Skip to main content
SpringerLink
Log in

Genetic diversity, antimicrobial resistance, and virulence genes of thermophilic Campylobacter isolated from broiler production chain

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the prevalence of thermophilic Campylobacter in the broiler production chain of southern Brazil, by evaluating broiler farms and slaughter line samples, and to determine the genetic diversity, antimicrobial resistance, and virulence genes of the isolates. Of the 140 samples investigated in this study, 75 (53.6%) were positive for thermophilic Campylobacter, and all isolates were identified by phenotypic and molecular tests as C. jejuni. The resistance to nalidixic acid was the most common (74%), followed by resistance to enrofloxacin (67.3%) and ciprofloxacin (37.1%). However, there was no resistance to the macrolides tested which are recommended for the treatment of human campylobacteriosis. The PFGE showed that the isolates were grouped in eight macrorestriction patterns (P1 to P8). A representative isolate of each macrorestriction pattern was investigated for the presence of virulence genes and all isolates carried the cadF, ciaB, cdtA, cdtB, cdtC, and flaA genes. The dnaJ gene was detected in 87.5% (7/8) of the isolates. The flhA and racR genes were detected in 75% (6/8), while the pldA gene was present in 62.5% (5/8) and the wlaN gene in 25% (2/8). The presence of C. jejuni in broiler farms and in the slaughterhouse is a hazard to consumer given that this pathogen can be maintained throughout the broiler production chain and contaminates the final product. Moreover, the presence of the major virulence genes in the isolates demonstrates that they have the ability to develop campylobacteriosis in humans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. EFSA (2018) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. doi: https://doi.org/10.2903/j.efsa.2018.5500

  2. WHO (2018) Campylobacter. https://www.who.int/news-room/fact-sheets/detail/campylobacterjejuni

  3. Romero MR, D’agostino M, Arias AP, Robles S, Casado CF, Iturbe LO, Lerma OG, Andreou M, Cook N (2016) An immunomagnetic separation/loop-mediated isothermal amplification method for rapid direct detection of thermotolerant Campylobacter spp. during poultry production. J Appl Microbiol 120:469–477. https://doi.org/10.1111/jam.13008

    Article  CAS  PubMed  Google Scholar 

  4. CDC (2019) Campylobacter (Campylobacteriosis) https://www.cdc.gov/campylobacter/index.html

  5. EFSA (2019) The European Union One Health 2018 Zoonoses Report. EFSA Journal 17(12):5926

    Google Scholar 

  6. Bolton DJ (2015) Campylobacter virulence and survival factors. Food Microbiol 48:99–108. https://doi.org/10.1016/j.fm.2014.11.017

    Article  PubMed  Google Scholar 

  7. Devi A, Mahony TJ, Wilkinson JM, Vanniasinkam T (2019) Antimicrobial susceptibility of clinical isolates of Campylobacter jejuni from New South Wales, Australia. J Glob Antimicrob Re 16:76–80. https://doi.org/10.1016/j.jgar.2018.09.011

    Article  Google Scholar 

  8. Whitehouse CA, Zhao S, Tate H. (2018) Antimicrobial resistance in Campylobacter species: mechanisms and genomic epidemiology

  9. Ge B, Wang F, Sjeolund-Karlsson M, Mcdermott PF (2013) Antimicrobial resistance in Campylobacter: susceptibility testing methods and resistance trends. J Microbiol Meth 95:57–67. https://doi.org/10.1016/j.mimet.2013.06.021

    Article  CAS  Google Scholar 

  10. Abu-Madi M, Behnke JM, Sharma A, Bearden R, Al-Banna N (2016) Prevalence of virulence/stress genes in Campylobacter jejuni from chicken meat sold in Qatari retail outlets. PLoS One 11:e0156938. https://doi.org/10.1371/journal.pone.0156938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Humphrey S, Chaloner G, Kemmett K, Davidson N, Williams N, Kipar A, Humphrey T, Wigleya P (2014) Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. Amer Soc Microbiol 5(4):e01364–e01314. https://doi.org/10.1128/mBio.01364-14

    Article  CAS  Google Scholar 

  12. Newell DG, Shreeve JE, Toszeghy M, Domingue G, Bull S, Humphrey T, Mead G (2001) Changes in the carriage of Campylobacter strains by poultry carcasses during processing in abattoirs. Appl Environ Microbiol 67:2636–2640. https://doi.org/10.1128/AEM.67.6.2636-2640.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Monteville MR, Yoon JE, Konkel ME (2002) Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer membrane protein and microfilament reorganisation. Microbiol 149:153–165

