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

Farm animals have been suggested to play an important role in the epidemiology of Clostridium difficile infection (CDI) in the community. The purpose of this study was to evaluate risk factors associated with C. difficile dissemination in family dairy farms, which are the most common farming model in the European Union. Environmental samples and fecal samples from cows and calves were collected repeatedly over a 1 year period on 20 mid-size family dairy farms. Clostridium difficile was detected in cattle feces on all farms using qPCR. The average prevalence between farms was 10% (0–44.4%) and 35.7% (3.7–66.7%) in cows and calves, respectively. Bacterial culture yielded 103 C. difficile isolates from cattle and 61 from the environment. Most C. difficile isolates were PCR-ribotype 033. A univariate mixed effect model analysis of risk factors associated dietary changes with increasing C. difficile prevalence in cows (P = 0.0004); and dietary changes (P = 0.004), breeding Simmental cattle (P = 0.001), mastitis (P = 0.003) and antibiotic treatment (P = 0.003) in calves. Multivariate analysis of risk factors found that dietary changes in cows (P = 0.0001) and calves (P = 0.002) increase C. difficile prevalence; mastitis was identified as a risk factor in calves (P = 0.001). This study shows that C. difficile is common on dairy farms and that shedding is more influenced by farm management than environmental factors. Based on molecular typing of C. difficile isolates, it could also be concluded that family dairy farms are currently not contributing to increased CDI incidence.

• Publication year

  2016

• Venue

  Veterinary Research

• Publication date

  2016-03-12

• Fields of study

  Agricultural and Food Sciences, Medicine, Biology, Environmental Science

• Identifiers
  DOI 10.1186/s13567-016-0326-0PMID 26968527PMCID 4788955
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• R: A language and environment for statistical computing.

  2014cited by this paper
• International Clostridium difficile animal strain collection and large diversity of animal associated strains

  2014influential reference
• Short communication: comparison of the effects of heat stress on milk and component yields and somatic cell score in Holstein and Jersey cows.

  2013cited by this paper
• Community-Acquired Clostridium Difficile Infection: Awareness and Clinical Implications.

  2013cited by this paper
• An improved qPCR protocol for rapid detection and quantification of Clostridium difficile in cattle feces.

  2013influential reference
• Cross-Sectional Study Reveals High Prevalence of Clostridium difficile Non-PCR Ribotype 078 Strains in Australian Veal Calves at Slaughter

  2013influential reference
• Infectious agents associated with diarrhoea in neonatal foals in central Kentucky: A comprehensive molecular study

  2013cited by this paper
• Gut Microbiota Patterns Associated with Colonization of Different Clostridium difficile Ribotypes

  2013cited by this paper
• Longitudinal study of Clostridium difficile and Methicillin-resistant Staphylococcus aureus associated with pigs from weaning through to the end of processing.

  2013cited by this paper
• Clostridium difficile genotypes other than ribotype 078 that are prevalent among human, animal and environmental isolates

  2012cited by this paper
• Vermin on pig farms are vectors for Clostridium difficile PCR ribotypes 078 and 045.

  2012cited by this paper
• Prevalence and molecular characterization of Clostridium difficile isolated from feedlot beef cattle upon arrival and mid-feeding period

  2012cited by this paper
• Prevalence of Clostridium difficile Toxin Genes in the Feces of Veal Calves and Incidence of Ground Veal Contamination

  2012cited by this paper
• Clostridium difficile in young farm animals and slaughter animals in Belgium.

  2012cited by this paper
• Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates.

  2012influential reference
• Prevalence and Genotypic Characterization of Clostridium difficile From Ruminants in Switzerland

  2012influential reference
• Longitudinal study of Clostridium difficile and antimicrobial susceptibility of Escherichia coli in healthy horses in a community setting.

  2012cited by this paper
• Different Antibiotic Resistance and Sporulation Properties within Multiclonal Clostridium difficile PCR Ribotypes 078, 126, and 033 in a Single Calf Farm

  2012influential reference
• Transient Fecal Shedding and Limited Animal-to-Animal Transmission of Clostridium difficile by Naturally Infected Finishing Feedlot Cattle

  2011cited by this paper
• The relation between farm specific factors and prevalence of Clostridium difficile in slaughter pigs.

  2011cited by this paper
• Acquisition of Clostridium difficile by piglets.

  2011cited by this paper
• Clostridium difficile from healthy food animals: optimized isolation and prevalence.

  2011cited by this paper
• Epidemiology of Clostridium difficile on a veal farm: prevalence, molecular characterization and tetracycline resistance.

  2011cited by this paper
• Clostridium difficile: prevalence in horses and environment, and antimicrobial susceptibility.

  2010cited by this paper
• Study of faecal shedding of Clostridium difficile in horses treated with penicillin.

