Occurrence and Multidrug Resistance of Campylobacter in Chicken Meat from Different Production Systems
Abstract
:1. Introduction
2. Material and Methods
2.1. Sample Collection
2.2. Detection and Enumeration of Campylobacter spp.
2.3. Confirmation of Campylobacter Species
2.4. Subtyping by Pulse-Field Gel Electrophoresis (PFGE)
2.5. Antimicrobial Susceptibility Testing
3. Results
3.1. Occurrence of Campylobacter spp. among Chicken Samples Derived from Different Production Systems
3.2. PFGE Analysis
3.3. Antimicrobial Susceptibility Patterns
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- European Food Safety Authority; European Centre for Disease Prevention and Control. The European Union One Health 2020 Zoonoses Report. EFSA J. 2021, 19, e06971. [Google Scholar] [CrossRef]
- Kaakoush, N.O.; Castaño-Rodríguez, N.; Mitchell, H.M.; Man, S.M. Global Epidemiology of Campylobacter Infection. Clin. Microbiol. Rev. 2015, 28, 687–720. [Google Scholar] [CrossRef][Green Version]
- Fitzgerald, C. Campylobacter. Clin. Lab. Med. 2015, 35, 289–298. [Google Scholar] [CrossRef]
- Silva, J.; Leite, D.; Fernandes, M.; Mena, C.; Gibbs, P.A.; Teixeira, P. Campylobacter spp. as a Foodborne Pathogen: A Review. Front. Microbiol. 2011, 2, 200. [Google Scholar] [CrossRef][Green Version]
- Bolinger, H.; Kathariou, S. The Current State of Macrolide Resistance in Campylobacter spp.: Trends and Impacts of Resistance Mechanisms. Appl. Environ. Microbiol. 2017, 83, e00416-17. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Sproston, E.L.; Wimalarathna, H.M.L.; Sheppard, S.K. Trends in Fluoroquinolone Resistance in Campylobacter. Microb. Genom. 2018, 4, e000198. [Google Scholar] [CrossRef] [PubMed]
- Pitkänen, T. Review of Campylobacter spp. in Drinking and Environmental Waters. J. Microbiol. Methods 2013, 95, 39–47. [Google Scholar] [CrossRef] [PubMed]
- Heuvelink, A.E.; van Heerwaarden, C.; Zwartkruis-Nahuis, A.; Tilburg, J.J.H.C.; Bos, M.H.; Heilmann, F.G.C.; Hofhuis, A.; Hoekstra, T.; Boer, E. Two Outbreaks of Campylobacteriosis Associated with the Consumption of Raw Cows’ Milk. Int. J. Food Microbiol. 2009, 134, 70–74. [Google Scholar] [CrossRef] [PubMed]
- Hakeem, M.J.; Lu, X. Survival and Control of Campylobacter in Poultry Production environment. Front. Cell. Infect. Microbiol. 2021, 10, 615049. [Google Scholar] [CrossRef]
- Hwang, H.; Singer, R.S. Survey of the U.S. Broiler Industry regarding Pre- and Postharvest Interventions Targeted to Mitigate Campylobacter Contamination on Broiler Chicken Products. J. Food Prot. 2020, 83, 1137–1148. [Google Scholar] [CrossRef]
- Commission Regulation (EC). No 2073/2005 of 15 November 2005 on Microbiological Criteria for Foodstuffs. Available online: https://www.fsai.ie/uploadedFiles/Reg2073_2005(1).pdf (accessed on 16 May 2022).
- Myintzaw, P.; Jaiswal, A.K.; Jaiswal, S. A Review on Campylobacteriosis Associated with Poultry Meat Consumption. Food Rev. Int. 2022, 1, 1–15. [Google Scholar] [CrossRef]
- Myintzaw, P.; Moran, F.; Jaiswal, A.K. Campylobacteriosis, Consumer’s Risk Perception, and Knowledge Associated with Domestic Poultry Handling in Ireland. J. Food Saf. 2020, 40, e12799. [Google Scholar] [CrossRef]
- ISO 10272-2:2017; Microbiology of the Food Chain—Horizontal Method for Detection and Enumeration of Campylobacter spp.—Part 2: Colony-Count Technique. International Organisation for Standardisation (ISO): Geneva, Switzerland, 2017.
