Skip to main content

Advertisement

SpringerLink
Log in

Control of a nosocomial measles outbreak among previously vaccinated adults in a population with high vaccine coverage: Korea, 2019

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

We describe a measles outbreak among previously vaccinated healthcare workers (HCWs) and inpatients and the control measures implemented at a tertiary care hospital in 2019. Case-patients were laboratory-confirmed measles with throat swabs tested by quantitative polymerase chain reactions (PCR), during April–May 2019. Medical histories and documented immunization records were obtained. We compared attack rates (ARs) among HCWs by occupational subgroup and age and examined the outbreak-associated costs. The index case was not ascertained. Among 26 measles case-patients (22 HCWs, four inpatients) aged 18–28 years, 25 had previously received measles–mumps–rubella (MMR) vaccine (12/26, 46% (two doses); 13/26, 50% (one dose)), and 16 (62%) had positive results of measles IgG prior to measles diagnosis. ARs were higher among HCWs aged < 30 years (1.88%), especially in the subgroup under 25 years of age (2.22%). Control measures included work restrictions for seronegative HCWs (218/2320, 9.4%) in immunity verification, administration of the MMR vaccine (207 HCWs) or intravenous immunoglobulin (2 HCWs and 11 inpatients), enhanced health surveillance of HCWs, and mandatory assessment of patients with measles-like symptoms at the infectious diseases screening units. The hospital spent 90,417,132 Korean won (US $79,733) in response to the outbreak. Measles outbreaks can occur in healthcare settings despite high population immunity, highlighting the importance of stronger vaccination policies, particularly among young HCWs. Moreover, an effective outbreak response comprising immunization activities and enhanced surveillance of HCWs and patients to rapidly detect measles-like symptoms at a prodromal phase is essential to control nosocomial measles outbreaks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and material

The data are available upon reasonable request by contacting the corresponding author.

References

  1. Guerra FM, Bolotin S, Lim G, Heffernan J, Deeks SL, Li Y, Crowcroft NS (2017) The basic reproduction number (R0) of measles: a systematic review. Lancet Infect Dis 17:e420–e428. https://doi.org/10.1016/S1473-3099(17)30307-9

    Article  PubMed  Google Scholar 

  2. Steingart KR, Thomas AR, Dykewicz CA, Redd SC (1999) Transmission of measles virus in healthcare settings during a communitywide outbreak. Infect Control Hosp Epidemiol 20:115–119. https://doi.org/10.1086/501595

    Article  CAS  PubMed  Google Scholar 

  3. Choi WS, Sniadack DH, Jee Y, Go UY, So JS, Cho H, Bae GR, Lee DH, Kim K, Yoon HS, Chung YS, Kang C, Park H, Park O, Lee JK (2011) Outbreak of measles in the Republic of Korea, 2007: importance of nosocomial transmission. J Infect Dis 204:S483–S490. https://doi.org/10.1093/infdis/jir087

    Article  PubMed  Google Scholar 

  4. Hagan JE, Takashima Y, Sarankhuu A, Dashpagma O, Jantsansengee B, Pastore R, Nyamaa G, Yadamsuren B, Mulders MN, Wannemuehler KA, Anderson R, Bankamp B, Rota P, Goodson JL (2017) Risk factors for measles virus infection among adults during a large outbreak in post elimination era in Mongolia, 2015. J Infect Dis 216:1187–1195. https://doi.org/10.1093/infdis/jix449

    Article  PubMed  Google Scholar 

  5. Botelho-Nevers E, Gautret P, Biellik R, Brouqui P (2012) Nosocomial transmission of measles: an updated review. Vaccine 30:3996–4001. https://doi.org/10.1016/j.vaccine.2012.04.023

    Article  CAS  PubMed  Google Scholar 

  6. Maltezou HC, Wicker S (2013) Measles in health care settings. Am J Infect Control 41:661–663. https://doi.org/10.1016/j.ajic.2012.09.017

    Article  PubMed  Google Scholar 

  7. Cherry JD, Zahn M (2018) Clinical characteristics of measles in previously vaccinated and unvaccinated patients in California. Clin Infect Dis 67:1315–1319. https://doi.org/10.1093/cid/ciy286

    Article  PubMed  Google Scholar 

  8. 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:S559–S563. https://doi.org/10.1093/infdis/jir098

    Article  PubMed  Google Scholar 

  9. Choe YJ, Park YJ, Kim JW, Eom HE, Park O, Oh MD, Lee JK (2017) An outbreak of measles in a university in Korea, 2014. J Korean Med Sci 32:1876–1878. https://doi.org/10.3346/jkms.2017.32.11.1876

