Advances in the Prevention and Control of HAIs

Victoria Parker, Caroline Logan, Brian Currie

Abstract

This paper presents data from an assessment of intensive care unit (ICU) staff-perceived barriers to implementation of an enhanced carbapenem-resistant Enterobacteriaceae (CRE) control intervention across all ICUs in three hospitals in a New York City academic inpatient health care network. The enhanced CRE control measure included the initiation of an active CRE surveillance program in all ICU units, with all CRE-positive patients being placed in contact isolation. Active surveillance had not been previously used as an infection control strategy at any hospital or ICU in the health care network. This study was designed to assess ICU staff knowledge of CRE and perceived barriers to implementing the enhanced CRE control intervention. Data collection included pre- and post-intervention interviews of stratified samples of ICU staff (n=30 and n=34, respectively) and a post-intervention online survey offered to all ICU staff (n=205; 19.5 percent response rate). Interviews and surveys included samples of nursing, physician, and physician assistant ICU staff. Responses were used to identify consensus themes in staff perceptions and indicated that awareness of the Klebsiella pneumoniae carbapenemase (KPC) variant of CRE as an emerging nosocomial threat was low across all occupational groups at baseline. Staff identified sustained education on the scope of the issue and evidence for interventions as key facilitators in the implementation of new processes. Post-intervention, staff were much more knowledgeable, and they identified the need to also involve ancillary staff and patient family members in educational activities around the new interventions. Results are presented in the context of existing literature to provide insight and guidance to designing and successfully implementing future CRE control interventions.

Introduction

Carbapenem-resistant Enterobacteriaceae (CRE) infections have rapidly emerged as a global public health issue. In the United States, the presence of CRE is almost exclusively the result of the emergence and rapid dissemination of the KPC (Klebsiella pneumoniae carbapenemase) variant of CRE.^1,2 KPC was first reported in North Carolina in 2001 and, by 2006, had been responsible for a number of well-documented hospital-based outbreaks in the New York City area.^3–7 Over the next 6 years, KPC was noted to have become endemic in New York City hospitals and had rapidly disseminated, both on a national and global basis.^2,8 By 2012, KPC was reported from 42 States; internationally, it was reported from every continent.^2,9 Infections caused by KPC-producing bacteria have resulted in substantial morbidity and mortality because of limited treatment options, and they present significant therapeutic and infection control challenges in health care settings.²

Prevention of nosocomial transmission of KPC has surfaced as an emerging priority. A demonstration project funded by the Agency for Healthcare Quality and Research (AHRQ) was initiated in 2009 at Montefiore Medical Center, in the Bronx, New York, that was designed to assess the impact of implementing Centers for Disease Control and Prevention (CDC) recommendations for enhanced infection control interventions to prevent the transmission of KPC among intensive care unit (ICU) patients. The CDC recommendations were developed in 2006 and updated in 2009.^1,0 The interventions included the use of a rapid molecular test (a polymerase chain reaction [PCR] assay) to drive an active surveillance program to detect KPC-colonized patients, coupled with the rapid institution of contact isolation precautions for all KPC-positive patients. The design and rollout of the intervention included a multidisciplinary planning and implementation team and a focused KPC staff educational program. A pre-post study design was used to evaluate the impact of the intervention, with baseline data collected over a 4-month period and compared to data from a 4-month post-intervention period. The intent was to create a successful, replicable intervention that could be exported to other institutions through the use of a toolkit.

The study design included provisions to assess ICU staff knowledge and understanding of KPC and the need for KPC control interventions, knowledge and acceptance of routine infection prevention practices, and perceived barriers to implementing enhanced KPC screening and control measures. Additionally, the study determined how the intervention rollout and education efforts influenced the adoption of the new KPC intervention. The study was initiated to provide insight and guidance to designing a successful intervention, including identification of potential barriers to implementation that may not have been previously anticipated and addressed in the project planning process. Study results are presented and discussed here.

Methods

This study was conducted in eight ICUs located in three hospitals in Montefiore Medical Center (MMC), an academic tertiary care hospital network located in the Bronx, New York. The intervention investigations were approved by the MMC Institutional Review Board (IRB), and the activities described in this paper were approved by both the MMC and Boston University School of Public Health (BUSPH) IRBs.

Sample

Stratified staff samples, including key leaders, were chosen from among physician, nursing, and physician assistant staff in all ICU settings for both before and after interviews (n=30 and n=34, respectively), and an electronic survey was sent to all nursing staff, physicians, and physician assistants (n=205) employed in all MMC ICUs during the post-intervention period.

