Cited by 11Salmonella and Campylobacter epidemiologyAntibiotic Use and ResistanceAntibiotic Resistance in Bacteria

Antibiotic-resistant Campylobacter coli and Campylobacter jejuni in commercial and smallholder farm animals in the Asante Akim North Municipality of Ghana

Open access
Paintsil, Ellis Kobina, Ofori, Linda Aurelia, Akenten, Charity Wiafe, Zautner, Andreas E., Mbwana, Joyce, Jaeger, Anna, Lamshöft, Maike, May, Jürgen +4 more·2022·Frontiers in Microbiology

Abstract

Worldwide, farm animals, in particular poultry, are an important reservoir for Campylobacter spp. However, information on Campylobacter colonization in farm animals in Africa is scarce. Hence, this cross-sectional study determined antibiotic-resistant Campylobacter from both commercial and smallholder farm animals in the Asante Akim North Municipality of Ghana. Fecal samples from poultry and livestock kept by commercial and smallholder farms were collected and analyzed using standard microbiological methods. The overall Campylobacter frequency was 20.3% (n/N = 322/1,585), and frequencies detected were similarly high in isolates from commercial (21.0%, n/N = 169/805) and smallholder (19.6%, n/N = 153/780) farms. Species isolated were C. coli (67.7%, n/N = 218/322) and C. jejuni (32.3%, n/N = 104/322). However, the frequency of C. coli was 2.1 (95% CI: 1.8–2.5) times higher than what was found for C. jejuni. Campylobacter frequencies in the rainy season was 22.2% (n/N = 258/1,160) and 15.1% (n/N = 64/425) in the dry season (prevalence ratio = 1.48, 95% CI: 1.2–1.9). About 1.7% (n/N = 6/322) of the Campylobacter isolates, all from smallholder farms, were susceptible to all antibiotics tested. Multidrug resistance was observed for 4.7% (n/N = 15/322) of the Campylobacter isolates, of which 93.3% (n/N = 14/15) occurred in isolates from commercial farms. This study highlights the need for the implementation of control programs, in commercial farming but also at the smallholder farm level, to formulate clear guidelines aimed at decreasing Campylobacter contamination of meat products and reducing the use of antibiotics in the farming sector.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fmicb.2022.983047

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • 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 [50]

    The Results section (page not provided) reports that 23.3% of animal-derived Campylobacter isolates resisted three or more antibiotics, which falls within the cited range. But the paper separately defines MDR as resistance to erythromycin, tetracycline, and ciprofloxacin and reports that measure at 4.7%, below the claimed range. This source alone cannot establish the results of all four cited studies. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 48

