Detection of Vibrio parahaemolyticus in shellfish by use of multiplexed real-time PCR with TaqMan fluorescent probes

Applied and Environmental Microbiology

Volumn 72, Issue 3, 2006, Pages 2031-2042

  Ward, Linda N ^a,b   Bej, Asim K ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b Identigene Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; EPIDEMIOLOGY; FOOD PRODUCTS; GENES; PROBES; REAL TIME SYSTEMS; TISSUE;

OLIGONUCLEOTIDE PRIMERS; SHELLFISH; THERMOLABILE HEMOLYSIN GENE (TLH); VIBRIO PARAHAEMOLYTICUS;

BIODIVERSITY;

BACTERIAL DNA; GENOMIC DNA; HEMOLYSIN; OLIGONUCLEOTIDE;

POLYMERASE CHAIN REACTION;

ACUTE GASTROENTERITIS; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIUM DETECTION; CONTROLLED STUDY; EPIDEMIC; NONHUMAN; OLIGONUCLEOTIDE PROBE; OPEN READING FRAME; OYSTER; PANDEMIC; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SEROTYPE; SHELLFISH; TDH GENE; TISSUE HOMOGENATE; TLH GENE; TRH GENE; VIBRIO PARAHAEMOLYTICUS;

ANIMALS; COLONY COUNT, MICROBIAL; DNA PRIMERS; FLUORESCENT DYES; OSTREIDAE; POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SHELLFISH; TAQ POLYMERASE; VIBRIO PARAHAEMOLYTICUS;

ANIMALIA; BACTERIA (MICROORGANISMS); OSTREIDAE; VIBRIO PARAHAEMOLYTICUS;

EID: 33644932926     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.72.3.2031-2042.2006     Document Type: Article

References (62)

