Laboratory Analysis of an Outbreak of Candida auris in New York from 2016 to 2018: Impact and Lessons Learned.

Candida auris is a multidrug-resistant yeast which has emerged in health care facilities worldwide; however, little is known about identification methods, patient colonization, environmental survival, spread, and drug resistance. Colonization on both biotic (patients) and abiotic (health care objects) surfaces, along with travel, appear to be the major factors for the spread of this pathogen across the globe. In this investigation, we present laboratory findings from an ongoing C. auris outbreak in New York (NY) from August 2016 through 2018. A total of 540 clinical isolates, 11,035 patient surveillance specimens, and 3,672 environmental surveillance samples were analyzed. Laboratory methods included matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) for yeast isolate identification, real-time PCR for rapid surveillance sample screening, culture on selective/nonselective media for recovery of C. auris and other yeasts from surveillance samples, antifungal susceptibility testing to determine the C. auris resistance profile, and Sanger sequencing of the internal transcribed spacer (ITS) and D1/D2 regions of the ribosomal gene for C. auris genotyping. Results included (a) identification and confirmation of C. auris in 413 clinical isolates and 931 patient surveillance isolates as well as identification of 277 clinical cases and 350 colonized cases from 151 health care facilities, including 59 hospitals, 92 nursing homes, 1 long-term acute care hospital (LTACH), and 2 hospices, (b) successful utilization of an in-house developed C. auris real-time PCR assay for the rapid screening of patient and environmental surveillance samples, (c) demonstration of relatively heavier colonization of C. auris in nares than in the axilla/groin, and (d) predominance of the South Asia clade I with intrinsic resistance to fluconazole and elevated MIC to voriconazole (81%), amphotericin B (61%), flucytosine (5FC) (3%), and echinocandins (1%). These findings reflect greater regional prevalence and incidence of C. auris and the deployment of better detection tools in an unprecedented outbreak.

Candida auris in Healthcare Facilities, New York, USA, 2013-2017.

Candida auris is an emerging yeast that causes healthcare-associated infections. It can be misidentified by laboratories and often is resistant to antifungal medications. We describe an outbreak of C. auris infections in healthcare facilities in New York City, New York, USA. The investigation included laboratory surveillance, record reviews, site visits, contact tracing with cultures, and environmental sampling. We identified 51 clinical case-patients and 61 screening case-patients. Epidemiologic links indicated a large, interconnected web of affected healthcare facilities throughout New York City. Of the 51 clinical case-patients, 23 (45%) died within 90 days and isolates were resistant to fluconazole for 50 (98%). Of screening cultures performed for 572 persons (1,136 total cultures), results were C. auris positive for 61 (11%) persons. Environmental cultures were positive for samples from 15 of 20 facilities. Colonization was frequently identified during contact investigations; environmental contamination was also common.

Methicillin-resistant Staphylococcus aureus (MRSA) clusters in neonatal intensive care units (NICUs) and other neonatal units in New York State (NYS), 2001 to 2017.

BACKGROUND: New York State (NYS) mandates reporting of all hospital-associated communicable disease outbreaks. We describe trends in NYS surveillance for neonatal unit methicillin-resistant Staphylococcus aureus (MRSA) outbreaks, the evolution of national MRSA infection prevention and control (IPC) recommendations, and IPC measures taken by NYS neonatal units. METHODS: We evaluated trends of reported neonatal unit MRSA outbreaks by etiology from 2001 to 2017. We reviewed all reports and the use of IPC recommendations over time. RESULTS: From 2001 to 2017, 124 MRSA outbreaks were reported in 47 hospital neonatal units, with a total of 1,055 laboratory-confirmed infant cases, 18 infant deaths, and 52 laboratory-confirmed staff cases. The number of outbreaks increased with the level of care. During the study period, a higher proportion of hospitals reported implementing IPC measures, including reinforcing hand hygiene compliance (increased from 79.2% to 95.1%) and enhancing environmental cleaning and disinfection (increased from 4.2% to 78.0%) as well as performing active surveillance testing (AST) on exposed neonates (increased from 4.2% to 51.2%) and molecular testing on MRSA-positive isolates (increased from 5.3% to 18.9%). CONCLUSIONS: From 2001 to 2017, IPC measures in neonatal units increased in parallel with expanded national IPC recommendations. However, MRSA outbreaks in neonatal units continued to be frequent occurrences in NYS.