  1. Abraham S. Sahibzada S. Hewson K. Laird T. Abraham R. Pavic A.. (2020). Emergence of fluoroquinolone-resistant campylobacter jejuni and campylobacter coli among Australian chickens in the absence of fluoroquinolone use. Appl. Environ. Microbiol. 86, e02765– e02819. doi: 10.1128/AEM.02765-19 32033955 PMC7117913 · DOI
  2. Adam M. A. Wang J. Enan K. A. Shen H. Wang H. El Hussein A. R.. (2018). Molecular survey of viral and bacterial causes of childhood diarrhea in Khartoum state. Front. Microbiol. 9: 112. doi: 10.3389/fmicb.2018.00112, PMID: 29487571 PMC5816574 · DOI
  3. Asante-Addo C. Weible D. (2020). Is there hope for domestically produced poultry meat? A choice experiment of consumers in Ghana. Agribusiness 36, 281– 298. doi: 10.1002/agr.21626 · DOI
  4. Barros A. J. Hirakata V. N. (2003). Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med. Res. Methodol. 3, 1– 13. doi: 10.1186/1471-2288-3-21 14567763 PMC521200 · DOI
  5. Basler C. Nguyen T. A. Anderson T. C. Hancock T. Behravesh C. B. (2016). Outbreaks of human salmonella infections associated with live poultry, United States, 1990–2014. Emerg. Infect. Dis. 22, 1705– 1711. doi: 10.3201/eid2210.150765, PMID: 27649489 PMC5038410 · DOI
  6. Bénéjat L. Sifré E. Martins C. D. Ducournau A. Buissonnière A. Bessède E.. (2018). Epidemiologic cutoff values to separate wild-type from non–wild-type campylobacter fetus to ciprofloxacin. Diagn. Microbiol. Infect. Dis. 92, 164– 167. doi: 10.1016/j.diagmicrobio.2018.05.012, PMID: 29884563 · DOI
  7. Blaser M. J. Melby M. K. Lock M. Nichter M. (2021). Accounting for variation in and overuse of antibiotics among humans. BioEssays 43: 2000163. 33410142
  8. Chala G. Eguale T. Abunna F. Asrat D. Stringer A. (2021). Identification and characterization of campylobacter species in livestock, humans, and water in livestock owning households of Peri-urban Addis Ababa, Ethiopia: A one health approach. Front. Public Health 9: 750551. doi: 10.3389/fpubh.2021.750551, PMID: 34926375 PMC8677049 · DOI
  9. Colles F. M. McCarthy N. D. Bliss C. M. Layton R. Maiden M. C. (2015). The long-term dynamics of campylobacter colonizing a free-range broiler breeder flock: an observational study. Environ. Microbiol. 17, 938– 946. doi: 10.1111/1462-2920.12415, PMID: 25588789 PMC4390391 · DOI
  10. Corry J. E. Atabay H. I. Forsythe S. J. Mansfield L. P. (2003). “ Culture media for the isolation of campylobacters, helicobacters and arcobacters,” in Progress in Industrial Microbiology, Vol. 37. eds. Janet Corry E. L. Curtis G. D. W. Baird R. M. (Elsevier publishing company), 271– 316.
  11. Cox N. A. Cosby D. E. Thippareddi H. Ritz C. W. Berrang M. E. Jackson J. S.. (2018). Incidence, species and antimicrobial resistance of naturally occurring campylobacter isolates from quail carcasses sampled in a commercial processing facility. J. Food Saf. 38: e12438. doi: 10.1111/jfs.12438 · DOI
  12. Dai L. Sahin O. Grover M. Zhang Q. (2020). New and alternative strategies for the prevention, control, and treatment of antibiotic-resistant campylobacter. Transl. Res. 223, 76– 88. doi: 10.1016/j.trsl.2020.04.009, PMID: 32438073 PMC7423705 · DOI
  13. Dekker D. Eibach D. Boahen K. G. Akenten C. W. Pfeifer Y. Zautner A. E.. (2019). Fluoroquinolone-resistant salmonella enterica, campylobacter spp., and Arcobacter butzleri from local and imported poultry meat in Kumasi, Ghana. Foodborne Pathog. Dis. 16, 352– 358. doi: 10.1089/fpd.2018.2562, PMID: 30907631 PMC6529854 · DOI · Paper page
  14. Dias T. S. Nascimento R. J. Machado L. D. S. Abreu D. L. C. do Nascimento E. R. Pereira V. L. A.. (2021). Comparison of antimicrobial resistance in thermophilic campylobacter strains isolated from conventional production and backyard poultry flocks. Br. Poult. Sci. 62, 188– 192. doi: 10.1080/00071668.2020.1833302, PMID: 33026245 · DOI
  15. Djennad A. Iacono G. L. Sarran C. Lane C. Elson R. Höser C.. (2019). Seasonality and the effects of weather on campylobacter infections. BMC Infect. Dis. 19, 1– 10. doi: 10.1186/s12879-019-3840-7 30866826 PMC6417031 · DOI
  16. El-Adawy H. Ahmed M. F. Hotzel H. Tomaso H. Tenhagen B. A. Hartung J.. (2015). Antimicrobial susceptibilities of campylobacter jejuni and campylobacter coli recovered from organic Turkey farms in Germany. Poult. Sci. 94, 2831– 2837. doi: 10.3382/ps/pev259, PMID: 26371330 · DOI
