Identification of risk factors influencing Clostridium difficile prevalence in middle-size dairy farms

Veterinary Research

Volumn 47, Issue 1, 2016, Pages

  Bandelj, Petra ^a   Blagus, Rok ^a   Briski, France ^b   Frlic, Olga ^c   Vergles Rataj, Aleksandra ^a   Rupnik, Maja ^d,e,f   Ocepek, Matjaz ^a   Vengust, Modest ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b Environment and Food ^*  (Slovenia)

^c University of Maribor ^*  (Slovenia)

^d National Laboratory for Health Environment and Food   (Slovenia)

^e UNIVERSITY OF MARIBOR   (Slovenia)

^f Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BOVINE; CATTLE DISEASES; CLASSIFICATION; CLOSTRIDIUM INFECTIONS; DAIRYING; FECES; FEMALE; MICROBIOLOGY; PEPTOCLOSTRIDIUM DIFFICILE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PREVALENCE; RISK FACTOR; SLOVENIA; VETERINARY;

ANIMALS; CATTLE; CATTLE DISEASES; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; DAIRYING; FECES; FEMALE; POLYMERASE CHAIN REACTION; PREVALENCE; RISK FACTORS; SLOVENIA;

EID: 84960942974     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1186/s13567-016-0326-0     Document Type: Article

References (68)

