DPI Project Proposal Chapter 2 - Literature Review

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central-line-associated-bloodstream-infection-clabsi-change-package.pdf

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PREVENTING HARM FROM CLABSI >>>

2018 UPDATE

CENTRAL LINE-ASSOCIATED BLOODSTREAM INFECTIONS (CLABSI) CHANGE PACKAGE

>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>

ACKNOWLEDGEMENTS The analyses upon which this report is based were performed under Contract Number HHSM-500-2016-

00067C, entitled Hospital Improvement and Innovation Network (HIIN), sponsored by the Centers for

Medicare & Medicaid Services, Department of Health and Human Services.

We would like to recognize the contributions of the Health Research & Educational Trust (HRET) Hospital

Improvement Innovation Network (HIIN) team and Cynosure Health for their work in developing the

content of this change package.

Suggested Citation: Health Research & Educational Trust (June 2018). Central Line-Associated Bloodstream Infections (CLABSI) Change Package: 2018 Update. Chicago, IL: Health Research &

Educational Trust. Accessed at http://www.hret-hiin.org/

Accessible at: http://www.hret-hiin.org/

Contact: [email protected]

© 2018 Health Research & Educational Trust. All rights reserved. All materials contained in this publication are available to anyone for download on www.hret.org for personal, non-commercial use only. No part of this publication may be reproduced and distributed in any form without permission of the publication or in the case of third party materials, the owner of that content, except in the case of brief quotations followed by the above suggested citation. To request permission to reproduce any of these materials, please email [email protected].

>>> TABLE OF CONTENTS PART 1: Adverse Event Area (AEA) Definition and Scope 2

PART 2: Measurement 4

PART 3: Approaching your AEA 5

PART 4: Conclusion and Action Planning 18

PART 5: Appendices 19

PART 6: References 23

How to Use this Change Package

This change package is intended for hospitals participating in the Hospital Improvement Innovation

Network (HIIN) project led by the Centers for Medicare & Medicaid Services (CMS) and Partnership for

Patients (PFP); it is meant to be a tool to help you make patient care safer and improve care transitions.

This change package is a summary of themes from the successful practices of high performing health

organizations across the country. It was developed through clinical practice sharing, organization site

visits and subject matter expert contributions. This change package includes a menu of strategies, change

concepts and specific actionable items that any hospital can implement based on need or for purposes

of improving patient quality of life and care. This change package is intended to be complementary to

literature reviews and other evidence-based tools and resources.

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PART 1: ADVERSE EVENT AREA (AEA) DEFINITION AND SCOPE

CURRENT DEFINITION Hospital-acquired central line-associated bloodstream infections (CLABSI) are serious but preventable infections when evidence-based guidelines for central

line insertion and maintenance are properly prioritized and implemented.1

Magnitude of the Problem

If not prevented, CLABSIs result in increased length of hospital stay, increased cost and increased patient

morbidity and mortality. An estimated 30,100 CLABSIs occur in U.S. ICUs each year.2 Patient mortality

rates associated with CLABSIs range from 12 to 25 percent3 and the cost of CLABSIs per episode of care

ranges from $3,700 to $36,000.4

Between 2008 and 2013, the adoption and implementation of evidence-based practices has been associated

with a 46 percent reduction in CLABSIs.5 Leveraging this improvement, further efforts are needed to

prevent patient harm, especially in noncritical care settings including hemodialysis centers and inpatient

wards. As the majority of CLABSIs occur outside the ICU1,the maintenance, application and spread of

ICU improvement successes are necessary to realize safety goals across patient populations.

Fortunately, CLABSI prevention strategies are applicable to both critical and noncritical care settings. The

CLABSI central venous catheter (CVC) insertion bundle includes: procedural pause, hand hygiene, aseptic

technique, optimal site selection, chlorhexidine for skin preparation and maximal sterile (full-barrier)

precautions.6 The CLABSI maintenance bundle includes central line site dressing changes, administration

tubing changes, IV fluid changes and daily review of line necessity with timely removal.1

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> HEN 1.0 Progress

• Through the work of the AHA/HRET Hospital Engagement Network, from 2011 through 2014, more than

1,400 hospitals worked to prevent CLABSI. Under this initiative, 893 CLABSI harms were prevented and

an estimated $15,181,000 was saved.7

> HEN 2.0 Reduction Progress

• Through the work of the AHA/HRET Hospital Engagement Network 2.0, from 2015 through 2016, more

than 1,400 hospitals worked to prevent CLABSI. Under the second phase of this initiative, 505 CLABSI

harms were prevented and an estimated $7,469,000 was saved.

