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Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus

Incidence of vibriosis is rising globally, with evidence that changing climatic conditions are influencing environmental factors that enhance growth of pathogenic Vibrio spp. in aquatic ecosystems. To determine the impact of environmental factors on occurrence of pathogenic Vibrio spp., samples were...

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Autores principales: Brumfield, Kyle D., Chen, Arlene J., Gangwar, Mayank, Usmani, Moiz, Hasan, Nur A., Jutla, Antarpreet S., Huq, Anwar, Colwell, Rita R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10304686/
https://www.ncbi.nlm.nih.gov/pubmed/37222620
http://dx.doi.org/10.1128/aem.00307-23
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author Brumfield, Kyle D.
Chen, Arlene J.
Gangwar, Mayank
Usmani, Moiz
Hasan, Nur A.
Jutla, Antarpreet S.
Huq, Anwar
Colwell, Rita R.
author_facet Brumfield, Kyle D.
Chen, Arlene J.
Gangwar, Mayank
Usmani, Moiz
Hasan, Nur A.
Jutla, Antarpreet S.
Huq, Anwar
Colwell, Rita R.
author_sort Brumfield, Kyle D.
collection PubMed
description Incidence of vibriosis is rising globally, with evidence that changing climatic conditions are influencing environmental factors that enhance growth of pathogenic Vibrio spp. in aquatic ecosystems. To determine the impact of environmental factors on occurrence of pathogenic Vibrio spp., samples were collected in the Chesapeake Bay, Maryland, during 2009 to 2012 and 2019 to 2022. Genetic markers for Vibrio vulnificus (vvhA) and Vibrio parahaemolyticus (tlh, tdh, and trh) were enumerated by direct plating and DNA colony hybridization. Results confirmed seasonality and environmental parameters as predictors. Water temperature showed a linear correlation with vvhA and tlh, and two critical thresholds were observed, an initial increase in detectable numbers (>15°C) and a second increase when maximum counts were recorded (>25°C). Temperature and pathogenic V. parahaemolyticus (tdh and trh) were not strongly correlated; however, the evidence showed that these organisms persist in oyster and sediment at colder temperatures. Salinity (10 to 15 ppt), total chlorophyll a (5 to 25 μg/L), dissolved oxygen (5 to 10 mg/L), and pH (8) were associated with increased abundance of vvhA and tlh. Importantly, a long-term increase in Vibrio spp. numbers was observed in water samples between the two collection periods, specifically at Tangier Sound (lower bay), with the evidence suggesting an extended seasonality for these bacteria in the area. Notably, tlh showed a mean positive increase that was ca. 3-fold overall, with the most significant increase observed during the fall. In conclusion, vibriosis continues to be a risk in the Chesapeake Bay region. A predictive intelligence system to assist decision makers, with respect to climate and human health, is warranted. IMPORTANCE The genus Vibrio includes pathogenic species that are naturally occurring in marine and estuarine environments globally. Routine monitoring for Vibrio species and environmental parameters influencing their incidence is critical to provide a warning system for the public when the risk of infection is high. In this study, occurrence of Vibrio parahaemolyticus and Vibrio vulnificus, both potential human pathogens, in Chesapeake Bay water, oysters, and sediment samples collected over a 13-year period was analyzed. The results provide a confirmation of environmental predictors for these bacteria, notably temperature, salinity, and total chlorophyll a, and their seasonality of occurrence. New findings refine environmental parameter thresholds of culturable Vibrio species and document a long-term increase in Vibrio populations in the Chesapeake Bay. This study provides a valuable foundation for development of predicative risk intelligence models for Vibrio incidence during climate change.
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spelling pubmed-103046862023-06-29 Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus Brumfield, Kyle D. Chen, Arlene J. Gangwar, Mayank Usmani, Moiz Hasan, Nur A. Jutla, Antarpreet S. Huq, Anwar Colwell, Rita R. Appl Environ Microbiol Environmental Microbiology Incidence of vibriosis is rising globally, with evidence that changing climatic conditions are influencing environmental factors that enhance growth of pathogenic Vibrio spp. in aquatic ecosystems. To determine the impact of environmental factors on occurrence of pathogenic Vibrio spp., samples were collected in the Chesapeake Bay, Maryland, during 2009 to 2012 and 2019 to 2022. Genetic markers for Vibrio vulnificus (vvhA) and Vibrio parahaemolyticus (tlh, tdh, and trh) were enumerated by direct plating and DNA colony hybridization. Results confirmed seasonality and environmental parameters as predictors. Water temperature showed a linear correlation with vvhA and tlh, and two critical thresholds were observed, an initial increase in detectable numbers (>15°C) and a second increase when maximum counts were recorded (>25°C). Temperature and pathogenic V. parahaemolyticus (tdh and trh) were not strongly correlated; however, the evidence showed that these organisms persist in oyster and sediment at colder temperatures. Salinity (10 to 15 ppt), total chlorophyll a (5 to 25 μg/L), dissolved oxygen (5 to 10 mg/L), and pH (8) were associated with increased abundance of vvhA and tlh. Importantly, a long-term increase in Vibrio spp. numbers was observed in water samples between the two collection periods, specifically at Tangier Sound (lower bay), with the evidence suggesting an extended seasonality for these bacteria in the area. Notably, tlh showed a mean positive increase that was ca. 3-fold overall, with the most significant increase observed during the fall. In conclusion, vibriosis continues to be a risk in the Chesapeake Bay region. A predictive intelligence system to assist decision makers, with respect to climate and human health, is warranted. IMPORTANCE The genus Vibrio includes pathogenic species that are naturally occurring in marine and estuarine environments globally. Routine monitoring for Vibrio species and environmental parameters influencing their incidence is critical to provide a warning system for the public when the risk of infection is high. In this study, occurrence of Vibrio parahaemolyticus and Vibrio vulnificus, both potential human pathogens, in Chesapeake Bay water, oysters, and sediment samples collected over a 13-year period was analyzed. The results provide a confirmation of environmental predictors for these bacteria, notably temperature, salinity, and total chlorophyll a, and their seasonality of occurrence. New findings refine environmental parameter thresholds of culturable Vibrio species and document a long-term increase in Vibrio populations in the Chesapeake Bay. This study provides a valuable foundation for development of predicative risk intelligence models for Vibrio incidence during climate change. American Society for Microbiology 2023-05-24 /pmc/articles/PMC10304686/ /pubmed/37222620 http://dx.doi.org/10.1128/aem.00307-23 Text en Copyright © 2023 Brumfield et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Environmental Microbiology
Brumfield, Kyle D.
Chen, Arlene J.
Gangwar, Mayank
Usmani, Moiz
Hasan, Nur A.
Jutla, Antarpreet S.
Huq, Anwar
Colwell, Rita R.
Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus
title Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus
title_full Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus
title_fullStr Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus
title_full_unstemmed Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus
title_short Environmental Factors Influencing Occurrence of Vibrio parahaemolyticus and Vibrio vulnificus
title_sort environmental factors influencing occurrence of vibrio parahaemolyticus and vibrio vulnificus
topic Environmental Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10304686/
https://www.ncbi.nlm.nih.gov/pubmed/37222620
http://dx.doi.org/10.1128/aem.00307-23
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