  2010cited by this paper
• Low occurrence of Clostridium difficile in fecal samples of healthy calves and pigs at slaughter and in minced meat in Switzerland.

  2010cited by this paper
• Longitudinal investigation of Clostridium difficile shedding in piglets.

  2010cited by this paper
• Linking birds, fields and farmers.

  2009cited by this paper
• Prevalence of Clostridium difficile in diarrhoeic and non-diarrhoeic piglets.

  2009cited by this paper
• Decrease of hypervirulent Clostridium difficile PCR ribotype 027 in the Netherlands.

  2009influential reference
• Possible Seasonality of Clostridium difficile in Retail Meat, Canada

  2009cited by this paper
• Diversity of Clostridium difficile in pigs and other animals in Slovenia.

  2009influential reference
• Clostridium difficile Strains from Community-Associated Infections

  2009cited by this paper
• Varied prevalence of Clostridium difficile in an integrated swine operation.

  2009cited by this paper
• Calf nutrition from birth to breeding.

  2008cited by this paper
• Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility.

  2008influential reference
• Clostridium difficile: a new zoonotic agent?

  2008cited by this paper
• High diversity of Clostridium difficile genotypes isolated from a single poultry farm producing replacement laying hens.

  2008cited by this paper
• Isolation of Clostridium difficile from food animals in Slovenia.

  2008influential reference
• A case-control study of community-associated Clostridium difficile infection.

  2008cited by this paper
• Prevalence and risk factors for Clostridium difficile colonization in dogs and cats hospitalized in an intensive care unit.

  2008cited by this paper
• A Prospective, Case Control Study Evaluating the Association between Clostridium Difficile Toxins in the Colon of Neonatal Swine and Gross and Microscopic Lesions

  2007cited by this paper
• Prevalence of PCR Ribotypes among Clostridium difficile Isolates from Pigs, Calves, and Other Species

  2007influential reference
• Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms.

  2007influential reference
• A possible role for Clostridium difficile in the etiology of calf enteritis

  2007cited by this paper
• Characteristics and incidence of Clostridium difficile-associated disease in The Netherlands, 2005.

  2007cited by this paper
• Temperature-humidity indices as indicators of milk production losses due to heat stress.

  2007cited by this paper
• Clostridium difficile in Retail Ground Meat, Canada

  2007cited by this paper
• Clostridium difficile PCR Ribotypes in Calves, Canada

  2006cited by this paper
• How farming styles influence biodiversity maintenance in Austrian agricultural landscapes

  2005cited by this paper
• Severe Clostridium difficile-associated disease in populations previously at low risk--four states, 2005.

  2005cited by this paper
• A REVIEW OF ISSUES SURROUNDING THE FEEDING OF WASTE MILK AND PASTEURIZATION OF WASTE MILK AND COLOSTRUM

  2004cited by this paper
• Effects of heat-stress on production in dairy cattle.

  2003cited by this paper
• Colonization for the Prevention of Clostridium difficile Disease in Hamsters

  2002cited by this paper
• Infection of neonatal swine with Clostridium difficile

  2000cited by this paper
• Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile.

  2000cited by this paper
• Colonization for the prevention of Clostridium difficile disease in hamsters.

  1999cited by this paper
• Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing.

  1999cited by this paper
• A Novel Toxinotyping Scheme and Correlation of Toxinotypes with Serogroups of Clostridium difficileIsolates

  1998cited by this paper
• Clostridium difficile associated with acute colitis in mares when their foals are treated with erythromycin and rifampicin for Rhodococcus equi pneumonia.

  1998cited by this paper
• The association of erythromycin ethylsuccinate with acute colitis in horses in Sweden.

  1997cited by this paper
• Clostridium difficile associated with acute colitis in mature horses treated with antibiotics.

  1997cited by this paper
• Fecal Shedding of Clostridium Difficile in Dogs: A Period Prevalence Survey in a Veterinary Medical Teaching Hospital

  1994cited by this paper
• Diagnosis of Enteritis and Enterotoxemia due to Clostridium Difficile in Captive Ostriches (Struthio Camelus)

  1993cited by this paper
• Diagnosing Helminthiasis Through Coprological Examination.

  1981cited by this paper
• The Assessment of Sultriness. Part I: A Temperature-Humidity Index Based on Human Physiology and Clothing Science

  1979cited by this paper

• Clostridioides difficile infection in animals: a literature review.

  2026cites this paper
• Clostridioides difficile in feral horse populations in Australia

  2025cites this paper
• Comparison of Anaerobic Culture Methods for Detecting Clostridioides difficile in Bovine Faeces

  2024cites this paper
• Genomic study of European Clostridioides difficile ribotype 002/sequence type 8

  2024cites this paper
• Effects of supplementing direct-fed microbials on health and growth of pre-weaning Gyr × Holstein dairy calves.

  2024cites this paper
• Non-human Clostridioides difficile Reservoirs and Sources: Animals, Food, Environment.

