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Anesthesia & Analgesia:
doi: 10.1213/ANE.0b013e31824970a2
Patient Safety: Research Reports

Multiple Reservoirs Contribute to Intraoperative Bacterial Transmission

Loftus, Randy W. MD*; Brown, Jeremiah R. PhD, MS; Koff, Matthew D. MD, MS*; Reddy, Sundara MD; Heard, Stephen O. MD§; Patel, Hetal M. BS, MLT*; Fernandez, Patrick G. MD*; Beach, Michael L. MD*; Corwin, Howard L. MD; Jensen, Jens T. MS*; Kispert, David BA*; Huysman, Bridget BA*; Dodds, Thomas M. MD*; Ruoff, Kathryn L. PhD; Yeager, Mark P. MD*

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Author Information

From the *Department of Anesthesiology, Dartmouth–Hitchcock Medical Center, Lebanon, NH; Dartmouth Institute for Health Policy and Clinical Practice, Dartmouth College of Medicine, Lebanon, NH; Department of Anesthesiology, University of Iowa Hospitals and Clinics, Iowa City, IA; §Department of Anesthesiology, University of Massachusetts Memorial Medical Center, Worcester, MA; Department of Critical Care Medicine, Dartmouth–Hitchcock Medical Center Lebanon, NH; Department of Pathology, Dartmouth–Hitchcock Medical Center, Lebanon, NH.

Funding: Anesthesia Patient Safety Foundation, 2009.

The authors declare no conflict of interest.

Reprints will not be available from the authors.

Address correspondence to Randy W. Loftus, MD, Dartmouth–Hitchcock Medical Center, 1 Medical Center Dr., Lebanon, NH 03756. Address e-mail to randy.loftus@hitchcock.org.

Accepted December 7, 2011

Published ahead of print March 30, 2012

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Abstract

BACKGROUND: Intraoperative stopcock contamination is a frequent event associated with increased patient mortality. In the current study we examined the relative contributions of anesthesia provider hands, the patient, and the patient environment to stopcock contamination. Our secondary aims were to identify risk factors for stopcock contamination and to examine the prior association of stopcock contamination with 30-day postoperative infection and mortality. Additional microbiological analyses were completed to determine the prevalence of bacterial pathogens within intraoperative bacterial reservoirs. Pulsed-field gel electrophoresis was used to assess the contribution of reservoir bacterial pathogens to 30-day postoperative infections.

METHODS: In a multicenter study, stopcock transmission events were observed in 274 operating rooms, with the first and second cases of the day in each operating room studied in series to identify within- and between-case transmission events. Reservoir bacterial cultures were obtained and compared with stopcock set isolates to determine the origin of stopcock contamination. Between-case transmission was defined by the isolation of 1 or more bacterial isolates from the stopcock set of a subsequent case (case 2) that were identical to reservoir isolates from the preceding case (case 1). Within-case transmission was defined by the isolation of 1 or more bacterial isolates from a stopcock set that were identical to bacterial reservoirs from the same case. Bacterial pathogens within these reservoirs were identified, and their potential contribution to postoperative infections was evaluated. All patients were followed for 30 days postoperatively for the development of infection and all-cause mortality.

RESULTS: Stopcock contamination was detected in 23% (126 out of 548) of cases with 14 between-case and 30 within-case transmission events confirmed. All 3 reservoirs contributed to between-case (64% environment, 14% patient, and 21% provider) and within-case (47% environment, 23% patient, and 30% provider) stopcock transmission. The environment was a more likely source of stopcock contamination than provider hands (relative risk [RR] 1.91, confidence interval [CI] 1.09 to 3.35, P = 0.029) or patients (RR 2.56, CI 1.34 to 4.89, P = 0.002). Hospital site (odds ratio [OR] 5.09, CI 2.02 to 12.86, P = 0.001) and case 2 (OR 6.82, CI 4.03 to 11.5, P < 0.001) were significant predictors of stopcock contamination. Stopcock contamination was associated with increased mortality (OR 58.5, CI 2.32 to 1477, P = 0.014). Intraoperative bacterial contamination of patients and provider hands was linked to 30-day postoperative infections.

CONCLUSIONS: Bacterial contamination of patients, provider hands, and the environment contributes to stopcock transmission events, but the surrounding patient environment is the most likely source. Stopcock contamination is associated with increased patient mortality. Patient and provider bacterial reservoirs contribute to 30-day postoperative infections. Multimodal programs designed to target each of these reservoirs in parallel should be studied intensely as a comprehensive approach to reducing intraoperative bacterial transmission.

