, Taiwan:dynamics of transmission, vaccine effectiveness, and herd immunity. Int J Infect Dis. 1998;3:64–9.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Doshi S, Khetsuriani N, Zakhashvili K, Baidoshvili L, Imnadze P, Uzicanin A. Ongoing measles and rubella transmission in Georgia, 2004–05: implications for the national and regional elimination efforts. Int J Epidemiol. 2009;38:182–91.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Akramuzzaman SM, Cutts FT, Hossain MJ, et al. Measles vaccine effectiveness and risk factors for measles in Dhaka, Bangladesh. Bull World Health Organ. 2002;80:776–82.PubMedPubMedCentralGoogle Scholar
  58. 58.
    Pillsbury A, Quinn H. An assessment of measles vaccine effectiveness, Australia, 2006–2012. West Pac Surveill Response J. 2015;6:43–50.CrossRefGoogle Scholar
  59. 59.
    Kuter BJ, Brown M, Wiedmann RT, Hartzel J, Musey L. Safety and immunogenicity of M-M-RII (Combination Measles-Mumps-Rubella Vaccine) in clinical trials of healthy children conducted between 1988 and 2009. Pediatr Infect Dis J. 2016;35:1011–20.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Fazilli A, Mir AA, Shah RJ, Bhat IA, Fomda BA, Bhat MA. Effect of second dose of measles vaccine on measles antibody status:a randomized controlled trial. Indian Pediatr. 2013;50:473–6.PubMedCrossRefGoogle Scholar
  61. 61.
    MMR-158 Study Group. A second dose of a measles-mumps-rubella vaccine administered to healthy four-to-six-year-old children:a phase III, observer-blind, randomized, safety and immunogenicity study comparing GSK MMR and MMR II with and without DTaP-IPV and varicella vaccines co-administration. Hum Vaccines Immunother. 2019;15:1–14.CrossRefGoogle Scholar
  62. 62.
    MMR-161 Study Group. Immunogenicity and safety of measles-mumps-rubella vaccine at two different potency levels administered to healthy children aged 12–15 months:A phase III, randomized, non-inferiority trial. Vaccine. 2018;36:5781–8.CrossRefGoogle Scholar
  63. 63.
    MMR-162 Study Group. Safety and immunogenicity of an upper-range release titer measles-mumps-rubella vaccine in children vaccinated at 12–15 months of age:a phase III, randomized study. Hum Vaccines Immunother. 2018;14:1–11.CrossRefGoogle Scholar
  64. 64.
    Klein NP, Abu-Elyazeed R, Povey M, et al. Immunogenicity and safety of a measles-mumps-rubella vaccine administered as a first dose to children aged 12–15 months: a phase III, randomized, noninferiority, lot-to-lot consistency study. J Pediatr Infect Dis Soc. 2019. Scholar
  65. 65.
    Abu-Elyazeed R, Jennings W, Severance R, et al. Immunogenicity and safety of a second dose of a measles-mumps-rubella vaccine administered to healthy participants 7 years of age or older: a phase III, randomized study. Hum Vaccines Immunother. 2018;14:2624–31.Google Scholar
  66. 66.
    MVDP author group, Cape S, Chaudhari A, et al. Safety and immunogenicity of dry powder measles vaccine administered by inhalation: a randomized controlled Phase I clinical trial. Vaccine. 2014;32:6791–7.CrossRefGoogle Scholar
  67. 67.
    Huang L-M, Lee B-W, Chan PC, Povey M, Henry O. Immunogenicity and safety of combined measles-mumps-rubella-varicella vaccine using new measles and rubella working seeds in healthy children in Taiwan and Singapore. Hum Vaccines Immunother. 2013;9:1308–15.CrossRefGoogle Scholar
  68. 68.
    Berry AA, Abu-Elyazeed R, Diaz-Perez C, et al. Two-year antibody persistence in children vaccinated at 12–15 months with a measles-mumps-rubella virus vaccine without human serum albumin. Hum Vaccines Immunother. 2017;13:1516–22.CrossRefGoogle Scholar
  69. 69.
    Mufson MA, Diaz C, Leonardi M, et al. Safety and immunogenicity of human serum albumin-free MMR vaccine in US children aged 12–15 months. J Pediatr Infect Dis Soc. 2015;4:339–48.CrossRefGoogle Scholar
  70. 70.
