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Association of Household Pets, Common Dietary Factors, and Lifestyle Factors with Clostridium difficile Infection

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Abstract

Background

Clostridium difficile infection (CDI) is one of the most common hospital-acquired infections and is associated with significant morbidity and mortality. Since owning a cat or dog could enrich the gut microbiome, we hypothesized that it would be protective against CDI.

Aims

We conducted a survey study on patients tested for CDI in order to assess whether living in the presence of a pet is associated with a decreased risk of CDI.

Methods

We surveyed subjects aged 18–90 over a 14-month period using a retrospective case–control design. Subjects with CDI were matched by gender and age to patients who tested negative and had no prior history of CDI. A web-based survey was provided to subjects by mail or assisted by phone. Conditional logistic regression was used to assess for associations between CDI and the various risk factors.

Results

205 CDI positive and 205 CDI negative subjects (response rate of 50.2%) were included. After matching for age and sex, living with a cat or dog was not associated with negative CDI testing. Exploratory multivariable modeling identified an unexpected association between positive CDI testing and high meat intake (OR 2.13, 95% CI 1.21–3.77) as well as between positive CDI testing and cat allergies (OR 1.88, 95% CI 1.02–3.46).

Conclusion

Living with a cat or dog was not associated with negative CDI testing. Several novel risk factors for CDI have been identified including high meat intake and cat allergies.

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Abbreviations

ADL:

Activity of daily living

CDI:

Clostridium difficile infection

EIA:

Enzyme immunoassay

GI:

Gastrointestinal

H2RA:

Histamine 2 receptor antagonists

PPI:

Proton pump inhibitor

SAR:

Subacute rehabilitation facility

SNF:

Skilled nursing facility

Th:

T helper

References

  1. Magill SS, Edwards JR, Bamberg W, et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med. 2014;370:1198–1208.

    Article  CAS  Google Scholar 

  2. Hall AJ, Curns AT, McDonald LC, Parashar UD, Lopman BA. The roles of Clostridium difficile and norovirus among gastroenteritis-associated deaths in the United States, 1999–2007. Clin Infect Dis. 2012;55:216–223.

    Article  Google Scholar 

  3. Lessa FC, Winston LG, McDonald LC, Team EIPCdS. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372:2369–2370.

    Article  Google Scholar 

  4. Zhang S, Palazuelos-Munoz S, Balsells EM, Nair H, Chit A, Kyaw MH. Cost of hospital management of Clostridium difficile infection in United States-a meta-analysis and modelling study. BMC Infect Dis. 2016;16:447.

    Article  Google Scholar 

  5. Peled N, Pitlik S, Samra Z, Kazakov A, Bloch Y, Bishara J. Predicting Clostridium difficile toxin in hospitalized patients with antibiotic-associated diarrhea. Infect Control Hosp Epidemiol. 2007;28:377–381.

    Article  Google Scholar 

  6. Dial S, Delaney JA, Barkun AN, Suissa S. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA. 2005;294:2989–2995.

    Article  CAS  Google Scholar 

  7. Al-Tureihi FI, Hassoun A, Wolf-Klein G, Isenberg H. Albumin, length of stay, and proton pump inhibitors: key factors in Clostridium difficile-associated disease in nursing home patients. J Am Med Dir Assoc. 2005;6:105–108.

    Article  Google Scholar 

  8. Chang JY, Antonopoulos DA, Kalra A, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197:435–438.

    Article  Google Scholar 

  9. Ooi JH, Li Y, Rogers CJ, Cantorna MT. Vitamin D regulates the gut microbiome and protects mice from dextran sodium sulfate-induced colitis. J Nutr. 2013;143:1679–1686.

    Article  CAS  Google Scholar 

  10. Preidis GA, Versalovic J. Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology. 2009;136:2015–2031.

    Article  CAS  Google Scholar 

  11. Chen HM, Yu YN, Wang JL, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr. 2013;97:1044–1052.

    Article  CAS  Google Scholar 

  12. Stein MM, Hrusch CL, Gozdz J, et al. Innate immunity and asthma risk in Amish and Hutterite farm children. N Engl J Med. 2016;375:411–421.

    Article  CAS  Google Scholar 

  13. Álvarez-Pérez S, Blanco JL, Harmanus C, Kuijper EJ, García ME. Prevalence and characteristics of Clostridium perfringens and Clostridium difficile in dogs and cats attended in diverse veterinary clinics from the Madrid region. Anaerobe. 2017;48:47–55.

    Article  Google Scholar 

  14. Wei Y, Sun M, Zhang Y, et al. Prevalence, genotype and antimicrobial resistance of Clostridium difficile isolates from healthy pets in Eastern China. BMC Infect Dis. 2019;19:46.

    Article  Google Scholar 

  15. Orden C, Blanco JL, Álvarez-Pérez S, et al. Isolation of Clostridium difficile from dogs with digestive disorders, including stable metronidazole-resistant strains. Anaerobe. 2017;43:78–81.

