Multi-site Analysis Reveals Widespread Antibiotic Resistance in the Marine Pathogen Vibrio vulnificus
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Multi-site Analysis Reveals Widespread Antibiotic Resistance in the Marine Pathogen Vibrio vulnificus
Article in Microbial Ecology · January 2009
DOI: 10.1007/s00248-008-9413-8 · Source: PubMed
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Centre for Environment, Fisheries and Aqu…
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University of Georgia
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University of Georgia
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University of North Carolina at Charlotte
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ORIGINAL ARTICLE
Multi-site Analysis Reveals Widespread Antibiotic Resistance in the Marine Pathogen Vibrio vulnificus
Craig Baker-Austin & J. V. McArthur & Angela H. Lindell & Meredith S. Wright & R. Cary Tuckfield & Jan Gooch & Liza Warner & James Oliver & Ramunas Stepanauskas
Received: 10 December 2007 /Accepted: 21 May 2008 # Springer Science + Business Media, LLC 2008
Abstract Vibrio vulnificus is a serious opportunistic human pathogen commonly found in subtropical coastal waters, and is the leading cause of seafood-borne mortality in the USA. This taxon does not sustain prolonged presence in clinical or agricultural settings, where it would undergo human-induced selection for antibiotic resistance. There- fore, few studies have verified the effectiveness of commonly prescribed antibiotics in V. vulnificus treatment. Here we screened 151 coastal isolates and 10 primary
septicaemia isolates against 26 antimicrobial agents repre- senting diverse modes of action. The frequency of multiple resistances to antibiotics from all sources was unexpectedly high, particularly during summer months, and a substantial proportion of isolates (17.3%) were resistant to eight or more antimicrobial agents. Numerous isolates demonstrated resistance to antibiotics routinely prescribed for V. vulnifi- cus infections, such as doxycycline, tetracycline, amino- glycosides and cephalosporins. These resistances were detected at similar frequencies in virulent and non-virulent strains (PCR-based virulence typing) and were present in septicaemia isolates, underlying the public health implica- tions of our findings. Among environmental isolates, there were no consistent differences in the frequency of resis- tance between pristine and anthropogenically impacted estuaries, suggesting natural rather than human-derived sources of resistance traits. This report is the first to demonstrate prevalent antibiotic resistance in a human pathogen with no clinical reservoirs, implying the impor- tance of environmental studies in understanding the spread, evolution and public health relevance of antibiotic resis- tance factors.
Introduction
Bacteria of the genus Vibrio are commonly found in coastal and estuarine waters. Select strains of V. cholerae, V. parahaemolyticus, V. vulnificus and V. mimicus are consid- ered serious human pathogens, [44]. V. vulnificus causes food-borne diseases and wound infections. It carries the highest fatality rate of any food-borne pathogen in the US, often exceeding 50% [29, 30, 34], and 95% of all deaths resulting from seafood consumption in the US are caused by this bacterium [29]. About 85% of V. vulnificus infections
Microb Ecol DOI 10.1007/s00248-008-9413-8
Electronic supplementary material The online version of this article (doi:10.1007/s00248-008-9413-8) contains supplementary material, which is available to authorized users.
C. Baker-Austin : J. V. McArthur :A. H. Lindell :M. S. Wright Savannah River Ecology Laboratory, Drawer E, Aiken, SC, USA
R. C. Tuckfield Savannah River National Laboratory, Bldg. 773-42A, Aiken, SC, USA
J. Gooch National Oceanographic and Atmospheric Administration, Charleston, SC, USA
L. Warner : J. Oliver Department of Biology, University of North Carolina at Charlotte, Charlotte, NC, USA
R. Stepanauskas Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, ME, USA
C. Baker-Austin (*) Centre for Environment, Fisheries and Aquaculture Science, Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK e-mail: craig.baker-austin@cefas.co.uk
http://dx.doi.org/10.1007/s00248-008-9413-8
https://www.researchgate.net/publication/15363824_Infectious_diseases_associated_with_Molluscan_shellfish_consumption?el=1_x_8&enrichId=rgreq-63ba7b2b3fc6e57412c162cf75800213-XXX&enrichSource=Y292ZXJQYWdlOzUxNDE2MTE0O0FTOjMwMTg2MDExMDQzODQwMEAxNDQ4OTgwNDY2NDA0
https://www.researchgate.net/publication/7414979_Microarray-based_detection_of_genetic_heterogeneity_antimicrobial_resistance_and_the_viable_but_nonculturable_state_in_human_pathogenic_Vibrio_spp?el=1_x_8&enrichId=rgreq-63ba7b2b3fc6e57412c162cf75800213-XXX&enrichSource=Y292ZXJQYWdlOzUxNDE2MTE0O0FTOjMwMTg2MDExMDQzODQwMEAxNDQ4OTgwNDY2NDA0
occur between May and October, as this pathogen thrives in warm water (>20°C) [34]. With advances in refrigeration, seafood originating from habitats where V. vulnificus are most abundant may be consumed by at-risk individuals almost anywhere [43]. It is believed that a large number of V. vulnificus infections may go unreported (CDC estimates ~50% reported), which could greatly contribute to under- estimates of the morbidity and mortality burden associated with this pathogen.