Health care-associated infections (HCAIs) are a major public health concern.15 Bacterial cross-contamination is thought to play an important role in HCAI development, but the relative importance of the known hospital bacterial reservoirs (health care provider hands, patient, and environment, including health care equipment) in this process is unknown.611 A better understanding of how bacterial cross-contamination occurs can provide the basis for the development of evidence-based preventive measures. The relatively controlled intraoperative environment provides a unique opportunity to examine these relationships. Studies have shown that intraoperative bacterial contamination of patient IV stopcock sets is common and is related to bacterial contamination of anesthesia provider hands before patient care.1214 However, the relative contributions of other known intraoperative bacterial reservoirs including the patient, the patient environment, and provider hand contamination throughout the process of patient care to stopcock transmission have not been characterized. The primary aim of the current study was to examine these relationships. The secondary aims were to identify risk factors for stopcock contamination and to examine the prior association of stopcock contamination with increased 30-day postoperative infection and mortality. Additional microbiological analyses were completed to determine the frequency with which provider hands serve as vectors for transmission between intraoperative bacterial reservoirs, to examine the efficacy of current environmental decontamination practices, and to determine the prevalence of bacterial pathogens within intraoperative bacterial reservoirs and the contribution of those pathogens to 30-day postoperative infection development. The frequency of provider hourly hand decontamination events (HDEs) was also observed.

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METHODS

General Description

This was a prospective, randomized, observational study performed at 3 institutions, Dartmouth–Hitchcock Medical Center (DHMC) in New Hampshire, the University of Iowa Hospitals and Clinics in Iowa, and the University of Massachusetts Memorial Medical Center in Massachusetts. The study took place over 12 consecutive months (March 2009 to February 2010) with approval obtained at each study site from the respective IRB for the protection of human subjects with a waiver for informed patient consent. Adult patients undergoing surgery requiring general anesthesia and IV catheter placement were considered eligible for enrollment. Absence of an IV catheter and/or surgery requiring only monitored anesthesia care, pediatric patients, and lack of scheduled sequential operative cases were the exclusion criteria.

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Primary aims:

To identify the reservoir of origin for between-case and within-case stopcock transmission events.

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Secondary aims.

To identify risk factors for stopcock contamination and to verify the prior association of stopcock contamination and increased postoperative infection and mortality.

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Microbiological analyses.

To determine the frequency with which provider hands serve as vectors for transmission between intraoperative bacterial reservoirs, to examine the efficacy of current environmental decontamination practices, and to determine the prevalence of bacterial pathogens within intraoperative bacterial reservoirs and the contribution of those pathogens to postoperative infection development.

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Observation.

The frequency of provider HDEs was also observed.

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Operating room selection.

A computer-generated list was used to randomly select operating rooms at each institution. The randomized unit study design was intended to include a wide variety of surgical procedures, patient comorbidities, infection control measures, and health care providers.

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General Protocol

The first 2 consecutive patients undergoing general anesthesia in each of 274 randomly selected operating rooms at 3 institutions were studied as a case pair to identify between-case and within-case bacterial stopcock transmission events. Previously sterile stopcock sets were cultured at case end for both case 1 and case 2 of each of 274 case pairs. Bacterial reservoirs including provider hands throughout patient care, patients, and the anesthesia machine adjustable pressure-limiting (APL) valve and vaporizer agent dial, proven representatives of the intraoperative patient environment,1214 were sampled in parallel throughout the process of intraoperative patient care for both operative cases. Reservoir isolates were then compared to stopcock bacterial isolates and the origin determined via standard microbiological techniques, biotype analysis, and temporal association (timing of transmission events linked to an appropriate reservoir exposure) using a previously validated protocol (see below).12,13 The sequence of sample acquisition events is detailed in Figure 1.

Figure 1
Figure 1
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In addition, the relative efficacy of routine and active environmental cleaning procedures was assessed, the contribution of baseline and case end environmental contamination to stopcock transmission was compared, and the frequency of anesthesia provider hand decontamination was observed. Patients were followed prospectively for 30 postoperative days to assess for HCAI development and/or all-cause mortality. Bacterial pathogens isolated from intraoperative bacterial reservoirs were compared via pulsed-field gel electrophoresis (PFGE) to causative organisms of infection.

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Reservoir and Stopcock Sampling

Reservoir and stopcock sampling procedures (see below) were standardized at all 3 study sites with quality assurance monitoring of sampling techniques performed on 2 separate occasions. Appendix A contains details of the sampling procedures in addition to those provided below.

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Hand sampling.

Using a previously validated, modified glove juice technique, provider hands were sampled before, during, and after patient care.13,15

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Patient sampling.

The patient's nasopharynx was sampled to assess the patient reservoir because nasopharyngeal pathogens have been strongly associated with postoperative surgical-site infections.16 The patient's axilla was also sampled because the axilla harbors up to 15%–30% of pathogens colonizing patient skin.17

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Environmental sampling.

Sampling of the anesthesia environment has been described previously.1214,18,19 Two sites on the anesthesia machine, the APL valve and the agent dial, are proven representatives of the anesthesia environment and have been associated with an increase in the probability of bacterial contamination of the IV stopcock set.12 These sites were sampled at baseline (after active decontamination at case start for case 1 and routine decontamination at case start for case 2) and at end of the case via a standardized method described in Appendix A. Active decontamination involved targeted cleaning of the study sites by the study investigators using a quaternary ammonium compound (Dimension III; Butcher's, Sturtevant, WI) strictly according to the manufacturer's protocol, while routine decontamination was performed by the usual operating room personnel according to their standard procedure applied to the environment between operative cases. Routine decontamination also involved use of the same quaternary ammonium compound, but personnel were not asked to specifically target the APL and agent dial.

