Skip to main content
Top
Published in: Gut Pathogens 1/2016

Open Access 01-12-2016 | Research

Prevalence, genotyping and risk factors of thermophilic Campylobacter spreading in organic turkey farms in Germany

Authors: Marwa Fawzy El Metwaly Ahmed, Hosny El-Adawy, Helmut Hotzel, Herbert Tomaso, Heinrich Neubauer, Nicole Kemper, Joerg Hartung, Hafez Mohamed Hafez

Published in: Gut Pathogens | Issue 1/2016

Login to get access

Abstract

Background

The need for organic food of animal origin has increased rapidly in recent years. However, effects of organic animal husbandry on food safety have not been rigorously tested especially in meat turkey flocks. This study provides for the first time an overview on the prevalence and genetic diversity of Campylobacter species (spp.) in five organic meat turkey farms located in different regions in Germany, as well as on potential risk factors of bacterial spreading. Thirty cloacal swabs as well as water samples and darkling beetles were collected from each flock and examined for the presence of Campylobacter by conventional and molecular biological methods. The isolates were genotyped by flaA-RFLP.

Results

Campylobacter spp. were detected in cloacal swabs in all 5 turkey flocks with prevalence ranged from 90.0 to 100 %. 13 cloacal swabs collected from birds in farm III and IV were harboured mixed population of thermophilic campylobacters. In total, from 158 Campylobacter isolated from turkeys 89 (56.33 %) were identified as C. coli and 69 (43.76 %) as C. jejuni. Three Campylobacter (2 C. jejuni and 1 C. coli) were detected in drinkers of two farms and 3 C. coli were isolated from darkling beetles of one farm. No Campylobacter were isolated from main water tanks. flaA-RFLP assay showed that turkey farms can harbour more than one genotype. In a single turkey two different genotypes could be detected. The genotypes of campylobacters isolated from water samples or beetles were identical with those isolated from turkeys. No effect was found of some environmental parameters [ammonia concentration (NH3), carbon dioxide concentration (CO2), relative humidity (RH) and air temperature)] on Campylobacter prevalence in organic turkey farms. Additionally, drinking water and darkling beetles might be considered as risk factors for the spreading of Campylobacter in turkey flocks.

