Microbial Sharing between Pediatric Patients and Therapy Dogs during Hospital Animal-Assisted Intervention Programs
Abstract
:1. Introduction
2. Methods
2.1. Experimental Design and Sample Collection
2.2. Laboratory Processing
2.2.1. 16SS rRNA Gene Amplification and Sequencing
2.2.2. Bioinformatics and Quality Control
2.3. Statistical Analysis
3. Results
3.1. Study Population and Samples
3.2. Relative Abundance
3.3. Alpha Diversity
3.4. Beta Diversity
3.4.1. Beta Diversity Distribution
3.4.2. Beta Diversity Distance
4. Discussion
4.1. Distinct Microbial Profiles and Shifts in Patients and Therapy Dogs
4.2. Closer Contact between the Patient and Therapy Dog Increased Microbial Sharing
4.3. Canine Decolonization Intervention Modified Microbial Sharing
4.4. Strengths, Limitations, and Future Directions
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Dudzik, C. The IAHAIO Definitions for Animal Assisted Intervention and Guidelines for Wellness of Animals Involved in AAI; IAHAIO: Seattle, WA, USA, 2018. [Google Scholar]
- Santaniello, A.; Dic, F.; Claudia, R.; Amato, A.; Fioretti, A.; Menna, L.F. Methodological and Terminological Issues in Animal-Assisted Interventions: An Umbrella Review of Systematic Reviews. Animals 2020, 10, 759. [Google Scholar] [CrossRef] [PubMed]
- Bert, F.; Gualano, M.R.; Camussi, E.; Pieve, G.; Voglino, G.; Siliquini, R. Animal assisted intervention: A systematic review of benefits and risks. Eur. J. Integr. Med. 2016, 8, 695–706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Charry-Sanchez, J.D.; Pradilla, I.; Talero-Gutierrez, C. Effectiveness of Animal-Assisted Therapy in the Pediatric Population: Systematic Review and Meta-Analysis of Controlled Studies. J. Dev. Behav. Pediatr. 2018, 39, 580–590. [Google Scholar] [CrossRef]
- Kamioka, H.; Okada, S.; Tsutani, K.; Park, H.; Okuizumi, H.; Handa, S.; Oshio, T.; Park, S.; Kitayuguchi, J.; Abe, T.; et al. Effectiveness of animal-assisted therapy: A systematic review of randomized controlled trials. Complement. Ther. Med. 2014, 22, 371–390. [Google Scholar] [CrossRef] [PubMed]
- Waite, T.C.; Hamilton, L.; O’Brien, W. A meta-analysis of Animal Assisted Interventions targeting pain, anxiety and distress in medical settings. Complement. Ther. Clin. Pract. 2018, 33, 49–55. [Google Scholar] [CrossRef] [PubMed]
- Overgaauw, P.A.M.; Vinke, C.M.; van Hagen, M.A.E.; Lipman, L.J.A. A one health perspective on the human-companion animal relationship with emphasis on zoonotic aspects. Int. J. Environ. Res. Public Health 2020, 17, 3789. [Google Scholar] [CrossRef] [PubMed]
- Rabold, D.; Espelage, W.; Abu Sin, M.; Eckmanns, T.; Schneeberg, A.; Neubauer, H.; Mobius, N.; Hille, K.; Wieler, L.H.; Seyboldt, C.; et al. The zoonotic potential of Clostridium difficile from small companion animals and their owners. PLoS ONE 2018, 13, e0193411. [Google Scholar] [CrossRef]
- Springer, B.; Orendi, U.; Much, P.; Höger, G.; Ruppitsch, W.; Krziwanek, K.; Metz-Gercek, S.; Mittermayer, H. Methicillin-resistant Staphylococcus aureus: A new zoonotic agent? Wien. Klin. Wochenschr. 2009, 121, 86–90. [Google Scholar] [CrossRef]
- Boyle, S.F.; Corrigan, V.K.; Buechner-Maxwell, V.; Pierce, B.J. Evaluation of Risk of Zoonotic Pathogen Transmission in a University-Based Animal Assisted Intervention (AAI) Program. Front. Vet. Sci. 2019, 6. [Google Scholar] [CrossRef]
- Dalton, K.R.; Waite, K.B.; Ruble, K.; Carroll, K.C.; DeLone, A.; Frankenfield, P.; Serpell, J.A.; Thorpe, R.J.; Morris, D.O.; Agnew, J.; et al. Risks Associated with Animal-Assisted Intervention Programs: A Literature Review. Complement. Ther. Clin. Pract. 2020, 39, 101–145. [Google Scholar] [CrossRef]
