The Importance of Nursing Homes in the Spread of Methicillin-resistant Staphylococcus aureus (MRSA) Among Hospitals
Lee, Bruce Y. MD, MBA*,†; Bartsch, Sarah M. MPH*,†; Wong, Kim F. PhD‡; Singh, Ashima MS*,†; Avery, Taliser R. MS§; Kim, Diane S. BS∥; Brown, Shawn T. PhD¶,#; Murphy, Courtney R. PhD∥; Yilmaz, Server Levent PhD‡; Potter, Margaret A. MS, JD**; Huang, Susan S. MD, MPH∥
Departments of *Medicine and Biomedical Informatics
†Epidemiology, Graduate School of Public Health
‡Center for Simulation and Modeling, University of Pittsburgh, Pittsburgh, PA
§Department of Population Medicine, Harvard Medical School, Harvard Pilgrim Health Care Institute, Boston, MA
∥Division of Infectious Diseases and Health Policy Research Institute, University of California, Irvine, CA
¶Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh
#Pittsburgh Supercomputing Center, Carnegie Mellon University
**Department of Health Management and Policy, Center for Public Health Practice, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA
Supported by the National Institute of General Medical Sciences Models of Infectious Disease Agent Study (MIDAS) grants 5U54GM088491-02 and 1U01GM076672 and the Pennsylvania Department of Health. This project was also funded under Contract No. HHSA29020050033I from the Agency for Healthcare Research and Quality, US Department of Health and Human Services as part of the Developing Evidence to Inform Decisions about Effectiveness (DEcIDE) program. The authors of this report are responsible for its content. Statements in the report should not be construed as endorsement by the Agency for Healthcare Research and Quality or the US Department of Health and Human Services. Computational resources were provided by the Center for Simulation and Modeling.
The authors declare no conflict of interest.
Reprints: Bruce Y. Lee, MD, MBA, Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, 200 Meyran Ave, Suite 200, Pittsburgh, PA 51213. E-mail: email@example.com.
Background: Hospital infection control strategies and programs may not consider control of methicillin-resistant Staphylococcus aureus (MRSA) in nursing homes in a county.
Methods: Using our Regional Healthcare Ecosystem Analyst, we augmented our existing agent-based model of all hospitals in Orange County (OC), California, by adding all nursing homes and then simulated MRSA outbreaks in various health care facilities.
Results: The addition of nursing homes substantially changed MRSA transmission dynamics throughout the county. The presence of nursing homes substantially potentiated the effects of hospital outbreaks on other hospitals, leading to an average 46.2% (range, 3.3%–156.1%) relative increase above and beyond the impact when only hospitals are included for an outbreak in OC’s largest hospital. An outbreak in the largest hospital affected all other hospitals (average 2.1% relative prevalence increase) and the majority (∼90%) of nursing homes (average 3.2% relative increase) after 6 months. An outbreak in the largest nursing home had effects on multiple OC hospitals, increasing MRSA prevalence in directly connected hospitals by an average 0.3% and in hospitals not directly connected through patient transfers by an average 0.1% after 6 months. A nursing home outbreak also had some effect on MRSA prevalence in other nursing homes.
Conclusions: Nursing homes, even those not connected by direct patient transfers, may be a vital component of a hospital’s infection control strategy. To achieve effective control, a hospital may want to better understand how regional nursing homes and hospitals are connected through both direct and indirect (with intervening stays at home) patient sharing.
