Optimization of one-step real-time reverse transcription-polymerase chain reaction assays for norovirus detection and molecular epidemiology of noroviruses in thailand

Journal of Virological Methods

Volumn 194, Issue 1-2, 2013, Pages 317-325

  Neesanant, Pimmnapar ^a,b   Sirinarumitr, Theerapol ^a   Chantakru, Siriruk ^a   Boonyaprakob, Ukadaj ^a   Chuwongkomon, Kaittawee ^a   Bodhidatta, Ladaporn ^b   Sethabutr, Orntipa ^b   Abente, Eugenio J ^b   Supawat, Krongkaew ^c   Mason, Carl J ^b  

^a KASETSART UNIVERSITY   (Thailand)

^b ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^c MINISTRY OF PUBLIC HEALTH   (Thailand)

Author keywords

Diagnosis; Molecular epidemiology; Norovirus; Real time RT PCR; Thailand

Indexed keywords

ACUTE GASTROENTERITIS; ARTICLE; BIOASSAY; CASE CONTROL STUDY; CHILD; CONTROLLED STUDY; CROSS REACTION; CULTURE OPTIMIZATION; FECES ANALYSIS; FREQUENCY ANALYSIS; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HUMAN; INFANT; LIMIT OF DETECTION; MAJOR CLINICAL STUDY; MOLECULAR EPIDEMIOLOGY; NONHUMAN; NOROVIRUS; NOROVIRUS INFECTION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRESCHOOL CHILD; PREVALENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; THAILAND; VIRUS CAPSID; VIRUS DETECTION; VIRUS STRAIN;

DIAGNOSIS; MOLECULAR EPIDEMIOLOGY; NOROVIRUS; REAL-TIME RT-PCR; THAILAND;

CALICIVIRIDAE INFECTIONS; CASE-CONTROL STUDIES; CHILD, PRESCHOOL; DNA PRIMERS; GEOGRAPHY; HUMANS; INFANT; MOLECULAR DIAGNOSTIC TECHNIQUES; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; MULTIPLEX POLYMERASE CHAIN REACTION; NOROVIRUS; PREVALENCE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; THAILAND;

EID: 84886410587     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2013.08.033     Document Type: Article

References (52)