> HIIN Reduction Goals:

• Decrease the rate of CLABSI by 20 percent in all tracked units by September 27, 2018.

of Eligible Acute/Critical Access Hospital/ Children’s Hospital Reporting data

93% 94% Weighted Reduction in CLABSI Across Multiple Measures

46%

$15,181,000 TOTAL PROJECT ESTIMATED COST SAVING

14 states 40% REDUCTION GOALMEETING THE 893CLABSI HARMS PREVENTED

WHAT DOES THAT MEAN?

of Eligible Acute/Critical Access Hospital/ Children’s Hospital Reporting data

98% Reduction in CLABSI Measures

11% Percent of participants that stated information provided will promote higher quality work

98%

WHAT DOES THAT MEAN?

15 states

MEETING THE 40% REDUCTION IN PREVENTABLE HARM GOAL

$7,469,000 TOTAL PROJECT ESTIMATED COST SAVINGS

505 CLABSI HARMS PREVENTED

of Positive Responses to CLABSI Education Events

“Chance The Information Will Improve My Effectiveness/Results”

of Eligible Acute/Critical Access Hospital/ Children’s Hospital Reporting data

93% 94% Weighted Reduction in CLABSI Across Multiple Measures

46%

$15,181,000 TOTAL PROJECT ESTIMATED COST SAVING

14 states 40% REDUCTION GOALMEETING THE 893CLABSI HARMS PREVENTED

WHAT DOES THAT MEAN?

of Eligible Acute/Critical Access Hospital/ Children’s Hospital Reporting data

98% Reduction in CLABSI Measures

11% Percent of participants that stated information provided will promote higher quality work

98%

WHAT DOES THAT MEAN?

15 states

MEETING THE 40% REDUCTION IN PREVENTABLE HARM GOAL

$7,469,000 TOTAL PROJECT ESTIMATED COST SAVINGS

505 CLABSI HARMS PREVENTED

of Positive Responses to CLABSI Education Events

“Chance The Information Will Improve My Effectiveness/Results”

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PART 2: MEASUREMENT

A key component to making patient care safer in your hospital is to track your progress toward

improvement. This section outlines the nationally recognized process and outcome measures that

you will be collecting and submitting data on for the HRET HIIN. Collecting these monthly data

points at your hospital will guide your quality improvement efforts as part of the Plan-Do-Study-

Act (PDSA) process. Tracking your data in this manner will provide valuable information you need

to study your data across time and determine the effect your improvement strategies are having

in your hospital at reducing patient harm. Furthermore, collecting these standardized metrics will

allow the HRET HIIN to aggregate, analyze, and report its progress toward reaching the project’s

20/12 goals across all AEAs by September 2018.

Nationally Recognized Measures: Process and Outcome

Please download and reference the encyclopedia of measures (EOM) on the HRET HIIN website for additional

measure specifications and for any updates after publication at: http://www.hret-hiin.org/data/hiin_eom_

core_eval_and_add_req_topics.pdf

> HIIN Evaluation Measures

• CLABSI standardized infection ratio (SIR) (NQF 0139) reported for

> ICU units, including NICU

> ICU and other units

• Central line utilization ratio (central line days/patient days) * 100

• CLABSI rates (CLABSIs per 1,000 central line days, CLABSIs per 10,000 patient days) reported for

> ICU units, including NICU

> ICU and other inpatient units

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Investigate Your Problem and Implement Best Practices

BRIEF DESCRIPTION OF DRIVER DIAGRAMS: A driver diagram visually demonstrates the causal relationship between change ideas, primary drivers, secondary drivers, and your overall aim. A description

of each of these components is outlined in the table below. This change package is organized by reviewing

the components of the driver diagram to: (1) help you and your care team identify potential change ideas

to implement at your facility and (2) to show how this quality improvement tool can be used by your team to

tackle new process problems.