- Lefebvre, S.L.; Reid-Smith, R.J.; Waltner-Toews, D.; Weese, J.S. Incidence of acquisition of methicillin-resistant Staphylococcus aureus, Clostridium difficile, and other healthcare-associated pathogens by dogs that participate in animal-assisted interventions. JAVMA 2009, 234, 1404–1417. [Google Scholar] [CrossRef] [Green Version]
- Hoffmann, A.R.; Patterson, A.P.; Diesel, A.; Lawhon, S.D.; Ly, H.J.; Stephenson, C.E.; Mansell, J.; Steiner, J.M.; Dowd, S.E.; Olivry, T.; et al. The skin microbiome in healthy and allergic dogs. PLoS ONE 2014, 9. [Google Scholar] [CrossRef]
- Oh, C.; Lee, K.; Cheong, Y.; Lee, S.W.; Park, S.Y.; Song, C.S.; Choi, I.S.; Lee, J.B. Comparison of the oral microbiomes of canines and their owners using next- generation sequencing. PLoS ONE 2015, 10, e0131468. [Google Scholar] [CrossRef] [Green Version]
- Swanson, K.S.; Dowd, S.E.; Suchodolski, J.S.; Middelbos, I.S.; Vester, B.M.; Barry, K.A.; Nelson, K.E.; Torralba, M.; Henrissat, B.; Coutinho, P.M.; et al. Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice. ISME J. 2011, 5, 639–649. [Google Scholar] [CrossRef]
- Misic, A.M.; Davis, M.F.; Tyldsley, A.S.; Hodkinson, B.P.; Tolomeo, P.; Hu, B.; Nachamkin, I.; Lautenbach, E.; Morris, D.O.; Grice, E.A. The shared microbiota of humans and companion animals as evaluated from Staphylococcus carriage sites. Microbiome 2015, 3, 1–19. [Google Scholar] [CrossRef] [Green Version]
- Song, S.J.; Lauber, C.; Costello, E.K.; Lozupone, C.A.; Humphrey, G.; Berg-Lyons, D.; Gregory Caporaso, J.; Knights, D.; Clemente, J.C.; Nakielny, S.; et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2013. [Google Scholar] [CrossRef]
- Azad, M.B.; Konya, T.; Maughan, H.; Guttman, D.S.; Field, C.J.; Sears, M.R.; Becker, A.B.; Scott, J.A.; Kozyrskyj, A.L. Infant gut microbiota and the hygiene hypothesis of allergic disease: Impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin. Immunol. 2013, 9, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Fall, T.; Lundholm, C.; Örtqvist, A.K.; Fall, K.; Fang, F.; Hedhammar, Å.; Kämpe, O.; Ingelsson, E.; Almqvist, C. Early exposure to dogs and farm animals and the risk of childhood asthma. JAMA Pediatr. 2015, 169, e153219. [Google Scholar] [CrossRef] [Green Version]
- Stein, M.M.; Hrusch, C.L.; Gozdz, J.; Igartua, C.; Pivniouk, V.; Murray, S.E.; Ledford, J.G.; Marques Dos Santos, M.; Anderson, R.L.; Metwali, N.; et al. Innate Immunity and Asthma Risk in Amish and Hutterite Farm Children. N. Engl. J. Med. 2016, 375, 411–421. [Google Scholar] [CrossRef] [Green Version]
- Tun, H.M.; Konya, T.; Takaro, T.K.; Brook, J.R.; Chari, R.; Field, C.J.; Guttman, D.S.; Becker, A.B.; Mandhane, P.J.; Turvey, S.E.; et al. Exposure to household furry pets influences the gut microbiota of infant at 3–4 months following various birth scenarios. Microbiome 2017, 5, 40. [Google Scholar] [CrossRef] [Green Version]
- Ludwig, S.; Jimenez-Bush, I.; Brigham, E.; Bose, S.; Diette, G.; McCormack, M.C.; Matsui, E.C.; Davis, M.F. Analysis of home dust for Staphylococcus aureus and staphylococcal enterotoxin genes using quantitative PCR. Sci. Total Environ. 2017, 581, 750–755. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fadrosh, D.W.; Bing Ma, P.G.; Sengamalay, N.; Ott, S.; Brotman, R.M.; Ravel, J. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2014, 2, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bolyen, E.; Rideout, J.R.; Dillon, M.R.; Bokulich, N.A.; Abnet, C.C.; Al-Ghalith, G.A.; Alexander, H.; Alm, E.J.; Arumugam, M.; Asnicar, F.; et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019, 37, 852–857. [Google Scholar] [CrossRef] [PubMed]
