Campylobacter Contamination in Retail Poultry Meats and By-Products in the World: A Literature Survey

SUZUKI, Hodaka; YAMAMOTO, Shigeki

doi:10.1292/jvms.71.255

Cited by 158Salmonella and Campylobacter epidemiologyListeria monocytogenes in Food SafetyFood Safety and Hygiene

Campylobacter Contamination in Retail Poultry Meats and By-Products in the World: A Literature Survey

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SUZUKI, Hodaka, YAMAMOTO, Shigeki·2009·Journal of Veterinary Medical Science

DOI 10.1292/jvms.71.255

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Abstract

Campylobacter species are common bacterial pathogens associated with human gastroenteritis worldwide. In North America, Europe and Japan, campylobacteriosis is one of the leading food-borne bacterial illnesses and the consumption of poultry meats and/or by-products is suspected a major cause of the illness. In this survey, we summarized the research papers describing Campylobacter contamination of retail poultry meats and by-products in various countries of the world. In most of the countries, a majority of retail poultry meats and by-products were contaminated with Campylobacter spp. C. jejuni was usually the dominant Campylobacter species isolated from retail poultry and C. coli was less frequently isolated, although the ratio of C. coli to C. jejuni was considerably different among the countries. However, in Thailand and South Africa, C. coli was the dominant Campylobacter species isolated from retail poultry. A large portion of retail poultry was contaminated with Campylobacter spp. in the world; therefore, further trials are required for finding proper countermeasures and attention should be paid for the sanitary handling of poultry products.

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Chicken ingredients might be considered likely sources of Campylobacter given the well-documented high prevalence of carcass contamination.
“Chicken ingredients might be considered likely sources of Campylobacter given the well‐documented high prevalence of carcass contamination (Suzuki & Yamamoto 2009, Gonçalves‐Tenório et al. 2018)”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Suzuki & Yamamoto 2009

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BackgroundInfluential
Raw diets for dogs and cats: a review, with particular reference to microbiological hazards.
Davies, R. H., Lawes, J. R., & Wales, A. D. (2019) · Journal of Small Animal Practice · doi:10.1111/jsap.13000 · Cited by 195 · see citing works
“Chicken ingredients might be considered likely sources of Campylobacter given the well-documented high prevalence of carcass contamination (Suzuki & Yamamoto 2009, GonçalvesTenório et al. 2018).”
Background
Prevalence and characterization of Campylobacter jejuni from chicken meat sold in French retail outlets
Guyard‐Nicodème, M., Rivoal, K., Houard, E., Rose, V., Quesne, S., Mourand, G., Rouxel, S., Kempf, I., Guillier, L., Gauchard, F., et al. (2015) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2015.02.013 · Cited by 100 · see citing works
Infection, colonization and shedding of Campylobacter and Salmonella in animals and their contribution to human disease: A review
Rukambile, E. J., Sintchenko, V., Muscatello, G., Kock, R. A., & Alders, R. (2019) · Zoonoses and Public Health · doi:10.1111/zph.12611 · Cited by 100 · see citing works
“Isolation of Campylobacter and Salmonella is common in animal‐source food products including poultry meat (Anihouvi et al., 2013; Bertasi et al., 2016; Inns et al., 2015; Suzuki & Yamamoto, 2009; Trongjit et al., 2017).”
Background
Review of current methodologies to isolate and identify Campylobacter spp. from foods
Gharst, G. A., Oyarzábal, O. A., & Hussain, S. K. (2013) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2013.07.014 · Cited by 92 · see citing works
“coli are the only species found in commercial chicken production worldwide (He et al., 2010; Oyarzabal et al., 1997; Suzuki and Yamamoto, 2009).”
Poultry consumers' behaviour, risk perception and knowledge related to campylobacteriosis and domestic food safety
Bearth, A., Cousin, M., & Siegrist, M. (2014) · Food Control · doi:10.1016/j.foodcont.2014.03.055 · Cited by 77 · see citing works
Lactobacillus gasseri SBT2055 Reduces Infection by and Colonization of Campylobacter jejuni
Nishiyama, K., Seto, Y., Yoshioka, K., Kakuda, T., Takaı̈, S., Yamamoto, Y., & Mukai, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108827 · Cited by 77 · see citing works
“prevalence of over 60% [9].”
