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Published in: Intensive Care Medicine 10/2011

01-10-2011 | Original

Limiting the spread of highly resistant hospital-acquired microorganisms via critical care transfers: a simulation study

Authors: Umanka H. Karkada, Lada A. Adamic, Jeremy M. Kahn, Theodore J. Iwashyna

Published in: Intensive Care Medicine | Issue 10/2011

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Abstract

Purpose

Hospital-acquired infections with highly resistant organisms are an important problem among critically ill patients. Control of these organisms has largely focused within individual hospitals. We examine the extent to which transfers of critically ill patients could be a vector for the wide spread of highly resistant organisms, and compare the efficiency of different approaches to targeting infection control resources.

Methods

We analyzed the network of interhospital transfers of intensive care unit patients in 2005 US Medicare data and 2004–2006 Pennsylvania all-payer data. We simulated the spread of highly resistant hospital-acquired infections by randomly choosing a single hospital to develop a highly resistant organism and following the spread of infection or colonization throughout the network under varying strategies of infection control and varying levels of infectivity.

Results

Critical care transfers could spread a highly resistant organism between any two US hospitals in a median of 3 years. Hospitals varied substantially in their importance to limiting potential spread. Targeting resources to a small subset of hospitals on the basis of their position in the transfer network was 16 times more efficient than distributing infection control resources uniformly. Within any set of targeted hospitals, the best strategy for infection control heavily concentrated resources at a few particularly important hospitals, regardless of level of infectivity.