    Fisker AB, Nebie E, Schoeps A, et al. A two-center randomized trial of an additional early dose of measles vaccine: effects on mortality and measles antibody levels. Clin Infect Dis. 2018;66:1573–80.PubMedCrossRefGoogle Scholar
  71. 71.
    Brond M, Martins CL, Byberg S, et al. Randomized trial of 2 versus 1 dose of measles vaccine: effect on hospital admission of children after 9 months of age. J Pediatr Infect Dis Soc. 2018;7:226–33.CrossRefGoogle Scholar
  72. 72.
    Schoeps A, Nebié E, Fisker AB, et al. No effect of an additional early dose of measles vaccine on hospitalization or mortality in children: a randomized controlled trial. Vaccine. 2018;36:1965–71.PubMedCrossRefGoogle Scholar
  73. 73.
    Krause PJ, Gross PA, Barrett TL, et al. Quality standard for assurance of measles immunity among health care workers. The Infectious Diseases Society of America. Infect Control Hosp Epidemiol. 1994;15:193–9.PubMedCrossRefGoogle Scholar
  74. 74.
    Steingart KR, Thomas AR, Dykewicz CA, Redd SC. Transmission of measles virus in healthcare settings during a communitywide outbreak. Infect Control Hosp Epidemiol. 1999;20:115–9.PubMedCrossRefGoogle Scholar
  75. 75.
    Lake JG, Luvsansharav U-O, Hagan JE, et al. Healthcare-associated measles after a nationwide outbreak in Mongolia. Clin Infect Dis. 2018;67:288–90.PubMedCrossRefGoogle Scholar
  76. 76.
    Botelho-Nevers E, Gautret P, Biellik R, Brouqui P. Nosocomial transmission of measles: an updated review. Vaccine. 2012;30:3996–4001.PubMedCrossRefGoogle Scholar
  77. 77.
    Fiebelkorn AP, Redd SB, Kuhar DT. Measles in healthcare facilities in the United States during the postelimination Era, 2001–2014. Clin Infect Dis. 2015;61:615–8.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Patel MK, Orenstein WA. Classification of global measles cases in 2013–17 as due to policy or vaccination failure: a retrospective review of global surveillance data. Lancet Glob Health. 2019;7:313–20.CrossRefGoogle Scholar
  79. 79.
    Cherry JD, Zahn M. Clinical characteristics of measles in previously vaccinated and unvaccinated patients in California. Clin Infect Dis. 2018;67:1315–9.PubMedCrossRefGoogle Scholar
  80. 80.
    Paunio M, Hedman K, Davidkin I, et al. Secondary measles vaccine failures identified by measurement of IgG avidity: high occurrence among teenagers vaccinated at a young age. Epidemiol Infect. 2000;124:263–71.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Kakoulidou M, Ingelman-Sundberg H, Johansson E, et al. Kinetics of antibody and memory B cell responses after MMR immunization in children and young adults. Vaccine. 2013;31:711–7.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Carazo Perez S, De Serres G, Bureau A, Skowronski DM. Reduced antibody response to infant measles vaccination: effects based on type and timing of the first vaccine dose persist after the second dose. Clin Infect Dis. 2017;65:1094–102.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Meeting of the Strategic Advisory Group of Experts on Immunization. Conclusions and recommendations. Releve Epidemiol Hebd. 2015;2015(90):681–99.Google Scholar
  84. 84.
    Gans H, Yasukawa L, Rinki M, et al. Immune responses to measles and mumps vaccination of infants at 6, 9, and 12 months. J Infect Dis. 2001;184:817–26.PubMedCrossRefGoogle Scholar
  85. 85.
    CDC. Measles prevention: recommendations of the immunization practices Advisory Committee (ACIP). Accessed 10 April 2019.
  86. 86.
    Paunio M, Peltola H, Valle M, Davidkin I, Virtanen M, Heinonen OP. Twice vaccinated recipients are better protected against epidemic measles than are single dose recipients of measles containing vaccine. J Epidemiol Community Health. 1999;53:173–8.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    De Serres G, Boulianne N, Defay F, et al. Higher risk of measles when the first dose of a 2-dose schedule of measles vaccine is given at 12–14 months versus 15 months of age. Clin Infect Dis. 2012;55:394–402.PubMedCrossRefGoogle Scholar
  88. 88.
