High concentrations of measles neutralizing antibodies and high-avidity measles IgG accurately identify measles reinfection cases

Clinical and Vaccine Immunology

Volumn 23, Issue 8, 2016, Pages 707-716

  Sowers, Sun B ^a   Rota, Jennifer S ^a   Hickman, Carole J ^a   Mercader, Sara ^a   Redd, Susan ^a   McNall, Rebecca J ^a   Williams, Nobia ^a   McGrew, Marcia ^a   Walls, M Laura ^a   Rota, Paul A ^a   Bellini, William J ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; MEASLES ANTIBODY; MEASLES MUMPS RUBELLA VACCINE; NEUTRALIZING ANTIBODY; IMMUNOGLOBULIN G; VIRUS ANTIBODY;

ADOLESCENT; ADULT; AGED; ANTIBODY BLOOD LEVEL; ANTIBODY TITER; AREA UNDER THE CURVE; ARTICLE; BLOOD SAMPLING; CHILD; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MEASLES; PRIORITY JOURNAL; RASH; REAL TIME POLYMERASE CHAIN REACTION; RECEIVER OPERATING CHARACTERISTIC; REINFECTION; SENSITIVITY AND SPECIFICITY; ANTIBODY AFFINITY; BLOOD; DIAGNOSTIC TEST; EVALUATION STUDY; IMMUNOLOGY; MEASLES VIRUS; MIDDLE AGED; PRESCHOOL CHILD; PROCEDURES; RECURRENT DISEASE; SERODIAGNOSIS; UNITED STATES; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; CHILD; CHILD, PRESCHOOL; DIAGNOSTIC TESTS, ROUTINE; FEMALE; HUMANS; IMMUNOGLOBULIN G; MALE; MEASLES; MEASLES VIRUS; MIDDLE AGED; NEUTRALIZATION TESTS; RECURRENCE; SENSITIVITY AND SPECIFICITY; UNITED STATES; YOUNG ADULT;

EID: 84982889622     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00268-16     Document Type: Article

References (60)

