Vibrio parahaemolyticus, a notably lethal human pathogen derived from seafood: A review of its pathogenicity, characteristics, subspecies characterization, and molecular methods of detection

Food Biotechnology

Volumn 20, Issue 1, 2006, Pages 93-128

  Levin, Robert E ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Characteristics; Detection; Ecology; Hemolysins; Molecular typing; O3:K6 serotype; Pathogenicity; Review; Symptoms; Vibrio parahaemolyticus

Indexed keywords

ECOLOGY; FOOD PRODUCTS; GENES; PATHOLOGY;

CHARACTERISTICS; HEMOLYSINS; PATHOGENICITY; VIBRIO PARAHAEMOLYTICUS;

BACTERIA;

NEGIBACTERIA; VIBRIO; VIBRIO PARAHAEMOLYTICUS;

EID: 33645331293     PISSN: 08905436     EISSN: 15324249     Source Type: Journal    
DOI: 10.1080/08905430500524275     Document Type: Review

References (165)

1. Abbott, S., Powers, C., Kaysner, C., Takeda, Y., Ishibashi, M., Joseph, S., Ianda, J. (1989). Emergence of a restricted bioserovar of Vibrio parahaemolyticus as the predominant cause of Vibrio- associated gastroenteritis on the West Coast of the United States and Mexico. J. Clin. Microbiol. 27:2891-2893.
2. Allen, R., Baumann, P. (1971). Structure and arrangement of flagella in species of the genus Beneckea and Photobacterium fisheri. J. Bacteriol. 107:295-302.
3. Anderson, R., Ordal, E. (1972). Deoxyribonucleic acid relationships among marine vibrios. J. Bacteriol. 109:696-706.
4. Asakawa, Y., Akahane, S., Noguchi, M. (1974). Quantitative studies on pollution with Vibrio parahaemolyticus during distribution of fish. In: Fugino, T, Sakaguchi, G., Sakazaki, R., Takeda, Y., eds. International Symposium on Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., pp. 97-103.
5. Atsumi, T., McCarter, L., Imae, Y. (1992). Polar and lateral flagellar motors of marine Vibrio gare driven by different ion-motive forces. Nature 355:182-184.
6. Baba, K., Shirai, H., Terai, A., Takeda, Y., Nishibuchi, M. (1991). Analysis of the tdh gene cloned from a tdh gene- and trh gene-positive strains of Vibrio parahaemolyticus. Microbiol. Immunol. 35:253-258.
7. Bag, P., Nandi, S., Bhadra, R., Ramamurthy, T., Bhattacharya, S., Nishibuchi, M., Hamabata, T., Yamasaki, S., Takeda, Y., Nair, G. (1999). Clonal diversity among recently emerged strains of Vibrio parahaemolyticus O3: K6 associated with pandemic strains. J. Clin. Microbiol. 37:2354-2357.
8. Barker, W., Gangarosa, E. (1974). Food poisoning due to Vibrio parahaemolyticus. Ann. Rev. Med. 25:75-81.
9. Baross, J., Liston, J., Morita, R. (1978). Ecological relationship between Vibrio parahaemolyticus and agar-digesting vibrios as evidenced by bacteriophage susceptibility patterns. Appl. Environ. Microbiol. 36:500-505.
10. Barrow, G., Miller, D. (1974). Growth studies on Vibrio parahaemolyticus in relation to pathogenicity. In: Fugino, G., Sakaguchi, R., Sakazaki, Y., Takeda, eds. Int. Symp. Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., pp. 205-209.
11. Baumann, P., Baumann, L., Mandel, M. (1971). Taxonomy of marine bacteria: the genus Beneckea. J. Bacteriol. 107:268-294.
12. Bej, A., Patterson, D., Brasher, C., Vickery, M., Jones, D., Kaysner, C. (1999). Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh, and trh. J. Microbiol. Meth. 36:215-225.
13. Belas, R., Simon, M., Silverman, M. (1986). Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167:210-218.
14. Beuchat, L.R. (1973). Interacting effects of pH, temperature, and salt concentration on growth and survival of Vibrio parahaemolyticus. Appl. Microbiol. 25:844-846.
15. Beuchat, L. (1977). Evaluation of enrichment broths for enumerating Vibrio parahaemolyticus in chilled and frozen crab meat. J. Fd. Protect. 40 (9):592-595.
16. Bhuiyan, N., Ansurazzaman, M., Kmruzzaman, M., Alam, K., Chowdhury, N., Nishibuchi, M., Faruque, S., Sack, D., Takeda, Y., Nair, G. (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.
17. Blackstone, G., Nordstrom, J., Vickery, M., Bowen, M., Meyer, R., DePaola, A. (2003). Detection of pathogenic Vibrio parahaemolyticus in oyster enrichments by real time PCR. J. Microbiol. Meth. 53:149-155.
18. Bolen, J., Zamiska, A., Greenough, W. (1974). Clinical features in enteritis due to Vibrio parahaemolyticus. Amer. J. Med. 57:638-641.
19. Bonner, J., Coker, A., Berryman, C., Polock, H. (1983). Spectrum of Vibrio infections in a Gulf Coast community. Ann. Intern. Med. 99:464-469.