1. CDCP (Center for Disease Control and Prevention) (2005) Severe Clostridium difficile-associated disease in populations previously at low risk-four states, 2005. MMWR Morb Mortal Wkly Rep 54:1201-1205
2. Paltansing S, van den Berg RJ, Guseinova RA, Visser CE, van der Vorm ER, Kuijper EJ (2007) Characteristics and incidence of Clostridium difficile-associated disease in The Netherlands, 2005. Clin Microbiol Infect 13:1058-1064
3. Wilcox MH, Mooney L, Bendall R, Settle CD, Fawley WN (2008) A case-control study of community-associated Clostridium difficile infection. J Antimicrob Chemother 62:388-396
4. Limbago BM, Long CM, Thompson AD, Killgore GE, Hannett GE, Havill NL, Mickelson S, Lathrop S, Jones TF, Park MM, Harriman KH, Gould LH, McDonald LC, Angulo FJ (2009) Clostridium difficile strains from community-associated infections. J Clin Microbiol 47:3004-3007
5. Keessen EC, van den Berkt AJ, Haasjes NH, Hermanus C, Kuijper EJ, Lipman LJA (2011) The relation between farm specific factors and prevalence of Clostridium difficile in slaughter pigs. Vet Microbiol 154:130-134
6. Juneau C, Mendias EN, Wagal N, Loeffelholz M, Savidge T, Croisant S, Dann S (2013) Community-acquired Clostridium difficile infection: awareness and clinical implications. J Nurse Pract 9:1-6
7. Avbersek J, Janezic S, Pate M, Rupnik M, Zidaric V, Logar K, Vengust M, Zemljic M, Pirs T, Ocepek M (2009) Diversity of Clostridium difficile in pigs and other animals in Slovenia. Anaerobe 15:252-255
8. Costa MC, Stämpfli HR, Arroyo LG, Pearl DL, Weese JS (2011) Epidemiology of Clostridium difficile on a veal farm: prevalence, molecular characterization and tetracycline resistance. Vet Microbiol 152:379-384
9. Burt SA, Siemeling L, Kuijper EJ, Lipman LJA (2012) Vermin on pig farms are vectors for Clostridium difficile PCR ribotypes 078 and 045. Vet Microbiol 160:256-258
10. Koene MGJ, Mevius D, Wagenaar JA, Harmanus C, Hensgens MPM, Meetsma AM, Putirulan FF, Van Bergen MAP, Kuijper EJ (2012) Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. Clin Microbiol Infect 18:778-784
11. Weese JS, Wakeford T, Reid-Smith R, Rousseau J, Friendship R (2010) Longitudinal investigation of Clostridium difficile shedding in piglets. Anaerobe 16:501-504
12. Frazier KS, Herron AJ, Hines ME II, Gaskin JM, Altman NH (1993) Diagnosis of enteritis and enterotoxemia due to Clostridium difficile in captive ostriches (Struthio camelus). J Vet Diagn Invest 5:623-625
13. Båverud V, Gustafsson A, Franklin A, Lindholm A, Gunnarsson A (1997) Clostridium difficile associated with acute colitis in mature horses treated with antibiotics. Equine Vet J 29:279-284
14. Gustafsson A, Båverud V, Gunnarsson A, Rantzien MH, Lindholm A, Franklin A (1997) The association of erythromycin ethylsuccinate with acute colitis in horses in Sweden. Equine Vet J 29:314-318
15. Båverud V, Franklin A, Gunnarsson A, Gustafsson A, Hellander-Edman A (1998) Clostridium difficile associated with acute colitis in mares when their foals are treated with erythromycin and rifampicin for Rhodococcus equi pneumonia. Equine Vet J 30:482-488
16. Songer JG, Post KW, Larson DJ, Jost BH, Glock RD (2000) Infection of neonatal swine with Clostridium difficile. Swine Health Prod 8:185-189
17. Båverud V, Gustafsson A, Franklin A, Aspán A, Gunnarsson A (2003) Clostridium difficile: prevalence in horses and enviroment, and antimicrobial susceptibility. Equine Vet J 35:465-471
18. Gustafsson A, Båverud V, Gunnarsson A, Pringle J, Franklin A (2004) Study of faecal shedding of Clostridium difficile in horses treated with penicillin. Equine Vet J 36:180-182
19. Clooten J, Kruth S, Arroyo L, Weese JS (2008) Prevalence and risk factors for Clostridium difficile colonization in dogs and cats hospitalized in an intensive care unit. Vet Microbiol 129:209-214
20. Hopman NEM, Keessen EC, Harmanus C, Sanders IMJG, van Leengoed LAMG, Kuijper EJ, Lipman LJA (2011) Acquisition of Clostridium difficile by piglets. Vet Microbiol 149:186-192
21. Hawken P, Weese JS, Friendship R, Warriner K (2013) Longitudinal study of Clostridium difficile and Methicillin-resistant Staphylococcus aureus associated with pigs from weaning through to the end of processing. J Food Prot 76:624-630
22. Houser BA, Soehnlen MK, Wolfgang DR, Lysczek HR, Burns CM, Jayarao BM (2012) Prevalence of Clostridium difficile toxin genes in the feces of veal calves and incidence of ground veal contamination. Foodborne Pathog Dis 9:32-36
