MLST-based genetic relatedness of Campylobacter jejuni isolated from chickens and humans in Poland


Autoři: Kinga Wieczorek aff001;  Tomasz Wołkowicz aff002;  Jacek Osek aff001
Působiště autorů: Department of Hygiene of Food of Animal Origin, National Veterinary Research Institute, Pulawy, Poland aff001;  Department of Bacteriology and Biocontamination Control, National Institute of Public Health—National Institute of Hygiene, Warsaw, Poland aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226238

Souhrn

Campylobacter jejuni infection is one of the most frequently reported foodborne bacterial diseases worldwide. The main transmission route of these microorganisms to humans is consumption of contaminated food, especially of chicken origin. The aim of this study was to analyze the genetic relatedness of C. jejuni from chicken sources (feces, carcasses, and meat) and from humans with diarrhea as well as to subtype the isolates to gain better insight into their population structure present in Poland. C. jejuni were genotyped using multilocus sequence typing (MLST) and sequence types (STs) were assigned in the MLST database. Among 602 isolates tested, a total of 121 different STs, including 70 (57.9%) unique to the isolates' origin, and 32 STs that were not present in the MLST database were identified. The most prevalent STs were ST464 and ST257, with 58 (9.6%) and 52 (8.6%) C. jejuni isolates, respectively. Isolates with some STs (464, 6411, 257, 50) were shown to be common in chickens, whereas others (e.g. ST21 and ST572) were more often identified among human C. jejuni. It was shown that of 47 human sequence types, 26 STs (106 isolates), 23 STs (102 isolates), and 29 STs (100 isolates) were also identified in chicken feces, meat, and carcasses, respectively. These results, together with the high and similar proportional similarity indexes (PSI) calculated for C. jejuni isolated from patients and chickens, may suggest that human campylobacteriosis was associated with contaminated chicken meat or meat products or other kinds of food cross-contaminated with campylobacters of chicken origin. The frequency of various sequence types identified in the present study generally reflects of the prevalence of STs in other countries which may suggest that C. jejuni with some STs have a global distribution, while other genotypes may be more restricted to certain countries.

Klíčová slova:

Campylobacter – Campylobacteriosis – Diarrhea – Chickens – Meat – Poland – Sequence databases – Campylobacter jejuni


Zdroje

1. EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J. 2018; 16: 5500. https://doi.org/10.2903/j.efsa.2018.5500

2. Humphrey T, O'Brien S, Madsen M. Campylobacters as zoonotic pathogens: a food production perspective. Intern J Food Microbiol 2007; 117: 237–257. doi: 10.1016/j.ijfoodmicro.2007.01.006

3. Tresse O, Alvarez-Ordóñez A, Connerton IF. Editorial: About the foodborne pathogen Campylobacter. Front Microbiol. 2017; 8: 1908. doi: 10.3389/fmicb.2017.01908 29067004

4. Kaakoush NO, Castaño-Rodriguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev. 2015; 28: 687–720. doi: 10.1128/CMR.00006-15 26062576

5. Skarp CPA, Hänninen ML, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect. 2016; 22: 103–109. doi: 10.1016/j.cmi.2015.11.019 26686808

6. Rosenquist H, Sommer HM, Nielsen NL, Christensen BB. The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter. Int J Food Microbiol. 2006; 108: 226–232. doi: 10.1016/j.ijfoodmicro.2005.12.007 16478636

7. Colles FM, Maiden MC. Campylobacter sequence typing databases: applications and future prospects. Microbiol. 2012; 158: 2695–2709. doi: 10.1099/mic.0.062000-0

8. Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, et al. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol. 2001; 39: 14–23. doi: 10.1128/JCM.39.1.14-23.2001 11136741

9. Sheppard SK, Dallas JF, MacRae M, McCarthy MD, Sproston LE, Gormley FJ, et al. Campylobacter genotypes from food animals, environmental sources and clinical disease in Scotland 2005/6. Intern J Food Microbiol. 2009: 134: 96–103. doi: 10.1016/j.ijfoodmicro.2009.02.010

10. Jay-Russel MT, Mandrell ME, Yuan J, Bates A, Manalac R, Mohle-Boetani M, et al. Using major outer membrane protein typing as an epidemiological tool to investigate outbreaks caused by milk-borne Campylobacter jejuni isolates in California. J Clin Microbiol. 2013; 51: 195–201. doi: 10.1128/JCM.01845-12 23115263

11. Wieczorek K, Kania I, Osek J. Prevalence and antimicrobial resistance of Campylobacter spp. isolated from poultry carcasses in Poland. J Food Prot. 2013; 76: 1451–1455. doi: 10.4315/0362-028X.JFP-13-035 23905805

12. Wieczorek K, Denis E, Lynch O, Osek J. Molecular characterization and antibiotic resistance profiling of Campylobacter isolated from cattle in Polish slaughterhouses. Food Microbiol. 2013; 34: 130–136. doi: 10.1016/j.fm.2012.12.003 23498189

