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1.  The Importance of Nursing Homes in the Spread of Methicillin-Resistant Staphylococcus aureus (MRSA) Among Hospitals 
Medical care  2013;51(3):205-215.
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 (RHEA), 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 healthcare 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 six 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 via patient transfers by an average 0.1% after six 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 via both direct and indirect (with intervening stays at home) patient sharing.
doi:10.1097/MLR.0b013e3182836dc2
PMCID: PMC3687037  PMID: 23358388
MRSA; Outbreak; Long-term Care; Nursing Homes; Hospitals
2.  Quantifying The Impact of Extra-Nasal Testing Body Sites for MRSA Colonization at the Time of Hospital or Intensive Care Unit Admission 
Objective
Methicillin-resistant Staphylococcus aureus (MRSA) is a common cause of healthcare-associated infections. Recent legislative mandates require nares screening for MRSA at hospital and ICU admission in many states. However, MRSA colonization at extra-nasal sites is increasingly recognized. We conducted a systematic review of the literature to identify the yield of extra-nasal testing for MRSA.
Design
We searched MEDLINE from January 1966 through January 2012 for articles comparing nasal and extra-nasal screening for MRSA colonization. Studies were categorized by population tested, specifically those admitted to ICUs, and those admitted to hospitals with a high prevalence (≥6%) or low prevalence (<6%) of MRSA carriers. Data were extracted using a standardized instrument.
Results
We reviewed 4,381 abstracts and 735 manuscripts. Twenty-three manuscripts met criteria for analysis (n=39,479 patients). Extra-nasal MRSA screening increased yield by approximately one-third over nares alone. The yield was similar upon ICU admission (weighted average 33%, range 9%–69%), and hospital admission in high (weighted average 37%, range 9–86%) and low prevalence (weighted average 50%, range 0–150%) populations. Comparing individual extra nasal sites, testing the oropharynx increased MRSA detection by 21% over nares alone; rectum by 20%; wounds by 17%; and axilla by 7%.
Conclusions
Extra-nasal MRSA screening at hospital or ICU admission in adults will increase MRSA detection by one-third compared to nares screening alone. Findings were consistent among subpopulations examined. Extra-nasal testing may be a valuable strategy for outbreak control or in settings of persistent disease, particularly when combined with decolonization or enhanced infection prevention protocols.
doi:10.1086/669095
PMCID: PMC3894230  PMID: 23295562
3.  Modeling the regional spread and control of vancomycin-resistant enterococci 
American journal of infection control  2013;41(8):10.1016/j.ajic.2013.01.013.
Background
Because patients can remain colonized with vancomycin-resistant enterococci (VRE) for long periods of time, VRE may spread from one health care facility to another.
Methods
Using the Regional Healthcare Ecosystem Analyst, an agent-based model of patient flow among all Orange County, California, hospitals and communities, we quantified the degree and speed at which changes in VRE colonization prevalence in a hospital may affect prevalence in other Orange County hospitals.
Results
A sustained 10% increase in VRE colonization prevalence in any 1 hospital caused a 2.8% (none to 62%) average relative increase in VRE prevalence in all other hospitals. Effects took from 1.5 to >10 years to fully manifest. Larger hospitals tended to have greater affect on other hospitals.
Conclusions
When monitoring and controlling VRE, decision makers may want to account for regional effects. Knowing a hospital’s connections with other health care facilities via patient sharing can help determine which hospitals to include in a surveillance or control program.
doi:10.1016/j.ajic.2013.01.013
PMCID: PMC3836830  PMID: 23896284
Vancomycin-resistant Enterococcus; Hospitals; Health care-associated infections; Modeling; Simulation
4.  Diversity of Methicillin-Resistant Staphylococcus aureus Strains Isolated from Residents of 26 Nursing Homes in Orange County, California 
Journal of Clinical Microbiology  2013;51(11):3788-3795.
Nursing homes represent a unique and important methicillin-resistant Staphylococcus aureus (MRSA) reservoir. Not only are strains imported from hospitals and the community, strains can be transported back into these settings from nursing homes. Since MRSA bacteria are prevalent in nursing homes and yet relatively poorly studied in this setting, a multicenter, regional assessment of the frequency and diversity of MRSA in the nursing home reservoir was carried out and compared to that of the MRSA from hospitals in the same region. The prospective study collected MRSA from nasal swabbing of residents of 26 nursing homes in Orange County, California, and characterized each isolate by spa typing. A total of 837 MRSA isolates were collected from the nursing homes. Estimates of admission prevalence and point prevalence of MRSA were 16% and 26%, respectively. The spa type genetic diversity was heterogeneous between nursing homes and significantly higher overall (77%) than the diversity in Orange County hospitals (72%). MRSA burden in nursing homes appears largely due to importation from hospitals. As seen in Orange County hospitals, USA300 (sequence type 8 [ST8]/t008), USA100 (ST5/t002), and a USA100 variant (ST5/t242) were the dominant MRSA clones in Orange County nursing homes, representing 83% of all isolates, although the USA100 variant was predominant in nursing homes, whereas USA300 was predominant in hospitals. Control strategies tailored to the complex problem of MRSA transmission and infection in nursing homes are needed in order to minimize the impact of this unique reservoir on the overall regional MRSA burden.
doi:10.1128/JCM.01708-13
PMCID: PMC3889768  PMID: 24025901
5.  The Potential Regional Impact of Contact Precaution Use in Nursing Homes to Control Methicillin-Resistant Staphylococcus aureus 
OBJECTIVE
Implementation of contact precautions in nursing homes to prevent methicillin-resistant Staphylococcus aureus (MRSA) transmission could cost time and effort and may have wide-ranging effects throughout multiple health facilities. Computational modeling could forecast the potential effects and guide policy making.
