Distribution and dissemination of antimicrobial-resistant  Salmonella  in broiler farms with or without enrofloxacin use

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Abstract

Background

Salmonella is a major zoonotic food-borne pathogen that persists on poultry farms, and animals undergo reinfection with endemic strains. The present study aimed to investigate the characteristics and dissemination of antimicrobial-resistant Salmonella within and between broiler farms that used enrofloxacin and those that did not.

Results

Cloacal and environmental (litter, feed, and water) samples from two selected flocks in each of 12 farms owned by the same company were collected three times over a 30-day period of two production cycles during 2015–2016. The rate of Salmonella isolation was 7.8% (123/1584). Nine Salmonella serotypes (116 isolates) and seven untypable isolates were identified, and Salmonella Montevideo was the most prevalent serotype. Azithromycin-resistant (17.9%) and colistin-resistant (3.3%) isolates were detected, and multidrug-resistant isolates (43.1%) were also observed. No isolate was resistant to enrofloxacin or ciprofloxacin; however, intermediate resistance to enrofloxacin was significantly higher ( P < 0.05) in farms that used enrofloxacin than in those that did not. The rate of multi-drug resistance among litter isolates (25/44, 56.8%) was significantly higher ( P < 0.05) than that among cloacal swab (24/67, 35.8%) and feed (4/12, 33.3%) isolates. Pulsed-field gel electrophoresis (PFGE) analysis of strains of the same serotype was conducted to determine their epidemiological relationship. The PFGE types were classified into 31 groups with a 100% correlation cutoff in dendrograms for Salmonella Montevideo isolates, which showed 100% genomic identity based on age, sample type, flock, and production cycle within and between farms.

Conclusion

The present study highlights the occurrence of horizontal transmission and cyclic contamination with antimicrobial-resistant Salmonella in broiler farms owned by the same company. Litter may be a good indicator of indoor environmental contamination with antimicrobial-resistant Salmonella on farms. Additionally, enrofloxacin use may be one of the factors promoting resistance towards it in Salmonella.

Electronic supplementary material

The online version of this article (10.1186/s12917-018-1590-1) contains supplementary material, which is available to authorized users.

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Most cited references 51

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The global burden of nontyphoidal Salmonella gastroenteritis.

Shannon Majowicz, Jennie Musto, Elaine Scallan … (2010)

To estimate the global burden of nontyphoidal Salmonella gastroenteritis, we synthesized existing data from laboratory-based surveillance and special studies, with a hierarchical preference to (1) prospective population-based studies, (2) "multiplier studies," (3) disease notifications, (4) returning traveler data, and (5) extrapolation. We applied incidence estimates to population projections for the 21 Global Burden of Disease regions to calculate regional numbers of cases, which were summed to provide a global number of cases. Uncertainty calculations were performed using Monte Carlo simulation. We estimated that 93.8 million cases (5th to 95th percentile, 61.8-131.6 million) of gastroenteritis due to Salmonella species occur globally each year, with 155,000 deaths (5th to 95th percentile, 39,000-303,000 deaths). Of these, we estimated 80.3 million cases were foodborne. Salmonella infection represents a considerable burden in both developing and developed countries. Efforts to reduce transmission of salmonellae by food and other routes must be implemented on a global scale.

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Population dynamics and antimicrobial resistance of the most prevalent poultry-associated Salmonella serotypes.

Devendra Shah, Narayan C. Paul, Willium Sischo … (2016)