20. Boutin, B., Reyes, A., Peeler, J., Twedt, R. (1985). Effect of temperature and suspending vehicle on survival of Vibrio parahaemolytcus and Vibrio vulnificus. J. Fd. Protect. 48:875-878.
21. Bradshaw, J.G., Francis, D.W., Twedt, R.M. (1974). Survival of Vibrio parahaemolyticus in cooked seafood at refrigeration temperatures. Appl. Microbiol. 27:657-661.
22. Brasher, C., DePaola, A., Jones, D., Bej., A. (1998). Detection of microbial pathogens in shellfish with multiplex PCR. Current Microbiol. 37:101-107.
23. Burstyn, D.G., McNicol, L.A., Voll, M. J. (1980). Isolation and characterization of spontaneously arising auxotrophic and Kanagawa phenomenon-negative mutants of Vibrio parahaemolyticus. Infect. Immun. 27:889-896.
24. Cal, Y., Ni, Y. (1996). Purification, characterization, and pathogenicity of urease produced by Vibrio parahaemolyticus. J. Clin. Lab. Anal. 10:70-73.
25. Centers for Disease Control (1998). Outbreak of Vibrio parahaemolyticus infections associated with eating raw oysters and clams harvested from Long Island Sound-Connecticut, New Jersey, and New York, 1998. MMWR 48:48-51.
26. Chang, B., Taniguchi, H., Miyamoto, H., Yoshida, S. (1998). Filamentous bacteriophages of Vibrio parahaemolyticus as a possible clue to genetic transmission. J. Bacteriol 180:5094-5101.
27. Cherwongrodzky, J., Clark, A. (1981). Effect of pH on the production of the Kanagawa hemolysin by Vibrio parahaemolyticus. Infect. Immun. 34:115-119.
28. Chiou, C., Hsu, S., Chiu, S., Wang, S. T., Chao, C. (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.
29. Chitu, M., Cufedu, C., Nacescu, N. (1977). The isolation and characterization of some Vibrio parahaemolyticus strains isolated from salted herring and roe. Zbl. Bakt. Hyg. 1. Abt. Orig. A 238:59-65.
30. Chowdhury, N., Chakraborty, S., Ramamurthy, T., Nishibuchi, M., Yamasaki, S., Takeda, Y., Nair, G. (2000). Molecular evidence of clonal Vibrio parahaemolyticus pandemic strains. Emerg. Inf. Dis. 6:631-636.
31. Chun, D., Chung, J., Tak, R. (1974). Some observations on Kanagawa type hemolysis of Vibrio parahaemolyticus. In: Fujino, T., Sakaguchi, G., Sakazaki, R., Takeda, Y., eds. Int. Symp. Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., pp. 99-204.
32. Colwell, R.R. (1970). Polyphasic taxonomy of the genus Vibrio: numerical taxonomy of Vibrio cholerae, Vibrio parahaemolyticus, and related Vibrio species. J. Bacteriol. 104:410-433.
33. Covert, D., Woodburn, M. (1972). Relationships of temperature and sodium concentration to the survival of Vibrio parahaemoltyicus in broth and fish homogenate. Appl. Microbiol. 23:321-325.
34. Daniels, N., Ray, B., Easton, A., Maaranao, N., Kahn, E., McShan, A., Del Rosario, L., Baldwin, T., Kingsleyk, M., Puhr, N., Wells, J., Angulo, F. (2000). Emergence of a newVibrio parahaemolyticus serotype in raw oysers. J.A.M.A. 284:1541-1545.
35. DePaola, A., Kaysner, C., Bowers, J., Cook, D. (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.
36. DePaola, A., Nordstrom, J., Bowers, J., Wells, J., Cook, D. (2003a). Seasonal abundance of total and pathogenic Vibrio parahaemolyticus in Alabama oysters. Appl. Environ. Microbiol. 69:1521-1526.
37. DePaola, A., Ulaszek, J., Kaysner, C., Tenge, B., Nordstrom, J., Wells, J., Puhr, N., Gendel, S. (2003b). Molecular, serological, and virulence characteristics of Vibrio parahaemoltyicus isolated from environmental, food, and clinical sources in North America and Asia. Appl. Environ. Microbiol. 69:3999-4005.
38. Dileep, V., Kumar, H., Kumar, Y., Nishubichi, M., Karunasagar, I. (2003). Application of polymerase chain reaction for detection of Vibrio parahaemolyicus associated with tropical seafoods and coastal environment. Lett. Appl Microbiol. 36:423-427.
39. DiRita, V. (1992). Co-ordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol. Microbiol. 6:451-458.
40. Douet, J., Castroviejo, M., Dodin, A., Bebear, C. (1992). Purification and characterization of Kanagawa haemolysin from Vibrio parahaemolyticus. Res, Microbiol 143:569-577.
41. Elliot, E., Kaysner, C., Jackson, L., Tamplin, M. (1998). Chapter 9. Vibrio cholerae, V. parahaemolyticus, V. vulnificus, and other Vibrio spp. U.S.F.D.A. Bacteriological Analytical Manual. A.O.A.C. International. Gaithersburg, MD, U.S.A., 9.01-9.27.
42. Felsenfeld, O., Cabirac, H. B. (1977). A study of the ecology of Vibrio parahaemolyticus and Vibrio alginolyticus in Southeast Louisiana USA with special consideration of seafood consumption. J. Appl. Nutr. 29:17-28.
