Molecular Detection, Phenotypic and Genotypic Characters of The Antimicrobial Resistance and Virulenece Factors of Campylobacter Jejuni and Campylobacter Coli Isolated from Poultry Meat
Campylobacter in poultry meat
Keywords:
Campylobacter Species; Antibiotic Resistance; Virulence Factors; Poultry MeatAbstract
oultry meat is recognized as a potential reservoir of Campylobacter jejuni and Campylobacter coli. This study was done to assess antibiotic resistance and virulence characteristics of C. jejuni and C. coli isolated from raw poultry meat. Raw poultry meat samples were collected. C. jejuni and C. coli were isolated after microbial examination. Disk diffusion was applied to apprise antibiotic resistance. Polymerase Chain Reaction was employed to determine the virulence and antibiotic resistance gene distribution. Raw poultry meat samples contamination rate with Campylobacter spp. was 19% (76 out of 400 samples). The highest contamination rate was observed amongst the raw duck meat samples (37.50%). Forty-three (56.57%) and twenty (26.31%) out of 76 Campylobacter spp. were recognized as C. jejuni and C. coli, respectively. C. jejuni and C. coli isolates harbored the uppermost rates of resistance toward tetracycline (67.44% and 50%), gentamicin (60.46% and 50%), ampicillin (48.89% and 40%), and erythromycin (48.89% and 35%), respectively. The prevalence of multidrug-resistant C. jejuni and C. coli was 81.39% and 75%, respectively. C. jejuni and C. coli bacteria harbored tetO (23.48% and 45%), cmeB (44.18% and 45%), and blaOXA (44.18% and 35%) antibiotic resistance genes, respectively. All isolates harbored fla and ciaB. Among the C. jejuni isolates, cadF (67.44%), racC (46.51%), and cdtB (46.51%) and amongst the C. coli isolates, pldA (50%), cdtA (35%), racC (30%), and cadF (30%) were major virulence factors. The role of raw poultry meat, particularly duck and goose, as antibiotic-resistant and virulent Campylobacter spp. reservoirs were confirmed.
References
Paintsil EK, Ofori LA, Adobea S, Akenten CW, Phillips RO, Maiga-Ascofare O, et al. Prevalence and antibiotic resistance in Campylobacter spp isolated from humans and food-producing animals in West Africa A systematic review and meta-analysis. Pathogens. 2022 Jan 24;11(2):140.
https://doi.org/10.3390/pathogens11020140
PMid:35215086 PMCid:PMC8877155
Sher AA, Ashraf MA, Mustafa BE, Raza MM. Epidemiological trends of foodborne Campylobacter outbreaks in the United States of America, 1998-2016. Food Microbiology. 2021 Aug 1;97:103751.
https://doi.org/10.1016/j.fm.2021.103751
PMid:33653524
Keithlin J, Sargeant J, Thomas MK, Fazil A. Systematic review and meta-analysis of the proportion of Campylobacter cases that develop chronic sequelae. BMC public health. 2014 Dec;14:1-9.
https://doi.org/10.1186/1471-2458-14-1203
PMid:25416162 PMCid:PMC4391665
Oh E, Andrews KJ, Jeon B. Enhanced biofilm formation by ferrous and ferric iron through oxidative stress in Campylobacter jejuni. Frontiers in microbiology. 2018 Jun 6;9:1204.
https://doi.org/10.3389/fmicb.2018.01204
PMid:29928267 PMCid:PMC5998592
Scharff RL. Food attribution and economic cost estimates for meat-and poultry-related illnesses. Journal of food protection. 2020 Jun 1;83(6):959-67.
https://doi.org/10.4315/JFP-19-548
PMid:32032420
Park SF. The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. International journal of food microbiology. 2002 Apr 5;74(3):177-88.
https://doi.org/10.1016/S0168-1605(01)00678-X
PMid:11981968
Tresse O, Alvarez-Ordóñez A, Connerton IF. About the foodborne pathogen Campylobacter. Frontiers in microbiology. 2017 Oct 10;8:1908.
https://doi.org/10.3389/fmicb.2017.01908
PMid:29067004 PMCid:PMC5641295
from Poultry TC. Antimicrobial resistance and antibiogram of thermotolerant Campylobacter recovered from poultry meat in Baghdad markets, Iraq. Archives of Razi Institute. 2022;77(1):249-55.