- Callahan, B.J.; Mcmurdie, P.J.; Rosen, M.J.; Han, A.W.; Johnson, A.J.A.; Holmes, S.P. DADA2: High Resolution Sample Inference from Illumina Amplicon Data. Nat. Methods 2016, 13, 581–583. [Google Scholar] [CrossRef] [Green Version]
- Katoh, K.; Misawa, K.; Kuma, K.I.; Miyata, T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002, 30, 3059–3066. [Google Scholar] [CrossRef] [Green Version]
- Price, M.N.; Dehal, P.S.; Arkin, A.P. FastTree 2—Approximately maximum-likelihood trees for large alignments. PLoS ONE 2010, 5. [Google Scholar] [CrossRef]
- Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261–5267. [Google Scholar] [CrossRef] [Green Version]
- McDonald, D.; Price, M.N.; Goodrich, J.; Nawrocki, E.P.; Desantis, T.Z.; Probst, A.; Andersen, G.L.; Knight, R.; Hugenholtz, P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012, 6, 610–618. [Google Scholar] [CrossRef]
- Davis, N.M.; Proctor, D.; Holmes, S.P.; Relman, D.A.; Callahan, B.J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 2018, 6, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Espinosa-Gongora, C.; Larsen, N.; Schonning, K.; Fredholm, M.; Guardabassi, L. Differential Analysis of the Nasal Microbiome of Pig Carriers or Non-Carriers of Staphylococcus aureus. PLoS ONE 2016, 11, e0160331. [Google Scholar] [CrossRef] [Green Version]
- McMurdie, P.J.; Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 2013, 8, e61217. [Google Scholar] [CrossRef] [Green Version]
- Willis, A. Rarefaction, alpha diversity, and statistics. Front. Microbiol. 2019, 10, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 1–21. [Google Scholar] [CrossRef] [Green Version]
- Brooks, B.; Olm, M.R.; Firek, B.A.; Baker, R.; Thomas, B.C.; Morowitz, M.J.; Banfield, J.F. Strain-resolved analysis of hospital rooms and infants reveals overlap between the human and room microbiome. Nat. Commun. 2017, 8, 1–7. [Google Scholar] [CrossRef]
- Lax, S.; Gilbert, J.A. Hospital-associated microbiota and implications for nosocomial infections. Trends Mol. Med. 2015, 21, 427–432. [Google Scholar] [CrossRef] [Green Version]
- Adams, R.I.; Bateman, A.C.; Bik, H.M.; Meadow, J.F. Microbiota of the indoor environment: A meta-analysis. Microbiome 2015, 3. [Google Scholar] [CrossRef] [Green Version]
- Oberauner, L.; Zachow, C.; Lackner, S.; Högenauer, C.; Smolle, K.H.; Berg, G. The ignored diversity: Complex bacterial communities in intensive care units revealed by 16S pyrosequencing. Sci. Rep. 2013, 3, 1–12. [Google Scholar] [CrossRef]
- Davis, E.M. Gene sequence analyses of the healthy oral microbiome in humans and companion animals: A comparative review. J. Vet. Dent. 2016, 33, 97–107. [Google Scholar] [CrossRef]
- Ross, A.A.; Müller, K.M.; Scott Weese, J.; Neufeld, J.D. Comprehensive skin microbiome analysis reveals the uniqueness of human skin and evidence for phylosymbiosis within the class Mammalia. Proc. Natl. Acad. Sci. USA 2018, 115, E5786–E5795. [Google Scholar] [CrossRef] [Green Version]
- Brooks, B.; Firek, B.A.; Miller, C.S.; Sharon, I.; Thomas, B.C.; Baker, R.; Morowitz, M.J. Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants. Microbiome 2014, 2, 1. [Google Scholar] [CrossRef] [Green Version]
- Ramos, T.; Dedesko, S.; Siegel, J.A.; Gilbert, J.A.; Stephens, B. Spatial and temporal variations in indoor environmental conditions, human occupancy, and operational characteristics in a new hospital building. PLoS ONE 2015, 10, e0118207. [Google Scholar] [CrossRef] [Green Version]
- Dalton, K.R.; Rock, C.; Carroll, K.C.; Davis, M.F. One Health in hospitals: How understanding the dynamics of people, animals, and the hospital built-environment can be used to better inform interventions for antimicrobial-resistant gram-positive infections. Antimicrob. Resist. Infect. Control 2020, 9, 78. [Google Scholar] [CrossRef]