Intervention

After baseline prevalence data had been collected by MMC research staff, the intervention was rolled out during an approximately 1-month period prior to beginning the collection of post-intervention KPC prevalence data. During the intervention phase, ICU nursing staff were trained to take weekly peri-rectal swabs from all patients and from any new admission at the time of arrival into the ICU. Research staff picked up all swab samples daily at 9:00 a.m. Samples were then analyzed, and any positive results were reported to the nurse managers in each ICU by 12:30 p.m. Contact isolation precaution orders were immediately entered into the electronic medical record and implemented.

The intervention rollout was initiated with an extensive educational program that included group meetings with the staff of each ICU. All sessions were timed in the morning to simultaneously capture day and evening staff, and a video presentation was created for off-hour staff who could not be present. Sessions (including the video) were presented by the medical center epidemiologist. They were approximately 50 minutes in duration and included opportunities for open-ended questions and comments. Video participants were encouraged to submit questions and comments via email to the medical center epidemiologist, who responded via email to each participant. Attendance at presentations was mandatory, and compliance was tracked with sign-in sheets.

The educational sessions included a basic overview of the epidemiology and clinical significance of KPC. The importance of asymptomatic colonized patients as a driving force for KPC dissemination was stressed and used as the rationale for initiating an intervention that included an active KPC surveillance program coupled with contact isolation of all KPC-positive patients. Baseline data were used to underscore the fact that the ICUs already had significant KPC prevalence. The intervention was described in its entirety, and the role of each ICU occupational group in the intervention was introduced and discussed. The importance of sampling all patients was stressed. Existing hand hygiene and contact isolation protocols were reviewed, including the need for high levels of adherence by all staff and visitors. The medical center epidemiologist provided contact information for any future questions or for reporting identified problems with the initiative. Placards and signage were provided that presented the intervention workflow and sampling method for future review.

MMC research staff reviewed, on a daily basis, progress toward effective intervention implementation and coached staff to help them successfully achieve each step of the workflow process. This process was particularly helpful in assisting nursing staff to incorporate patient sampling into routine workflow patterns, resulting in complete and timely sampling of all patients. Daily reviews also provided an ongoing opportunity to reinforce KPC awareness and key educational issues, answer staff questions, and identify potential unanticipated problems. After 2 weeks, the intervention process was effectively functional; however daily coaching visits by research staff were continued for an additional 2 weeks to support future intervention sustainability.

Data Collection

Staff were interviewed approximately 11 months before (n=30) and 6 weeks after (n=34) the new KPC screening and precaution guidelines were implemented in all ICUs. A semi-structured interview guide was used that focused on the importance of infection control in the ICU, challenges to it, awareness of KPC, and concerns about caring for patients on contact precautions. A research assistant took detailed interview notes. All interviewees completed a written informed consent form prior to participating in an interview. All interviews were voluntary and were conducted by BUSPH research staff. Participants were promised anonymity and that only aggregate data would be shared with MMC leadership. Baseline interviewees included 14 physicians, 7 nurses, and 9 physician assistants. Post-intervention interviewees included 18 physicians, 10 nurses, and 6 physician assistants.

In addition, a post-intervention survey was sent via email to all 205 physicians, nurses, physician assistants and fellows-in-training employed in the eight ICUs throughout the medical center. The emails contained an anonymous link to a secure online survey (using SurveyMonkey®). The survey was modified from a survey developed at the Columbia School of Nursing to assess nurse adherence to hand hygiene guidance.¹¹ This survey model was chosen because it had been demonstrated to have acceptable levels of test-retest reliability (0.86) and stability (Cronbach's alpha of 0.80).¹¹ Potential survey participants were informed that only aggregate data would be shared with MMC leadership. Reminder emails were sent on a weekly basis for 5 weeks, after which the survey was closed to participation.

The survey consisted of 32 questions in five sections and employed 5-point Likert response scales. Sections 1, 2, and 3 contained general statements about the care provided at the respondent's facility, specific unit, and care team, respectively. The last two parts contained specific statements related to the staff's KPC knowledge base and to the implemented KPC prevention and control guidelines. A total of 40 responses were received before the survey closed, for an overall response rate of 19.5 percent. Respondents included 32 nurses, 5 physicians, and 3 physician assistants.

Analysis

The interview notes were independently and systematically reviewed by the research assistant and by one of the principal investigators to identify recurring themes in staff perceptions. Each researcher generated a list of themes that were then compared and combined to generate a consensus list of themes. 12 Survey data were analyzed by combining the "strongly" and "somewhat" responses for each item, resulting in three response categories for each item (agree, neutral, disagree), and frequencies for each were computed. Due to the small size of the occupational groups, no meaningful subanalyses were possible.