Individual hospitals or hospital systems may not consider nursing homes when planning their infection control strategies. However, our previous work has shown that hospitals and nursing homes in a region may be highly interconnected by patient sharing.1,2 Patients often move among various hospitals and nursing homes either through direct transfers or with intervening stays at home,1,3–5 and in some instances repeatedly.6,7 Moreover, nursing homes are important reservoirs of multidrug-resistant organisms (MDROs), especially methicillin-resistant Staphylococcus aureus (MRSA),8,9 which tends to be more prevalent (20%–50%) in many long-term care settings9–13 than in acute care hospitals (5%–10%).14–16 Many questions remain. How might an MRSA outbreak in 1 hospital affect that of a nursing home and vice versa? Should hospitals and nursing homes work together to reduce MDROs? Although previous mathematical and computational models have explored MRSA spread among just hospitals,17–20 a single nursing home,21 or a small group of closely associated nursing homes and hospitals that directly transfer patients to one another,22 these studies did not examine all of the inpatient facilities in a large real-life region. One study modeled hospitals and nursing homes in a region of Canada (which has a different health care system).23 With facilities connected through patient sharing over considerable distances in a very complex manner through both direct and indirect patient sharing, predicting the effects of an outbreak in a single facility may be difficult as a variety of sources and sinks may emerge.
General Model Structure and Data Sources
We expanded our previously described agent-based model, generated by our custom-designed software, the Regional Healthcare Ecosystem Analyst (RHEA),17 of all adult acute care facilities to add all 71 nursing homes (providing postacute or long-term care) in Orange County (OC), CA. The RHEA-created model simulated the movement of virtual patients (ie, computational agents) to and from the community into and between health care facilities, and MRSA spread. We used 2007 patient-level data for all adult inpatient admissions from 100 total facilities (29 hospitals and 71 nursing homes). Data came from several sources, including a state mandatory hospitalization dataset, a national long-term care dataset (Minimum Data Set), and hospital and nursing home surveys conducted from 2006 to 2008 to assess the distribution of transferring locations (eg, specific hospitals, specific nursing homes, rehabilitation centers, assisted living facilities, and home) of patients admitted to and discharged from each facility during a consecutive 12-month period.24–27 Data on facility MRSA prevalence came from regional surveys and patient screenings.12,26 Table 1 shows our model inputs and characteristics for the OC health care facilities.
The appendix illustrates how patients move in the model. When a patient (either MRSA-carrier or noncarrier) is admitted to a hospital, he/she can enter either a general ward, or an intensive care unit (ICU), if present in the facility, and stay there for a length of stay (LOS) drawn from a distribution specific to that facility and ward. Patients mix homogenously with other patients within the same ward but not across wards. On the basis of actual facility-specific data, the LOS distribution for MRSA-positive patients is longer (average 5 d longer countywide) than that of MRSA-negative patients.24 Patients discharged from hospitals can return to the community, directly transfer to another OC facility (either hospital or nursing home), or return home to later return to the same or another hospital based on facility-specific probabilities derived from actual patient data.25
Although each hospital included multiple wards and units, each nursing home consisted of a single homogenously mixing ward to represent a high degree of social interactions (eg, group activities). Patients entering a nursing home drew a LOS from that facility’s distribution. Once a nursing home resident’s total LOS elapsed, he/she could move to the community, a hospital, or another nursing home. A fraction of those returning to the community were readmitted according to known regional readmission data.25
During a nursing home stay, a patient could also experience brief hospitalizations, during which the patient’s bed was “held” for his/her return. Nursing home residents with a LOS ≥14 days had a daily probability of brief readmission to a hospital (based on nursing home-specific frequencies for temporary discharges). The patient had probabilities of going to particular hospitals (for a LOS drawn from data of known temporary hospitalizations) from that nursing home (based on nursing home-specific data).
Sixty-one (85%) countywide nursing homes provided detailed distributions of patients’ locations before and after their stay. When combined with hospital survey data about admissions and discharges to and from nursing homes (27 hospitals, 93% participation), comprehensive transfer probabilities between hospitals and nursing homes as well as between nursing homes were compiled and used as model inputs. Three nursing homes had limited data and were not included in the analysis.