Conclusions

Critical care transfers provide a plausible vector for widespread dissemination of highly resistant hospital-acquired microorganisms. Infection control efforts can be made more efficient by selectively targeting hospitals most important for transmission.
Appendix
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Literature
1.
go back to reference Davin-Regali A, Monnet D, Saux P, Bosi C, Charrel R, Barthelemy A, Bollet C (1996) Molecular epidemiology of enterobacter aerogenes acquisition: one-year prospective study in two intensive care units. J Clin Microbiol 34:1474–1480 Davin-Regali A, Monnet D, Saux P, Bosi C, Charrel R, Barthelemy A, Bollet C (1996) Molecular epidemiology of enterobacter aerogenes acquisition: one-year prospective study in two intensive care units. J Clin Microbiol 34:1474–1480
2.
go back to reference Lai KK, Fontecchio SA, Kelly AL, Baker S, Melvin ZS (2003) The changing epidemiology of vancomycin-resistant enterococci. Infect Control Hosp Epidemiol 24:264–268PubMedCrossRef Lai KK, Fontecchio SA, Kelly AL, Baker S, Melvin ZS (2003) The changing epidemiology of vancomycin-resistant enterococci. Infect Control Hosp Epidemiol 24:264–268PubMedCrossRef
3.
go back to reference Huang SS, Avery TR, Song Y, Elkins KR, Nguyen CC, Nutter SK, Nafday AA, Condon CJ, Chang MT, Chrest D, Boos J, Bobashev G, Wheaton W, Frank SA, Platt R, Lipsitch M, Bush RM, Eubank S, Burke DS, Lee BY (2010) Quantifying interhospital patient sharing as a mechanism for infectious disease spread. Infect Control Hosp Epidemiol 31:1160–1169PubMedCrossRef Huang SS, Avery TR, Song Y, Elkins KR, Nguyen CC, Nutter SK, Nafday AA, Condon CJ, Chang MT, Chrest D, Boos J, Bobashev G, Wheaton W, Frank SA, Platt R, Lipsitch M, Bush RM, Eubank S, Burke DS, Lee BY (2010) Quantifying interhospital patient sharing as a mechanism for infectious disease spread. Infect Control Hosp Epidemiol 31:1160–1169PubMedCrossRef
4.
go back to reference Livermore DM (2003) Bacterial resistance: origins, epidemiology, and impact. Clin Infect Dis 36:S11–S23PubMedCrossRef Livermore DM (2003) Bacterial resistance: origins, epidemiology, and impact. Clin Infect Dis 36:S11–S23PubMedCrossRef
5.
go back to reference Howard DH, Scott RD II, Packard R, Jones D (2003) The global impact of drug resistance. Clin Infect Dis 36:S4–S10PubMedCrossRef Howard DH, Scott RD II, Packard R, Jones D (2003) The global impact of drug resistance. Clin Infect Dis 36:S4–S10PubMedCrossRef
6.
go back to reference Neuhauser MM, Weinstein RA, Rydman R, Danzinger LH, Karam G, Quinn JP (2003) Antibiotic resistance among gram-negative bacilli in us intensive care units: implications for fluoroquinolone use. JAMA 289:885–888PubMedCrossRef Neuhauser MM, Weinstein RA, Rydman R, Danzinger LH, Karam G, Quinn JP (2003) Antibiotic resistance among gram-negative bacilli in us intensive care units: implications for fluoroquinolone use. JAMA 289:885–888PubMedCrossRef
7.
go back to reference Harris AD, Kotetishvili M, Shurland S, Johnson JA, Morris JG, Nemoy LL, Johnson JK (2007) How important is patient-to-patient transmission in extended-spectrum beta-lactamase Escherichia coli acquisition. Am J Infect Control 35:97–101PubMedCrossRef Harris AD, Kotetishvili M, Shurland S, Johnson JA, Morris JG, Nemoy LL, Johnson JK (2007) How important is patient-to-patient transmission in extended-spectrum beta-lactamase Escherichia coli acquisition. Am J Infect Control 35:97–101PubMedCrossRef
8.
go back to reference Harris AD, Perencevich EN, Johnson JK, Paterson DL, Morris JG, Strauss SM, Johnson JA (2007) Patient-to-patient transmission is important in extended-spectrum beta-lactamase-producing Klebsiella pneumoniae acquisition. Clin Infect Dis 45:1347–1350PubMedCrossRef Harris AD, Perencevich EN, Johnson JK, Paterson DL, Morris JG, Strauss SM, Johnson JA (2007) Patient-to-patient transmission is important in extended-spectrum beta-lactamase-producing Klebsiella pneumoniae acquisition. Clin Infect Dis 45:1347–1350PubMedCrossRef