  17. Endtz H. P. (2020). “ Campylobacter infections,” in Hunter's Tropical Medicine and Emerging Infectious Diseases. eds. Ryan E. T. Hill D. R. Endy T. P. (Elsevier Publishing Company), 507– 511.
  18. Frediani-Wolf V. Stephan R. (2003). Resistance patterns of campylobacter spp. strains isolated from poultry carcasses in a big Swiss poultry slaughterhouse. Int. J. Food Microbiol. 89, 233– 240. doi: 10.1016/S0168-1605(03)00152-1, PMID: 14623389 · DOI
  19. Gahamanyi N. Mboera L. E. Matee M. I. Mutangana D. Komba E. V. (2020). Prevalence, risk factors, and antimicrobial resistance profiles of thermophilic campylobacter species in humans and animals in sub-saharan Africa: a systematic review. Int. J. Microbiol. 2020, 2092478– 2092478. doi: 10.1155/2020/2092478 32025233 PMC6983289 · DOI
  20. Gilbert W. Thomas L. F. Coyne L. Rushton J. (2021). Mitigating the risks posed by intensification in livestock production: the examples of antimicrobial resistance and zoonoses. Animal 15: 100123. doi: 10.1016/j.animal.2020.100123, PMID: 33573940 · DOI
  21. Golz J. C. Stingl K. (2021). Natural competence and horizontal gene transfer in campylobacter. Curr. Top. Microbiol. Immunol. 431, 265– 292. doi: 10.1007/978-3-030-65481-8_10 33620655 · DOI
  22. Greenland S. (2004). Model-based estimation of relative risks and other epidemiologic measures in studies of common outcomes and in case-control studies. Am. J. Epidemiol. 160, 301– 305. doi: 10.1093/aje/kwh221, PMID: 15286014 · DOI
  23. Guyard-Nicodème M. Rivoal K. Houard E. Rose V. Quesne S. Mourand G.. (2015). Prevalence and characterization of campylobacter jejuni from chicken meat sold in French retail outlets. Int. J. Food Microbiol. 203, 8– 14. doi: 10.1016/j.ijfoodmicro.2015.02.013, PMID: 25770428 · DOI
  24. Hald B. Skov M. N. Nielsen E. M. Rahbek C. Madsen J. J. Wainø M.. (2015). Campylobacter jejuni and campylobacter coli in wild birds on Danish livestock farms. Acta Vet. Scand. 58, 1– 10. doi: 10.1186/s13028-016-0192-9 PMC4739333 26842400 · DOI
  25. Han X. Zhu D. Lai H. Zeng H. Zhou K. Zou L.. (2016). Prevalence, antimicrobial resistance profiling and genetic diversity of campylobacter jejuni and campylobacter coli isolated from broilers at slaughter in China. Food Control 69, 160– 170. doi: 10.1016/j.foodcont.2016.04.051 · DOI
  26. Kagambèga A. Thibodeau A. Trinetta V. Soro D. K. Sama F. N. Bako É.. (2018). Salmonella spp. and campylobacter spp. in poultry feces and carcasses in Ouagadougou, Burkina Faso. Food Sci. Nutr. 6, 1601– 1606. doi: 10.1002/fsn3.725, PMID: 30258603 PMC6145270 · DOI · Paper page
  27. Karikari A. B. Obiri-Danso K. Frimpong E. H. Krogfelt K. A. (2016). Multidrug resistant campylobacter in fecal and carcasses of commercially produced poultry. Afr. J. Microbiol. Res. 11, 271– 277. doi: 10.5897/AJMR2015.8329 · DOI
  28. Kouglenou S. D. Agbankpe A. J. Dougnon V. Djeuda A. D. Deguenon E. Hidjo M.. (2020). Prevalence and susceptibility to antibiotics from campylobacter jejuni and campylobacter coli isolated from chicken meat in southern Benin, West Africa. BMC Res. Notes 13, 1– 6. doi: 10.1186/s13104-020-05150-x 32591026 PMC7318530 · DOI
  29. Kunadu A. P. H. Otwey R. Y. Mosi L. (2020). Microbiological quality and salmonella prevalence, serovar distribution and antimicrobial resistance associated with informal raw chicken processing in Accra, Ghana. Food Control 118: 107440. doi: 10.1016/j.foodcont.2020.107440 · DOI
  30. Mandomando I. M. Macete E. V. Ruiz J. Sanz S. Abacassamo F. Valles X.. (2007). Etiology of diarrhea in children younger than 5 years of age admitted in a rural hospital of southern Mozambique. Am. J. Trop. Med. Hygiene 76, 522– 527. doi: 10.4269/ajtmh.2007.76.522, PMID: 17360878 · DOI
  31. Ocejo M. Oporto B. Hurtado A. (2019). Occurrence of campylobacter jejuni and campylobacter coli in cattle and sheep in northern Spain and changes in antimicrobial resistance in two studies 10-years apart. Pathogens 8: 98. doi: 10.3390/pathogens8030098, PMID: 31288484 PMC6789816 · DOI
  32. Padungtod P. Kaneene J. B. (2005). Campylobacter in food animals and humans in northern Thailand. J. Food Prot. 68, 2519– 2526. doi: 10.4315/0362-028X-68.12.2519, PMID: 16355821 · DOI