- Morris, D.O.; Lautenbach, E.; Zaoutis, T.; Leckerman, K.; Edelstein, P.H.; Rankin, S.C. Potential for Pet Animals to Harbour Methicillin-Resistant Staphylococcus aureus When Residing with Human MRSA Patients. Zoonoses Public Health 2012, 59, 286–293. [Google Scholar] [CrossRef]
- Rodrigues, A.C.; Belas, A.; Marques, C.; Cruz, L.; Gama, L.T.; Pomba, C. Risk Factors for Nasal Colonization by Methicillin-Resistant Staphylococci in Healthy Humans in Professional Daily Contact with Companion Animals in Portugal. Microb. Drug Resist. 2018, 24, 434–446. [Google Scholar] [CrossRef]
- Havstad, S.; Wegienka, G.; Zoratti, E.M.; Lynch, S.V.; Boushey, H.A.; Nicholas, C.; Ownby, D.R.; Johnson, C.C. Effect of prenatal indoor pet exposure on the trajectory of total IgE levels in early childhood. J. Allergy Clin. Immunol. 2011, 128, 880–885. [Google Scholar] [CrossRef] [Green Version]
- Mandhane, P.J.; Sears, M.R.; Poulton, R.; Greene, J.M.; Lou, W.Y.W.; Taylor, D.R.; Hancox, R.J. Cats and dogs and the risk of atopy in childhood and adulthood. J. Allergy Clin. Immunol. 2009, 124, 745–750. [Google Scholar] [CrossRef]
- Grice, E.A.; Segre, J.A. The skin microbiome. Nat. Rev. Microbiol. 2011, 9, 244. [Google Scholar] [CrossRef] [PubMed]
- Naik, S.; Bouladoux, N.; Wilhelm, C.; Molloy, M.J.; Salcedo, R.; Kastenmuller, W.; Deming, C.; Quinones, M.; Koo, L.; Conlan, S. Compartmentalized control of skin immunity by resident commensals. Science 2012, 337, 1115–1119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
All Visits | Control Visits | Intervention Visits | |
---|---|---|---|
Study Population | |||
Patients | N (% Total) | N (% Total) | |
N total sampled | 49 *45 | 26 (53%) *23 | 23 (47%) *22 |
Male (%) | 31 (63%) | 15 (58%) | 16 (69%) |
Age (y), mean (range) | 11.68 (1.9–20.4) | 11.07 (1.9–18.4) | 12.41 (3.5–20.4) |
High Contact (%) | 25 (51%) | 12 (46%) | 13 (56%) |
Visits | N (% Total) | N (% Total) | |
Total | 13 | 8 (62%) | 5 (38%) |
Patients per visit, mean (range) | 3.77 (2–6) | 3.25 (2–5) | 4.6 (3–6) |
Therapy Dogs | |||
N Unique Dogs | 4 | ||
Male (%) | 1 (25%) | ||
Age (y), mean (range) | 6.43 (1.5–12) | ||
Samples | |||
From Patients | 79 | 43 (54%) | 36 (46%) |
From Dogs | 26 | 16 (62%) | 10 (38%) |
From Environment | 24 | 14 (58%) | 10 (42%) |
Total Samples | 129 | 73 (57%) | 56 (43%) |
Field Blanks | 12 | 7 (58%) | 5 (42%) |
Laboratory Controls | 21 | ||
Total Controls | 33 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dalton, K.R.; Ruble, K.; Redding, L.E.; Morris, D.O.; Mueller, N.T.; Thorpe, R.J., Jr.; Agnew, J.; Carroll, K.C.; Planet, P.J.; Rubenstein, R.C.; et al. Microbial Sharing between Pediatric Patients and Therapy Dogs during Hospital Animal-Assisted Intervention Programs. Microorganisms 2021, 9, 1054. https://doi.org/10.3390/microorganisms9051054
Dalton KR, Ruble K, Redding LE, Morris DO, Mueller NT, Thorpe RJ Jr., Agnew J, Carroll KC, Planet PJ, Rubenstein RC, et al. Microbial Sharing between Pediatric Patients and Therapy Dogs during Hospital Animal-Assisted Intervention Programs. Microorganisms. 2021; 9(5):1054. https://doi.org/10.3390/microorganisms9051054
Chicago/Turabian StyleDalton, Kathryn R., Kathy Ruble, Laurel E. Redding, Daniel O. Morris, Noel T. Mueller, Roland J. Thorpe, Jr., Jacqueline Agnew, Karen C. Carroll, Paul J. Planet, Ronald C. Rubenstein, and et al. 2021. "Microbial Sharing between Pediatric Patients and Therapy Dogs during Hospital Animal-Assisted Intervention Programs" Microorganisms 9, no. 5: 1054. https://doi.org/10.3390/microorganisms9051054