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Sampling of peripheral IV tubing 3-way stopcocks.

The sampling technique for stopcock sampling at case end used in this study has been described previously.1214 Bacterial cultures obtained from stopcock sets immediately upon removal from the packaging (at case start) were shown to be invariably negative. A positive stopcock set at case end was defined as more than or equal to 1 colony forming unit per culture plate, consistent with prior study protocols.20,21

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Identification of Origin of Bacterial Stopcock Transmission Events

Any bacterial isolate from a patient IV stopcock set at case end was compared via standard microbiological techniques, biotype analysis, and temporal resolution to all bacterial isolates from the bacterial reservoirs that were monitored in parallel for that case pair throughout intraoperative patient care. Organisms were considered identical if they were of the same class of organism with an identical biotype and an appropriate temporal association of reservoir exposure and transmission. In this experimental model, transmission of potential pathogens is linked to a specific day, a specific operating room, and a specific surgical case. The timing of a transmission event in relationship to a reservoir exposure can be placed into the sequence as described in Figure 1.

Between-case bacterial transmission was assumed to have occurred if the organism isolated in the internal lumen of the case 2 patient's stopcock set was identical to an organism isolated from 1 or more of the bacterial reservoirs from case 1. Within-case transmission was assumed to have occurred if an organism isolated in a stopcock set was identical to an organism isolated from 1 of the bacterial reservoirs from the same case.

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Overall stopcock contamination.

This was defined by contaminated stopcocks with and without an identified reservoir of origin.

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Provider origin.

Provider origin of contamination was assumed if the stopcock isolate was identical to an isolate from the hands of 1 or more anesthesia providers sampled upon room entry (Fig. 1) before patient care.

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Environmental origin.

Environmental origin of contamination was assumed if the stopcock isolate was identical to an isolate from the environment sampled at baseline or at case end but not isolated either from the hands of providers or from the patient at case start. The hands of all providers who would potentially interact with the anesthesia environment were sampled at baseline (Fig. 1).

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Patient origin.

Patient origin of contamination was assumed if the stopcock isolate was identical to an isolate from the patient sampled at case start but was not isolated either from the hands of providers at case start (as patient samples were obtained after induction of anesthesia) or from baseline environmental samples (Fig. 1).

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Comparison of Residual Baseline Contamination with Case End Contamination: An Assessment of the Efficacy of Environmental Cleaning Practices

For each case pair, residual environmental isolates after active (case 1 start) and routine (case 2 start) decontamination at baseline, and case end environmental isolates after patient care, but before decontamination between cases for case 1 and case 2 were quantified according to colony-forming units (CFUs) per culture plate and identified as described below. The relative contribution of these environmental isolates to stopcock contamination was evaluated and the number of CFUs compared.

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Evaluation of Provider Hand Decontamination Frequency

Providers were directly observed regarding HDE throughout each case while within each respective operating room for each case pair. One HDE was defined as any use of a wall-mounted alcohol-based gel dispenser, a machine-mounted alcohol-based foam dispenser, or a 70% ethanol liquid dispenser located on the anesthesia carts. As described previously,14 all observations were recorded by the same research assistant(s) at each institution, and providers were unaware of observational criteria and indications. Providers were aware of the presence of the trained observer. Interobserver variability was minimized by prior training, quality assurance checks, and the simplistic nature of the required observations. We also assessed hourly frequency of glove use and the rate of hand decontamination after glove removal by the provider at each site.

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Analysis of Postoperative Infections and Mortality

During the entire 30-day postoperative period, patients and/or patient charts were initially screened daily for the presence or absence of increased white blood cells, fever, anti-infective order, office visit documenting signs of infection, and/or the acquisition of bacterial cultures. The charts of patients positive for 1 or more of these initial criteria then underwent an extensive review by the principal investigator at each institution to determine whether the patient met criteria for the diagnosis of an HCAI according to National Healthcare Safety Network definitions.22 PFGE was used to examine whether pathogens isolated from intraoperative bacterial reservoirs were the original source of 30-day postoperative infections. PFGE studies were performed by Mayo Medical Laboratories using standard methodology.23

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Demographic Data

Basic patient, procedural, and provider demographic information collected included the hospital site, age, sex, case 1 or case 2, ASA physical status classification, Study on the Efficacy of Nosocomial Infection control (SENIC)24 score (an index predicting the probability of postoperative HCAI development for a given patient), case duration, patient comorbidities (Appendix B), patient origin, patient discharge location, and procedure type. Case duration of more than 2 hours was assessed given the prior association with increased risk of postoperative HCAIs.24

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Microbiological Methodology

All microbiological processing was done at DHMC with DHMC samples placed under similar environmental conditions (ambient temperature) during the 12-hour period required for shipping of those samples obtained from the University of Iowa and University of Massachusetts on each respective day. The sample incubation period began when all samples for a given study day were present at the DHMC microbiological laboratory. The methods used for bacterial identification, including gram stain, simple rapid tests, the commercially available bioMerieux API identification system (Marcy l'Etoile, France), and PFGE23 are described in Appendix A.