    Article  Google Scholar 

  14. Rivera-Amill V, Kim BJ, Seshu J, Konkel ME (2001) Secretion of the virulence associated Campylobacter invasion antigens from Campylobacter jejuni requires a stimulatory signal. J Infec Dis 183:1607–1616

    Article  CAS  Google Scholar 

  15. Smith JL, Bayles DO (2006) The contribution of cytolethal distending toxin to bacterial pathogenesis. Crit Rev Microbiol 32:227–248

    Article  CAS  Google Scholar 

  16. Panzenhagen PHN, Aguiar WS, Frasão BS, Pereira VLA, Abreu DLC, Rodrigues DP, do Nascimento ER, de Aquino MHC (2016) Prevalence and fluoroquinolones resistance of Campylobacter and Salmonella isolates from poultry carcasses in Rio de Janeiro, Brazil. Food Control 61:243–247. https://doi.org/10.1016/j.foodcont.2015.10.002

    Article  CAS  Google Scholar 

  17. ISO (International Organization for Standard) (2006) Microbiology of FOOD and animal feeding stuffs – Horizontal method for detection and enumeration of Campylobacter spp. – Part 1: Detection method. (ISO 10272-1:2006 [E]). 16 p

  18. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual. V. 1, Chapter 6, Protocol 7, Third edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  19. Müller J, Schulze F, Müller W, Hänel I (2006) PCR detection of virulence-associated genes in Campylobacter jejuni strains with differential ability to invade Caco-2 cells and to colonize the chick gut. Vet Microbiol 113:123–129. https://doi.org/10.1016/j.vetmic.2005.10.029

    Article  CAS  PubMed  Google Scholar 

  20. Linton D, Gilbert M, Hitchen PG, Dell A, Morris HR, Wakarchuk WW, Gregson NA, Wren BW (2000) Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Mol Microbiol 37(3):501–514

    Article  CAS  Google Scholar 

  21. Datta S, Niwa H, Itoh K (2003) Prevalence of 11 pathogenic genes of Campylobacter jejuni by PCR in strains isolated from humans, poultry meat and broiler and bovine faeces. J Med Microbiol 52:345–348. https://doi.org/10.1099/jmm.0.05056-0

    Article  CAS  PubMed  Google Scholar 

  22. Wieczorek K, Kania I, Osek J (2009) Identification of main virulence markers of food-borne pathogens recovered from bovine carcasses as an aid in assessing public health risk. B Vet I Pulawy 53:425–432

    Google Scholar 

  23. Zheng J, Meng JH, Zhao SH, Singh R, Song WX (2006) Adherence to and invasion of human intestinal epithelial cells by Campylobacter jejuni and Campylobacter coli isolates from retail meat products. J Food Protect 69:768–774

    Article  CAS  Google Scholar 

  24. Konkel ME, Kim BJ, Rivera-Amill V, Garvis SG (1999) Bacterial secreted proteins are required for the internalization of Campylobacter jejuni into cultured mammalian cells. Mol Microbiol 32:691–701. https://doi.org/10.1046/j.1365-2958.1999.01376.x

    Article  CAS  PubMed  Google Scholar 

  25. Josefsen MH, Lübeck PS, Hansen F, Hoorfar J (2004) Towards an international standard for PCR-based detection of foodborne thermotolerant campylobacters: interaction of enrichment media and pre-PCR treatment on carcass rinse samples. J Microbiol Meth 58:39–48. https://doi.org/10.1016/j.mimet.2004.03.001

    Article  CAS  Google Scholar 

  26. Maćkiw E, Korsak D, Rzewuska K, Tomczuk K, Rozynek E (2012) Antibiotic resistance in Campylobacter jejuni and Campylobacter coli isolated from food in Poland. Food Control 23:297–301. https://doi.org/10.1016/j.foodcont.2011.08.022

    Article  CAS  Google Scholar 

  27. Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antimicrobial susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496

    Article  CAS  Google Scholar 

  28. EUCAST (European Committee on Antimicrobial Susceptibility Testing) (2015) Breakpoint tables for interpretation of MICs and zone diameters. (http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_5.0_Breakpoint_Table_01.pdf)

  29. CLSI (2015) M100–S25. Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement. Wayne, PA, USA: clinical and laboratory standards institute