Petrović J, Stojanov I, Milanov D, Kapetanov M. Antimicrobial resistance of thermotolerant Campylobacter spp as a food safety issue. Biotechnology in Animal Husbandry. 2011;27(3):1321-8.
https://doi.org/10.2298/BAH1103321P
Igwaran A, Okoh AI. Human campylobacteriosis: A public health concern of global importance. Heliyon. 2019 Nov 14;5(11):e02814.
https://doi.org/10.1016/j.heliyon.2019.e02814
PMid:31763476 PMCid:PMC6861584
European Food Safety Authority. Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses, in the EU, 2008‐Part B: Analysis of factors associated with Campylobacter colonisation of broiler batches and with Campylobacter contamination of broiler carcasses; and investigation of the culture method diagnostic characteristics used to analyse broiler carcass samples. EFSA journal. 2010 Aug;8(8):1522.
https://doi.org/10.2903/j.efsa.2010.1522
Sałamaszyńska-Guz A, Rasmussen PK, Murawska M, Douthwaite S. Campylobacter jejuni virulence factors identified by modulating their synthesis on ribosomes with altered rRNA methylation. Frontiers in cellular and infection microbiology. 2022 Jan 13;11:803730.
https://doi.org/10.3389/fcimb.2021.803730
PMid:35096652 PMCid:PMC8794745
Hlashwayo DF, Sigauque B, Noormahomed EV, Afonso SM, Mandomando IM, Bila CG. A systematic review and meta-analysis reveal that Campylobacter spp and antibiotic resistance are widespread in humans in sub-Saharan Africa. PLoS One. 2021 Jan 27;16(1):e0245951.
https://doi.org/10.1371/journal.pone.0245951
PMid:33503068 PMCid:PMC7840040
Yang Y, Feye KM, Shi Z, Pavlidis HO, Kogut M, J Ashworth A, et al. A Historical Review on Antibiotic Resistance of Foodborne Campylobacter. Front Microbiol. 2019 Jul 26;10:1509.
https://doi.org/10.3389/fmicb.2019.01509
PMid:31402900 PMCid:PMC6676416
Tang M, Zhou Q, Zhang X, Zhou S, Zhang J, Tang X, Lu J, Gao Y. Antibiotic resistance profiles and molecular mechanisms of Campylobacter from chicken and pig in China. Frontiers in Microbiology. 2020 Oct 27;11:592496.
https://doi.org/10.3389/fmicb.2020.592496
PMid:33193261 PMCid:PMC7652819
Denis M, Refrégier‐Petton J, Laisney MJ, Ermel G, Salvat G. Campylobacter contamination in French chicken production from farm to consumers Use of a PCR assay for detection and identification of Campylobacter jejuni and Camp coli. Journal of applied microbiology. 2001 Aug 2;91(2):255-67.
https://doi.org/10.1046/j.1365-2672.2001.01380.x
PMid:11473590
Sifré E, Salha BA, Ducournau A, Floch P, Chardon H, Mégraud F, Lehours P. EUCAST recommendations for antimicrobial susceptibility testing applied to the three main Campylobacter species isolated in humans. Journal of microbiological methods. 2015 Dec 1;119:206-13.
https://doi.org/10.1016/j.mimet.2015.10.018
PMid:26519770
Wayne PA. Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing. (2011): 100-121.
Ranjbar R, Yadollahi Farsani F, Safarpoor Dehkordi F. Antimicrobial resistance and genotyping of vacA, cagA, and iceA alleles of the Helicobacter pylori strains isolated from traditional dairy products. Journal of Food Safety. 2019 Apr;39(2):e12594.
https://doi.org/10.1111/jfs.12594
Safarpoor Dehkordi F, Gandomi H, Basti AA, Misaghi A, Rahimi E. Phenotypic and genotypic characterization of antibiotic resistance of methicillin-resistant Staphylococcus aureus isolated from hospital food. Antimicrobial resistance & infection control. 2017 Dec;6:1-1.
https://doi.org/10.1186/s13756-017-0257-1
PMid:29034091 PMCid:PMC5628482
Mashak Z, Jafariaskari S, Alavi I, Sakhaei Shahreza M, Safarpoor Dehkordi F. Phenotypic and genotypic assessment of antibiotic resistance and genotyping of vacA, cagA, iceA, oipA, cagE, and babA2 alleles of Helicobacter pylori bacteria isolated from raw meat. Infection and drug resistance. 2020 Jan 29:257-72.