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Monitoring of Institutional Intraoperative Infection Control Policies

Intraoperative infection control policies at each institution were tracked and recorded during the study period. There were no changes in standardized environmental cleaning procedures across institutions during the observational period. For routine cleaning between cases, site 1 utilized surface disinfection wipes in addition to the standard quaternary ammonium compound utilized at sites 0 and 2. All providers had access to wall-mounted, 62% alcohol dispensers and to 70% alcohol dispensers located on the anesthesia carts. At site 1, a machine-mounted, foam-based alcohol dispenser was also available. Gloves were immediately available for use throughout patient care episodes at each institution. Use of preoperative chlorhexidine baths and/or nasal mupirocin by patients was infrequent across all 3 sites.

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Outcomes and Statistical Analysis

The primary outcomes of this study were the incidence and origin of intraoperative bacterial stopcock transmission events between and within cases. The relative contributions of the patient, environmental, and provider hand bacterial reservoirs to stopcock transmission events were compared using the Fisher exact test. An α level of P < 0.05 was defined as statistically significant.

Secondary outcomes included an assessment of risk factors for stopcock contamination, 30-day postoperative HCAIs, hourly HDE, and mortality. Nonparsimonious multivariable logistic regression with adjustment for potentially confounding variables including site, age, sex, case, ASA physical status, SENIC, case duration, patient comorbidities, origin, discharge location, and the square root of hand-washing events was used for comparisons for stopcock contamination, postoperative HCAIs, and mortality. Predictors for HDE were assessed in a multivariable model including stopcock contamination, site, age, sex, ASA, SENIC, case duration, comorbidities, origin, discharge location, and procedure. HDE was analyzed on the square root scale to achieve normality, and for consistency, this transformation was used as a covariate for models predicting stopcock contamination. Provider identity was not included in the final models because no single provider accounted for >10% of total cases. We assessed and excluded all 1-way interactions (P > 0.05), but did not evaluate all possible 2-way interactions owing to the limitations in sample size. We addressed multiple comparisons by defining P values <0.017 as statistically significant.

Additional microbiological (qualitative) analyses included an assessment of the frequency with which provider hands served as vectors for transmission between intraoperative bacterial reservoirs, an examination of the relative efficacy of current environmental decontamination practices, and an assessment of the relative prevalence of bacterial pathogens within intraoperative bacterial reservoirs and the contribution of those pathogens to 30-day postoperative HCAIs. The frequency of provider HDEs was also observed. Environmental contamination was considered continuous, with baseline and case-end CFUs compared via the Student t test. An α level of P < 0.05 was defined as statistically significant.

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Power Analysis

This study was powered to detect a rate of between-case stopcock bacterial transmission events of 5% with an alternative rate of 1%. Because prior work has demonstrated that between-case stopcock transmission events occur less frequently than within-case stopcock transmission events,13 we powered the study to assess between-case stopcock transmission to ensure that the sample size would be sufficient to examine both modes of transmission.13 We chose to design the study to detect a 5% rate of between-cases transmission with an alternative rate of 1% because we hypothesized that while between-case transmission may be as high as 5%, even a 1% rate would be clinically relevant. Given these criteria, approximately 400 patients (200 pairs) were needed for the study to be powered at 0.9 with a type 1 error rate of 0.05. We expected to enroll 100 pairs at each institution to account for anticipated missing data of up to 30% (broken plates, lost samples, etc).

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RESULTS

A total of 274 operating room case pairs (548 cases) were included in the final analysis with 99 case pairs at site 0, 72 case pairs at site 1, and 103 case pairs at site 2. The overall rate of missing data for the study period was 9%, including 1 incomplete case pair at site 0 (2 cases) and 28 missing case pairs (56 cases) at site 1 (due to early termination with transition to a closed catheter system). The study results reflect a variety of patients, providers, and surgical procedures consistent with the usual practice of surgery with general anesthesia (Table 1).

Table 1
Table 1
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Primary Outcomes

Overall stopcock contamination was detected in 23% (126 out of 548 total cases) of cases. There were 14 between-case and 30 within-case stopcock transmission events confirmed. All 3 reservoirs were shown by microbiological analysis to contribute to between-case (64% environment, 14% patient, and 21% baseline providers; Table 2) and within-case (47% environment, 23% patient, and 30% baseline providers; Table 3) transmission events. The environment was a more likely source of stopcock contamination than provider hands (relative risk [RR] 1.91, confidence interval [CI] 1.09 to 3.35, P = 0.029) or patients (RR 2.56, CI 1.34 to 4.89, P = 0.002).

Table 2
Table 2
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Table 3
Table 3
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Secondary Outcomes

Site 0 and the second operative case (case) were significant predictors for overall stopcock contamination (Table 4). HDE either on the transformed or raw scale did not change the results. A reduced risk of stopcock contamination was associated with increased HDE (OR 0.66, CI 0.49 to 0.88, P = 0.005).