MRSA Transmission Within Facilities
Each day in each ward in each facility, the following formula governed the number of new MRSA cases:
Equation (Uncited)Image Tools
where β is the transmission coefficient, S is the number of susceptible patients, and I is the number of colonized patients. Influx of MRSA carriers at hospitals reflected survey-reported prevalence and β was parameterized to produce an incidence of 1% in general wards and 3% in ICUs.17 For nursing homes, MRSA influx and transmission was based upon actual admission prevalence data and point prevalence screenings from 40% of nursing homes (having a mean 16% acquisition risk28). For those not sampled, estimated importation and transmission were extrapolated from generalized linear mixed models estimating carriage risk and incident disease based upon facility-level risk factors, including case mix. Therefore, the ward and facility-specific β accounted for differences in MRSA susceptibility among patients in different facilities and transmission through staff members. Our model did not have separate βs for patients with active MRSA infections (vs. asymptomatic carrier) based on evidence that suggest no difference.29
MRSA-positive patients could lose MRSA carriage over time30–33; one third had indefinite carriage34 and the remainder experienced a linear carriage loss with a half-life of 6 months.30,33
Different experimental scenarios simulated sustained (to estimate the potential maximal effect) and temporary (ie, 6 mo) MRSA outbreaks in selected hospitals and nursing homes: an absolute increase in MRSA prevalence of 10% in hospitals and 20% in nursing homes. We specifically simulated outbreaks in facilities that may have a high likelihood of experiencing an outbreak (because of their high volume and extensive patient sharing): the 2 largest hospitals and nursing homes by annual admissions, as well as the 2 hospitals and nursing homes sending the most number of patients to 1 facility of the opposite type (ie, the hospital sending the largest number of patients to 1 nursing home). For each outbreak, we assessed the impact on all hospitals and nursing homes in OC, individually and countywide. We compared experiments with and without simulated outbreaks to assess the attributable change in MRSA prevalence due to the outbreak and the number of excess MRSA carriers generated for each scenario across the entire county and in all other facilities. Additional experiments varied the outbreak size from 10%, 20%, and 30%. For each scenario, we averaged the results from 25,000 simulations for each facility. The percent relative increase in MRSA prevalence was measured for each facility and countywide averages are presented.
Outbreak in a Single Hospital
Adding nursing homes to the model substantially changed the dynamics of MRSA spread throughout the county. The presence of nursing homes substantially potentiated the effects of a hospital outbreak on other hospitals, leading to an average relative increase of 46.2% (range, 3.3%–156.1%) above and beyond the impact when only hospitals are included for an outbreak in OC’s largest hospital. The top half of Table 2 shows how hospital outbreaks affected the MRSA prevalence in other hospitals over time in the full model with all OC inpatient health care facilities. (The SD for each of the results in Table 2 ranged from 0.00041 to 0.0049.) Table 2 provides the mean, median, interquartile range, and total range of effects. The effects on other facilities were fairly heterogenous (ie, different facilities have different effects from the outbreak). Figure 1 shows the increase in daily number of MRSA carriers from each outbreak.
The bottom half of Table 2 shows the effects of single hospital outbreaks on nursing home MRSA prevalence over time. Figure 2 shows the number of nursing homes experiencing a given relative change in prevalence when the largest and second largest hospitals experienced an outbreak. Outbreak effects took time to manifest, with many nursing homes experiencing changes >4%. Figure 3 compares the resulting MRSA prevalence in select OC nursing homes (exemplifying large, moderate, and small effects) when an outbreak occurs in the largest hospital (also, the one sending the most patients to 1 nursing home) versus no hospital outbreak.
Table 2 also shows what happened when an outbreak occurred in the 2 hospitals sending the most patients to 1 nursing home (1063 patients and 752 patients to 2 different nursing homes over the course of a year, respectively); those nursing homes saw a 24.4% and 13.5% relative MRSA prevalence increase 6 months after outbreak. However, the nursing homes manifesting the highest relative prevalence changes were not the ones who directly received the most patients.
Increasing the MRSA outbreak size (20%–30% absolute increase) in hospitals increased the relative change and number of nursing homes affected. For example, 6 months after outbreak, a 20% outbreak in the largest hospital affected 61 nursing homes, with 18 experiencing ≥4% increase (5.6% average relative increase in prevalence in nursing homes), whereas a 30% outbreak affected 65 nursing homes (7.7% relative MRSA prevalence increase).
