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Archives of Virology

, Volume 162, Issue 11, pp 3389–3396 | Cite as

Detection of waterborne norovirus genogroup I strains using an improved real time RT-PCR assay

  • Han-Gil Cho
  • Sung-Geun Lee
  • Su-Kyoung Mun
  • Myung-Jin Lee
  • Po-Hyun Park
  • Weon-Hwa Jheong
  • Mi-Hye Yoon
  • Soon-Yong PaikEmail author
Original Article

Abstract

Noroviruses (NoVs) are the major global source of acute gastroenteritis (AGE) outbreaks. To detect NoVs, real-time reverse transcription-quantitative PCR (RT-qPCR) assays have been widely employed since the first decade of the 21st century. We developed a redesigned probe, JJV1PM, for RT-qPCR assay detection of NoV genogroup (G) I strains. The new RT-qPCR assay using the JJV1PM-probe showed broader strain reactivity for 10 NoV GI genotypes, while the old method, using the JJV1PT-probe assay, detected only 7 NoV GI genotypes in a validation panel using human fecal specimens. The improved RT-qPCR assay was also successfully applied to water samples. The JJV1PM-probe assay identified 7 NoV GI genotypes, whereas the JJV1PT-probe assay detected only 2 NoV GI genotypes from water samples. Notably, groundwater-borne NoV GI strains detected by the improved JJV1PM-probe assay were associated with groundwater-borne AGE outbreaks in South Korea. The results of this study underscore the importance of the evaluation of RT-qPCR assays using recently circulating NoV strains prior to field application.

Abbreviations

NoV

Norovirus

AGE

Acute Gastroenteritis

RT-qPCR

Real-Time Reverse Transcription-Quantitative PCR

ORF

Open Reading Frames

Notes

Acknowledgements

This research was supported by a Grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (Grant numbers: HI15C1781).

Compliance with ethical standards

Conflict of interest

The authors have declared that no competing interests exist.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