Salmonella spp. is the most predominant bacterial cause of foodborne gastroenteritis in humans. Due to the risk of human infection associated with poultry products and the prevalence of antimicrobial resistance, Salmonella also poses a significant challenge to commercial poultry production. During the last decade (2002 to 2012), the 12 most prevalent poultry-associated Salmonella serotypes (MPPSTs) were frequently and consistently isolated from poultry products in the United States. These MPPSTs and their percent prevalence in poultry products include Kentucky (4%), Enteritidis (2%) Heidelberg (2%), Typhimurium (2%), S. I 4,[5],12:i:- (0.31%), Montevideo (0.20%), Infantis (0.16%) Schwarzengrund (0.15%), Hadar (0.15%), Mbandaka (0.13%), Thompson (0.12%), and Senftenberg (0.04%). All MPPSTs except Kentucky are among the top 30 clinically significant serotypes that cause human illnesses in the United States. However with the exception of a few widely studied serotypes such as S. Enteritidis and Typhimurium, the ecology and epidemiology of the majority of MPPSTs still remain poorly investigated. Published data from the United States suggests that MPPSTs such as Heidelberg, Typhimurium, Kentucky, and Sentfenberg are more likely to be multi-drug resistant (MDR, ≥3 antimicobial classes) whereas Enteritidis, Montevideo, Schwarzengrund, Hadar, Infantis, Thompson, and Mbandaka are generally pan-susceptible or display resistance to fewer antimicobials. In contrast, the majority of MPPSTs isolated globally have been reported to display MDR phenotype. There also appears to be an international spread of a few MDR serotypes including Kentucky, Schwarzengrund, Hadar, Thomson, Sentfenberg, and Enteritidis, which may pose significant challenges to the public health. The current knowledge gaps on the ecology, epidemiology, and antimicrobial resistance of MPPSTs are discussed.

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What do we know about resistance to colistin in Enterobacteriaceae in avian and pig production in Europe?

Isabelle Kempf, Mickaël Alain Fleury, Djamel Drider … (2013)

Colistin is a cyclic decapeptide bound to a fatty acid chain. It is active against many Gram-negative bacteria by destabilising the bacterial outer membrane. Bacteria can become resistant to colistin by modification of their lipopolysaccharide, thereby reducing the affinity of polymyxins. Colistin is often administered orally in poultry and pig production to control colibacillosis. Resistant isolates are sometimes recovered from pathological cases, particularly in piglets. However, in Europe the percentage of resistance to colistin in Escherichia coli strains isolated from the digestive tract microbiota of healthy animals remains <1%. Copyright © 2013 Elsevier B.V. and the International Society of Chemotherapy. All rights reserved.

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Author and article information

Contributors

Ke Shang: shangke0624@gmail.com

Bai Wei: weibai116@hotmail.com

Min Kang:

ORCID: http://orcid.org/0000-0001-5650-1144

vet.minkang@gmail.com

Journal

Journal ID (nlm-ta): BMC Vet Res

Journal ID (iso-abbrev): BMC Vet. Res

Title: BMC Veterinary Research

Publisher: BioMed Central (London )

ISSN (Electronic): 1746-6148

Publication date (Electronic): 30 August 2018

Publication date PMC-release: 30 August 2018

Publication date Collection: 2018

Volume: 14

Electronic Location Identifier: 257

Affiliations

ISNI 0000 0004 0470 4320, GRID grid.411545.0, Department of Veterinary Infectious Diseases and Avian Diseases, College of Veterinary Medicine and Center for Poultry Diseases Control, , Chonbuk National University, ; 79 Gobong-ro, Iksan, 54596 South Korea

Author information

Min Kang http://orcid.org/0000-0001-5650-1144

Article

Publisher ID: 1590

DOI: 10.1186/s12917-018-1590-1

PMC ID: 6117923

PubMed ID: 30165845

SO-VID: a896c1fc-6e99-4715-be17-4c4a7aff7ac5

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 2 February 2018

Date accepted : 21 August 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003668, Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries;

Award ID: 716002-7, 315035-5

Award Recipient : Min Kang

Funded by: Research of animal and plant Quarantine agency

Award ID: Z-1543073-2015-16-01

Award Recipient : Min Kang

Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;

Award ID: 2017R1D1A1B03030883

Award Recipient : Min Kang

Custom metadata

ScienceOpen disciplines: Veterinary medicine

Keywords: salmonella,antimicrobial resistance,circulating contamination,enrofloxacin,broiler farm,litter,pfge

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ScienceOpen disciplines: Veterinary medicine

Keywords: salmonella, antimicrobial resistance, circulating contamination, enrofloxacin, broiler farm, litter, pfge

Distribution and dissemination of antimicrobial-resistant Salmonella in broiler farms with or without enrofloxacin use

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Most cited references 51

The global burden of nontyphoidal Salmonella gastroenteritis.

Population dynamics and antimicrobial resistance of the most prevalent poultry-associated Salmonella serotypes.

What do we know about resistance to colistin in Enterobacteriaceae in avian and pig production in Europe?

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