Outbreak in a Single Nursing Home
Table 2 also shows the results of outbreaks in a single nursing home (again, the SD for each of these results ranged from 0.00041 to 0.0049). An outbreak in a single nursing home also notably (albeit less in magnitude than a single hospital outbreak) affected multiple facilities. Figure 1 shows the increase in the daily number of MRSA carriers and Figure 2 shows the number of hospitals experiencing a given relative change in prevalence as a result of a nursing home outbreak.
As Figure 2 and Table 2 show, the second largest nursing home had a greater impact than an outbreak in the largest or the most connected nursing home, generating 12 new MRSA conversions within a year in all other facilities. This highlights the potential impact of other factors such as LOS and mixing patterns (as reflected in the transmission coefficient).
Outbreaks in nursing homes tended to most affect the hospital to which they sent the largest number of patients. The outbreak in the nursing home sending the most patients to 1 hospital had the largest effect on that hospital (1.9% relative prevalence increase after 6 mo), whereas it had little effect on the other hospitals (Fig. 2). Similarly, an outbreak in the nursing home sending the second most patients to 1 hospital caused a 4.6% relative increase in prevalence in that hospital within 6 months and 7.0% relative increase in prevalence within 2 years.
Varying the outbreak size varied the number and magnitude of change in MRSA prevalence in OC hospitals. For example, for the second largest nursing home, a 10% absolute MRSA outbreak affected 14 hospitals, whereas a 30% absolute outbreak affected 21 hospitals (relative change in prevalence >0%) after 1 year.
Nursing home MRSA outbreaks did have some effects on other OC nursing homes. Very few experienced relative MRSA prevalence increases of ≥1%. Even among those experiencing increases, effects took longer to manifest (Table 2). Two years after an outbreak in the largest nursing home, 66 others experienced <1% increase and 23 no effect, for an average 0.2% relative increase (Table 2). Four years later, 62 nursing homes showed <1% increase and 20 no effect.
Other OC nursing homes were still affected with smaller MRSA outbreaks in a nursing home; 37 saw a relative prevalence increase >0% when the second largest nursing home had a 10% MRSA outbreak. For a larger outbreak (30% absolute increase), 42 other OC nursing homes had a change >0%.
Impact of 6-Month Outbreaks
A 6-month outbreak in the largest hospital showed maximum effects in all other OC facilities 6 months after outbreak for an average relative 2.4% increase in MRSA prevalence (range, no effect to 36.4%); 4 nursing homes experienced a ≥10% prevalence increase. Although effects steadily decreased after the outbreak concluded, MRSA prevalence in affected facilities did not return to preoutbreak levels until 4 years later. A short outbreak in the second largest nursing home resulted in a relative prevalence increase of 0.1% (range, no effect to 4.5%) in all other OC health care facilities 6 month after outbreak (16 hospitals were affected, of which 3 were ≥2%). These affects dwindled within 1 year.
Our study suggests that to fully understand the spread and control of an infectious pathogen such as MRSA, one must consider how all of the inpatient facilities (both hospitals and nursing homes) in a large geographic region are connected by both direct and indirect patient sharing. However, many hospital infection control efforts focus exclusively on hospitals. Even existing multi-institutional collaboratives tend to exclude nursing homes.35–37 Hospital infection control efforts that do include nursing homes tend to only include a few nursing homes that receive or send a substantial number of direct transfers (eg, strong fiscal/administrative ties with the hospital).