43. Fishbein, M., Wenz, B., Landry, W. L., MacFachern, B. (1974). Vibrio parahaemolyticus isolates in the U.S.: 1969-1972. In: Fujino, T., Sakaguchi, G., Sakazaki, R., Takeda, Y., eds. Int. Symp. Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., p. p53.
44. Fujino, T., Miwatani, T., Takeda, Y., Tomaru, A. (1969). A thermolabile direct hemolysin of Vibrio parahaemolyticus. Biken J. 12:145-148.
45. Fujino, T. (1951). Bacterial Food Poisoning. Saishin Igaku 6:263-271. In Japanese.
46. Fujino, T., Miwatani, T., Yasuda, J., Kondo, M., Takeda, Y., Akita, Y., Kotera, K., Okada, M., Nishimune, H., Shimizu, Y., Tamura, T., Tamura, Y. (1965). Taxonomic studies on the bacterial strains isolated from cases of "shirasu" food poisoning (Pasteurella parahaemolytica) and related organisms. Biken J. 8:63-71.
47. Fujino, T., Okuno, Y., Nakada, D., Aoyama, A., Fukai, K., Mukai, T., Ueho, T. (1953). On the bacteriological examination of shirasu food poisoning. Med. J. Osaka Univ. 4:299-304.
48. Fujino, T., Sakazaki, R., Tamura, K. (1974). Designation of the type strain of Vibrio parahaemolyticus and description of 200 strains of the species. Int. J. Syst. Bacteriol. 24:447-449.
49. Gendel, S., Ulaszek, J., Nishibuchi, M., DePaola, A. (2001). Automated ribotyping differentiates Vibrio parahaemolyticus O3:K6 strains associated with a Texas outbreak from other clinical strains. J. Food Prot. 64:1617-1620.
50. Ghosh, H., Bowen, T. (1980). Halophilic vibrios from human tissue infections on the Pacific coast of Australia. Pathology. 12:397-402.
51. Goatcher, L., Engler, S., Wagner, D., Westhoff, D. (1974). Effect of storage at 5 C on survival of Vibrio parahaemolyticus in procesed Maryland oysters. (Crassostrea virginica). J. Milk Food Technol. 37:74-77.
52. Hara-Kudo, Y., Sugiyama, K., Nishibuchi, M., Showdhury, A., Yatsuyanagi, J., Ohtomo, Y., Saito, A., Hidetoshi, N., Nishina, T., Nakagawa, H., Konuma, H., Miyara, M., Kumagail, S. (2003). Prevalence of pandemic thermostable direct hemolysin-producing Vibrio parahaemolyticus O3:K6 in seafood and the coastal environment of Japan. Appl. Environ. Microbol. 69:3883-3891.
53. Hollis, D., Weaver, R., Baker, C., Thornsberry, C. (1976). Halophilic Vibrio species isolated from blood cultures. J. Clin. Microbiol. 3:425-431.
54. Honda, T., Chearskul, S., Takeda, Y., Miwatani, T. (1980). Immunological methods for detection of Kanagawa phenomenon of Vibrio parahaemolyticus. J. Clin. Microbiol. 11 (6):600-603.
55. Honda, S., Goto, I., Minematsu, I., Ikeda, N., Ishibashi, M., Kinoshita, Y., Nishibuchi, M., Honda, T., Miwatani, T. (1987). Gastroenteritis due to Kanagawa negative Vibio parahaemolyticus. In: Lancet, i: 331-332.
56. Honda, T., Ni, Y., Miwatani, T. (1988). Purification and characterization of a hemolysin produced by a clinical isolate of Kanagawa phenomenon-negative Vibrio parahaemolyticus and related to the thermostable direct hemolysin. Infect. Immun. 56:961-965.
57. Honda, T., Abad-Lapuebla, M., Ni, Y., Yamamoto, K., Miwatani, T. (1991). Characterization of a new thermostable direct haemolysin produced by a Kanagawa-phenomenon-negative clinical isolate of vibrio parahaemolyticus. J. Gen. Microbiol. 137:253-259.
58. Horie, S., Okuzuma, M., Kato, N., Saito, K. (1966). Comparative observation on the range of growth temperature among three biotypes of Vibrio parahaemolyticus. Bull. Jap. Soc., Fish. 32:424-426.
59. Hugh, R., Sakazaki, R. (1972). Minimal number of characters for the identification of Vibrio species, Vibrio cholerae, and Vibrio parahaemolyticus. Conf. Public Health Lab. Directors. 30:133-137.
60. Hughes, J., Boyce, J., Alem, A., Wells, A., Rhaman, A., Curlin, G. (1978). Vibrio parahaemoltcus enterocolitis in Bangdladesh: Report of an outbreak. Amer. J. Trop. Med. Hyg. 27:106-112.
61. Iida, T., Hattori, A., Tagomori, K., Nasu, H., Naim, R., Honda, T. (2001). Filamentous phage associated with recent pandemic strains of Vibrio parahaemolyticus. Emerg. Infec. Dis. 7:477-478.
62. Iida, T., Yamamoato, K. (1990). Cloning and expression of two genes encoding highly homologous hemolysins from a Kanagawa-phenomenon-positive Vibrio parahaemolyticus T4750. Gene. 93:9-15.