DESIGN
Our multihospital computational agent-based model, Regional Healthcare Ecosystem Analyst (RHEA).
SETTING
All hospitals and nursing homes in Orange County, California.
METHODS
Our simulation model compared the following 3 contact precaution strategies: (1) no contact precautions applied to any nursing home residents, (2) contact precautions applied to those with clinically apparent MRSA infections, and (3) contact precautions applied to all known MRSA carriers as determined by MRSA screening performed by hospitals.
RESULTS
Our model demonstrated that contact precautions for patients with clinically apparent MRSA infections in nursing homes resulted in a median 0.4% (range, 0%–1.6%) relative decrease in MRSA prevalence in nursing homes (with 50% adherence) but had no effect on hospital MRSA prevalence, even 5 years after initiation. Implementation of contact precautions (with 50% adherence) in nursing homes for all known MRSA carriers was associated with a median 14.2% (range, 2.1%–21.8%) relative decrease in MRSA prevalence in nursing homes and a 2.3% decrease (range, 0%–7.1%) in hospitals 1 year after implementation. Benefits accrued over time and increased with increasing compliance.
CONCLUSIONS
Our modeling study demonstrated the substantial benefits of extending contact precautions in nursing homes from just those residents with clinically apparent infection to all MRSA carriers, which suggests the benefits of hospitals and nursing homes sharing and coordinating information on MRSA surveillance and carriage status.
doi:10.1086/669091
PMCID: PMC3763186  PMID: 23295561
6.  Simulation Shows Hospitals That Cooperate On Infection Control Obtain Better Results Than Hospitals Acting Alone 
Health affairs (Project Hope)  2012;31(10):2295-2303.
Efforts to control life-threatening infections, such as with methicillin-resistant Staphylococcus aureus (MRSA), can be complicated when patients are transferred from one hospital to another. Using a detailed computer simulation model of all hospitals in Orange County, California, we explored the effects when combinations of hospitals tested all patients at admission for MRSA and adopted procedures to limit transmission among patients who tested positive. Called “contact isolation,” these procedures specify precautions for health care workers interacting with an infected patient, such as wearing gloves and gowns. Our simulation demonstrated that each hospital’s decision to test for MRSA and implement contact isolation procedures could affect the MRSA prevalence in all other hospitals. Thus, our study makes the case that further cooperation among hospitals—which is already reflected in a few limited collaborative infection control efforts under way—could help individual hospitals achieve better infection control than they could achieve on their own.
doi:10.1377/hlthaff.2011.0992
PMCID: PMC3763190  PMID: 23048111
7.  Trends in Antibiotic Use in Massachusetts Children, 2000–2009 
Pediatrics  2012;130(1):15-22.
OBJECTIVE:
Antibiotic use rates have declined dramatically since the 1990s. We aimed to determine if, when, and at what level the decline in antibiotic-dispensing rates ended and which diagnoses contributed to the trends.
METHODS:
Antibiotic dispensings and diagnoses were obtained from 2 health insurers for 3- to <72-month-olds in 16 Massachusetts communities from 2000 to 2009. Population-based antibiotic-dispensing rates per person-year (p-y) were determined according to year (September–August) for 3 age groups. Fit statistics were used to identify the most likely year for a change in trend. Rates for the first and last years were compared according to antibiotic category and associated diagnosis.
RESULTS:
From 2000–2001 to 2008–2009, the antibiotic-dispensing rate for 3- to <24-month-olds decreased 24% (2.3–1.8 antibiotic dispensings per p-y); for 24- to <48-month-olds, it decreased 18% (1.6–1.3 antibiotic dispensings per p-y); and for 48- to <72-month-olds, it decreased 20% (1.4–1.1 antibiotic dispensings per p-y). For 3- to <48-month-olds, rates declined until 2004–2005 and remained stable thereafter; the downward trend for 48- to <72-month-olds ended earlier in 2001–2002. Among 3- to <24-month-olds, first-line penicillin use declined 26%. For otitis media, the dispensing rate decreased 14% and the diagnosis rate declined 9%, whereas the treatment fraction was stable at 63%.