Despite their much smaller size and less frequent turnover compared with hospitals, the impact of nursing homes is substantial and reaches across many miles. This may be due in part to the relatively high prevalence of MRSA in nursing homes, averaging 25% in OC,12,38 consistent with published literature.11,12,39–42 MRSA acquisition has substantial sequelae43; MRSA-positive nursing home residents have a 10% risk of MRSA infection within the first month of arrival, with risks as high as 40% within 1 year.41,42,44 These infections are costly and often result in hospital readmission.41,45,46 Of patients hospitalized with MRSA infection, 20%–40% were recently in nursing homes.43,47,48
Nursing homes can influence hospital infection control by several means. First, nursing homes can multiply/magnify the effects of a hospital outbreak on other hospitals. The close quarters, heavy social mixing, and already high prevalence of MRSA in nursing homes can “fuel” a hospital MRSA outbreak by serving a “cauldron” of transmission, multiplying the number of cases, and then sending them to hospitals throughout the county. A nursing home can link 2 hospitals that were not otherwise strongly linked, acting as a bridge for infectious pathogens to spread from facility to facility. Secondly, outbreaks originating in a nursing home can affect multiple hospitals in a region, even those geographically distant. Even if a hospital keeps its own MRSA levels low, it is at risk for an outbreak if nursing homes in the same region do not maintain effective infection control. Third, when an outbreak occurs, determining the original culprit can be challenging. The result of an outbreak in a single hospital or nursing home could seem like multiple outbreaks in many different facilities. Different facilities may rush to control their “outbreaks” without uncovering the true origin, leading to a fruitless chase. Our study did not even consider outbreaks originating concurrently in >1 facility, which could very readily occur in such a large region with so many people (OC has a population of 3.1 million and is the sixth largest US County). Such concurrent outbreaks could produce even more synergistic transmission effects, potentially turning a smaller controllable outbreak into one much more difficult to control. One could envision an outbreak in a community served by multiple facilities leading to such an eventuality.17
Previously published models may not fully capture these effects. Hospital-only models17–20 miss key nursing home reservoirs. A literature search found 2 models that included both hospitals and nursing homes. Barnes et al22 constructed a theoretical mathematical model comprised of a single generic hospital and 2 connected nursing homes. Their model suggested that hospitals can affect MRSA prevalence in a nursing home, but transferring patients from a nursing home to a hospital would have a negligible effect on MRSA prevalence in that hospital unless patients are consistently transferred to the same unit in that hospital. Lesosky et al23 constructed a stochastic discrete-time Monte Carlo simulation comprised of teaching hospitals, nonteaching hospitals, and nursing homes. Their model only focused on MRSA acquisition rate, but suggested transfer patterns and rate changes do not affect MRSA transmission. Our study, which includes many more nursing homes and hospitals and their complex connections, suggests otherwise: nursing homes do not have to transfer patients to the same unit of hospital to affect the hospital (in our model patients went from nursing homes to many different wards/units in many different hospitals) and transfer patterns and rate changes may be key drivers of MRSA transmission (an outbreak in a nursing home has heterogenous effects on hospitals). The differing findings likely emerge from 3 considerable differences from our model. First, the Barnes and Lesosky models are theoretical and simplified; one assumes uniform characteristics for each of the facility types and the other does not model actual facilities. In contrast, our model uses extensive and detailed real-world data, (eg, parameterized with facility-specific admission volume, ICU volume, bed capacity, LOS, and transfer probabilities MRSA carriage, and transmission). Second, our model included a much larger geographic region and all of their inpatient facilities. Third, our model accounted for both direct and indirect patient sharing among facilities. Our previous work showed that excluding indirect patient sharing (ie, patient movement from facility to facility with an intervening stay in the community) neglects the majority of patient sharing1,2 and in turn MRSA transmission routes.
The difference between prior models and our models can serve a lesson for infection control. Not considering nursing homes, true connections based on real-world data among hospitals and nursing homes, all of the facilities in a region, and indirect patient sharing could limit the understanding and implementation of infection control. Even if adequate control is maintained in all hospitals, a single nursing home with poor MRSA control can affect multiple facilities. Understanding drivers and mitigators of pathogen spread in nursing homes is urgently needed as the Department of Health and Human Services has named nursing homes the focus of Phase 3 of its Action Plan to reduce health care–associated infections.
Our model may underestimate the amount of MRSA in nursing homes as we assumed that MRSA-positive nursing home residents lost MRSA carriage at the same rate as hospitalized patients (ie, 6 mo half-life), where in fact carriage may persist for several years in these settings.32,49 In addition, homogenous mixing may potentially overestimate the actual contact rate.