Table 4
Table 4
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Over the 30-day postoperative period, 48 total infections occurred in 44 patients (8%) including 46% (22 of 48) urinary tract infections; 40% (19 of 48) surgical site infections; 8% (4 of 48) respiratory infections; and 6% (3 of 48) deep organ site infections. The overall HCAI, surgical site infection, and mortality rates were 8%, 3%, and 1.6%, respectively, and consistent with what is typically found in the United States.

ASA status, SENIC, and hospital site were independent predictors of increased risk of infection (Table 5). ASA status (odds ratio [OR] 74.1, CI 4.94 to 1112.2, P = 0.002) and positive stopcock sets (OR 58.5, CI 2.32 to 1477, P = 0.014) were independent predictors of increased patient mortality (Table 6).

Table 5
Table 5
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Table 6
Table 6
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Microbiological Analyses of Environmental Contamination, Vectors of Transmission, the Frequency of Reservoir Bacterial Pathogens, and the Contribution of Reservoir Pathogens to Postoperative Infections (Pulsed-Field Gel Electrophoresis)
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Environmental contamination.

The anesthesia work area, as represented by bacterial isolates obtained from the APL valve, became more contaminated at case end than baseline controls after active decontamination (mean increase of 33 CFUs, CI 7.5 to 58.4, P = 0.015). There was no apparent increase in bacterial contamination of the agent dial throughout patient care. There were 19 case-start environmental contributions to stopcock transmission events (9 after active decontamination, 10 after routine decontamination) and 26 case-end environmental contributions to stopcock transmission events.

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Vectors of transmission.

Provider hands were confirmed as vectors for transmission, between the contaminated environment and contaminated stopcock sets, in 27% (12 of 44) of between-case and within-case stopcock transmission events (Tables 2 and 3).

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Reservoir pathogens.

We examined 2170 environmental sites, 2640 health care provider hands, and 1087 patient samples. From these reservoirs, more 6000 potential and 2184 true bacterial pathogens were isolated. Table 7 describes the relative frequency of bacterial pathogens within each bacterial reservoir. In comparison with patients or provider hands during or after care, provider hands before care were more likely to serve as a reservoir for vancomycin-resistant Enterococcus, while hands before, during, and after patient care were more likely to harbor methicillin-sensitive Enterococcus and Gram-negative pathogens. Patients were the more likely reservoir for methicillin-resistant and methicillin-sensitive Staphylococcus aureus (Fig. 2).

Table 7
Table 7
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Figure 2
Figure 2
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Pulsed-field gel electrophoresis.

Postoperative bacterial culture identified the causative organism of infection in 45% (20 of 44) of patients with diagnosed HCAIs in the 30-day postoperative period. In 30% (6 of 20) of these patients, PFGE analysis confirmed that the causative organism was present in at least 1 major intraoperative bacterial reservoir. Overall, 13.6% (6 of 44) of patients were diagnosed with 30-day postoperative HCAIs caused by bacterial organisms present at the time of the operation. Five of these infections were patient-derived and involved 3 cases of Staphylococcus aureus infection (2 wound infections and 1 case of pneumonia), 1 Proteus mirabilis urinary tract infection, and 1 case of Serratia liquefaciens pneumonia. One case of Enterobacter aerogenes pneumonia was linked by PFGE to the hands of a provider before patient care.

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Observation of Provider HDEs and Glove Use

Anesthesia providers' hourly HDEs were observed over 1463 hours during the study period. The average number of HDEs for health care providers across all 3 sites was 0.39 ± 1.06. The site-specific average HDEs were as follows: site 0 (0.35 ± 1.01), site 1 (0.104 ± 0.36), and site 2 (0.63 ± 1.34). The site-specific hourly HDE median and range were as follows: site 0 (median 1, range 0 to 18), site 1(median 0, range 0 to 6), and site 2 (median 0, range 0 to 22).

A total of 1586 glove use events were observed during the study period with an average of 2.39 ± 1.60 events per case. In 40% (636 of 1586) of glove use events, provider hands were not washed after glove removal.

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DISCUSSION

We have previously reported the overall frequency and importance of intraoperative bacterial transmission events to patient IV stopcock sets.12 The current study extends these observations by determining the relative contributions of known intraoperative bacterial reservoirs to these transmission events and by providing new insight into the underlying mechanisms of intraoperative bacterial cross-contamination.

We observed an overall stopcock contamination rate of 23%, which is within the previously reported range.12,13 Consistent with prior work,13 the providers' hands in this study served as the source of transmission to less than half of the contaminated stopcock sets. Thus, these results do not suggest that anesthesia providers are the major reservoir for intraoperative bacterial transmission. Instead, we observed that the surrounding patient environment was a more likely source. Given the number of confirmed transmission events linked to environmental contamination, residual environmental contamination could have partially explained the increased risk of stopcock contamination associated with the second case of the day across institutions. Our results clearly demonstrate a need for improvement in both active and routine environmental cleaning strategies currently used in the operative environment.