    Haralambieva IH, Kennedy RB, Ovsyannikova IG, Whitaker JA, Poland GA. Variability in humoral immunity to measles vaccine: new developments. Trends Mol Med. 2015;21:789–801.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Gomber S, Arora SK, Das S, Ramachandran VG. Immune response to second dose of MMR vaccine in Indian children. Indian J Med Res. 2011;134:302–6.PubMedPubMedCentralGoogle Scholar
  90. 90.
    Li Y, Chu SY, Yue C, et al. Immunogenicity and safety of measles-rubella vaccine co-administered with attenuated Japanese encephalitis SA 14-14-2 vaccine in infants aged 8 months in China: a non-inferiority randomised controlled trial. Lancet Infect Dis. 2019;19:402–9.PubMedCrossRefGoogle Scholar
  91. 91.
    Clifford HD, Hayden CM, Khoo S-K, et al. Genetic variants in the IL-4/IL-13 pathway influence measles vaccine responses and vaccine failure in children from Mozambique. Viral Immunol. 2017;30:472–8.PubMedCrossRefGoogle Scholar
  92. 92.
    Izadi S, Zahraei SM, Salehi M, Mohammadi M, Tabatabaei SM, Mokhtari-Azad T. Head-to-head immunogenicity comparison of Edmonston-Zagreb vs. AIK-C measles vaccine strains in infants aged 8–12 months: a randomized clinical trial. Vaccine. 2018;36:631–6.PubMedCrossRefGoogle Scholar
  93. 93.
    Markowitz LE, Preblud SR, Fine PE, Orenstein WA. Duration of live measles vaccine-induced immunity. Pediatr Infect Dis J. 1990;9:101–10.PubMedCrossRefGoogle Scholar
  94. 94.
    Krugman S. Present status of measles and rubella immunization in the United States: a medical progress report. J Pediatr. 1977;90:1–12.PubMedCrossRefGoogle Scholar
  95. 95.
    Kennedy RB, Ovsyannikova IG, Thomas A, Larrabee BR, Rubin S, Poland GA. Differential durability of immune responses to measles and mumps following MMR vaccination. Vaccine. 2019;37:1775–84.PubMedCrossRefGoogle Scholar
  96. 96.
    Poethko-Müller C, Mankertz A. Seroprevalence of measles-, mumps- and rubella-specific IgG antibodies in German children and adolescents and predictors for seronegativity. PLoS ONE. 2012;7:42867.CrossRefGoogle Scholar
  97. 97.
    Kim S-K, Park H-Y, Kim S-H. A third dose of measles vaccine is needed in young Korean health care workers. Vaccine. 2018;36:3888–9.PubMedCrossRefGoogle Scholar
  98. 98.
    Cherry JD, Feigin RD, Shackelford PG, Hinthorn DR, Schmidt RR. A clinical and serologic study of 103 children with measles vaccine failure. J Pediatr. 1973;82:802–8.PubMedCrossRefGoogle Scholar
  99. 99.
    Anders JF, Jacobson RM, Poland GA, Jacobsen SJ, Wollan PC. Secondary failure rates of measles vaccines: a metaanalysis of published studies. Pediatr Infect Dis J. 1996;15:62.PubMedCrossRefGoogle Scholar
  100. 100.
    Ammari LK, Bell LM, Hodinka RL. Secondary measles vaccine failure in healthcare workers exposed to infected patients. Infect Control Hosp Epidemiol. 1993;14:81–6.PubMedCrossRefGoogle Scholar
  101. 101.
    Pannuti CS, Morello RJ, de Moraes JC, et al. Identification of primary and secondary measles vaccine failures by measurement of immunoglobulin G avidity in measles cases during the 1997 São Paulo epidemic. Clin Diagn Lab Immunol. 2004;11:119–22.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Santibanez S, Prosenc K, Lohr D, et al. Measles virus spread initiated at international mass gatherings in Europe, 2011. Euro Surveill 2014;19(35):20891.PubMedCrossRefGoogle Scholar
  103. 103.
    Orosz L, Gáspár G, Rózsa Á, Rákos N, Sziveri S, Bosnyákovits T. Epidemiological situation of measles in Romania, Italy, and Hungary: on what threats should we focus nowadays? Acta Microbiol Immunol Hung. 2018;65:127–34.PubMedCrossRefGoogle Scholar
  104. 104.
