Vibrio parahaemolyticus is a major foodborne pathogen in China and other countries. In this study, a total of 578 clinical V. parahaemolyticus strains and 51 foodborne strains were isolated during the period from 2009 to 2011 in the eastern coastal city of Shanghai, China. Their serotypes, virulence genes, pandemic traits, and genotyping were investigated. A total of nine O groups and 20 K types were identified by serological analysis of all isolates. Six different O groups and 14 different K types were detected among the 578 clinical strains. Eight different O groups and five K types were detected among the 51 foodborne strains. The O3:K6 serotype was the dominant serotype. A total of 200 representative clinical strains and 51 foodborne isolates were analyzed for virulence genes, pandemic traits, and genotyping. Of the clinical strains, 92.5% had the virulence genes tdh and/or trh. Four foodborne isolates had virulence genes; one trh-positive strain was O3:K6 and three tdh-positive strains were either O4:KUT or O3:KUT. Molecular typing by pulsed-field gel electrophoresis also showed divergence among the nonpandemic strains, although the pandemic strains formed a cluster. These results suggest high serodiversity and genetic diversity of V. parahaemolyticus. Pathogenic isolates were present in food, thus representing a public health risk and warranting epidemiological and ecological monitoring to ensure safety.
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References
1.
AnsaruzzamanM, LucasM, DeenJL, BhuiyanNA, WangXY, SafaA, SultanaM, ChowdhuryA, NairGB, SackDA, Von SeidleinL, PuriMK, AliM, ChaignatCL, ClemensJD, BarretoA. Pandemic serotypes (O3:K6 and O4:K68) of Vibrio parahaemolyticus associated with diarrhea in Mozambique: Spread of the pandemic into the African continent. J Clin Microbiol, 2005; 43:2559–2562.
2.
ArakawaE, MuraseT, ShimadaT, OkitsuT, YamaiS, WatanabeH. Emergence and prevalence of a novel Vibrio parahaemolyticus O3:K6 clone in Japan. Jpn J Infect Dis, 1999; 52:246–247.
3.
BejAK, PattersonDP, BrasherCW, VickeryMC, JonesDD, KaysnerCA. Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh. J Microbiol Meth, 1999; 36:215–225.
4.
BoydEF, CohenAL, NaughtonLM, UsseryD, BinnewiesTT, StineOC, ParentMA. Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus. BMC Microbiol, 2008; 8:110.
5.
[CDC] Centers for Disease Control and Prevention. http://www.pulsenetinternational.org/SiteCollectionDocuments/pfge/5.72_2009_PNetStandProtVparahaem.pdf. 2010 June 23.
6.
ChaoGX, JiaoXN, ZhouXH, YangZQ, HuangJL, PanZM, ZhouL, QianXQ. Serodiversity, pandemic O3:K6 clone, molecular typing and antibiotic susceptibility of foodborne and clinical Vibrio parahaemolyticus isolates in Jiangsu, China. Foodborne Pathog Dis, 2009; 8:1021–1028.
7.
ChaoGX. Ph.D. thesis, Yangzhou University, Jiangsu. Characterization of transmission and molecular epidemiology of Vibrio parahaemolyticus and multilocus sequences typing of O3:K6 pandemic clone, 2010.
ChowdhuryA, IshibashiM, ThiemVD, TuyetDT, TungTV, ChienBT, von SeidleinL, CanhDG, ClemensJ. Emergence and serovar transition 339 of Vibrio parahaemolyticus pandemic strains isolated during a diarrhea outbreak in Vietnam between 1997–1999. Microbiol Immunol, 2004; 48:319–327.
10.
DanielsNA, MackinnonL, BishopR, AltekruseS, RayB, HammondRM, ThompsonS, WilsonS, BeanNH, GriffinPM, SlutskerL. Vibrio parahaemolyticus infections in the United States, 1973–1998. J Infect Dis, 2000; 181:1661–1666.
11.
DePaolaA, KaysnerCA, BowersJ, CookDW. Environmental investigations of Vibrio parahaemolyticus in oysters after outbreaks in Washington, Texas and New York (1997 and 1998)Appl Environ Microbiol, 2000; 66:4649–4654.
12.
DePaolaA, UlaszekJ, KaysnerCA, TengeBJ, NordstromJL, WellJ, PuhrN, GendelSM. Molecular, serological, and virulence characteristics of Vibrio parahaemolyticus isolated from environmental, food, and clinical sources in North America and Asia. Appl Environ Microbiol, 2003; 69:3999–4005.
13.
DiRitaVJ. Co-ordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol Microbiol, 1992; 6:451–458.
IshibashiM, OhtaK, ShimadaT, HondaT, SugiyamaJ, MiwataniT, YokooH. Current status of OK serotype combinations of Vibrio parahaemolyticus. Nippon Saikingaku Zasshi, 2000; 55:539–541. (In Japanese.)
20.