9.
go back to reference Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, Farr BM (2003) SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 24:362–386PubMedCrossRef Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, Farr BM (2003) SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 24:362–386PubMedCrossRef
10.
go back to reference Siegel JD, Rhinehart E, Jackson M, Chiarello L (2007) Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control 35:S165–S193PubMedCrossRef Siegel JD, Rhinehart E, Jackson M, Chiarello L (2007) Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control 35:S165–S193PubMedCrossRef
11.
go back to reference Svoboda T, Henry B, Shulman L, Kennedy E, Rea E, Ng W, Wallington T, Yaffe B, Gournis E, Vicencio E, Basrur S, Glazier RH (2004) Public health measures to control the spread of the severe acute respiratory syndrome during the outbreak in Toronto. N Engl J Med 350:2352–2361PubMedCrossRef Svoboda T, Henry B, Shulman L, Kennedy E, Rea E, Ng W, Wallington T, Yaffe B, Gournis E, Vicencio E, Basrur S, Glazier RH (2004) Public health measures to control the spread of the severe acute respiratory syndrome during the outbreak in Toronto. N Engl J Med 350:2352–2361PubMedCrossRef
12.
go back to reference Arlet G, Rouveau M, Casin I, Bouvet PJM, Lagrange PH, Philippon A (1994) Molecular epidemiology of Klebsiella pneumoniae strains that produce the SHV-4 beta-lactamase and which were isolated in 14 French hospitals. J Clin Microbiol 32:2553–2558PubMed Arlet G, Rouveau M, Casin I, Bouvet PJM, Lagrange PH, Philippon A (1994) Molecular epidemiology of Klebsiella pneumoniae strains that produce the SHV-4 beta-lactamase and which were isolated in 14 French hospitals. J Clin Microbiol 32:2553–2558PubMed
13.
go back to reference Roman RS, Smith J, Walker M, Byrne S, Ramotar K, Dyck B, Kabani A, Nicolle LE (1997) Rapid geographic spread of a methicillin-resistant Staphylococcus aureus strain. Clin Infect Dis 25:698–705PubMedCrossRef Roman RS, Smith J, Walker M, Byrne S, Ramotar K, Dyck B, Kabani A, Nicolle LE (1997) Rapid geographic spread of a methicillin-resistant Staphylococcus aureus strain. Clin Infect Dis 25:698–705PubMedCrossRef
14.
go back to reference Tansel O, Kuloglu F, Mutlu B, Anthony RM, Uyar A, Vahaboglu H, French GL (2003) A methicillin-resistant Staphylococcus aureus outbreak in a new university hospital due to a strain transferred with an infected patient from another city six months previously. New Microbiologica 26:175–180PubMed Tansel O, Kuloglu F, Mutlu B, Anthony RM, Uyar A, Vahaboglu H, French GL (2003) A methicillin-resistant Staphylococcus aureus outbreak in a new university hospital due to a strain transferred with an infected patient from another city six months previously. New Microbiologica 26:175–180PubMed
15.
go back to reference Wiener J, Quinn JP, Bradford PA, Goering RV, Nathan C, Bush K, Weinstein RA (1999) Multiple antibiotic–resistant Klebsiella and Escherichia coli in nursing homes. JAMA 281:517–523PubMedCrossRef Wiener J, Quinn JP, Bradford PA, Goering RV, Nathan C, Bush K, Weinstein RA (1999) Multiple antibiotic–resistant Klebsiella and Escherichia coli in nursing homes. JAMA 281:517–523PubMedCrossRef
16.
go back to reference Trick WE, Keuhnert MJ, Quirk SB, Arduino MJ, Aguero SM, Carson LA, Hill BC, Banerjee SN, Jarvis WR (1999) Regional dissemination of vancomycin-resistant enterococci resulting from interfacility transfer of colonized patients. J Infect Dis 180:391–396PubMedCrossRef Trick WE, Keuhnert MJ, Quirk SB, Arduino MJ, Aguero SM, Carson LA, Hill BC, Banerjee SN, Jarvis WR (1999) Regional dissemination of vancomycin-resistant enterococci resulting from interfacility transfer of colonized patients. J Infect Dis 180:391–396PubMedCrossRef
17.