1. Papania MJ, Wallace GS, Rota PA, Icenogle JP, Fiebelkorn AP, Armstrong GL, Reef SE, Redd SB, Abernathy ES, Barskey AE, Hao L, McLean HQ, Rota JS, Bellini WJ, Seward JF. 2014. Elimination of endemic measles, rubella, and congenital rubella syndrome from the western hemisphere: the US experience. JAMA Pediatr 168:148-155. http://dx.doi.org/10.1001/jamapediatrics.2013.4342.
2. Fiebelkorn AP, Redd SB, Gallagher K, Rota PA, Rota J, Bellini W, Seward J. 2010. Measles in the United States during the postelimination era. J Infect Dis 202:1520-1528. http://dx.doi.org/10.1086/656914.
3. Orenstein WA, Papania MJ, Wharton ME. 2004. Measles elimination in the United States. J Infect Dis 189(Suppl 1):S1-S3. http://dx.doi.org/10.1086/377693.
4. Perry RT, Gacic-Dobo M, Dabbagh A, Mulders MN, Strebel PM, Okwo-Bele JM, Rota PA, Goodson JL, Centers for Disease Control and Prevention. 2014. Global control and regional elimination of measles, 2000-2012. MMWR Morb Mortal Wkly Rep 63:103-107. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6305a5.htm.
5. Vega JS, Escobedo M, Schulte CR, Rosen JB, Schauer S, Wiseman R, Lippold SA, Regan JJ, Centers for Disease Control and Prevention. 2014. Notes from the field: measles transmission at a domestic terminal gate in an international airport-United States, January 2014. MMWR Morb Mortal Wkly Rep 63:1211. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6350a9.htm.
6. Halsey N, Salmon D. 2015. Measles at Disneyland, a problem for all ages. Ann Intern Med 162:655-656. http://dx.doi.org/10.7326/M15-0447.
7. Centers for Disease Control and Prevention. 2013. Measles-United States, January 1-August 24, 2013. MMWR Morb Mortal Wkly Rep 62:741-743. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6236a2.htm.
8. Gastañaduy PA, Redd SB, Fiebelkorn AP, Rota JS, Rota PA, Bellini WJ, Seward JF, Wallace GS, Division of Viral Disease, National Center for Immunization and Respiratory Diseases, CDC. 2014. Measles-United States, January 1-May 23, 2014. MMWR Morb Mortal Wkly Rep 63:496-499. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6322a4.htm.
9. Christopher PJ, MacDonald PA, Murphy AM, Buckley PR. 1983. Measles in the 1980s. Med J Aust 2:488-491.
10. Mercader S, Garcia P, Bellini WJ. 2012. Measles virus IgG avidity assay for use in classification of measles vaccine failure in measles elimination settings. Clin Vaccine Immunol 19:1810-1817. http://dx.doi.org/10.1128/CVI.00406-12.
11. Rosen JB, Rota JS, Hickman CJ, Sowers SB, Mercader S, Rota PA, Bellini WJ, Huang AJ, Doll MK, Zucker JR, Zimmerman CM. 2014. Outbreak of measles among persons with prior evidence of immunity, New York City, 2011. Clin Infect Dis 58:1205-1210. http://dx.doi.org/10.1093/cid/ciu105.
12. Hamkar R, Mahmoodi M, Nategh R, Jelyani KN, Eslami MB, Mohktari-Azad T. 2006. Distinguishing between primary measles infection and vaccine failure reinfection by IgG avidity assay. East Mediterr Health J 12:775-782.
13. Mosquera MM, de Ory F, Gallardo V, Cuenca L, Morales M, Sanchez-Yedra W, Cabezas T, Hernandez JM, Echevarria JE. 2005. Evaluation of diagnostic markers for measles virus infection in the context of an outbreak in Spain. J Clin Microbiol 43:5117-5121. http://dx.doi.org/10.1128/JCM.43.10.5117-5121.2005.
14. Anders JF, Jacobson RM, Poland GA, Jacobsen SJ, Wollan PC. 1996. Secondary failure rates of measles vaccines: a metaanalysis of published studies. Pediatr Infect Dis J 15:62-66. http://dx.doi.org/10.1097/00006454-199601000-00014.
15. Ammari LK, Bell LM, Hodinka RL. 1993. Secondary measles vaccine failure in healthcare workers exposed to infected patients. Infect Control Hosp Epidemiol 14:81-86.
16. Chen RT, Markowitz LE, Albrecht P, Stewart JA, Mofenson LM, Preblud SR, Orenstein WA. 1990. Measles antibody: reevaluation of protective titers. J Infect Dis 162:1036-1042. http://dx.doi.org/10.1093/infdis/162.5.1036.
17. Atrasheuskaya AV, Blatun EM, Neverov AA, Kameneva SN, Maksimov NL, Karpov IA, Ignatyev GM. 2005. Measles in Minsk, Belarus, 2001-2003: clinical, virological and serological parameters. J Clin Virol 34:179-185. http://dx.doi.org/10.1016/j.jcv. 2004.11.024.
18. Rota JS, Hickman CJ, Sowers SB, Rota PA, Mercader S, Bellini WJ. 2011. Two case studies of modified measles in vaccinated physicians exposed to primary measles cases: high risk of infection but low risk of transmission. J Infect Dis 204(Suppl 1):S559-S563. http://dx.doi.org/10.1093/infdis/jir098.
19. Aaby P, Bukh J, Leerhoy J, Lisse IM, Mordhorst CH, Pedersen IR. 1986. Vaccinated children get milder measles infection: a community study from Guinea-Bissau. J Infect Dis 154:858-863. http://dx.doi.org/10.1093/infdis/154.5.858.