1. Ando T., Monroe S.S., Gentsch J.R., Jin Q., Lewis D.C., Glass R.I. Detection and differentiation of antigenically distinct small round-structured viruses (Norwalk-like viruses) by reverse transcription-PCR and southern hybridization. J. Clin. Microbiol. 1995, 33:64-71.
2. Ando T., Monroe S.S., Noel J.S., Glass R.I. A one-tube method of reverse transcription-PCR to efficiently amplify a 3-kilobase region from the RNA polymerase gene to the poly(A) tail of small round-structured viruses (Norwalk-like viruses). J. Clin. Microbiol. 1997, 35:570-577.
3. Atmar R.L., Bernstein D.I., Harro C.D., Al-Ibrahim M.S., Chen W.H., Ferreira J., Estes M.K., Graham D.Y., Opekun A.R., Richardson C., Mendelman P.M. Norovirus vaccine against experimental human Norwalk Virus illness. N. Engl. J. Med. 2011, 365:2178-2187.
4. Atmar R.L., Estes M.K. Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin. Microbiol. Rev. 2001, 14:15-37.
5. Bok K., Abente E.J., Realpe-Quintero M., Mitra T., Sosnovtsev S.V., Kapikian A.Z., Green K.Y. Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J. Virol. 2009, 83:11890-11901.
6. Bok K., Parra G.I., Mitra T., Abente E., Shaver C.K., Boon D., Engle R., Yu C., Kapikian A.Z., Sosnovtsev S.V., Purcell R.H., Green K.Y. Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:325-330.
7. Boon D., Mahar J.E., Abente E.J., Kirkwood C.D., Purcell R.H., Kapikian A.Z., Green K.Y., Bok K. Comparative evolution of GII.3 and GII.4 norovirus over a 31-year period. J. Virol. 2011, 85:8656-8666.
8. Bull R.A., Tu E.T., McIver C.J., Rawlinson W.D., White P.A. Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J. Clin. Microbiol. 2006, 44:327-333.
9. Chakravarty S., Hutson A.M., Estes M.K., Prasad B.V. Evolutionary trace residues in noroviruses: importance in receptor binding, antigenicity, virion assembly, and strain diversity. J. Virol. 2005, 79:554-568.
10. Fankhauser R.L., Monroe S.S., Noel J.S., Humphrey C.D., Bresee J.S., Parashar U.D., Ando T., Glass R.I. Epidemiologic and molecular trends of Norwalk-like viruses associated with outbreaks of gastroenteritis in the United States. J. Infect. Dis. 2002, 186:1-7.
11. Gallimore E. Acute abdominal pain. Nurs. Stand 2007, 21:59.
12. Guntapong R., Hansman G.S., Oka T., Ogawa S., Kageyama T., Pongsuwanna Y., Katayama K. Norovirus and sapovirus infections in Thailand. Jpn. J. Infect. Dis. 2004, 57:276-278.
13. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999, 41:95-98.
14. Hansman G.S., Katayama K., Maneekarn N., Peerakome S., Khamrin P., Tonusin S., Okitsu S., Nishio O., Takeda N., Ushijima H. Genetic diversity of norovirus and sapovirus in hospitalized infants with sporadic cases of acute gastroenteritis in Chiang Mai, Thailand. J. Clin. Microbiol. 2004, 42:1305-1307.
15. Ho E.C., Cheng P.K., Lau A.W., Wong A.H., Lim W.W. Atypical norovirus epidemic in Hong Kong during summer of 2006 caused by a new genogroup II/4 variant. J. Clin. Microbiol. 2007, 45:2205-2211.
16. Hutson A.M., Atmar R.L., Estes M.K. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 2004, 12:279-287.
17. Hymas W., Atkinson A., Stevenson J., Hillyard D. Use of modified oligonucleotides to compensate for sequence polymorphisms in the real-time detection of norovirus. J. Virol. Methods 2007, 142:10-14.
18. Jiang X., Wang J., Graham D.Y., Estes M.K. Detection of Norwalk virus in stool by polymerase chain reaction. J. Clin. Microbiol. 1992, 30:2529-2534.
19. Jiang X., Wang M., Graham D.Y., Estes M.K. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J. Virol. 1992, 66:6527-6532.
20. Jones K.E., Patel N.G., Levy M.A., Storeygard A., Balk D., Gittleman J.L., Daszak P. Global trends in emerging infectious diseases. Nature 2008, 451:990-993.
21. Jothikumar N., Lowther J.A., Henshilwood K., Lees D.N., Hill V.R., Vinje J. 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. 2005, 71:1870-1875.
22. Kageyama T., Kojima S., Shinohara M., Uchida K., Fukushi S., Hoshino F.B., Takeda N., Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 2003, 41:1548-1557.
23. Kamata K., Shinozaki K., Okada M., Seto Y., Kobayashi S., Sakae K., Oseto M., Natori K., Shirato-Horikoshi H., Katayama K., Tanaka T., Takeda N., Taniguchi K. Expression and antigenicity of virus-like particles of norovirus and their application for detection of noroviruses in stool samples. J. Med. Virol. 2005, 76:129-136.
24. Kapikian A.Z., Wyatt R.G., Dolin R., Thornhill T.S., Kalica A.R., Chanock R.M. Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. J. Virol. 1972, 10:1075-1081.
25. Katayama K., Shirato-Horikoshi H., Kojima S., Kageyama T., Oka T., Hoshino F., Fukushi S., Shinohara M., Uchida K., Suzuki Y., Gojobori T., Takeda N. Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology 2002, 299:225-239.
26. Khamrin P., Maneekarn N., Peerakome S., Tonusin S., Malasao R., Mizuguchi M., Okitsu S., Ushijima H. Genetic diversity of noroviruses and sapoviruses in children hospitalized with acute gastroenteritis in Chiang Mai, Thailand. J. Med. Virol. 2007, 79:1921-1926.
27. Kittigul L., Pombubpa K., Taweekate Y., Diraphat P., Sujirarat D., Khamrin P., Ushijima H. Norovirus GII-4 2006 variant circulating in patients with acute gastroenteritis in Thailand during a 2006-2007 study. J. Med. Virol. 2010, 82:854-860.