AI M PRIMARY DRIVER

SECONDARY DRIVER Change Idea

SECONDARY DRIVER Change Idea

PRIMARY DRIVER SECONDARY DRIVER Change Idea

PART 3: APPROACHING CLABSI

> Suggested Bundles and Toolkits

• Institute for Healthcare Improvement (IHI) How-to Guide: Prevent Central Line- Associated Bloodstream Infection, retrieved from www.ihi.org/knowledge/Pages/Tools/ HowtoGuidePreventCentralLineAssociatedBloodstreamInfection.aspx

• Agency for Healthcare Research & Quality (AHRQ) Tools for Reducing Central Line-Associated Blood Stream Infections, retrieved from www.ahrq.gov/professionals/education/curriculum-tools/ clabsitools/index.html

• Centers for Disease Control and Prevention (CDC) Guidelines for the Prevention of Intravascular Catheter Related Infections, 2011, retrieved from www.cdc.gov/hicpac/pdf/guidelines/bsi- guidelines-2011.pdf

• The Society for Healthcare Epidemiology of America/Infectious Diseases Society of America (SHEA/IDSA) Compendium on CLABSI — Strategies to Prevent Central Line-Associated Bloodstream Infections in Acute Care Hospitals: 2014 Update, retrieved from www.jstor.org/ stable/10.1086/676533

• For key tools and resources related to preventing and reducing CLABSI, visit www.hret-hiin.org.

• Health Research & Educational Trust (HRET) Hospital Improvement Innovation Network. 2016 UP Campaign Start Up Tool — focus on SOAP Up. Retrieved from http://www.hret-hiin.org/Resources/ up_campaign/17/up_campaign_setup_tool.pdf

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AIM: A clearly articulated goal or objective describing the desired outcome. It should be specific, measurable, and time-bound.

PRIMARY DRIVER: System components or factors that contribute directly to achieving the aim.

SECONDARY DRIVER: Action, interventions, or lower-level components necessary to achieve the primary driver.

CHANGE IDEAS: Specific change ideas which will support or achieve the secondary driver.

Drivers in This Change Package

RE D

U CE

C LA

BS I

STANDARDIZE INSERTION PROCESS

IMPLEMENT INSERTION CHECKLIST Change Idea

IMPLEMENT "STOP THE LINE" Change Idea

OPTIMAL SITE AND DEVICE SELECTION Change Idea

HAND HYGIENE, ASEPTIC TECHNIQUE Change Idea

PREP WITH 2 PERCENT CHG Change Idea

REVIEW LINE NECESSITY DAILY

REVIEW LINE NECESSITY DAILY Change Idea

STANDARDIZE MAINTENANCE PROCESS

BUNDLE TOGETHER ELEMENTS Change Idea

INCORPORATE INTO DAILY ASSESSMENT Change Idea

SCRUB THE HUB Change Idea

BLOOD CULTURE COLLECTION

SPECIALIZE TACTICS: BEYOND THE BUNDLES

USE CHG DRESSINGS Change Idea

BATHE WITH CHG Change Idea

USE A NON-SUTURE SECUREMENT Change Idea

USE ANTIMICROBIAL-IMPREGNANTED CVCS Change Idea

INVOLVE PATIENTS AND FAMILIES Change Idea

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AIM

Secondary Driver > IMPLEMENT AN INSERTION CHECKLIST

An insertion checklist can help ensure that all recommendations for insertion of a CVC are followed each time. The checklist includes a list of actions that should occur before (e.g., procedural pause), during (e.g., skin prep with 2 percent chlorhexidine gluconate (CHG)) and after (e.g., appropriate site dressing) CVC insertion.13,14 Use of a checklist is an effective approach to ensure patients are receiving appropriate care. See Appendix II for an example of CVC insertion checklists.

Change Ideas

> Adopt and use a CVC insertion checklist using the following guidelines:

• Engage staff nurses to adopt and adapt a CVC insertion checklist to promote patient safety

• Enlist the medical director or other provider champion to support the use of the checklist and to educate and mentor providers

• Determine who will complete the insertion checklist at the time of insertion: the nurse assisting, an independent nurse observer, or a technician

• Determine what is to be done with the paper or electronic checklist after it has been completed for tracking of compliance to the insertion bundle (e.g., could be sent to infection prevention manager or CLABSI prevention champion)

Suggested Process Measure for Your Test of Change

• Percent compliance of insertion bundle guidelines

Secondary Driver > IMPLEMENT “STOP THE LINE”

A checklist ensures best practices for CLABSI reduction are followed. It is important to create a safe process for staff to speak up if a violation of infection prevention practices is observed during a central line insertion. Staff and providers must work together to ensure that all aspects of the checklist are instituted with every patient. If a break in practice occurs, the procedure should be halted and corrections must be made. Corrections could include changing a contaminated glove, replacing the guide wire or using a full body drape instead of a short drape. Successful implementation of a checklist requires effective interpersonal communication skills and can give staff an opportunity to learn teamwork skills experientially.