CONCLUSIONS:
The downward trend in antibiotic dispensings to young children in these communities ended by 2004–2005. This trend was driven by a declining otitis media diagnosis rate. Continued monitoring of population-based dispensing rates will support efforts to avoid returning to previous levels of antibiotic overuse.
doi:10.1542/peds.2011-3137
PMCID: PMC3382917  PMID: 22732172
antibiotic use; managed care programs; otitis media
8.  Chlorhexidine and Mupirocin Susceptibilities of Methicillin-Resistant Staphylococcus aureus from Colonized Nursing Home Residents 
Chlorhexidine and mupirocin are used in health care facilities to eradicate methicillin-resistant Staphylococcus aureus (MRSA) carriage. The objective of this study was to assess the frequency of chlorhexidine and mupirocin resistance in isolates from nares carriers in multiple nursing homes and to examine characteristics associated with resistance. Nasal swab samples were collected from approximately 100 new admissions and 100 current residents in 26 nursing homes in Orange County, CA, from October 2008 to May 2011. MRSA isolates were tested for susceptibility by using broth microdilution, disk diffusion, and Etest; for genetic relatedness using pulsed-field gel electrophoresis; and for qac gene carriage by PCR. Characteristics of the nursing homes and their residents were collected from the Medicare Minimum Data Set and Long-Term Care Focus. A total of 829 MRSA isolates were obtained from swabbing 3,806 residents in 26 nursing homes. All isolates had a chlorhexidine MIC of ≤4 μg/ml. Five (0.6%) isolates harbored the qacA and/or qacB gene loci. Mupirocin resistance was identified in 101 (12%) isolates, with 78 (9%) isolates exhibiting high-level mupirocin resistance (HLMR). HLMR rates per facility ranged from 0 to 31%. None of the isolates with HLMR displayed qacA or qacB, while two isolates carried qacA and exhibited low-level mupirocin resistance. Detection of HLMR was associated with having a multidrug-resistant MRSA isolate (odds ratio [OR], 2.69; P = 0.004), a history of MRSA (OR, 2.34; P < 0.001), and dependency in activities of daily living (OR, 1.25; P = 0.004). In some facilities, HLMR was found in nearly one-third of MRSA isolates. These findings may have implications for the increasingly widespread practice of MRSA decolonization using intranasal mupirocin.
doi:10.1128/AAC.01623-12
PMCID: PMC3535956  PMID: 23147721
9.  Methicillin-Resistant Staphylococcus aureus (MRSA) Burden in Nursing Homes is Associated with Environmental Contamination of Common Areas 
Background
Variation in MRSA prevalence across nursing homes is poorly understood. Differences in environmental cleaning may be one source of variable MRSA burden.
Design
Prospective study of environmental contamination and cleaning quality.
Setting/Participants
10 California nursing homes.
Measurements
We categorized nursing homes into two groups based upon high and low differences in MRSA point prevalence and admission prevalence (delta prevalence) from nares screenings of nursing home residents. We evaluated environmental cleaning and infection control practices by (a) culturing common area objects for MRSA, (b) assessing removal of intentionally-applied marks visible only under ultraviolet light (c) administering surveys on infection control and cleaning.
Results
Overall, 16% (78/500) of objects were MRSA-positive, and 22% (129/577) of UV-visible marks were removed. A higher proportion of MRSA-positive objects was found in the high vs. low nursing home groups (19% vs. 10%, p=0.005). Infection control and cleaning policies varied, including the frequency of common room cleaning (mean 2.5 times daily, range 1–3) and time spent cleaning per room (mean 18 min, range 7–45). In multivariate models, MRSA-positive objects were associated with high delta prevalence nursing homes (OR=2.8, p=0.005), facilities spending less time cleaning each room (OR = 2.9, p<0.001) and facilities where common rooms were cleaned less frequently (OR =1.5, p=0.01).
Conclusions
We found substantial variation in MRSA environmental contamination, infection control practices, and cleaning quality. MRSA environmental contamination was associated with larger differences between MRSA point and admission prevalence, less frequent common room cleaning, and less time spent cleaning per room. This suggests that modifying cleaning practices may reduce both MRSA environmental contamination and burden among nursing homes.
doi:10.1111/j.1532-5415.2012.03978.x
PMCID: PMC3376013  PMID: 22670708
Methicillin-resistant Staphylococcus aureus (MRSA); environmental contamination; cleaning quality; infection control; long term care facility
10.  Frequent Hospital Readmissions for Clostridium difficile Infection and the Impact on Estimates of Hospital-Associated C. difficile Burden 
Background
Clostridium difficile infection (CDI) is associated with medical care and may cause readmission following hospitalization for any reason. The incidence of readmissions due to CDI is not well known.
Design
Retrospective cohort study of adult inpatients in one county from 2000–2007, using mandatory hospital discharge data.
Setting
All hospitals in Orange County, California
Patients
All adult inpatients readmitted with new-onset Clostridium difficile infection within 12 weeks of discharge.
Measurements
We assessed trends in hospital-associated CDI (HA-CDI) incidence, with and without inclusion of post-discharge CDI (PD-CDI) events resulting in re-hospitalization within 12 weeks of discharge. We measured the effect of including PD-CDI events on hospital-specific CDI incidence, a mandatory reporting measure in California, and on relative hospital ranks by CDI incidence.
Results
From 2000 to 2007, countywide hospital-onset CDI (HO-CDI) incidence increased from 15/10,000 to 22/10,000 admissions. When including PD-CDI events, HA-CDI incidence doubled (29/10,000 in 2000 and 52/10,000 in 2007). Overall, including PD-CDI events resulted in significantly higher hospital-specific CDI incidence, although hospitals had disproportionate amounts of HA-CDI occurring post-discharge. This resulted in substantial shifts in some hospitals’ rankings by CDI incidence. In multivariate models, both HO and PD-CDI were associated with increasing age, higher length of stay, and select comorbidities. Race and Hispanic ethnicity were predictive of PD-CDI but not HO-CDI.