63. Jackson, H. (1974). Temperature relationships of Vibrio parahaemolyticus. In: Fujino, T., G., Sakaguchi, R., Sakazaki, Y., Takeda, eds. International symposium on Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., pp. 139-145.
64. Jegathesan, M., Paramasivam, T. (1976). Hydrogen sulphide production as an aid to the identification of Vibrio parahaemolyticus. S.W. Asian J. of Trop. Med. and P. H. 7:377-379.
65. Joseph, S., Colwell, R., Kaper, J. (1982). Vibrioparahaemolyycus and related halophilic vibrios. Crit. Rev. In Microbiol. 10:77-124.
66. Jiang, X., Chai, T. (1996). Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. App. Environ. Microbiol. 62:1300-1305.
67. Johnson, H.C., Liston, J. (1973). Sensitivity of Vibrio parahaemolyticus to cold in oysters, fish fillets, and crab meat. J. Food Sci. 38:437-441.
68. Joseph, S.W., Colwell, R.R., Kaper, J.B. (1982). Vibrio parahaemolyticus and related halophilic vibrios. Crit. Revs. In Microbiol. 10:77-124.
69. Kaper, J., Campen, R., Seidler, R., Baldini, M., Falkow, S. (1984). Cloning of the thermostable direct hemolysin or Kanagawa phenomenon-associated hemolysin of Vibrio parahaemolyticus. Inf. Immun. 45:290-292.
70. Kaufman, G., Myers, M., Pass, C., Bej, A., Kaysner, C. (2002). Molecular analysis of Vibrio parahaemolyticus isolated from human patients and shellfish during US Pacific north-west outbreaks. Lett. Appl. Microbiol. 34:155-161.
71. Kelly, M., Stroh, E. (1989). Urease-positive, Kanagawa-negative Vibrio parahaemolyticus from patients and the environment in the Pacific Northwest. J. Clin. Microbiol. 27:2820-2822.
72. Khan, A., McCarthy, S., Wang, R., Cerniglia, C. (2002). Characterization of United States outbreak isolates of Vibria parahaemolyticus using enterobacterial repetitive intergenic consensus (ERIC) PCR and development of a rapid PCR method for detection of O3:K6 isolates. FEMS Microbiol. Lett. 206:209-214.
73. Kim, Y., Okuda, J., Matsumoto, C., Takahashi, N., Hashimoto, S., Nishibuchi, M. (1999). Identification of Vibrio parahaemolyticus strains at the species level by PCR targeted to the toxrR gene. J. Clin. Microbiol. 37:1173-1177.
74. Kimura, K., Tateiri, S., Iida, H. (1979). Effects of pH of the medium on flagellation of Vibrio parahaemolyticus. Appl. Environ. Microbiol. 37:1248-1249.
75. Kishishita, M., Matsuoka, N., Kumagai, K., Yamasaki, S., Takeda, Y., Nishibuchi, M. (1992). Sequence variation in the thermostable direct hemolysin-related hemolysin (trh) gene of Vibrio parahaemolyticus. Appl. Environ. Microbiol. 58:2449-2457.
76. Kita-Tsukamoto, K., Oyaizu, H., Namba, K., Shimidu, U. (1993). Phylogeneic relationships of marine bacteria, mainly members of the family Vibrionaceae, determined on the basis of 16S rRNA sequences. Int. J. Syst. Bacteriol. 43:8-19.
77. Kobayashi, T., Enomoto, S., Sakazaki, R., Kuwabaara, S. (1963). A new selective isolation medium for the Vibrio group (modified Nakanishi's medium - TCBS agar. Jap. J. Bacteriol. 18:387-392.
78. Lee, C., Cheng, M., Yu, M., Pan, M. (2002). Isolation and characterization of a putative virulence factor, serine protease, from vibrio parahaemolyticus. FEMS Microbiol. Lett. 209:31-37.
79. Lin, Z., Kumagai, K.K., Baba, K., Mekalanos, J., Nishibuchi, M. (1993). Vibrio parahaemolyticus has a homolog of the Vibrio cholerae toxRS operon that mediates environmentally induced regulation of the thermostable direct hemolysin gene. J. Bacteriol. 175:3844-3855.
80. Lozano-León, A., Tores, J., Osorio, C., Martinex-Urtaza, J. (2003). Identification of tdh-positive Vibrio parahaemolyticus from an outbreak associated with raw oyster consumption in Spain. FEMS Microbiology Letters 226:281-284.
81. Lu, B. (2003). The isolation, enumeration, biochemical and molecular identification of Vibrio vulnificus and Vibrio parahaemolyticus from shellfish. M.S. thesis University of Massachusetts, Amherst, MA.
82. Magalháes, M., Takeda, Y., Magalháes, V., Tateno, S. (1992). Brazilian urease-positive strains of Vibrio parahaemolyticus carry genetic potential to produce TDH-related hemolysin. Mem,. Inst. Oswaldo Cruz. 87:167-168.
83. Marshall, S., Clark, S.G., Wang, G., Mulvey, M., Kelly, M.T., Johnson, W.M. (1999). comparison of molecular methods for typing Vibrio parahaemolyticus. J. Clin. Microbiol. 37:2473-2478.
84. Matches, J.R., Liston, J., Daneault, L.P. (1971). Survival of Vibrio parahaemolyticus in fish homogenate during storage at low temperature. Appl. Microbiol. 21:951-952.