Conclusions

This study highlights the high prevalence and genotypic diversity of Campylobacter spp. isolated from organic turkey flocks. Further research is needed to assess other potential risk factors responsible for bacteria spreading in order to mitigate the spread of Campylobacter in organic turkey flocks by improving biosecurity control measures.
Appendix
Available only for authorised users
Literature
1.
go back to reference EFSA. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA J. 2015;12:3547. EFSA. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA J. 2015;12:3547.
2.
go back to reference European Commission, Directorate-General for Agriculture and Rural Development. An analysis of the EU organic sector. Brussels; 2010. European Commission, Directorate-General for Agriculture and Rural Development. An analysis of the EU organic sector. Brussels; 2010.
3.
go back to reference Kijlstra A, Meerburg B, Bos A. Food safety in free-range and organic livestock systems: risk management and responsibility. J Food Prot. 2009;72(12):2629–37.PubMed Kijlstra A, Meerburg B, Bos A. Food safety in free-range and organic livestock systems: risk management and responsibility. J Food Prot. 2009;72(12):2629–37.PubMed
4.
go back to reference Bull S, Allen V, Domingue G, Jørgensen F, Frost J, Ure R, et al. Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl Environ Microbiol. 2006;72(1):645–52.CrossRefPubMedPubMedCentral Bull S, Allen V, Domingue G, Jørgensen F, Frost J, Ure R, et al. Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl Environ Microbiol. 2006;72(1):645–52.CrossRefPubMedPubMedCentral
5.
go back to reference Wilson D, Rathinam V, Qi W, Wick L, Landgraf J, Bell J, et al. Genetic diversity in Campylobacter jejuni is associated with differential colonization of broiler chickens and C57BL/6J IL10-deficient mice. Microbiology. 2010;156(7):2046–57.CrossRefPubMedPubMedCentral Wilson D, Rathinam V, Qi W, Wick L, Landgraf J, Bell J, et al. Genetic diversity in Campylobacter jejuni is associated with differential colonization of broiler chickens and C57BL/6J IL10-deficient mice. Microbiology. 2010;156(7):2046–57.CrossRefPubMedPubMedCentral
6.
go back to reference El-Adawy H, Hotzel H, Tomaso H, Neubauer H, Taboada E, Ehricht R, et al. Detection of genetic diversity in Campylobacter jejuni isolated from a commercial turkey flock using flaA typing, MLST analysis and microarray assay. PLoS One. 2013;8(2):e51582.CrossRefPubMedPubMedCentral El-Adawy H, Hotzel H, Tomaso H, Neubauer H, Taboada E, Ehricht R, et al. Detection of genetic diversity in Campylobacter jejuni isolated from a commercial turkey flock using flaA typing, MLST analysis and microarray assay. PLoS One. 2013;8(2):e51582.CrossRefPubMedPubMedCentral
7.
go back to reference Wieczorek K, Denis E, Osek J. Comparative analysis of antimicrobial resistance and genetic diversity of Campylobacter from broilers slaughtered in Poland. Int J Food Microbiol. 2015;210:24–32.CrossRefPubMed Wieczorek K, Denis E, Osek J. Comparative analysis of antimicrobial resistance and genetic diversity of Campylobacter from broilers slaughtered in Poland. Int J Food Microbiol. 2015;210:24–32.CrossRefPubMed
9.
go back to reference Vandeplas S. Prevalence and sources of Campylobacter spp. contamination in free-range broiler production in the southern part of Belgium. Biotechnol Agron Soc Environ. 2010;14:279–88. Vandeplas S. Prevalence and sources of Campylobacter spp. contamination in free-range broiler production in the southern part of Belgium. Biotechnol Agron Soc Environ. 2010;14:279–88.
10.
go back to reference Agunos A, Waddell L, Léger D, Taboada E. A systematic review characterizing on-farm sources of Campylobacter spp. for broiler chickens. PLoS One. 2014;9(8):e104905.CrossRefPubMedPubMedCentral Agunos A, Waddell L, Léger D, Taboada E. A systematic review characterizing on-farm sources of Campylobacter spp. for broiler chickens. PLoS One. 2014;9(8):e104905.CrossRefPubMedPubMedCentral
11.