Results

Pre-Intervention Interviews

During the pre-intervention interviews, staff identified a number of factors that they considered important facilitators of infection control activities at MMC including:

• Clear interest in activities from top leaders.
• Regular data collection and feedback to staff.
• Development of a "speak up culture" to intercept potential breaches in practice.
• Accountability for those not following current protocols.
• Conveniently placed and consistently available supplies and personal protective equipment.
• Past success with ICU-based multidisciplinary approaches to reduce nosocomial infections (such as implementation of a central line bundled approach to reducing central line–associated bloodstream infections).

They also identified a number of existing problems that they considered barriers to infection control practice, which largely focused on the initiation of contact isolation. These observations included:

• Feeling a need to "do it all" to avoid multiple encounters with patients in contact isolation, resulting in the possibility that patients on contact precaution might get less attention.
• Challenge of educating family members and ancillary staff about contact isolation precautions.
• Difficulty of transferring ICU patients on contact isolation to the next level of care because of the limited number of single-patient rooms.

Awareness of KPC as an emerging nosocomial problem was uniformly low at baseline/pre-intervention across all categories of ICU occupational groups interviewed. While a few were aware of KPC, most were unaware of its dramatic emergence, the clinical implications of KPC infection, or the existence of new guidelines to prevent horizontal transmission of KPC among patients. Interviewees emphasized the importance of providing staff with a clear rationale and evidence for any new procedures to be implemented, offering repeated educational opportunities, having educational materials available for reference at all times, and providing feedback about the results of new efforts as part of existing data reporting processes on "zero target" infection prevention.

Post-Intervention Interviews

During the post-intervention interviews, staff again described their perceptions of implementation facilitators and barriers. Regarding facilitators, interviewees identified a number of thematic elements that had previously surfaced during the pre-intervention interviews. These elements now focused on factors that would enhance compliance with contact isolation precautions for patients who had screened positive for KPC:

• A "speak up culture" that empowered all members of the team to remind others to comply with contact isolation protocols.
• Easy access to personal protective equipment required for contact isolation.
• Consistent unit staffing with individuals familiar with contact isolation protocols.
• Use of dedicated equipment in isolation rooms, including blood pressure cuffs, stethoscopes, etc.

Factors identified as potential barriers to implementation included:

• Presence of non-ICU ancillary staff who would be less aware of the intervention guidelines.
• Presence of patients' family members who would not be familiar with contact isolation protocols.
• Concern with "alert fatigue" with respect to contact isolation signage outside rooms.
• A sense of fatalism about not being able to prevent all patient-to-patient transmission of KPC.

A prominent theme that surfaced was the perception that communication and education would be very important to successful implementation of the KPC intervention. This element of concern extended beyond the ICU staff and encompassed the need to educate ancillary staff who would be entering the ICUs and patients' family members about the seriousness of KPC infections in order to elicit interest and motivation. All interviewees, across all occupational groups, now exhibited a high degree of awareness regarding KPC, including the clinical and infection control implications of KPC infection and colonization. Staff identified the need for comprehensive in-service education, use of visual reminders, and on-site support as important components of a communication strategy for successful implementation of the KPC intervention. Nursing staff identified the collection of peri-rectal swab samples as a sensitive issue and believed that collaboration with nursing staff to ascertain the best way to integrate the sampling process into clinical workflow (both on admission and for weekly surveillance purposes) would be an important determinant of successful implementation of the KPC intervention.

Survey Data

A total of 40 individuals responded to the survey before it closed, for an overall response rate of 19.5 percent. Responses to Parts 1 and 2, which pertained to the care provided at the respondent's facility, suggest that, overall, respondents thought that their facility was committed to high quality patient care and infection control. Key findings are presented in Table 1. Part 3 of the survey addressed the respondent's care team and how the team members do their work. In general, respondents agreed with statements suggesting that care teams work systematically to improve processes of care, but findings from this section also suggest there may be opportunities for the organization to better support this kind of work. Key findings from this section are also presented in Table 1.

The final two parts of the survey, Parts 4 and 5, pertain to respondents' specific knowledge about KPC and the implementation of the new KPC clinical guidelines. Responses indicated that the implementation team was able to successfully educate staff about KPC and develop guidelines that integrated well into existing workflows; however, the findings also provided suggestions for areas of improvement, specifically in ensuring that non-ICU ancillary staff fully understand the guidelines and the rationale for new screening and patient handling processes.