https://doi.org/10.2147/IDR.S233612
PMid:32099418 PMCid:PMC6996226
Abdolmaleki Z, Mashak Z, Safarpoor Dehkordi F. Phenotypic and genotypic characterization of antibiotic resistance in the methicillin-resistant Staphylococcus aureus strains isolated from hospital cockroaches. Antimicrobial Resistance & Infection Control. 2019 Dec;8:1-4.
https://doi.org/10.1186/s13756-019-0505-7
PMid:30911380 PMCid:PMC6416839
Datta S, Niwa H, Itoh K. Prevalence of 11 pathogenic genes of Campylobacter jejuni by PCR in strains isolated from humans, poultry meat and broiler and bovine faeces. Journal of medical microbiology. 2003 Apr;52(4):345-8.
https://doi.org/10.1099/jmm.0.05056-0
PMid:12676874
Obeng AS, Rickard H, Sexton M, Pang Y, Peng H, Barton M. Antimicrobial susceptibilities and resistance genes in Campylobacter strains isolated from poultry and pigs in Australia. Journal of applied microbiology. 2012 Aug 1;113(2):294-307.
https://doi.org/10.1111/j.1365-2672.2012.05354.x
PMid:22672511
Ruiz J, Goñi P, Marco F, Gallardo F, Mirelis B, Anta TJ, Vila J. Increased resistance to quinolones in Campylobacter jejuni: a genetic analysis of gyrA gene mutations in quinolone-resistant clinical isolates. Microbiology and immunology. 1998;42(3):223-6.
https://doi.org/10.1111/j.1348-0421.1998.tb02274.x
PMid:9580533
Shahreza MS. Ready To Eat Food Samples As Reservoirs Of Shiga Toxigenic Escherichia Coli. Journal of Pharmaceutical Negative Results. 2022 Dec 31:9761-6.
Ranjbar R, Shahreza MH, Rahimi E, Jonaidi-Jafari N. Methicillin-resistant Staphylococcus aureus isolates from Iranian restaurant food samples: Panton-Valentine Leukocidin, SCCmec phenotypes and antimicrobial resistance. Tropical Journal of Pharmaceutical Research. 2017 Sep 7;16(8):1939-49.
https://doi.org/10.4314/tjpr.v16i8.26
Kim HY. Statistical notes for clinical researchers: Chi-squared test and Fisher's exact test. Restorative dentistry & endodontics. 2017 May 1;42(2):152-5.
https://doi.org/10.5395/rde.2017.42.2.152
PMid:28503482 PMCid:PMC5426219
Zakaria AI, Sabala RF. Potential public health hazards related to consumption of poultry contaminated with antibiotic resistant Listeria monocytogenes in Egypt. BMC microbiology. 2024 Jan 29;24(1):41.
https://doi.org/10.1186/s12866-024-03183-x
PMid:38287241 PMCid:PMC10823629
Olsen A, Bonardi S, Barco L, Sandberg M, Langkabel N, Roasto M, Majewski M, Brugger B, Kautto AH, Blagojevic B, Cota JB. A comparison of European surveillance programs for Campylobacter in broilers. Food Control. 2024 Jan 1;155:110059.
https://doi.org/10.1016/j.foodcont.2023.110059
Frosth S, Karlsson-Lindsjö O, Niazi A, Fernström LL, Hansson I. Identification of transmission routes of Campylobacter and on-farm measures to reduce Campylobacter in chicken. Pathogens. 2020 May 9;9(5):363.
https://doi.org/10.3390/pathogens9050363
PMid:32397445 PMCid:PMC7281276
Tedersoo T, Roasto M, Mäesaar M, Kisand V, Ivanova M, Meremäe K. The prevalence, counts, and MLST genotypes of Campylobacter in poultry meat and genomic comparison with clinical isolates. Poultry Science. 2022 Apr 1;101(4):101703.
https://doi.org/10.1016/j.psj.2022.101703
PMid:35124442 PMCid:PMC8819112
Schets FM, Jacobs-Reitsma WF, van der Plaats RQ, Heer LK, van Hoek AH, Hamidjaja RA, de Roda Husman AM, Blaak H. Prevalence and types of Campylobacter on poultry farms and in their direct environment. Journal of Water and Health. 2017 Dec 1;15(6):849-62.
https://doi.org/10.2166/wh.2017.119
PMid:29215350
Sibanda N, McKenna A, Richmond A, Ricke SC, Callaway T, Stratakos AC, et al. A review of the effect of management practices on Campylobacter prevalence in poultry farms. Frontiers in microbiology. 2018 Aug 24;9:2002.