Inhibition of Campylobacter jejuni on fresh chicken breasts by κ-carrageenan/chitosan-based coatings containing allyl isothiocyanate or deodorized oriental mustard extract
Olaimat, A. N., Fang, Y., & Holley, R. A. (2014) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2014.07.003 · Cited by 75 · see citing works
Prevalence, quantification and antimicrobial resistance of Campylobacter spp. on chicken neck-skins at points of slaughter in 5 major cities located on 4 continents
Garin, B., Gouali, M., Wouafo, M., Perchec, A.-M., Thu, P. M., Ravaonindrina, N., Urbès, F., Gay, M., Diawara, A., Leclercq, A., et al. (2012) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2012.04.020 · Cited by 75 · see citing works
Reduction of Campylobacter jejuni by natural antimicrobials in chicken meat-related conditions
Piskernik, S., Klančnik, A., Riedel, C. T., Brøndsted, L., & Možina, S. S. (2010) · Food Control · doi:10.1016/j.foodcont.2010.11.002 · Cited by 69 · see citing works
Tracing Campylobacter jejuni strains along the poultry meat production chain from farm to retail by pulsed-field gel electrophoresis, and the antimicrobial resistance of isolates
Melero, B., Juntunen, P., Hänninen, M., Jaime, I., & Rovira, J. (2012) · Food Microbiology · doi:10.1016/j.fm.2012.04.020 · Cited by 67 · see citing works
Antibiotic Resistance in Campylobacter: A Systematic Review of South American Isolates
Portes, A. B., Panzenhagen, P., dos Santos, A. M. P., & Conte‐Júnior, C. A. (2023) · Antibiotics · doi:10.3390/antibiotics12030548 · Cited by 69 · see citing works
Campylobacter, a zoonotic pathogen of global importance: Prevalence and risk factors in the fast-evolving chicken meat system of Nairobi, Kenya
Carron, M., Chang, Y., Momanyi, K., Akoko, J. M., Kiiru, J., Bettridge, J., Chaloner, G. L., Rushton, J., O’Brien, S. J., Williams, N. J., et al. (2018) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0006658 · Cited by 65 · see citing works
Epidemiology of antimicrobial resistant Campylobacter spp. isolated from retail meats in Canada
Narváez-Bravo, C. A., Taboada, E. N., Mutschall, S. K., & Aslam, M. (2017) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2017.04.019 · Cited by 64 · see citing works
Antibiotic resistance in Campylobacter jejuni and Campylobacter coli isolated from food in Poland
Maćkiw, E., Korsak, D., Rzewuska, K., Tomczuk, K., & Rozynek, E. (2011) · Food Control · doi:10.1016/j.foodcont.2011.08.022 · Cited by 62 · see citing works
Genetic diversity in Campylobacter jejuni is associated with differential colonization of broiler chickens and C57BL/6J IL10-deficient mice
Wilson, D. L., Rathinam, V. A. K., Qi, W., Wick, L. M., Landgraf, J., Bell, J. A., Plovanich‐Jones, A. E., Parrish, J. R., Finley, R. L., Mansfield, L. S., et al. (2010) · Microbiology · doi:10.1099/mic.0.035717-0 · Cited by 60 · see citing works
“The prevalence of C. jejuni in commercial broiler flocks has been well documented in Europe, Australia and the USA (reviewed by Humphrey et al., 2007; Horrocks et al., 2009; Suzuki & Yamamoto, 2009).”
Background
Campylobacter jejuni biofilm cells become viable but non-culturable (VBNC) in low nutrient conditions at 4 °C more quickly than their planktonic counterparts
Magajna, B., & Schraft, H. (2014) · Food Control · doi:10.1016/j.foodcont.2014.08.022 · Cited by 60 · see citing works
Characterization of Antimicrobial Resistance Patterns and Detection of Virulence Genes in Campylobacter Isolates in Italy
Giannatale, E. D., Serafino, G. D., Zilli, K., Alessiani, A., Sacchini, L., Garofolo, G., Aprea, G., & Marotta, F. (2014) · Sensors · doi:10.3390/s140203308 · Cited by 58 · see citing works
“Campylobacter is among the major causes of food-borne illness worldwide [1].”
Background
Campylobacter and its multi-resistance in the food chain
Možina, S. S., Kurinčič, M., Klančnik, A., & Mavri, A. (2010) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2010.09.003 · Cited by 57 · see citing works
Campylobacters and their bacteriophages from chicken liver: The prospect for phage biocontrol
Firlieyanti, A. S., Connerton, P. L., & Connerton, I. F. (2016) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2016.08.026 · Cited by 57 · see citing works
Prevalence and Antibiotic Resistance Patterns ofCampylobacterspp. Isolated from Broiler Chickens in the North of Tunisia
Gharbi, M., Béjaoui, A., Hamda, C. B., Jouini, A., Ghedira, K., Zrelli, C., Hamrouni, S., Aouadhi, C., Bessoussa, G., Ghram, A., et al. (2018) · BioMed Research International · doi:10.1155/2018/7943786 · Cited by 56 · see citing works
“Transmission of Campylobacter to humans occurs mainly through consumption of contaminated raw/undercooked poultry products, or through close contact with infected animals [7, 8].”
Background
Reduction of Listeria monocytogenes on chicken breasts by combined treatment with UV-C light and bacteriophage ListShield
Yang, S., Sadekuzzaman, M., & Ha, S. (2017) · LWT · doi:10.1016/j.lwt.2017.07.060 · Cited by 54 · see citing works
Pentavalent Single-Domain Antibodies Reduce Campylobacter jejuni Motility and Colonization in Chickens
Riazi, A., Strong, P. C. R., Coleman, R., Chen, W., Hirama, T., van Faassen, H., Henry, M., Logan, S. M., Szymanski, C. M., MacKenzie, R., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083928 · Cited by 51 · see citing works
Transmission of Bacterial Zoonotic Pathogens between Pets and Humans: The Role of Pet Food
Lambertini, E., Buchanan, R. L., Narrod, C., & Pradhan, A. K. (2015) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2014.902356 · Cited by 51 · see citing works
“Suzuki and Yamamoto, 2009a E. coli Carcasses or portions at retail Australia 59.6–100% Whole birds: 85.7–100% (14–28 samples); chicken portions: 59.6–90.1% (141–252 samples).”
BackgroundInfluential
Population Diversity ofCampylobacter jejuniin Poultry and Its Dynamic of Contamination in Chicken Meat
Marotta, F., Garofolo, G., Donato, G. D., Aprea, G., Platone, I., Cianciavicchia, S., Alessiani, A., & Giannatale, E. D. (2015) · BioMed Research International · doi:10.1155/2015/859845 · Cited by 50 · see citing works
“Recent studies have reported that the prevalence of Campylobacter in retail chicken products ranges from 90 to 100% across several countries [11, 12].”
