A case-control analysis of traceback investigations for Vibrio parahaemolyticus infections (vibriosis) and pre-harvest environmental conditions in Washington State, 2013-2018

Benjamin J K Davis; Anne E Corrigan; Zhe Sun; Erika Atherly; Angelo DePaola; Frank C Curriero

doi:10.1016/j.scitotenv.2020.141650

A case-control analysis of traceback investigations for Vibrio parahaemolyticus infections (vibriosis) and pre-harvest environmental conditions in Washington State, 2013-2018

Sci Total Environ. 2021 Jan 15:752:141650. doi: 10.1016/j.scitotenv.2020.141650. Epub 2020 Aug 12.

Authors

Benjamin J K Davis¹, Anne E Corrigan², Zhe Sun³, Erika Atherly⁴, Angelo DePaola⁵, Frank C Curriero⁶

Affiliations

¹ Spatial Science for Public Health Center, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 627 N. Washington Street, Baltimore, MD 21205, USA; Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 615 N. Wolfe Street, Baltimore, MD 21205, USA; Center for Chemical Regulation and Food Safety, Exponent, Inc., 1105 Connective Avenue #1100, Washington, DC 20036, USA.
² Spatial Science for Public Health Center, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 627 N. Washington Street, Baltimore, MD 21205, USA; Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 615 N. Wolfe Street, Baltimore, MD 21205, USA.
³ Department of Environmental Health and Engineering, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 615 N. Wolfe Street, Baltimore, MD 21205, USA.
⁴ Office of Environmental Health & Safety, Division of Environmental Public Health, Washington State Department of Health, Olympia, WA, USA.
⁵ Angelo DePaola Consulting, Coden, AL, USA.
⁶ Spatial Science for Public Health Center, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 627 N. Washington Street, Baltimore, MD 21205, USA; Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 615 N. Wolfe Street, Baltimore, MD 21205, USA. Electronic address: fcurriero@jhu.edu.

Abstract

Background: Vibrio parahaemolyticus is a major cause of seafood-borne illness. It is naturally prevalent in brackish waters and accumulates in shellfish. Vibriosis cases are rising globally, likely due to rising temperatures.

Objectives: To identify associations between vibriosis in Washington State and pre-harvest environmental and V. parahaemolyticus genetic measurements sampled from shellfish.

Methods: Successful vibriosis traceback investigations were spatiotemporally matched to routine intertidal oyster (Crassostrea gigas) sampling events, which included measurements of temperature, salinity, and V. parahaemolyticus genetic targets (thermolabile hemolysin: tlh; thermostable direct hemolysin: tdh; thermostable direct-related hemolysin: trh). Unmatched sampling events were treated as controls. Associations were evaluated using logistic regression models.

Results: Systematic differences were observed across Washington harvesting zones. These included positive associations between the odds of vibriosis and all three genetic targets in South Puget Sound, with a large odds ratio (OR) = 13.0 (95% CI: 1.5, 115.0) for a 1-log₁₀ increase in tdh when total bacterium abundance was low (tlh < 1 log₁₀ MPN/g). A positive association also occurred for a 1 °C increase in tissue temperature OR = 1.20 (95% CI: 1.10, 1.30) while a negative association occurred for a similar increase in water temperature OR = 0.70 (95% CI: 0.59, 0.81). In contrast, the coastal bays displayed positive associations for water temperature OR = 2.16 (95% CI, 1.15, 4.05), and for a 1-log₁₀ increase in the tdh:trh ratio OR = 5.85 (95% CI, 1.06, 32.26).

Discussion: The zonal variation in associations indicates unique pathogenic strain prominence, suggesting tdh+/trh+ strains in South Puget Sound, such as the O4:K12 serotype, and tdh+/trh- strains in the coastal bays. The temperature discrepancy between water and oyster tissue suggests that South Puget Sound pathogenic strains flourish with exposure to relatively warm air during low tide. These findings identify new ecological risk factors for vibriosis in Washington State that can be used in future prevention efforts.

Keywords: Environmental epidemiology; Infectious diseases; Thermolabile hemolysin; Thermostable direct hemolysin; Thermostable direct-related hemolysin; Water temperature.

MeSH terms

Animals
Bacterial Proteins
Hemolysin Proteins
Shellfish
Vibrio Infections* / epidemiology
Vibrio parahaemolyticus*
Washington / epidemiology

Substances

Bacterial Proteins
Hemolysin Proteins

Grants and funding

R01 AI123931/AI/NIAID NIH HHS/United States