Limitations
PD-CDI incidence may be underestimated since outpatient events were not evaluated. Inaccuracies in claims data may cause under or over-estimation of CDI cases. Whether C. difficile was acquired in the hospital or community post-discharge for PD-CDI is not known.
Conclusions
PD-CDI events associated with re-hospitalization are increasingly common. The majority of HA-CDI cases now may be occurring post-discharge, raising important questions about both accurate reporting and effective prevention strategies. Some risk factors for PD-CDI may be different than those for HO-CDI, allowing additional identification of high-risk groups before discharge.
doi:10.1086/663209
PMCID: PMC3657466  PMID: 22173518
11.  Gastrointestinal Disease Outbreak Detection Using Multiple Data Streams from Electronic Medical Records 
Foodborne Pathogens and Disease  2012;9(5):431-441.
Abstract
Background: Passive reporting and laboratory testing delays may limit gastrointestinal (GI) disease outbreak detection. Healthcare systems routinely collect clinical data in electronic medical records (EMRs) that could be used for surveillance. This study's primary objective was to identify data streams from EMRs that may perform well for GI outbreak detection. Methods: Zip code-specific daily episode counts in 2009 were generated for 22 syndromic and laboratory-based data streams from Kaiser Permanente Northern California EMRs, covering 3.3 million members. Data streams included outpatient and inpatient diagnosis codes, antidiarrheal medication dispensings, stool culture orders, and positive microbiology tests for six GI pathogens. Prospective daily surveillance was mimicked using the space-time permutation scan statistic in single and multi-stream analyses, and space-time clusters were identified. Serotype relatedness was assessed for isolates in two Salmonella clusters. Results: Potential outbreaks included a cluster of 18 stool cultures ordered over 5 days in one zip code and a Salmonella cluster in three zip codes over 9 days, in which at least five of six cases had the same rare serotype. In all, 28 potential outbreaks were identified using single stream analyses, with signals in outpatient diagnosis codes most common. Multi-stream analyses identified additional potential outbreaks and in one example, improved the timeliness of detection. Conclusions: GI disease-related data streams can be used to identify potential outbreaks when generated from EMRs with extensive regional coverage. This process can supplement traditional GI outbreak reports to health departments, which frequently consist of outbreaks in well-defined settings (e.g., day care centers and restaurants) with no laboratory-confirmed pathogen. Data streams most promising for surveillance included microbiology test results, stool culture orders, and outpatient diagnoses. In particular, clusters of microbiology tests positive for specific pathogens could be identified in EMRs and used to prioritize further testing at state health departments, potentially improving outbreak detection.
doi:10.1089/fpd.2011.1036
PMCID: PMC3377951  PMID: 22429155
12.  Diversity of Methicillin-Resistant Staphylococcus aureus (MRSA) Strains Isolated from Inpatients of 30 Hospitals in Orange County, California 
PLoS ONE  2013;8(4):e62117.
There is a need for a regional assessment of the frequency and diversity of MRSA to determine major circulating clones and the extent to which community and healthcare MRSA reservoirs have mixed. We conducted a prospective cohort study of inpatients in Orange County, California, systematically collecting clinical MRSA isolates from 30 hospitals, to assess MRSA diversity and distribution. All isolates were characterized by spa typing, with selective PFGE and MLST to relate spa types with major MRSA clones. We collected 2,246 MRSA isolates from hospital inpatients. This translated to 91/10,000 inpatients with MRSA and an Orange County population estimate of MRSA inpatient clinical cultures of 86/100,000 people. spa type genetic diversity was heterogeneous between hospitals, and relatively high overall (72%). USA300 (t008/ST8), USA100 (t002/ST5) and a previously reported USA100 variant (t242/ST5) were the dominant clones across all Orange County hospitals, representing 83% of isolates. Fifteen hospitals isolated more t008 (USA300) isolates than t002/242 (USA100) isolates, and 12 hospitals isolated more t242 isolates than t002 isolates. The majority of isolates were imported into hospitals. Community-based infection control strategies may still be helpful in stemming the influx of traditionally community-associated strains, particularly USA300, into the healthcare setting.