By definition, all models are simplifications of real life and as such cannot represent every possible outcome or event.50 Our model does not include comorbidities that may affect MRSA transmission, but its admission and readmission rates in nursing homes and hospitals reflect the health status of this California region. We did not include emergency departments, which could have a potential impact, as inpatients were the scope of this study. In addition, our model does not include pediatric hospitalizations or account for the effect on health care facilities outside of OC. Nevertheless, as pediatric patients uncommonly mix with adult patients during hospitalizations or nursing home care and as the vast majority of hospitalized adults remain within OC facilities (≥83.4% for all types of patient transfers), this model is a reasonable representation for adult transmission of MRSA. OC may not be representative of all counties or regions. However, similar findings may apply regions similar to OC, that is, metropolitan counties with multiple facilities and health care systems.
Nursing homes may play an important role in the spread and control of infectious pathogens such as MRSA. Nursing homes may multiply the effects of a hospital outbreak, originate outbreaks that in turn affect multiple hospitals, and make it even more difficult to trace the source of an outbreak. Even if hospitals maintain effective infection control, even a single nursing home with poor infection control can lead to hospital outbreaks. These findings have several implications for hospital infection control. Hospitals should consider and even include nursing homes in their infection control measures. Hospitals should better understand the true (based on real-world data) connections among other hospitals and nursing homes in their county/region through patient sharing. These connections should include both direct and indirect patient sharing. There may be benefit in applying the same rigor in infection control seen in many hospitals to nursing homes. Ultimately, controlling MRSA and other MDROs may necessitate close collaboration among hospitals and nursing homes across financial and administrative relationships.
1. Lee BY, Song Y, Bartsch SM, et al. Long-term care facilities: important participants of the acute care facility social network? PLoS One. 2011;6:e29342
2. Lee BY, McGlone SM, Song Y, et al. Social network analysis of patient sharing among hospitals in Orange County, California. Am J Public Health. 2011;101:707–713
3. Buntin MB. Access to postacute rehabilitation. Arch Phys Med Rehabil. 2007;88:1488–1493
4. Konetzka RT, Spector W, Limcanqco MR. Reducing hospitalizations from long-term care settings. Med Care Res Rev. 2008;65:40–66
5. Smith PW, Bennet G, Bradley SF, et al. SHEA/APIC guideline: infection prevention and control in the long-term care facility. Am J Infect Control. 2008;36:504–535
6. Mor V, Intrator O, Feng Z, et al. The revolving door of rehospitalization from skilled nursing facilities. Health Aff (Millwood). 2010;29:57–64
7. Ouslander JG, Diaz S, Hain D, et al. Frequency and diagnoses associated with 7- and 30-day readmission of skilled nursing facility patients to a nonteaching community hospital. J Am Med Dir Assoc. 2011;12:195–203
8. Rebmann T, Aureden K. Preventing methicillin-resistant Staphylococcus aureus
transmission in long-term care facilities: an executive summary of the APIC elimination guide. Am J Infect Control. 2011;39:235–238
9. Stone ND, Lewis DR, Lowery HK, et al. Importance of bacterial burden among methicillin-resistant Staphylococcus aureus
carriers in a long-term care facility. Infect Control Hosp Epidemiol. 2008;29:143–148
10. Mermel LA, Eells S, Acharya MK, et al. Quantitative analysis and molecular fingerprinting of methicillin-resistant Staphyloccus aureus
nasal colonization in different patient populations: a prospective, multicenter study. Infect Control Hosp Epidemiol. 2010;31:592–597
11. Furuno JP, Hebden JN, Standiford HC, et al. Prevalence of methicillin-resistant Staphylococcus aureus