The patient reservoir also contributed to stopcock contamination less frequently than the environment. However, stopcock transmission events from patients did involve major pathogens, some of which were transmitted from one patient to another during sequential operative cases. On the basis of these findings, further studies of preventive measures involving patient decolonization are warranted. This premise is supported by earlier work demonstrating HCAI reduction after patient decolonization in surgical and dialysis patients2528 and by work suggesting that patient bacterial flora is easily transferred to provider hands during the process of patient care.29,30

Our findings suggest that stopcock contamination occurs independently of factors associated with the severity of patient illness and/or procedural complexity. Stopcock contamination was associated with the second case of the day and hospital site. In a secondary analysis evaluating predictors for HDE, a reduced risk of stopcock contamination was also associated with increased HDE. These results are consistent with the large contribution of environmental contamination to stopcock transmission events, because the magnitude of environmental contamination is likely influenced by individual and/or institutional variation in aseptic practice, including hand hygiene compliance, environmental cleaning efficacy, and possibly patient decolonization procedures. In turn, these factors are likely influenced by the second case of the day and hospital site. Variation in these factors, including glove use, may in fact explain significant differences in stopcock contamination between hospital sites.

While anesthesia providers are not the major reservoir for intraoperative bacterial transmission to patient IV stopcock sets, multiple findings in this study strengthen the argument for the importance of hand hygiene throughout the patient care episode.8 We have provided direct microbiological evidence confirming that provider hands are vectors of transmission between bacterial reservoirs. As such, improved intraoperative hand hygiene compliance and environmental decontamination efforts may have an additive or synergistic relationship.31 In addition, we found that anesthesia provider hands are a major reservoir for enterococcal and Gram-negative organisms throughout a patient care episode, and we were able to confirm via PFGE analysis that provider hand contamination does contribute to subsequent postoperative infection development.

Consistent with prior reports,12 stopcock contamination was associated with an increase in mortality. This association should be interpreted with caution because it is a secondary outcome involving few events. However, bacterial contamination of intravascular devices has been shown to be associated with increased morbidity in other health care settings.3237

These study results confirm that the previously reported problems of stopcock contamination, suboptimal hand hygiene, and suboptimal environmental decontamination are not limited to a single institution.1214 Thus, there is a universal need for improvement in intraoperative infection control. This premise is further supported by the finding in this study that 13.6% (6 of 48) of 30-day postoperative HCAIs were linked by PFGE to intraoperative bacterial exposure.

After the evaluation of >6000 potential pathogen isolates, we found that staphylococcal pathogens largely reside with patients, while enterococcal and Gram-negative pathogens largely reside on provider hands before, during, and after patient care. PFGE results parallel this distribution with most patient-derived infections due to Staphylococcus aureus and the only confirmed provider-derived infection was due to Enterobacter aerogenes, a Gram-negative organism. Taken together, these results suggest that an optimal approach to improvement in intraoperative infection control would involve a multimodal program incorporating improved environmental decontamination and preventive measures targeting both patient decolonization and provider hand hygiene in parallel.

A limitation of this study is the insensitivity of the culture methods used; however, this in fact is likely to underestimate the true magnitude of the bacterial transmission problem.38 In addition, we used a previously validated method, the combination of temporal association and biotype analysis,13 as evidence for bacterial origin for stopcock contamination as opposed to molecular typing methods such as PFGE. Though PFGE has been shown to be more discriminating than biotype analysis alone,39,40 to our knowledge, the benefit of this technique has not been proven superior to the combination of biotype analysis and temporal resolution as used in this study. Finally, the source for the contaminated stopcocks without identification of a reservoir of origin remains unclear; however, patient and environmental reservoirs are more likely sources in comparison with anesthesia providers, because unlike provider hands, the number of sample sites was relatively limited.

In conclusion, the relative importance of patient, health care provider, and environmental reservoirs in bacterial cross-contamination has not been previously examined but is heavily debated.2528,4146 Using an intraoperative model of stopcock contamination,1214 we have shown that several bacterial reservoirs contribute to bacterial cross-contamination and, in fact, are intricately related. We have also shown that these reservoirs harbor unique subsets of major bacterial pathogens that can contribute to postoperative infection development. As such, the results of this study strongly suggest that the impact of a multimodal program targeting each step in the cross-contamination sequence and the primary reservoir for each class of major pathogen on subsequent postoperative HCAI development should be intensely studied to improve intraoperative patient safety.

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DISCLOSURES

Name: Randy W. Loftus, MD.

Contribution: This author helped design the study, conduct the study, analyze the data, and write the manuscript.

Attestation: Randy W. Loftus has seen the original study data, reviewed the analysis of the data, approved the final manuscript, and is the author responsible for archiving the study files.

Name: Jeremiah R. Brown, PhD, MS.

Contribution: This author helped analyze the data, write the statistical sections, and revised manuscript.

Attestation: Jeremiah R. Brown has approved the final manuscript.

Name: Matthew D. Koff, MD, MS.

Contribution: This author helped design the study, conduct the study, and write the manuscript.

Attestation: Matthew D. Koff has seen the original study data, reviewed the analysis of the data, approved the final manuscript, and is the author responsible for archiving the study files.