Change Ideas

> Adopt policies that combine individual accountability with a blame-free, patient-centered approach to errors

> Use the medical director or another provider champion to support the “stop the line” approach and communicate the value to other providers

> Create a process, with staff, to “stop the line.” Scripting can be helpful. One hospital’s staff adopted the phrase “the sterile field has been contaminated” to be uttered by the nurse or technician auditing the process15

> Determine specific incidents that prompt the staff to “stop the line,” e.g., not everyone in the room is wearing maximal barrier precautions, there is a break in the sterile field, a full-body drape is not being used or proper skin prep has not been done

> Develop a strategy in your clinical area to support the staff who “stop the line,” i.e., what to do if a violation is identified and if the provider fails to correct the violation. Possible options could include paging the unit nursing director or medical director to intervene

Primary Driver:

STANDARDIZE INSERTION PROCESS (INSERTION BUNDLES)

Following established

guidelines for central

venous catheter (CVC)

insertion will decrease

CLABSI rates.8,9,10 All

units should adopt and

implement this evidence-

based insertion bundle.11,12

The insertion bundle

includes: indications for

CVCs, maximal sterile

barrier precautions,

aseptic technique, hand

hygiene, proper skin

prep, and correct

insertion technique.

REDUCE CLABSI

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> Ensure policies and processes are in place for use of the checklist and “stop the line.” Executive support for staff “stopping the line” is needed before and after breaches in policies occur

> Consider TeamSTEPPS® training to support crucial communication and teamwork16

Secondary Driver > OPTIMAL SITE AND DEVICE SELECTION Research data suggest that certain CVC sites may have a lower risk of infection. 17,18,19,20,21,22 The current CDC/NHSN and SHA/IDSA practice recommendation is to avoid using the femoral vein for central venous access in adult patients.23,24,25,26 The subclavian site may be superior to the jugular site in terms of CLABSI risk; however, other risks associated with the subclavian site must be considered (e.g., pneumothorax). Site selection is based on patient need and risks, and some new evidence suggests the femoral site is not as prone to risk of infection as once reported. If the femoral site is used, site prep and line maintenance done according to guidelines are vitally important. Consider alternatives to central lines when clinically indicated such as midline catheters or longer dwell-time peripheral intravenous catheters.

Change Ideas

> Include site selection as an item on insertion checklist

> Promote documentation of rationale for use of femoral site if it is selected for CVC placement

Suggested Process Measure for Your Test of Change

• Percent compliance with appropriate CVC insertion site selection

Secondary Driver > ULTRASOUND GUIDANCE FOR LINE PLACEMENT The use of ultrasound (US) to guide insertion may reduce the risk of iatrogenic harm and increase accuracy of line placement. Studies have demonstrated that, as compared to the technique of using landmarks, US guidance in placement of CVC in adults and children decreases the number of anatomical sites utilized and decreases the number of attempts to achieve successful placement.27,28,29 US guidance may therefore decrease patient discomfort, risk of harm and time to successful CVC placement, and may increase compliance with insertion guidelines. US guidance may encourage the use of the subclavian or internal jugular entry site versus the femoral site because it reduces the risk of iatrogenic pneumothorax and other complications.

Change Ideas

> Have the physician champion and other early adopters promote the use of ultrasound guidance

> Ask the lead physician to host in-services and provide continuing medical education (CME) credit on the use and benefit of using ultrasound for CVC placement. Include hands-on practice for physicians attending. Follow state and hospital credentialing for physician use of ultrasound guidance for line placement. Education and demonstrated competency will be required

> Partner with your infection prevention practitioner when introducing US-guided CVC placement

Suggested Process Measures for Your Test of Change

• Percentage of central lines placed with ultrasound guidance

Secondary Driver > FOLLOW RECOMMENDED PRACTICES FOR HAND HYGIENE, ASEPTIC TECHNIQUE AND MAXIMAL STERILE BARRIER PRECAUTIONS

Establish a process to ensure appropriate practices for hand hygiene, aseptic technique, and maximal sterile barrier precautions are followed. Hand hygiene continues to be an

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integral part of any infection prevention program.30,31 Following aseptic technique for insertion and care is crucial to prevent CLABSI. Aseptic technique includes using maximal sterile barrier precautions such as a cap, mask, sterile gown, sterile gloves, and a sterile full-body drape during insertions of CVCs and PICCs or during guide wire exchange.32

Change Ideas

> Provide easy access to hand hygiene agents such as conventional soap and water or alcohol-based hand sanitizers to facilitate hand hygiene before and after each procedure

> Include hand hygiene and maximal barrier precautions as part of a CVC insertion checklist