85. Matsumoto, C., Okuda, J., Ishibashi, M., Iwanaga, M., Garg, P., Rammamurthy, T., Wong, H., DePaola, A., Kim., Y., Albert, M., Nishibuchi, M. (2000). J. Clin. Microbiol. 38:578-585.
86. McCarter, I., Hilmen, M., Silverman, M. (1988). Flagellar dynamometer controls swarmer cell differentiation of Vibrio parahaemolyticus. Cell 54:345-351.
87. McCarthy, A., DePaola, A., Cook, D., Kaysner, C., Hill, W. (1999). Evaluation of alkaline phosphatase- and digoxigenin-labeled probes for detection of the thermolabile hemolysin (tlh) gene of Vibrio parahaemolyticus. Lett. Appl. Microbiol. 28:66-70.
88. McCarthy, S., DePaola, A., Kaysner, C., Hill, W., Cook, D. (2000). Evaluation of nonitotopic DNA hybridization methods for detection of the tdh gene of Vibrio parahaemolyticus. J. Food Prot. 63:1660-1664.
89. Myers, M., Panicker, G., Bej, A. (2003). PCR detection of a newly emerged pandemic Vibrio parahaemolyticus O3:K6 pathogen in pure cultures and seeded waters from the Gulf of Mexico. App. Environ. Microbiol. 69:2194-2200.
90. Miller, Y., Taylor, R., Mekalanos, J. (1987). Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48:271-279.
91. Misaki, H., Matsumoto, M. (1978). Purification of lysophospholipase of Vibrio parahaemolyticus and its properties. J. Biochem. 83:1395-1405.
92. Miwatani, T., Sakurai, J., Takeda, Y., and Shinoda, S. (1974). Studies on direct hemolysins of vibrio parahaemolyticus. In: International Symposium on Vibrio parahaemolyticus,
93. T., Miwatani, T. and Takeda, Y. (1976). Vibria parahaemolyticus - A Causative Bacterium of Food Poisoning. Saikon Publ. Co., Tokyo. 149 p.
94. Miwatani, T., Sakurai, J., Yoshihara, A., Takeda, Y. (1972). Isolation and partial purification of thermolabile direct hemolysin of Vibrio parahaemolyticus. Biken J. 15:61-66.
95. Miwatani, T., Takeda, Y. (1976). Vibrio parahaemolyticus - A Causative Bacterium of food Poisoning. Miwatani, T. and Takeda, Y. Eds. Saikon Publ. Co, Tokyo. 149 pp.
96. Miyamoto, Y., Obara, Y., Nikkawa, T., Yamai, S., Kato, T., Yamada, Y., Ohashi, M. (1980). Simplified purification and biophysicochemical characteristics of Kanagawa phenomenon-associated hemolysin of Vibrio parahaemolyticus. Inf. Immun. 28:567-576.
97. Miyamoto, Y., Kato, T., Obara, Y., Akiyama, S., Takizawa, K., Yamai, S. (1969). In vitro hemolytic characteristic of Vibrio parahaemolyticus: its close correlation with human pathogenicity. J. Bacteriol. 100:1147-1149.
98. Nakaguchi, Y., Okuda, J., Iida, T., Nishibuchi, M. (2003). The urease gene cluster of vibrio parahaemolyhticus does not influence the expression of the thermostable direct hemolysin gene or the TDH-related hemolysin gene. Microbiol. Immunol. 47:233-239.
99. Nakanishi, H., Iida, Y., Maeshima, K., Teramoto, T., Hosaka, Y., Ozaki, M. (1966). Isolation and properties of bacteriophages of Vibrio parahaemolyticus. Biken J. 9:149-157.
100. Nasu, H., Iida, T., Sugahara, T., Yamaichi, Y., Park, K., Yokoyama, K., Makino, H., Shinagawa, H., Honda, T. (2000). A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3:K6 strains. J. Clin. Microbiol. 38:2156-2161.
101. Nishibuchi, M., Fasano, A., Russell, R., Kaper, J. (1992). Enerotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect. Immun. 60:3539-3545.
102. Nishibuchi, M., Kaper, J.B. (1985). Nucleotide sequence of the thermostable direct hemolysin gene of Vibrio parahaemolyticus. J. Bacteriol. 162:558-564.
103. Nishibuchi, M., Kaper, J. (1990). Duplication and variation of the thermostable direct haemolytisin (tdh) gene in Vibrio parahaemoltyicus. Molec. Microbiol. 4:87-99.
104. Nishibuchi, M., Taniguchi, T., Misawa, T., Khaeomanee-Iam, V., Honda, T., Miwatani, T. (1989). Cloning and nucleotide sequence of the gene (trh) encoding the hemolysin related to the thermostable direct hemolysin of Vibrio parahaemoticus. Inf. Immun. 57:2691-2697.
105. Nishibuchi, M., Ishibashi, M., Takeda, Y., Kaper, J. (1985). Detection of the thermostable direct hemolysin gene and related DNA sequences in Vibrio parahaemolyticus and other Vibrio species by the DNA colony hybridization test. Inf. Immun. 49:481-486.
106. Obara, Y. (1971). Studies on hemolytic factors of Vibrio parahaemolyticus. II. The extraction, and its properties. J. Jap. Assoc. Infect. Dis. 45:392-398.
