Abstract
Norovirus (NoV) genogroup (G) IV has been infrequently isolated from patients suffering from acute gastroenteritis (AGE), although this virus has not been detected in Korea. Klassevirus, a novel virus belonging to the family Picornaviridae and a possible etiologic agent of AGE, and pepper mild mottle virus (PMMoV), which originates from processed pepper products and is shed in human feces, are suggested to be new indicators of fecal pollution. We aimed to investigate the presence of NoV-GIV, klassevirus, and PMMoV in sewage samples collected in Korea. Between December 2010 and February 2012, influent sewage samples were collected every month from a wastewater treatment plant located in the eastern part of Seoul in Korea. The sewage samples were concentrated by the adsorption elution method using an HA (pore size of 0.45 μm with mixed cellulose ester) electronegative filter with an acid-rinse procedure. RT-PCR was performed using specific primers for the capsid gene of NoV-GII and NoV-GIV, the coat gene of PMMoV, and the VP0/VP1 gene of klassevirus. Among the 14 sewage samples tested, klassevirus was detected in eight (57.1 %), PMMoV in eight (57.1 %), NoV-GII in five (35.7 %), and NoV-GIV in three (21.4 %). NoV-GIV was detected in December 2010 and January and March 2011. PMMoV and klassevirus were frequently detected in winter. Phylogenetic analysis revealed that the NoV-GIV detected in this study belonged to G-IV1 lineage. This is the first study to confirm the presence of NoV-GIV, klassevirus, and PMMoV in sewage samples in Korea.
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References
Fernandez MD, Torres C, Poma HR, Riviello-Lopez G, Martinez LC, Cisterna DM, Rajal VB, Nates SV, Mbayed VA (2012) Environmental surveillance of norovirus in Argentina revealed distinct viral diversity patterns, seasonality and spatio-temporal diffusion processes. Sci Total Environ 437:262–269
Fumian TM, Vieira CB, Leite JP, Miagostovich MP (2013) Assessment of burden of virus agents in an urban sewage treatment plant in Rio de Janeiro, Brazil. J Water Health 11:110–119
Rodriguez RA, Gundy PM, Rijal GK, Gerba CP (2012) The impact of combined sewage overflows on the viral contamination of receiving waters. Food Environ Virol 4:34–40
Kim WJ, Managaki S, Furumai H, Nakajima F (2009) Diurnal fluctuation of indicator microorganisms and intestinal viruses in combined sewer system. Water Sci Technol 60:2791–2801
Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe S (2006) Norovirus classification and proposed strain nomenclature. Virology 346:312–313
Ando T, Noel JS, Fankhauser RL (2000) Genetic classification of “Norwalk-like viruses”. J Infect Dis 181:S336–S348
Bon F, Ambert-Balay K, Giraudon H, Kaplon J, Le Guyader S, Pommepuy M, Gallay A, Vaillant V, de Valk H, Chikhi-Brachet R, Flahaut A, Pothier P, Kohli E (2005) Molecular epidemiology of caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from December 1998 to February 2004. J Clin Microbiol 43:4659–4664
Frankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, ANdo T, Glass RI (2001) Epidemiologic and molecular trends of “Norwalk like viruses” associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186:1–7
Phan TG, Okame M, Nguyen TA, Maneekam N, Nishio O, Okitsu S, Ushijima H (2004) Human astrovirus, norovirus (GI, GII), and sapovirus infections in Pakistani children with diarrhea. J Med Virol 73:256–261
Gomes KA, Stupka JA, Gómez J, Parra GI (2007) Molecular characterization of calicivirus strains detected in outbreaks of gastroenteritis in Argentina. J Med Virol. 79:1703–1709
Khamrin P, Maneekarn N, Thongprachum A, Chaimongkol N, Okitsu S, Ushijima H (2010) Emergence of new norovirus variants and genetic heterogeneity of noroviruses and sapoviruses in children admitted to hospital with diarrhea in Thailand. J Med Virol 82:289–296
Kitajima M, Haramoto E, Phanuwan C, Katayama H, Ohgaki S (2009) Detection of genogroup IV norovirus in wastewater and river water in Japan. Lett Appl Microbiol. 49:655–658
Kremer JR, Langlet J, Skraber S, Weicherding P, Weber B, Cauchie HM, De Landtsheer S, Even J, Muller CP, Hoffmann L, Mossong J (2010) Genetic diversity of noroviruses from outbreaks, sporadic cases and wastewater in Luxembourg 2008-2009. Clin Microbiol Infect 17:1173–1176
La Rosa G, Iaconelli M, Pourshaban M, Fratini M, Muscillo M (2010) Molecular detection and genetic diversity of norovirus genogroup IV: a year-long monitoring of sewage throughout Italy. Arch Virol 155:589–593
Martella V, Decaro N, Lorusso E, Radogna A, Moschidou P, Amorisco F, Lucente MS, Desario C, Mari V, Elia G, Banyai K, Carmichael LE, Buonavoglia C (2009) Genetic heterogeneity and recombination in canine noroviruses. J Virol 83:11391–11396
Chung JY, Han TH, Park SH, Kim SW, Hwang ES (2010) Detection of GII-4/2006b variant and recombinant noroviruses in children with acute gastroenteritis. J Med Virol 82:146–152
Han TH, Kim CH, Chung JY, Park SH, Hwang ES (2011) Emergence of norovirus GII-4/2008 variant and recombinant strains in Seoul, Korea. Arch Virol 156:323–329