> Have supplies and equipment easily available, e.g., a central line insertion kit with maximal barrier precaution supplies, central line dressing kits, and administration sets. Consider enlisting staff to help build an insertion kit or line cart and to keep it stocked

> Package CVC, skin antiseptic, and maximal barrier precautions in insertion kits to make it easier for providers to follow recommended guidelines

> Introduce the HRET HIIN SOAP UP CAMPAIGN to promote hand hygiene and CVC care and removal

Suggested Process Measure for Your Test of Change

• Percent compliance with maximum barrier drape

• Percent compliance with hand hygiene prior to CVC insertion

Secondary Driver > SKIN PREP WITH 2% CHLORHEXIDINE (CHG)

The preferred agent for skin antisepsis before catheter insertion and during dressing changes is two percent chlorhexidine (2 percent chlorhexidine in 70 percent isopropyl alcohol) unless the patient is allergic to chlorhexidine or under two months of age.33,34

Change Ideas

> Include two percent CHG swabs in the CVC insertion kits and on the CVC line cart

> Include skin prep with two percent CHG as an item on the insertion checklist

Suggested Process Measures for Your Test of Change

• Percent compliance with use of CHG skin prep

Hardwire the Process

Hardwiring tactics for the central line insertion bundle includes many of the change ideas. Ongoing monitoring of compliance to insertion guidelines is vital to sustain recommended practices.

> Engage staff and providers in the design and development of tools and support systems such as an insertion checklist and a CVC line cart.

> Attach the checklist to the central line insertion kit for easy access.

> Implement the use of an insertion checklist and empower the designated observers to enforce use of the checklist and adherence to recommended insertion practices.

> Audit compliance and provide feedback to providers regarding the audit results and recommendations for improvement. Report results regularly in quality or infection prevention committees. If compliance to insertion guidelines decreases, engage practitioners and nurses to examine contributing factors, barriers, and potential changes.

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Secondary Driver > DAILY REVIEW OF LINE NECESSITY

Current CDC and SHEA/IDSA practice guidelines recommend daily review of line necessity and prompt removal of the line when no longer necessary.37,38

Change Ideas

> Combine daily review of line necessity with other best practice reviews such as daily urinary catheter review. Line necessity is determined by a patient’s clinical needs

> Incorporate daily review into routine workflow, such as charge nurse rounds or daily multidisciplinary rounds

> Include an infection preventionist as part of rounds. He or she can help support line necessity review

> If using an electronic practice management system, institute computer-based pop-up reminders to review line necessity

Suggested Process Measures for Your Test of Change

• Percent compliance with daily review of the necessity for a central line

Hardwire the Process

To hardwire daily review of line necessity, make the process a part of the daily workflow. Do small tests of change with staff to determine the best implementation process. Methods for hardwiring include:

> Adding daily review of line necessity as a standing item in nurse-to-nurse handoff reports.

> Auditing daily line review compliance and providing feedback to the care team. If compliance is low, ask why, and engage staff in identifying problems and refining the process of daily review.

> Assigning responsibility for daily line necessity and documentation to the primary care provider.

Primary Driver:

DAILY REVIEW OF LINE NECESSITY.

One of the most

effective strategies for

preventing CLABSIs is

to eliminate or reduce

exposure to CVCs. The

decision regarding the

need for a central line is

complex, however, and

difficult to standardize

or incorporate into

a practice guideline.

Nevertheless, to reduce

exposure to CVCs, the

multidisciplinary team

should adopt a strategy

to systematically

evaluate on a daily basis

whether all central lines

remain necessary or

can be removed.35,36

11

Current recommendations for most CVCs from CDC/NHSN guidelines and SHEA/IDSA 2014 practice recommendations include:

1. Use sterile, transparent, semipermeable dressing (or sterile gauze) to cover the catheter site.

a. Replace site dressing every seven days (every two days if made of gauze) or if it becomes loose, soiled, or damp.

b. Use of topical antibiotic ointment or creams is not recommended unless the line is a dialysis catheter.

2. Replace administration tubing at intervals of less than 96 hours.

a. See CDC guidelines regarding blood products, fat emulsions, etc.41 Establish and implement facility guidelines for intravenous fluid administration bag changes. For further details, please see the actual guidelines referenced above as “Key Resources.”

Secondary Driver > BUNDLE TOGETHER ELEMENTS

Bundling care practices and supplies together helps the caregiver to remember the evidence-based practices required and to comply with the guidelines.