Discussion

Many of the facilitating factors and perceived barriers to implementation of enhanced KPC infection control interventions that ICU staff identified in this study have been previously described in the infection control literature. These factors and barriers relate to the impact of active surveillance and contact precautions on (1) hospital contact isolation capacity and potential "throughput" problems in transferring colonized patients to other clinical units within hospitals, (2) concerns regarding staff and family adherence to contact isolation precautions, and (3) a potential reduction in health care worker–patient contacts, interrupted workflow patterns, and the potential for a negative impact on patient care.^13-17

Table 1. Post-intervention survey: staff perceptions

Note: C. difficile = Clostridium difficile; KPC = carbapenemase-producing Klebsiella pneumoniae; MRSA = methicillin-resistant Staphylococcus aureus.
 

Given that patients for whom contact isolation precautions are implemented should be placed in single-patient rooms, it is important for each facility to assess the capacity to absorb an increased volume of isolated patients. If availability of single-patient rooms is limited and bed occupancy rates are high, as is the case at MMC, policies should be developed to outline criteria for other placement options, such as cohorting.

Past experience at MMC had already identified delayed transfer of ICU patients resulting from a lack of single-room availability at the receiving clinical unit. Of note, infection control staff were already routinely monitoring transfer of ICU contact isolation patients on a 24/7 basis and were able to identify an appropriate single room for the transferred patient on every occasion. When this issue was raised during the intervention rollout, infection control staff reassured the ICU staff that monitoring would continue, and results would be shared with ICU staff on a regular basis. In fact, the demand for single rooms was lower than anticipated because 16 percent of KPC-colonized ICU patients were already on contact isolation for a different multiple drug-resistant organism and because there was a significant reduction in the prevalence of KPC colonization of ICU patients post-intervention (7.4 percent vs. 3.5 percent, p<0.001).

ICU staff concerns were well placed regarding staff and family adherence to hand hygiene and contact isolation precautions; published observational studies have identified compliance rates of less than 30 percent.¹⁵ Ongoing campaigns at MMC had targeted compliance with both hand hygiene and contact isolation precautions over a 6-year period prior to this study, and these are continuing. Compliance rates were documented via surreptitious direct observation using a standardized tool on all clinical units at irregular intervals, with feedback to clinical staff. Observed rates of compliance in the ICUs during this study consistently ranged from 85 percent to 93 percent.

In spite of documented high rates of adherence, training sessions during the intervention rollout were used to review medical center protocols for hand hygiene and contact isolation and to remind staff about their accountability for their own compliance and for helping to ensure adherence by other staff and patient families. Staff concerns regarding non-ICU ancillary staff adherence to protocols resulted in the extension of group training sessions to respiratory therapy staff and to house staff at the beginning of their ICU rotations.

ICU staff concerns about the negative impact that contact isolation might have on patient care also have been previously documented in the literature. Published reports and small studies have suggested that both ICU and non-ICU patients on contact isolation have fewer health care visits, less patient contact time, half as many attending physician examinations on rounds, increased frequency of depression and anxiety, and decreased satisfaction; they also suffer increased adverse events and experience poorer outcomes relative to control patients not on contact isolation.^13,14,17 However, these studies have had many design issues and invariably have been based on small sample sizes. A more recent report that included large sample sizes from four hospitals confirmed fewer visits and shorter visits for patients on contact isolation, except in ICU units, where the duration of health care worker contact did not vary between contact isolation and non-contact isolation patients in all four study hospitals.¹⁶ This observation was believed to possibly be related to the use of single-patient rooms for all ICU patients; higher proportions of patients on contact isolation precautions in the ICU; the higher acuity of care in the ICU; and the higher nurse-to-patient ratio in ICUs, resulting in the need for less changing of gowns and gloves.¹⁶ Given the uncertainty in the literature and the uncertain clinical significance of observed changes in health care worker interactions with contact isolation patients, it is probably best to sensitize all ICU occupation groups to remain alert for the possibility of potential disparities in the care provided to these patients.

Although the spread of KPC and the need for new approaches to screening and prevention of horizontal transmission in health care settings have been well recognized in the infectious disease and infection control communities, the baseline findings from this study suggest that KPC awareness among intensive care clinicians was much less prevalent. This finding was concerning, given that the KPC epidemic in New York City was more than 10 years old, and that ICU patients carry a high risk for KPC infection. It also underscored the need for repeated, multi-model, continuous education activities to be integrated into the KPC intervention rollout process. Clinicians who had been exposed to such education understood the reason for the new processes and reported commitment to carrying them out. Respondents who had missed some of the education sessions were less clear on the need for the intervention. Our findings also underscore the need for the implementation process to include clinical staff in problem-solving about how to incorporate new screening steps and infection prevention activities into existing workflows.