- ISO 10272-1:2017; Microbiology of the Food Chain—Horizontal Method for Detection and Enumeration of Campylobacter spp.—Part 1: Detection Method. International Organisation for Standardisation (ISO): Geneva, Switzerland, 2017.
- Wang, G.; Clark, C.G.; Taylor, T.M.; Pucknell, C.; Barton, C.; Price, L.; Woodward, D.L.; Rodgers, F.G. Colony Multiplex PCR Assay for Identification and Differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J. Clin. Microbiol. 2002, 40, 4744–4747. [Google Scholar] [CrossRef] [PubMed][Green Version]
- CDC. Centers for Disease Control and Prevention, PulseNet. Standard Operating Procedure for PulseNet PFGE of Campylobacter jejuni. PNL03 Last Updated July. Available online: https://www.cdc.gov/pulsenet/pdf/campylobacter-pfge-protocol-508c.pdf (accessed on 28 March 2022).
- Magiorakos, A.P.; Srinivasan, A.; Carey, R.B.; Carmeli, Y.; Falagas, M.E.; Giske, C.G.; Harbarth, S.; Hindler, J.F.; Kahlmeter, G.; Olsson-Liljequist, B.; et al. Multidrug-Resistant, Extensively Drug-Resistant and Pandrug-Resistant Bacteria: An International Expert Proposal for Interim Standard Definitions for Acquired Resistance. Clin. Microbiol. Infect. 2012, 18, 268–281. [Google Scholar] [CrossRef] [PubMed][Green Version]
- World Health Organization. Prioritization of Pathogens to Guide Discovery, research and Development of New Antibiotics for Drug-Resistant Bacterial Infections, Including Tuberculosis; World Health Organization: Geneva, Switzerland, 2017; reference number WHO/EMP/IAU/2017.12.
- Lynch, C.T.; Lynch, H.; Egan, J.; Whyte, P.; Bolton, D.; Coffey, A.; Lucey, B. Antimicrobial Resistance of Campylobacter Isolates Recovered from Broilers in the Republic of Ireland in 2017 and 2018: An Update. Br. Poult. Sci. 2020, 61, 550–556. [Google Scholar] [CrossRef]
- Zhang, X.; Yin, T.; Du, X.; Yang, W.; Huang, J.; Jiao, X. Occurrence and Genotypes of Campylobacter Species in Broilers During the Rearing Period. Avian Pathol. 2017, 46, 215–223. [Google Scholar] [CrossRef][Green Version]
- Jore, S.; Viljugrein, H.; Brun, E.; Heier, B.T.; Borck, B.; Ethelberg, S.; Hakkinen, M.; Kuusi, M.; Reiersen, J.; Hansson, I.; et al. Trends in Campylobacter Incidence in Broilers and Humans in Six European Countries, 1997–2007. Prev. Vet. Med. 2010, 93, 33–41. [Google Scholar] [CrossRef]
- Carreira, A.C.; Clemente, L.; Rocha, T.; Tavares, A.; Geraldes, M.; Barahona, M.J.; Botelho, A.; Cunha, M.V. Comparative Genotypic and Antimicrobial Susceptibility Analysis of Zoonotic Campylobacter Species Isolated from Broilers in a Nationwide Survey, Portugal. J. Food Protect. 2012, 75, 2100–2109. [Google Scholar] [CrossRef]
- Mendes, Â.J.; Ferreira, N.; Costa, F.M.; Lopes, E.P.; da Silva, J.F.; Inácio, .; Moreira, F.A.; da Costa, P.M. External Contamination of Broilers by Campylobacter spp. Increases from the Farm to the Slaughterhouse. Br. Poult. Sci. 2020, 61, 550–556. [Google Scholar] [CrossRef]
- Golden, C.E.; Mishra, A. Prevalence of Salmonella and Campylobacter spp. in Alternative and Conventionally Produced Chicken in the United States: A Systematic Review and Meta-Analysis. J. Food Protect. 2020, 83, 1181–1197. [Google Scholar] [CrossRef]