go back to reference Colles F, Jones T, McCarthy N, Sheppard S, Cody A, Dingle K, et al. Campylobacter infection of broiler chickens in a free-range environment. Environ Microbiol. 2008;10(8):2042–50.CrossRefPubMedPubMedCentral Colles F, Jones T, McCarthy N, Sheppard S, Cody A, Dingle K, et al. Campylobacter infection of broiler chickens in a free-range environment. Environ Microbiol. 2008;10(8):2042–50.CrossRefPubMedPubMedCentral
12.
go back to reference Templeton J, De Jong A, Blackall P, Miflin J. Survival of Campylobacter spp. in darkling beetles (Alphitobius diaperinus) and their larvae in Australia. Appl Environ Microbiol. 2006;72(12):7909–11.CrossRefPubMedPubMedCentral Templeton J, De Jong A, Blackall P, Miflin J. Survival of Campylobacter spp. in darkling beetles (Alphitobius diaperinus) and their larvae in Australia. Appl Environ Microbiol. 2006;72(12):7909–11.CrossRefPubMedPubMedCentral
13.
go back to reference Bates C, Hiett KL, Stern NJ. Relationship of Campylobacter isolated from poultry and from darkling beetles in New Zealand. Avian Dis. 2004;48(1):138–47.CrossRefPubMed Bates C, Hiett KL, Stern NJ. Relationship of Campylobacter isolated from poultry and from darkling beetles in New Zealand. Avian Dis. 2004;48(1):138–47.CrossRefPubMed
14.
go back to reference Hazeleger W, Bolder N, Beumer R, Jacobs-Reitsma W. Darkling beetles (Alphitobius diaperinus) and their larvae as potential vectors for the transfer of Campylobacter jejuni and Salmonella enterica serovar paratyphi B variant java between successive broiler flocks. Appl Environ Microbiol. 2008;74(22):6887–91.CrossRefPubMedPubMedCentral Hazeleger W, Bolder N, Beumer R, Jacobs-Reitsma W. Darkling beetles (Alphitobius diaperinus) and their larvae as potential vectors for the transfer of Campylobacter jejuni and Salmonella enterica serovar paratyphi B variant java between successive broiler flocks. Appl Environ Microbiol. 2008;74(22):6887–91.CrossRefPubMedPubMedCentral
15.
go back to reference Bronowski C, James C, Winstanley C. Role of environmental survival in transmission of Campylobacter jejuni. FEMS Microbiol Lett. 2014;356(1):8–19.CrossRefPubMed Bronowski C, James C, Winstanley C. Role of environmental survival in transmission of Campylobacter jejuni. FEMS Microbiol Lett. 2014;356(1):8–19.CrossRefPubMed
16.
go back to reference Pérez-Boto D, García-Peña F, Abad-Moreno J, Hurtado-Pizarro M, Pérez-Cobo I, Aurora Echeita M. Drinking water as the source of Campylobacter coli infection in grandparent heavy breeders. Avian Pathol. 2010;39(6):483–7.CrossRefPubMed Pérez-Boto D, García-Peña F, Abad-Moreno J, Hurtado-Pizarro M, Pérez-Cobo I, Aurora Echeita M. Drinking water as the source of Campylobacter coli infection in grandparent heavy breeders. Avian Pathol. 2010;39(6):483–7.CrossRefPubMed
17.
go back to reference El-Adawy H, Hotzel H, Tomaso H, Neubauer H, Hafez H. Elucidation of colonization time and prevalence of thermophilic Campylobacter species during turkey rearing using multiplex polymerase chain reaction. Poult Sci. 2012;91(2):454–9.CrossRefPubMed El-Adawy H, Hotzel H, Tomaso H, Neubauer H, Hafez H. Elucidation of colonization time and prevalence of thermophilic Campylobacter species during turkey rearing using multiplex polymerase chain reaction. Poult Sci. 2012;91(2):454–9.CrossRefPubMed
18.
go back to reference Heuer O, Pedersen K, Andersen J, Madsen M. Prevalence and antimicrobial susceptibility of thermophilic Campylobacter in organic and conventional broiler flocks. Lett Appl Microbiol. 2001;33(4):269–74.CrossRefPubMed Heuer O, Pedersen K, Andersen J, Madsen M. Prevalence and antimicrobial susceptibility of thermophilic Campylobacter in organic and conventional broiler flocks. Lett Appl Microbiol. 2001;33(4):269–74.CrossRefPubMed
19.
go back to reference Van Overbeke I, Duchateau L, Zutter L, Albers G, Ducatelle R. A comparison survey of organic and conventional broiler chickens for infectious agents affecting health and food safety. Avian Dis. 2006;50(2):196–200.CrossRefPubMed Van Overbeke I, Duchateau L, Zutter L, Albers G, Ducatelle R. A comparison survey of organic and conventional broiler chickens for infectious agents affecting health and food safety. Avian Dis. 2006;50(2):196–200.CrossRefPubMed
20.