Background
Campylobacter species in animal, food, and environmental sources, and relevant testing programs in Canada
Huang, H., Brooks, B. W., Lowman, R., & Carrillo, C. D. (2015) · Canadian Journal of Microbiology · doi:10.1139/cjm-2014-0770 · Cited by 50 · see citing works
Prevalence and quantification of thermophilic Campylobacter spp. in Italian retail poultry meat: Analysis of influencing factors
Stella, S., Soncini, G., Ziino, G., Panebianco, A., Pedonese, F., Nuvoloni, R., Giannatale, E. D., Colavita, G., Alberghini, L., & Giaccone, V. (2016) · Food Microbiology · doi:10.1016/j.fm.2016.10.028 · Cited by 50 · see citing works
“%) are sometimes detected, and the presence of some heavily contaminated (>104 CFU/g) meat cuts and preparations have been reported by several authors (Humphrey et al., 2007; Suzuki and Yamamoto, 2009; Uyttendaele et al., 2006).”
BackgroundInfluential
Prevalence of Campylobacter spp. in skinless, boneless retail broiler meat from 2005 through 2011 in Alabama, USA
Williams, A., & Oyarzábal, O. A. (2012) · BMC Microbiology · doi:10.1186/1471-2180-12-184 · Cited by 49 · see citing works
“The prevalence among different countries varies from as low as 25% in Switzerland to as high as 100% in the Czech Republic [31,33,34].”
BackgroundResult
Current Status of Campylobacter Food Poisoning in Japan
Vetchapitak, T., & Misawa, N. (2019) · Food Safety · doi:10.14252/foodsafetyfscj.d-19-00001 · Cited by 49 · see citing works
Prevalence and pattern of antibiotic resistance of Campylobacter spp. in poultry meat in Southern Italy
Nobile, C. G. A., Costantino, R., Bianco, A., Pileggi, C., & Pavía, M. (2013) · Food Control · doi:10.1016/j.foodcont.2013.02.011 · Cited by 48 · see citing works
Immunogenicity and protective efficacy of mucosal delivery of recombinant hcp of Campylobacter jejuni Type VI secretion system (T6SS) in chickens
Singh, A., Nisaa, K., Bhattacharyya, S., & Mallick, A. I. (2019) · Molecular Immunology · doi:10.1016/j.molimm.2019.04.016 · Cited by 47 · see citing works
Ultraviolet-C Radiation on the Fresh Chicken Breast: Inactivation of Major Foodborne Viruses and Changes in Physicochemical and Sensory Qualities of Product
Park, S. Y., & Ha, S. (2014) · Food and Bioprocess Technology · doi:10.1007/s11947-014-1452-1 · Cited by 46 · see citing works
Investigation of the Role of Campylobacter Infection in Suspected Acute Polyradiculoneuritis in Dogs
Martinez‐Anton, L., Marenda, M. S., Firestone, S. M., Bushell, R. N., Child, G., Hamilton, A. I., Long, S., & Chevoir, M. L. (2018) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.15030 · Cited by 46 · see citing works
A Genome-Wide Association Study to Identify Diagnostic Markers for Human Pathogenic Campylobacter jejuni Strains
Buchanan, C. J., Webb, A. L., Mutschall, S. K., Kruczkiewicz, P., Barker, D. O. R., Hetman, B. M., Gannon, V. P. J., Abbott, D. W., Thomas, J. E., Inglis, G. D., et al. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01224 · Cited by 44 · see citing works
“This bacterium is highly prevalent in raw poultry meat and poultry by-products (Suzuki and Yamamoto, 2009; Williams and Oyarzabal, 2012), and the consumption and handling of contaminated poultry products is thought to be the primary source of exposure leading to human infection.”
Background
The Virulence Factor PEB4 (Cj0596) and the Periplasmic Protein Cj1289 Are Two Structurally Related SurA-like Chaperones in the Human Pathogen Campylobacter jejuni
Kale, A., Phansopa, C., Suwannachart, C., Craven, C. J., Rafferty, J. B., & Kelly, D. J. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.220442 · Cited by 43 · see citing works
Monitoring Campylobacter in the poultry production chain — From culture to genes and beyond
Josefsen, M. H., Bhunia, A. K., Engvall, E. O., Fachmann, M. S. R., & Hoorfar, J. (2015) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2015.03.007 · Cited by 42 · see citing works
“Worldwide, although the prevalence varies among countries, a literature survey by Suzuki and Yamamoto (2009) shows an average prevalence in retail poultry meat of 60%.”
Background
Multiple contaminations of chickens with Campylobacter, Escherichia coli and Salmonella in Yaounde (Cameroon)
Nzouankeu, A., Ngandjio, A., Ejenguele, G., Njiné, T., & Wouafo, M. (2010) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.1019 · Cited by 40 · see citing works
“jejuni was the most frequent Campylobacter in poultry [18].”
Background
Campylobacter species occurrence within internal organs and tissues of commercial caged Leghorn laying hens
Cox, N. A., Richardson, L. J., Buhr, R. J., & Fedorka–Cray, P. J. (2009) · Poultry Science · doi:10.3382/ps.2009-00195 · Cited by 38 · see citing works
Reducing Campylobacter jejuni colonization in broiler chickens by in-feed supplementation with hyperimmune egg yolk antibodies
Vandeputte, J., Martel, A., Canessa, S., Rysselberghe, N. V., Zutter, L. D., Heyndrickx, M., Haesebrouck, F., Pasmans, F., & Garmyn, A. (2019) · Scientific Reports · doi:10.1038/s41598-019-45380-z · Cited by 37 · see citing works
Prevalence and Characteristics of Salmonella and Campylobacter in Retail Poultry Meat in Japan
Furukawa, I., Ishihara, T., Teranishi, H., Saito, S., Yatsuyanagi, J., Wada, E., Kumagai, Y., Takahashi, S., Konno, T., Kashio, H., et al. (2016) · Japanese Journal of Infectious Diseases · doi:10.7883/yoken.jjid.2016.164 · Cited by 37 · see citing works
Prevalence, antibiotic resistance and genotypes of Campylobacter jejuni and Campylobacter coli isolated from chickens in Irbid governorate, Jordan
Alaboudi, A. R., Malkawi, I. M., Osaili, T. M. I., Abu‐Basha, E. A., & Guitián, J. (2020) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2020.108656 · Cited by 34 · see citing works
“A review conducted in 2009 suggests that in most countries, in which studies have been conducted, a majority of poultry products on retail are contaminated with Campylobacter (Suzuki and Yamamoto, 2009).”
