Characteristics of a sharp decrease in Vibrio parahaemolyticus infections and seafood contamination in Japan
Introduction
Vibrio parahaemolyticus is a halophilic bacterium and a major foodborne pathogen. The first V. parahaemolyticus outbreak in Japan, in 1950, was associated with semidried sardines. Strains carrying the tdh gene, which encodes the thermostable direct hemolysin (TDH); the trh gene, which encodes the TDH-related hemolysin (TRH); or both genes are considered virulent strains (Nishibuchi and Kaper, 1995). A new clone, the O3:K6 strain, which carries the tdh but not the trh gene, was responsible for a pandemic that was widespread over regions of Asia (Bag et al., 1999, Chiou et al., 2000, National Institute of Infectious Diseases and Tuberculosis and Infectious Diseases Control Division, Ministry of Health, Labour and Welfare, 1999, Vuddhakul et al., 2000, Wong et al., 2000), North America (Gendel et al., 2001), South America (González-Escalona et al., 2005), and Europe (Martinez-Urtaza et al., 2005, Ottaviani et al., 2008) beginning in 1996. The pandemic clone complex consisted of a number of serotypes such as O4:K68, O1:K25 and O1:KUT (Nair et al., 2007). V. parahaemolyticus has been a dominant cause of foodborne infections in Japan since the 1960s and the infections occurred constantly (Fig. 1, this figure was prepared from data published in the annual Handbook of Health and Welfare Statistics from the Ministry of Health, Labour and Welfare in Japan). Surveillance in a prefecture started in 1963 reported that the major serotypes were O2:K3, O3:K7, O4:K8, O4:K12, O5:K15 and O4:K63, and other serotypes accounted for more than half of the infections for 22 years (Akahane et al., 1984). However, proportion of serotype O3:K6 rapidly increased from 1996, and serotype O3:K6 was the most major serotype from 1997 to 1999 (Fig. 2, this figure was prepared from the reports of Infectious Disease Surveillance Center, National Institute of Infectious Diseases in Japan). The increase was coincident a large wave of infections involving V. parahaemolyticus from 1997 in Japan (Fig. 1). The number of cases per year doubled (12,318 cases) and that of outbreaks per year tripled (839 outbreaks) to a peak in 1998 compared with outbreaks in 1996 (Fig. 1). However, the numbers of cases and outbreaks of V. parahaemolyticus infections decreased 40-fold and 60-fold, respectively, from 1998 to 2009 (Fig. 1). Such an enormous decrease has never been previously recorded for V. parahaemolyticus infections.
In 1999 and 2000, the Japanese Ministry of Health, Labour, and Welfare (MHLW) advised seafood handlers to use disinfected or artificial seawater or potable water to process shellfish and finfish. The maximum temperature for seafood during distribution and storage was set at ≤ 10 °C and recommended to be ≤ 4 °C. The microbiological standards of V. parahaemolyticus levels in seafood were set at < 100 most probable number per gram (MPN/g) and non-detectable levels per 25 g for raw consumption and ready-to-eat boiled seafood, respectively. It was also advised for consumers to consume seafood within 2 h after taking seafood from the refrigerator. Although these hygienic control measures were the first regulations to control the cooling down of boiled seafood with hygienic water and temperature for storage, and limit V. parahaemolyticus contamination level, the contributions of hygienic control measures on seafood are unknown.
To delineate the characteristics of the V. parahaemolyticus infection epidemic and the changes in the pathogen's incidence in seafood in Japan during the drastic decrease of infections, we analysed serotypes and genotypes of V. parahaemolyticus isolated from outbreaks and seafood. We also investigated the frequencies and levels of total V. parahaemolyticus and tdh-positive V. parahaemolyticus in seafood collected from wholesale markets in 2007–2009 in Japan and compared these values with those reported in 2001 (Hara-Kudo et al., 2003).
Section snippets
Information on V. parahaemolyticus outbreaks
Questionnaire on V. parahaemolyticus outbreaks spanning 1998 to 2007; date of occurrence, place of occurrence, number of cases, implicated food, and information of V. parahaemolyticus isolates (serotype and tdh and/or trh genes harboring), was sent from the National Institute of Health Sciences to 30 prefectures/cities in Japan. The answers were sent to the National Institute of Health Sciences. Information on V. parahaemolyticus serotypes from 977 outbreaks was collected. When different
V. parahaemolyticus serotype in outbreaks
The data that we collected since 1998 on V. parahaemolyticus serotypes involved in outbreaks identified serotype O3:K6 in almost 50% of the total outbreaks during each year (Fig. 3). Serotypes O1:K25, O1:K56, O4:K8, and O4:K68 were relatively dominant presences among more than 60 types of serotypes. However, various serotypes were associated with the outbreaks, and there was a decrease in the number of outbreaks independent of the serotype.
Analysis of total and tdh-positive V. parahaemolyticus in seafood
V. parahaemolyticus was detected in 717 of 842 samples
Discussion
V. parahaemolyticus infections in Japan rapidly increased from 1997 to 1998 and then decreased through to 2009. The surge was linked to increased incidences of the pandemic O3:K6 strain, which has spread worldwide since 1996. From the results of GS-PCR and PFGE analyses, it was demonstrated that serotype O3:K6 pandemic strains isolated from bloody clams imported from Korea in 2009 and patients in 2005, 2007 and 2009 are of the same type as O3:K6 strains isolated from seafood and patients in
Acknowledgements
This research was supported by a grant from the Ministry of Health, Labour and Welfare, Japan. We are grateful to the Infectious Disease Surveillance Center, National Institute of Infectious Diseases for providing information on V. parahaemolyticus serotype. We appreciate the following governments in prefectures; Okinawa, Kagoshima, Saga, Oita, Fukuoka, Hiroshima, Gunma, Toyama, Ishikawa, Fukui, Gifu, Aichi, Tokyo Metropolitan, Chiba, Fukushima, Miyagi, Iwate, Aomori and Hokkaido, and in
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