    Article  Google Scholar 

  16. Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of illness in the aged. The index of ADL: a standardized measure of biological and psychosocial function. JAMA. 1963;185:914–919.

    Article  CAS  Google Scholar 

  17. VanderWeele TJ, Ding P. Sensitivity analysis in observational research: introducing the E-value. Ann Intern Med. 2017;167:268–274.

    Article  Google Scholar 

  18. Jarvis WR, Schlosser J, Jarvis AA, Chinn RY. National point prevalence of Clostridium difficile in US health care facility inpatients, 2008. Am J Infect Control. 2009;37:263–270.

    Article  Google Scholar 

  19. Simor AE, Bradley SF, Strausbaugh LJ, Crossley K, LE Nicolle, Committee SL-T-C. Clostridium difficile in long-term-care facilities for the elderly. Infect Control Hosp Epidemiol. 2002;23:696–703.

    Article  Google Scholar 

  20. Campbell RJ, Giljahn L, Machesky K, et al. Clostridium difficile infection in Ohio hospitals and nursing homes during 2006. Infect Control Hosp Epidemiol. 2009;30:526–533.

    Article  Google Scholar 

  21. Songer JG, Trinh HT, Killgore GE, Thompson AD, McDonald LC, Limbago BM. Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis. 2009;15:819–821.

    Article  CAS  Google Scholar 

  22. Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS. Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis. 2007;13:485–487.

    Article  CAS  Google Scholar 

  23. Zhu Y, Lin X, Zhao F, et al. Meat, dairy and plant proteins alter bacterial composition of rat gut bacteria. Sci Rep. 2015;5:15220.

    Article  CAS  Google Scholar 

  24. Zhu Y, Lin X, Li H, et al. Intake of meat proteins substantially increased the relative abundance of genus lactobacillus in rat feces. PLoS ONE. 2016;11:e0152678.

    Article  Google Scholar 

  25. Ben Q, Sun Y, Chai R, Qian A, Xu B, Yuan Y. Dietary fiber intake reduces risk for colorectal adenoma: a meta-analysis. Gastroenterology. 2014;146:689–699.e686.

    Article  CAS  Google Scholar 

  26. Abt MC, Lewis BB, Caballero S, et al. Innate immune defenses mediated by two ILC subsets are critical for protection against Acute Clostridium difficile infection. Cell Host Microbe. 2015;18:27–37.

    Article  CAS  Google Scholar 

  27. Trifan A, Stanciu C, Girleanu I, et al. Proton pump inhibitors therapy and risk of Clostridium difficile infection: systematic review and meta-analysis. World J Gastroenterol. 2017;23:6500–6515.

    Article  CAS  Google Scholar 

  28. Allegretti JR, Kao D, Phelps E, et al. Risk of Clostridium difficile infection with systemic antimicrobial therapy following successful fecal microbiota transplant: should we recommend anti-Clostridium difficile antibiotic prophylaxis? Dig Dis Sci. 2019;64:1668–1671. https://doi.org/10.1007/s10620-018-5450-4.

    Article  CAS  Google Scholar 

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Funding

Grant support: JAB is supported by T32 DK062708.

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Authors and Affiliations

  1. Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of Michigan, 1500 E. Medical Center Drive, Ann Arbor, MI, 48109, USA

    Jeffrey A. Berinstein, Calen A. Steiner, Katelin J. Roth, Emily Briggs & Peter D. R. Higgins

  2. Institute for Healthcare Policy and Innovation, University of Michigan, Ann Arbor, MI, USA

    Jeffrey A. Berinstein

  3. Division of Infectious Disease, Department of Internal Medicine, University of Michigan, Ann Arbor, MI, USA

    Krishna Rao

Authors
  1. Jeffrey A. Berinstein
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  2. Calen A. Steiner
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  3. Katelin J. Roth
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  4. Emily Briggs
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  5. Krishna Rao
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  6. Peter D. R. Higgins
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Contributions

PDRH, KR, JAB, and EB contributed to study concept and design; JAB and KJR were involved in acquisition; JAB, KR and PDRH drafted the manuscript; JAB contributed to figures; all authors worked for analysis, interpretation of data, critical revision of the manuscript, and final approval.

Corresponding author

Correspondence to Jeffrey A. Berinstein.

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Conflict of interest

PDRH received consulting fees from AbbVie, Amgen, Genentech, JBR Pharma, and Lycera. All other authors report no disclosures.

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Berinstein, J.A., Steiner, C.A., Roth, K.J. et al. Association of Household Pets, Common Dietary Factors, and Lifestyle Factors with Clostridium difficile Infection. Dig Dis Sci 66, 206–212 (2021). https://doi.org/10.1007/s10620-020-06123-7

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  • DOI: https://doi.org/10.1007/s10620-020-06123-7

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