https://doi.org/10.3389/fmicb.2018.02002
PMid:30197638 PMCid:PMC6117471
Kouglenou SD, Agbankpe AJ, Dougnon V, Djeuda AD, Deguenon E, Hidjo M, Baba-Moussa L, Bankole H. Prevalence and susceptibility to antibiotics from Campylobacter jejuni and Campylobacter coli isolated from chicken meat in southern Benin, West Africa. BMC research notes. 2020 Dec;13:1-6.
https://doi.org/10.1186/s13104-020-05150-x
PMid:32591026 PMCid:PMC7318530
Poudel S, Li T, Chen S, Zhang X, Cheng WH, Sukumaran AT, Kiess AS, Zhang L. Prevalence, antimicrobial resistance, and molecular characterization of Campylobacter isolated from broilers and broiler meat raised without antibiotics. Microbiology Spectrum. 2022 Jun 29;10(3):e00251-22.
https://doi.org/10.1128/spectrum.00251-22
PMid:35536038 PMCid:PMC9241809
Korsak D, Maćkiw E, Rożynek E, Żyłowska M. Prevalence of Campylobacter spp in retail chicken, turkey, pork, and beef meat in Poland between 2009 and 2013. Journal of food protection. 2015 May 1;78(5):1024-8.
https://doi.org/10.4315/0362-028X.JFP-14-353
PMid:25951401
Shange N, Gouws PA, Hoffman LC. Prevalence of Campylobacter and Arcobacter species in ostriches from Oudtshoorn, South Africa. Journal of food protection. 2020 Apr 1;83(4):722-8.
https://doi.org/10.4315/JFP-19-472
PMid:31855449
Dipineto L, Russo TP, Gargiulo A, Borrelli L, De Luca Bossa LM, Santaniello A, Buonocore P, Menna LF, Fioretti A. Prevalence of enteropathogenic bacteria in common quail (Coturnix coturnix). Avian Pathology. 2014 Nov 2;43(6):498-500.
https://doi.org/10.1080/03079457.2014.966055
PMid:25245588
Chon JW, Lee SK, Yoon Y, Yoon KS, Kwak HS, Joo IS, Seo KH. Quantitative prevalence and characterization of Campylobacter from chicken and duck carcasses from poultry slaughterhouses in South Korea. Poultry science. 2018 Aug 1;97(8):2909-16.
https://doi.org/10.3382/ps/pey120
PMid:29757448
Jamali H, Ghaderpour A, Radmehr B, Wei KS, Chai LC, Ismail S. Prevalence and antimicrobial resistance of Campylobacter species isolates in ducks and geese. Food Control. 2015 Apr 1;50:328-30.
https://doi.org/10.1016/j.foodcont.2014.09.016
Rahimi E, Alian F, Alian F. Prevalence and characteristic of Campylobacter species isolated from raw duck and goose meat in Iran. IPCBEE. 2011;9:171-5.
Colles FM, Ali JS, Sheppard SK, McCarthy ND, Maiden MC. Campylobacter populations in wild and domesticated Mallard ducks (Anas platyrhynchos). Environmental microbiology reports. 2011 Oct;3(5):574-80.
https://doi.org/10.1111/j.1758-2229.2011.00265.x
PMid:22164198 PMCid:PMC3229703
Kasrazadeh M, Genigeorgis C. Origin and prevalence of Campylobacter jejuni in ducks and duck meat at the farm and processing plant level. Journal of Food Protection. 1987 Apr 1;50(4):321-6.
https://doi.org/10.4315/0362-028X-50.4.321
PMid:30965421
Mohan V. Faeco-prevalence of Campylobacter jejuni in urban wild birds and pets in New Zealand. BMC research notes. 2015 Dec;8:1-7.
https://doi.org/10.1186/1756-0500-8-1
PMid:25645429 PMCid:PMC4417317
Hadiyan M, Momtaz H, Shakerian A. Prevalence, antimicrobial resistance, virulence gene profile and molecular typing of Campylobacter species isolated from poultry meat samples. Veterinary Medicine and Science. 2022 Nov;8(6):2482-93.
https://doi.org/10.1002/vms3.944
PMid:36253836 PMCid:PMC9677401
Mousavinafchi SB, Rahimi E, Shakerian A. Campylobacter spp isolated from poultry in Iran: Antibiotic resistance profiles, virulence genes, and molecular mechanisms. Food science & nutrition. 2023 Feb;11(2):1142-53.