23. Zidaric V, Pardon B, dos Vultos T, Deprez P, Brouwer MSM, Roberts AP, Henriques AO, Rupnik M (2012) Different antibiotic resistance and sporulation properties within multiclonal Clostridium difficile PCR ribotypes 078, 126, and 033 in a single calf farm. Appl Environ Microbiol 78:8515-8522
24. Rodriguez-Palacios A, Staempfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, Brazier JS, Weese JS (2006) Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis 12:1730-1736
25. European Commission. Agriculture and rural development - Family farming (2015) http://ec.europa.eu/agriculture/family-farming/index-en.htm. Accessed 20 May 2015
26. Drackley JK (2008) Calf nutrition from birth to breeding. Vet Clin North Am Food Anim Pract 24:55-86
27. Bandelj P, Logar K, Usenik AM, Vengust M, Ocepek M (2013) An improved qPCR protocol for rapid detection and quantification of Clostridium difficile in cattle feces. FEMS Microbiol Lett 341:115-121
28. Bidet P, Barbut F, Lalande V, Burghoffer B, Petit JC (1999) Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett 175:261-266
29. Janezic S, Ocepek M, Zidaric V, Rupnik M (2012) Clostridium difficile genotypes other than ribotype 078 that are prevalent among human, animal and environmental isolates. BMC Microbiol 12:48
30. Rupnik M, Avesani V, Janc M, von Eichel-Streiber C, Delmée M (1998) A novel toxinotyping scheme and correlation of toxinotypes with serogroups of Clostridium difficile isolates. J Clin Microbiol 36:2240-2247
31. Stubbs S, Rupnik M, Gibert M, Brazier J, Duerden B, Popoff M (2000) Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. FEMS Microbiol Lett 186:307-312
32. Thienpont D, Rochette F, Vanparijs OFJ (1979) Diagnosing helminthiasis through coprological examination. Janssen Research Foundation, Beerse, pp 31-34
33. Steadman RG (1979) The assessment of sultriness. Part I: a temperature-humidity index based on human physiology and clothing science. J Appl Meteor 18:861-873
34. R Core Team. R: A language and environment for statistical computing (2013) R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 20 May 2015
35. Simango C, Mwakurudza S (2008) Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int J Food Microbiol 124:268-270
36. Knight DR, Thean S, Putsathit P, Fenwick S, Riley TV (2013) Cross-sectional study reveals high prevalence of Clostridium difficile non-PCR ribotype 078 strains in Australian veal calves at slaughter. Appl Environ Microbiol 79:2630-2635
37. Hammitt MC, Bueschel DM, Keel MK, Glock RD, Cuneo P, DeYoung DW, Reggiardo C, Trinh HT, Songer JG (2008) A possible role for Clostridium difficile in the etiology of calf enteritis. Vet Microbiol 127:343-352
38. Zidaric V, Zemljic M, Janezic S, Kocuvan A, Rupnik M (2008) High diversity of Clostridium difficile genotypes isolated from a single poultry farm producing replacement laying hens. Anaerobe 14:325-327
39. CIWF (Compassion in world farming) (2013) Zoonotic diseases, human health and farm animal welfare. http://www.ciwf.org.uk/includes/documents/cm-docs/2013/z/zoonoses-4page-report.pdf. Accessed 20 May 2015
40. Schmitzberger I, Wrbka Th, Steurer B, Aschenbrenner G, Peterseil J, Zechmeister HG (2005) How farming styles influence biodiversity maintenance in Austrian agricultural landscapes. Agric Ecosyst Environ 108:274-290
41. Swagemakers P, Wiskerke H, Van Der Ploeg JD (2009) Linking birds, fields and farmers. J Environ Manage 90(Suppl 2):S185-S192
42. Schoster A, Staempfli HR, Arroyo LG, Reid-Smith RJ, Janecko N, Shewen PE, Weese JS (2012) Longitudinal study of Clostridium difficile and antimicrobial susceptibility of Escherichia coli in healthy horses in a community setting. Vet Microbiol 159:364-370
43. Romano V, Albanese F, Dumontet S, Krovacek K, Petrini O, Pasquale V (2012) Prevalence and genotypic characterization of Clostridium difficile from ruminants in Switzerland. Zoonoses Public Health 59:545-548
44. Thitaram SN, Frank JF, Lyon SA, Siragusa GR, Bailey JS, Lombard JE, Haley CA, Wagner BA, Dargatz DA, Fedorka-Cray PJ (2011) Clostridium difficile from healthy food animals: optimized isolation and prevalence. J Food Prot 74:130-133
45. Indra A, Lassnig H, Baliko N, Much P, Fiedler A, Huhulescu S, Allerberger F (2009) Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr 121:91-95
46. Pirs T, Ocepek M, Rupnik M (2008) Isolation of Clostridium difficile from food animals in Slovenia. J Med Microbiol 57:790-792
