1887
Research Open Access
Like 0

Abstract

Background

Carriage of multidrug-resistant organisms (MDROs) in humans constitutes an important public health concern. Cross-transmission of bacteria between animals and humans has been demonstrated before.

Aim

Our aim was to quantify the risk factor ‘pet ownership’ for MDRO colonisation in hospital patients.

Methods

We performed a matched case–control study from 2019 to 2022 in Berlin, Germany and compared MDRO-positive and MDRO-negative patients in terms of contact with pets and other risk factors for MDRO acquisition. Patients completed a questionnaire-based interview and provided nasal and rectal swabs. Pet owners provided swab samples from the throat and stool of their pets (dogs and cats). Phenotypically matching samples of owners and pets were analysed via whole genome sequencing.

Results

The analyses included 2,891 patients. Reported pet ownership was 17.7% in MDRO-positives (154/871) and 23.4% in MDRO-negatives (472/2,020). Among 397 owner–pet pairs, we identified one pair sharing genotypically indistinguishable pathogens (0.3%). A risk factor analysis of pet ownership was performed for carriers of meticillin-resistant (MRSA) (OR = 0.662; 95% CI: 0.343–1.277), vancomycin-resistant enterococci (VRE) (OR = 0.764; 95% CI: 0.522–1.118) and multidrug-resistant Gram-negative bacteria (MDR-GNB) (OR = 0.819; 95% CI: 0.620–1.082). Colonisation with MDRO was rare in pets, and dogs were more often colonised than cats (MRSA: 0% vs 0%, VRE: 1.5% vs 1.0%, MDR-GNB: 17.2% vs 3.6%).

Conclusion

Transmission of MDROs between humans and pets is possible though rare. In an urban living space, neither cat nor dog ownership appears as a relevant risk factor for MDRO carriage in hospital patients.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.39.2300714
2024-09-26
2024-11-24
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.39.2300714
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/39/eurosurv-29-39-3.html?itemId=/content/10.2807/1560-7917.ES.2024.29.39.2300714&mimeType=html&fmt=ahah