Risk factors for surgical site infection after abdominal hysterectomy, New York State, 2015-2018.

BACKGROUND: To identify risk factors for surgical site infections (SSIs) after abdominal hysterectomy (HYST) procedures using National Health care Safety Network (NHSN) data augmented with diagnosis codes available using administrative data. METHODS: We analyzed 66,001 HYST procedures in 166 New York State hospitals between January 2015 and December 2018, reported in NHSN, and matched to billing data. Risks factors for SSI after abdominal HYST were identified using logistic regression models. RESULTS: A total of 66,001 HYST procedures were analyzed. SSI was reported following 1,093 procedures, resulting in an infection rate of 1.66%. Risk factors associated with SSIs were open approach (not laparoscopic) with an adjusted odds ratio (AOR) of 2.72 and 95% confidence interval (CI) of 2.37-3.12, contaminated or dirty wound class (AOR 2.28, 95% CI 1.61-3.24), body mass index ≥30 (AOR 1.78, 95% CI 1.56-2.02), procedures lasting 186 minutes or more (AOR 1.78, 95% CI 1.56-2.02), American Society of Anesthesia (ASA) score ≥3 (AOR 1.74, 95% CI 1.52-1.99), gynecological cancer (AOR 1.54, 95% CI 1.32-1.80), and diabetes mellitus (AOR 1.46, 95% CI 1.24-1.70). CONCLUSIONS: Obesity, prolonged procedure duration, diabetes mellitus, wound contamination, open approach, ASA score ≥3, and gynecological cancer were significant independent risk factors associated with SSI after HYST.

Candida auris admission screening pilot in select units of New York City health care facilities, 2017-2019.

BACKGROUND: This pilot project implemented admission screening for Candida auris (C. auris) using real-time polymerase chain reaction (rt-PCR) in select high-risk units within health care facilities in New York City. METHODS: An admission screening encounter consisted of collecting 2 swabs, to be tested by rt-PCR, and a data collection form for individuals admitted to ventilator units at 2 nursing homes (NHA and NHB), and the ventilator/pulmonary unit, intensive care unit, and cardiac care unit at a hospital (Hospital C) located in New York City from November 2017 to November 2019. RESULTS: C. auris colonization was identified in 6.9% (n = 188/2,726) of admissions to participating units. Rates were higher among admissions to NHA and NHB (20.7% and 22.0%, respectively) than Hospital C (3.6%). Within Hospital C, the ventilator/pulmonary unit had a higher rate (5.7%) than the intensive care unit (3.8%) or cardiac care unit (2.5%). DISCUSSION: Consistent with prior research, we found that individuals admitted to ventilator units were at higher risk of C. auris colonization. CONCLUSIONS: This project demonstrates the utility of admission screening using rt-PCR testing to rapidly identify C. auris colonization among admissions to health care facilities so that appropriate transmission-based precautions and control measures can be implemented rapidly to help decrease transmission.

Dealing with highly skewed hospital length of stay distributions: The use of Gamma mixture models to study delivery hospitalizations.

The increased focus on addressing severe maternal morbidity and maternal mortality has led to studies investigating patient and hospital characteristics associated with longer hospital stays. Length of stay (LOS) for delivery hospitalizations has a strongly skewed distribution with the vast majority of LOS lasting two to three days in the United States. Prior studies typically focused on common LOSs and dealt with the long LOS distribution tail in ways to fit conventional statistical analyses (e.g., log transformation, trimming). This study demonstrates the use of Gamma mixture models to analyze the skewed LOS distribution. Gamma mixture models are flexible and, do not require data transformation or removal of outliers to accommodate many outcome distribution shapes, these models allow for the analysis of patients staying in the hospital for a longer time, which often includes those women experiencing worse outcomes. Random effects are included in the model to account for patients being treated within the same hospitals. Further, the role and influence of differing placements of covariates on the results is discussed in the context of distinct model specifications of the Gamma mixture regression model. The application of these models shows that they are robust to the placement of covariates and random effects. Using New York State data, the models showed that longer LOS for childbirth hospitalizations were more common in hospitals designated to accept more complicated deliveries, across hospital types, and among Black women. Primary insurance also was associated with LOS. Substantial variation between hospitals suggests the need to investigate protocols to standardize evidence-based medical care.