  33. Paintsil E. K. Ofori L. A. Adobea S. Akenten C. W. Phillips R. O. Maiga-Ascofare O.. (2022). Prevalence and antibiotic resistance in campylobacter spp. isolated from humans and food-producing animals in West Africa: A systematic review and meta-analysis. Pathogens 11: 140. doi: 10.3390/pathogens11020140, PMID: 35215086 PMC8877155 · DOI
  34. Paintsil E. K. Ofori L. A. Akenten C. W. Fosu D. Ofori S. Lamshöft M.. (2021). Antimicrobial usage in commercial and domestic poultry farming in two communities in the Ashanti region of Ghana. Antibiotics 10: 800. doi: 10.3390/antibiotics10070800, PMID: 34209451 PMC8300702 · DOI
  35. Plishka M. Sargeant J. M. Greer A. L. Hookey S. Winder C. (2021). The prevalence of campylobacter in live cattle, Turkey, chicken, and swine in the United States and Canada: A systematic review and meta-analysis. Foodborne Pathog. Dis. 18, 230– 242. doi: 10.1089/fpd.2020.2834, PMID: 33290141 · DOI
  36. Sainato R. ElGendy A. Poly F. Kuroiwa J. Guerry P. Riddle M. S.. (2018). Epidemiology of campylobacter infections among children in Egypt. Am. J. Trop. Med. Hygiene 98, 581– 585. doi: 10.4269/ajtmh.17-0469, PMID: 29260646 PMC5929192 · DOI
  37. Sibanda N. McKenna A. Richmond A. Ricke S. C. Callaway T. Stratakos A. C.. (2018). A review of the effect of management practices on campylobacter prevalence in poultry farms. Front. Microbiol. 9: 2002. doi: 10.3389/fmicb.2018.02002, PMID: 30197638 PMC6117471 · DOI
  38. Skarp C. P. A. Hänninen M. L. Rautelin H. I. K. (2016). Campylobacteriosis: the role of poultry meat. Clin. Microbiol. Infect. 22, 103– 109. doi: 10.1016/j.cmi.2015.11.019 26686808 · DOI
  39. Stringer A. Chala G. Eguale T. Abunna F. Asrat D. (2021). Identification and characterization of campylobacter species in livestock, humans and water in livestock owning households of peri-urban Addis Ababa, Ethiopia: a one health approach. Front. Public Health 9: 750551. doi: 10.3389/fpubh.2021.750551, PMID: 34926375 PMC8677049 · DOI
  40. Szosland-Fałtyn A. N. N. A. Bartodziejska B. Krolasik J. Paziak-Domańska B. Korsak D. Chmiela M. (2018). The prevalence of campylobacter spp. in polish poultry meat. Pol. J. Microbiol. 67, 117– 120. doi: 10.5604/01.3001.0011.6152 30015434 · DOI
  41. Tamhane A. R. Westfall A. O. Burkholder G. A. Cutter G. R. (2016). Prevalence odds ratio versus prevalence ratio: choice comes with consequences. Stat. Med. 35, 5730– 5735. doi: 10.1002/sim.7059, PMID: 27460748 PMC5135596 · DOI
  42. Torralbo A. Borge C. García-Bocanegra I. Méric G. Perea A. Carbonero A. (2015). Higher resistance of campylobacter coli compared to campylobacter jejuni at chicken slaughterhouse. Comp. Immunol. Microbiol. Infect. Dis. 39, 47– 52. doi: 10.1016/j.cimid.2015.02.003, PMID: 25770597 · DOI
  43. Uddin M. Neogi S. B. Islam S. S. Ferdous J. Khan M. Rahman S.. (2021). Occurrence and multidrug resistance of campylobacter spp. at duck farms and associated environmental and anthropogenic risk factors in Bangladesh. BMC Infect. Dis. 21, 1– 17. doi: 10.1186/s12879-021-06834-w 34743683 PMC8574054 · DOI
  44. Varga C. Guerin M. T. Brash M. L. Slavic D. Boerlin P. Susta L. (2019). Antimicrobial resistance in campylobacter jejuni and campylobacter coli isolated from small poultry flocks in Ontario, Canada: A two-year surveillance study. PLoS One 14: e0221429. doi: 10.1371/journal.pone.0221429., PMID: 31465474 PMC6715200 · DOI
  45. Wieczorek K. Bocian Ł. Osek J. (2020). Prevalence and antimicrobial resistance of campylobacter isolated from carcasses of chickens slaughtered in Poland–a retrospective study. Food Control 112: 107159. doi: 10.1016/j.foodcont.2020.107159 · DOI
  46. Wieczorek K. Bocian Ł. Osek J. (2021). Bovine and pig carcasses as a source of campylobacter in Poland: a reservoir for antimicrobial-resistant campylobacter coli. Foodborne Pathog. Dis. 18, 462– 468. doi: 10.1089/fpd.2020.2914, PMID: 33887151 · DOI
  47. Yang Y. Feye K. M. Shi Z. Pavlidis H. O. Kogut M. Ashworth J.. (2019). A historical review on antibiotic resistance of foodborne campylobacter. Front. Microbiol. 10: 1509. doi: 10.3389/fmicb.2019.01509, PMID: 31402900 PMC6676416 · DOI
  48. Zhang Q. Sahin O. (2020). Campylobacteriosis. Dis. Poultry. 1, 754– 769. doi: 10.1002/9781119371199.ch17 · DOI