    Article  PubMed  PubMed Central  Google Scholar 

  10. Sá Machado R, Perez Duque M, Almeida S, Cruz I, Sottomayor A, Almeida I, Oliveira JR, Antunes D (2018) Measles outbreak in a tertiary level hospital, Porto, Portugal, 2018: challenges in the post-elimination era. Euro Surveill 23:18–00224. https://doi.org/10.2807/1560-7917.ES.2018.23.20.18-00224

    Article  PubMed Central  Google Scholar 

  11. Gohil SK, Okubo S, Klish S, Dickey L, Huang SS, Zahn M (2016) Healthcare workers and post-elimination era measles: lessons on acquisition and exposure prevention. Clin Infect Dis 62:155–172. https://doi.org/10.1093/cid/civ802

    Article  Google Scholar 

  12. Hahné SJ, Nic Lochlainn LM, van Burgel ND, Kerkhof J, Sane J, Yap KB, van Binnendijk RS (2016) Measles outbreak among previously immunized healthcare workers, the Netherlands, 2014. J Infect Dis 214:1980–1986. https://doi.org/10.1093/infdis/jiw480

    Article  PubMed  Google Scholar 

  13. 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:S549–S558. https://doi.org/10.1093/infdis/jir106

    Article  PubMed  Google Scholar 

  14. Kontio M, Jokinen S, Paunio M, Peltola H, Davidkin I (2012) Waning antibody levels and avidity: implications for MMR vaccine-induced protection. J Infect Dis 206:1542–1548. https://doi.org/10.1093/infdis/jis568

    Article  CAS  PubMed  Google Scholar 

  15. Avramovich E, Indenbaum V, Haber M, Amitai Z, Tsifanski E, Farjun S, Sarig A, Bracha A, Castillo K, Markovich MP, Galor I (2018) Measles outbreak in highly vaccinated population – Israel, July-August 2017. MMWR Morb Mortal Wkly Rep 67:1186–1188. https://doi.org/10.15585/mmwr.mm6742a4

    Article  PubMed  PubMed Central  Google Scholar 

  16. Mizumoto K, Kobayashi T, Chowell G (2018) Transmission potential of modified measles during an outbreak, Japan, March-May 2018. Euro Surveill 23:1800239. https://doi.org/10.2807/1560-7917.ES.2018.23.24.1800239

    Article  PubMed Central  Google Scholar 

  17. Gibney KB, Attwood LO, Nicholson S, Tran T, Druce J, Healy J, Strachan J, Franklin L, Hall R, Cross GB (2020) Emergence of attenuated measles illness among IgG-positive/IgM-negative measles cases: Victoria, Australia, 2008–2017. Clin Infect Dis 70:1060–1067. https://doi.org/10.1093/cid/ciz363

    Article  PubMed  Google Scholar 

  18. Rosen JB, Rota JS, Hickman CJ, Sowers SB, Mercader S, Rota PA, Bellini WJ, Huang AJ, Doll MK, Zucker JR, Zimmerman CM (2014) Outbreaks of measles among persons with prior evidence of immunity, New York City, 2011. Clin Infect Dis 58:1205–1210. https://doi.org/10.1093/cid/ciu105

    Article  CAS  PubMed  Google Scholar 

  19. Kang JH (2020) Review of measles in Korea: quarantine and elimination. Infect Chemother 52:113–122. https://doi.org/10.3947/ic.2020.52.1.113

    Article  PubMed  PubMed Central  Google Scholar 

  20. Choe YJ, Jee Y, Oh MD, Lee JK (2015) Measles elimination activities in the Western Pacific Region: experience from the Republic of Korea. J Korean Med Sci 30:S115-121. https://doi.org/10.3346/jkms.2015.30.S2.S115

    Article  PubMed  PubMed Central  Google Scholar 

  21. Yang TU, Kim JW, Eom HE, Oh HK, Kim ES, Kang HJ, Nam JG, Kim KS, Kim SS, Lee CK, Park YJ, Park O (2015) Resurgence of measles in a country of elimination: interim assessment and current control measures in the Republic of Korea in early 2014. Int J Infect Dis 33:12–14. https://doi.org/10.1016/j.ijid.2014.09.016

    Article  CAS  PubMed  Google Scholar 

  22. Helfand RF, Heath JL, Anderson LJ, Maes EF, Guris D, Bellini WJ (1997) Diagnosis of measles with and IgM capture EIA: the optimal timing of specimen collection after rash onset. J Infect Dis 175:195–199. https://doi.org/10.1093/infdis/175.1.195