    Komabayashi K, Seto J, Tanaka S, et al. The largest measles outbreak, including 38 modified measles and 22 typical measles cases in its elimination Era in Yamagata, Japan, 2017. Jpn J Infect Dis. 2018;71:413–8.PubMedCrossRefGoogle Scholar
  105. 105.
    Hahné SJM, Nic Lochlainn LM, van Burgel ND, et al. Measles outbreak among previously immunized healthcare workers, The Netherlands, 2014. J Infect Dis. 2016;214:1980–6.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Rosen JB, Rota JS, Hickman CJ, et al. Outbreak of measles among persons with prior evidence of immunity, New York City, 2011. Clin Infect Dis. 2014;58:1205–10.PubMedCrossRefGoogle Scholar
  107. 107.
    WHO. Manual for the Laboratory-based Surveillance of Measles, Rubella, and Congenital Rubella Syndrome. Accessed 18 April 2019.
  108. 108.
    Haralambieva IH, Kennedy RB, Ovsyannikova IG, Schaid DJ, Poland GA. Current perspectives in assessing humoral immunity after measles vaccination. Expert Rev Vaccines. 2019;18:75–87.PubMedCrossRefGoogle Scholar
  109. 109.
    Fatemi Nasab GS, Salimi V, Abbasi S, Adjami Nezhad Fard F, Mokhtari Azad T. Comparison of neutralizing antibody titers against outbreakassociated measles genotypes (D4, H1 and B3) in Iran. Pathog Dis. 2016;74:ftw089.PubMedCrossRefGoogle Scholar
  110. 110.
    Klingele M, Hartter HK, Adu F, Ammerlaan W, Ikusika W, Muller CP. Resistance of recent measles virus wild-type isolates to antibody-mediated neutralization by vaccinees with antibody. J Med Virol. 2000;62:91–8.PubMedCrossRefGoogle Scholar
  111. 111.
    Bellini W. Genetic diversity of wild-type measles viruses: implications for global measles elimination programs. Emerg Infect Dis. 1998;4:29–35.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Rota PA, Brown K, Mankertz A, et al. Global distribution of measles genotypes and measles molecular epidemiology. J Infect Dis. 2011;204(Suppl 1):S514–23.PubMedCrossRefGoogle Scholar
  113. 113.
    Mulders MN, Rota PA, Icenogle JP, et al. Global measles and rubella laboratory network support for elimination goals, 2010–2015. MMWR. 2016;65:438–42.PubMedGoogle Scholar
  114. 114.
    Ackley SF, Hacker JK, Enanoria WTA, et al. Genotype-specific measles transmissibility: a branching process analysis. Clin Infect Dis. 2018;66:1270–5.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Gil H, Fernández-García A, Mosquera MM, et al. Measles virus genotype D4 strains with non-standard length M-F non-coding region circulated during the major outbreaks of 2011–2012 in Spain. PLoS ONE. 2018;13:e0199975.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Muñoz-Alía MÁ, Muller CP, Russell SJ. Antigenic drift defines a new D4 subgenotype of measles virus. J Virol. 2017;91:e00209–17.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Xu S, Zhang Y, Rivailler P, et al. Evolutionary genetics of genotype H1 measles viruses in China from 1993 to 2012. J Gen Virol. 2014;95:1892–9.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Xu W, Tamin A, Rota JS, Zhang L, Bellini WJ, Rota PA. New genetic group of measles virus isolated in the People’s Republic of China. Virus Res. 1998;54:147–56.PubMedCrossRefGoogle Scholar
  119. 119.
    Finsterbusch T, Wolbert A, Deitemeier I, et al. Measles viruses of genotype H1 evade recognition by vaccine-induced neutralizing antibodies targeting the linear haemagglutinin noose epitope. J Gen Virol. 2009;90:2739–45.PubMedCrossRefGoogle Scholar
  120. 120.
    Shi J, Zheng J, Huang H, et al. Measles incidence rate and a phylogenetic study of contemporary genotype H1 measles strains in China: is an improved measles vaccine needed? Virus Genes. 2011;43:319–26.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Pütz MM, Hoebeke J, Ammerlaan W, Schneider S, Muller CP. Functional fine-mapping and molecular modeling of a conserved loop epitope of the measles virus hemagglutinin protein. Eur J Biochem. 2003;270:1515–27.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Zharikova D, Mozdzanowska K, Feng J, Zhang M, Gerhard W. Influenza type A virus escape mutants emerge in vivo in the presence of antibodies to the ectodomain of matrix protein 2. J Virol. 2005;79:6644–54.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Weinberger DM, Malley R, Lipsitch M. Serotype replacement in disease following pneumococcal vaccination: a discussion of the evidence. Lancet. 2011;378:1962–73.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Santibanez S, Niewiesk S, Heider A, et al. Probing neutralizing-antibody responses against emerging measles viruses (MVs):immune selection of MV by H protein-specific antibodies? J Gen Virol. 2005;86:365–74.PubMedCrossRefGoogle Scholar
  125. 125.