Background
Low contamination of Campylobacter spp. on chicken carcasses in Minas Gerais state, Brazil: Molecular characterization and antimicrobial resistance
Húngaro, H. M., Mendonça, R. C. S., Rosa, V. O., Badaró, A. C. L., Moreira, M. A. S., & Chaves, J. B. P. (2014) · Food Control · doi:10.1016/j.foodcont.2014.11.001 · Cited by 34 · see citing works
“A world literature survey showed that about 58% of chicken carcasses and by-products are contaminated by Campylobacter spp., but greatvariations in thefindingswereobserved (Suzuki & Yamamoto, 2009).”
Background
Tethered DNA scaffolds on optical sensor platforms for detection of hipO gene from Campylobacter jejuni
Gnanaprakasa, T. J., Oyarzábal, O. A., Olsen, E. V., Pedrosa, V. A., & Simonian, A. L. (2011) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2011.04.037 · Cited by 34 · see citing works
“Campylobacter jejuni is a significant cause of human bacterial gastroenteritis [1] [2] [3] and can be acquired from contact with farm animals or ingestion of contaminated poultry products, raw milk or water.”
The prevalence, counts, and MLST genotypes of Campylobacter in poultry meat and genomic comparison with clinical isolates
Tedersoo, T., Roasto, M., Mäesaar, M., Kisand, V., Ivanova, M., & Meremäe, K. (2022) · Poultry Science · doi:10.1016/j.psj.2022.101703 · Cited by 33 · see citing works
Prevalence and counts of Campylobacter spp. in poultry meat at retail level in Estonia
Mäesaar, M., Praakle, K., Meremäe, K., Kramarenko, T., Sõgel, J., Viltrop, A., Muutra, K., Kovaļenko, K., Matt, D., Hörman, A., et al. (2014) · Food Control · doi:10.1016/j.foodcont.2014.03.044 · Cited by 32 · see citing works
“A worldwide literature survey has showed that about 58% of chickens are contaminated with Campylobacter (Suzuki & Yamamoto, 2009).”
Background
Prevalence and risk factors for thermotolerant species of Campylobacter in poultry meat at retail in Europe
Osimani, A., Aquilanti, L., Pasquini, M., & Clementi, F. (2017) · Poultry Science · doi:10.3382/ps/pex143 · Cited by 32 · see citing works
“The present survey ideally follows the review published by Suzuki and Yamamoto (2009) on Campylobacter contamination in retail poultry meat and byproducts in the world.”
Background
Prevalence and antimicrobial susceptibility of Campylobacter isolated from retail chickens in Thailand
Wangroongsarb, P., Cheunban, N., Jittaprasatsin, C., Kamthalang, T., Saipradit, N., Chaichana, P., Pulsrikarn, C., Parnmen, S., & Sripichai, O. (2020) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2020.109017 · Cited by 33 · see citing works
Effect of crust freezing applied alone and in combination with ultraviolet light on the survival of Campylobacter on raw chicken
Haughton, P. N., Lyng, J. G., Cronin, D. A., Fanning, S., & Whyte, P. (2012) · Food Microbiology · doi:10.1016/j.fm.2012.05.004 · Cited by 32 · see citing works
“Campylobacter jejuni is the leading cause of human gastroenteritis worldwide and chicken meat is recognized as a significant source of infection (Suzuki and Yamamoto, 2009; Zilbauer et al., 2008).”
Background
Influence of measurement and control of microaerobic gaseous atmospheres in methods for Campylobacter growth studies
Macé, S., Haddad, N., Zagorec, M., & Tresse, O. (2015) · Food Microbiology · doi:10.1016/j.fm.2015.07.014 · Cited by 30 · see citing works
“least 50% of poultry meats were positive for Campylobacter (Suzuki and Yamamoto, 2009).”
Background
Prevalence of putative virulence markers inCampylobacter jejuniandCampylobacter coliisolated from hospitalized children, raw chicken, and raw beef in Tehran, Iran
Hamidian, M., Sanaei, M., Bolfion, M., Dabiri, H., Zali, M. R., & Walther‐Rasmussen, J. (2011) · Canadian Journal of Microbiology · doi:10.1139/w10-089 · Cited by 29 · see citing works
“coli has also been reported in other investigations (Rozynek et al. 2005; Suzuki and Yamamoto 2009; Rahimi et al. 2010; Thakur et al. 2010).”
Result
Isolation, identification, and antimicrobial susceptibility pattern of Campylobacter jejuni and Campylobacter coli from cattle, goat, and chicken meats in Mekelle, Ethiopia
Hagos, Y., Gugsa, G., Awol, N., Ahmed, M., Tsegaye, Y., Abebe, N., & Bsrat, A. (2021) · PLoS ONE · doi:10.1371/journal.pone.0246755 · Cited by 29 · see citing works
Antimicrobial Resistance Profiles of Campylobacter spp. Isolated from Broiler Chicken Meat of Estonian, Latvian and Lithuanian Origin at Estonian Retail Level and from Patients with Severe Enteric Infections in Estonia
Mäesaar, M., Kramarenko, T., Meremäe, K., Sõgel, J., Lillenberg, M., Häkkinen, L., Ivanova, M., Kovaļenko, K., Hörman, A., Hänninen, M., et al. (2015) · Zoonoses and Public Health · doi:10.1111/zph.12208 · Cited by 27 · see citing works
“According to the data of Suzuki and Yamamoto (2009), 58% of chickens are contaminated by Campylobacter spp.”