References

  1. World Health Organization (WHO). Global action plan on antimicrobial resistance. Geneva: WHO; 2015. Available from: https://www.who.int/publications/i/item/9789241509763
  2. Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. , Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629-55.  https://doi.org/10.1016/S0140-6736(21)02724-0  PMID: 35065702 
  3. Berthe FCJ, Bouley T, Karesh WB, Le Gall FG, Machalaba CC, Plante CA, et al. Operational framework for strengthening human, animal and environmental public health systems at their interface. Washington, DC: World Bank Group. 2018.
  4. World Health Organization (WHO). The FAO-OIE-WHO collaboration. Sharing responsibilities and coordinating global activities to address health risks at the animal-human-ecosystems interfaces. A Tripartite Concept Note. Geneva: WHO; 2010. Available from: https://www.who.int/publications/m/item/the-fao-oie-who-collaboration
  5. Karesh WB, Dobson A, Lloyd-Smith JO, Lubroth J, Dixon MA, Bennett M, et al. Ecology of zoonoses: natural and unnatural histories. Lancet. 2012;380(9857):1936-45.  https://doi.org/10.1016/S0140-6736(12)61678-X  PMID: 23200502 
  6. Harrison EM, Weinert LA, Holden MT, Welch JJ, Wilson K, Morgan FJ, et al. A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. MBio. 2014;5(3):e00985-13.  https://doi.org/10.1128/mBio.00985-13  PMID: 24825010 
  7. Köck R, Daniels-Haardt I, Becker K, Mellmann A, Friedrich AW, Mevius D, et al. Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin Microbiol Infect. 2018;24(12):1241-50.  https://doi.org/10.1016/j.cmi.2018.04.004  PMID: 29654871 
  8. Guardabassi L, Schwarz S, Lloyd DH. Pet animals as reservoirs of antimicrobial-resistant bacteria. J Antimicrob Chemother. 2004;54(2):321-32.  https://doi.org/10.1093/jac/dkh332  PMID: 15254022 
  9. Ferreira JP, Anderson KL, Correa MT, Lyman R, Ruffin F, Reller LB, et al. Transmission of MRSA between companion animals and infected human patients presenting to outpatient medical care facilities. PLoS One. 2011;6(11):e26978.  https://doi.org/10.1371/journal.pone.0026978  PMID: 22102871 
  10. Nienhoff U, Kadlec K, Chaberny IF, Verspohl J, Gerlach GF, Schwarz S, et al. Transmission of methicillin-resistant Staphylococcus aureus strains between humans and dogs: two case reports. J Antimicrob Chemother. 2009;64(3):660-2.  https://doi.org/10.1093/jac/dkp243  PMID: 19608580 
  11. Davis MF, Misic AM, Morris DO, Moss JT, Tolomeo P, Beiting DP, et al. Genome sequencing reveals strain dynamics of methicillin-resistant Staphylococcus aureus in the same household in the context of clinical disease in a person and a dog. Vet Microbiol. 2015;180(3-4):304-7.  https://doi.org/10.1016/j.vetmic.2015.09.007  PMID: 26411322 
  12. Morgan M. Methicillin-resistant Staphylococcus aureus and animals: zoonosis or humanosis? J Antimicrob Chemother. 2008;62(6):1181-7.  https://doi.org/10.1093/jac/dkn405  PMID: 18819971 
  13. Hackmann C, Gastmeier P, Schwarz S, Lübke-Becker A, Bischoff P, Leistner R. Pet husbandry as a risk factor for colonization or infection with MDR organisms: a systematic meta-analysis. J Antimicrob Chemother. 2021;76(6):1392-405.  https://doi.org/10.1093/jac/dkab058  PMID: 33864082 
  14. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373-83.  https://doi.org/10.1016/0021-9681(87)90171-8  PMID: 3558716 
  15. Weber RE, Pietsch M, Frühauf A, Pfeifer Y, Martin M, Luft D, et al. IS26-mediated transfer of blaNDM-1 as the main route of resistance transmission during a polyclonal, multispecies outbreak in a German hospital. Front Microbiol. 2019;10:2817.  https://doi.org/10.3389/fmicb.2019.02817  PMID: 31921015 
  16. de Been M, Pinholt M, Top J, Bletz S, Mellmann A, van Schaik W, et al. Core genome multilocus sequence typing scheme for high- resolution typing of Enterococcus faecium. J Clin Microbiol. 2015;53(12):3788-97.  https://doi.org/10.1128/JCM.01946-15  PMID: 26400782 