13. Vandamme P, Van Doorn LJ, al Rashid ST, Quint WGV, van der Plas J, Chan VL, et al. Campylobacter hyoilei Alderton et al. 1995 and Campylobacter coli Wron and Chatelain 1973 are subjective synonyms. Intern J Syst Bacteriol. 1997; 47: 1055–1060. doi: 10.1099/00207713-47-4-1055

14. Wieczorek K, Wołkowicz T, Osek J. Antimicrobial resistance and virulence-associated traits of Campylobacter jejuni isolated from poultry food chain and humans with diarrhea. Front Microbiol. 2018; 9: 1508. doi: 10.3389/fmicb.2018.01508 30022977

15. Wieczorek K, Denis E, Lachtara B, Osek J. Distribution of Campylobacter jejuni multilocus sequence types isolated from chickens in Poland. Poultry Science 2017; 96: 703–709. doi: 10.3382/ps/pew343 27702925

16. Hunter PR, Gaston MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol. 1988; 26: 2465–2466. 3069867

17. Garrett N, Devane ML, Hudson JA, Nicol C, Ball A, Klena JD, et al. Statistical comparison of Campylobacter jejuni subtypes from human cases and environmental sources. J Appl Microbiol. 2007; 103: 2113–2121. doi: 10.1111/j.1365-2672.2007.03437.x 18045395

18. Llarena AK, Huneau A, Hakkinen M, Hanninen ML. Predominant Campylobacter jejuni sequence types persist in Finnish chicken production. PloS ONE 2015; 10: e0116585. doi: 10.1371/journal.pone.0116585 25700264

19. Vidal AB, Colles FM, Rodgers JD, McCarthy ND, Davies RH, Maiden MCJ, et al. Genetic diversity of Campylobacter jejuni and Campylobacter coli isolates from conventional broiler flocks and the impacts of sampling strategy and laboratory method. Appl Environ Microbiol. 2016; 82: 2347–2355. doi: 10.1128/AEM.03693-15 26873321

20. Smid JH, Mughini Gras L, de Boer AG, French NP, Havelaar AH, Wagenaar JA, et al. Practicalities of using non-local or non-recent multilocus sequence typing data for source attribution in space and time of human campylobacteriosis. PLoS ONE 2013; 8: e55029. doi: 10.1371/journal.pone.0055029 23405107

21. Iglesias-Torrens Y, Miró E, Guirado P, Llovet T, Muñoz C, Cerdà-Cuéllar M, et al. Population structure, antimicrobial resistance, and virulence-associated genes in Campylobacter jejuni isolated from three ecological niches: gastroenteritis patients, broilers, and wild birds. Front Microbiol. 2018; 9: 1676. doi: 10.3389/fmicb.2018.01676 30116225

22. Vinueza-Burgos C, Wautier M, Martiny D, Cisneros M, Van Damme I, De Zutter L. Prevalence, antimicrobial resistance and genetic diversity of Campylobacter coli and Campylobacter jejuni in Ecuadorian broilers at slaughter age. Poultry Sci. 2017; 96: 2366–2374. doi: 10.3382/ps/pew487

23. Ohishi T, Aoki K, Ishii Y, Usui M, Tamura Y, Kawanishi M, et al. Molecular epidemiological analysis of human- and chicken-derived isolates of Campylobacter jejuni in Japan using next-generation sequencing. J Infect Chemother. 2017; 23: 165–172. doi: 10.1016/j.jiac.2016.11.011 28087306

24. Ramonaite S, Tamuleviciene E, Alter T, Kasnauskyte N, Malakauskas M. MLST genotypes of Campylobacter jejuni isolated from broiler products, dairy cattle and human campylobacteriosis cases in Lithuania. BMC Infect Dis. 2017; 17: 430. doi: 10.1186/s12879-017-2535-1 28619013

25. Islam Z, van Belkum A, Wagenaar JA, Cody AJ, de Boer AG, Sarker SK, et al. Comparative population structure analysis of Campylobacter jejuni from human and poultry origin in Bangladesh. Eur J Clin Microbiol Infect Dis. 2014; 33: 2173–2181. doi: 10.1007/s10096-014-2184-x 24962195

26. Prachantasena S, Charununtakorn P, Muangnoicharoen S, Hankla L, Techawal N, Chaveerach P, et al. Distribution and genetic profiles of Campylobacter in commercial broiler production from breeder to slaughter in Thailand. PloS ONE 2016: 11: e0149585. doi: 10.1371/journal.pone.0149585 26886590

27. Műllner P, Collins-Emerson JM, Midwinter AC, Carter P, Spencer SE, van der Logt P, et al. Molecular epidemiology of Campylobacter jejuni in a geographically isolated country with a uniquely structured poultry industry. Appl Environ Microbiol. 2010; 76: 2145–2154. doi: 10.1128/AEM.00862-09 20154115