107. Ohashi, M., Ohta, K., Tsuno, M., Zen-Yoji, H. (1977). Development of a sensitive serological assay, reversed passive hemagglutination test, for detection of enteropathogenic toxin (Kanagawa hemolysin) of Vibrio parahaemolyticus, and re-evaluation of the toxin producibility of the isolates from various sources. Proc. 13th Joint Conf. Cholera, DEHW Publ No. (NIH) 78-1590, 403-413.
108. Okuda, J., Ishibashi, M., Abbott, I., Janda, J., Nishibuchi, M. (1997a). Analysis of the thermostable direct hemolysin (tdh) gene and the tdh- related hemolysin (trh) genes in the urease-positive strains of Vibrio parahaemolyticus isolated on the West Coast of the United States. J Clin. Microbol. 35:1965-1971.
109. Okuda, J., Ishibashi, Hayakawa, E., Nishino, T., Takeda, Y., Mukhopadhyay, A., Garg, S., Bhattacharya, S., Nair, G., Nishibuchi, M. (1997b). 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. 35:3150-3135.
110. Okuda, J., Nishibuchi, M. (1998). Manifestation of the Kanagawa phenomenon, the virulence-associated phenotype, of Vibrio parahaemolyicus depends on a particular single base change in the promoter of the thermostable direct hemolysin. Molec. Microbiol. 39:499-511.
111. Olsen, H. (1978). Vibrio parahaemolyticus isolated from discharge from the ear in two patients exposed to sea water. Acta Pathol. Microbiol. Scand. Sect. B 86:247-248.
112. Omori, G., Iwao, M., Iida, S., Kuroda, K. (1966). Studies on K antigen of Vibrio parahaemolyticus. I. Isolation and purification of K antigen from Vibrio parahaemolyticus A55 and some of its biological properties. Biken J. 9:33-43.
113. Osawa, R., Okitsu, T., Morozumi, H., Yamai, S. (1996). Occurrence of urease-positive Vibrio parahaemolyticus in Kanagawa, Japan, with specific reference to presence of thermostable direct hemolysin (TDH) and the TDH-related hemolysin genes. Appl. Environ. Microbiol. 62:725-727.
114. Ray, B., Hawkins, S., Hackney, C. (1978). Method for the detection of injured Vibrio parahaemolyticus in Seafoods. Appl. Environ. Microbiol. 35:1121-1127.
115. Roland, F. (1970). Leg gangrene and endotoxin sock due to Vibrio parahaemolyticus: an infection acquired in New England Coastal Waters. N. Engl. J. Med. 282:1306.
116. Ruimy, R., Breittmayer, V., Elbaze, P., Lafay, B., Boussemart, O., Gauthier, M., Christine, R. (1994). Phylogenetic analysis and assessment of the genera Vibrio, Photobacterium, Aeromonas, and Pleisiomonas deduced from small-subunit rRNA sequences. Int. J. Syst. Bacteriol. 44:416-426.
117. Sakai, S., Kudoh, Y., Zen-Yoji, H. (1974). Food poisoning caused by indole-negative strains of Vibrio parahaemolyticus in Tokyo. In: Fugino, T., Sakaguchi, G., Sakazaki, R., Takeda, Y., eds. International Symposium on Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., pp. 59-62.
118. Sakazaki, R., Iwanami, S., Fukumi, H. (1963). Studies on the enteropathogenic, facultatively halophilic bacteria, Vibrio parahaemolyticus. I. Morphological, cultural, and biochemical properties and its taxonomic position. Jap. J. M. Sc. & Biol. 16:161-188.
119. Sakazaki, R., Iwanami, S., Fukumi, H. (1968). Studies on the enteropathogenic, facultatively halophilic baceria, Vibrio parahaemolyticus. II. Serological characteristics. Jap. J. Med. Sci. Biol. 21:313-324.
120. Sakazaki, R., Tamura, K., Kato, T., Obara, Y., Yamai, S., Hobo, K. (1968). Studies on the enteropathogenic, facultatively halophilic bacterium Vibrio parahaemolyticus. III. Enteropathogenicity. Jap. J. Med. Sci. Biol. 21:325-331.
121. Sakazaki, R., Tamura, K., Nakamura, K., Kurata, T., Gohda, A., Kazuno, Y. (1974). Studies on enterophathogenic activity of Vibrio parahaemolyticus using ligated gut loop model in rabbits. Jap. J. Med. Sci. Biol. 27:35-43.
122. Sakurai, J., Matsuzaki, A., Miwatani, T. (1973). Purification and characterization of thermostable direct hemolysin of Vibrio parahaemolyticus. Infect. Immun. 8:775-780.
123. Sanyal, S.C., Sen, P.C. (1974). Human volunteer study on the pathogenicity of Vibrio parahaemolyticus. In: T.G., Sakaguchi, R., Sakazaki, Y., Takeda, eds. International symposium on Vibrio parahaemolyticus. Saikon Publ. Co.: Tokyo, pp. 227-230.
124. Schwartz, J.R., Colwell, R.R. (1974). Effect of hydrostatic pressure on growth and viability of Vibrio parahaemolyticus. Appl. Microbiol. 28:977-981.