    Article  CAS  PubMed  Google Scholar 

  23. Cho HJ, Kang HJ (2014) Genotype analysis of measles outbreaks in Korea 2013. Public Health Wkly Rep 7:470–475

    Google Scholar 

  24. McLean HQ, Fiebelkorn AP, Temte JL, Wallace GS, Centers for Disease Control and Prevention, (2013) Prevention of measles, rubella, congenital rubella syndrome, and mumps, 2013: summary recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 62:1–34

    Google Scholar 

  25. Venkat H, Briggs G, Brady S, Komatsu K, Hill C, Leung J, Patel M, Livar E, Su CP, Kassem A, Sowers SB, Mercader S, Rota PA, Elson D, Timme E, Robinson S, Fitzpatrick K, Franco J, Hickman C, Gastañaduy PA (2019) Measles outbreak at a privately operated detention facility: Arizona, 2016. Clin Infect Dis 68:2018–2025. https://doi.org/10.1093/cid/ciy819

    Article  PubMed  Google Scholar 

  26. Botelho-Nevers E, Cassir N, Minodier P, Laporte R, Gautret P, Badiaga S, Thiberville DJ, Ninove L, Charrel R, Brouqui P (2011) Measles among healthcare workers: a potential for nosocomial outbreaks. Euro Surveill 16:19764

    Article  Google Scholar 

  27. Barrett P, Cotter S, Ryan F, Connell J, Cronin A, Ward M, Fitzgerald R, Lynch C, Margiotta T, on Behalf of the Outbreak Control Team (2018) A national measles outbreak in Ireland linked to a single imported case, April to September, 2016. Euro Surveill 23:1700655. https://doi.org/10.2807/1560-7917.ES.2018.23.31.1700655

    Article  PubMed Central  Google Scholar 

  28. Chen SY, Anderson S, Kutty PK, Lugo F, McDonald M, Rota PA, Ortega-Sanchez IR, Komatsu K, Armstrong GL, Sunenshine R, Seward JF (2011) Healthcare-associated measles outbreak in the United States after an importation: challenges and economic impact. J Infect Dis 203:1517–1525. https://doi.org/10.1093/infdis/jir115

    Article  PubMed  Google Scholar 

  29. Biribawa C, Atuhairwe JA, Bulage L, Okethwangu DO, Kwesiga B, Ario AR, Zhu BP (2020) Measles outbreak amplified in a pediatric ward: Lyantonde district, Uganda, August 2017. BMC Infect Dis 20:398. https://doi.org/10.1186/s12879-020-05120-5

    Article  PubMed  PubMed Central  Google Scholar 

  30. Porretta A, Quattrone F, Aquino F, Pieve G, Bruni B, Gemignani G, Vatteroni ML, Pistello M, Privitera GP, Lopalco PL (2017) A nosocomial measles outbreak in Italy, February-April 2017. Euro Surveill 22:30597. https://doi.org/10.2807/1560-7917.ES.2017.22.33.30597

    Article  PubMed  PubMed Central  Google Scholar 

  31. Jia H, Ma C, Lu M, Fu J, Rodewald LE, Su Q, Wang H, Hao L (2018) Transmission of measles among healthcare workers in hospital W, Xinjiang autonomous region, China, 2016. BMC Infect Dis 18:36. https://doi.org/10.1186/s12879-018-2950-y

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kang HJ, Han YW, Kim SJ, Kim YJ, Kim AR, Kim JA, Jung HD, Eom HE, Park O, Kim SS (2017) An increasing, potentially measles-susceptible population over time after vaccination in Korea. Vaccine 35:4126–4132. https://doi.org/10.1016/j.vaccine.2017.06.058

    Article  PubMed  Google Scholar 

  33. Chang HH, Kim SW, Kwon KT, Kim HI, Kim MJ, Ryu SY, Kim HA, Hur J, Kwon HH, Hong HL (2019) Preliminary report of seroprevalence of anti-measles immunoglobulin G among healthcare workers of 6 teaching hospitals of Daegu, Korea in 2019. Infect Chemother 51:54–57. https://doi.org/10.3947/ic.2019.51.1.54

    Article  PubMed  PubMed Central  Google Scholar 

  34. Jung J, Kim SK, Kwak SH, Hong MJ, Kim SH (2019) Seroprevalence of measles in healthcare workers in South Korea. Infect Chemother 51:58–61. https://doi.org/10.3947/ic.2019.51.1.58

    Article  PubMed  PubMed Central  Google Scholar 

  35. Maltezou HC, Wicker S, Borg M, Heininger U, Puro V, Theodoridou M, Poland GA (2011) Vaccination policies for health-care workers in acute health-care facilities in Europe. Vaccine 29:9557–9562