1. American Public Health Association. 1970. Recommended procedures for the examination of seawater and shellfish, 4th ed. American Public Health Association, Washington, D.C.
2. Atlas, R. M. 1993. Handbook of microbiological media, p. 529. CRC Press, Boca Raton, Fla.
3. Atlas, R. M., and A. K. Bej. 1994. Polymerase chain reaction, p. 418-435. In P. Gerhardt, R. G. E. Murray, W. A. Wood, and N. R. Krieg (ed.), Methods for general and molecular bacteriology. ASM Press, Washington, D.C.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Smith, J. G. Sideman, and K. Struhl (ed.). 1987. Current protocols in molecular biology, p. 2.10-2.11. John Wiley & Sons, Inc., New York, N.Y.
5. Bates, T. C., and J. D. Oliver. 2004. The viable but nonculturable state of Kanagawa positive and negative strains of Vibrio parahaemolyticus. J. Microbiol. 42:74-79.
6. Bej, A. K., D. P. Patterson, C. W. Brasher, M. C. L. Vickery, D. D. Jones, and C. A. Kaysner. 1999. Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh. J. Microbiol. Methods 36:215-225.
7. Bhuiyan, N. A., M. Anasaruzzaman, M. Kamruzzaman, K. Alam, N. R. Chowdhury, M. Nishibuchi, S. M. Faruque, D. A. Sack, Y. Takeda, and G. B. Nair. 2002. Prevalence of the pandemic genotype of Vibrio parahaemolyticus in Dhaka, Bangladesh, and significance of its distribution across different serotypes. J. Clin. Microbiol. 40:284-286.
8. Blackstone, G. M., J. L. Nordstrom, M. C. L. Vickery, M. D. Bowen, R. F. Meyer, and A. DePaola. 2003. Detection of pathogenic Vibrio parahaemolyticus in oyster enrichments by real time PCR. J. Microbiol. Methods 53:149-155.
9. Blake, P. A., R. E. Weaver, and D. G. Hollis. 1980. Disease of humans (other than cholera) caused by vibrios. Annu. Rev. Microbiol. 34:341-367.
10. Brasher, C. W., A. DePaola, D. D. Jones, and A. K. Bej. 1998. Detection of microbial pathogens in shellfish with multiplex PCR. Curr. Microbiol. 37:101-107.
11. Centers for Disease Control and Prevention. 1998. Outbreak of Vibrio parahaemolyticus infections associated with eating raw oysters-Pacific Northwest, 1997. Morb. Mortal. Wkly. Rep. 47:457-462.
12. Centers for Disease Control and Prevention. 1999. Outbreak of Vibrio parahaemolyticus infection associated with eating raw oysters or clams harvested from Long Island Sound, Connecticut, New Jersey, and New York, 1998. Morb. Moral. Wkly. Rep. 48:48-51.
13. Chaiyanan, S., S. Chaiyanan, A. Huq, T. Maugel, and R. R. Colwell. 2001. Viability of the nonculturable Vibrio cholerae O1 and O139. Syst. Appl. Microbiol. 24:331-341.
14. Chiou, C.-S., S.-Y. Hsu, S.-I. Chiu, T.-K. Wang, and C.-S. Chao. 2000. Vibrio parahaemolyticus serovar O3:K6 as cause of unusually high incidence of food-borne disease outbreaks in Taiwan from 1996 to 1999. J. Clin. Microbiol. 38:4621-4625.
15. Daniels, N. A., B. Ray, A. Easton, N. Marano, E. Kahn, A. L. McShan, L. Del Rosario, T. Baldwin, M. A. Kingsley, N. D. Puhr, J. G. Wells, and F. J. Angulo. 2000. Emergence of a new Vibrio parahaemolyticus serotype in raw oysters. JAMA 284:1541-1545.
16. Davis, C. R., L. C. Heller, K. K. Peak, D. L. Wingfield, C. L. Goldstein-Hart, D. W. Bodager, A. C. Cannons, P. T. Amuso, and J. Cattanii. 2004. Real-time PCR detection of the thermostable direct hemolysin and thermolabile hemolysin genes in a Vibrio parahaemolyticus cultured from mussels and mussel homogenate associated with a foodborne outbreak. J. Food Prot. 67:1005-1008.
17. DePaola, A., C. A. Kaysner, J. Bowers, and D. W. Cook. 2000. Environmental investigations of Vibrio parahaemolyticus in oysters after outbreaks in Washington, Texas, and New York (1997 and 1998). Appl. Environ. Microbiol. 66:4649-4654.
18. DePaola, A., J. L. Nordstrom, J. C. Bowers, J. G. Wells, and D. W. Cook. 2003. Seasonal abundance of total and pathogenic Vibrio parahaemolyticus in Alabama oysters. Appl. Environ. Microbiol. 69:1521-1526.
19. Fukushima, H., Y. Tsunomori, and R. Seki. 2003. Duplex real-time SYBR green PCR assays for detection of 17 species of food- or waterborne pathogens in stools. J. Clin. Microbiol. 41:5134-5146.
20. Hein, I., A. Lehner, P. Rieck, K. Klein, E. Brandl, and M. Wagner. 2001. Comparison of different approaches to quantify Staphylococcus aureus cells by real-time quantitative PCR and application of this technique for examination of cheese. Appl. Environ. Microbiol. 67:3122-3126.
