Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern California

Shrimp is one of the most consumed seafood products globally. Antimicrobial drugs play an integral role in disease mitigation in aquaculture settings, but their prevalent use raises public health concerns on the emergence and spread of antimicrobial resistant microorganisms. Vibrio spp., as the most...

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Main Authors: Brady Hirshfeld, Kurtis Lavelle, Katie Yen Lee, Edward Robert Atwill, David Kiang, Bakytzhan Bolkenov, Megan Gaa, Zhirong Li, Alice Yu, Xunde Li, Xiang Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1192769/full
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author Brady Hirshfeld
Kurtis Lavelle
Katie Yen Lee
Katie Yen Lee
Edward Robert Atwill
David Kiang
Bakytzhan Bolkenov
Megan Gaa
Zhirong Li
Alice Yu
Xunde Li
Xunde Li
Xiang Yang
author_facet Brady Hirshfeld
Kurtis Lavelle
Katie Yen Lee
Katie Yen Lee
Edward Robert Atwill
David Kiang
Bakytzhan Bolkenov
Megan Gaa
Zhirong Li
Alice Yu
Xunde Li
Xunde Li
Xiang Yang
author_sort Brady Hirshfeld
collection DOAJ
description Shrimp is one of the most consumed seafood products globally. Antimicrobial drugs play an integral role in disease mitigation in aquaculture settings, but their prevalent use raises public health concerns on the emergence and spread of antimicrobial resistant microorganisms. Vibrio spp., as the most common causative agents of seafood-borne infections in humans, and Enterococcus spp., as an indicator organism, are focal bacteria of interest for the monitoring of antimicrobial resistance (AMR) in seafood. In this study, 400 samples of retail shrimp were collected from randomly selected grocery stores in the Greater Sacramento, California, area between September 2019 and June 2020. The prevalence of Vibrio spp. and Enterococcus spp. was 60.25% (241/400) and 89.75% (359/400), respectively. Subsamples of Vibrio (n = 110) and Enterococcus (n = 110) isolates were subjected to antimicrobial susceptibility testing (AST). Vibrio isolates had high phenotypic resistance to ampicillin (52/110, 47.27%) and cefoxitin (39/110, 35.45%). Enterococcus were most frequently resistant to lincomycin (106/110, 96.36%), quinupristin-dalfopristin (96/110, 87.27%), ciprofloxacin (93/110, 84.55%), linezolid (86/110, 78.18%), and erythromycin (58/110, 52.73%). For both Vibrio and Enterococcus, no significant associations were observed between multidrug resistance (MDR, resistance to ≥3 drug classes) in isolates from farm raised and wild caught shrimp (p > 0.05) and in isolates of domestic and imported origin (p > 0.05). Whole genome sequencing (WGS) of a subset of Vibrio isolates (n = 42) speciated isolates as primarily V. metschnikovii (24/42; 57.14%) and V. parahaemolyticus (12/42; 28.57%), and detected 27 unique antimicrobial resistance genes (ARGs) across these isolates, most commonly qnrVC6 (19.05%, 8/42), dfrA31 (11.90%, 5/42), dfrA6 (9.5%, 4/42), qnrVC1 (9.5%, 4/42). Additionally, WGS predicted phenotypic resistance in Vibrio isolates with an overall sensitivity of 11.54% and specificity of 96.05%. This study provides insights on the prevalence and distribution of AMR in Vibrio spp. and Enterococcus spp. from retail shrimp in California which are important for food safety and public health and exemplifies the value of surveillance in monitoring the spread of AMR and its genetic determinants.