Result
Prevalence of potentially neuropathic Campylobacter jejuni strains on commercial broiler chicken products
Hardy, C. G., Lackey, L. G., Cannon, J., Price, L. B., & Silbergeld, E. K. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.12.027 · Cited by 27 · see citing works
Prevalence of thermotolerant Campylobacter spp. in broilers at retail in the Czech Republic and their antibiotic resistance
Bardoň, J., Kolář, M., Karpíšková, R., & Hricová, K. (2010) · Food Control · doi:10.1016/j.foodcont.2010.08.001 · Cited by 27 · see citing works
A strategy for trade monitoring and substitution of the organs of threatened animals
Luo, J., Yan, D., Song, J., Zhang, D., Xing, X., Han, Y., Yang, M., Dong, X., Peng, C. Y., Chen, S., et al. (2013) · Scientific Reports · doi:10.1038/srep03108 · Cited by 26 · see citing works
Prevalence and antimicrobial resistance of Campylobacter isolated from carcasses of chickens slaughtered in Poland – a retrospective study
Wieczorek, K., Bocian, Ł., & Osek, J. (2020) · Food Control · doi:10.1016/j.foodcont.2020.107159 · Cited by 24 · see citing works
Metabolome and Microbiota Analysis Reveals the Conducive Effect of Pediococcus acidilactici BCC-1 and Xylan Oligosaccharides on Broiler Chickens
Wu, Y., Lei, Z., Wang, Y., Yin, D., Aggrey, S. E., Guo, Y., & Yuan, J. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.683905 · Cited by 22 · see citing works
Prevalence, strain identification and antimicrobial resistance of Campylobacter spp. isolated from slaughtered pig carcasses in Brazil
Biasi, R., de Macedo, R. E. F., Malaquias, M. A. S., & Franchin, P. R. (2010) · Food Control · doi:10.1016/j.foodcont.2010.10.005 · Cited by 22 · see citing works
Comparison of 2 types of broths and 3 selective agars for the detection of Campylobacter species in whole-chicken carcass-rinse samples
Chon, J., Hyeon, J., Park, J.-H., Song, K., & Seo, K. (2012) · Poultry Science · doi:10.3382/ps.2011-01980 · Cited by 22 · see citing works
“Bolton broth, a Campylobacter selective enrichment broth, is a selective enrichment medium commonly used by many food authorities (Line, 2006; Odongo et al., 2009; Suzuki and Yamamoto, 2009).”
Background
Campylobacter jejuni Strains Associated with Wild Birds and Those Causing Human Disease in Six High-Use Recreational Waterways in New Zealand
Shrestha, R., Midwinter, A. C., Marshall, J. C., Collins-Emerson, J. M., Pleydell, E. J., & French, N. P. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.01228-19 · Cited by 21 · see citing works
Loads and antimicrobial resistance of Campylobacter spp. on fresh chicken meat in Nueva Ecija, Philippines
Sison, F. B., Chaisowwong, W., Alter, T., Tiwananthagorn, S., Pichpol, D., Lampang, K. N., Baumann, M., & Gölz, G. (2014) · Poultry Science · doi:10.3382/ps.2013-03791 · Cited by 21 · see citing works
Isolation and Identification of Campylobacter spp. from Poultry and Poultry By-Products in Tunisia by Conventional Culture Method and Multiplex Real-Time PCR
Jribi, H., Sellami, H., Siala, M., Smaoui, S., Ghorbel, A., Hachicha, S., Bénéjat, L., Messadi-Akrout, F., Mégraud, F., & Gdoura, R. (2017) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-16-321 · Cited by 21 · see citing works
Prevalence of Thermotolerant Campylobacter spp. in Chicken Meat in Croatia and Multilocus Sequence Typing of a Small Subset of Campylobacter jejuni and Campylobacter coli Isolates
Mikulić, M., Humski, A., Njari, B., Ostović, M., Duvnjak, S., & Cvetnić, Ž. (2016) · Food Technology and Biotechnology · doi:10.17113/ftb.54.04.16.4647 · Cited by 21 · see citing works
“Using data from the available literature on the prevalence of Campylobacter spp. in retail poultry meat, Suzuki and Yamamoto (20) provided a review of Campylobacter spp. prevalence in fresh poultry meat across the world (in %): North America 63.8, Central and South America 82.3, Europe 53.3, Africa 73.1, Asia 60.3, Oc…”
BackgroundInfluential
Campylobacteriosis: A rising threat in foodborne illnesses
Khairullah, A. R., Yanestria, S. M., Effendi, M. H., Moses, I. B., Kusala, M. K. J., Fauzia, K. A., Ayuti, S. R., Fauziah, I., Silaen, O. S. M., Riwu, K. H. P., et al. (2024) · Open Veterinary Journal · doi:10.5455/ovj.2024.v14.i8.1 · Cited by 20 · see citing works
“Poultry meat from laying hens, turkeys, ostriches, ducks, and broilers is frequently consumed (Suzuki and Yamamoto, 2009).”
