Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-23T21:47:46.191Z Has data issue: false hasContentIssue false

Patients as Patches: Ecology and Epidemiology in Healthcare Environments

Published online by Cambridge University Press:  20 October 2016

Eric T. Lofgren
Affiliation:
Paul G. Allen School for Global Animal Health, Washington State University, Pullman, Washington Community Health Analytics Initiative, Washington State University, Pullman, Washington The Command, Control and Interoperability Center for Advanced Data Analysis (CCICADA), Piscataway, New Jersey
Andrea M. Egizi
Affiliation:
Tick-Borne Disease Laboratory, Monmouth County Mosquito Control Division, Tinton Falls, New Jersey Center for Vector Biology, Department of Entomology, Rutgers University, New Brunswick, New Jersey
Nina H. Fefferman*
Affiliation:
The Command, Control and Interoperability Center for Advanced Data Analysis (CCICADA), Piscataway, New Jersey Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee
*
Address correspondence to Nina H. Fefferman, Department of Ecology and Evolutionary Biology, 569 Dabney Hall, Knoxville, TN 37996-1610 (feffermn@dimacs.rutgers.edu).

Abstract

The modern healthcare system involves complex interactions among microbes, patients, providers, and the built environment. It represents a unique and challenging setting for control of the emergence and spread of infectious diseases. We examine an extension of the perspectives and methods from ecology (and especially urban ecology) to address these unique issues, and we outline 3 examples: (1) viewing patients as individual microbial ecosystems; (2) the altered ecology of infectious diseases specifically within hospitals; and (3) ecosystem management perspectives for infection surveillance and control. In each of these cases, we explore the accuracy and relevance of analogies to existing urban ecological perspectives, and we demonstrate a few of the potential direct uses of this perspective for altering research into the control of healthcare-associated infections.