Change Ideas

> Have supplies and equipment stored together and easily available, e.g., central line dressing kits, chlorhexidine dressings, IV fluid infusion bags, and administration sets

> Have supplies for accessing IV tubing and ports together and easily available, e.g., chlorhexidine, povidone iodine, an iodophor or 70 percent alcohol, and alcohol- impregnated caps for unused ports

> Establish a specific day of the week for line changes, e.g., every Wednesday

> Assign dressing change responsibility to a core group of individuals who are highly trained and competent (e.g., the PICC team)

Suggested Process Measures for Your Test of Change

• Percent compliance with site dressing done according to standard

Secondary Driver > INCORPORATE INTO DAILY ASSESSMENT AND REVIEW

Incorporate a daily review of the maintenance bundle to ensure that dressings, administration tubing, and IV fluid are current and not expired. If any missing element is found during the review, establish a process to correct the missing element.

Change Ideas

> Perform maintenance bundle review along with daily line necessity review. Items to review can be included in the charge nurse’s checklist. If the bedside nurse has not had time to change the dressing or administration tubing, for example, the charge nurse can delegate the task to another nurse

> Develop a process to ensure CVC maintenance is completed as needed

Suggested Process Measures for Your Test of Change

• Percent compliance with maintenance bundle of individual bundle elements

• Percent compliance of all-or-none bundle element

• See Appendix III for an example of a CVC maintenance audit or monitoring tool

Primary Driver:

STANDARDIZE THE MAINTENANCE PROCESS.

The bundle approach

provides a means to

incorporate evidence-

based interventions into

patient care. Adopt and

embed evidence-based

guidelines (bundle)

for CVC maintenance

after insertion across

care settings. Because

a significant proportion

of central line days

and CLABSIs occur in

non-ICU settings, it is

important to include

them in the maintenance

process implementation.39

Implementation of a

post-insertion care

bundle in addition to an

insertion bundle has been

shown to be effective

in reducing CLABSI.40

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%

Secondary Driver > SCRUB THE HUB Before accessing the line, disinfect catheter hubs, needleless connectors, and injection ports.42 SHEA/IDSA 2014 practice recommendations state to scrub the hub with a CHG preparation or 70 percent alcohol combination for a minimum of five seconds.43,44,45

See Appendix IV for a Scrub the Hub flyer.

Change Ideas

> Have supplies for disinfecting line access sites easily available, e.g., IV carts, medication carts

> Incorporate use of antiseptic impregnated caps for all central line ports. This minimizes the need to scrub the hub46

Suggested Process Measures for Your Test of Change

• Percent compliance with scrub the hub prior to accessing line

Hardwire the Process

Strategies to hardwire catheter maintenance and maintenance bundle compliance are similar to those used for insertion bundle and daily line necessity reviews. Hardwiring should be included in the initial planning and testing. Making the implementation and review processes as routine as possible will ensure that CLABSI prevention is addressed in every patient with a CVC in any care area.

> Incorporate daily maintenance bundle item review along with line necessity review into the daily workflow.

> Include bundle review as a standing item in nurse-to-nurse handoff reports. Enlist all shifts (24/7) in reducing risk of harm by implementing the guidelines and performing necessary tasks such as dressing changes.

> Review central line care and maintenance with staff upon hire and at least annually and assess staff competency in this arena.

> Audit maintenance care compliance and provide feedback to the care team. If compliance is low, ask why, and engage staff in identifying problems and refining the process of implementation and review.

> Incorporate daily rounds to have staff identify the presence of invasive devices such as central lines and urinary catheters (often referred to as “plastic rounds”).

Secondary Driver > BLOOD CULTURE COLLECTION

Increase the accuracy of CLABSI identification and treatment by optimizing best practice in the collection, handling, and management of blood culture specimens

Change Ideas

> Make the right thing the easy thing by preassembling peripheral blood culture collection supplies to promote best practices

> Review blood culture collection practices with staff to assure reliabilty of practices

Suggested Process Measures for Your Test of Change

Percent of blood culture draws from peripheral vein

Hardwire the Process

Blood culture draws from central lines are perceived as "better" for the patient as they don't require a peripheral stick. Educate staff to assure they understand that there have been nine studies that demonstrated a higher blood culture contaminate rate when blood was drawn from a central venous catheter.

> Consider drawing venipunture samples on the opposite extremity of an infusion

> Assure optimal aseptic technique during blood culture collection

13

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Primary Driver:

SPECIALIZE TACTICS “BEYOND THE BUNDLES”.

