Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Gut Pathogens
Published in: Gut Pathogens 1/2018

Open Access 01-12-2018 | Research

Characterization of Salmonella enterica serovars recovered from meat products legally and illegally imported into the EU reveals the presence of multiresistant and AmpC-producing isolates

Authors: Anja Müller, Wiebke Jansen, Nils Th. Grabowski, Corinna Kehrenberg

Published in: Gut Pathogens | Issue 1/2018

Login to get access

Abstract

Background

Food products of animal origin brought into the EU from third countries, both legally and illegally, can harbor foodborne pathogens such as Salmonella enterica. In this study, we examined five S. enterica isolates recovered either from legally imported chicken meat (n = 3) or from meat products confiscated from air travel passengers arriving in Germany (n = 2). The isolates were serotyped and further characterized by antimicrobial susceptibility testing, PCR-detection and sequencing of genes associated with antimicrobial resistances, and macrorestriction analysis. Transferability of resistance to third-generation cephalosporins was assessed by conjugation experiments and the plasmids tested for their incompatibility groups.

Results

The three isolates from legal imports were identified as S. Heidelberg or as non-flagellated. All three isolates were identified as AmpC producers carrying blaCMY-2 and as non-susceptible to ciprofloxacin. They were additionally resistant to tetracycline and sulfamethoxazole. The blaCMY-2-carrying plasmids were transferable by conjugation and belonged to incompatibility groups IncI1 or IncA/C. The two isolates from illegally imported meat belonged to the serovars Infantis or Weltevreden. The former was phenotypically resistant to five classes of antimicrobial agents while the S. Weltevreden isolate was fully susceptible to all agents tested.