20. Moore C, Cottrell S, Hoffmann J, Carr M, Evans H, Dunford L, Lawson H, Brown KE, Jones R. 2015. Self-collected buccal swabs and rapid, real-time PCR during a large measles outbreak in Wales: Evidence for the protective effect of prior MMR immunisation. J Clin Virol 67:1-7. http://dx.doi.org/10.1016/j.jcv. 2015.03.012.
21. Mitchell P, Turner N, Jennings L, Dong H. 2013. Previous vaccination modifies both the clinical disease and immunological features in children with measles. J Prim Health Care 5:93-98.
22. Hickman CJ, Hyde TB, Sowers SB, Mercader S, McGrew M, Williams NJ, Beeler JA, Audet S, Kiehl B, Nandy R, Tamin A, Bellini WJ. 2011. Laboratory characterization of measles virus infection in previously vaccinated and unvaccinated individuals. J Infect Dis 204(Suppl 1):S549-S558. http://dx.doi.org/10.1093/infdis/jir106.
23. Hummel KB, Erdman DD, Heath J, Bellini WJ. 1992. Baculovirus expression of the nucleoprotein gene of measles virus and utility of the recombinant protein in diagnostic enzyme immunoassays. J Clin Microbiol 30:2874-2880.
24. Hummel KB, Lowe L, Bellini WJ, Rota PA. 2006. Development of quantitative gene-specific real-time RT-PCR assays for the detection of measles virus in clinical specimens. J Virol Methods 132:166-173. http://dx.doi.org/10.1016/j.jviromet.2005.10.006.
25. Cohen BJ, Audet S, Andrews N, Beeler J, test WHO Working Group on Measles Plaque Reduction Neutralization Test. 2007. Plaque reduction neutralization test for measles antibodies: Description of a standardised laboratory method for use in immunogenicity studies of aerosol vaccination. Vaccine 26:59-66. http://dx.doi.org/10.1016/j.vaccine.2007.10.046.
26. Greiner M, Pfeiffer D, Smith RD. 2000. Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests. Prev Vet Med 45:23-41. http://dx.doi.org/10.1016/S0167-5877 (00) 00115-X.
27. Hanley JA, McNeil BJ. 1982. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29-36. http://dx.doi.org/10.1148/radiology.143.1.7063747.
28. Kutty P, Rota J, Bellini W, Redd S, Barskey A, Wallace G. 2013. VPD surveillance manual, 6th edition, chapter 7: measles. http://stacks.cdc.gov/view/cdc/35640. Accessed 27 June 2016.
29. Nagy G, Kosa S, Takatsy S, Koller M. 1984. The use of IgM tests for analysis of the causes of measles vaccine failures: experience gained in an epidemic in Hungary in 1980 and 1981. J Med Virol 13:93-103. http://dx.doi.org/10.1002/jmv. 1890130111.
30. Smith FR, Curran AS, Raciti KA, Black FL. 1982. Reported measles in persons immunologically primed by prior vaccination. J Pediatr 101:391-393. http://dx.doi.org/10.1016/S0022-3476 (82) 80064-4.
31. Edmonson MB, Addiss DG, McPherson JT, Berg JL, Circo SR, Davis JP. 1990. Mild measles and secondary vaccine failure during a sustained outbreak in a highly vaccinated population. JAMA 263:2467-2471.
32. Mamaeva TA, Lipskaia G, Naumova MA, Shul'ga SV, Mulders M, Featherstone DA, Zav'ialova LA, Chernysheva EV, Zamiatina EP, Kuznetsova NN. 2012. Peculiarity of the laboratory diagnostic of the measles virus infection in previously vaccinated and unvaccinated patients. Vopr Virusol 57:21-26. (In Russian.)
33. Bernasconi NL, Traggiai E, Lanzavecchia A. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199-2202. http://dx.doi.org/10.1126/science.1076071.
34. Fulginiti VA, Kempe CH. 1963. Measles exposure among vaccine recipients. Response to measles exposure and antibody persistence among recipients of measles vaccines. Am J Dis Child 106:450-461.
35. Chen TH, Kutty P, Lowe LE, Hunt EA, Blostein J, Espinoza R, Dykewicz CA, Redd S, Rota JS, Rota PA, Lute JR, Lurie P, Nguyen MD, Moll M, Reef SE, Sinclair JR, Bellini WJ, Seward JF, Ostroff SM. 2010. Measles outbreak associated with an international youth sporting event in the United States, 2007. Pediatr Infect Dis J 29:794-800. http://dx.doi.org/10.1097/INF.0b013e3181dbaacf.
36. Chretien JH, Garagusi VF. 1980. Epidemic measles in college students. J Am Coll Health Assoc 28:254-256.
37. Cherry JD, Feigin RD, Lobes LA, Jr, Hinthorn DR, Shackelford PG, Shirley RH, Lins RD, Choi SC. 1972. Urban measles in the vaccine era: a clinical, epidemiologic, and serologic study. J Pediatr 81:217-230. http://dx.doi.org/10.1016/S0022-3476 (72) 80287-7.
38. Schaffner W, Schluederberg AE, Byrne EB. 1968. Clinical epidemiology of sporadic measles in a highly immunized population. N Engl J Med 279:783-789. http://dx.doi.org/10.1056/NEJM196810102791501.
39. Wyll SA, Witte JJ. 1971. Measles in previously vaccinated children. An epidemiological study. JAMA 216:1306-1310.
40. Cherry JD, Feigin RD, Lobes LA, Jr, Shackelford PG. 1972. Atypical measles in children previously immunized with attenuated measles virus vaccines. Pediatrics 50:712-717.