Background
Characterization and Application of Lytic Bacteriophages against Campylobacter jejuni Isolated from Poultry in Japan
FURUTA, M., Nasu, T., 梅木, 晃., Minh, D. H., Honjoh, K., & Miyamoto, T. (2017) · Biocontrol Science · doi:10.4265/bio.22.213 · Cited by 20 · see citing works
Occurrence and antimicrobial resistance of Campylobacter jejuni isolates from poultry in Casablanca-Settat, Morocco
Es-soucratti, K., Hammoumi, A., Bouchrif, B., ASMAI, R., En-nassiri, H., & Karraouan, B. (2020) · Italian Journal of Food Safety · doi:10.4081/ijfs.2020.8692 · Cited by 20 · see citing works
Chlorine Induces Physiological and Morphological Changes on Chicken Meat Campylobacter Isolates
Weerasooriya, G., McWhorter, A. R., & Chousalkar, K. K. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00503 · Cited by 19 · see citing works
“A recent review revealed that depending on geographical location, between 19–100% of post-production poultry meat products can be contaminated with Campylobacter (Suzuki and Yamamoto, 2009).”
Background
Rapid Detection of Campylobacter jejuni, Campylobacter coli, and Campylobacter lari in Fresh Chicken Meat and By-Products in Bangkok, Thailand, Using Modified Multiplex PCR
Saiyudthong, S., Phusri, K., & Buates, S. (2015) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-14-415 · Cited by 19 · see citing works
Improved protocol for isolation of Campylobacter spp. from retail broiler meat and use of pulsed field gel electrophoresis for the typing of isolates
Oyarzábal, O. A., Williams, A., Zhou, P., & Samadpour, M. (2013) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2013.03.008 · Cited by 19 · see citing works
“Using the reference method as described in this publication, a consistently larger proportion of positive samples have been reported for thighs and a lower proportion of positive sample has been reported for tenderloins (Oyarzabal and Liu, 2010; Oyarzabal et al., 2007; Suzuki and Yamamoto, 2009; Williams and Oyarzabal…”
Method
Occurrence of Campylobacter spp. in poultry meat at retail and processing plants’ levels in Central Italy
Mezher, Z., Saccares, S., Marcianò, R., Santis, P. D., Rodas, E. M. F., Angelis, V. D., & Condoleo, R. (2016) · Italian Journal of Food Safety · doi:10.4081/ijfs.2016.5495 · Cited by 18 · see citing works
Impact of humanCampylobacterinfections in Southeast Asia: The contribution of the poultry sector
Premarathne, J. M. K. J. K., Satharasinghe, D. A., Huat, J. T. Y., Basri, D. F., Rukayadi, Y., Nakaguchi, Y., Nishibuchi, M., & Radu, S. (2016) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2016.1266297 · Cited by 18 · see citing works
“in poultry meat were reported to be as low as 25% and as high as 100% in Switzerland and the Czech Republic, respectively (Ledergerber et al., 2003; Suzuki and Yamamoto, 2009).”
Background
Antibiotic Susceptibility, Genetic Diversity, and the Presence of Toxin Producing Genes in Campylobacter Isolates from Poultry
Lee, J., Jeong, J., Lee, H., Ha, J., Kim, S., Choi, Y., Oh, H., Seo, K., Yoon, Y., & Lee, S. (2017) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14111400 · Cited by 18 · see citing works
Sensitive detection of Campylobacter jejuni using one-step strategy based on functional nanospheres of immunomagnetic capture and quantum dots
He, K., Zhang, X., Chen, L., Zhao, R., & Wang, L. (2018) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.07.050 · Cited by 17 · see citing works
Association of Campylobacter spp. levels between chicken grow-out environmental samples and processed carcasses
Schroeder, M., Eifert, J. D., Ponder, M. A., & Schmale, D. G. (2014) · Poultry Science · doi:10.3382/ps.2013-03646 · Cited by 17 · see citing works
“5% of retail poultry meats in the United States (Suzuki and Yamamoto, 2009).”
Background
Use of Electron Beams in Food Preservation
Bhat, R., Alias, A. K., & Paliyath, G. (2012) · doi:10.1002/9781119962045.ch17 · Cited by 17 · see citing works
Distribution and Molecular Characterization of Campylobacter Species at Different Processing Stages in Two Poultry Processing Plants
Lee, S., Park, H.-J., Lee, J., Lim, J.-S., Seo, K., Heo, E., Kim, Y., Wee, S., & Moon, J. (2017) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2016.2218 · Cited by 16 · see citing works
“An estimated 20–40% of human Campylobacter infections are linked to the cross-contamination during processing or consumption of under-cooked chicken products (Friedman et al. , 2004; Humphrey et al. , 2007; Suzuki and Yamamoto, 2009; EFSA, 2010).”
Occurrence of Campylobacter spp. in Poultry and Poultry Products for Sale on the Polish Retail Market
Maćkiw, E., Rzewuska, K., Stos, K., Jarosz, M., & Korsak, D. (2011) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-10-503 · Cited by 15 · see citing works
Detection of Campylobacter DNA using magnetic nanoparticles coupled with PCR and a colorimetric end-point system
Jansaento, W., Jangpatarapongsa, K., Polpanich, D., & Wonglumsom, W. (2016) · Food Science and Biotechnology · doi:10.1007/s10068-016-0029-3 · Cited by 14 · see citing works
Identification and differentiation of Campylobacter isolated from chicken meat using real-time polymerase chain reaction and high resolution melting analysis of hipO and glyA genes
Syarifah, I. K., Latif, H., Basri, C., & Rahayu, P. (2020) · Veterinary World · doi:10.14202/vetworld.2020.1875-1883 · Cited by 14 · see citing works
“The melt peak temperature for isolate JKT-1 was 78.7°C, while the positive control for C. coli was 78.4°C. Veterinary World, EISSN: 2231-0916 1882 Resource Development Ministry of Agriculture and the Quality Control Laboratory and Certification of Animal Products (QCLCAP/BPMSPH) Bogor of the Ministry of Agriculture (g…”
BackgroundInfluential
Detection and Genotyping of Campylobacter jejuni and Campylobacter coli by Use of DNA Oligonucleotide Arrays
Marotta, F., Zilli, K., Tonelli, A., Sacchini, L., Alessiani, A., Migliorati, G., & Giannatale, E. D. (2012) · Molecular Biotechnology · doi:10.1007/s12033-012-9512-0 · Cited by 12 · see citing works
“Campylobacter is the most common cause of human acute bacterial food-borne gastroenteritis worldwide [1].”