125. Shewan, J., Véron, M. (1974). R. E., Buchanan, N.E., Gibbons, eds. Genus I. Vibrio Pacini 1854, 8th ed. of Bergy's Manual of Determinative Bacteriology. Baltimore, MD: The Williams and Wilkins co., p. 342.
126. Shinoda, S., Kariyama, R., Ogawa, M., Takeda, Y., Miwatani, T. (1976). Flagellar antigens of various species of the genus Vibrio and related genera. Int. J. Syst. Bacteriol. 26:97-101.
127. Shinoda, S., Honda, T., Takeda, Y., Miwatani, T. (1974). Antigenic difference between polar monotrichous and peritrichous flagella of Vibrio parahaemolyticus. J. Bacteriol. 120:923-928.
128. Shinoda, S., Nakahara, N., Nonomiya, Y., Itoh, K., Haruaki, K. (1983). Serological method for identification of Vibrio parahaemolyticus from marine sediments. Appl. Environ. Microbiol. 45:148-152.
129. Shirai, H., Ito, H., Hirayama, T., Nakabayashi, Y., Kumagai, K., Takeda, Y., Nishibuchi, M. (1990). Molecular epidemiological evidence for association of thermostable direct hemolysin (TDH) and TDH-related hemolysin of Vibrio parahaemolyticus with gastroenteritis. Infect. Immun. 58:3568-3573.
130. Sircar, B., Deb, B., De, S., Ghosh, A., Pal, S. (1976). Clinical and epidemiological studies on V. parahaemolyticus infection in Calcutta. Indian J. Med. Res. 64:1576-1580.
131. Steinkuller, P., Kelly, M., Sands, S., Barber, J. (1980). Vibrio parahaemolyticus endophthalmitis. J. Pediatr. Ophthalmol. Strabismus. 17:150-153.
132. Stewart, B., McCarter, L. (2003). Lateral flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 185:4508-4518.
133. Suthienkul, O., Ishibashi, M., Iida, T., Nettip, N., Supavej, S., Eampokalap, B., Makino, M., Honda, T. (1995). Urease production correlates with possession of the trh gene in Vibrio parahaemolyticus strains isolated in Thailand. J. Infect. Dis. 172:1405-1408.
134. Sutton, R.G. (1974). Some quantitative aspects of Vibrio parahaemolyticus in oysters inthe Sydney area. In: T, Fugino, G., Sakaguchi, R., Sakazaki, Y., Takeda, eds. International Symposium on Vibrio parahaemolyticus. Tokyo.: Saikon Publ. Co., pp. 71-76.
135. Tacket, C., Barret, T., Sanders, G., Blake, P. (1982). Panophthalmitis caused by Vibrio parahaemolyticus. J. Clin. Microbiol. 16:195-196.
136. Tada, J., Ohashi, T., Nishimura, N., Shirasaki, Y., Ozaki, H., Fukushima, S., Takano, J., Nishibuchi, M., Takeda, Y. (1992). Detection of the thermostable direct hemolysin gene (tdh) and the thermostable direct hemolysin-related gene (trh) of Vibrio parahaemolyticus by polymerase chain reaction. Mol. Cell Probes 6:477-487.
137. Takeda, Y., Thaga, S., Miwatani, T. (1978). Evidence that thermostable direct hemolysin of Vibrio parahaemoltyicus is composed of two subunits. FEMS Microbiol. Let. 4:271-274.
138. Takikawa, I. (1958). Studies on pathogenic halophilic bacteria. Yokohama M. Bull. 2:313-322.
139. Taniguchi, H., Hirano, H., Kubomura, S., Higashi, K., Misuguchi, Y. (1986). Comparison of the nucleotide sequences of the genes for the thermostable direct hemolysin and the thermolabile hemolysin from. Virbio parahaemolyticus. Microb. Path. 1:425-432.
140. Taniguchi, H., Sato, K., Ogawa, M., Udou, T., Mizuguchi, Y. (1984). Isolation and characterization of a filamentous phage, Vf33, specific for Vibrio parahaemolyticus. Microbiol. Immunol. 28:327-337.
141. Taniguchi, H., Ohta, H., Ogawa, M., Mizuguchi, Y. (1985). Cloning and expression in Escherichia coll of Vibrio parahaemolyticus themostable hemolysin and thermolabile hemolysin genes. J. Bacteriol. 162:510-515.
142. Temyo, R. (1966). Studies on the prevention of outbreaks of food poisoning caused by Vibri parahaemolyticus. Bull. Tokyo Med. Dent. Univ. 13:89-510.
143. Thompson, W., Thacker, C. (1973). Effect of temperature on vibrio parahaemolyticus in oysters at refrigerator and deep freeze temperatures. Can Inst. Food Sci. Technol. J. 6:156-158.
144. Thompson, C., Ja.Vanderzant, C., Ray, S. (1976). Serological and hemolytic characteristics of Vibrio parahaemolyticus from marine sources. J. Food Sci. 41:204-205.
145. Torii, M., An, T., Igarashi, K., Sakai, K., Kuroda, K. (1969). Immunochemical studies on O-antigens of Vibrio parahaemolyticus. 1. Preparation, specificity and chemical nature of the antigens. Biken J. 12:77-84.
146. Torii, M. (1974). Extraction and antigenic specificity of o-antigens of Vibrio parahaemolyticus. In: Fugino, T., Sakaguchi, G., Sakazaki, R., Takeda, Y., eds. International Symposium on Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., pp. 187-192.