Name: Sundara Reddy, MD.

Contribution: This author helped design the study, conduct the study, and write the manuscript.

Attestation: Sundara Reddy has approved the final manuscript.

Name: Stephen O. Heard, MD.

Contribution: This author helped design the study, conduct the study, and write the manuscript.

Attestation: Stephen O. Heard has approved the final manuscript.

Name: Hetal M. Patel, BS, MLT.

Contribution: This author helped conduct the study.

Attestation: Hetal M. Patel has approved the final manuscript.

Name: Patrick G. Fernandez, MD.

Contribution: This author helped write the manuscript.

Attestation: Patrick G. Fernandez has approved the final manuscript.

Name: Michael L. Beach, MD.

Contribution: This author helped design the study, conduct the study, and analyze the data.

Attestation: Michael L. Beach has approved the final manuscript.

Name: Howard L. Corwin, MD.

Contribution: This author helped write the manuscript.

Attestation: Howard L. Corwin has approved the final manuscript.

Name: Jens T. Jensen, MS.

Contribution: This author helped conduct the study and analyze the data.

Attestation: Jens T. Jensen has approved the final manuscript.

Name: David Kispert, BA.

Contribution: This author helped conduct the study.

Attestation: David Kispert has approved the final manuscript.

Name: Bridget Huysman, BA.

Contribution: This author helped conduct the study.

Attestation: Bridget Huysman has approved the final manuscript.

Name: Thomas M. Dodds, MD.

Contribution: This author helped write the manuscript.

Attestation: Tom M. Dodds has approved the final manuscript.

Name: Kate L. Ruoff, PhD.

Contribution: This author helped design and conduct the study.

Attestation: Kate L. Ruoff has approved the final manuscript.

Name: Mark P. Yeager, MD.

Contribution: This author helped write the manuscript.

Attestation: Mark P. Yeager has approved the final manuscript.

This manuscript was handled by: Sorin J. Brull, MD, FCARCSI (Hon).

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ACKNOWLEDGMENTS

Dartmouth–Hitchcock Medical Center Study Coordinator: Tammara A. Wood, M.T. (A.M.T.), Department of Anesthesiology.

Dartmouth–Hitchcock Medical Center Study Consultant: Megan E. Read, M.T. (A.S.C.P.), Department of Pathology.

Dartmouth–Hitchcock Medical Center Research Assistant: Rachel Barr, Department of Anesthesiology.

University of Iowa Study Coordinators: Andy Fahlgren, Medical Student, Department of Anesthesiology; Julie Weeks, Research Assistant, Department of Anesthesiology; Molly Sabers, Medical Student, Department of Anesthesiology; Donald Anciaux, Research Assistant, Department of Anesthesiology.

Michael Todd, University of Iowa, Professor of Anesthesiology.

University of Massachusetts Medical School Study Coordinators: Karen J. Longtine, RN, Department of Anesthesiology; Melissa A. O'Neill, RN, Department of Anesthesiology; Jaclyn K. Longtine, BS, Department of Anesthesiology.

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Sampling of the Anesthesia Environment

Sampling of the anesthesia environment has been described previously.1214 Following decontamination of the adjustable pressure-limiting valve complex and agent dial with Dimension III disinfectant solution according to manufacturer's recommendations, baseline cultures were obtained by utilizing sterile polyester fiber-tipped applicator swabs moistened with sterile transport medium (EsSwab, Copan Diagnostic Inc., Corona, CA) to roll several times over the selected areas followed by culturing on sheep blood agar plates with a zigzag pattern and swab rotation to detect both Gram-positive and Gram-negative bacteria. Environmental cultures were obtained once again following completion of each case in the study unit but prior to disinfection according to current protocol. Environmental isolates obtained from case start were considered to represent a baseline, such that any new pathogen cultured from the environment at the end of surgery was presumed to be acquired in the operating room during the process of patient care. Organisms found in the environment at case end but not on patients or on the hands of providers at case start were presumed to have been transmitted to the measured environmental sites from other environmental reservoirs within the surrounding patient environment. Environmental isolates were quantified as colony-forming units (CFUs) per culture plate.

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Sampling of Anesthesia Provider Hands

Using a previously validated glove juice technique, provider hands were sampled before, during, and after patient care for each provider caring for the patient in each operating room. Operating suites were randomized to either dominant or nondominant hand sampling. In addition, provider hands were sampled upon entry to the operating room following every departure. The procedure for hand sampling has been described previously.13,15 Participants submerged their dominant hand for 60 seconds into a sterile polyethylene bag of modified glove juice formula containing 50 mL of sampling solution (pH 7.9, containing 3.0 g/L NaCl, 0.1 g/L CaCl, 0.2 g/L KCl, 0.1 g/L MgCl2, 0.2 g/L KH2orally4, 1.15 g/L K2HPO4). This solution was intended to neutralize residual antiseptic on the skin and facilitate identification and quantification of microorganisms by dispersing the colonies into single cells, which were then counted as CFUs. The sterility of glove juice solution was evaluated and confirmed at regular intervals.