Background
Surveillance of Shiga toxin-producing Escherichia coli and Campylobacter spp. in wild Japanese deer (Cervus nippon) and boar (Sus scrofa)
TOMINO, Y., Andoh, M., Horiuchi, Y., Jiye, S. H. I. N., Ai, R., NAKAMURA, T., Toda, M., Yonemitsu, K., Takano, A., Shimoda, H., et al. (2020) · Journal of Veterinary Medical Science · doi:10.1292/jvms.19-0265 · Cited by 12 · see citing works
“coli, which are the major species associated with worldwide foodborne bacterial contamination [41], is consistent with previous reports for wild deer and boar.”
Result
Genotypic characterization, antimicrobial susceptibility and virulence determinants of Campylobacter jejuni and Campylobacter coli isolated from pastured poultry farms
Awad, A., Yeh, H., Ramadan, H. H., & Rothrock, M. J. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1271551 · Cited by 12 · see citing works
“Campylobacter contaminates poultry meats prior to or during processing representing a potential health threat to consumers (Suzuki and Yamamoto, 2009).”
Background
Uninvited Guests at the Table – A Consumer Intervention for Safe Poultry Preparation
Bearth, A., Cousin, M., & Siegrist, M. (2013) · Journal of Food Safety · doi:10.1111/jfs.12063 · Cited by 12 · see citing works
Current Evidence on Raw Meat Diets in Pets: A Natural Symbol, but a Nutritional Controversy
Lyu, Y., Wu, C., Li, L., & Pu, J. (2025) · Animals · doi:10.3390/ani15030293 · Cited by 15 · see citing works
“Campylobacter contamination has been noted in RMBDs as well, particularly based on poultry meat and by-products [78,81,82,104–106].”
A culture-based assessment of the microbiota of conventional and free-range chicken meat from Irish processing facilities.
Marmion, M., Soro, A. B., Whyte, P., & Scannell, A. G. M. (2023) · Food Microbiology · doi:10.1016/j.fm.2023.104306 · Cited by 10 · see citing works
Contamination by Meat Juice When Shopping for Packages of Raw Poultry
Chen, F., Godwin, S., Chambers, D. H., Chambers, E., Cates, S. C., Stone, R., & Donelan, A. K. (2018) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-17-467 · Cited by 10 · see citing works
Prevalence of Multidrug-Resistant Foodborne Pathogens and Indicator Bacteria from Edible Offal and Muscle Meats in Nashville, Tennessee
Liu, S., Kilonzo‐Nthenge, A., Nahashon, S. N., Pokharel, B., Mafiz, A. I., & Nzomo, M. (2020) · Foods · doi:10.3390/foods9091190 · Cited by 10 · see citing works
“Suzuki and Yamamoto [56] reported that Campylobacter is frequently associated with the handling and consumption of meat products, especially raw poultry.”
Background
Prevalence of bacterial contamination on wild meat processing and cooking surfaces in rural Cameroon
Soto, S. M., Castellsagués, L., Ballén, V., Gabasa, Y., Mayor, P., Brull, G. R., Funk, S. M., & Fa, J. E. (2025) · One Health · doi:10.1016/j.onehlt.2025.101028 · Cited by 9 · see citing works
“However, studies of bacterial contamination in worldwide poultry and retail poultry products have focused on Campylobacter [33,34].”
Campylobacter: Animal Reservoirs, Human Infections, and Options for Control
Wagenaar, J. A., Newell, D. G., Kalupahana, R. S., & Mughini‐Gras, L. (2023) · Springer eBooks · doi:10.1007/978-3-031-27164-9_6 · Cited by 9 · see citing works
Campylobacter jejuni,Campylobacter coli, and Cytolethal Distending Toxin Genes in Laying Hens
Dipineto, L., Antonio Gargiulo, Russo, T. P., Bossa, L. M. D. L., Borrelli, L., Menna, L. F., & Fioretti, A. (2011) · Avian Diseases · doi:10.1637/9525-091510-resnote.1 · Cited by 9 · see citing works
“In fact, there are many reports in the world describing Campylobacter contamination in retail poultry meats and by-products (17).”
Background
Overview of Foodborne Pathogens
Scannell, A. (2012) · doi:10.1002/9781444355321.ch2 · Cited by 10 · see citing works
Prevalence of Salmonella, Campylobacter, and Shiga Toxin–Producing Escherichia coli on the Surfaces of Raw Poultry Packages
Chen, F., Godwin, S., Green, A., Chowdhury, S., & Stone, R. (2018) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-18-149 · Cited by 8 · see citing works
Campylobacter jejuni Strain Dynamics in a Raccoon (Procyon lotor) Population in Southern Ontario, Canada: High Prevalence and Rapid Subtype Turnover
Mutschall, S. K., Hetman, B. M., Bondo, K. J., Gannon, V. P. J., Jardine, C. M., & Taboada, E. N. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.00027 · Cited by 7 · see citing works
“While Campylobacter is highly prevalent in poultry and poultry meat (7), it is also commonly found in a wide range of animal hosts that not only include livestock such as cattle and swine, but also household pets and wildlife (6, 8).”