    Béraud G, Abrams S, Beutels P, Dervaux B, Hens N. Resurgence risk for measles, mumps and rubella in France in 2018 and 2020. Euro Surveill. 2018;23:1700796.PubMedCentralCrossRefPubMedGoogle Scholar
  126. 126.
    Hummel KB, Lowe L, Bellini WJ, Rota PA. Development of quantitative gene-specific real-time RT-PCR assays for the detection of measles virus in clinical specimens. J Virol Methods. 2006;132:166–73.PubMedCrossRefGoogle Scholar
  127. 127.
    Bankamp B, Byrd-Leotis LA, Lopareva EN, et al. Improving molecular tools for global surveillance of measles virus. J Clin Virol. 2013;58:176–82.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Roy F, Mendoza L, Hiebert J, et al. Rapid identification of measles virus vaccine genotype by real-time PCR. J Clin Microbiol. 2017;55:735–43.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Ripa T, Nilsson P. A variant of Chlamydia trachomatis with deletion in cryptic plasmid: implications for use of PCR diagnostic tests. Euro Surveill. 2006;11:3076.Google Scholar
  130. 130.
    WHO. Standardization of the nomenclature for describing the genetic characteristics of wild-type measles viruses. Weekly Epidemiol Rec. 1998;73:265–72.Google Scholar
  131. 131.
    Murti M, Krajden M, Petric M, et al. Case of vaccine-associated measles five weeks post-immunisation, British Columbia, Canada, October 2013. Euro Surveill. 2013;18:20649.PubMedCrossRefPubMedCentralGoogle Scholar
  132. 132.
    Jorba J, Diop OM, Iber J, et al. Update on vaccine-derived polioviruses—worldwide, January 2017-June 2018. MMWR. 2018;67:1189–94.PubMedPubMedCentralGoogle Scholar
  133. 133.
    Quick J, Loman NJ, Duraffour S, et al. Real-time, portable genome sequencing for Ebola surveillance. Nature. 2016;530:228–32.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Barbot O. New York City Department of Health and Mental Hygiene. Order of the Commissioner. 9 April 2019. Accessed 28 April 2019.
  135. 135.
    Heywood AE. Measles: a re-emerging problem in migrants and travellers. J Travel Med. 2018. Scholar
  136. 136.
    Becker R. How measles snuck into California despite strict vaccine legislation. The Verge. 2019; published online Feb 28. Accessed 28 April 2019.
  137. 137.
    Barraza L, Schmit C, Hoss A. The latest in vaccine policies: selected issues in school vaccinations, healthcare worker vaccinations, and pharmacist vaccination authority laws. J Law Med Ethics. 2017;45:16–9.PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    McKee A, Ferrari MJ, Shea K. Correlation between measles vaccine doses:implications for the maintenance of elimination. Epidemiol Infect. 2018;146:468–75.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Marin M. Recommendation of the advisory committee on immunization practices for use of a third dose of mumps virus-containing vaccine in persons at increased risk for mumps during an outbreak. MMWR. 2018;67:33–8.PubMedPubMedCentralGoogle Scholar
  140. 140.
    Fiebelkorn AP, Coleman LA, Belongia EA, et al. Measles virus neutralizing antibody response, cell-mediated immunity, and IgG antibody avidity before and after a third dose of measles-mumps-rubella vaccine in young adults. J Infect Dis. 2016;213:1115–23.PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    Van Valen L. A new evolutionary law. Evol Therory. 1973;1:1–30.Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laveran Military Teaching HospitalMarseilleFrance
  2. 2.IHU-Méditerranée InfectionMarseilleFrance
  3. 3.IRD, AP-HM, SSA, VITROMEAix Marseille UniversityMarseilleFrance
  4. 4.IRD, AP-HM, SSA, MEPHIAix Marseille UniversityMarseilleFrance

Personalised recommendations