go back to reference Austin DJ, Anderson RM (1999) Studies of antibiotic resistance within the patient, hospitals and the community using simple mathematical models. Philos Trans R Soc Lond B 354:721–738CrossRef Austin DJ, Anderson RM (1999) Studies of antibiotic resistance within the patient, hospitals and the community using simple mathematical models. Philos Trans R Soc Lond B 354:721–738CrossRef
18.
go back to reference Lipsitch M, Bergstrom CT, Levin BR (2000) The epidemiology of antibiotic resistance in hospitals: paradoxes and prescriptions. PNAS 97:1938–1943PubMedCrossRef Lipsitch M, Bergstrom CT, Levin BR (2000) The epidemiology of antibiotic resistance in hospitals: paradoxes and prescriptions. PNAS 97:1938–1943PubMedCrossRef
19.
go back to reference Pelupessy I, Bonten MJM, Diekmann O (2002) How to assess the relative importance of different colonization routes of pathogens within hospital settings. PNAS 99:5601–5605PubMedCrossRef Pelupessy I, Bonten MJM, Diekmann O (2002) How to assess the relative importance of different colonization routes of pathogens within hospital settings. PNAS 99:5601–5605PubMedCrossRef
20.
go back to reference Webb GF, D’Agata EMC, Magai P, Ruan S (2005) A model of antibiotic-resistant bacterial epidemics in hospitals. PNAS 102:13343–13348PubMedCrossRef Webb GF, D’Agata EMC, Magai P, Ruan S (2005) A model of antibiotic-resistant bacterial epidemics in hospitals. PNAS 102:13343–13348PubMedCrossRef
21.
go back to reference Smith DL, Dushoff J, Perencevich EN, Harris AD, Levin SA (2004) Persistent colonization and the spread of antibiotic resistance in nosocomial pathogens: resistance is a regional problem. PNAS 101:3709–3714PubMedCrossRef Smith DL, Dushoff J, Perencevich EN, Harris AD, Levin SA (2004) Persistent colonization and the spread of antibiotic resistance in nosocomial pathogens: resistance is a regional problem. PNAS 101:3709–3714PubMedCrossRef
22.
go back to reference Cooper BS, Medley GF, Stone SP, Kibbler CC, Cookson BD, Roberts JA, Duckworth G, Lai R, Ebrahim S (2004) Methicillin-resistant Staphylococcus aureus in hospitals and the community: stealth dynamics and control catastrophes. PNAS 101:10223–10228PubMedCrossRef Cooper BS, Medley GF, Stone SP, Kibbler CC, Cookson BD, Roberts JA, Duckworth G, Lai R, Ebrahim S (2004) Methicillin-resistant Staphylococcus aureus in hospitals and the community: stealth dynamics and control catastrophes. PNAS 101:10223–10228PubMedCrossRef
23.
go back to reference Smith DL, Levin SA, Laxminarayan R (2005) Strategic interactions in multi-institutional epidemics of antibiotic resistance. PNAS 102:3153–3158PubMedCrossRef Smith DL, Levin SA, Laxminarayan R (2005) Strategic interactions in multi-institutional epidemics of antibiotic resistance. PNAS 102:3153–3158PubMedCrossRef
24.
go back to reference Iwashyna TJ, Christie JD, Kahn JM, Asch DA (2009) Uncharted paths: hospital networks in critical care. Chest 135:827–833PubMedCrossRef Iwashyna TJ, Christie JD, Kahn JM, Asch DA (2009) Uncharted paths: hospital networks in critical care. Chest 135:827–833PubMedCrossRef
25.
go back to reference Iwashyna TJ, Christie JD, Moody J, Kahn JM, Asch DA (2009) The structure of critical care transfer networks. Med Care 47:787–793PubMedCrossRef Iwashyna TJ, Christie JD, Moody J, Kahn JM, Asch DA (2009) The structure of critical care transfer networks. Med Care 47:787–793PubMedCrossRef
27.
go back to reference Zingg W, Imhof A, Maggiorini M, Stocker R, Keller E, Ruef C (2009) Impact of a prevention strategy targeting hand hygiene and catheter care on the incidence of catheter-related bloodstream infections. Crit Care Med 37:2167–2173PubMedCrossRef Zingg W, Imhof A, Maggiorini M, Stocker R, Keller E, Ruef C (2009) Impact of a prevention strategy targeting hand hygiene and catheter care on the incidence of catheter-related bloodstream infections. Crit Care Med 37:2167–2173PubMedCrossRef
28.