Conclusion

The results of this study demonstrate that meat products imported from third countries, both legally and illegally, can harbor multiresistant Salmonella enterica. Consequently, these imports could constitute a source for the dissemination of antimicrobial resistant isolates, including those resistant to third-generation cephalosporins and fluoroquinolones.
Literature
1.
European Food Safety Authority (EFSA) and the European Centre for Disease Prevention and Control (ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2016. EFSA J. 2017;15(12):e05077.
2.
Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatr Neonatol. 2013;54(3):147–52.CrossRef
3.
Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev. 2015;28(4):901–37.CrossRef
4.
Ramachandran G, Panda A, Higginson EE, Ateh E, Lipsky MM, Sen S, et al. Virulence of invasive Salmonella Typhimurium ST313 in animal models of infection. PLoS Negl Trop Dis. 2017;11(8):e0005697.CrossRef
5.
Foley SL, Nayak R, Hanning IB, Johnson TJ, Han J, Ricke SC. Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Appl Environ Microbiol. 2011;77(13):4273–9.CrossRef
6.
Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis: the role of poultry meat. Clin Microbiol Infect. 2016;22(2):110–21.CrossRef
7.
Liakopoulos A, Geurts Y, Dierikx CM, Brouwer MS, Kant A, Wit B, et al. Extended-spectrum cephalosporin-resistant Salmonella enterica serovar Heidelberg strains, the Netherlands. Emerg Infect Dis. 2016;22(7):1257–61.CrossRef
8.
Campos J, Mourão J, Silveira L, Saraiva M, Correia CB, Maçãs AP, et al. Imported poultry meat as a source of extended-spectrum cephalosporin-resistant CMY-2-producing Salmonella Heidelberg and Salmonella Minnesota in the European Union, 2014–2015. Int J Antimicrob Agents. 2017;51(1):151–4.CrossRef
9.
Jansen W, Merkle M, Daun A, Flor M, Grabowski NT, Klein G. The quantity and quality of illegally imported products of animal origin in personal consignments into the European Union seized at two German airports between 2010 and 2014. PLoS ONE. 2016;11(2):e0150023.CrossRef
10.
Müller A, Seinige D, Jansen W, Klein G, Ehricht R, Monecke S, et al. Variety of antimicrobial resistances and virulence factors in Staphylococcus aureus isolates from meat products legally and illegally introduced to Germany. PLoS ONE. 2016;11(12):e0167864.CrossRef
11.
Rodríguez-Lázaro D, Ariza-Miguel J, Diez-Valcarce M, Stessl B, Beutlich J, Fernandez-Natal I, et al. Identification and molecular characterization of pathogenic bacteria in foods confiscated from non-EU flights passengers at one Spanish airport. Int J Food Microbiol. 2014;209:20–5.CrossRef
12.
Beutlich J, Hammerl JA, Appel B, Nöckler K, Helmuth R, Jöst K, et al. Characterization of illegal food items and identification of foodborne pathogens brought into the European Union via two major German airports. Int J Food Microbiol. 2015;209:13–9.CrossRef
13.
Jansen W, Woudstra S, Müller A, Grabowski N, Schoo G, Gerulat B, et al. The safety and quality of pork and poultry meat imports for the common European market received at border inspection post Hamburg Harbour between 2014 and 2015. PLoS ONE. 2018;13(2):e0192550.CrossRef
14.
Miller T, Braun PG, Fehlhaber K, Prager R, Pfeifer Y, Rabsch W. Typing of Salmonella enterica serovar Infantis isolates from 51 outbreaks in Germany between 1974 and 2009 by a novel phage-typing scheme. Epidemiol Infect. 2014;142(1):75–83.PubMed
15.
Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, et al. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis. 2006;3(1):59–67.CrossRef
16.
Clinical and Laboratory Standards Institute (CLSI). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard—ninth edition CLSI document M07-A9. CLSI: Wayne; 2012.
17.
Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. Twenty-fourth informational supplement. CLSI document M100-S24. CLSI: Wayne; 2014.
18.
Prüller S, Rensch U, Meemken D, Kaspar H, Kopp PA, Klein G, et al. Antimicrobial susceptibility of Bordetella bronchiseptica isolates from swine and companion animals and detection of resistance genes. PLoS ONE. 2015;10(8):e0135703.CrossRef
19.
Dallenne C, Da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J Antimicrob Chemother. 2010;65(3):490–5.CrossRef
20.
Sandvang D, Aarestrup FM. Characterization of aminoglycoside resistance genes and class 1 integrons in porcine and bovine gentamicin-resistant Escherichia coli. Microb Drug Resist. 2000;6(1):19–27.CrossRef
21.
Kehrenberg C, Friederichs S, de Jong A, Michael GB, Schwarz S. Identification of the plasmid-borne quinolone resistance gene qnrS in Salmonella enterica serovar Infantis. J Antimicrob Chemother. 2006;58(1):18–22.CrossRef
22.
Vredenburg J, Varela AR, Hasan B, Bertilsson S, Olsen B, Narciso-da-Rocha C, et al. Quinolone-resistant Escherichia coli isolated from birds of prey in Portugal are genetically distinct from those isolated from water environments and gulls in Portugal, Spain and Sweden. Environ Microbiol. 2014;16(4):995–1004.CrossRef
23.
Arcangioli MA, Leroy-Sétrin S, Martel JL, Chaslus-Dancla E. A new chloramphenicol and florfenicol resistance gene flanked by two integron structures in Salmonella typhimurium DT104. FEMS Microbiol Lett. 1999;174(2):327–32.CrossRef
24.
Kadlec K, Kehrenberg C, Schwarz S. Molecular basis of resistance to trimethoprim, chloramphenicol and sulphonamides in Bordetella bronchiseptica. J Antimicrob Chemother. 2005;56(3):485–90.CrossRef
25.
Senda K, Arakawa Y, Ichiyama S, Nakashima K, Ito H, Ohsuka S, et al. PCR detection of metallo-beta-lactamase gene (bla IMP) in Gram-negative rods resistant to broad-spectrum β-lactams. J Clin Microbiol. 1996;34(12):2909–13.PubMedPubMedCentral
26.
O’Regan E, Quinn T, Pagès JM, McCusker M, Piddock L, Fanning S. Multiple regulatory pathways associated with high-level ciprofloxacin and multidrug resistance in Salmonella enterica serovar Enteritidis: involvement of ramA and other global regulators. Antimicrob Agents Chemother. 2009;53(3):1080–7.CrossRef
27.
28.
Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods. 2005;63(3):219–28.CrossRef