  30. Ribot EM, Fitzgerald C, Kubota K, Swaminathan B, Barrett TJ (2001) Rapid pulsed-field gel electrophoresis protocol for subtyping of Campylobacter jejuni. J Clin Microbiol 39:1889–1894. https://doi.org/10.1128/JCM.39.5.1889-1894.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Wieczorek K, Denis E, Osek J (2015) Comparative analysis of antimicrobial resistance and genetic diversity of Campylobacter from broilers slaughtered in Poland. Int J Food Microbiol 210:24–32. https://doi.org/10.1016/j.ijfoodmicro.2015.06.006

    Article  CAS  PubMed  Google Scholar 

  32. Høg B, Sommer HM, Larsen LS, Sorensen AIV, David B, Hofshagen M, Rosenquist H (2016) Farm specific risk factors for Campylobacter colonisation in Danish and Norwegian broilers. Prev Vet Med 130:137–145. https://doi.org/10.1016/j.prevetmed.2016.04.002

    Article  Google Scholar 

  33. Krause M, Josefsen MH, Lund M, Jacobsen NR, Brorsen L, Moos M, Stockmarr A, Hoorfar J (2006) Comparative, collaborative, and on-site validation of a TaqMan PCR method as a tool for certified production of fresh, Campylobacter-free chickens. Appl Environ Microb 72(8):5463–5468. https://doi.org/10.1128/AEM.00291-06

    Article  CAS  Google Scholar 

  34. Messad S, Hamdi TM, Bouhamed R, Ramdani-Bouguessa N, Tazir M (2014) Frequency of contamination and antimicrobial resistance of thermotolerant Campylobacter isolated from some broiler farms and slaughterhouses in the region of Algiers. Food Control 40:324–328. https://doi.org/10.1016/j.foodcont.2013.12.016

    Article  CAS  Google Scholar 

  35. Sommer HM, Heuer OE, Sørensena AIV, Madsenc M (2013) Analysis of factors important for the occurrence of Campylobacter in Danish broiler flocks. Prev Vet Med 111:100–111. https://doi.org/10.1016/j.prevetmed.2013.04.004

    Article  CAS  PubMed  Google Scholar 

  36. Battersby T, Whyte P, Bolton D (2016) Protecting broilers against Campylobacter infection by preventing direct contact between farm staff and broilers. Food Control 69:346–351. https://doi.org/10.1016/j.foodcont.2016.04.053

    Article  Google Scholar 

  37. Humphrey T, O’Brien S, Madsen M (2007) Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117:237–257. https://doi.org/10.1016/j.ijfoodmicro.2007.01.006

    Article  PubMed  Google Scholar 

  38. EFSA (European Food Safety Authority) (2012) The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2010. EFSA J 10:2598. https://doi.org/10.2903/j.efsa.2012.2598

    Article  CAS  Google Scholar 

  39. García-Sánchez L, Melero B, Jaime I, Hänninen ML, Rossi M, Rovira J (2017) Campylobacter jejuni survival in a poultry processing plant environment. Food Microbiol 65:185–192. https://doi.org/10.1016/j.fm.2017.02.009

    Article  PubMed  Google Scholar 

  40. Chokboonmongkol C, Patchanee P, Golz G, Zessin KH, Alter T (2013) Prevalence, quantitative load, and antimicrobial resistance of Campylobacter spp. from broiler ceca and broiler skin samples in Thailand. Poultry Sci 92:462–467. https://doi.org/10.3382/ps.2012-02599

    Article  CAS  Google Scholar 

  41. Gharbi M, Béjaoui A, Hmada CB, Jouini A, Ghedira K, Zrelli C, Hamrouni S, Aouadhi C, Bessoussa G, Ghram A, Maaroufi A (2018) Prevalence and antibiotic resistance patterns of Campylobacter spp. isolated from broiler chickens in the north of Tunisia. BioMed Res Int 2018:7943786–7943787. https://doi.org/10.1155/2018/7943786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Oliveira MG, Rizzi C, Galli V, Lopes GV, Haubert L, Dellagostin OA, Silva WP (2019) Presence of genes associated with adhesion, invasion, and toxin production in Campylobacter jejuni isolates and effect of temperature on their expression. Can J Microbiol 65:4. https://doi.org/10.1139/cjm-2018-0539

    Article  CAS  Google Scholar 

  43. Seliwiorstow T, Baré J, Berkvens D, Van Damme I, Uyttendaele M, de Zutter L (2016) Identification of risk factors for Campylobacter contamination levels on broiler carcasses during the slaughter process. Int J Food Microbiol 226:26–32. https://doi.org/10.1016/j.ijfoodmicro.2016.03.010