go back to reference Raymond DP, Pelletier SJ, Crabtree TD, Gleason TG, Hamm LL, Pruett TL, Sawyer RG (2001) Impact of a rotating empiric antibiotic schedule on infectious mortality in an intensive care unit. Crit Care Med 29:1101–1108PubMedCrossRef Raymond DP, Pelletier SJ, Crabtree TD, Gleason TG, Hamm LL, Pruett TL, Sawyer RG (2001) Impact of a rotating empiric antibiotic schedule on infectious mortality in an intensive care unit. Crit Care Med 29:1101–1108PubMedCrossRef
29.
go back to reference Martinez JA, Nicolas JM, Marco F, Horcajada JP, Garcia-Segarra G, Trilla A, Codina C, Torres A, Mensa J (2006) Comparison of antimicrobial cycling and mixing strategies in two medical intensive care units. Crit Care Med 34:329–336PubMedCrossRef Martinez JA, Nicolas JM, Marco F, Horcajada JP, Garcia-Segarra G, Trilla A, Codina C, Torres A, Mensa J (2006) Comparison of antimicrobial cycling and mixing strategies in two medical intensive care units. Crit Care Med 34:329–336PubMedCrossRef
30.
go back to reference Koeman M, van der Ven AJ, Hak E, Joore HC, Kaasjager K, de Smet AG, Ramsay G, Dormans TP, Aarts LP, de Bel EE, Hustinx WN, van der Tweel I, Hoepelman AM, Bonten MJ (2006) Oral decontamination with chlorhexidine reduces the incidence of ventilator-associated pneumonia. Am J Respir Crit Care Med 173:1348–1355PubMedCrossRef Koeman M, van der Ven AJ, Hak E, Joore HC, Kaasjager K, de Smet AG, Ramsay G, Dormans TP, Aarts LP, de Bel EE, Hustinx WN, van der Tweel I, Hoepelman AM, Bonten MJ (2006) Oral decontamination with chlorhexidine reduces the incidence of ventilator-associated pneumonia. Am J Respir Crit Care Med 173:1348–1355PubMedCrossRef
31.
go back to reference Cerda E, Abella A, de la Cal MA, Lorente JA, Garcia-Hierro P, van Saene HK, Alia I, Aranguren A (2007) Enteral vancomycin controls methicillin-resistant Staphylococcus aureus endemicity in an intensive care burn unit: a 9-year prospective study. Ann Surg 245:397–407PubMedCrossRef Cerda E, Abella A, de la Cal MA, Lorente JA, Garcia-Hierro P, van Saene HK, Alia I, Aranguren A (2007) Enteral vancomycin controls methicillin-resistant Staphylococcus aureus endemicity in an intensive care burn unit: a 9-year prospective study. Ann Surg 245:397–407PubMedCrossRef
32.
go back to reference Bennett KM, Scarborough JE, Sharpe M, Dodds-Ashley E, Kaye KS, Hayward TZ 3rd, Vaslef SN (2007) Implementation of antibiotic rotation protocol improves antibiotic susceptibility profile in a surgical intensive care unit. J Trauma 63:307–311PubMedCrossRef Bennett KM, Scarborough JE, Sharpe M, Dodds-Ashley E, Kaye KS, Hayward TZ 3rd, Vaslef SN (2007) Implementation of antibiotic rotation protocol improves antibiotic susceptibility profile in a surgical intensive care unit. J Trauma 63:307–311PubMedCrossRef
33.
go back to reference Babcock HM, Zack JE, Garrison T, Trovillion E, Jones M, Fraser VJ, Kollef MH (2004) An educational intervention to reduce ventilator-associated pneumonia in an integrated health system: a comparison of effects. Chest 125:2224–2231PubMedCrossRef Babcock HM, Zack JE, Garrison T, Trovillion E, Jones M, Fraser VJ, Kollef MH (2004) An educational intervention to reduce ventilator-associated pneumonia in an integrated health system: a comparison of effects. Chest 125:2224–2231PubMedCrossRef
34.
go back to reference Marias E, de Jong G, Ferraz V, Maloba B, Duse AG (2004) Interhospital transfer of pan-resistant Acinetobacter strains in Johannesburg, South Africa. Am J Infect Control 32:278–281CrossRef Marias E, de Jong G, Ferraz V, Maloba B, Duse AG (2004) Interhospital transfer of pan-resistant Acinetobacter strains in Johannesburg, South Africa. Am J Infect Control 32:278–281CrossRef
35.