28. Kittigul L., Pombubpa K., Taweekate Y., Yeephoo T., Khamrin P., Ushijima H. Molecular characterization of rotaviruses, noroviruses, sapovirus, and adenoviruses in patients with acute gastroenteritis in Thailand. J. Med. Virol. 2009, 81:345-353.
29. Kroneman A., Vennema H., Deforche K.v.d., Avoort H., Penaranda S., Oberste M.S., Vinje J., Koopmans M. An automated genotyping tool for enteroviruses and noroviruses. J. Clin. Virol. 2011, 51:121-125.
30. Lindesmith L.C., Donaldson E.F., Lobue A.D., Cannon J.L., Zheng D.P., Vinje J., Baric R.S. Mechanisms of GII.4 norovirus persistence in human populations. PLoS. Med. 2008, 5:e31.
31. Mahar J.E., Kirkwood C.D. Characterization of norovirus strains in Australian children from 2006 to 2008: prevalence of recombinant strains. J. Med. Virol. 2011, 83:2213-2219.
32. Malasao R., Maneekarn N., Khamrin P., Pantip C., Tonusin S., Ushijima H., Peerakome S. Genetic diversity of norovirus, sapovirus, and astrovirus isolated from children hospitalized with acute gastroenteritis in Chiang Mai, Thailand. J. Med. Virol. 2008, 80:1749-1755.
33. Mattison K., Grudeski E., Auk B., Charest H., Drews S.J., Fritzinger A., Gregoricus N., Hayward S., Houde A., Lee B.E., Pang X.L., Wong J., Booth T.F., Vinje J. Multicenter comparison of two norovirus ORF2-based genotyping protocols. J. Clin. Microbiol. 2009, 47:3927-3932.
34. Moe C.L., Gentsch J., Ando T., Grohmann G., Monroe S.S., Jiang X., Wang J., Estes M.K., Seto Y., Humphrey C. Application of PCR to detect Norwalk virus in fecal specimens from outbreaks of gastroenteritis. J. Clin. Microbiol. 1994, 32:642-648.
35. Monica B., Ramani S., Banerjee I., Primrose B., Iturriza-Gomara M., Gallimore C.I., Brown D.W., Fathima M, Moses P.D., Gray J.J., Kang G. Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. J. Med. Virol. 2007, 79:544-551.
36. Nguyen T.A., Khamrin P., Takanashi S., Le Hoang P., Pham le D., Hoang K.T., Satou K., Masuoka Y., Okitsu S., Ushijima H. Evaluation of immunochromatography tests for detection of rotavirus and norovirus among Vietnamese children with acute gastroenteritis and the emergence of a novel norovirus GII.4 variant. J. Trop. Pediatr. 2007, 53:264-269.
37. Okada M., Ogawa T., Kaiho I., Shinozaki K. Genetic analysis of noroviruses in Chiba Prefecture, Japan, between 1999 and 2004. J. Clin. Microbiol. 2005, 43:4391-4401.
38. Ozawa K., Oka T., Takeda N., Hansman G.S. Norovirus infections in symptomatic and asymptomatic food handlers in Japan. J. Clin. Microbiol. 2007, 45:3996-4005.
39. Patel M.M., Widdowson M.A., Glass R.I., Akazawa K., Vinje J., Parashar U.D. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 2008, 14:1224-1231.
40. Phan T.G., Khamrin P., Akiyama M., Yagyu F., Okitsu S., Maneekarn N., Nishio O., Ushijima H. Detection and genetic characterization of norovirus in oysters from China and Japan. Clin. Lab. 2007, 53:405-412.
41. Prasad B.V., Rothnagel R., Jiang X., Estes M.K. Three-dimensional structure of baculovirus-expressed Norwalk virus capsids. J. Virol. 1994, 68:5117-5125.
42. Radford A.D., Gaskell R.M., Hart C.A. Human norovirus infection and the lessons from animal caliciviruses. Curr. Opin. Infect. Dis. 2004, 17:471-478.
43. Richards G.P., Watson M.A., Fankhauser R.L., Monroe S.S. Genogroup I and II noroviruses detected in stool samples by real-time reverse transcription-PCR using highly degenerate universal primers. Appl. Environ. Microbiol. 2004, 70:7179-7184.
44. Siebenga J.J., Vennema H., Renckens B., de Bruin E., van der Veer B., Siezen R.J., Koopmans M. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J. Virol. 2007, 81:9932-9941.
45. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
46. Trujillo A.A., McCaustland K.A., Zheng D.P., Hadley L.A., Vaughn G., Adams S.M., Ando T., Glass R.I., Monroe S.S. Use of TaqMan real-time reverse transcription-PCR for rapid detection, quantification, and typing of norovirus. J. Clin. Microbiol. 2006, 44:1405-1412.
47. Van Stelten A., Kreman T.M., Hall N., Desjardin L.E. Optimization of a real-time RT-PCR assay reveals an increase of genogroup I norovirus in the clinical setting. J. Virol. Methods 2011, 175:80-84.
48. Vinje J., Hamidjaja R.A., Sobsey M.D. Development and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J. Virol. Methods 2004, 116:109-117.
49. White P.A., Hansman G.S., Li A., Dable J., Isaacs M., Ferson M., McIver C.J., Rawlinson W.D. Norwalk-like virus 95/96-US strain is a major cause of gastroenteritis outbreaks in Australia. J. Med. Virol. 2002, 68:113-118.
50. Widdowson M.A., Sulka A., Bulens S.N., Beard R.S., Chaves S.S., Hammond R., Salehi E.D., Swanson E., Totaro J., Woron R., Mead P.S., Bresee J.S., Monroe S.S., Glass R.I. Norovirus and foodborne disease, United States, 1991-2000. Emerg. Infect. Dis. 2005, 11:95-102.
51. Wolf S., Williamson W.M., Hewitt J., Rivera-Aban M., Lin S., Ball A., Scholes P., Greening G.E. Sensitive multiplex real-time reverse transcription-PCR assay for the detection of human and animal noroviruses in clinical and environmental samples. Appl. Environ. Microbiol 2007, 73:5464-5470.
52. Zheng D.P., Ando T., Fankhauser R.L., Beard R.S., Glass R.I., Monroe S.S. Norovirus classification and proposed strain nomenclature. Virology 2006, 346:312-323.