Cited by

Sorted by citations

Authors
Paintsil, E. K., Ofori, L. A., Akenten, C. W., Zautner, A. E., Mbwana, J., Jaeger, A., Lamshöft, M., May, J., Obiri-Danso, K., Philipps, R. O., Krumkamp, R., & Dekker, D.
Affiliations
  • Kwame Nkrumah University of Science and Technology (GH)
  • Otto-von-Guericke-Universität Magdeburg (DE)
  • National Institute for Medical Research (TZ)
  • Bernhard Nocht Institute for Tropical Medicine (DE)
  • German Center for Infection Research (DE)
  • University Medical Center Hamburg-Eppendorf (DE)
  • Kumasi Centre for Collaborative Research in Tropical Medicine (GH)
Corresponding author
Paintsil, Ellis Kobina
Venue
Frontiers in Microbiology
Published
2022-11-04
Volume
13
Pages
983047-983047
ISSN
1664-302X (ISSN-L)
OpenAlex
W4308336326
Cited by
11
References
0
Citations by year
2026: 1 · 2025: 3 · 2024: 3 · 2023: 4
FWCI
1.46
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Microbiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Greater South Information System
Funders
German Research Foundation (380545990)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
Keywords
Campylobacter coli, Campylobacter jejuni, antibiotic resistance, multidrug resistance, smallholder farming, commercial farms, poultry, livestock, fecal carriage, seasonal variation, meat safety

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review