  2024cites this paper
• Clostridioides difficile in calves, cattle and humans from Dutch dairy farms: Predominance of PCR ribotype 695 (clade 5, sequence type 11) in cattle

  2024cites this paper
• Presence of Clostridioides difficile on Spinach, Carrots, Cheese and Milk in Turkey.

  2024cites this paper
• Clostridioides difficile in Pigs and Dairy Cattle in Northern Italy: Prevalence, Characterization and Comparison between Animal and Human Strains

  2023cites this paper
• Genomic Analysis of Clostridioides difficile Recovered from Horses in Western Australia

  2023cites this paper
• Clostridioides difficile in South American Camelids in Germany: First Insights into Molecular and Genetic Characteristics and Antimicrobial Resistance

  2023cites this paper
• Clostridioides difficile infection and One Health: an equine perspective

  2022cites this paper
• Clostridioides difficile infection: an emerging zoonosis?

  2021cites this paper
• Survival of Clostridioides difficile in finished dairy compost under controlled conditions

  2021cites this paper
• The prevalence of Clostridioides difficile on farms, in abattoirs and in retail foods in Ireland.

  2021cites this paper
• An investigation of the survival and/or growth of Clostridioides (Clostridium) difficile in beef stored under aerobic, anaerobic and commercial vacuum packaging conditions at 2 °C and 20 °C

  2021cites this paper
• Clostridioides difficile in Calves in Central Italy: Prevalence, Molecular Typing, Antimicrobial Susceptibility and Association with Antibiotic Administration

  2021cites this paper
• Isolation, Identification and Function of Pichia anomala AR2016 and Its Effects on the Growth and Health of Weaned Pigs

  2021cites this paper
• Raw milk and fecal microbiota of commercial Alpine dairy cows varies with herd, fat content and diet

  2020cites this paper
• Clostridium (Clostridioides) difficile in animals

  2020cites this paper
• The Colonisation of Calves in Czech Large-Scale Dairy Farms by Clonally-Related Clostridioides difficile of the Sequence Type 11 Represented by Ribotypes 033 and 126

  2020cites this paper
• Incidence and Profiles of Antibiotic Resistance and Putative Genes of the Clostridium difficile Recovered From Fish

  2020cites this paper
• Evaluation of the occurrence of sporulating and nonsporulating pathogenic bacteria in manure and in digestate of five agricultural biogas plants

  2019cites this paper
• Genomic Delineation of Zoonotic Origins of Clostridium difficile

  2019cites this paper
• Clostridioides difficile in bat guano.

  2019cites this paper
• Thermal resistance of Clostridium difficile endospores in dairy compost upon exposure to wet and dry heat treatments

  2019cites this paper
• CONTAMINATION OF THE ENVIRONMENT BY PATHOGENIC BACTERIA IN A LIVESTOCK FARM IN LIMPOPO PROVINCE, SOUTH AFRICA

  2019cites this paper
• Quantification of Clostridioides (Clostridium) difficile in feces of calves of different age and determination of predominant Clostridioides difficile ribotype 033 relatedness and transmission between family dairy farms using multilocus variable-number tandem-repeat analysis

  2018cites this paper
• Clostridium difficile colitis and zoonotic origins—a narrative review

  2018cites this paper
• Non-human C. difficile Reservoirs and Sources: Animals, Food, Environment.

  2018cites this paper
• Wild mice in and around the city of Utrecht, the Netherlands, are carriers of Clostridium difficile but not ESBL‐producing Enterobacteriaceae, Salmonella spp. or MRSA

  2018cites this paper
• Clostridial Abomasitis and Enteritis in Ruminants

  2018cites this paper
• Neonatal Dönem Buzağı İshallerinde Clostridium difficile

  2018cites this paper
• Retracted: Prevalence, antibiotic resistance, and toxigenic gene profile of the Clostridium difficile isolated from molluscan shellfish

  2018cites this paper
• Risk factors associated with fecal shedding of Listeria monocytogenes by dairy cows and calves

  2018cites this paper
• Clostridium difficile in beef cattle farms, farmers and their environment: Assessing the spread of the bacterium.

  2017cites this paper
• Annual Surveillance Summary: Clostridium difficile Infections in the Military Health System (MHS), 2016

  2017cites this paper
• Dissemination of Clostridium difficile in food and the environment: Significant sources of C. difficile community‐acquired infection?

  2017influential citation
• Antimicrobial Susceptibility Patterns of Clostridium difficile Isolates from Family Dairy Farms

  2017cites this paper
• Review on Usage of Vancomycin in Livestock and Humans: Maintaining Its Efficacy, Prevention of Resistance and Alternative Therapy

  2017cites this paper
• nega-Effects of supplementing direct-fed microbials on health and growth of pre-weaning Gyr × Holstein dairy calves

  year unknowncites this paper