doi:10.1371/journal.pone.0062117
PMCID: PMC3634754  PMID: 23637976
13.  Beyond 30 Days: Does limiting the duration of surgical site infection follow-up limit detection? 
Concern over consistency and completeness of surgical site infection (SSI) surveillance has increased due to public reporting of hospital SSI rates and imminent non-payment rules for hospitals that do not meet national benchmarks. 1 Already, hospitals no longer receive additional payment from the Centers for Medicare & Medicaid Services (CMS) for certain infections following coronary artery bypass graft (CABG) surgery, orthopedic procedures, and bariatric surgery.2
One major concern is incomplete and differential post-discharge surveillance. At present, substantial variation exists in how and whether hospitals identify SSI events after the hospitalization in which the surgery occurred. Parameters used for SSI surveillance such as the duration of the window of time that surveillance takes place following the surgical procedure can impact the completeness of surveillance data. Determination of the optimal surveillance time period involves balancing the potential increased case ascertainment associated with a longer follow-up period with the increased resources that would be required. Currently, the time window for identifying potentially preventable SSIs related to events at the time of surgery is not fully standardized. The Centers for Disease Control and Prevention (CDC) National Healthcare Surveillance Network (NHSN) requires a 365-day postoperative surveillance period for procedures involving implants and a 30-day period for non-implant procedures. 3 In contrast, the National Surgical Quality Improvement Program (NSQIP) and the Society of Thoracic Surgeons (STS) systems employ 30-day post-operative surveillance regardless of implant. As consensus builds towards national quality measures for hospital-specific SSI rates, it will be important to assess the frequency of events beyond the 30-day post-surgical window that may quantify the value of various durations of surveillance, and ultimately inform the choice of specific outcome measures.
doi:10.1086/663715
PMCID: PMC3608264  PMID: 22227993
14.  Pneumococcal Carriage and Antibiotic Resistance in Young Children before 13-Valent Conjugate Vaccine 
Background
We sought to measure trends in Streptococcus pneumoniae (SP) carriage and antibiotic resistance in young children in Massachusetts communities after widespread adoption of heptavalent pneumococcal conjugate vaccine (PCV7) and before the introduction of the 13-valent pneumococcal conjugate vaccine (PCV13).
Methods
We conducted a cross-sectional study including collection of questionnaire data and nasopharyngeal specimens among children <7 years in primary care practices from 8 Massachusetts communities during the winter season of 2008–9 and compared with to similar studies performed in 2001, 2003–4, and 2006–7. Antimicrobial susceptibility testing and serotyping were performed on pneumococcal isolates, and risk factors for colonization in recent seasons (2006–07 and 2008–09) were evaluated.
Results
We collected nasopharyngeal specimens from 1,011 children, 290 (29%) of whom were colonized with pneumococcus. Non-PCV7 serotypes accounted for 98% of pneumococcal isolates, most commonly 19A (14%), 6C (11%), and 15B/C (11%). In 2008–09, newly-targeted PCV13 serotypes accounted for 20% of carriage isolates and 41% of penicillin non-susceptible S. pneumoniae (PNSP). In multivariate models, younger age, child care, young siblings, and upper respiratory illness remained predictors of pneumococcal carriage, despite near-complete serotype replacement. Only young age and child care were significantly associated with PNSP carriage.
Conclusions
Serotype replacement post-PCV7 is essentially complete and has been sustained in young children, with the relatively virulent 19A being the most common serotype. Predictors of carriage remained similar despite serotype replacement. PCV13 may reduce 19A and decrease antibiotic-resistant strains, but monitoring for new serotype replacement is warranted.
doi:10.1097/INF.0b013e31824214ac
PMCID: PMC3288953  PMID: 22173142
Streptococcus pneumoniae; pneumococcal conjugate vaccine; antibiotic resistance; serotype; colonization
15.  Nursing home characteristics associated with methicillin-resistant Staphylococcus aureus (MRSA) Burden and Transmission 
BMC Infectious Diseases  2012;12:269.
Background
MRSA prevalence in nursing homes often exceeds that in hospitals, but reasons for this are not well understood. We sought to measure MRSA burden in a large number of nursing homes and identify facility characteristics associated with high MRSA burden.
Methods
We performed nasal swabs of residents from 26 nursing homes to measure MRSA importation and point prevalence, and estimate transmission. Using nursing home administrative data, we identified facility characteristics associated with MRSA point prevalence and estimated transmission risk in multivariate models.
Results
We obtained 1,649 admission and 2,111 point prevalence swabs. Mean MRSA point prevalence was 24%, significantly higher than mean MRSA admission prevalence, 16%, (paired t-test, p<0.001), with a mean estimated MRSA transmission risk of 16%.
In multivariate models, higher MRSA point prevalence was associated with higher admission prevalence (p=0.005) and higher proportions of residents with indwelling devices (p=0.01). Higher estimated MRSA transmission risk was associated with higher proportions of residents with diabetes (p=0.01) and lower levels of social engagement (p=0.03).
Conclusions
MRSA importation was a strong predictor of MRSA prevalence, but MRSA burden and transmission were also associated with nursing homes caring for more residents with chronic illnesses or indwelling devices. Frequent social interaction among residents appeared to be protective of MRSA transmission, suggesting that residents healthy enough to engage in group activities do not incur substantial risks of MRSA from social contact. Identifying characteristics of nursing homes at risk for high MRSA burden and transmission may allow facilities to tailor infection control policies and interventions to mitigate MRSA spread.
doi:10.1186/1471-2334-12-269
PMCID: PMC3528666  PMID: 23095678
MRSA; Healthcare-associated infection; Long-term care; Nursing home
16.  Modeling the Spread of Methicillin-Resistant Staphylococcus aureus (MRSA) Outbreaks throughout the Hospitals in Orange County, California 
Background
Since hospitals in a region often share patients, an outbreak of methicillin-resistant Staphylococcus aureus (MRSA) infection in one hospital could affect other hospitals.