29.
Kayser FH, Morenzoni G, Homberger F. Activity of cefoperazone against ampicillin-resistant bacteria in agar and broth dilution tests. Antimicrob Agents Chemother. 1982;22(1):15–22.CrossRef
30.
Doumith M, Day MJ, Hope R, Wain J, Woodford N. Improved multiplex PCR strategy for rapid assignment of the four major Escherichia coli phylogenetic groups. J Clin Microbiol. 2012;50(9):3108–10.CrossRef
31.
Kehrenberg C, Schwarz S. Occurrence and linkage of genes coding for resistance to sulfonamides, streptomycin and chloramphenicol in bacteria of the genera Pasteurella and Mannheimia. FEMS Microbiol Lett. 2001;205(2):283–90.CrossRef
32.
McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature. 2001;413(6858):852–6.CrossRef
33.
Schwarz S, Silley P, Simjee S, Woodford N, van Duijkeren E, Johnson AP, et al. Assessing the antimicrobial susceptibility of bacteria obtained from animals. Vet Microbiol. 2010;141(1–2):1–4.CrossRef
34.
35.
Dominguez SA, Schaffner DW. Survival of Salmonella in processed chicken products during frozen storage. J Food Prot. 2009;72(10):2088–92.CrossRef
36.
37.
Khan AS, Georges K, Rahaman S, Abdela W, Adesiyun AA. Prevalence and serotypes of Salmonella spp. on chickens sold at retail outlets in Trinidad. PLoS ONE. 2018;13(8):e0202108.CrossRef
38.
Domingues AR, Vieira AR, Hendriksen RS, Pulsrikarn C, Aarestrup FM. Spatio-temporal analysis of Salmonella surveillance data in Thailand. Epidemiol Infect. 2014;142(8):1614–24.CrossRef
39.
Lettini AA, Vo Than T, Marafin E, Longo A, Antonello K, Zavagnin P, et al. Distribution of Salmonella serovars and antimicrobial susceptibility from poultry and swine farms in central Vietnam. Zoonoses Public Health. 2016;63(7):569–76.CrossRef
40.
Li B, Yang X, Tan H, Ke B, He D, Wang H, et al. Whole genome sequencing analysis of Salmonella enterica serovar Weltevreden isolated from human stool and contaminated food samples collected from the southern coastal area of China. Int J Food Microbiol. 2018;266:317–23.CrossRef
41.
Makendi C, Page AJ, Wren BW, Le Thi Phuong T, Clare S, Hale C, et al. A phylogenetic and phenotypic analysis of Salmonella enterica serovar Weltevreden, an emerging agent of diarrheal disease in tropical regions. PLoS Negl Trop Dis. 2016;10(2):e0004446.CrossRef
42.
Hindermann D, Gopinath G, Chase H, Negrete F, Althaus D, Zurfluh K, et al. Salmonella enterica serovar Infantis from food and human infections, Switzerland, 2010–2015: poultry-related multidrug resistant clones and an emerging ESBL producing clonal lineage. Front Microbiol. 2017;8:1322.CrossRef
43.
Haiko J, Westerlund-Wikström B. The role of the bacterial flagellum in adhesion and virulence. Biology (Basel). 2013;2(4):1242–67.PubMedPubMedCentral
44.
Lockman HA, Curtiss R. Salmonella typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect Immun. 1990;58(1):137–43.PubMedPubMedCentral
45.
RKI. Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für, Infectious disease epidemiology annual report for 2016. Berlin: Robert Koch-Institut; 2016. p. 2017.
46.
47.
Edirmanasinghe R, Finley R, Parmley EJ, Avery BP, Carson C, Bekal S, et al. A whole-genome sequencing approach to study cefoxitin-resistant Salmonella enterica serovar Heidelberg isolates from various sources. Antimicrob Agents Chemother. 2017;61(4):e01919.CrossRef
48.
Voss-Rech D, Vaz CS, Alves L, Coldebella A, Leão JA, Rodrigues DP, et al. A temporal study of Salmonella enterica serotypes from broiler farms in Brazil. Poult Sci. 2015;94(3):433–41.CrossRef
49.
50.
Commission European. Commission Regulation (EU) N° 1086/2011 of 27 October 2011 amending Annex II to Regulation (EC) N° 2160/2003 of the European Parliament and of the Council and Annex I to Commission Regulation (EC) N° 2073/2005 as regards Salmonella in fresh poultry meat. Off J Eur Union L. 2011;281:7–11.
51.
European Centre for Disease Prevention and Control (ECDC), European Food Safety Authority (EFSA), European Medicines Agency (EMA), Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR). Joint opinion on antimicrobial resistance (AMR) focused on zoonotic infections. EFSA J. 2009;7(11):1372.CrossRef
52.
Rodríguez I, Barownick W, Helmuth R, Mendoza MC, Rodicio MR, Schroeter A, et al. Extended-spectrum β-lactamases and AmpC β-lactamases in ceftiofur-resistant Salmonella enterica isolates from food and livestock obtained in Germany during 2003-07. J Antimicrob Chemother. 2009;64(2):301–9.CrossRef
53.
European Food Safety Authority (EFSA) and the European Centre for Disease Prevention and Control (ECDC). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2015. EFSA J. 2017;15(2):e04694.
54.
Mataseje LF, Baudry PJ, Zhanel GG, Morck DW, Read RR, Louie M, et al. Comparison of CMY-2 plasmids isolated from human, animal, and environmental Escherichia coli and Salmonella spp. from Canada. Diagn Microbiol Infect Dis. 2010;67(4):387–91.CrossRef
Metadata
Title
Characterization of Salmonella enterica serovars recovered from meat products legally and illegally imported into the EU reveals the presence of multiresistant and AmpC-producing isolates
Authors
Anja Müller
Wiebke Jansen
Nils Th. Grabowski
Corinna Kehrenberg
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2018
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-018-0268-3

Other articles of this Issue 1/2018

Gut Pathogens 1/2018 Go to the issue

Review

Involvement of gut microbiome in human health and disease: brief overview, knowledge gaps and research opportunities

Review

Antibiotic resistance, the 3As and the road ahead

Research

Determination of virulence and fitness genes associated with the pheU, pheV and selC integration sites of LEE-negative food-borne Shiga toxin-producing Escherichia coli strains

Short Report

A hybrid reference-guided de novo assembly approach for generating Cyclospora mitochondrion genomes

Research

N-Acetyl-glucosamine influences the biofilm formation of Escherichia coli

Case Report

Takayasu’s arteritis associated with eosinophilic gastroenteritis, possibly via the overactivation of Th17
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits