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Cited by 53Salmonella and Campylobacter epidemiologyAntibiotic Resistance in BacteriaAntibiotic Use and Resistance

Fluoroquinolone-Resistant Salmonella enterica , Campylobacter spp., and Arcobacter butzleri from Local and Imported Poultry Meat in Kumasi, Ghana

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Dekker, Denise, Eibach, Daniel, Boahen, Kennedy G., Akenten, Charity Wiafe, Pfeifer, Yvonne, Zautner, Andreas E., Mertens, Eva, Krumkamp, Ralf +4 more·2019·Foodborne Pathogens and Disease
DOI 10.1089/fpd.2018.2562PMC PMC6529854
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Abstract

Salmonella and Campylobacter are important gastroenteric pathogens. Arcobacter butzleri is an emerging enteric pathogen. Data on the frequencies of these poultry-associated pathogens on meat products sold in sub-Saharan Africa are scarce. This study aimed to analyze the frequency of Salmonella , Campylobacter , and Arcobacter antibiotic resistance and underlying mechanisms of resistance to fluoroquinolones in locally produced and imported poultry sold in urban Ghana. Chicken meat was collected and cultured on standard media. Bacterial strains were identified by biochemical methods and by mass spectrometry. Antibiotic susceptibility was tested by disk diffusion. Ciprofloxacin-resistant strains were assessed for molecular mechanisms of resistance. Among 200 samples, comprising 34% ( n = 68) from the Ghanaian poultry industry and 66% ( n = 132) from imports, 9% ( n = 17) contained Salmonella , 11% ( n = 22) Campylobacter , and 26.5% ( n = 53) A. butzleri . Higher overall contamination frequencies were found in local meat. Most common Salmonella serovars identified were Kentucky ( n / N = 5/16; 31%) and Poona ( n / N = 4/16; 25%). Campylobacter were C. coli ( n / N = 10/19; 53%) and C. jejuni ( n / N = 9/19; 47%). Resistance to fluoroquinolones was high with 63% ( n = 10), 75% ( n = 15), and 52% ( n = 25) in Salmonella , Campylobacter , and Arcobacter , respectively. A link between Salmonella Kentucky [sequence type (ST) 198] and a ciprofloxacin minimum inhibitory concentration of 16 μg/mL was found. Salmonella Poona-ST308 revealed transferable qnrB2 fluoroquinolone resistance genes. Markedly high frequencies of resistant Salmonella , Campylobacter , and Arcobacter predominant in locally produced meat represent a probable transmission reservoir for human infections. These findings highlight the need for implementation of surveillance systems that focus on food hygiene, use of antibiotics in animal husbandry, and continuous monitoring of the quality of meat products from imports.

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  • Campylobacter spp., reported only from animals, had resistance prevalence of 75% to ciprofloxacin and 70% to tetracycline in one study.

    “For example, in the case of Campylobacter spp., which were reported from only animals, one study reported a resistance prevalence of 75% to ciprofloxacin and 70% to tetracycline [55]”

    From A Systematic Review on Antimicrobial Resistance in Ghana from a One Health Perspective (2024) · cites this paper as [55]

    Table 1 in the Results reports ciprofloxacin resistance of 15/20 (75%) and tetracycline resistance of 14/20 (70%) among Campylobacter isolates from poultry meat. However, the Results prose gives tetracycline resistance as 17/20 (85%), so the paper is internally inconsistent on that figure. The study sampled poultry meat, not human cases. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Four animal studies reported MDR traits ranging from 20% to 66.6% in Campylobacter spp.

    “Four “animal studies” reported MDR traits ranging from 20% to 66.6% in Campylobacter spp. [50,52,53,55].”

    From A Systematic Review on Antimicrobial Resistance in Ghana from a One Health Perspective (2024) · cites this paper as [55]

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  1. Abdelbaqi K, Ménard A, Prouzet-Mauleon V, Bringaud F, Lehours P, Mégraud F Nucleotide sequence of the gyrA gene of Arcobacter species and characterization of human ciprofloxacin-resistant clinical isolates. FEMS Immunol Med Microbiol 2007; 49: 337– 345 17378897
  2. Abdi RD, Mengstie F, Beyi AF, Beyene T, Waktole H, Mammo B, Ayana D, Abunna F Determination of the sources and antimicrobial resistance patterns of Salmonella isolated from the poultry industry in Southern Ethiopia. BMC Infect Dis 2017; 17: 352 28521744 PMC5437651
  3. Adesiji YO, Alli OT, Adekanle MA, Jolayemi JB Prevalence of Arcobacter, Escherichia coli, Staphylococcus aureus and Salmonella spp. in retail chicken, pork, beef, goat meat in Osogbo, Nigeria. Sierra Leon J of Biomed Res 2012; 3: 8– 12
  4. Adu-Gyamfi A, Torgby-Tetteh W, Appiah V Microbiological quality of chicken sold in Accra and determination of D10-value of E. coli. Food Nutr Sci 2012; 3: 6
  5. Aldred KJ, Kerns RJ, Osheroff N Mechanism of quinolone action and resistance. Biochemistry 2014; 53: 1565– 1574 24576155 PMC3985860
  6. Andoh LA, Dalsgaard A, Obiri-Danso K, Newman MJ, Barco L, Olsen JE Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry in Ghana. Epidemiol Infect 2016; 144: 3288– 3299 27334298 PMC9150280
  7. Atabay HI, Aydin F, Houf K, Sahin M, Vandamme P The prevalence of Arcobacter spp. on chicken carcasses sold in retail markets in Turkey, and identification of the isolates using SDS-PAGE. Int J Food Microbiol 2003; 81: 21– 28 12423915
  8. Chan KF, Le Tran H, Kanenaka RY, Kathariou S Survival of clinical and poultry-derived isolates of Campylobacter jejuni at a low temperature (4 degrees C). Appl Environ Microbiol 2001; 67: 4186– 4191 11526022 PMC93146
  9. Chang Q, Wang W, Regev-Yochay G, Lipsitch M, Hanage WP Antibiotics in agriculture and the risk to human health: How worried should we be? Evol Appl 2015; 8: 240– 247 25861382 PMC4380918
  10. Chau TT, Campbell JI, Galindo CM, Van Minh Hoang N, Diep TS, Nga TT, Van Vinh Chau N, Tuan PQ, Page AL, Ochiai RL, Schultsz C, Wain J, Bhutta ZA, Parry CM, Bhattacharya SK, Dutta S, Agtini M, Dong B, Honghui Y, Anh DD, Canh DG, Naheed A, Albert MJ, Phetsouvanh R, Newton PN, Basnyat B, Arjyal A, La TT, Rang NN, Phuong LT, Van Be Bay P, von Seidlein L, Dougan G, Clemens JD, Vinh H, Hien TT, Chinh NT, Acosta CJ, Farrar J, Dolecek C Antimicrobial drug resistance of Salmonella enterica serovar Typhi in Asia and molecular mechanism of reduced susceptibility to the fluoroquinolones. Antimicrob Agents Chemother 2007; 51: 4315– 4323 17908946 PMC2167998
  11. Collado L, Figueras MJ Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin Microbiol Rev 2011; 24: 174– 192 21233511 PMC3021208
  12. Corry J, Atabay HI Poultry as a source of Campylobacter and related organisms. Symp Ser Soc Appl Microbiol 2001; 30: 96– 114 11422565
  13. EFSA 2010 scientific report. Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella prevalence estimates. EFSA J 2010; 8: 1503
  14. EFSA and ECDC scientific report 2015 EU Summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food 2013. EFSA J 2015; 13: 4036
  15. Eibach D, Al-Emran HM, Dekker D, Krumkamp R, Adu-Sarkodie Y, Cruz Espinoza LM, Ehmen C, Boahen K, Heisig P, Im J, Jaeger A, von Kalckreuth V, Pak GD, Panzner U, Park SE, Reinhardt A, Sarpong N, Schütt-Gerowitt H, Wierzba TF, Marks F, May J The emergence of reduced ciprofloxacin susceptibility in Salmonella enterica causing bloodstream infections in Rural Ghana. Clin Infect Dis 2016; 62(Suppl. 1): S32– S36 26933017
  16. Eibach D, Dekker D, Gyau Boahen K, Wiafe C Akenten, Sarpong N, Belmar Campos C, Berneking L, Aepfelbacher M, Krumkamp R, Owusu-Dabo E, May J Extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in local and imported poultry meat in Ghana. Vet Microbiol 2018; 217: 7– 12 29615260
  17. Geilhausen B, Schütt-Gerowitt H, Aleksic S, Koenen R, Mauff G, Pulverer G Campylobacter and Salmonella contaminating fresh chicken meat. Zentralbl Bakteriol 1996; 284: 241– 245 8837384
  18. Kluytmans JA, Overdevest IT, Willemsen I, Kluytmans-van den Bergh MF, van der Zwaluw K, Heck M, Rijnsburger M, Vandenbroucke-Grauls CM, Savelkoul PH, Johnston BD, Gordon D, Johnson JR Extended-spectrum β-lactamase-producing Escherichia coli from retail chicken meat and humans: Comparison of strains, plasmids, resistance genes, and virulence factors. Clin Infect Dis 2013; 56: 478– 487 23243181
  19. Kotloff KL, Platts-Mills JA, Nasrin D, Roose A, Blackwelder WC Levine MM Global burden of diarrheal diseases among children in developing countries: Incidence, etiology, and insights from new molecular diagnostic techniques. Vaccine 2017; 35(49 Pt A): 6783– 6789 28765005
  20. Krumkamp R, Sarpong N, Schwarz NG, Adlkofer J, Loag W, Eibach D, Hagen RM, Adu-Sarkodie Y, Tannich E, May J Correction: Gastrointestinal infections and diarrheal disease in ghanaian infants and children: An outpatient case-control study. PLoS Negl Trop Dis 2015; 9: e0003728 25738935 PMC4349824
  21. Kudirkiene E, Andoh LA, Ahmed S, Herrero-Fresno A, Dalsgaard A, Obiri-Danso K, Olsen JE The use of a combined bioinformatics approach to locate antibiotic resistance genes on plasmids from whole genome sequences of Salmonella enterica serovars from humans in Ghana. Front Microbiol 2018; 9: 1010 29867897 PMC5966558
  22. Le Hello S, Hendriksen RS, Doublet B, Fisher I, Nielsen EM, Whichard JM, Bouchrif B, Fashae K, Granier SA, Jourdan-Da Silva N, Cloeckaert A, Threlfall EJ, Angulo FJ, Aarestrup FM, Wain J, Weill FX International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J Infect Dis 2011; 204: 675– 684 21813512
  23. Maron DF, Smith TJ, Nachman KE Restrictions on antimicrobial use in food animal production: An international regulatory and economic survey. Global Health 2013; 9: 48 24131666 PMC3853314
  24. Niehaus AJ, Apalata T, Coovadia YM, Smith AM, Moodley P An outbreak of foodborne salmonellosis in rural KwaZulu-Natal, South Africa. Foodborne Pathog Dis 2011; 8: 693– 697 21388293
  25. Paul NC, Sullivan TS, Shah DH Differences in antimicrobial activity of chlorine against twelve most prevalent poultry-associated Salmonella serotypes. Food Microbiol 2017; 64: 202– 209 28213027
  26. Pfeifer Y, Matten J, Rabsch W Salmonella enterica serovar Typhi with CTX-M beta-lactamase, Germany. Emerg Infect Dis 2009; 15: 1533– 1535 PMC2819882 19788837
  27. Pham NT, Ushijima H, Trinh QD, Khamrin P, Komine-Aizawa S, Okitsu S, Maneekarn N, Hayakawa S Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli from adult hospitalized patients with diarrhea in Thailand. Clin Lab 2015; 61: 1809– 1812 26749592
  28. Pietsch M, Eller C, Wendt C, Holfelder M, Falgenhauer L, Fruth A, Grössl T, Leistner R, Valenza G, Werner G, Pfeifer Y Molecular characterisation of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli isolates from hospital and ambulatory patients in Germany. Vet Microbiol 2007; 200: 130– 137 26654217
  29. Raufu I, Fashae K, Ameh JA, Ambali A, Ogunsola FT, Coker AO, Hendriksen RS Persistence of fluoroquinolone-resistant Salmonella enterica serovar Kentucky from poultry and poultry sources in Nigeria. J Infect Dev Ctries 2014; 8: 384– 388 24619272
  30. Sackey BA, Mensah P, Collison E, Sakyi-Dawson E Campylobacter, Salmonella, Shigella and Escherichia coli in live and dressed poultry from metropolitan Accra. Int J Food Microbiol 2001; 71: 21– 28 11764888
  31. Tang Y, Sahin O, Pavlovic N, LeJeune J, Carlson J, Wu Z, Dai L, Zhang Q Rising fluoroquinolone resistance in Campylobacter isolated from feedlot cattle in the United States. Sci Rep 2017; 7: 494 28356558 PMC5428712
  32. Wasyl D, Hoszowski A, Zając M Prevalence and characterisation of quinolone resistance mechanisms in Salmonella spp. Vet Microbiol 2014; 171: 307– 314 24613291

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Authors
Dekker, D., Eibach, D., Boahen, K. G., Akenten, C. W., Pfeifer, Y., Zautner, A. E., Mertens, E., Krumkamp, R., Jaeger, A., Flieger, A., Owusu-Dabo, E., & May, J.
Affiliations
  • German Center for Infection Research (DE)
  • Bernhard Nocht Institute for Tropical Medicine (DE)
  • Kumasi Centre for Collaborative Research in Tropical Medicine (GH)
  • Robert Koch Institute (DE)
  • Universitätsmedizin Göttingen (DE)
  • Kumasi Centre for Collaborative Research in Tropical Medicine (KCCR), Kumasi, Ghana.
Corresponding author
Dekker, Denise
ORCID
Venue
Foodborne Pathogens and Disease
Publisher
SAGE Publications
Published
2019-05
Volume
16
Issue
5
Pages
352-358
ISSN
  • 1535-3141 (ISSN-L)
  • 1556-7125
DOI
10.1089/fpd.2018.2562
PMC
PMC6529854
OpenAlex
W2940886616
Cited by
53
References
1
Citations by year
2026: 7 · 2025: 12 · 2024: 7 · 2023: 9 · 2022: 8 · 2021: 5 · 2020: 3 · 2019: 2
FWCI
3.47
Type
journal article
Language
en
Open access
Licence
Locations
  • Foodborne Pathogens and Disease (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Publication server of the Robert Koch Institute (Robert Kock Institute) (submittedVersion, cc-by)
  • GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
Funders
Deutsches Zentrum für Infektionsforschung (8000 201-3)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
Keywords
Salmonella enterica, Campylobacter, Arcobacter butzleri, fluoroquinolone resistance, ciprofloxacin resistance, poultry meat, imported meat, antimicrobial resistance, Salmonella Kentucky, Salmonella Poona, Campylobacter jejuni, Campylobacter coli, foodborne pathogens, Kumasi, Ghana
MeSH terms
Animals, Anti-Bacterial Agents, Campylobacter, Ciprofloxacin, Food Microbiology, Ghana, Meat Products, Microbial Sensitivity Tests, Poultry, Gram-Negative Bacterial Infections, Salmonella enterica, Arcobacter, Fluoroquinolones, Drug Resistance, Multiple, Bacterial

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