Methods
Using extensive data collected from Orange County (OC), California, we developed a detailed agent-based model to represent patient movement among all OC hospitals. Experiments simulated MRSA outbreaks in various wards, institutions, and regions. Sensitivity analysis varied lengths of stay, intraward transmission coefficients (β), MRSA loss rate, probability of patient transfer or readmission, and time to readmission.
Results
Each simulated outbreak eventually affected all of the hospitals in the network, with effects depending on the outbreak size and location. Increasing MRSA prevalence at a single hospital (from 5% to 15%) resulted in a 2.9% average increase in relative prevalence at all other hospitals (ranging from no effect to 46.4%). Single-hospital intensive care unit outbreaks (modeled increase from 5% to 15%) caused a 1.4% average relative increase in all other OC hospitals (ranging from no effect to 12.7%).
Conclusion
MRSA outbreaks may rarely be confined to a single hospital but instead may affect all of the hospitals in a region. This suggests that prevention and control strategies and policies should account for the interconnectedness of health care facilities.
doi:10.1086/660014
PMCID: PMC3388111  PMID: 21558768
17.  Carried Pneumococci in Massachusetts Children; The Contribution of Clonal Expansion and Serotype Switching 
doi:10.1097/INF.0b013e318201a154
PMCID: PMC3175614  PMID: 21085049
MLST; conjugate vaccination; Streptococcus pneumoniae; nasopharyngeal carriage
18.  Social Network Analysis of Patient Sharing Among Hospitals in Orange County, California 
American journal of public health  2011;101(4):707-713.
Objectives
We applied social network analyses to determine how hospitals within Orange County, California, are interconnected by patient sharing, a system which may have numerous public health implications.
Methods
Our analyses considered 2 general patient-sharing networks: uninterrupted patient sharing (UPS; i.e., direct interhospital transfers) and total patient sharing (TPS; i.e., all interhospital patient sharing, including patients with intervening nonhospital stays). We considered these networks at 3 thresholds of patient sharing: at least 1, at least 10, and at least 100 patients shared.
Results
Geographically proximate hospitals were somewhat more likely to share patients, but many hospitals shared patients with distant hospitals. Number of patient admissions and percentage of cancer patients were associated with greater connectivity across the system. The TPS network revealed numerous connections not seen in the UPS network, meaning that direct transfers only accounted for a fraction of total patient sharing.
Conclusions
Our analysis demonstrated that Orange County’s 32 hospitals were highly and heterogeneously interconnected by patient sharing. Different hospital populations had different levels of influence over the patient-sharing network.
doi:10.2105/AJPH.2010.202754
PMCID: PMC3052345  PMID: 21330578
19.  Differences in Methicillin-Resistant Staphylococcus aureus Strains Isolated from Pediatric and Adult Patients from Hospitals in a Large County in California 
Journal of Clinical Microbiology  2012;50(3):573-579.
Studies of U.S. epidemics of community- and health care-associated methicillin-resistant Staphylococcus aureus (MRSA) suggested differences in MRSA strains in adults and those in children. Comprehensive population-based studies exploring these differences are lacking. We conducted a prospective cohort study of inpatients in Orange County, CA, collecting clinical MRSA isolates from 30 of 31 Orange County hospitals, to characterize differences in MRSA strains isolated from children compared to those isolated from adults. All isolates were characterized by spa typing. We collected 1,124 MRSA isolates from adults and 159 from children. Annual Orange County population estimates of MRSA inpatient clinical cultures were 119/100,000 adults and 22/100,000 children. spa types t008, t242, and t002 accounted for 83% of all isolates. The distribution of these three spa types among adults was significantly different from that among children (χ2 = 52.29; P < 0.001). Forty-one percent of adult isolates were of t008 (USA300), compared to 69% of pediatric isolates. In multivariate analyses, specimens from pediatric patients, wounds, non-intensive care unit (ICU) wards, and hospitals with a high proportion of Medicaid-insured patients were significantly associated with the detection of t008 strains. While community- and health care-associated MRSA reservoirs have begun to merge, significant differences remain in pediatric and adult patient populations. Community-associated MRSA spa type t008 is significantly more common in pediatric patients.
doi:10.1128/JCM.05336-11
PMCID: PMC3295185  PMID: 22205805
20.  Successful strategies for high participation in three regional healthcare surveys: an observational study 
Background
Regional healthcare facility surveys to quantitatively assess nosocomial infection rates are important for confirming standardized data collection and assessing health outcomes in the era of mandatory reporting. This is particularly important for the assessment of infection control policies and healthcare associated infection rates among hospitals. However, the success of such surveys depends upon high participation and representativeness of respondents.
Methods
This descriptive paper provides methodologies that may have contributed to high participation in a series of administrative, infection control, and microbiology laboratory surveys of all 31 hospitals in a large southern California county. We also report 85% (N = 72) countywide participation in an administrative survey among nursing homes in this same area.
Results
Using in-person recruitment, 48% of hospitals and nursing homes were recruited within one quarter, with 75% recruited within three quarters.