  17. Textor J, van der Zander B, Gilthorpe MS, Liśkiewicz M, Ellison GTH. Robust causal inference using directed acyclic graphs: the R package ‘dagitty’. Int J Epidemiol. 2016;45(6):1887-94. PMID: 28089956 
  18. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2022. Available from: https://www.R-project.org
  19. Hamprecht A, Rohde AM, Behnke M, Feihl S, Gastmeier P, Gebhardt F, et al. Colonization with third-generation cephalosporin-resistant Enterobacteriaceae on hospital admission: prevalence and risk factors. J Antimicrob Chemother. 2016;71(10):2957-63.  https://doi.org/10.1093/jac/dkw216  PMID: 27317445 
  20. Rohde AM, Walker S, Behnke M, Eisenbeis S, Falgenhauer L, Falgenhauer JC, et al. Vancomycin-resistant Enterococcus faecium: admission prevalence, sequence types and risk factors-a cross-sectional study in seven German university hospitals from 2014 to 2018. Clin Microbiol Infect. 2023;29(4):515-22.  https://doi.org/10.1016/j.cmi.2022.11.025  PMID: 36481293 
  21. Bui MT, Rohde AM, Schwab F, Märtin N, Kipnis M, Boldt AC, et al. Prevalence and risk factors of colonisation with vancomycin-resistant Enterococci faecium upon admission to Germany’s largest university hospital. GMS Hyg Infect Control. 2021;16:Doc06. PMID: 33643773 
  22. McKinnell JA, Miller LG, Eells SJ, Cui E, Huang SS. A systematic literature review and meta-analysis of factors associated with methicillin-resistant Staphylococcus aureus colonization at time of hospital or intensive care unit admission. Infect Control Hosp Epidemiol. 2013;34(10):1077-86.  https://doi.org/10.1086/673157  PMID: 24018925 
  23. Jordan D, Simon J, Fury S, Moss S, Giffard P, Maiwald M, et al. Carriage of methicillin-resistant Staphylococcus aureus by veterinarians in Australia. Aust Vet J. 2011;89(5):152-9.  https://doi.org/10.1111/j.1751-0813.2011.00710.x  PMID: 21495985 
  24. Alevizakos M, Gaitanidis A, Nasioudis D, Tori K, Flokas ME, Mylonakis E. Colonization with vancomycin-resistant enterococci and risk for bloodstream infection among patients with malignancy: a systematic review and meta-analysis. Open Forum Infect Dis. 2016;4(1):ofw246.  https://doi.org/10.1093/ofid/ofw246  PMID: 28480243 
  25. Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MCJ, van Genderen PJJ, Goorhuis A, et al. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis. 2017;17(1):78-85.  https://doi.org/10.1016/S1473-3099(16)30319-X  PMID: 27751772 
  26. Westgarth C, Pinchbeck GL, Bradshaw JWS, Dawson S, Gaskell RM, Christley RM. Factors associated with dog ownership and contact with dogs in a UK community. BMC Vet Res. 2007;3(1):5.  https://doi.org/10.1186/1746-6148-3-5  PMID: 17407583 
  27. Murray JK, Browne WJ, Roberts MA, Whitmarsh A, Gruffydd-Jones TJ. Number and ownership profiles of cats and dogs in the UK. Vet Rec. 2010;166(6):163-8.  https://doi.org/10.1136/vr.b4712  PMID: 20139379 
  28. Goerge T, Lorenz MB, van Alen S, Hübner N-O, Becker K, Köck R. MRSA colonization and infection among persons with occupational livestock exposure in Europe: Prevalence, preventive options and evidence. Vet Microbiol. 2017;200:6-12.  https://doi.org/10.1016/j.vetmic.2015.10.027  PMID: 26658156 
  29. Dahms C, Hübner N-O, Kossow A, Mellmann A, Dittmann K, Kramer A. Occurrence of ESBL-producing Escherichia coli in livestock and farm workers in Mecklenburg-Western Pomerania, Germany. PLoS One. 2015;10(11):e0143326.  https://doi.org/10.1371/journal.pone.0143326  PMID: 26606146 
  30. Köck R, Cuny C. (Multidrug-resistant bacteria in animals and humans). Med Klin Intensivmed Notfmed. 2020;115(3):189-97. German.
  31. Jeon D, Chavda S, Rennert-May E, Leal J. Clinical prediction tools for identifying antimicrobial-resistant organism (ARO) carriage on hospital admissions: a systematic review. J Hosp Infect. 2023;134:11-26.  https://doi.org/10.1016/j.jhin.2023.01.003  PMID: 36657490 
  32. Hagel S, Makarewicz O, Hartung A, Weiß D, Stein C, Brandt C, et al. ESBL colonization and acquisition in a hospital population: The molecular epidemiology and transmission of resistance genes. PLoS One. 2019;14(1):e0208505.  https://doi.org/10.1371/journal.pone.0208505  PMID: 30640915 