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Sampling of the Patient Nasopharynx and Axilla

Immediately following induction of general anesthesia, the nasopharynx and axilla of each patient were cultured.

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Nasopharynx.

A sterile nasopharyngeal swab moistened with sterile transport medium was inserted gently into the internal surface of each nasopharynx bilaterally and rotated 360° 10 times to obtain a culture. Each swab was inoculated onto a sheep's blood agar plate using a zigzag pattern and swab rotation.

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Axilla.

A sterile nasopharyngeal swab moistened with sterile transport medium was inserted gently into the axilla bilaterally and rotated 360° 10 times to obtain a culture. Each swab was inoculated onto a sheep's blood agar plate using a zigzag pattern and swab rotation.

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Sampling of Peripheral IV tubing 3-way stopcocks

The sampling technique for stopcock sampling at case end used in this study has been described previously.1214 A sterile nasopharyngeal swab (ESwab) moistened with sterile transport medium was inserted into the internal surfaces of each injection port of the 3-way stopcocks and rotated 360° 10 times to culture. Each bacterial swab of the injection port lumen was inoculated on a sheep blood agar plate using a zigzag pattern and swab rotation. Bacterial cultures obtained from stopcock sets immediately upon removal from the packaging (at case start) were shown to be invariably negative. A positive stopcock set was defined as greater than or equal to 1 colony per surface area sampled, consistent with prior study protocols.21,22

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Microbial Culture Conditions

All culturing was done in the same laboratory at Dartmouth–Hitchcock Medical Center. Samples shipped from the University of Iowa and University of Massachusetts were placed under similar environmental conditions (ambient temperature) during the 12 hours required for shipping. Samples collected on the same day at Dartmouth–Hitchcock Medical Center did not require shipping but were kept at ambient temperature to mimic the environment of those samples being shipped. No samples for a given study day were incubated until all samples for that day from all research sites were present at Dartmouth–Hitchcock Medical Center.

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Bacterial Identification

Bacterial isolates obtained from the anesthesia environment, IV stopcock sets, provider hands before, during, and after patient care, and patients were initially identified by colony morphology, Gram stain, and simple rapid tests. Bacterial organisms were then identified and isotypes specified using the commercially available bioMerieux API identification system (Marcy l'Etoile, France). The API (analytical profile index) system is a standardized protocol for identification of Gram-negative (nonfastidious, nonenteric as well as enteric), Gram-positive (staphylococcus and streptococcus) and coryneform bacteria. Using this system, we identified organisms on the basis of modified conventional and chromogenic tests utilizing pH changes, substrate utilization, and growth in the presence of antimicrobial agents under specified incubation conditions. Interpretation of the samples following incubation resulted in a 7- to 9-digit identification number; this number was then cross-referenced using the API database to obtain the final organism biotype. Pulsed-field gel electrophoresis was used to compare reservoir isolates to causative organisms of 30-day postoperative infections. 23Methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant Enterococcus (VRE) were confirmed by agar dilution minimal inhibitory concentration.

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APPENDIX B: LIST OF COMORBIDITIES ASSESSED AS PART OF PATIENT DEMOGRAPHICS

1. Cardiovascular: history of hypertension, coronary artery disease (ASCVD, coronary artery bypass graft, angina), major vascular disease (aortoocclusive disease, abdominal aortic aneurysm [AAA], peripheral vascular disease [PVD], carotid stenosis, carotid endarterectomy, major vascular surgery, or transplant).

2. Neurological: history of cerebral aneurysm, stroke (CVA), and/or brain tumor.

3. Pulmonary: history of chronic obstructive pulmonary disease (COPD), congestive heart failure, severe asthma (on chronic steroid treatment: daily steroids such as prednisone), recurrent pneumonias, cystic fibrosis [CF], pulmonary fibrosis, transplant, cancer (bronchogenic carcinoma–squamous cell, small cell, mesothelioma, etc.).

4. Renal: history of renal failure or insufficiency, transplant, dialysis, and/or renal cell carcinoma.

5. Endocrine: diabetes type I or II, adrenal insufficiency on steroid replacement, and/or history of multiple endocrine neoplasia (MEN).

6. Infectious disease: history of suppressed immune system (on steroids, history of splenectomy, and/or malignancy). Active respiratory, wound, or blood stream infections.

7. Hematological: history of acute or chronic myelogenous leukemia, acute or chronic lymphocytic leukemia, multiple myeloma, polycythemia vera, and/or essential thrombophilia. A history of anemia requiring transfusions.

8. Rheumatological: history of rheumatoid arthritis, sarcoidosis, Sjogren's syndrome, systemic lupus erythematous (SLE), vasculitis (Wegener's granulomatosis, Good Pasteur's syndrome, polyarteritis nodosa, dermatomyositis, and seronegative spondyloarthropathy).

9. Other: history of lung, breast, renal cell, urinary tract, uterine, or extensive skin carcinoma requiring radiation and/or chemotherapy.

10. Gastrointestinal: history of bowel, liver, or gastric malignancy, pancreatitis, ulcerative colitis, Crohn's disease, and other inflammatory bowel disease.

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