Acknowledgments

This project was funded under contract number HSSA290200600012i (TO #9) from the Agency for Healthcare Research and Quality (AHRQ), U.S. Department of Health and Human Services. The findings and conclusions in this document are those of the authors, who are responsible for its content, and do not necessarily represent the views of AHRQ. No statement in this report should be construed as an official position of AHRQ or of the U.S. Department of Health and Human Services.

We thank Dr. Arjun Srinivasan and Dr. Kendall Hall for their advice and guidance.
 

Authors' Affiliations

Boston University School of Public Health, Boston, MA (VP, CL). Albert Einstein College of Medicine and Montefiore Medical Center, Bronx, NY (BC).

Address correspondence to: Brian Currie, M.D., MPH, Montefiore Medical Center, 111 East 210th Street, Bronx, NY 10467; Email: bcurrie@montefiore.org.

References

1. Centers for Disease Control and Prevention. Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities. MMWR Morb Mortal Wkly Rep 2009 March 20;58(10):256-60. PMID: 19300408.

2. Currie B. The emergence of carbapenemase-producing Enterobacteriaceae. Inf Dis sp. ed. 2012;15:9-13.

3. Yigit H, Queenan AM, Anderson GJ, et al.. Novel carbapenem-hydrolyzing β-latamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother 2001 Apr;45(4):1151-61. PMID: 11257029.

4. Bratu S, Mooty M, Nichani S, et al. Emergence of KPC-possessing Klebsiella pneumoniae in Brooklyn, New York: epidemiology and recommendations for detection. Antimicrob Agents Chemother 2005 Jul;49(7):3018-20. PMID: 15980389.

5. Endimiani A, Hujer AM, Perez F, et al. Characterization of blaKPC-containing Klebsiella pneumoniae isolates detected in different institutions in the Eastern USA. J Antimicrob Chemother 2009 Mar;63(3):427-37. PMID: 19155227.

6. Won S, Munoz L, Lolans K, et al.; Centers for Disease Control and Prevention Epicenter Program. Emergence and rapid regional spread of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin Infect Dis 2011;53(6):532-540.

7. Simkins J, Pokharel R, Dogra S, et al. Prevalence of carbapenemase producing Klebsiella pneumoniae colonization at an academic medical center in New York City. Presented at 49th Annual Meeting of the Infectious Diseases Society of America; 2011 Oct 20-23; Boston, MA.

8. Nordmann P, Naas T, Poirel, L. Global spread of carbapenamase-producing Enterobacteriaceae. Emerg Infect Dis 2011 Oct;17(10):1791-8. PMID: 22000347.

9. Centers for Disease Control and Prevention. Vital signs: carbapenem-resistant Enterobacteriaceae. MMWR Morb Mortal Wkly Rep 2013 Mar 8;62(9):165-70. PMID: 23466435.

10. Siegel, JD, Rhinehart E, Jackson M; Healthcare Infection Control Practices Advisory Committee. Management of multidrug-resistant organisms in health care settings, 2006. Atlanta, GA: Centers for Disease Control and Prevention; 2007. Available at www.cdc.gov/hicpac/pdf/MDRO/MDROGuideline2006.pdf (PDF File,  234 KB).

11. Larson E. A tool to assess barriers to adherence to hand hygiene guidelines. Amer. J Infect Control 2004 Feb;32(1):48-51. PMID: 14755236.

12. Miles MB, Huberman AM. Qualitative Data Analysis: An Expanded Sourcebook. Thousand Oaks, CA: Sage Press; 1994.

13. Santos RP, Mayo TW, Siegel JD. Healthcare epidemiology: active surveillance cultures and contact precautions for control of multidrug-resistant organisms: ethical considerations. Clin Infect Dis 2008 Jul;47(1):110-16. PMID: 18491966.

14. Diekema DJ, Edmond MB. Look before you leap: active surveillance for multidrug-resistant organisms. Clin Infect Dis 2007 Apr;44(8):1101-7. PMID: 17366459.

15. Afif W, Huor P, Brassard P, et al. Compliance with methicillin-resistant Staphylococcus aureus precautions in a teaching hospital. Am J Infect Control 2002 Nov;30(7):430-3. PMID: 12410221.

16. Morgan DJ, Pineles L, Shardell M, et al. The effect of contact precautions on healthcare worker activity in acute care hospitals. Infect Control Hosp Epidemiol 2013 Jan;34(1):69-73. PMID: 23221195.

17. Morgan DJ, Diekma DJ, Sepkowitz K, et al. Adverse outcomes associated with contact precautions: a review of the literature. Am J Infect Control 2009 Mar;37(2):85-93. PMID: 19249637.