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spelling doaj.art-64faac48cb06408e86fe2b125132c7872023-06-28T16:59:52ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-06-011410.3389/fmicb.2023.11927691192769Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern CaliforniaBrady Hirshfeld0Kurtis Lavelle1Katie Yen Lee2Katie Yen Lee3Edward Robert Atwill4David Kiang5Bakytzhan Bolkenov6Megan Gaa7Zhirong Li8Alice Yu9Xunde Li10Xunde Li11Xiang Yang12Department of Animal Science, University of California, Davis, Davis, CA, United StatesWestern Institute for Food Safety and Security, University of California, Davis, Davis, CA, United StatesWestern Institute for Food Safety and Security, University of California, Davis, Davis, CA, United StatesDepartment of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, Davis, CA, United StatesDepartment of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, Davis, CA, United StatesCalifornia Department of Public Health, Richmond, CA, United StatesDepartment of Animal Science, University of California, Davis, Davis, CA, United StatesWestern Institute for Food Safety and Security, University of California, Davis, Davis, CA, United StatesCalifornia Department of Public Health, Richmond, CA, United StatesCalifornia Department of Public Health, Richmond, CA, United StatesWestern Institute for Food Safety and Security, University of California, Davis, Davis, CA, United StatesDepartment of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, Davis, CA, United StatesDepartment of Animal Science, University of California, Davis, Davis, CA, United StatesShrimp is one of the most consumed seafood products globally. Antimicrobial drugs play an integral role in disease mitigation in aquaculture settings, but their prevalent use raises public health concerns on the emergence and spread of antimicrobial resistant microorganisms. Vibrio spp., as the most common causative agents of seafood-borne infections in humans, and Enterococcus spp., as an indicator organism, are focal bacteria of interest for the monitoring of antimicrobial resistance (AMR) in seafood. In this study, 400 samples of retail shrimp were collected from randomly selected grocery stores in the Greater Sacramento, California, area between September 2019 and June 2020. The prevalence of Vibrio spp. and Enterococcus spp. was 60.25% (241/400) and 89.75% (359/400), respectively. Subsamples of Vibrio (n = 110) and Enterococcus (n = 110) isolates were subjected to antimicrobial susceptibility testing (AST). Vibrio isolates had high phenotypic resistance to ampicillin (52/110, 47.27%) and cefoxitin (39/110, 35.45%). Enterococcus were most frequently resistant to lincomycin (106/110, 96.36%), quinupristin-dalfopristin (96/110, 87.27%), ciprofloxacin (93/110, 84.55%), linezolid (86/110, 78.18%), and erythromycin (58/110, 52.73%). For both Vibrio and Enterococcus, no significant associations were observed between multidrug resistance (MDR, resistance to ≥3 drug classes) in isolates from farm raised and wild caught shrimp (p > 0.05) and in isolates of domestic and imported origin (p > 0.05). Whole genome sequencing (WGS) of a subset of Vibrio isolates (n = 42) speciated isolates as primarily V. metschnikovii (24/42; 57.14%) and V. parahaemolyticus (12/42; 28.57%), and detected 27 unique antimicrobial resistance genes (ARGs) across these isolates, most commonly qnrVC6 (19.05%, 8/42), dfrA31 (11.90%, 5/42), dfrA6 (9.5%, 4/42), qnrVC1 (9.5%, 4/42). Additionally, WGS predicted phenotypic resistance in Vibrio isolates with an overall sensitivity of 11.54% and specificity of 96.05%. This study provides insights on the prevalence and distribution of AMR in Vibrio spp. and Enterococcus spp. from retail shrimp in California which are important for food safety and public health and exemplifies the value of surveillance in monitoring the spread of AMR and its genetic determinants.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1192769/fullVibrio spp.Enterococcus spp.foodborneshrimpantimicrobial resistancewhole genome sequencing
spellingShingle Brady Hirshfeld
Kurtis Lavelle
Katie Yen Lee
Katie Yen Lee
Edward Robert Atwill
David Kiang
Bakytzhan Bolkenov
Megan Gaa
Zhirong Li
Alice Yu
Xunde Li
Xunde Li
Xiang Yang
Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern California
Frontiers in Microbiology
Vibrio spp.
Enterococcus spp.
foodborne
shrimp
antimicrobial resistance
whole genome sequencing
title Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern California
title_full Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern California
title_fullStr Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern California
title_full_unstemmed Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern California
title_short Prevalence and antimicrobial resistance profiles of Vibrio spp. and Enterococcus spp. in retail shrimp in Northern California
title_sort prevalence and antimicrobial resistance profiles of vibrio spp and enterococcus spp in retail shrimp in northern california
topic Vibrio spp.
Enterococcus spp.
foodborne
shrimp
antimicrobial resistance
whole genome sequencing
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1192769/full
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