Conclusions
Potentially useful strategies for successful recruitment included in-person recruitment, partnership with the local public health department, assurance of anonymity when presenting survey results, and provision of staff labor for the completion of detailed survey tables on the rates of healthcare associated pathogens. Data collection assistance was provided for three-fourths of surveys. High compliance quantitative regional surveys require substantial recruitment time and study staff support for high participation.
doi:10.1186/1471-2288-11-176
PMCID: PMC3261126  PMID: 22208721
21.  Long-Term Care Facilities: Important Participants of the Acute Care Facility Social Network? 
PLoS ONE  2011;6(12):e29342.
Background
Acute care facilities are connected via patient sharing, forming a network. However, patient sharing extends beyond this immediate network to include sharing with long-term care facilities. The extent of long-term care facility patient sharing on the acute care facility network is unknown. The objective of this study was to characterize and determine the extent and pattern of patient transfers to, from, and between long-term care facilities on the network of acute care facilities in a large metropolitan county.
Methods/Principal Findings
We applied social network constructs principles, measures, and frameworks to all 2007 annual adult and pediatric patient transfers among the healthcare facilities in Orange County, California, using data from surveys and several datasets. We evaluated general network and centrality measures as well as individual ego measures and further constructed sociograms. Our results show that over the course of a year, 66 of 72 long-term care facilities directly sent and 67 directly received patients from other long-term care facilities. Long-term care facilities added 1,524 ties between the acute care facilities when ties represented at least one patient transfer. Geodesic distance did not closely correlate with the geographic distance among facilities.
Conclusions/Significance
This study demonstrates the extent to which long-term care facilities are connected to the acute care facility patient sharing network. Many long-term care facilities were connected by patient transfers and further added many connections to the acute care facility network. This suggests that policy-makers and health officials should account for patient sharing with and among long-term care facilities as well as those among acute care facilities when evaluating policies and interventions.
doi:10.1371/journal.pone.0029342
PMCID: PMC3246493  PMID: 22216255
22.  Serotype Specific Invasive Capacity and Persistent Reduction in Invasive Pneumococcal Disease 
Vaccine  2010;29(2):283-288.
Defining the propensity of Streptoccocus pneumoniae (SP) serotypes to invade sterile body sites following nasopharyngeal (NP) acquisition has the potential to inform about how much invasive pneumococcal disease (IPD) may occur in a typical population with a given distribution of carriage serotypes. Data from enhanced surveillance for IPD in Massachusetts children ≤7 years in 2003/04, 2006/07 and 2008/09 seasons and surveillance of SP NP carriage during the corresponding respiratory seasons in 16 Massachusetts communities in 2003/04 and 8 of the 16 communities in both 2006/07 and 2008/09 were used to compute a serotype specific “invasive capacity (IC)” by dividing the incidence of IPD due to serotype x by the carriage prevalence of that same serotype in children of the same age. A total of 206 IPD and 806 NP isolates of SP were collected during the study period. An approximate 50-fold variation in the point estimates between the serotypes having the highest (18C, 33F, 7F, 19A, 3 and 22F) and lowest (6C, 23A, 35F, 11A, 35B, 19F, 15A, and 15BC) IC was observed. Point estimates of IC for most of the common serotypes currently colonizing children in Massachusetts were low and likely explain the continued reduction in IPD from the pre-PCV era in the absence of specific protection against these serotypes. Invasive capacity differs among serotypes and as new pneumococcal conjugate vaccines are introduced, ongoing surveillance will be essential to monitor whether serotypes with high invasive capacity emerge (e.g. 33F, 22F) as successful colonizers resulting in increased IPD incidence due to replacement serotypes.
doi:10.1016/j.vaccine.2010.10.032
PMCID: PMC3139683  PMID: 21029807
Streptoccocus pneumoniae; serotype; invasive capacity
23.  Quantifying Interhospital Patient Sharing as a Mechanism for Infectious Disease Spread 
BACKGROUND
Assessments of infectious disease spread in hospitals seldom account for interfacility patient sharing. This is particularly important for pathogens with prolonged incubation periods or carrier states.
METHODS
We quantified patient sharing among all 32 hospitals in Orange County (OC), California, using hospital discharge data. Same-day transfers between hospitals were considered “direct” transfers, and events in which patients were shared between hospitals after an intervening stay at home or elsewhere were considered “indirect” patient-sharing events. We assessed the frequency of readmissions to another OC hospital within various time points from discharge and examined interhospital sharing of patients with Clostridium difficile infection.
RESULTS
In 2005, OC hospitals had 319,918 admissions. Twenty-nine percent of patients were admitted at least twice, with a median interval between discharge and readmission of 53 days. Of the patients with 2 or more admissions, 75% were admitted to more than 1 hospital. Ninety-four percent of interhospital patient sharing occurred indirectly. When we used 10 shared patients as a measure of potential interhospital exposure, 6 (19%) of 32 hospitals “exposed” more than 50% of all OC hospitals within 6 months, and 17 (53%) exposed more than 50% within 12 months. Hospitals shared 1 or more patient with a median of 28 other hospitals. When we evaluated patients with C. difficile infection, 25% were readmitted within 12 weeks; 41% were readmitted to different hospitals, and less than 30% of these readmissions were direct transfers.
