Emergent Vibrio parahaemolyticus Gastroenteritis Outbreaks in New Zealand, 2019–2022: Trans-Pacific Spread of ST36 and Emergence of ST50
核心洞察
Four successive V. parahaemolyticus acute gastroenteritis outbreaks in New Zealand from 2019–2022 were linked to commercially supplied and wild-harvested shellfish, primarily green-lipped mussels.
The first outbreak marked the Trans-Pacific expansion of pandemic clone ST36 to Oceania, with isolates clustering closely with a Pacific Northwest/northeast USA lineage.
Two subsequent outbreaks revealed the emergence of pathogenic tdh+/trh+ ST50, which replaced ST36 predominance and was later detected in an Australian oysterborne outbreak.
A comprehensive genomic and epidemiologic investigation has revealed the emergence and rapid evolution of pathogenic Vibrio parahaemolyticus strains causing gastroenteritis outbreaks across New Zealand between 2019 and 2022, documenting the Trans-Pacific expansion of a pandemic clone and the rise of a previously uncommon sequence type in the region.
In response to a surge in clinical notifications in May 2019, multidisciplinary teams undertook four successive outbreak investigations involving enhanced epidemiologic investigation, establishment of national V. parahaemolyticus whole-genome sequencing capability, and extensive environmental investigations including food source traceback, testing of implicated seafoods, sea surface temperature measurements, and seafood supply chain inquiries.
During January 2019–May 2022, 136 of the 182 cases entered into the national notifiable disease database had viable V. parahaemolyticus isolates referred to the New Zealand Institute for Public Health and Forensic Science (搜索): 90 outbreak-related and 46 background isolates, the latter predominantly locally acquired (38 of 46) owing to COVID-19 border restrictions during the period. Four additional shellfish isolates were identified from outbreak-implicated mussel farms, sampled by the New Zealand Institute for Bioeconomy Science (搜索) and Ministry for Primary Industries (搜索) in 2020 and 2021.
Trans-Pacific Expansion of Pandemic Clone ST36
The first outbreak was caused by pandemic clone ST36, widely distributed to cases through commercially supplied New Zealand green-lipped mussels. This finding represented the Trans-Pacific expansion of tdh+/trh+ ST36 to Oceania, with New Zealand isolates clustering within fewer than 30–50 single-nucleotide polymorphisms (SNPs) of a Pacific Northwest/northeast USA lineage detected since 2007. An ST36 infection also occurred in April 2019 in a background case from a seafood area distinct from the winter outbreak source. The close clustering of this isolate with outbreak isolates — fewer than 5 SNPs — demonstrated ST36's high clonality and wide dispersal in New Zealand. Five closely related clinical isolates were later reported in Australia in 2021.
Emergence of ST50 and Replacement of ST36 Predominance
Two subsequent outbreaks in winter 2020 and summer 2021, also associated with commercially supplied mussels, marked the emergence of pathogenic tdh+/trh+ ST50 in New Zealand. Clinical and mussel-derived outbreak isolates were closely related to background ST50 infections associated with geographically dispersed seafood growing areas, suggesting a bloom of clonal ST50 in New Zealand's marine environment in 2020 that replaced pandemic ST36 predominance.
Internationally, ST50 is relatively uncommon, and New Zealand ST50 was genetically distinct from most international isolates, except those later emerging in an Australian oysterborne outbreak. Australia's 2021 samples formed a monophyletic group, with some closely related to New Zealand samples. However, investigators noted that these results are insufficient to demonstrate dispersal from New Zealand, as separate incursions from a common source may have occurred. Suspected mechanisms for the extensive global dispersal of related clones include the international shellfish trade and contaminated ballast from cargo ships, while environmental conditions associated with aquaculture may also promote the evolution of Vibrio spp. virulence.
Unusual Wintertime Outbreaks and Environmental Drivers
The occurrence of wintertime outbreaks is unusual when compared with similarly temperate areas overseas. Sea surface temperatures above 15°C, salinity, and rainfall can affect V. parahaemolyticus abundance and pathogenicity in seafood. Rising seawater temperatures in New Zealand may be contributing to recent trends in seafoodborne illness; sea surface temperatures recorded at mussel farms during winter outbreaks averaged 16.3°C in 2019 and 18°C in 2020.
Investigators also identified a third tdh+/trh+ V. parahaemolyticus type, ST199, isolated from cases who had consumed mussels associated with sea surface temperatures below 16°C, suggesting this strain may have pathogenic preponderance at lower temperatures. Another hypothesized contributor to winter outbreaks is consumption of raw New Zealand green-lipped mussels as a naturopathic arthritis remedy, though investigators did not collect information from cases regarding reasons for mussel consumption.
Summer Outbreaks and Environmental Amplification
Outbreaks 3 and 4 occurred during more typical summer months. Outbreak 4 showed diversity in both implicated seafood sources and V. parahaemolyticus strains, with cases becoming predominantly associated with self-collection of wild shellfish. ST50 from those outbreaks showed multiple distinct subclusters embedded within the wider diversity of historical clinical and environmental isolates. Outbreak 4 was likely driven by a surge of ST50 lineages already established across New Zealand, possibly triggered by an environmental amplification event. The summer of 2021–22 was New Zealand's fifth warmest recorded summer, with daily sea surface temperatures reaching 4°C–5°C above average.
Regulatory Response and Future Directions
The mix of pathogen-specific virulence and environmental factors contributing to the emergence of epidemic V. parahaemolyticus disease aligns with experiences reported in Peru associated with El Niño climatic events and arrivals of pandemic Vibrio spp. In that context, the expansion of monitoring of harvest sites could support the early detection of pathogenic V. parahaemolyticus events. In response to New Zealand's outbreaks, the Ministry for Primary Industries (搜索) amended national regulations for commercial shellfish growing areas. The findings also suggest the need for further research into New Zealand ST50's emergence and underscore the interconnected nature of international marine ecosystems and emerging infectious disease risks.