21. Hobbie, J. E., R. J. Daley, and S. Jasper. 1977. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33:1225-1228.
22. Honda, S., I. Goto, I. Minematsu, N. Ikeda, N. Asano, M. Ishibashi, Y. Kinoshita, M. Nishibuchi, T. Ohnda, and T. Miwatani. 1987. Vibrio parahaemolyticus infectious disease caused by Kanagawa phenomenon-negative O3:K6 originated from Maldives. Kansenshogaku Zasshi 61:1070-1078.
23. Honda, T., and T. Iida. 1993. The pathogenicity of Vibrio parahaemolyticus and the role of the thermostable direct haemolysin and related haemolysins. Rev. Med. Microbiol. 4:106-113.
24. Honda, T., Y. Ni, and T. Miwatani. 1989. Purification of a TDH-related hemolysin produced by a Kanagawa phenomenon-negative clinical isolate of Vibrio parahaemolyticus O6:K46. FEMS Microbiol. Lett. 57:241-245.
25. Honda, T., Y. X. Ni, and T. Miwatani. 1988. Purification and characterization of a hemolysin produced by clinical isolate of Kanagawa phenomenon-negative Vibrio parahaemolyticus and related to the thermostable direct hemolysin. Infect. Immun. 56:961-965.
26. Iida, T., A. Hattori, K. Tagomori, H. Nasu, R. Naim, and T. Honda. 2001. Filamentous phage associated with recent pandemic strains of Vibrio parahaemolyticus. Emerg. Infect. Dis. 7:477-478.
27. Iijima, Y., N. T. Asako, M. Aihara, and K. Hayashi. 2004. Improvement in the detection rate of diarrhoeagenic bacteria in human stool specimens by a rapid real-time PCR assay. J. Med. Microbiol. 53:617-622.
28. Interstate Shellfish Sanitation Conference. 2000. Vibrio parahaemolyticus interim control plan for oysters. Interstate Shellfish Sanitation Conference, Columbia, S.C.
29. Janda, J. M., C. Powers, R. G. Bryant, and S. Abbot. 1988. Current perspectives on the epidemiology and pathogenesis of clinically significant Vibrio spp. Clin. Microbiol. Rev. 1:245-267.
30. Jiang, X., and T. J. Chai. 1996. Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl. Environ. Microbiol. 62:1300-1305.
31. Kaufman, G. E., M. L. Myers, C. L. Pass, A. K. Bej, and C. A. Kaysner. 2002. Molecular analysis of Vibrio parahaemolyticus isolated from human patients and shellfish during US Pacific Northwest outbreaks. Lett. Appl. Microbiol. 34:155-161.
32. Kaysner, C. A., and A. DePaola, Jr. 2001. Vibrio, p. 405-420. In F. P. Downes and K. Ito (ed.), Compendium of methods for the microbiological examination of food. American Public Health Association, Washington, D.C.
33. Lozano-Leon, A., J. Torres, C. R. Osorio, and J. Martinez-Urtaza. 2003. Identification of tdh-positive Vibrio parahaemolyticus from an outbreak associated with raw oyster consumption in Spain. FEMS Microbiol. Lett. 226:281-284.
34. Lunge, V. R., B. J. Miller, K. J. Livak, and C. A. Batt. 2002. Factors affecting the performance of 5′ nuclease PCR assays for Listeria monocytogenes detection. J. Microbiol. Methods 51:361-368.
35. Matsumoto, C., J. Okuda, M. Ishibashi, M. Iwanaga, P. Garg, T. Ramamurthy, H. C. Wong, A. DePaola, Y. B. Kim, M. J. Albert, and M. Nishibuchi. 2000. Pandemic spread of an O3:K6 clone of Vibrio parahaemolyticus and emergence of related strains evidenced by arbitrarily primed PCR and toxRS sequence analyses. J. Clin. Microbiol. 38:578-585.
36. Miyamoto, Y., T. Kato, S. Obra, S. Akiyama, K. Takizawa, and S. Yamai. 1969. In vitro hemolytic characteristic of Vibrio parahaemolyticus: its close correlation with human pathogenicity. J. Bacteriol. 100:1147-1149.
37. Myers, M. L., G. Panicker, and A. K. Bej. 2003. PCR detection of a newly emerged pandemic Vibrio parahaemolyticus O3:K6 pathogen in pure cultures and seeded waters from the Gulf of Mexico. Appl. Environ. Microbiol. 69:2194-2200.
38. Nasu, H., T. Iida, T. Sugahara, Y. Yamaichi, K.-S. Park, K. Yokoyama, K. Makino, H. Shinagawa, and T. Honda. 2000. A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3:K6 strains. J. Clin. Microbiol. 38:2156-2161.
39. Okuda, J., M. Ishibashi, E. Hayakawa, T. Nishino, Y. Takeda, A. K. Mukhopadhyay, S. Garg, S. K. Bhattacharya, G. B. Nair, and M. Nishibuchi. 1997. Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Calcutta, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J. Clin. Microbiol. 35:3150-3155.
40. Okuda, J., and M. Nishibuchi. 1998. Manifestation of the Kanagawa phenomenon, the virulence-associated phenotype, of Vibrio parahaemolyticus depends on a particular single base change in the promoter of the thermostable direct haemolysin gene. Mol. Microbiol. 30:499-511.