and Acinetobacter baumannii
in a long-term acute care facility. Am J Infect Control. 2008;36:768–471
12. Reynolds C, Quan V, Kim D, et al. Methicillin-resistant Staphylococcus aureus
(MRSA) carriage in 10 nursing homes in Orange County, California. Infect Control Hosp Epidemiol. 2011;32:91–93
13. Garazi M, Edwards B, Caccavale D, et al. Nursing homes as reservoirs of MRSA: myth or reality? J Am Med Dir Assoc. 2009;10:414–418
14. Harbarth S, Fankhauser C, Schrenzel J, et al. Universal screening for methicillin-resistant Staphylococcus aureus
at hospital admission and nosocomial infection in surgical patients. JAMA. 2008;299:1149–1157
15. Hidron AI, Kourbatova EV, Halvosa JS, et al. Risk factors for colonization with methicillin-resistant Staphylococcus aureus
(MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clin Infect Dis. 2005;41:159–166
16. Robicsek A, Beaumont JL, Paule SM, et al. Universal surveillance for methicillin-resistant Staphylococcus aureus
in 3 affiliated hospitals. Ann Intern Med. 2008;148:409–418
17. Lee BY, McGlone SM, Wong KF, et al. Modeling the spread of methicillin-resistant Staphylococcus aureus
(MRSA) outbreaks throughout the hospitals in Orange County, California. Infect Control Hosp Epidemiol. 2011;32:562–572
18. Donker T, Wallinga J, Grundmann H. Patient referral patterns and the spread of hospital-acquired infections through national health care networks. Plos Comput Biol. 2010;6:e1000715
19. Robotham JV, Scarff CA, Jenkins DR, et al. Meticillin-resistant Staphylococcus aureus
(MRSA) in hospitals and the community: model predictions based on the UK situation. J Hosp Infect. 2007;65(S2):93–99
20. Smith DL, Levin SA, Laxminarayan R. Strategic interactions in multi-institutional epidemics of antibiotic resistance. Proc Natl Acad Sci USA. 2005;102:3153–3158
21. Chamchod F, Ruan S. Modeling the spread of methicillin-resistant Staphylococcus aureus
in nursing homes for elderly. PLoS One. 2012;7:e29757
22. Barnes SL, Harris AD, Golden BL, et al. Contribution of interfacility patient movement to overall methicillin-resistant Staphylococcus aureus
prevalence levels. Infect Control Hosp Epidemiol. 2011;32:1073–1078
23. Lesosky M, McGeer A, Simor A, et al. Effect of patterns of transferring patients among healthcare institutions on rates of nosocomial methicillin-resistant Staphylococcus aureus
transmission: a monte carlo simulation. Infect Control Hosp Epidemiol. 2011;32:136–147
24. Office of Statewide Health Planning and Development,. Sacramento, CA2010 [updated October 4, 2010; cited 2010]; Available at: http://www.oshpd.ca.gov/
. Last accessed October 5, 2010
25. Huang SS, Avery TR, Song Y, et al. Quantifying interhospital patient sharing as a mechanism for infectious disease spread. Infect Control Hosp Epidemiol. 2010;31:1160–1169
26. Elkins KR, Nguyen CC, Kim D, et al. Successful strategies for high participation in three regional healthcare surveys: an observational study. BMC Med Res Methodol. 2011;11:176
27. Minimum Data Set. 2007 Baltimore, MD US Department of Health and Human Services
28. Murphy CR, Quan V, Kim D, et al. Nursing home characteristics associated with methicillin-resistant Staphylococcus aureus
(MRSA) burden and transmission. BMC Infect Dis. 2012;12:269
29. Chang S, Sethi AK, Eckstein BC, et al. Skin and environmental contamination with methicillin-resistant Staphylococcus aureus
among carriers identified clinically versus through active surveillance. Clin Infect Dis. 2009;48:1423–1428
30. Huang SS, Rifas-Shiman SL, Warren DK, et al. Improving methicillin-resistant Staphylococcus aureus
surveillance and reporting in intensive care units. J Infect Dis. 2007;195:330–338
31. Robicsek A, Beaumont JL, Peterson LR. Duration of colonization by methicillin-resistant Staphylococcus aureus
after hospital discharge and risk. Clin Infect Dis. 2009;48:910–913
32. Sanford MD, Widmer AF, Bale MJ, et al. Efficient detection and long-term persistance of the carriage for methicillin-resistant Staphylococcus aureus.