Infect Control Hosp Epidemiol. 2016;1507–1512

Type
Commentaries
Copyright
© 2016 by The Society for Healthcare Epidemiology of America. All rights reserved 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1. McDonnell, MJ. The history of urban ecology: an ecologist’s perspective. In: Niemelä J, Breuste JH, Elmqvist T, Guntenspergen PJ, McIntyre NE, eds. Urban Ecology: Patterns, Processes, and Applications. Oxford, UK: Oxford University Press; 2011:513.Google Scholar
2. Grimm, NB, Faeth, SH, Golubiewski, NE, et al. Global change and the ecology of cities. Science 2008;319:756760.Google Scholar
3. Alberti, M. The effects of urban patterns on ecosystem function. Int Reg Sci Rev 2005;28:168192.CrossRefGoogle Scholar
4. McKinney, M. Effects of urbanization on species richness: a review of plants and animals. Urban Ecosys 2008;11:161176.Google Scholar
5. King, G. Urban microbiomes and urban ecology: How do microbes in the built environment affect human sustainability in cities? J Microbiol 2014;52:721728.Google Scholar
6. Calfee, DP. Crisis in hospital-acquired, healthcare-associated infections. Ann Rev Med 2012;63:359371.Google Scholar
7. Galea, S, Vlahov, D. Urban health: evidence, challenges, and directions. Annu Rev Public Health 2005;26:341365.Google Scholar
8. Lee, BY, Bartsch, SM, Wong, KF, et al. The importance of nursing homes in the spread of methicillin-resistant Staphylococcus aureus (MRSA) among hospitals. Med Care 2013;51:205215.Google Scholar
9. Pickett, STA, White, PS. eds. The Ecology of Natural Disturbance and Patch Dynamics. San Diego, CA: Academic Press; 1985.Google Scholar
10. Hilty, JA, Lidicker, WZ Jr, Merenlender, AM. Corridor Ecology: The Science and Practice of Linking Landscapes for Biodiversity Conservation. Washington, DC: Island Press; 2006.Google Scholar
11. Jesse, M, Ezanno, P, Davis, S, Heesterbeek, JAP. A fully coupled, mechanistic model for infectious disease dynamics in a metapopulation: movement and epidemic duration. J Theoret Biol 2008;254:331338.Google Scholar
12. Gilbert-Norton, L, Wilson, R, Stevens, JR, Beard, KH. A meta-analytic review of corridor effectiveness—una revisión meta-analítica de la efectividad de los corredores. Conserv Biol 2010;24:660668.Google Scholar
13. Sullivan, A, Edlund, C, Nord, CE. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis 2001;1:101114.Google Scholar
14. Dethlefsen, L, Huse, S, Sogin, ML, Relman, DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008;6:e280.CrossRefGoogle Scholar
15. Jarchum, I, Pamer, EG. Regulation of innate and adaptive immunity by the commensal microbiota. Curr Opin Immunol 2011;23:353360.Google Scholar
16. Lloyd-Smith, JO. Vacated niches, competitive release and the community ecology of pathogen eradication. Phil Trans Royal Soc B 2013;368.Google Scholar
17. Al-Nassir, WN, Sethi, AK, Li, Y, Pultz, MJ, Riggs, MM, Donskey, CJ. Both oral metronidazole and oral vancomycin promote persistent overgrowth of vancomycin-resistant Enterococci during treatment of Clostridium difficile-associated disease. Antimicrob Agents Chemother 2008;52:24032406.Google Scholar
18. Lofgren, E, Fefferman, NH, Naumov, YN, Gorski, J, Naumova, EN. Influenza seasonality: underlying causes and modeling theories. J Virol 2007;81:54295436.Google Scholar
19. Fisman, D. Seasonality of viral infections: mechanisms and unknowns. Clin Microbiol Infect 2013;18:946954.Google Scholar
20. Lal, A, Hales, S, French, N, Baker, MG. Seasonality in human zoonotic enteric diseases: a systematic review. PLoS One 2013;7:e31883.Google Scholar
21. O’Brien-Pallas, L, Murphy, GT, Shamian, J, Li, X, Hayes, LJ. Impact and determinants of nurse turnover: a pan-Canadian study. J Nurs Manag 2010;18:10731086.Google Scholar
22. Phillips, D, Barker, GC. A July spike in fatal medication errors: a possible effect of new medical residents. J Gen Intern Med 2010;25:774779.Google Scholar
23. Weissman, JS, Rothschild, JM, Bendavid, E, et al. Hospital workload and adverse events. Med Care 2007;45:448455.Google Scholar
24. Hirshberg, A, Scott, BG, Granchi, T, Wall, MJ Jr, Mattox, KL, Stein, M. How does casualty load affect trauma care in urban bombing incidents? A quantitative analysis. J Trauma Acute Care Surg 2005;58.Google Scholar
25. Abir, M, Choi, H, Cooke, CR, Wang, SC, Davis, MM. Effect of a mass casualty incident: clinical outcomes and hospital charges for casualty patients versus concurrent inpatients. Acad Emerg Med 2012;19:280286.Google Scholar
26. Magill, SS, Edwards, JR, Beldavs, ZG, et al. Prevalence of antimicrobial use in US acute care hospitals, May–September 2011. JAMA 2014;312:14381446.Google Scholar
27. Weber, DJ, Rutala, WA, Miller, MB, Huslage, K, Sickbert-Bennett, E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect Control 2010;38:S25S33.Google Scholar
28. Otter, JA, Yezli, S, French, GL. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol 2011;32:687699.Google Scholar
29. O’Keefe, KJ. The evolution of virulence in pathogens with frequency-dependent transmission. J Theoret Biol 2005;233:5564.Google Scholar