https://doi.org/10.1002/fsn3.3152
PMid:36789060 PMCid:PMC9922131
Sabzmeydani A, Rahimi E, Shakerian A. Incidence and antibiotic resistance properties of Campylobacter species isolated from poultry meat. International Journal of Enteric Pathogens. 2020 May 28;8(2):60-5.
https://doi.org/10.34172/ijep.2020.13
Walker LJ, Wallace RL, Smith JJ, Graham T, Saputra T, Symes S, Stylianopoulos A, Polkinghorne BG, Kirk MD, Glass K. Prevalence of Campylobacter coli and Campylobacter jejuni in retail chicken, beef, lamb, and pork products in three Australian states. Journal of Food Protection. 2019 Dec 1;82(12):2126-34.
https://doi.org/10.4315/0362-028X.JFP-19-146
PMid:31729918
Mohamed K. Prevalence of Campylobacter Spp And Its Pathogenic Genes In Poultry Meat, Human And Environment In Aswan, Upper Egypt. Assiut Veterinary Medical Journal. 2019 Apr 9;65(161):151-8.
https://doi.org/10.21608/avmj.2019.168777
Sabzmeydani A, Rahimi E, Shakerian A. Incidence and antimicrobial resistance of campylobacter species isolated from poultry eggshell samples. Egyptian Journal of Veterinary Sciences. 2020 Sep 1;51(3):329-35.
https://doi.org/10.21608/ejvs.2020.26303.1163
Nebola M, Borilova G, Steinhauserova I. Prevalence of Campylobacter subtypes in pheasants (Phasianus colchicus spp torquatus) in the Czech Republic. VETERINARNI MEDICINA-PRAHA-. 2007 Nov 30;52(11):496.
https://doi.org/10.17221/2063-VETMED
Dipineto L, Gargiulo A, De Luca Bossa LM, Rinaldi L, Borrelli L, Menna LF, Fioretti A. Prevalence of thermotolerant Campylobacter in pheasants (Phasianus colchicus). Avian pathology. 2008 Oct 1;37(5):507-8.
https://doi.org/10.1080/03079450802356987
PMid:18798025
Kovanen S, Rossi M, Pohja-Mykrä M, Nieminen T, Raunio-Saarnisto M, Sauvala M, Fredriksson-Ahomaa M, Hänninen ML, Kivistö R. Population genetics and characterization of Campylobacter jejuni isolates from western jackdaws and game birds in Finland. Applied and Environmental Microbiology. 2019 Feb 15;85(4):e02365-18.
https://doi.org/10.1128/AEM.02365-18
PMid:30552190 PMCid:PMC6365822
Paulsen P, Bauer A, Smulders FJ, editors. Game meat hygiene: Food safety and security. Wageningen Academic Publishers; 2017 Feb 10.
https://doi.org/10.3920/978-90-8686-840-7
Seguino A, Chintoan-Uta C, Smith SH, Shaw DJ. Public health significance of Campylobacter spp colonisation of wild game pheasants (Phasianus colchicus) in Scotland. Food microbiology. 2018 Sep 1;74:163-70.
https://doi.org/10.1016/j.fm.2018.04.002
PMid:29706332
Shakir ZM, Alhatami AO, Ismail Khudhair Y, Muhsen Abdulwahab H. Antibiotic resistance profile and multiple antibiotic resistance index of Campylobacter species isolated from poultry. Archives of Razi Institute. 2021 Dec 1;76(6):1677-86.
Kurinčič M, Berce I, Zorman T, Smole Možina S. The prevalence of multiple antibiotic resistance in Campylobacter spp from retail poultry meat. Food Technology and Biotechnology. 2005 Jun 15;43(2):157-63.
Kittl S, Kuhnert P, Hächler H, Korczak BM. Comparison of genotypes and antibiotic resistance of Campylobacter jejuni isolated from humans and slaughtered chickens in Switzerland. Journal of applied microbiology. 2011 Feb 1;110(2):513-20.
https://doi.org/10.1111/j.1365-2672.2010.04906.x
PMid:21143711
Agbankpe AJ, Kougblenou SD, Dougnon TV, Oussou A, Gbotche E, Koudokpon CH, Legba BB, Baba-Moussa L, Bankole HS. Prevalence and Antimicrobial Resistance of Campylobacter coli and Campylobacter jejuni Isolated from Pig Guts, Pig Feces, and Surface Swabs from the Cutting Tables at Slaughterhouse and Taverns in Southern Benin. International Journal of Microbiology. 2022;2022(1):5120678.