    Article  Google Scholar 

  36. Maltezou HC, Botelho-Nevers E, Brantsæter AB et al (2019) Vaccination of healthcare personnel in Europe: update to current policies. Vaccine 37:7576–7584. https://doi.org/10.1016/j.vaccine.2011.09.076

    Article  PubMed  Google Scholar 

  37. Fiebelkorn AP, Seward JF, Orenstein WA (2014) A global perspective of vaccination of healthcare personnel against measles: systematic review. Vaccine 32:4823–4839. https://doi.org/10.1016/j.vaccine.2013.11.005

    Article  PubMed  Google Scholar 

  38. Six C, Blanes de Canecaude J, Duponchel J, Lafont E, Decoppet A, Travanut M, Pingeon J, Coulon L, Peloux-Petiot F, Grenier-Tisserant P, Delaroziere J, Charlet F, Malfait P (2010) Spotlight on measles 2010: measles outbreak in the Provence-Alpes-Cote d Azur region, France, January to November 2010 - substantial underreporting of cases. Euro Surveill 15:19754

    Article  Google Scholar 

  39. Park SH, Lee MS, Kim SR, Kwak YG (2020) A national survey on the hospital vaccination policies in Korea. J Korean Med Sci 35:e76. https://doi.org/10.3346/jkms.2020.35.e76

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lindley M, Horlick G, Shefer A, Shaw F, Gorji M (2007) Assessing state immunization requirements for healthcare workers and patients. Am J Prev Med 32:459–465. https://doi.org/10.1016/j.amepre.2007.02.009

    Article  PubMed  Google Scholar 

  41. Sydnor E, Perl TM (2014) Healthcare providers as sources of vaccine-preventable diseases. Vaccine 32:4814–4822. https://doi.org/10.1016/j.vaccine.2014.03.097

    Article  PubMed  Google Scholar 

  42. Lefebvre F, Merle V, Savoye G, Lemée V, Chapuzet C, Marini H, Géhanno JF, Chefson-Girault C, Gueit I, Freymuth F, Lerebours E, Czernichow P (2011) Nosocomial transmission of measles: do we need extra precautions to avoid it? J Hosp Infect 79:185–187. https://doi.org/10.1016/j.jhin.2011.05.025

    Article  CAS  PubMed  Google Scholar 

  43. Fu J, Chu J, Wang J, Cai R, Cheng W, Shi L, Zhang F, Xu Z, Xing Y (2019) A hospital-associated measles outbreak in health workers in Beijing: implications for measles elimination in China, 2018. Int J Infect Dis 78:85–92. https://doi.org/10.1016/j.ijid.2018.10.023

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Korea

    Kyunghyun Song, Song Mi Moon & Yong Kyun Kim

  2. Department of Infection Control, Hallym University Sacred Heart Hospital, Anyang, Korea

    Ju Mi Lee, Eun Ju Lee, Bo Ram Lee, Ji Young Choi, Jihee Yun, Se Na Lee, Mi Young Jang, Han Wool Kim, Han-Sung Kim, Song Mi Moon & Yong Kyun Kim

  3. Department of Pediatrics, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Korea

    Han Wool Kim

  4. Department of Laboratory Medicine, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Korea

    Han-Sung Kim

  5. Division of Infectious Diseases, Department of Internal Medicine, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Korea

    Song Mi Moon & Yong Kyun Kim

Authors
  1. Kyunghyun Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ju Mi Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eun Ju Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bo Ram Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ji Young Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jihee Yun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Se Na Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mi Young Jang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Han Wool Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Han-Sung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Song Mi Moon
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yong Kyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

(1) Conception and design: SS and YKK; (2) acquisition of data and administrative support: SS and JML; (3) provision of study materials or patients: BRL, JYC, JY, SNL, and MYJ; (4) collection and assembly of data: HWK; (5) data analysis and interpretation: HSK, SMM, and YKK; (6) manuscript writing: all authors; (7) final approval of manuscript: all authors.

Corresponding author

Correspondence to Yong Kyun Kim.

Ethics declarations

Ethics approval

This study was approved by the hospital ethics committee.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interests

The authors declare that they have no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, K., Lee, J.M., Lee, E.J. et al. Control of a nosocomial measles outbreak among previously vaccinated adults in a population with high vaccine coverage: Korea, 2019. Eur J Clin Microbiol Infect Dis 41, 455–466 (2022). https://doi.org/10.1007/s10096-021-04390-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-021-04390-4

Keywords

Search

Navigation