Additional strategies

are recommended to

further reduce CLABSI

rates if the rates remain

unacceptably high after

implementation of basic

CLABSI prevention

strategies. More research

has emerged on the use

of CHG dressings and

CHG-containing sponge

dressings, CHG bathing,

the use of nonsuture

securement devices,

the use of antimicrobial-

impregnated CVCs for

adult patients, and

ultrasound guidance

to place lines. Both

SHEA/IDSA and CDC/

NHSN guidelines also

recommend against

routine replacement

of CVCs.47,48

Secondary Driver > USE OF CHLORHEXIDINE (CHG)-CONTAINING DRESSINGS

Apply CHG-containing sponge dressings directly to the insertion site (encircle the catheter itself) for temporary short-term catheters under a transparent dressing.49,50,51 Also emerging as a recommendation for catheter sites is the use of a transparent dressing with infused CHG that covers the site.52

Change Ideas

> Include CHG dressing use in staff trainings on CVC site care and maintenance and assess staff understanding and competency

> Include CHG-infused sponge dressings or CHG dressings in the dressing kit or supplies

> Review the use of CHG dressing sponges daily as part of the maintenance bundle review

Suggested Process Measures for Your Test of Change

• Percent compliance with CVC dressing changes

Secondary Driver > CHG BATHING

Daily bathing with CHG has been shown to reduce the incidence of health care- associated bloodstream infections and is now a recommended practice as an additional intervention.53,54,55,56 CHG bathing reduces the bio-burden on the patient’s skin and thereby reduces the risk of CVC site infection and CLABSI. Bathe patients older than two months of age daily with two percent CHG.57,58

Change Ideas

> Include CHG bathing as part of staff central line care and maintenance training and assess staff competency

> Have two percent CHG-saturated cloths easily available to staff

> Incorporate use of two percent CHG cloths for daily skin cleansing into the daily workflow such as nurse’s aides’ delivery of daily hygiene care

> Incorporate CHG skin cleansing daily as part of the maintenance bundle review

Suggested Process Measures for Your Test of Change

• Percent compliance with daily CHG bathing and bathing technique

Secondary Driver > USE A NONSUTURE SECUREMENT DEVICE

The use of a nonsuture securement device reduces the risk of infection at the CVC site and is included in the CDC/NHSN guidelines.59

Change Ideas

> Include a nonsuture device in the CVC insertion kits. Do not include sutures in the kit. Work with the supplier or assembler of the insertion kits to include all needed supplies.

Suggested Process Measures for Your Test of Change

• Percent compliance with nonsuture securement device

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Secondary Driver > ANTISEPTIC- OR ANTIMICROBIAL-IMPREGNATED CVCS FOR ADULT PATIENTS Use a CVC impregnated with CHG/silver sulfadiazine or minocycline/rifampin in patients whose catheter is expected to remain in place for more than five days (contraindicated if the patient is allergic to the impregnated substance). Use of antimicrobial-impregnated CVCs can also be an additional strategy to reduce CLABSI rate in facilities with continued high CLABSI rates after the implementation of insertion and maintenance bundles.60,61 Consider the use of these CVCs in other situations, such as for inpatients with limited venous access and a history of recurrent CLABSI and for patients who have increased risk for severe sequelae from a CLABSI (e.g., patients with recently implanted intravascular devices).62

Change Ideas

> Test the use of an antiseptic- or antimicrobial-impregnated CVC in patients whose CVC is expected to remain in place for more than five days

> Include an antiseptic- or antimicrobial-impregnated CVC as an option for placement in the CVC line cart

Suggested Process Measures for Your Test of Change

• Percent compliance with antiseptic- or antimicrobial-impregnated CVC in appropriate patients

Secondary Driver > DO NOT ROUTINELY REPLACE CVCS Routine replacement of CVCs is NOT recommended by either CDC/NHSN guidelines or SHEA/IDSA. CVCs including PICCs should not be removed on the basis of fever alone.63 CDC/NHSN recommends that physicians use clinical judgment regarding the appropriateness of removing the CVC if infection is evidenced elsewhere or if a noninfectious cause of fever is suspected.64 CDC/NHSN guidelines also caution against the use of routine guide wire exchanges to prevent infection and to replace a catheter suspected of infection.

Change Ideas

> Incorporate into policy the recommendation that CVCs are not to be replaced routinely

Suggested Process Measures for Your Test of Change

• Percent of CVCs not replaced

Secondary Driver > PATIENT AND FAMILY ENGAGEMENT: INVOLVE PATIENTS AND FAMILIES IN INFECTION PREVENTION PRACTICES Educate patients and families on all the steps being taken to prevent central line infection using a teach-back method. Patient and family education should include the purpose of a central line, expected duration of use, and why it is important to remove it as soon as it is no longer clinically indicated.