https://doi.org/10.1155/2022/5120678
PMid:36212611 PMCid:PMC9536969
Rahimi E, Ameri M. Antimicrobial resistance patterns of Campylobacter spp isolated from raw chicken, turkey, quail, partridge, and ostrich meat in Iran. Food Control. 2011 Aug 1;22(8):1165-70.
https://doi.org/10.1016/j.foodcont.2011.01.010
Di Francesco A, Salvatore D, Bertelloni F, Ebani VV. Tetracycline resistance genes in wild birds from a wildlife recovery centre in Central Italy. Animals. 2022 Dec 24;13(1):76.
https://doi.org/10.3390/ani13010076
PMid:36611686 PMCid:PMC9817859
Andrzejewska M, Szczepańska B, Śpica D, Klawe JJ. Trends in the occurrence and characteristics of Campylobacter jejuni and Campylobacter coli isolates from poultry meat in Northern Poland. Food Control. 2015 May 1;51:190-4.
https://doi.org/10.1016/j.foodcont.2014.11.014
Chen X, Naren GW, Wu CM, Wang Y, Dai L, Xia LN, Luo PJ, Zhang Q, Shen JZ. Prevalence and antimicrobial resistance of Campylobacter isolates in broilers from China. Veterinary microbiology. 2010 Jul 29;144(1-2):133-9.
https://doi.org/10.1016/j.vetmic.2009.12.035
PMid:20116182
Kovaļenko K, Roasto M, Šantare S, Bērziņš A, Hörman A. Campylobacter species and their antimicrobial resistance in Latvian broiler chicken production. Food Control. 2014 Dec 1;46:86-90.
https://doi.org/10.1016/j.foodcont.2014.05.009
Adzitey F, Rusul G, Huda N, Cogan T, Corry J. Prevalence, antibiotic resistance and RAPD typing of Campylobacter species isolated from ducks, their rearing and processing environments in Penang, Malaysia. International journal of food microbiology. 2012 Mar 15;154(3):197-205.
https://doi.org/10.1016/j.ijfoodmicro.2012.01.006
PMid:22285201
Zendehbad B, Arian AA, Alipour A. Identification and antimicrobial resistance of Campylobacter species isolated from poultry meat in Khorasan province, Iran. Food Control. 2013 Aug 1;32(2):724-7.
https://doi.org/10.1016/j.foodcont.2013.01.035
Gharbi M, Béjaoui A, Hamda CB, Ghedira K, Ghram A, Maaroufi A. Distribution of virulence and antibiotic resistance genes in Campylobacter jejuni and Campylobacter coli isolated from broiler chickens in Tunisia. Journal of Microbiology, Immunology and Infection. 2022 Dec 1;55(6):1273-82.
https://doi.org/10.1016/j.jmii.2021.07.001
PMid:34340908
Gharbi M, Kamoun S, Hkimi C, Ghedira K, Béjaoui A, Maaroufi A. Relationships between virulence genes and antibiotic resistance phenotypes/genotypes in Campylobacter spp isolated from layer hens and eggs in the north of Tunisia: Statistical and computational insights. Foods. 2022 Nov 8;11(22):3554.
https://doi.org/10.3390/foods11223554
PMid:36429146 PMCid:PMC9689815
Hull DM, Harrell E, van Vliet AH, Correa M, Thakur S. Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018-2019. PloS one. 2021 Feb 11;16(2):e0246571.
https://doi.org/10.1371/journal.pone.0246571
PMid:33571292 PMCid:PMC7877606
Du Y, Wang C, Ye Y, Liu Y, Wang A, Li Y, Zhou X, Pan H, Zhang J, Xu X. Molecular identification of multidrug-resistant Campylobacter species from diarrheal patients and poultry meat in Shanghai, China. Frontiers in microbiology. 2018 Jul 31;9:1642.
https://doi.org/10.3389/fmicb.2018.01642
PMid:30108555 PMCid:PMC6079250
Laconi A, Tolosi R, Drigo I, Bano L, Piccirillo A. Association between ability to form biofilm and virulence factors of poultry extra-intestinal Campylobacter jejuni and Campylobacter coli. Veterinary Microbiology. 2023 Jul 1;282:109770.
https://doi.org/10.1016/j.vetmic.2023.109770
PMid:37150060
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Galen Medical Journal
This work is licensed under a Creative Commons Attribution 4.0 International License.