28. Stone D, Davis M, Baker K, Besser T, Roopnarine R. Sharma R. MLST genotypes and antibiotic resistance of Campylobacter spp. isolated from poultry in Grenada. Biomed Res Intern. 2013; 794643. doi: 10.1155/2013/79464

29. Newell DG, Shreeve JE, Toszeghy M, Domingue G, Bull S, Humphrey T, et al. Changes in the carriage of Campylobacter strains by poultry carcasses during processing in abattoirs. Appl Environ Microbiol. 2001; 67: 2636–2640. doi: 10.1128/AEM.67.6.2636-2640.2001 11375174

30. Habib I, Miller WG, Uyttendaele M, Houf K, De Zutter L. Clonal population structure and antimicrobial resistance of Campylobacter jejuni in chicken meat from Belgium. Appl Environ Microbiol. 2009; 75: 4264–4272. doi: 10.1128/AEM.00168-09 19411429

31. Nielsen LN, Sheppard SK, McCarthy ND, Maiden MCJ, Ingmer H, Krogfelt KA. MLST clustering of Campylobacter jejuni isolates from patients with gastroenteritis, reactive arthritis and Guillain–Barre´ syndrome. J Appl Microbiol. 2010; 108: 591–599. doi: 10.1111/j.1365-2672.2009.04444.x 19702866

32. Kovanen SM, Kivisto RI, Rossi M, Schott T, Karkkainen UM, Tuuminen T, et al. MLST and whole-genome MLST of human Campylobacter jejuni isolates from three districts during a seasonal peak in Finland. J Clin Microbiol. 2014; 12: 4147–4154. doi: 10.1128/JCM.01959-14

33. de Haan CPA, Kivistö R, Hakkinen M, Rautelin H, Hänninen ML. Decreasing trend of overlapping multilocus sequence types between human and chicken Campylobacter jejuni isolates over a decade in Finland. Appl Environ Microbiol. 2010; 76: 5228–5236. doi: 10.1128/AEM.00581-10 20543048

34. Kärenlampii R, Rautelin H, Schönberg-Norio D, Paulin L, Hänninen ML. Longitudinal study of Finnish Campylobacter jejuni and C. coli isolates from humans, using multilocus sequence typing, including comparison with epidemiological data and isolates from poultry and cattle. Appl Environ Microbiol. 2007; 73: 148–155. doi: 10.1128/AEM.01488-06 17085689

35. 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. J Appl Microbiol. 2010; 110: 513–520. doi: 10.1111/j.1365-2672.2010.04906.x 21143711

36. Műllner P, Spencer SEF, Wilson DJ, Jones G, Noble AD, Midwinter AC, et al. Assigning the source of human campylobacteriosis in New Zealand: A comparative genetic and epidemiological approach. Infect Gen Evol. 2009; 9: 1311–1319. doi: 10.1016/j.meegid.2009.09.003

37. Mickan L, Doyle R, Valcanis M, Dingle KE, Unicomb L, Lanser J, and the Australian Campylobacter Subtyping Study Group. Multilocus sequence typing of Campylobacter jejuni isolates from New South Wales, Australia. J Appl Microbiol. 2007; 102: 144–152. doi: 10.1111/j.1365-2672.2006.03049.x 17184329

38. Kittl S, Heckler G, Korczak BM, Kuhnert P. Source attribution of human Campylobacter isolates by MLST and fla-typing and association of genotypes with quinolone resistance. PLoS ONE 2013; 8: e81796. doi: 10.1371/journal.pone.0081796 24244747

39. Wirz SE, Overesch G, Kuhnert P, Korczak BM. Genotype and antibiotic resistance analyses of Campylobacter isolates from ceca and carcasses of slaughtered broiler flocks. Appl Environ Microbiol. 2010; 76: 6377–6386. doi: 10.1128/AEM.00813-10 20709846

40. Griekspoor P, Olsson Engval E, Åkerlind B, Olsen B, Waldenström J. Genetic diversity and host associations in Campylobacter jejuni from human cases and broilers in 2000 and 2008. Vet Microbiol. 2015; 178: 94–98. doi: 10.1016/j.vetmic.2015.04.025 25960333

41. Ravel A, Hurst M, Petrica N, David J, Mutschall SK, Pintar K, et al. Source attribution of human campylobacteriosis at the point of exposure by combining comparative exposure assessment and subtype comparison based on comparative genomic fingerprinting. PLoS ONE 2017; 12: e0183790. doi: 10.1371/journal.pone.0183790 28837643

42. Kovac J, Stessl B, Čadež N, Gruntar I, Cimerman M, Stingl K, et al. Population structure and attribution of human clinical Campylobacter jejuni isolates from central Europe to livestock and environmental sources. Zoonozes Public Health 2018; 65: 51–58. doi: 10.1111/zph.12366

43. Smith JM, Smith NH, O’Rourke M, Spratt BG. How clonal are bacteria? Proc Natl Acad Sci USA 1993; 90: 4384–4388. doi: 10.1073/pnas.90.10.4384 8506277


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