V. vulnificus infections are characterised by an extremely short time-span between the onset of symptoms and subsequent clinical outcome, and immediate antibiotic therapy for suspected cases is considered critical. If treatment is delayed greater than 72 h, the fatality rate of primary septicaemia-associated V. vulnificus infections is 100% [20]. Interestingly, V. vulnificus is considered to have low levels of antibiotic resistance, and previous studies have shown sensitivity to tetracyclines, aminoglycosides, third- generation cephalosporins, chloramphenicol and newer fluoroquinolones [26, 41, 43]. Paradoxically, the two V. vulnificus strains CMCP6 and YJ016, for which genomes are publicly available, contain enzymatic-modification systems, active drug transporters and permeases suggestive of a genetic basis for antibiotic resistance. The significant morbidity and mortality associated with V. vulnificus infections, combined with the speed with which these infections progress and symptoms develop, underlie the need for a thorough analysis of the antibiotic resistance capabilities of this species.
The occurrence, diversity and public health implications of environmental antibiotic resistance have only recently been appreciated [2, 6, 16, 33, 42]. Considering the proliferation of antibiotic resistance in clinical settings [22], an understanding of the selective pressures maintain- ing environmental reservoirs of resistance may have a direct impact on the treatment of infectious diseases, particularly for pathogens that persist in the environment. Given the considerable spatial and temporal heterogeneity in the distribution of resistance and the complex factors that affect its evolution, dissemination and persistence, antibiotic resistance is being increasingly viewed as an ecological problem [36]. Addressing antibiotic resistance from an environmental standpoint can promote a better understand- ing of the ecology and evolution of antibiotic resistance, and may provide an early detection system for the development of antibiotic resistance mechanisms in clini- cally relevant bacteria [10]. For example, several recent reports have implicated the role of industrial contamination, and in particular metal contamination, as an indirect selective agent for antibiotic resistance [2, 24, 39, 40, 46].
Of the few studies that have addressed antibiotic resistance in this important human pathogen, most have involved only a few V. vulnificus isolates and relatively few
antimicrobials. Morris and Tenney [26] analysed the antibiotic resistance capabilities of 19 V. vulnificus strains against seven antimicrobial agents. Zanetti et al. [48] tested six V. vulnificus isolates taken from Italian coastal waters for sensitivity to 11 antimicrobials, while Ottaviani et al. [31] studied the resistance of eight environmental isolates to 27 antibiotics, including some antibiotics tested in this study. Thus, the aim of our study was to determine the antibiotic resistance capabilities across a much larger library of V. vulnificus strains (151 isolates) derived from three different estuarine environments and to determine the sensitivity of these isolates to a wide range of antimicrobial agents (26 drugs). Two of the sites analysed in this study are extensively contaminated with heavy metals (Shipyard Creek, Charleston, SC, USA and LCP Chemicals, Bruns- wick, GA, USA), whilst the reference site (the ACE Basin, Beaufort, SC, USA) is considered a pristine estuarine habitat. These habitats were chosen to assess the potential contribution of industrial contamination in driving environ- mental antibiotic resistance in this taxon. In addition, a small number of strains isolated from V. vulnificus- associated primary septicaemia clinical cases were also screened. Our results suggest that the diversity and level of antibiotic resistance in V. vulnificus is far greater than previously thought, with potentially significant clinical ramifications.
Materials and Methods