go back to reference Rodenburg T, Hulst-van Arkel M, van der Kwakkel R. Campylobacter and Salmonella infections on organic broiler farms. NJAS Wagening J Life Sci. 2004;52:101–8.CrossRef Rodenburg T, Hulst-van Arkel M, van der Kwakkel R. Campylobacter and Salmonella infections on organic broiler farms. NJAS Wagening J Life Sci. 2004;52:101–8.CrossRef
21.
go back to reference Tuyttens F, Heyndrickx M, De Boeck M, Moreels A, Van Nuffel A, Van Poucke E, et al. Broiler chicken health, welfare and fluctuating asymmetry in organic versus conventional production systems. Livest Sci. 2008;113(2–3):123–32.CrossRef Tuyttens F, Heyndrickx M, De Boeck M, Moreels A, Van Nuffel A, Van Poucke E, et al. Broiler chicken health, welfare and fluctuating asymmetry in organic versus conventional production systems. Livest Sci. 2008;113(2–3):123–32.CrossRef
22.
go back to reference Luangtongkum T, Morishita T, Ison A, Huang S, McDermott P, Zhang Q. Effect of conventional and organic production practices on the prevalence and antimicrobial resistance of Campylobacter spp. in poultry. Appl Environ Microbiol. 2006;72(5):3600–7.CrossRefPubMedPubMedCentral Luangtongkum T, Morishita T, Ison A, Huang S, McDermott P, Zhang Q. Effect of conventional and organic production practices on the prevalence and antimicrobial resistance of Campylobacter spp. in poultry. Appl Environ Microbiol. 2006;72(5):3600–7.CrossRefPubMedPubMedCentral
23.
go back to reference ISO. Microbiology of food and animal feeding stuffs—horizontal method for detection and enumeration of Campylobacter spp. Part 1: Detection method. Geneva. International Organization for Standardization; [ISO 10272-1:2006] 2006. ISO. Microbiology of food and animal feeding stuffs—horizontal method for detection and enumeration of Campylobacter spp. Part 1: Detection method. Geneva. International Organization for Standardization; [ISO 10272-1:2006] 2006.
24.
go back to reference Ahmed M, Schulz J, Hartung J. Air samplings in a Campylobacter jejuni positive laying hen flock. Ann Agric Environ Med. 2013;20(1):16–20.PubMed Ahmed M, Schulz J, Hartung J. Air samplings in a Campylobacter jejuni positive laying hen flock. Ann Agric Environ Med. 2013;20(1):16–20.PubMed
25.
go back to reference Mathewson J, Keswick B, DuPont H. Evaluation of filters for recovery of Campylobacter jejuni from water. Appl Environ Microbiol. 1983;46(5):985–7.PubMedPubMedCentral Mathewson J, Keswick B, DuPont H. Evaluation of filters for recovery of Campylobacter jejuni from water. Appl Environ Microbiol. 1983;46(5):985–7.PubMedPubMedCentral
26.
go back to reference Hagstrum D, Klejdysz T, Subramanyam B, Nawrot J. Stored-product insect. In: Atlas of stored-product insects and mites: AACC International Press; 2009. p. 3–8. Hagstrum D, Klejdysz T, Subramanyam B, Nawrot J. Stored-product insect. In: Atlas of stored-product insects and mites: AACC International Press; 2009. p. 3–8.
27.
go back to reference Rivoal K, Denis M, Salvat G, Colin P, Ermel G. Molecular characterization of the diversity of Campylobacter spp. isolates collected from a poultry slaughterhouse: analysis of cross-contamination. Lett Appl Microbiol. 1999;29(6):370–4.CrossRefPubMed Rivoal K, Denis M, Salvat G, Colin P, Ermel G. Molecular characterization of the diversity of Campylobacter spp. isolates collected from a poultry slaughterhouse: analysis of cross-contamination. Lett Appl Microbiol. 1999;29(6):370–4.CrossRefPubMed
28.
go back to reference Hald B, Knudsen K, Lind P, Madsen M. Study of the infectivity of saline-stored Campylobacter jejuni for day-old chicks. Appl Environ Microbiol. 2001;67(5):2388–92.CrossRefPubMedPubMedCentral Hald B, Knudsen K, Lind P, Madsen M. Study of the infectivity of saline-stored Campylobacter jejuni for day-old chicks. Appl Environ Microbiol. 2001;67(5):2388–92.CrossRefPubMedPubMedCentral
29.
go back to reference Wittwer M, Keller J, Wassenaar T, Stephan R, Howald D, Regula G, et al. Genetic diversity and antibiotic resistance patterns in a Campylobacter population isolated from poultry farms in Switzerland. Appl Environ Microbiol. 2005;71(6):2840–7.CrossRefPubMedPubMedCentral Wittwer M, Keller J, Wassenaar T, Stephan R, Howald D, Regula G, et al. Genetic diversity and antibiotic resistance patterns in a Campylobacter population isolated from poultry farms in Switzerland. Appl Environ Microbiol. 2005;71(6):2840–7.CrossRefPubMedPubMedCentral