Lee H, Kim M, Lee JE, Lim M, Kim M, Kim JM, Jehong WH, Kim J, Ko G (2011) Investigation of norovirus occurrence in ground water in metropolitan Seoul, Korea. Sci Total Environ 409:2078–2084
Lee SG, Jehong 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 77:1466–1474
Li L, Victoria J, Kapoor A, Blinkova O, Wang C, Babrzadeh F, Mason CJ, Pandey P, Triki H, Bahri O, Oderinde BS, Baba MM, Bukbuk DN, Besser JM, Bartkus JM, Delwart EL (2011) A novel picornavirus associated with gastroenteritis. J Virol 83:12002–12006
Shan T, Wang C, Cui L, Yu Y, Delwart E, Zhao W, Zhu C, Lan D, Dai X, Hua X (2010) Picornavirus salivirus/klassevirus in children with diarrhea, China. Emerg Infect Dis 16:1303–1305
Han TH, Kim CH, Chung JY, Park SH, Hwang ES (2010) Klassevirus infection in children, South Korea. Emerg Infect Dis 16:1623–1625
Greninger AL, Runckel C, Chiu CY, Haggerty T, Parsonnet J, Ganem D, DeRisi JL (2009) The complete genome of klassevirus—a novel picornavirus in pediatric stool. Virol J 6:82
Holtz LR, Finkbeiner SR, Zhao G, Kirkwood CD, Girones R, Pipas JM, Wand D (2009) Klassevirus 1, a previously undescribed member of the family Picornaviridae, is globally widespread. Virol J 6:86
Haramoto E, Otagiri M (2013) Prevalence and genetic diversity of klassevirus in waste water. Food Environ Virol 5:46–51
Zhang T, Breitbart M, Lee WH, Run JQ, Wei CL, Soh SW, Hibberd ML, Liu ET, Rohwer F, Ruan Y (2006) RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol 4:e3
Hamza IA, Jurzik L, Uberla K, Wilhelm M (2011) Evaluation of pepper mild mottle virus, human picobirnavirus and Torque tenovirus as indicators of fecal contamination in river water. Water Res 45:1358–1368
Rosario K, Symonds EM, Sinigallioano C, Stewart J, Breitbart M (2009) Pepper mild mottle virus as an indicator of fecal solution. Appl Environ Microbiol 75:7261–7267
Katayama H, Shimasaki A, Ohgaki S (2002) Development of a virus concentration method and its application to detection of enterovirus and Norwalk virus from coastal seawater. Appl Environ Microbiol 68:1033–1039
Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, Uchida K (2002) Genogroup specific PCR primers for detection of Norwalk viruses. J Virol Methods 100:107–114
Chung BN, Choi HS, Yang EY, Cho JD, Cho IS, Choi GS, Choi SK (2012) Tomato spotted wilt virus isolates giving different infection in commercial capsicum annuum Cultivars. Plant Pathol J 28:87–92
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Ng TF, Marine R, Wang C, Simmonds P, Kapusinszky B, Bodhidatta L, Oderinede BS, Wommack KE, Delwart E (2012) High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage. J Virol 86:12161–12175
Iwai M, Hasegawa S, Obara M, Nakamura K, Horimoto E, Takizawa T, Kurata T, Sogen SI, Shiraki K (2009) Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyama, Japan (2006 to 2008). Appl Environ Microbiol 75:1264–1270
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 44:1405–1412
La Rosa G, Pourshaban M, Iaconelli M, Muscillo M (2008) Detection of genogroup IV noroviruses in environmental and clinical samples and partial sequencing through rapid amplification of cDNA endes. Arch Virol 153:2077–2083
La Rosa G, Fratini M, Vennarucci VS, Guerico A, Purpari G, Muscillo M (2012) GIV noroviruses and other enteric viruses in bivalves: a preliminary study. New Microbiol 35:27–34
Kitajima M, Oka T, Haramoto E, Phanuwan C, Takeda N, Katayama K, Katayama H (2010) Genetic diversity of genogroup IV noroviruses in wastewater in Japan. Lett Appl Microbiol 52:181–184
Eden JS, Lim KL, White PA (2012) Complete genome of human norovirus GIV.1 strain Lake Macquarie virus. J Virol 86:10251–10252
Kitajima M, Haramoto E, Phanuwan C, Katayama H, Furumai H (2012) Molecular detection and genotyping of human noroviruses in influent and effluent water at a wastewater treatment plant in Japan. J Appl Microbiol 112:605–613
Haramoto E, Kitajima M, Otagiri M (2013) Development of a reverse transcription-quantitative PCR assay for detection of salivirus/klassevirus. Appl Environ Microbiol 79:3529–3532
Colson P, Richet H, Desnues C, Balique F, Moal V, Grob JJ, Berbis P, Lecoq H, Harle JR, Berland Y, Raoult D (2010) Pepper mild mottle virus, a plant virus associated with specific immune responses, fever, abdominal pains, and pruritus in humans. PLoS One 5:e10041
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This work was partially supported by a 2012 Inje University Research Grant.
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This work was partially supported by the 2012 Inje University Research Grant.
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Han, TH., Kim, SC., Kim, ST. et al. Detection of norovirus genogroup IV, klassevirus, and pepper mild mottle virus in sewage samples in South Korea. Arch Virol 159, 457–463 (2014). https://doi.org/10.1007/s00705-013-1848-7
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DOI: https://doi.org/10.1007/s00705-013-1848-7