30. King, AA, Shrestha, S, Harvill, ET, Bjørnstad, ON. Evolution of acute infections and the invasion-persistence trade-off. Amer Naturalist 2009;173:446455.Google Scholar
31. Reznick, D, Bryant, MJ, Bashey, F. r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 2002;83:15091520.Google Scholar
32. Phillips, BL, Brown, GP, Shine, R. Life-history evolution in range-shifting populations. Ecology 2010;91:16171627.Google Scholar
33. Lax, S, Gilbert, JA. Hospital-associated microbiota and implications for nosocomial infections. Trends Molec Med 2015;21:427432.Google Scholar
34. Jombart, T, Cori, A, Didelot, X, Cauchemez, S, Fraser, C, Ferguson, N. Bayesian reconstruction of disease outbreaks by combining epidemiologic and genomic data. PLoS Comput Biol 2014;10:e1003457.Google Scholar
35. Lofgren, ET, Moehring, RW, Anderson, DJ, Weber, DJ, Fefferman, NH. A mathematical model to evaluate the routine use of fecal microbiota transplantation to prevent incident and recurrent Clostridium difficile infection. Infect Control 2014;35:1827.Google Scholar
36. Septimus, E, Weinstein, RA, Perl, TM, Goldmann, DA, Yokoe, DS. Approaches for preventing healthcare-associated infections: go long or go wide? Infect Control Hosp Epidemiol 2014;35:797801.Google Scholar
37. Edmond, M, Munoz-Price, S. Surveillance cultures for carbapenem-resistant Gram-negatives: to do or not to do. Paper presented at: SHEA conference, May 14, 2015; Orlando, FL.Google Scholar
38. Hillebrand, H, Bennett, DM, Cadotte, MW. Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 2008;89:15101520.Google Scholar
39. Shochat, E, Lerman, SB, Anderies, JM, Warren, PS, Faeth, SH, Nilon, CH. Invasion, competition, and biodiversity loss in urban ecosystems. BioScience 2010;60:199208.Google Scholar
40. Chang, JY, Antonopoulos, DA, Kalra, A, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008;197:435438.Google Scholar
41. Buffie, CG, Jarchum, I, Equinda, M, et al. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect Immun 2012;80:6273.Google Scholar
42. Lemon, KP, Armitage, GC, Relman, DA, Fischbach, MA. Microbiota-targeted therapies: an ecological perspective. Sci Transl Med 2012;4:137rv135137rv135.Google Scholar
43. Hooper, DU, Chapin, FS, Ewel, JJ, et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 2005;75:335.Google Scholar
44. Cadotte, MW, Carscadden, K, Mirotchnick, N. Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 2011;48:10791087.Google Scholar
45. Kurokawa, K, Itoh, T, Kuwahara, T, et al. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 2007;14:169181.Google Scholar
46. Turnbaugh, PJ, Hamady, M, Yatsunenko, T, et al. A core gut microbiome in obese and lean twins. Nature 2009;457:480484.Google Scholar
47. Weinstock, GM. Genomic approaches to studying the human microbiota. Nature 2012;489:250256.Google Scholar
48. Gerding, DN, Meyer, T, Lee, C, et al. Administration of spores of nontoxigenic Clostridium difficile strain M3 for prevention of recurrent C. difficile infection. JAMA 2015;313:17191727.Google Scholar
49. Deasy, AM, Guccione, E, Dale, AP, et al. Nasal inoculation of the commensal Niseria lactamica inhibits carriage of Neisseria meningitides by young adults: a controlled human infection study. Clin Infect Dis 2015;60:15121520.Google Scholar
50. Zipperer, A, Konnerth, MC, Laux, C, et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature 2016;535:511516.Google Scholar
51. Robinson, CJ, Bohannan, BJ, Young, VB. From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 2010;74:453476.Google Scholar
52. Costello, EK, Stagaman, K, Dethlefsen, L, Bohannan, BJ, Relman, DA. The application of ecological theory toward an understanding of the human microbiome. Science 2012;336:12551262.Google Scholar
53. Relman, DA. The human microbiome: ecosystem resilience and health. Nutr Rev 2012;70:S2S9.Google Scholar
54. Smith, D, Alverdy, J, An, G, et al. The hospital microbiome project: meeting report for the 1st hospital microbiome project workshop on sampling design and building science measurements, Chicago, IL, June 7–8, 2012. Stand Genomic Sci 2013;8:112117.Google Scholar
55. Kembel, SW, Jones, E, Kline, J, et al. Architectural design influences the diversity and structure of the built environment microbiome. ISME J 2012;6:14691479.Google Scholar
56. McKinney, ML. Urbanization as a major cause of biotic homogenization. Biol Conserv 2006;127:247260.Google Scholar
57. Smith, VH, Rubinstein, RJ, Park, S, Kelly, L, Klepac-Ceraj, V. Microbiology and ecology are vitally important to premedical curricula. Evol Med Pub Health 2015;179192.Google Scholar
58. Johnson, PTJ, de Roode, JC, Fenton, A. Why infectious disease research needs community ecology. Science 2015;349:1069.Google Scholar
59. Gaston, KJ. ed. Urban Ecology. Cambridge University Press: Cambridge, UK; 2010.Google Scholar
60. Adler, FR, Tanner, CJ. Urban Ecosystems: Ecological Principles for the Built Environment. Cambridge University Press: Cambridge, UK; 2013.Google Scholar