KamKM, LueyCKY, ParsonsMB, CooperKLF, NairGB, AlamM, IslamMA, CheungDTL, ChuYW, RamamurthyT, PazhaniGP, BhattacharyaSK, WatanabeH, TerajimaJ, ArakawaE, RatchtrachenchaiOA, HuttayananontS, RibotEM, Gerner-SmidtP, SwaminathanB. Vibrio parahaemolyticus PulseNet PFGE Protocol Working Group. Evaluation and validation of a PulseNet standardized pulsed-field gel electrophoresis protocol for subtyping Vibrio parahaemolyticus: An international multicenter collaborative study. J Clin Microbiol, 2008; 8:2766–2773.
21.
KeBX, TanHL, LiBS, HeDM, MaC, LiuMZ, ChenJD, KeCW. Etiologic characteristics of Vibrio parahaemolyticus strains causing outbreak and sporadic cases in Guangdong. Chin J Epidemiol, 2011; 12:1237–1241. (In Chinese.)
22.
LiuH. Analysis of the collective food poisoning events in Shanghai from 1990 to 2000. Chinese J Natural Med, 2003; 5:17–20. (In Chinese.)
23.
LiuXM, ChenY, FanYX, WangMQ. Foodborne disease occurred in 2003—Report of the National Foodborne Diseases Surveillance Systems. Wei Sheng Yan Jiu, 2006; 35:201–204. (In Chinese.)
24.
MahmudZH, NeogiSB, KassuA, WadaT, IalamMS, NairGB, OtaF. Seaweeds as a reservoir for diverse Vibrio parahaemolyticus populations in Japan. Int J Food Microbiol, 2007; 118:92–96.
25.
Martinez-UrtazaJ, Lozano-LeonA, DepaolaA, IshibashiM, ShimadaK, NishibuchiM, LiebanaE. Characterization of pathogenic Vibrio parahaemolyticus isolates from clinical sources in Spain and comparison with Asian and North American pandemic isolates. J Clin Microbiol, 2004; 42:4672–4678.
26.
MatsumotoC, OkudaJ, IshibashiM, IwanagaM, GargP, RammamurthyT, WongHC, DepaolaA, KimYB, AlbertMJ, NishibuchiM. Pandemic spread of an O3:K6 clone of Vibrio parahaemolyticus and emergence of related evidence by arbitrarily primed PCR and toxRS sequence analyses. J Clin Microbiol, 2000; 38:578–585.
27.
NairGB, RamamurthyT, BhattacharyaSK, DuttaB, TakedaY, SackDA. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin Microbiol Rev, 2007; 20:39–48.
28.
NishibuchiM, KaperJB. Thermostable direct hemolysin gene of Vibrio parahaemolyticus: A virulence gene acquired by a marine bacterium. Infect Immun, 1995; 63:2093–2099.
29.
NordstromJL, VickeryMC, BlackstoneGM, MurraySL, DePaolaA. Development of a multiplex real-time PCR assay with an internal amplification control for the detection of total and pathogenic Vibrio parahaemolyticus bacteria in oysters. Appl Environ Microbiol, 2007; 73:5840–5847.
30.
OkudaJ, IshibashiM, HayakawaE, NishinoT, TakedaY, MukhopadhyayAK, GargS, BhattacharyaSK, NairGB, NishibuchiM. Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Kolkata, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J Clin Microbiol, 1997; 35:3150–3155.
31.
OkuraM, OsawaR, IguchiA, ArakawaE, TerjimaJ, WatanabeH. Genotypic analysis of Vibrio parahaemolyticus and development of a pandemic group-specific multiplex PCR assay. J Clin Microbiol, 2003; 41:4674–4682.
32.
PalD, DasN. Isolation, identification and molecular characterization of Vibrio parahaemolyticus from fish samples in Kolkata. Eur Rev Med Pharmacol Sci, 2010; 14:545–549.
33.
QuM, ZhangX, LiuDR, HuangY, LiJ, LiXT, LiuY, YanHQ, LiuBW, LiXY, WangQY, HuangF. Analysis on the etiological and molecular epidemiological characteristics of Vibrio parahaemolyticus in Beijing. Chin J Epidemiol, 2011; 12:1255–1258. (In Chinese.)
34.
ReichKA, SchoolnikGK. The light organ symbiont Vibrio fischeri possesses a homolog of the Vibrio cholerae transmembrane transcriptional activator ToxR. J Bacteriol, 1994; 176:3085–3088.
35.
SmolikovaL, LomovM, KhomenkoTV, MurnachevGP, KudriakovaTA, FetsaľlovaOP, SanamiantsEM, MakedonovaLD, KachkinaGV, GolenishchevaEN. Studies on halophilic vibrios causing a food poisoning outbreak in the city of Vladivostok. ZH. Microbiol Epidemiol Immunobiol, 2001; 63:3–7.
36.
Velazquez-RomanJ, Leòn-SicairosN, Flores-VillaseňorH, Villafaňa-RaudaS, Canizalez-RomanA. Association of pandemic Vibrio parahaemolyticus O3:K6 present in the coastal environment of Northwest Mexico with cases of recurrent diarrhea between 2004 and 2010. Appl Environ Microbiol, 2012; 78:1794–1803.
37.
WongHC, LiuSH, WangTK, LeeCL, ChiouCS, LiuDP, NishibuchiM, LeeBK. Characterization of Vibrio parahaemolyticus O3:K6 from Asia. Environ Microbiol, 2000; 66:3981–3986.