Surveillance of the short-term impact of fine particle air pollution on cardiovascular disease hospitalizations in New York State.

BACKGROUND: Studies have shown that the effects of particulate matter on health vary based on factors including the vulnerability of the population, health care practices, exposure factors, and the pollutant mix. METHODS: We used time-stratified case-crossover to estimate differences in the short-term impacts of PM2.5 on cardiovascular disease hospital admissions in New York State by geographic area, year, age, gender, co-morbid conditions, and area poverty rates. RESULTS: PM2.5 had a stronger impact on heart failure than other cardiovascular diagnoses, with 3.1% of heart failure admissions attributable to short-term PM2.5 exposure over background levels of 5 ug/m3. Older adults were significantly more susceptible to heart failure after short-term ambient PM2.5 exposure than younger adults. CONCLUSION: The short-term impact of PM2.5 on cardiovascular disease admissions, and modifications of that impact, are small and difficult to measure with precision. Multi-state collaborations will be necessary to attain more precision to describe spatiotemporal differences in health impacts.

Development of an interactive environmental public health tracking system for data analysis, visualization, and reporting.

Healthcare providers and governmental agencies routinely collect and report data on health outcomes. In addition, governmental agencies and industry collect and report information on environmental hazards and exposures that may impact health. Use of these data for environmental public health tracking has been a challenge because these data are managed by different data stewards, may contain confidential information that must be protected, and have not been collected in a manner to facilitate linkages. Available tools for analysis, visualization, and reporting of these data are either difficult to use or not available through a common user interface. The New York State Department of Health has developed a user-friendly interactive system to access and link these data while protecting confidential information. The Environmental Public health tracking system provides tools for describing the geographic patterns, trends, and statistical associations between health, environmental exposure, and environmental hazard data. These tools provide descriptive statistics and automated techniques that smooth the data in order to protect patient confidentiality and reduce random fluctuations in rates due to small numbers. This article describes the user interface, data linkages, and analytic, visualization, and reporting tools.

Lessons learned from initial reporting of carbapenem-resistant Enterobacteriaceae in New York State hospitals, 2013-2014.

BACKGROUND: Carbapenem-resistant Enterobacteriaceae (CRE) are an urgent concern in health care in the United States because of high attributable mortality and versatile resistance mechanisms. CRE reporting was mandated in New York State (NYS) hospitals in July 2013. METHODS: Infection preventionists from the NYS Department of Health audited hospital-reported CRE data by comparing laboratory records with cases reported to the National Healthcare Safety Network (NHSN). Information regarding microbiology laboratory testing methodologies was obtained through a survey in October 2013. RESULTS: There were 1,151 CRE laboratory reports audited, with 13.6% determined not to have been reported to the NHSN when they should have been and 4.6% determined to be reported in error. There were a variety of errors, including lapses in surveillance and misinterpretation of the surveillance definition. CONCLUSION: Educational initiatives that include microbiology laboratory staff, improvements in the use of laboratory information systems to communicate with infection prevention, and updated NHSN definitions should improve the accuracy and consistency of CRE reporting in NYS.

Effect of 2013 National Healthcare Safety Network definition changes on central line bloodstream infection rates: audit results from the New York State Department of Health.

Surveillance criteria for central line-associated bloodstream infections (CLABSIs) are continually being refined to more accurately reflect infections related to central lines. An audit of 567 medical records from adult, pediatric, and neonatal intensive care unit patients with a central line and a positive blood culture showed a 16% decrease in CLABSI rates after the 2013 National Healthcare Safety Network definitions compared with the 2012 definitions.

Geographic analysis of blood lead levels in New York State children born 1994-1997.