- Kassem, I.I.; Kehinde, O.; Kumar, A.; Rajashekara, G. Antimicrobial-Resistant Campylobacter in Organically and Conventionally Raised Layer Chickens. Foodborne Pathog. Dis. 2017, 14, 29–34. [Google Scholar] [CrossRef]
- Martínez Michel, L.; Anders, S.; Wismer, W.V. Consumer Preferences and Willingness to Pay for Value-Added Chicken Product Attributes. J. Food Sci. 2011, 76, S469–S477. [Google Scholar] [CrossRef] [PubMed]
- Da Rosa, P.P.; Ávila, B.P.; Angelo, I.D.V.; Chesini, R.G.; Fernandes, T.A.; da Silva Camacho, J.; Bugoni, M.; Buttow Roll, V.F.; Gularte, M.A. Impact of Different Chicken Meat Production Systems on Consumers’ Purchase Perception. Br. Poult. Sci. 2021, 62, 387–395. [Google Scholar] [CrossRef] [PubMed]
- Sofos, J.N. Challenges to Meat Safety in the 21st Century. Meat Sci. 2008, 78, 3–13. [Google Scholar] [CrossRef] [PubMed]
- Smith-spangler, C.; Brandeau, M.L.; Hunter, G.E.; Clay Bavinger, J.; Pearson, M.; Eschbach, P.J.; Sundaram, V.; Liu, H.; Schirmer, P.; Stave, C.; et al. Are Organic Foods Safer or Healthier Than Conventional Alternatives? Ann. Intern. Med. 2012, 157, 680. [Google Scholar] [CrossRef][Green Version]
- Hegde, N.V.; Kariyawasam, S.; DebRoy, C. Comparison of Antimicrobial Resistant Genes in Chicken Gut Microbiome Grown on Organic and Conventional Diet. Vet. Anim. Sci. 2016, 1–2, 9–14. [Google Scholar] [CrossRef][Green Version]
- Anderson, J.; Horn, B.J.; Gilpin, B.J. The prevalence and genetic diversity of Campylobacter spp. in domestic ‘backyard’poultry in Canterbury, New Zealand. Zoonoses Public Health 2012, 59, 52–60. [Google Scholar] [CrossRef]
- Keerthirathne, T.P.; Ross, K.; Fallowfield, H.; Whiley, H. Examination of Australian backyard poultry for Salmonella, Campylobacter and Shigella spp., and related risk factors. Zoonoses Public Health 2022, 69, 13–22. [Google Scholar] [CrossRef]
- Moore, J.E.; Corcoran, D.; Dooley, J.S.G.; Fanning, S.; Lucey, B.; Matsuda, M.; McDowell, D.A.; Mégraud, F.; Millar, C.; O’Mahony, R.; et al. Campylobacter. Vet. Res. 2005, 36, 351–382. [Google Scholar] [CrossRef][Green Version]
- Sheppard, S.K.; Maiden, M.C.J. The Evolution of Campylobacter jejuni and Campylobacter coli. Cold Spring Harb. Perspect. Biol. 2015, 7, a018119. [Google Scholar] [CrossRef][Green Version]
- Gilpin, B.; Cornelius, A.; Robson, B.; Boxall, N.; Ferguson, A.; Nicol, C.; Henderson, T. Application of Pulsed-Field Gel Electrophoresis to Identify Potential Outbreaks of Campylobacteriosis in New Zealand. J. Clin. Microbiol. 2006, 44, 406–412. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Oyarzabal, O.A.; Backert, S.; Williams, L.L.; Lastovica, A.J.; Miller, R.S.; Pierce, S.J.; Vieira, S.L.; Rebollo-Carrato, F. Molecular Typing, Serotyping and Cytotoxicity Testing of Campylobacter jejuni Strains Isolated from Commercial Broilers in Puerto Rico. J. Appl. Microbiol. 2008, 105, 800–812. [Google Scholar] [CrossRef]
- Cardoso, M.J.; Ferreira, V.; Truninger, M.; Maia, R.; Teixeira, P. Cross-contamination Events of Campylobacter spp. in Domestic Kitchens Associated with Consumer Handling Practices of Raw Poultry. Int. J. Food Microbiol. 2021, 338, 108984. [Google Scholar] [CrossRef] [PubMed]