  33. Heininger A, Zimmermann S, Bootsveld C, Boutin S, Nurjadi D. Low prevalence of combined linezolid- and vancomycin-resistant Enterococcus faecium from hospital admission screening in an endemic region in Germany. J Glob Antimicrob Resist. 2020;22:646-50.  https://doi.org/10.1016/j.jgar.2020.05.003  PMID: 32439568 
  34. Raschpichler G, Raupach-Rosin H, Akmatov MK, Castell S, Rübsamen N, Feier B, et al. Development and external validation of a clinical prediction model for MRSA carriage at hospital admission in Southeast Lower Saxony, Germany. Sci Rep. 2020;10(1):17998.  https://doi.org/10.1038/s41598-020-75094-6  PMID: 33093607 
  35. Paget J, Aangenend H, Kühn M, Hautvast J, van Oorschot D, Olde Loohuis A, et al. MRSA carriage in community outpatients: a cross-sectional prevalence study in a high-density livestock farming area along the Dutch-German border. PLoS One. 2015;10(11):e0139589.  https://doi.org/10.1371/journal.pone.0139589  PMID: 26619190 
  36. Pomba C, Rantala M, Greko C, Baptiste KE, Catry B, van Duijkeren E, et al. Public health risk of antimicrobial resistance transfer from companion animals. J Antimicrob Chemother. 2017;72(4):957-68. PMID: 27999066 
  37. Feuer L, Frenzer SK, Merle R, Leistner R, Bäumer W, Bethe A, et al. Prevalence of MRSA in canine and feline clinical samples from one-third of veterinary practices in Germany from 2019-2021. J Antimicrob Chemother. 2024;79(9):2273-80.  https://doi.org/10.1093/jac/dkae225  PMID: 39007221 
  38. Walter J, Noll I, Feig M, Weiss B, Claus H, Werner G, et al. Decline in the proportion of methicillin resistance among Staphylococcus aureus isolates from non-invasive samples and in outpatient settings, and changes in the co-resistance profiles: an analysis of data collected within the Antimicrobial Resistance Surveillance Network, Germany 2010 to 2015. BMC Infect Dis. 2017;17(1):169.  https://doi.org/10.1186/s12879-017-2271-6  PMID: 28231850 
  39. Lee AS, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers. 2018;4(1):18033.  https://doi.org/10.1038/nrdp.2018.33  PMID: 29849094 
  40. Stacey HJ, Clements CS, Welburn SC, Jones JD. The prevalence of methicillin-resistant Staphylococcus aureus among diabetic patients: a meta-analysis. Acta Diabetol. 2019;56(8):907-21.  https://doi.org/10.1007/s00592-019-01301-0  PMID: 30955124 
  41. Furuya-Kanamori L, Stone J, Yakob L, Kirk M, Collignon P, Mills DJ, et al. Risk factors for acquisition of multidrug-resistant Enterobacterales among international travellers: a synthesis of cumulative evidence. J Travel Med. 2020;27(1):taz083.  https://doi.org/10.1093/jtm/taz083  PMID: 31691808 
  42. Brown DG, Worby CJ, Pender MA, Brintz BJ, Ryan ET, Sridhar S, et al. Development of a prediction model for the acquisition of extended spectrum beta-lactam-resistant organisms in U.S. international travellers. J Travel Med. 2023;30(6):taad028.  https://doi.org/10.1093/jtm/taad028  PMID: 36864572 
  43. Dazio V, Nigg A, Schmidt JS, Brilhante M, Campos-Madueno EI, Mauri N, et al. Duration of carriage of multidrug-resistant bacteria in dogs and cats in veterinary care and co-carriage with their owners. One Health. 2021;13:100322.  https://doi.org/10.1016/j.onehlt.2021.100322  PMID: 34522760 
  44. Möbius N, Hille K, Verspohl J, Wefstaedt P, Kreienbrock L. Owner-collected swabs of pets: a method fit for the purpose of zoonoses research. Epidemiol Infect. 2013;141(9):1892-6.  https://doi.org/10.1017/S0950268812002373  PMID: 23114113 
  45. Wieler L, Rexroth U, Gottschalk R. Emerging COVID-19 success story: the challenge of maintaining progress. Exemplars in Global Health; 2023. Available from: https://www.exemplars.health/emerging-topics/epidemic-preparedness-and-response/covid-19/germany
/content/10.2807/1560-7917.ES.2024.29.39.2300714
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error