We examined the geographic distribution of the blood lead levels (BLLs) of 677,112 children born between 1994 and 1997 in New York State and screened before 2 years of age. Five percent of the children screened had BLLs higher than the current Centers for Disease Control and Prevention action level of 10 microg/dL. Rates were higher in upstate cities than in the New York City area. We modeled the relationship between BLLs and housing and socioeconomic characteristics at the ZIP code level. Older housing stock, a lower proportion of high school graduates, and a higher percentage of births to African-American mothers were the community characteristics most associated with elevated BLLs. Although the prevalence of children with elevated BLLs declined 44% between those born in 1994 and those born in 1997, the rate of improvement may be slowing down. Lead remains an environmental health problem in inner-city neighborhoods, particularly in upstate New York. We identified areas having a high prevalence of children with elevated BLLs. These communities can be targeted for educational and remediation programs. The model locates areas with a higher or lower prevalence of elevated BLLs than expected. These communities can be studied further at the individual level to better characterize the factors that contribute to these differences.

Seasonality and trend in blood lead levels of New York State children.

BACKGROUND: Environmental exposure to lead remains a significant health problem for children. The costs of lead exposure in children are estimated to be considerably more than other childhood diseases of environmental origin. While long-term trends in blood lead levels (BLLs) among children are declining, seasonal variation persists. Cross-sectional studies have found a peak in summer months. Part of this variation may be due to increased exposure to lead paint on window sills and through increased contact with soils containing lead during the summer. The current study represents the largest published population-based study on seasonality and trends in the BLLs of children to date. In addition, the results offer a comparison of recent data on seasonality of BLLs in New York State children, to studies conducted over the past three decades. METHODS: 262,687 New York State children born between 1994 and 1997 were screened for blood lead within 2 weeks of their first or second birthdays. Time series analyses of blood lead data from these children were conducted to study the seasonality and trends of BLLs. RESULTS: Children's blood lead values showed a distinct seasonal cycle on top of a long-term decreasing trend. The geometric mean BLL declined by about 24% for children born between 1994 and 1997. The prevalence of elevated BLLs in two-year-olds was almost twice that in one-year-olds over the time period. Nearly twice as many children had elevated BLLs in the late summer compared to late winter/early spring. In this and previous cross-sectional studies, the amount of seasonality as a proportion of the mean ranged between 15% and 30%. CONCLUSION: Pediatricians should be aware of the seasonality of BLLs. For example, if a two-year-old receives a borderline result during the winter, it is possible that the levels would have been higher if he had been tested during the summer. However, physicians should continue to screen children at their normally scheduled well-child visits rather than delaying until summertime and possibly postponing the discovery of an elevated BLL. Age, season, and time trends still need to be considered in lead studies and result interpretation.

Quantifying sources of bias in National Healthcare Safety Network laboratory-identified Clostridium difficile infection rates.

OBJECTIVE: To assess the effect of multiple sources of bias on state- and hospital-specific National Healthcare Safety Network (NHSN) laboratory-identified Clostridium difficile infection (CDI) rates. DESIGN: Sensitivity analysis. SETTING: A total of 124 New York hospitals in 2010. METHODS: New York NHSN CDI events from audited hospitals were matched to New York hospital discharge billing records to obtain additional information on patient age, length of stay, and previous hospital discharges. "Corrected" hospital-onset (HO) CDI rates were calculated after (1) correcting inaccurate case reporting found during audits, (2) incorporating knowledge of laboratory results from outside hospitals, (3) excluding days when patients were not at risk from the denominator of the rates, and (4) adjusting for patient age. Data sets were simulated with each of these sources of bias reintroduced individually and combined. The simulated rates were compared with the corrected rates. Performance (ie, better, worse, or average compared with the state average) was categorized, and misclassification compared with the corrected data set was measured. RESULTS: Counting days patients were not at risk in the denominator reduced the state HO rate by 45% and resulted in 8% misclassification. Age adjustment and reporting errors also shifted rates (7% and 6% misclassification, respectively). CONCLUSIONS: Changing the NHSN protocol to require reporting of age-stratified patient-days and adjusting for patient-days at risk would improve comparability of rates across hospitals. Further research is needed to validate the risk-adjustment model before these data should be used as hospital performance measures.

Surgical site infection risk factors identified for patients undergoing colon procedures, New York State 2009-2010.