- Bull, S.A.; Allen, V.M.; Domingue, G.; Jorgensen, F.; Frost, J.A.; Ure, R.; Whyte, R.; Tinker, D.; Corry, J.E.L.; Gillard-King, J.; et al. Sources of Campylobacter spp. Colonizing Housed Broiler Flocks During Rearing. Appl. Environ. Microbiol. 2006, 72, 645–652. [Google Scholar] [CrossRef][Green Version]
- Hein, I.; Schneck, C.; Knogler, M.; Feierl, G.; Plesss, P.; Kofer, J.; Achmann, R.; Wagner, M. Campylobacter jejuni Isolated from Poultry and Humans in Styria, Austria: Epidemiology and Ciprofloxacin Resistance. Epidemiol. Infect. 2003, 130, 377–386. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Schiaffino, F.; Platts-Mills, J.; Kosek, M.N. A One Health Approach to Prevention, Treatment, and Control of Campylobacteriosis. Curr. Opin. Infect. Dis. 2019, 32, 453–460. [Google Scholar] [CrossRef]
- Dai, L.; Sahin, O.; Grover, M.; Zhang, Q. New and Alternative Strategies for the Prevention, Control, and Treatment of Antibiotic-Resistant Campylobacter. Trans. Res. 2020, 223, 76–88. [Google Scholar] [CrossRef]
- Wieczorek, K.; Wolkowicz, T.; Osek, J. Antimicrobial Resistance and Virulence-Associated Traits of Campylobacter jejuni Isolated from Poultry Food Chain and Humans with Diarrhea. Front. Microbiol. 2018, 9, 1508. [Google Scholar] [CrossRef] [PubMed]
- Iglesias-Torrens, Y.; Miró, E.; Guirado, P.; .Llovet, T.; Muñoz, C.; Cerdà-Cuéllar, M.; Madrid, C.; Balsalobre, C.; Navarro, F. Population Structure, Antimicrobial Resistance, and Virulence-Associated Genes in Campylobacter jejuni Isolated from Three Ecological Niches: Gastroenteritis Patients, Broilers, and Wild Birds. Front. Microbiol. 2018, 9, 1676. [Google Scholar] [CrossRef][Green Version]
- Schets, F.M.; Jacobs-Reitsma, W.F.; Van Der Plaats, R.Q.J.; Heer, L.K.-D.; Van Hoek, A.H.A.M.; Hamidjaja, R.A.; Husman, A.M.D.R.; Blaak, H. Prevalence and Types of Campylobacter on Poultry Farms and in Their Direct Environment. J. Water Health 2017, 15, 849–862. [Google Scholar] [CrossRef][Green Version]
- Duarte, A.; Santos, A.; Manageiro, V.; Martins, A.; Fraqueza, M.J.; Caniça, M.; Domingues, F.C.; Oleastro, M. Human, Food and Animal Campylobacter spp. Isolated in Portugal: High Genetic Diversity and Antibiotic Resistance Rates. Int. J. Antimicrob. Agents 2014, 44, 306–313. [Google Scholar] [CrossRef] [PubMed]
Production-System | Shopping Place | Producer | Sample Code | Detection (in 10 g) | Enumeration (CFU/g) | Species Identification |
---|---|---|---|---|---|---|
Free-range | Supermarket chain A | P1 | C2 | Absent | 3.0 × 102 | C. jejuni and C. coli |
Supermarket chain A | P2 | GC1 | Present | 6.0 × 102 | C. jejuni | |
Supermarket chain A | P2 | GC2 | Absent | 1.0 × 103 | C. jejuni and C. coli | |
Supermarket chain B | P3 | GC3 | Present | <10 | C. coli | |
Supermarket chain C | P4 | GC4 | Present | 8.10 × 102 | C. coli | |
Supermarket chain C | P5 | GC5 | Present | 2.0 × 102 | C. jejuni and C. coli | |
Supermarket chain A | P5 | GC6 | Present | 1.0 × 102 | C. jejuni and C. coli | |
Butcher shop D | Unknown | GC7 | Present | <10 | C. coli | |
Butcher shop F | Unknown | GC8 | Present | 1.0 × 102 | C. jejuni and C. coli | |
Butcher shop F | Unknown | GC9 | Absent | 4.0 × 102 | C. jejuni | |
Conventionally reared | Supermarket chain A | P4 | RT1 | Present | 1.0 × 104 | C. coli |
Supermarket chain A | P4 | RT2 | Absent | 1.0 × 102 | C. jejuni | |
Butcher shop E | P6 | RT3 | Absent | 6.0 × 103 | C. coli | |