    Article  PubMed  Google Scholar 

  44. Bull SA, Allen VM, Domingue G, Jorgensen F, Frost JA, Ure R, Whyte R, Tinker D, Corry JEL, Gillard-King J, Humphrey TJ (2006) Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl Environ Microbiol 72:645–652. https://doi.org/10.1128/AEM.72.1.645-652.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Berrang ME, Northcutt JK, Fletcher DL, Cox NA (2003) Role of dump cage fecal contamination in the transfer of Campylobacter to carcasses of previously negative broilers. J Appl Poult Res 12:190–195. https://doi.org/10.1093/japr/12.2.190

    Article  Google Scholar 

  46. Gruntar I, Biasizzo M, Kušar D, Pate M, Ocepek M (2015) Campylobacter jejuni contamination of broiler carcasses: population dynamics and genetic profiles at slaughterhouse level. Food Microbiol 50:97–101. https://doi.org/10.1016/j.fm.2015.03.007

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  48. Franchin PR, Ogliari PJ, Batista CRV (2007) Frequency of thermophilic Campylobacter in broiler chickens during industrial processing in a southern Brazil slaughterhouse. Brit Poultry Sci 48:127–132. https://doi.org/10.1080/00071660701261286

    Article  CAS  Google Scholar 

  49. Nobile CGA, Costantino R, Bianco A, Pileggi C, Pavia M (2013) Prevalence and pattern of antibiotic resistance of Campylobacter spp. in poultry meat in Southern Italy. Food Control 32(2):715–718. https://doi.org/10.1016/j.foodcont.2013.02.011

    Article  CAS  Google Scholar 

  50. Ruiz-Palacios GM (2007) The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken. Clin Infect Dis 44:701–703. https://doi.org/10.1086/509936

    Article  PubMed  Google Scholar 

  51. Avrain L, Humbert F, L’Hospitalier R, Sanders P, Vernozy-Rozand C, Kempf I (2003) Antimicrobial resistance in Campylobacter from broilers: association with production type and antimicrobial use. Vet Microbiol 96(3):267–276. https://doi.org/10.1016/j.vetmic.2003.07.001

    Article  CAS  PubMed  Google Scholar 

  52. Chen X, Naren GW, Wu CM, Wang Y, Dai L, Xia LN (2010) Prevalence and antimicrobial resistance of Campylobacter isolates in broilers from China. Vet Microbiol 144:133–139. https://doi.org/10.1016/j.vetmic.2009.12.035

    Article  CAS  PubMed  Google Scholar 

  53. Farnell MB, Donoghue AM, Cole K, Reyes-Herrera I, Blore PJ, Donoghue DJ (2005) Campylobacter susceptibility to ciprofloxacin and corresponding fluoroquinolone concentrations within the gastrointestinal tracts of chickens. J Appl Microbiol 99:1043–1050. https://doi.org/10.1111/j.1365-2672.2005.02712.x

    Article  CAS  PubMed  Google Scholar 

  54. Miflin JK, Templeton JM, Blackall PJ (2007) Antibiotic resistance in Campylobacter jejuni and Campylobacter coli isolated from poultry in the South-East Queensland region. J Antimicrob Chemoth 59:775–778. https://doi.org/10.1093/jac/dkm024

    Article  CAS  Google Scholar 

  55. Gruntar I, Ocepek M, Avbersek J, Mićunović J, Pate M (2010) A pulsed-field gel electrophoresis study of the genetic diversity of Campylobacter jejuni and Campylobacter coli in poultry flocks in Slovenia. Acta Vet Hung 58(1):19–28. https://doi.org/10.1556/AVet.58.2010.1.2

    Article  PubMed  Google Scholar 

  56. Lindmark H, Harbom B, Thebo L, Andersson L, Hedin G, Osterman B, Lindberg T, Andersson Y, Westöö A, Engvall EO (2004) Genetic characterization and antibiotic resistance of Campylobacter jejuni isolated from meats, water, and humans in Sweden. J Clin Microbiol 42(2):700–706. https://doi.org/10.1128/JCM.42.2.700-706.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Workman SN, Mathison GE, Lavoie MC (2008) An investigation of sources of Campylobacter in a poultry production and packing operation in Barbados. Int J Food Microbiol 121:106–111. https://doi.org/10.1016/j.ijfoodmicro.2007.10.014

    Article  CAS  PubMed  Google Scholar 

  58. Ghorbanalizadgan M, Bakhshi B, Najar-Peerayeh S (2018) Heterogeneity of cytolethal distending toxin sequence types of Campylobacter jejuni and correlation to invasion/ cytotoxicity potential: The first molecular survey from Iran. Microb Pathogenesis 114:213–218. https://doi.org/10.1016/j.micpath.2017.11.035