41. Gustafson TL, Lievens AW, Brunell PA, Moellenberg RG, Buttery CM, Sehulster LM. 1987. Measles outbreak in a fully immunized secondaryschool population. N Engl J Med 316:771-774. http://dx.doi.org/10.1056/NEJM198703263161303.
42. Nkowane BM, Bart SW, Orenstein WA, Baltier M. 1987. Measles outbreak in a vaccinated school population: epidemiology, chains of transmission and the role of vaccine failures. Am J Public Health 77:434-438. http://dx.doi.org/10.2105/AJPH.77.4.434.
43. Linnemann CC, Jr, Rotte TC, Schiff GM, Youtsey JL. 1972. A seroepidemiologic study of a measles epidemic in a highly immunized population. Am J Epidemiol 95:238-246.
44. Cherry JD, Feigin RD, Shackelford PG, Hinthorn DR, Schmidt RR. 1973. A clinical and serologic study of 103 children with measles vaccine failure. J Pediatr 82:802-808. http://dx.doi.org/10.1016/S0022-3476 (73) 80070-8.
45. Krause PJ, Cherry JD, Deseda-Tous J, Champion JG, Strassburg M, Sullivan C, Spencer MJ, Bryson YJ, Welliver RC, Boyer KM. 1979. Epidemic measles in young adults. Clinical, epidemiologic, and serologic studies. Ann Intern Med 90:873-876.
46. Plotkin SA. 1973. Failures of protection by measles vaccine. J Pediatr 82:908-911. http://dx.doi.org/10.1016/S0022-3476 (73) 80107-6.
47. Gonçalves G, Frade J, Nunes C, Mesquita JR, Nascimento MS. 2015. Persistence of measles antibodies, following changes in the recommended age for the second dose of MMR-vaccine in Portugal. Vaccine 33:5057-5063. http://dx.doi.org/10.1016/j.vaccine.2015.08.057.
48. Chen CJ, Lee PI, Hsieh YC, Chen PY, Ho YH, Chang CJ, Liu DP, Chang FY, Chiu CH, Huang YC, Lee CY, Lin TY. 2012. Waning population immunity to measles in Taiwan. Vaccine 30:6721-6727. http://dx.doi.org/10.1016/j.vaccine.2012.05.019.
49. Poland GA, Jacobson RM, Thampy AM, Colbourne SA, Wollan PC, Lipsky JJ, Jacobsen SJ. 1997. Measles reimmunization in children seronegative after initial immunization. JAMA 277:1156-1158.
50. Poland GA, Jacobson RM, Schaid D, Moore SB, Jacobsen SJ. 1998. The association between HLA class I alleles and measles vaccine-induced antibody response: evidence of a significant association. Vaccine 16:1869-1871. http://dx.doi.org/10.1016/S0264-410X (98) 00017-6.
51. Pichichero ME. 2009. Booster vaccinations: can immunologic memory outpace disease pathogenesis? Pediatrics 124:1633-1641. http://dx.doi.org/10.1542/peds.2008-3645.
52. Haralambieva IH, Ovsyannikova IG, Pankratz VS, Kennedy RB, Jacobson RM, Poland GA. 2013. The genetic basis for interindividual immune response variation to measles vaccine: new understanding and new vaccine approaches. Expert Rev Vaccines 12:57-70. http://dx.doi.org/10.1586/erv. 12.134.
53. Tan PL, Jacobson RM, Poland GA, Jacobsen SJ, Pankratz VS. 2001. Twin studies of immunogenicity-determining the genetic contribution to vaccine failure. Vaccine 19:2434-2439. http://dx.doi.org/10.1016/S0264-410X (00) 00468-0.
54. Paunio M, Hedman K, Davidkin I, Peltola H. 2003. IgG avidity to distinguish secondary from primary measles vaccination failures: prospects for a more effective global measles elimination strategy. Expert Opin Pharmacother 4:1215-1225. http://dx.doi.org/10.1517/14656566.4.8.1215.
55. Thomas A, Xu D, Wooten K, Morrow B, Redd S. 1999. Timing and effectiveness of requirements for a second dose of measles vaccine. Pediatr Infect Dis J 18:266-270. http://dx.doi.org/10.1097/00006454-199903000-00012.
56. LeBaron CW, Beeler J, Sullivan BJ, Forghani B, Bi D, Beck C, Audet S, Gargiullo P. 2007. Persistence of measles antibodies after 2 doses of measles vaccine in a postelimination environment. Arch Pediatr Adolesc Med 161:294-301. http://dx.doi.org/10.1001/archpedi.161.3.294.
57. Rager-Zisman B, Bazarsky E, Skibin A, Chamney S, Belmaker I, Shai I, Kordysh E, Griffin DE. 2003. The effect of measles-mumps-rubella (MMR) immunization on the immune responses of previously immunized primary school children. Vaccine 21:2580-2588. http://dx.doi.org/10.1016/S0264-410X (03) 00053-7.
58. Markowitz LE, Albrecht P, Rhodes P, Demonteverde R, Swint E, Maes EF, Powell C, Patriarca PA. 1996. Changing levels of measles antibody titers in women and children in the United States: impact on response to vaccination. Kaiser Permanente Measles Vaccine Trial Team. Pediatrics 97:53-58.
59. Markowitz LE, Albrecht P, Orenstein WA, Lett SM, Pugliese TJ, Farrell D. 1992. Persistence of measles antibody after revaccination. J Infect Dis 166:205-208. http://dx.doi.org/10.1093/infdis/166.1.205.
60. Fiebelkorn AP, Redd SB, Gastañaduy PA, Clemmons N, Rota PA, Rota JS, Bellini WJ, Wallace GS. 13 December 2015. A comparison of postelimination measles epidemiology in the United States, 2009-2014 versus 2001-2008. J Pediatric Infect Dis Soc http://dx.doi.org/10.1093/jpids/piv080.