41. Okura, M., R. Osawa, A. Iguchi, E. Arakawa, J. Terjima, and H. Watanabe. 2003. Genotypic analyses of Vibrio parahaemolyticus and development of a pandemic group-specific multiplex PCR assay. J. Clin. Microbiol. 41:4676-4682.
42. Oliver, J. D. 2005. The viable but nonculturable state in bacteria. J. Microbiol. 43:93-100.
43. Panicker, G., M. L. Myers, and A. K. Bej. 2004. Rapid detection of Vibrio vulnificus in shellfish and Gulf of Mexico water by real-time PCR. Appl. Environ. Microbiol. 70:498-507.
44. Panicker, G., M. L. Myers, and A. K. Bej. 2005. Real-time PCR detection of Vibrio vulnificus in oysters: comparison of oligonucleotide primers and probes targeting vvhA. Appl. Environ. Microbiol. 71:5702-5709.
45. Potasman, I., A. Paz, and M. Odeh. 2002. Infectious outbreaks associated with bivalve shellfish consumption: a worldwide perspective. Clin. Infect. Dis. 35:921-928.
46. Rippey, S. R. 1994. Infectious diseases associated with molluscan shellfish consumption. Clin. Microbiol. Rev. 7:419-425.
47. Rychilk, W., and R. E. Rhoads. 1989. A computer program for choosing 16 optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucleic Acids Res. 17:8543-8551.
48. Shirai, H., H. Ito, T. Hirramaya, T. Nakamoto, N. Nakabayashi, K. Kumagai, Y. Takeda, and M. Nishibuchi. 1990. Molecular epidemiologic evidence for association of thermostable direct hemolysin (TDH) and TDH-related hemolysin of Vibrio parahaemolyticus with gastroenteritis. Infect. Immun. 58:3568-3573.
49. Smolikova, L. M., I. M. Lomov, T. V. Khomenko, G. P. Murnachev, T. A. Kudriakova, O. P. Fetsailova, E. M. Sanamiants, L. D. Makedonova, G. V. Kachkina, and E. N. Golenishcheva. 2001. Studies on halophilic vibrios causing a food poisoning outbreak in the city of Vladivostok. Zh. Mikrobiol. Epidemiol. Immunobiol. 6:3-7.
50. Takeda, Y. 1982. Thermostable direct hemolysin of Vibrio parahaemolyticus. Pharmacol. Ther. 19:123-146.
51. Taniguchi, H., H. Hirano, S. Kubomura, K. Higashi, and Y. Mizuguchi. 1986. Comparison of the nucleotide sequences of the genes for the thermostable direct hemolysin and the thermolabile hemolysin from Vibrio parahaemolyticus. Microb. Pathog. 1:425-432.
52. Taniguchi, H., H. Ohta, M. Ogawa, and Y. Mizuguchi. 1985. Cloning and expression in Escherichia coli of Vibrio parahaemolyticus thermostable direct hemolysin and thermolabile hemolysin genes. J. Bacteriol. 162:510-515.
53. Twedt, R. M. 1989. Vibrio parahaemolyticus, p. 552-554. In M. P. Doyle (ed.), Foodborne bacterial pathogens. Marcel Dekker Inc., New York, N.Y.
54. Ugozzoli, L. A., and K. Hamby. 2004. Four-color multiplex 5′ nuclease assay for the simultaneous detection of the factor V Leiden and the prothrombin G20210A mutations. Mol. Cell. Probes 18:161-166.
55. Vickery, M. C. L., G. M. Blackstone, J. L. Nordstrom, and A. DePaola. 2005. Detection and quantification of total and potentially virulent Vibrio parahaemolyticus using a 4-channel multiplex real-time PCR targeting the tl, tdh, and trh genes and a novel PCR internal control. [Online.] http://www.cepheid.com/Sites/cepheid/litpdfs/vibrio_quantification.pdf.
56. Wagatsuma, S. 1968. A medium for the test of the hemolytic activity of Vibrio parahaemolyticus. Media Circle 13:159.
57. Weichart, D., and S. Kjelleberg. 1996. Stress resistance and recovery of culturable and viable but nonculturable cells of Vibrio vulnificus. Microbiology 142:845-853.
58. Wittwer, C. T., M. G. Hermann, C. N. Gundry, and K. S. Elenitoba-Johnson. 2001. Real-time multiplex PCR assays. Methods 25:430-442.
59. World Health Organization. 1999. Vibrio parahaemolyticus, Japan, 1996-1998. Wkly. Epidemiol. Rec. 74:357-364.
60. Xu, H., N. Roberts, F. Singleton, R. Atwell, D. Grimes, and R. R. Colwell. 1982. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. FEMS Microbiol. Ecol. 8:313-323.
61. Yamazaki, M., K. Inuzuka, M. Matsumoto, Y. Miwa, R. Hiramatsu, H. Matsui, K. Sakae, Y. Suzuki, and Y. Miyazaki. 2003. Epidemiological study of outbreaks and sporadic cases due to Vibrio parahaemolyticus-serotype O3:K6 in Aichi Prefecture, Japan, during 1988 and 2001. Kansenshogaku Zasshi 77:1015-1023.
62. Zangenberg, G., R. Saiki, and R. Reynolds. 1999. Multiplex PCR: optimization guidelines, p. 73-94. In M. A. Innis, D. H. Gelfand, and J. J. Sninsky (ed.), PCR applications: protocols for functional genomics. Academic Press, San Diego, CA.