Clin Infect Dis. 1994;19:1123–1128
33. Scanvic A, Denic L, Gaillon S, et al. Duration of colonization by methicillin-resistant Staphylococcus aureus
after hospital discharge and risk factors for prolonged carriage. Clin Infect Dis. 2001;32:1393–1398
34. Kluytman J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus
: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10:505–520
35. Kellie SM, Timmins A, Brown C. A statewide collaborative to reduce methicillin-resistant Staphylococcus aureus
bacteremias in New Mexico. Jt Comm J Qual Patient Saf. 2011;37:154–162
36. Flanagan ME, Welsh CA, Kiess C, et al. A national collaborative for reducing health careassociated infections: current initiatives, challenges, and opportunities. Am J Infect Control. 2011;39:685–689
37. Ward MM, Clabaugh G, Evans TC, et al. A successful, voluntary, multicomponent statewide effort to reduce health care-associated infections. Am J Med Qual. 2012;27:66–73
38. Datta R, Quan V, Kim D, et al. Negative Correlation Between MRSA and MSSA Prevalence in Nursing Homes. 2011 Dallas, TX Society for Healthcare Epidemiology of America Annual Meeting
39. Mody L, Kauffman CA, Donabedian S, et al. Epidemiology of Staphylococcus aureus
colonization in nursing home residents. Clin Infect Dis. 2008;46:1368–1373
40. Trick WE, Weinstein RA, DeMarais PL, et al. Colonization of skilled-care facility residents with antimicrobial-resistant pathogens. J Am Geriatr Soc. 2001;49:270–276
41. Bradley SF, Terpenning MS, Ramsey MA, et al. Methicillin-resistant Staphylococcus aureus
: colonization and infection in a long-term care facility. Ann Intern Med. 1991;115:417–422
42. Muder RR, Brennen C, Wagener MM, et al. Methicillin-resistant staphylococcal colonization and infection in a long-term care facility. Ann Intern Med. 1991;114:107–112
43. Huang SS, Hinrichsen VL, Datta R, et al. Methicillin-resistant Staphylococcus aureus
infection and hospitalization in high-risk patients in the year following detection. PLoS One. 2011;6:e24340
44. Mulhausen PL, Harrell LJ, Weinberger M, et al. Contrasting methicillin-resistant Staphylococcus aureus
colonization in Veterans Affairs and community nursing homes. Am J Med. 1996;100:24–31
45. Capitano B, Leshem OA, Nightingale CH, et al. Cost effect of managing methicillin-resistant Staphylococcus aureus
in a long-term care facility. J Am Geriatr Soc. 2003;51:10–16
46. Suetens C, Niclaes L, Jans B, et al. Methicillin-resistant Staphylococcus aureus
colonization is associated with higher mortality in nursing home residents with impaired cognitive status. J Am Geriatr Soc. 2006;54:1854–1860
47. Klevens RM, Morrison MA, Nadle J, et al. Invasive methicillin-resistant Staphylococcus aureus
infections in the United States. J Am Med Assoc. 2007;298:1763–1771
48. Avery TR, Kleinman KP, Klompas M, et al. Inclusion of 30-day postdischarge detection triples the incidence of hospital-onset methicillin-resistant Staphylococcus aureus.
Infect Control Hosp Epidemiol. 2012;33:114–121
49. Bradley SF. Issues in the management of resistant bacteria in long-term-care facilites. Infect Control Hosp Epidemiol. 1999;20:362–367
50. Lee BY. Digital decision making: computer models and antibiotic prescribing in the twenty-first century. Clin Infect Dis. 2008;46:1139–1141
MRSA; outbreak; long-term care; nursing homes; hospitals
© 2013 Lippincott Williams & Wilkins, Inc.
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Highlight selected keywords in the article text.
Data is temporarily unavailable. Please try again soon.