147. Tsunasawa, S., Sugihara, A, Masaki, T., Sakiyama, T., Takeda, F., Miwatani, T., Narita, K. (1987). Amino acid sequence of thermosable direc hemolyhsin produced by Vibrio parahaemolyticus. J. Biochem. 101:111-121.
148. Twedt, R.M. (1989). Vibrio parahaemolyticus. In: M. P., Doyle, ed. Foodborne Bacterial pathogens. New York: Marcel Dekker, pp. 543-600.
149. Twedt, R.M., Spaulding, P.L., Hall, H.E. (1969). Morphological, cultural, biochemical, and serological comparison of Japanese strains of Vibrio parahaemoltyicus with related cultures isolated in the United States. J. Bacteriol. 98:511-518.
150. Vanderzant, C., Nickelson, R. (1972). Survival of Vibrio parahaemoyticus in shrimp tissue under varius environmental conditions. Appl. Microbiol. 23:34-37.
151. Vanderzant, C., Nickelson, R., Hazelwood, R.W. (1974). Effect of isolation-enumeration procedures on the recovery of normal and stressed cells of Vibrio parahaemolyticus. In: T, Fugino, G., Sakaguchi, R., Sakazaki, Y., Takeda, eds. International Symposium on Vibrio parahaemolyticus. Tokyo.: Saikon Publ. Co., pp. 111-116.
152. Venkateswaran, K., Dohmoto, N., Harayama, S. (1998). Cloning and nucleotide sequence of the gyrB gene of Vibrio parahaemolyticus and its application in detection of this pathogen in shrimp. Appl. Environ. Microbiol. 64:681-687.
153. Vuddhakul, V., Chowdbury, A, Laohaprertthisan, V., Pungrasamee, P., Patararungrong, N., Thianmonyri, P., Ishibasi, M., Matsumoto, C., Nishibuchi, M. (2000). Isolation of a pandemic O3:K6 clone of a Vibrio parahaemolyticus strain from environment and clinical sources in Thailand. Appl. Environ. Microbiol. 66:2685-2689.
154. Wagatsuma, S. (1968). On a medium for hemolytic reaction. Media Circle 13:159-162. (in Japanese).
155. Waldor, M., Mekalanos, J. (1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910-1914.
156. Wong, H., Liu, K., Pan, T., Lee, D., Shih, Y. (1996). Subspecies typing of Vibrio parahaemolyticus by pulsed-field gel electrophoresis. J. Clin. Microbiol. 34:1536-1539.
157. Wong, H., Liu, C., Pan, T., Wang, T., Lee, D., Shih, Y. (1999). Molecular typing of Vibrio parahaemolyticus isolates obtained form patients involved in food poisoning outbreaks in Taiwan by random amplified polymorphic DNA analysis. J. Clin. Microboil. 37:1809-1812.
158. Xu, M., Iida, T., Yamamoto, K., Takarada, Y., Miwatani, T., Honda, T. (1994). Demonstration and characterization of simultaneous production of a thermostable direct hemolysin ((TDHI) and a TDH-related hemolysin (TRHx) by a clinically isolated Vibrio parahaemolyticus strain, TH3766. Infect. Imun. 62:166-171.
159. Yabuuchi, E., Miwatani, T., Takeda, Y., Arita, M. (1974a). Flagellar morphology of Vibrio parahaemolyticus. In: Fujino, T., Sakaguchi, G., Sakazaki, R., Takeda, Y., eds. International Symposium on Vibrio parahaemolyticus. Tokyo: Saikon Publ Co., pp. 163-168.
160. Yabuuchi, E., Miwatani, T., Takeda, Y., Arita, M. (1974b). Flagellar morphology of Vibrio parahaemolyticus (Fujino et al.) Sakazaki, Iwanami and Fukumi (1963). Jap. J. Microbol. 18:295-305.
161. Yanagase, Y., Inoue, K., Ozaki, M., Ochi, T., Amano, T., Chazano, M. (1970). Hemolysins and related enzymes of vibrio parahaemoltycus. I. Identificaitn and partial purification of enzymes. Biken J. 13:77-92.
162. Yanagase, Y., Ozaki, M., Ochi, T., Amano, T. (1968). Lecithinase of Vibrio parahaemolyticus. Jap. J. Bacteriol. 23:35-36.
163. Yanagase, Y., Inoue, K., Ozaki, M., Ochi, T., Amano, T., Chazano, M. (1970). Hemolysin and related enzymes of Vibrio parahaemolyticus. I. Identification and partial purification of enzymes. Biken. J. 13:77-92.
164. Yoh, M., Honda, T., Miwatani, T., Nishibuchi, M. (1991). Characterization of thermostable direct hemolysins encoded by four representative tdh genes of Vibrio parahaemolyhticus. Microb. Pathog. 10:165-172.
165. Zen-Yoji, H., Kudoh, Y., Igarashi, H., Ohta, K., Fukai, K. (1974). Purification and identification of enteropathogenic toxins "a" and "a"' produced by Vibrio parahaemolyticus, and their biological and pathological activities. In: T, Fugino, G., Sakaguchi, R., Sakazaki, Y., Takeda, eds. International Symposium on Vibrio parahaemolyticus. Tokyo: Saikon Publ. Co., pp. 237-243.