30.
go back to reference Wright S, Carver D, Siletzky R, Romine S, Morrow W, Kathariou S. Longitudinal study of prevalence of Campylobacter jejuni and Campylobacter coli from turkeys and swine grown in close proximity. J Food Prot. 2008;71(9):1791–6.PubMed Wright S, Carver D, Siletzky R, Romine S, Morrow W, Kathariou S. Longitudinal study of prevalence of Campylobacter jejuni and Campylobacter coli from turkeys and swine grown in close proximity. J Food Prot. 2008;71(9):1791–6.PubMed
31.
go back to reference Smith K, Reimers N, Barnes J, Lee B, Siletzky RM, Kathariou S. Campylobacter colonization of sibling turkey flocks reared under different management conditions. J Food Prot. 2004;67(7):1463–8.PubMed Smith K, Reimers N, Barnes J, Lee B, Siletzky RM, Kathariou S. Campylobacter colonization of sibling turkey flocks reared under different management conditions. J Food Prot. 2004;67(7):1463–8.PubMed
32.
go back to reference Kashoma I, Kumar A, Sanad Y, Gebreyes W, Kazwala R, Garabed R, et al. Phenotypic and genotypic diversity of thermophilic Campylobacter spp. in commercial turkey flocks: a longitudinal study. Foodborne Pathog Dis. 2014;11(11):850–60.CrossRefPubMedPubMedCentral Kashoma I, Kumar A, Sanad Y, Gebreyes W, Kazwala R, Garabed R, et al. Phenotypic and genotypic diversity of thermophilic Campylobacter spp. in commercial turkey flocks: a longitudinal study. Foodborne Pathog Dis. 2014;11(11):850–60.CrossRefPubMedPubMedCentral
33.
go back to reference Petersen L, Newell DG. The ability of fla-typing schemes to discriminate between strains of Campylobacter jejuni. J Appl Microbiol. 2001;91(2):217–24.CrossRefPubMed Petersen L, Newell DG. The ability of fla-typing schemes to discriminate between strains of Campylobacter jejuni. J Appl Microbiol. 2001;91(2):217–24.CrossRefPubMed
34.
go back to reference Anderson J, Horn BJ, Gilpin BJ. The prevalence and genetic diversity of Campylobacter spp. in domestic ‘backyard’ poultry in Canterbury, New Zealand. Zoonoses Public Health. 2012;59(1):52–60.CrossRefPubMed Anderson J, Horn BJ, Gilpin BJ. The prevalence and genetic diversity of Campylobacter spp. in domestic ‘backyard’ poultry in Canterbury, New Zealand. Zoonoses Public Health. 2012;59(1):52–60.CrossRefPubMed
35.
go back to reference Noormohamed A, Fakhr M. Prevalence and antimicrobial susceptibility of Campylobacter spp. in Oklahoma conventional and organic retail poultry. Open Microbiol J. 2014;8:130–7.CrossRefPubMedPubMedCentral Noormohamed A, Fakhr M. Prevalence and antimicrobial susceptibility of Campylobacter spp. in Oklahoma conventional and organic retail poultry. Open Microbiol J. 2014;8:130–7.CrossRefPubMedPubMedCentral
36.
go back to reference Bokkers E, de Boer I. Economic, ecological, and social performance of conventional and organic broiler production in the Netherlands. Brit Poult Sci. 2009;50(5):546–57.CrossRef Bokkers E, de Boer I. Economic, ecological, and social performance of conventional and organic broiler production in the Netherlands. Brit Poult Sci. 2009;50(5):546–57.CrossRef
37.
go back to reference Ridley A, Allen V, Sharma M, Harris J, Newell D. Real-time PCR approach for detection of environmental sources of Campylobacter strains colonizing broiler flocks. Appl Environ Microbiol. 2008;74(8):2492–504.CrossRefPubMedPubMedCentral Ridley A, Allen V, Sharma M, Harris J, Newell D. Real-time PCR approach for detection of environmental sources of Campylobacter strains colonizing broiler flocks. Appl Environ Microbiol. 2008;74(8):2492–504.CrossRefPubMedPubMedCentral
38.
go back to reference Humphrey T, Henley A, Lanning D. The colonization of broiler chickens with Campylobacter jejuni: some epidemiological investigations. Epidemiol Infect. 1993;110(3):601–7.CrossRefPubMedPubMedCentral Humphrey T, Henley A, Lanning D. The colonization of broiler chickens with Campylobacter jejuni: some epidemiological investigations. Epidemiol Infect. 1993;110(3):601–7.CrossRefPubMedPubMedCentral
39.