47. Rodriguez C, Taminiau B, Van Broeck J, Avesani V, Delmée M, Daube G (2012) Clostridium difficile in young farm animals and slaughter animals in Belgium. Anaerobe 18:621-625
48. Rodriguez-Palacios A, Pickworth C, Loerch S, LeJeune JT (2011) Transient fecal shedding and limited animal-to-animal transmission of Clostridium difficile by naturally infected finishing feedlot cattle. Appl Environ Microbiol 77:3391-3397
49. Costa MC, Reid-Smith R, Gow S, Hannon SJ, Booker C, Rousseau J, Benedict KM, Morley PS, Weese JS (2012) Prevalence and molecular characterization of Clostridium difficile isolated from feedlot beef cattle upon arrival and mid-feeding period. BMC Vet Res 8:38
50. Keel K, Brazier JS, Post KW, Weese JS, Songer JG (2007) Prevalence of PCR Ribotypes among Clostridium difficile isolates from pigs, calves, and other species. J Clin Microbiol 45:1963-1964
51. Janezic S, Zidaric V, Pardon B, Indra A, Kokotovic B, Blanco JL, Seyboldt C, Diaz CR, Poxton IR, Perreten V, Drigo I, Jiraskova A, Ocepek M, Weese JS, Songer JG, Wilcox MH, Rupnik M (2014) International Clostridium difficile animal strain collection and large diversity of animal associated strains. BMC Microbiol 14:173
52. Hensgens MP, Goorhuis A, Notermans DW, van Benthem BH, Kuijper EJ (2009) Decrease of hypervirulent Clostridium difficile PCR ribotype 027 in the Netherlands. Euro Surveill 14:19402
53. Skraban J, Dzeroski S, Zenko B, Mongus D, Gangi S, Rupnik M (2013) Gut microbiota patterns associated with colonization of different Clostridium difficile ribotypes. PLoS One 8:e58005
54. Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS (2007) Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis 13:485-487
55. Rodriguez-Palacios A, Reid-Smith RJ, Staempfli HR, Daignault D, Janecko N, Avery BP, Martin H, Thomspon AD, McDonald LC, Limbago B, Weese JS (2009) Possible seasonality of Clostridium difficile in retail meat, Canada. Emerg Infect Dis 15:802-805
56. Hofer E, Haechler H, Frei R, Stephan R (2010) Low occurrence of Clostridium difficile in fecal samples of healthy calves and pigs at slaughter and in minced meat in Switzerland. J Food Prot 73:973-975
57. Sambol SP, Merrigan MM, Tang JK, Johnson S, Gerding DN (2002) Colonization for the prevention of Clostridium difficile disease in hamsters. J Infect Dis 186:1781-1789
58. Songer JG, Jones R, Anderson MA, Barbara AJ, Post KW, Trinh HT (2007) Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms. Vet Microbiol 124:358-361
59. Godden S, Feirtag J, Green L, Wells S, Fetrow J (2003) A review of issues surrounding the feeding of waste milk and pasteurization of waste milk and colostrum. Proceedings of the Minnesota Dairy Health Conference, 2003. College of Veterinary Medicine, University of Minnesota. http://purl.umn.edu/108982 Accessed 27 January 2016
60. Struble AL, Tang YJ, Kass PH, Gumerlock PH, Madewell BR, Silva J Jr (1994) Fecal shedding of Clostridium difficile in dogs: a period prevalence survey in a veterinary medical teaching hospital. J Vet Diagn Invest 6:342-347
61. Yaeger MJ, Kinyon JM, Songer JG (2007) A prospective, case control study evaluating the association between Clostridium difficile toxins in the colon of neonatal swine and gross and microscopic lesions. J Vet Diagn Invest 19:52-59
62. Alvarez-Perez S, Blanco JL, Bouza E, Alba P, Gibert X, Maldonado J, Garcia ME (2009) Prevalence of Clostridium difficile in diarrhoeic and non-diarrhoeic piglets. Vet Microbiol 137:302-305
63. Hammitt MC, Bueschel DM, Keel MK, Glock RD, Cuneo P, DeYoung DW, Reggiardo C, Trinh HT, Songer JG (2008) A possible role for Clostridium difficile in the etiology of calf enteritis. Vet Microbiol 127:343-352
64. Slovis NM, Elam J, Estrada M, Leutenegger CM (2014) Infectious agents associated with diarrhoea in neonatal foals in central Kentucky: a comprehensive molecular study. Equine Vet J 46:311-316
65. West JW (2003) Effect of heat-stress on production in dairy cattle. J Dairy Sci 86:2131-2144
66. Bohmanova J, Misztal I, Cole JB (2007) Temperature-humidity indices as indicators of milk production losses due to heat stress. J Dairy Sci 90:1947-1956
67. Norman KN, Harvey RB, Scott HM, Hume ME, Andrews K, Brawley AD (2009) Varied prevalence of Clostridium difficile in an integrated swine operation. Anaerobe 15:256-260
68. Smith DL, Smith T, Rude BJ, Ward SH (2013) Short communication: comparison of the effects of heat stress on milk and component yields and somatic cell score in Holstein and Jersey cows. J Dairy Sci 96:3028-3033