References

  1. 1.
    Hall AJ, Vinjé J, Lopman B, Park GW, Yen C, Gregoricus N, Parashar U (2011) Updated norovirus outbreak management and disease prevention guidelines. MMWR Recomm Rep 60(RR-3):1–18Google Scholar
  2. 2.
    Hall AJ, Lopman BA, Payne DC, Patel MM, Gastanaduy PA, Vinje J, Parashar UD (2013) Norovirus disease in the United States. Emerg Infect Dis 19(8):1198–1205CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Vinje J (2015) Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol 53(2):373–381CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Kageyama T, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Kojima S, Takai R, Oka T, Takeda N, Katayama K (2004) Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to Norovirus in Japan. J Clin Microbiol 42(7):2988–2995CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Vega E, Barclay L, Gregoricus N, Shirley SH, Lee D, Vinje J (2014) Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J Clin Microbiol 52(1):147–155CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U, Tenge VR, Neill FH, Blutt SE, Zeng XL, Qu L, Kou B, Opekun AR, Burrin D, Graham DY, Ramani S, Atmar RL, Estes MK (2016) Replication of human noroviruses in stem cell-derived human enteroids. Science 353(6306):1387–1393CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Vinjé J, Vennema H, Maunula L, von Bonsdorff CH, Hoehne M, Schreier E, Richards A, Green J, Brown D, Beard SS, Monroe SS, de Bruin E, Svensson L, Koopmans MP (2003) International collaborative study to compare reverse transcriptase PCR assays for detection and genotyping of noroviruses. J Clin Microbiol 41(4):1423–1433CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    La Rosa G, Fontana S, Di Grazia A, Iaconelli M, Pourshaban M, Muscillo M (2007) Molecular identification and genetic analysis of Norovirus genogroups I and II in water environments: comparative analysis of different reverse transcription-PCR assays. Appl Environ Microbiol 73(13):4152–4161CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K (2003) Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41(4):1548–1557CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Vainio K, Myrmel M (2006) Molecular epidemiology of norovirus outbreaks in Norway during 2000 to 2005 and comparison of four norovirus real-time reverse transcriptase PCR assays. J Clin Microbiol 44(10):3695–3702CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Jothikumar N, Lowther JA, Henshilwood K, Lees DN, Hill VR, Vinje J (2005) Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol 71(4):1870–1875CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Hall AJ, Wikswo ME, Manikonda K, Roberts VA, Yoder JS, Gould LH (2013) Acute gastroenteritis surveillance through the National Outbreak Reporting System, United States. Emerg Infect Dis 19(8):1305–1309CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Hewitt J, Bell D, Simmons GC, Rivera-Aban M, Wolf S, Greening GE (2007) Gastroenteritis outbreak caused by waterborne norovirus at a New Zealand ski resort. Appl Environ Microbiol 73(24):7853–7857CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Maunula L, Miettinen IT, von Bonsdorff CH (2005) Norovirus outbreaks from drinking water. Emerg Infect Dis 11(11):1716–1721CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Matthews JE, Dickey BW, Miller RD, Felzer JR, Dawson BP, Lee AS, Rocks JJ, Kiel J, Montes JS, Moe CL, Eisenberg JN, Leon JS (2012) The epidemiology of published norovirus outbreaks: a review of risk factors associated with attack rate and genogroup. Epidemiol Infect 140(7):1161–1172CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Trujillo AA, McCaustland KA, Zheng DP, Hadley LA, Vaughn G, Adams SM, Ando T, Glass RI, Monroe SS (2006) Use of TaqMan real-time reverse transcription-PCR for rapid detection, quantification, and typing of norovirus. J Clin Microbiol 44(4):1405–1412CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Nenonen NP, Hannoun C, Larsson CU, Bergstrom T (2012) Marked genomic diversity of norovirus genogroup I strains in a waterborne outbreak. Appl Environ Microbiol 78(6):1846–1852CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Loisy F, Atmar RL, Guillon P, Le Cann P, Pommepuy M, Le Guyader FS (2005) Real-time RT-PCR for norovirus screening in shellfish. J Virol Methods 123(1):1–7CrossRefPubMedGoogle Scholar
  19. 19.
    Wolf S, Williamson WM, Hewitt J, Rivera-Aban M, Lin S, Ball A, Scholes P, Greening GE (2007) Sensitive multiplex real-time reverse transcription-PCR assay for the detection of human and animal noroviruses in clinical and environmental samples. Appl Environ Microbiol 73(17):5464–5470CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Cho HG, Park PH, Lee SG, Kim JE, Kim KA, Lee HK, Park EM, Park MK, Jung SY, Lee DY, Yoon MH, Lee JB, Paik SY (2015) Emergence of Norovirus GII.4 variants in acute gastroenteritis outbreaks in South Korea between 2006 and 2013. J Clin Virol 72:11–15CrossRefPubMedGoogle Scholar
  21. 21.
    Lee SG, Jheong WH, Suh CI, Kim SH, Lee JB, Jeong YS, Ko G, Jang KL, Lee GC, Paik SY (2011) Nationwide groundwater surveillance of noroviruses in South Korea, 2008. Appl Environ Microbiol 77(4):1466–1474CrossRefPubMedGoogle Scholar
  22. 22.
    Fout GS, Schaefer FW III, Messer JW, Dahling DR, Stetler RE (1996) ICR microbial laboratory manual. Environ Protect Agency, Washington DCGoogle Scholar
  23. 23.
    Cho HG, Lee SG, Kim WH, Lee JS, Park PH, Cheon DS, Jheong WH, Jho EH, Lee JB, Paik SY (2014) Acute gastroenteritis outbreaks associated with ground-waterborne norovirus in South Korea during 2008-2012. Epidemiol Infect 142(12):2604–2609CrossRefPubMedGoogle Scholar
  24. 24.
    Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, Uchida K, Natori K, Takeda N, Katayama K (2002) Genogroup-specific PCR primers for detection of Norwalk-like viruses. J Virol Methods 100(1–2):107–114CrossRefPubMedGoogle Scholar
  25. 25.
    Kutyavin IV, Afonina IA, Mills A, Gorn VV, Lukhtanov EA, Belousov ES, Singer MJ, Walburger DK, Lokhov SG, Gall AA, Dempcy R, Reed MW, Meyer RB, Hedgpeth J (2000) 3’-minor groove binder-DNA probes increase sequence specificity at PCR extension temperatures. Nucleic Acids Res 28(2):655–661CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Masago Y, Konta Y, Kazama S, Inaba M, Imagawa T, Tohma K, Saito M, Suzuki A, Oshitani H, Omura T (2016) Comparative evaluation of real-time PCR methods for human Noroviruses in wastewater and human stool. PLoS One 11(8):e0160825CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Svraka S, Duizer E, Vennema H, de Bruin E, van der Veer B, Dorresteijn B, Koopmans M (2007) Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. J Clin Microbiol 45(5):1389–1394CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Miura T, Parnaudeau S, Grodzki M, Okabe S, Atmar RL, Le Guyader FS (2013) Environmental detection of genogroup I, II, and IV noroviruses by using a generic real-time reverse transcription-PCR assay. Appl Environ Microbiol 79(21):6585–6592CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Bok K, Abente EJ, Realpe-Quintero M, Mitra T, Sosnovtsev SV, Kapikian AZ, Green KY (2009) Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J Virol 83(22):11890–11901CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Zhuo R, Hasing ME, Pang X, Team of Molecular Diagnostics (2015) A single nucleotide polymorphism at the TaqMan probe-binding site impedes real-time reverse transcription-PCR-based detection of Norovirus GII.4 Sydney. J Clin Microbiol 53(10):3353–3354CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hoehne M, Schreier E (2006) Detection of Norovirus genogroup I and II by multiplex real-time RT- PCR using a 3’-minor groove binder-DNA probe. BMC Infect Dis 6:69CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Feeney SA, Armstrong VJ, Mitchell SJ, Crawford L, McCaughey C, Coyle PV (2011) Development and clinical validation of multiplex TaqMan(R) assays for rapid diagnosis of viral gastroenteritis. J Med Virol 83(9):1650–1656CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria 2017

Authors and Affiliations

  • Han-Gil Cho
    • 1
  • Sung-Geun Lee
    • 2
  • Su-Kyoung Mun
    • 1
  • Myung-Jin Lee
    • 1
  • Po-Hyun Park
    • 1
  • Weon-Hwa Jheong
    • 3
  • Mi-Hye Yoon
    • 1
  • Soon-Yong Paik
    • 4
    Email author
  1. 1.Division of Public Health ResearchGyeonggi Province Institute of Health and EnvironmentSuwonRepublic of Korea
  2. 2.Korea Zoonosis Research InstituteChonbuk National UniversityIksanRepublic of Korea
  3. 3.Environmental Infrastructure Research DepartmentNational Institute of Environmental ResearchIncheonRepublic of Korea
  4. 4.Department of Microbiology, College of MedicineThe Catholic University of KoreaSeoulRepublic of Korea

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