    Article  CAS  Google Scholar 

  59. Jones MA, Marston KL, Woodall CA, Maskell DJ, Linton D, Karlyshev AV, Dorrell N, Wren BW, Barrow PA (2004) Adaptation of Campylobacter jejuni NCTC11168 to high level colonization of the avian gastrointestinal tract. Infect Immun 72:3769–3776. https://doi.org/10.1128/IAI.72.7.3769-3776.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Samad A, Abbas F, Ahmed Z, Akbar A, Naeem M, Sadiq MB, Ali I, Roomeela S, Bugti FS, Achakzai SK (2018) Prevalence, antimicrobial susceptibility, and virulence of Campylobacter jejuni isolated from chicken meat. J Food Safety 36:e12600. https://doi.org/10.1111/jfs.12600

    Article  CAS  Google Scholar 

  61. Konkel ME, Gray SA, Kim BJ, Garvis SG, Yoon J (1999) Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J Clin Microbiol 37(3):510–517 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC84446

    Article  CAS  Google Scholar 

  62. Monteville MR, Yoon JE, Konkel ME (2003) Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer membrane protein and microfilament reorganization. Microbiol 149:153–165. https://doi.org/10.1099/mic.0.25820-0

    Article  CAS  Google Scholar 

  63. Konkel ME, Kim BJ, Klena JD, Young CR, Ziprin R (1998) Characterization of the thermal stress response of Campylobacter jejuni. Infect Immun 66(8):3666–3672

    Article  CAS  Google Scholar 

  64. Brás AM, Chatterjee S, Wren BW, Newell DG, Ketley JM (1999) A novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J Bacteriol 181:3298–3302 https://www.ncbi.nlm.nih.gov/pubmed/10322038

    Article  Google Scholar 

  65. Gagnaire A, Nadel B, Raoult D, Neefjes J, Gorvel JP (2017) Collateral damage: insights into bacterial mechanisms that predispose host cells to cancer. Nat Rev Microbiol 15:109–128. https://doi.org/10.1038/nrmicro.2016.171

    Article  CAS  PubMed  Google Scholar 

  66. He Z, Gharaibeh RZ, Newsome RC, Pope JL, Dougherty MW, Tomkovich S, Pons B, Mirey G, Vignard J, Hendrixson DR, Jobin C (2019) Campylobacter jejuni promotes colorectal tumorigenesis through the action of cytolethal distending toxin. Gut 68:289–300

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001. The authors extend their thanks to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Process n. 309101/2016-6) and to the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) (Process n. 17/2551-0000956-8).

Author information

Authors and Affiliations

  1. Departamento de Ciência e Tecnologia Agroindustrial, Universidade Federal de Pelotas, Pelotas, Rio Grande do Sul, Brazil

    Tassiana Ramires, Mauricéia Greici de Oliveira, Natalie Rauber Kleinubing, Marcia Magalhães Mata, Graciela Volz Lopes & Wladimir Padilha da Silva

  2. Centro de Biotecnologia, Universidade Federal de Pelotas, Pelotas, Rio Grande do Sul, Brazil

    Simone de Fátima Rauber Würfel, Mariana Almeida Iglesias, Odir Antônio Dellagostin & Wladimir Padilha da Silva

Authors
  1. Tassiana Ramires
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mauricéia Greici de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalie Rauber Kleinubing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Simone de Fátima Rauber Würfel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marcia Magalhães Mata
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mariana Almeida Iglesias
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Graciela Volz Lopes
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Odir Antônio Dellagostin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wladimir Padilha da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Tassiana Ramires, Mauricéia Greici de Oliveira, Natalie Rauber Kleinubing, Simone de Fátima Rauber Würfel, Marcia Magalhães Mata, Mariana Almeida Iglesias, and Graciela Volz Lopes. The first draft of the manuscript was written by Tassiana Ramires and Mauricéia Greici de Oliveira, and all authors commented on previous versions of the manuscript. The manuscript was reviewed by Odir Antônio Dellagostin and Wladimir Padilha da Silva. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Wladimir Padilha da Silva.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict interest.

Additional information

Responsible Editor: Mariza Landgraf.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramires, T., de Oliveira, M.G., Kleinubing, N.R. et al. Genetic diversity, antimicrobial resistance, and virulence genes of thermophilic Campylobacter isolated from broiler production chain. Braz J Microbiol 51, 2021–2032 (2020). https://doi.org/10.1007/s42770-020-00314-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-020-00314-0

Keywords

Search

Navigation