Butcher shop E | P7 | RT4 | Present | 1.0 × 101 | C. coli | |
Supermarket chain B | P8 | RT5 | Present | 3.7 × 103 | C. coli | |
Butcher shop E | P6 | RT6 | Absent | 6.0 × 103 | C. jejuni | |
Supermarket chain C | P2 | RT7 | Absent | 1.8 × 102 | C. jejuni and C. coli | |
Supermarket chain A | P1 | RT8 | Present | 4.2 × 102 | C. jejuni and C. coli | |
Supermarket chain C | P9 | RT9 | Absent | 6.3 × 102 | C. jejuni | |
Supermarket chain C | P2 | RT10 | Absent | 2.6 × 103 | C. jejuni | |
Supermarket chain C | P8 | RT11 | Present | 1.6 × 102 | C. coli |
Backyard Farm | Sample Code | Detection (in 10 g) | Enumeration (CFU/g) | Species Identification |
---|---|---|---|---|
1 | BY1 | Absent | <10 | n.a. |
2 | BY2 | Present | 3.1 × 103 | C. coli |
3 | BY3 | Present | <10 | C. coli |
4 | BY4 | Present | 2.5 × 105 | C. jejuni |
5 | BY5 | Present | 2.0 × 101 | C. jejuni and C. coli |
6 | BY6 | Absent | <10 | n.a. |
7 | BY7 | Absent | <10 | n.a. |
8 | BY8 | Absent | 1.0 × 101 | C. jejuni |
9 | BY9 | Present | 8.8 × 102 | C. jejuni and C. coli |
10 | BY10 | Present | 7.2 × 101 | C. jejuni and C. coli |
11 | BY11 | Present | <10 | C. coli |
Species | Susceptibility a | Antibiotic b No. of Isolates (%) | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
AMP | AMC | CN | CIP | E | TE | IMP | MEM | NA | ||
C. coli | R | 62 (79.5%) | 1 (1.3%) | 0 | 78 (100%) | 21 (26.9%) | 76 (97.4%) | 0 | 0 | 78 (100%) |
I | 6 (7.7%) | 15 (19.2%) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
S | 10 (12.8%) | 62 (79.5%) | 78 (100%) | 0 | 57 (73.1%) | 2 (2.6%) | 78 (100%) | 78 (100%) | 0 | |
C. jejuni | R | 48 (92.3%) | 0 | 0 | 50 (96.2%) | 5 (9.6%) | 48 (92.3%) | 0 | 0 | 50 (96.2%) |
I | 1 (1.9%) | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
S | 3 (5.8%) | 52 (100%) | 52 (100%) | 2 (3.8%) | 47 (90.4%) | 4 (7.7%) | 52 (100%) | 52 (100%) | 2 (3.8%) |
Resistance Phenotype | C. jejuni | C. coli | |||||||
---|---|---|---|---|---|---|---|---|---|
MDR | Conventional | Free-Range | Backyard | Total | Conventional | Free-Range | Backyard | Total | |
AMPR CIPR NAR TER | Yes | 19 | 14 | 9 | 42 | 5 | 6 | 15 | 26 |
AMPR CIPR NAR ER TER | Yes | 4 | 1 | 5 | 7 | 9 | 2 | 18 | |
AMPR AMCI CIPR NAR TER | Yes | 6 | 6 | 12 | |||||
CIPR NAR TER | Yes | 1 | 1 | 3 | 2 | 5 | 10 | ||
AMPI CIPR NAR TER | Yes | 4 | 2 | 6 | |||||
AMPR CIPR NAR | Yes | 1 | 1 | 2 | 2 | ||||
AMPR AMCI CIPR NAR ER TER | Yes | 2 | 1 | 3 | |||||
CIPR NAR | No | 1 | 1 | ||||||
AMPR AMCR CIPR NAR TER | Yes | 1 | 1 |
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Santos-Ferreira, N.; Ferreira, V.; Teixeira, P. Occurrence and Multidrug Resistance of Campylobacter in Chicken Meat from Different Production Systems. Foods 2022, 11, 1827. https://doi.org/10.3390/foods11131827
Santos-Ferreira N, Ferreira V, Teixeira P. Occurrence and Multidrug Resistance of Campylobacter in Chicken Meat from Different Production Systems. Foods. 2022; 11(13):1827. https://doi.org/10.3390/foods11131827
Chicago/Turabian StyleSantos-Ferreira, Nânci, Vânia Ferreira, and Paula Teixeira. 2022. "Occurrence and Multidrug Resistance of Campylobacter in Chicken Meat from Different Production Systems" Foods 11, no. 13: 1827. https://doi.org/10.3390/foods11131827