CONCLUSIONS
In a large metropolitan county, interhospital patient sharing was a potential avenue for transmission of infectious agents. Indirect sharing with an intervening stay at home or elsewhere composed the bulk of potential exposures and occurred unbeknownst to hospitals.
doi:10.1086/656747
PMCID: PMC3064463  PMID: 20874503
24.  Methicillin-Resistant Staphylococcus aureus Infection and Hospitalization in High-Risk Patients in the Year following Detection 
PLoS ONE  2011;6(9):e24340.
Background
Many studies have evaluated methicillin-resistant Staphylococcus aureus (MRSA) infections during single hospitalizations and subsequent readmissions to the same institution. None have assessed the comprehensive burden of MRSA infection in the period after hospital discharge while accounting for healthcare utilization across institutions.
Methodology/Principal Findings
We conducted a retrospective cohort study of adult patients insured by Harvard Pilgrim Health Care who were newly-detected to harbor MRSA between January 1991 and December 2003 at a tertiary care medical center. We evaluated all MRSA-attributable infections associated with hospitalization in the year following new detection, regardless of hospital location. Data were collected on comorbidities, healthcare utilization, mortality and MRSA outcomes. Of 591 newly-detected MRSA carriers, 23% were colonized and 77% were infected upon detection. In the year following detection, 196 (33%) patients developed 317 discrete and unrelated MRSA infections. The most common infections were pneumonia (34%), soft tissue (27%), and primary bloodstream (18%) infections. Infections occurred a median of 56 days post-detection. Of all infections, 26% involved bacteremia, and 17% caused MRSA-attributable death. During the admission where MRSA was newly-detected, 14% (82/576) developed subsequent infection. Of those surviving to discharge, 24% (114/482) developed post-discharge infections in the year following detection. Half (99/185, 54%) of post-discharge infections caused readmission, and most (104/185, 55%) occurred over 90 days post-discharge.
Conclusions/Significance
In high-risk tertiary care patients, newly-detected MRSA carriage confers large risks of infection and substantial attributable mortality in the year following acquisition. Most infections occur post-discharge, and 18% of infections associated with readmission occurred in hospitals other than the one where MRSA was newly-detected. Despite gains in reducing MRSA infections during hospitalization, the risk of MRSA infection among critically and chronically ill carriers persists after discharge and warrants targeted prevention strategies.
doi:10.1371/journal.pone.0024340
PMCID: PMC3174953  PMID: 21949707
25.  Colonization with antibiotic-susceptible strains protects against methicillin-resistant Staphylococcus aureus but not vancomycin-resistant enterococci acquisition: a nested case-control study 
Critical Care  2011;15(5):R210.
Introduction
Harboring sensitive strains may prevent acquisition of resistant pathogens by competing for colonization of ecological niches. Competition may be relevant to decolonization strategies that eliminate sensitive strains and may predispose to acquiring resistant strains in high-endemic settings. We evaluated the impact of colonization with methicillin-sensitive Staphylococcus aureus (MSSA) and vancomycin-sensitive enterococci (VSE) on acquisition of methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant enterococci (VRE), respectively, when controlling for other risk factors.
Methods
We conducted a nested case-control study of patients admitted to eight ICUs performing admission and weekly bilateral nares and rectal screening for MRSA and VRE, respectively. Analyses were identical for both pathogens. For MRSA, patients were identified who had a negative nares screen and no prior history of MRSA. We evaluated predictors of MRSA acquisition, defined as a subsequent MRSA-positive clinical or screening culture, compared to those with a subsequent MRSA-negative nares screen within the same hospitalization. Medical records were reviewed for the presence of MSSA on the initial MRSA-negative nares screen, demographic and comorbidity information, medical devices, procedures, antibiotic utilization, and daily exposure to MRSA-positive patients in the same ward. Generalized linear mixed models were used to assess predictors of acquisition.
Results
In multivariate models, MSSA carriage protected against subsequent MRSA acquisition (OR = 0.52, CI: 0.29, 0.95), even when controlling for other risk factors. MRSA predictors included intubation (OR = 4.65, CI: 1.77, 12.26), fluoroquinolone exposure (OR = 1.91, CI: 1.20, 3.04), and increased time from ICU admission to initial negative swab (OR = 15.59, CI: 8.40, 28.94). In contrast, VSE carriage did not protect against VRE acquisition (OR = 1.37, CI: 0.54, 3.48), whereas hemodialysis (OR = 2.60, CI: 1.19, 5.70), low albumin (OR = 2.07, CI: 1.12, 3.83), fluoroquinolones (OR = 1.90, CI: 1.14, 3.17), third-generation cephalosporins (OR = 1.89, CI: 1.15, 3.10), and increased time from ICU admission to initial negative swab (OR = 15.13, CI: 7.86, 29.14) were predictive.
Conclusions
MSSA carriage reduced the odds of MRSA acquisition by 50% in ICUs. In contrast, VSE colonization was not protective against VRE acquisition. Studies are needed to evaluate whether decolonization of MSSA ICU carriers increases the risk of acquiring MRSA when discharging patients to high-endemic MRSA healthcare settings. This may be particularly important for populations in whom MRSA infection may be more frequent and severe than MSSA infections, such as ICU patients.
doi:10.1186/cc10445
PMCID: PMC3334754  PMID: 21914221

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