Background
Incidence and Antibiotic Resistance Properties of Campylobacter Species Isolated From Poultry Meat
Sabzmeydani, A., Rahimi, E., & Shakerian, A. (2020) · International Journal of Enteric Pathogens · doi:10.34172/ijep.2020.13 · Cited by 7 · see citing works
Distribution and Genotypic Characterization of Campylobacter jejuni Isolated from Poultry in Split and Dalmatia County, Croatia
Kovačić, A., Listeš, I., Vučica, C., Kozačinski, L., Tripković, I., & Šiško‐Kraljević, K. (2012) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2012.01519.x · Cited by 7 · see citing works
“The data range from 10% to even 88% of positive poultry samples (Logue et al., 2003; Davies and Conner, 2007; Suzuki and Yamamoto, 2009; Lyhs et al., 2010).”
BackgroundInfluential
Development of Multiple-Locus Variable-Number Tandem-Repeat Analysis for Molecular Subtyping of Campylobacter jejuni by Using Capillary Electrophoresis
Techaruvichit, P., Takahashi, H., Vesaratchavest, M., Keeratipibul, S., Kuda, T., & Kimura, B. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.01151-15 · Cited by 7 · see citing works
“jejuni, and most of the infections are found to be associated with the handling of raw poultry or eating raw or undercooked poultry meat (4, 5).”
Background
Comparison ofCampylobacter jejunipulsotypes isolated from humans and poultry in Split and Dalmatia County, Croatia
Kovačić, A., Carev, M., Tripković, I., Srečec, S., & Šiško-Kraljević, K. (2014) · International Journal of Environmental Health Research · doi:10.1080/09603123.2014.893565 · Cited by 7 · see citing works
“…remain unrevealed and are deemed to be sporadic (Michaud et al. 2001); it is believed that consumption of undercooked poultry is the main cause of this infection in humans (Ribot et al. 2001; Dickins et al. 2002; Rivoal et al. 2005; Van Deun et al. 2007; Denis et al. 2009; Suzuki & Yamamoto 2009).”
Background
Survival and Transmission of Selected Pathogens on Airplane Cabin Surfaces and Selection of Phages Specific for Campylobacter jejuni
Vaglenov, K. A. (2014) · Cited by 7 · see citing works
Prevalence, cytotoxicity and antibiotic susceptibility of Campylobacter species recovered from retail chicken meat in Mansoura, Egypt
A., A. H., Younis, G., M., M. E.-S., & Awad, A. (2018) · African Journal of Microbiology Research · doi:10.5897/ajmr2018.8865 · Cited by 7 · see citing works
“…different studies in which C. jejuni was the most prevalent than other Campylobacter spp. (Andrzejewska et al., 2015; Guyard-Nicodème et al. 2015; Suzuki and Yamamoto, 2009; Whyte et al., 2004) Among C. jejuni positive samples, C. jejuni biotype I was the predominant biotype detected in the…”
Result
Estimating the performance of four culture media used for enumeration and detection of Campylobacter species in chicken meat
Ανδρίτσος, Ν. Δ., Tzimotoudis, N., & Mataragas, M. (2019) · LWT · doi:10.1016/j.lwt.2019.108808 · Cited by 6 · see citing works

Campylobacter contamination in retail poultry meats and by-products in Japan: A literature survey
Suzuki, H., & Yamamoto, S. (2008) · Food Control · doi:10.1016/j.foodcont.2008.08.016 · Cited by 46 · see citing works
Self-citation
Prevalence of Campylobacter spp. in Chicken from Retail Markets in Nakhon Pathom Province
Saengthongpinit, C., Viriyarampa, S., & Sakpuaram, T. (2005) · Agriculture and Natural Resources · Cited by 3 · see citing works
Occurrence of Campylobacter spp. in poultry meat at retail and processing plants’ levels in Central Italy
Mezher, Z., Saccares, S., Marcianò, R., Santis, P. D., Rodas, E. M. F., Angelis, V. D., & Condoleo, R. (2016) · Italian Journal of Food Safety · doi:10.4081/ijfs.2016.5495 · Cited by 18 · see citing works
Poultry flocks as a source of Campylobacter contamination of broiler carcasses
Wieczorek, K., & Osek, J. (2015) · Polish Journal of Veterinary Sciences · doi:10.1515/pjvs-2015-0013 · Cited by 13 · see citing works
DOI 10.1515/pjvs-2015-0013 Original article Poultry flocks as a source of Campylobacter contamination of broiler carcasses
Wieczorek, K., & Osek, J. (2016)

Authors: SUZUKI, H., & YAMAMOTO, S.
Affiliations: National Institute of Health Sciences (LK)
ORCID: SUZUKI, Hodaka
YAMAMOTO, Shigeki
Venue: Journal of Veterinary Medical Science
Publisher: Japanese Society of Veterinary Science
Published: 2009
Volume: 71
Issue: 3
Pages: 255-261
ISSN: 0916-7250 (ISSN-L)
1347-7439
DOI: 10.1292/jvms.71.255
OpenAlex: W1999157658
Cited by: 158
References: 81
Citations by year: 2026: 4 · 2025: 4 · 2024: 8 · 2023: 9 · 2022: 7 · 2021: 2 · 2020: 12 · 2019: 11 · 2018: 11 · 2017: 8 · 2016: 12 · 2015: 12 · 2014: 16 · 2013: 12 · 2012: 10
FWCI: 1.30
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
Locations: Journal of Veterinary Medical Science (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Funders: U.S. National Library of Medicine
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Listeria monocytogenes in Food Safety
Life Sciences › Agricultural and Biological Sciences › Food Science › Food Safety and Hygiene
Keywords: Campylobacter, Campylobacter jejuni, Campylobacter coli, retail poultry meat, poultry by-products, food contamination, foodborne pathogens, campylobacteriosis, cross-national comparison, poultry hygiene
MeSH terms: Animals, Campylobacter, Food Microbiology, Meat, Poultry, Global Health

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Campylobacter Contamination in Retail Poultry Meats and By-Products in the World: A Literature Survey

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