go back to reference Jacobs-Reitsma W, van de Giessen A, Bolder N, Mulder R. Epidemiology of Campylobacter spp. at two Dutch broiler farms. Epidemiol Infect. 1995;114(3):413–21.CrossRefPubMedPubMedCentral Jacobs-Reitsma W, van de Giessen A, Bolder N, Mulder R. Epidemiology of Campylobacter spp. at two Dutch broiler farms. Epidemiol Infect. 1995;114(3):413–21.CrossRefPubMedPubMedCentral
40.
go back to reference Guerin M, Martin W, Reiersen J, Berke O, McEwen S, Bisaillon J, et al. A farm-level study of risk factors associated with the colonization of broiler flocks with Campylobacter spp. in Iceland, 2001–2004. Acta Vet Scand. 2007;49(18):1–12. Guerin M, Martin W, Reiersen J, Berke O, McEwen S, Bisaillon J, et al. A farm-level study of risk factors associated with the colonization of broiler flocks with Campylobacter spp. in Iceland, 2001–2004. Acta Vet Scand. 2007;49(18):1–12.
41.
go back to reference Sasaki Y, Tsujiyama Y, Tanaka H, Yoshida S, Goshima T, Oshima K, et al. Risk factors for Campylobacter colonization in broiler flocks in Japan. Zoonoses Public Health. 2011;58(5):350–6.CrossRefPubMed Sasaki Y, Tsujiyama Y, Tanaka H, Yoshida S, Goshima T, Oshima K, et al. Risk factors for Campylobacter colonization in broiler flocks in Japan. Zoonoses Public Health. 2011;58(5):350–6.CrossRefPubMed
42.
go back to reference Miflin J, Templeton J, More S. Epidemiological studies on Campylobacter colonization in broiler flock in south east Queensland. In: Proceedings of the Australia Poulty Science Symposium, vol. 13; 2001. p. 140–3. Miflin J, Templeton J, More S. Epidemiological studies on Campylobacter colonization in broiler flock in south east Queensland. In: Proceedings of the Australia Poulty Science Symposium, vol. 13; 2001. p. 140–3.
43.
go back to reference Patriarchi A, Maunsell B, O’Mahony E, Fox Á, Fanning S, Buckley J, et al. Prevalence of Campylobacter spp. in a subset of intensive poultry flocks in Ireland. Lett Appl Microbiol. 2009;49(3):305–10.CrossRefPubMed Patriarchi A, Maunsell B, O’Mahony E, Fox Á, Fanning S, Buckley J, et al. Prevalence of Campylobacter spp. in a subset of intensive poultry flocks in Ireland. Lett Appl Microbiol. 2009;49(3):305–10.CrossRefPubMed
44.
go back to reference Gregory E, Barnhart H, Dreesen D, Stern N, Corn J. Epidemiological study of Campylobacter spp. in broilers: source, time of colonization, and prevalence. Avian Dis. 1997;41(4):890–8.CrossRefPubMed Gregory E, Barnhart H, Dreesen D, Stern N, Corn J. Epidemiological study of Campylobacter spp. in broilers: source, time of colonization, and prevalence. Avian Dis. 1997;41(4):890–8.CrossRefPubMed
45.
go back to reference Strother K, Steelman C, Gbur E. Reservoir competence of lesser mealworm (Coleoptera: Tenebrionidae) for Campylobacter jejuni (Campylobacterales: Campylobacteraceae). J Med Entomol. 2005;42(1):42–7.CrossRefPubMed Strother K, Steelman C, Gbur E. Reservoir competence of lesser mealworm (Coleoptera: Tenebrionidae) for Campylobacter jejuni (Campylobacterales: Campylobacteraceae). J Med Entomol. 2005;42(1):42–7.CrossRefPubMed
46.
go back to reference Neubauer C, Bibl D, Szolgyenyi W, Jauk V, Schmidt M, Gabler C, et al. Epidemiological investigation of Campylobacter spp. in Austrian broiler flocks: prevalence and risk factors. Wien Tierarztliche Mon. 2005;92:4–10. Neubauer C, Bibl D, Szolgyenyi W, Jauk V, Schmidt M, Gabler C, et al. Epidemiological investigation of Campylobacter spp. in Austrian broiler flocks: prevalence and risk factors. Wien Tierarztliche Mon. 2005;92:4–10.
47.
go back to reference Zimmer M, Barnhart H, Idris U, Lee M. Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens. Avian Dis. 2003;47:101–7.CrossRefPubMed Zimmer M, Barnhart H, Idris U, Lee M. Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens. Avian Dis. 2003;47:101–7.CrossRefPubMed
Metadata
Title
Prevalence, genotyping and risk factors of thermophilic Campylobacter spreading in organic turkey farms in Germany
Authors
Marwa Fawzy El Metwaly Ahmed
Hosny El-Adawy
Helmut Hotzel
Herbert Tomaso
Heinrich Neubauer
Nicole Kemper
Joerg Hartung
Hafez Mohamed Hafez
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2016
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-016-0108-2

Other articles of this Issue 1/2016

Gut Pathogens 1/2016 Go to the issue