BACKGROUND: Since 2007, New York State (NYS) hospitals have been required to report surgical site infections (SSIs) following colon procedures to the NYS Department of Health, using the National Healthcare Safety Network (NHSN). The purpose of this study was to identify risk factors for the development of SSIs in patients undergoing colon procedures. METHODS: NYS has been conducting validation studies at hospitals to assess the accuracy of the surveillance data reported by the participating hospitals. A sample of patients undergoing colon procedures in NYS hospitals were included in hospital-acquired infection program validation studies in 2009 and 2010. Medical chart reviews and on-site visits were performed to verify patient information reported and to evaluate additional risk factors for SSI. Bivariable and multivariable logistic regressions were performed. RESULTS: A total of 2,656 colon procedures were included in this analysis, including 698 SSI cases. Multivariable analysis indicated that SSI following colon procedure was associated with body mass index greater than 30 (odds ratio [OR], 1.48 [95% confidence interval (CI), 1.21-1.80]), male sex (OR, 1.34 [95% CI, 1.10-1.64]), American Society of Anesthesiologists physical classification score greater than 3 (OR, 1.33 [95% CI, 1.08-1.64]), procedure duration, transfusion (OR, 1.32 [95% CI, 1.05-1.66]), left-side colon surgical procedures, other gastroenterologic procedures, irrigation, hospital bed size greater than 500, and medical school affiliation. CONCLUSIONS: Male sex, obesity, transfusion, type of procedure, and prolonged duration were significant factors associated with overall infection risk after adjusting other factors. Additional factors not collected in the NHSN slightly improved prediction of SSIs.

Comparison of 2 Clostridium difficile surveillance methods: National Healthcare Safety Network's laboratory-identified event reporting module versus clinical infection surveillance.

OBJECTIVE: To determine whether the Centers for Disease Control and Prevention's National Healthcare Safety Network (NHSN) laboratory-identified (LabID) event reporting module for Clostridium difficile infection (CDI) is an adequate proxy measure of clinical CDI for public reporting purposes by comparing the 2 surveillance methods. DESIGN: Validation study. SETTING: Thirty New York State acute care hospitals. METHODS: Six months of data were collected by 30 facilities using a clinical infection surveillance definition while also submitting the NHSN LabID event for CDI. The data sets were matched and compared to determine whether the assigned clinical case status matched the LabID case status. A subset of mismatches was evaluated further, and reasons for the mismatches were quantified. Infection rates determined using the 2 definitions were compared. RESULTS: A total of 3,301 CDI cases were reported. Analysis of the original data yielded a 67.3% (2,223/3,301) overall case status match. After review and validation, there was 81.3% (2,683/3,301) agreement. The most common reason for disagreement (54.9%) occurred because the symptom onset was less than 48 hours after admission but the positive specimen was collected on hospital day 4 or later. The NHSN LabID hospital onset rate was 29% higher than the corresponding clinical rate and was generally consistent across all hospitals. CONCLUSIONS: Use of the NHSN LabID event minimizes the burden of surveillance and standardizes the process. With a greater than 80% match between the NHSN LabID event data and the clinical infection surveillance data, the New York State Department of Health made the decision to use the NHSN LabID event CDI data for public reporting purposes.

Trends in validity of central line-associated bloodstream infection surveillance data, New York State, 2007-2010.

BACKGROUND: In 2007, New York State (NYS) hospitals began mandatory public reporting of central line-associated bloodstream infection (CLABSI) data associated with intensive care units (ICUs) into the National Healthcare Safety Network (NHSN). Facilities were required to use the NHSN device-associated CLABSI criteria to identify laboratory-confirmed bloodstream infections. METHODS: Onsite audits were conducted in ICUs by NYS hospital-acquired infection program staff using a standardized database. Hospitals provided ICU patient medical records with a positive blood culture during a selected time frame. RESULTS: Between 2007 and 2010, an average of 79% of all reporting hospitals were audited annually. Of the 5,697 patients audited, 3,104 (54%) had a central line in place, and 650 of the patients with a central line (21%) were identified as having a CLABSI by the hospital-acquired infection program reviewer. Between 2007 and 2010, the specificity increased from 90% to 99%, whereas the sensitivity remained stable at approximately 71%. As a result of the audit process, the NYS 2010 CLABSI rate increased by 5.6%. CONCLUSIONS: A standardized audit process has helped improve the accuracy of CLABSI reporting. Data validation provides consistent data for measuring the progress of infection prevention strategies and allows for relevant comparison of ICU data.