go back to reference Landman D, Quale JM, Mayorga D, Adedeji A, Vangala K, Ravishankar J, Flores C, Brooks S (2002) Citywide clonal outbreak of multiresistant Acinetobacter baumannii and Pseudomonas aeruginosa in Brooklyn. Arch Intern Med 162:1515–1520PubMedCrossRef Landman D, Quale JM, Mayorga D, Adedeji A, Vangala K, Ravishankar J, Flores C, Brooks S (2002) Citywide clonal outbreak of multiresistant Acinetobacter baumannii and Pseudomonas aeruginosa in Brooklyn. Arch Intern Med 162:1515–1520PubMedCrossRef
36.
go back to reference Donker T, Wallinga J, Grundmann H (2010) Patient referral patterns and the spread of hospital-acquired infections through national health care networks. PLoS Comput Biol 6:e1000715PubMedCrossRef Donker T, Wallinga J, Grundmann H (2010) Patient referral patterns and the spread of hospital-acquired infections through national health care networks. PLoS Comput Biol 6:e1000715PubMedCrossRef
37.
go back to reference Cutler DM (2002) Health Care and the Public Sector. In: Auerbach AJ, Feldstein M (eds) Handbook of public economics. Elsevier, New York Cutler DM (2002) Health Care and the Public Sector. In: Auerbach AJ, Feldstein M (eds) Handbook of public economics. Elsevier, New York
38.
go back to reference Lautenbach E (2008) Expanding the Universe of Methicillin-resistant Staphylococcus aureus prevention. Ann Intern Med 148:474–476PubMed Lautenbach E (2008) Expanding the Universe of Methicillin-resistant Staphylococcus aureus prevention. Ann Intern Med 148:474–476PubMed
39.
go back to reference Valente TW (1995) Network models of diffusion of innovation. Hampton, Cresskill Valente TW (1995) Network models of diffusion of innovation. Hampton, Cresskill
40.
go back to reference Pastor-Satorras R, Vespignani A (2002) Immunization of complex networks. Phys Rev E 65:36104CrossRef Pastor-Satorras R, Vespignani A (2002) Immunization of complex networks. Phys Rev E 65:36104CrossRef
41.
go back to reference Chen Y, Paul G, Havlin S, Liljeros F, Stanley HE (2006) Finding a better immunization strategy. Phys Rev Lett 101:05871 Chen Y, Paul G, Havlin S, Liljeros F, Stanley HE (2006) Finding a better immunization strategy. Phys Rev Lett 101:05871
42.
go back to reference Borgatti SP (2006) Identifying key players in a social network. Comput Math Organ Theory 12:21–34 Borgatti SP (2006) Identifying key players in a social network. Comput Math Organ Theory 12:21–34
43.
go back to reference Valente TW, Fujimoto K (2010) Briding: locating critical connectors in a network. Social Netw 32:212–220CrossRef Valente TW, Fujimoto K (2010) Briding: locating critical connectors in a network. Social Netw 32:212–220CrossRef
44.
go back to reference Perez-Padilla R, de la Rosa-Zamboni D, Ponce de Leon S, Hernandez M, Quinones-Falconi F, Bautista E, Ramirez-Venegas A, Rojas-Serrano J, Ormsby CE, Corrales A, Higuera A, Mondragon E, Cordova-Villalobos JA (2009) Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N Engl J Med 361:680–689 Perez-Padilla R, de la Rosa-Zamboni D, Ponce de Leon S, Hernandez M, Quinones-Falconi F, Bautista E, Ramirez-Venegas A, Rojas-Serrano J, Ormsby CE, Corrales A, Higuera A, Mondragon E, Cordova-Villalobos JA (2009) Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N Engl J Med 361:680–689
45.
go back to reference Freeman LC (1978/79) Centrality in social networks: conceptual clarification. Social Netw 1:215–239 Freeman LC (1978/79) Centrality in social networks: conceptual clarification. Social Netw 1:215–239
46.
go back to reference Tukey JW (1977) Exploratory data analysis. Addison-Wesley, Reading Tukey JW (1977) Exploratory data analysis. Addison-Wesley, Reading
Metadata
Title
Limiting the spread of highly resistant hospital-acquired microorganisms via critical care transfers: a simulation study
Authors
Umanka H. Karkada
Lada A. Adamic
Jeremy M. Kahn
Theodore J. Iwashyna
Publication date
01-10-2011
Publisher
Springer-Verlag
Published in
Intensive Care Medicine / Issue 10/2011
Print ISSN: 0342-4642
Electronic ISSN: 1432-1238
DOI
https://doi.org/10.1007/s00134-011-2341-y

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