Use of administrative data in efficient auditing of hospital-acquired surgical site infections, New York State 2009-2010.

OBJECTIVE: To efficiently validate the accuracy of surgical site infection (SSI) data reported to the National Healthcare Safety Network (NHSN) by New York State (NYS) hospitals. DESIGN: Validation study. SETTING: 176 NYS hospitals. METHODS: NYS Department of Health staff validated the data reported to NHSN by review of a stratified sample of medical records from each hospital. The four strata were (1) SSIs reported to NHSN; (2) records with an indication of infection from diagnosis codes in administrative data but not reported to NHSN as SSIs; (3) records with discordant procedure codes in NHSN and state data sets; (4) records not in the other three strata. RESULTS: A total of 7,059 surgical charts (6% of the procedures reported by hospitals) were reviewed. In stratum 1, 7% of reported SSIs did not meet the criteria for inclusion in NHSN and were subsequently removed. In stratum 2, 24% of records indicated missed SSIs not reported to NHSN, whereas in strata 3 and 4, only 1% of records indicated missed SSIs; these SSIs were subsequently added to NHSN. Also, in stratum 3, 75% of records were not coded for the correct NHSN procedure. Errors were highest for colon data; the NYS colon SSI rate increased by 7.5% as a result of hospital audits. CONCLUSIONS: Audits are vital for ensuring the accuracy of hospital-acquired infection (HAI) data so that hospital HAI rates can be fairly compared. Use of administrative data increased the efficiency of identifying problems in hospitals' SSI surveillance that caused SSIs to be unreported and caused errors in denominator data.

Risk factors for coronary artery bypass graft chest surgical site infections in New York State, 2008.

BACKGROUND: All hospitals in New York State (NYS) are required to report surgical site infections (SSIs) occurring after coronary artery bypass graft surgery. This report describes the risk adjustment method used by NYS for reporting hospital SSI rates, and additional methods used to explore remaining differences in infection rates. METHODS: All patients undergoing coronary artery bypass graft surgery in NYS in 2008 were monitored for chest SSI following the National Healthcare Safety Network protocol. The NYS Cardiac Surgery Reporting System and a survey of hospital infection prevention practices provided additional risk information. Models were developed to standardize hospital-specific infection rates and to assess additional risk factors and practices. RESULTS: The National Healthcare Safety Network risk score based on duration of surgery, American Society of Anesthesiologists score, and wound class were not highly predictive of chest SSIs. The addition of diabetes, obesity, end-stage renal disease, sex, chronic obstructive pulmonary disease, and Medicaid payer to the model improved the discrimination between procedures that resulted in SSI and those that did not by 25%. Hospital-reported infection prevention practices were not significantly related to SSI rates. CONCLUSIONS: Additional risk factors collected using a secondary database improved the prediction of SSIs, however, there remained unexplained variation in rates between hospitals.

Developing consistent data and methods to measure the public health impacts of ambient air quality for Environmental Public Health Tracking: progress to date and future directions.

Environmental Public Health Tracking (EPHT) staff at the state and national levels are developing nationally consistent data and methods to estimate the impact of ozone and fine particulate matter on hospitalizations for asthma and myocardial infarction. Pilot projects have demonstrated the feasibility of pooling state hospitalization data and linking these data to The United States Environmental Protection Agency (EPA) statistically based ambient air estimates for ozone and fine particulates. Tools were developed to perform case-crossover analyses to estimate concentration-response (C-R) functions. A weakness of analyzing one state at a time is that the effects are relatively small compared to their confidence intervals. The EPHT program will explore ways to statistically combine the results of peer-reviewed analyses from across the country to provide more robust C-R functions and health impact estimates at the local level. One challenge will be to routinely share data for these types of analyses at fine geographic and temporal scales without disclosing confidential information. Another challenge will be to develop C-R estimates which take into account time, space, or other relevant effect modifiers.