Change Ideas

> Educate the patient and his or her family or caregivers about what they can do to help prevent a central line infection, e.g., invite the patient and the family to remind health care providers to wash their hands and to ask each day if the central line continues to be necessary

> Make available to patients and families educational material on central lines, such as the CDC’s FAQs About Catheter-Associated Bloodstream Infection, retrieved at www.cdc.gov/hai/pdfs/bsi/BSI_tagged.pdf

Suggested Process Measures for Your Test of Change

• Percent compliance with documentation of patient and family education

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PDSA in Action | Tips on How to Use the Model for Improvement

Choice of Tests and Interventions for CLABSI Reduction:

> Implement the CVC maintenance bundle and line necessity review one unit at a time.

• Engage front-line staff from the beginning on process design and on the adoption and

adaptation of procedures.

• Consider testing maintenance bundle and line necessity in non-ICU settings.

IMPLEMENT SMALL TESTS OF CHANGE

PLAN > Do not reinvent the wheel. Pick a daily review tool that has been successful at another hospital and adapt it for your facility. See appendices III and IV for examples.

> Engage front-line staff in designing the implementation process, e.g., the day shift charge nurse on morning rounds will review maintenance bundle items and line necessity with the bedside nurse.

> Ask a receptive, early-adopter bedside nurse and charge nurse to test these changes on their next patient with a CVC.

DO > Test “small:" one charge nurse, one bedside nurse, one patient with a CVC, one shift. > Coordinate with the trial nurses to begin the daily review of the maintenance bundle and line necessity with one patient.

STUDY > Debrief as soon as possible after the test with those involved, asking: • What happened?

• What went well?

• What didn’t go well?

• What do we need to do differently next time?

PDSA

Hardwire the Process

Hardwiring is key to sustaining change. Making it easy for caregivers to do the right thing is a cornerstone hardwiring strategy. Be sure to include staff on the decision making of the design process.

> Bundle CHG dressings with other needed items into a CVC dressing kit.

> Store CHG bathing cloths in a place easily accessible to staff.

> Elicit feedback from patients and families on not only the care received but also the support they received from communication and education.

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ACT > Do not wait for the next committee meeting to make changes. Revise the procedures and re-test as soon as possible with the same bedside nurse and charge nurse.

> Grow the second test to include all patients on one unit on one shift and additional bedside nurses.

Potential Barriers

> Assess for practice drift periodically even if your rates are low. Engage with staff to discuss any barriers

to full implementation of the insertion and maintenance bundles.

• Do a spot check to determine bundle compliance for each element by checking five patients with CVCs

(including PICCs). Spot-check questions include:

> Were all of the insertion bundle elements completed?

> Is the site dressed according to the guidelines, is the dressing current, and is the CHG sponge

applied correctly?

> Is the administration tubing current?

> Was the CVC assessed daily for necessity?

> Recognize that there may be some pushback from physicians regarding changing practice.

• Engage a physician champion to support your change efforts.

• Listen to physicians’ feedback and engage them in process design and equipment and supply selection.

• Begin implementation with early-adopter physicians who can lead and recruit other early-adopter

champions from among specialty groups and intensivists.

• Despite the research evidence showing benefits from these guidelines, some physicians may be reluctant

to wear a cap or other items required for maximal barrier precautions. One hospital approached this

challenge by discussing the research evidence and the pros and cons of the recommendations with the

medical director of the ICU. The value of complying with the recommendations was emphasized. After

the medical director and other early-adopter champions modeled the new practices, the rest of the

medical staff agreed to adopt the evidence-based recommendations as well.

> Nurses may feel uncomfortable with “stopping the line” for an observed violation of infection control

practices and physicians may feel their credibility and authority is being challenged when a break in

technique is called out. To address these concerns:

• Both physician and nursing leadership need to be visible and to communicate the expectations of

adherence to the insertion bundle. They can coach staff on the importance of consistency in procedure

implementation and on how to “call a halt” or “stop the line.”65

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• Invite senior or unit-level leadership to meet with nursing and physician staff to emphasize that

the focus is on teamwork to promote patient safety and improve patient outcomes.

• Develop an algorithm for the observer to follow if a “stop the line” intervention is resisted. For example,

the observer could page the unit director 24/7 to intervene.

• Audit the percentage of CVC insertions that had the checklist properly completed. Calculate the rates

of compliance with evidence-based practice and the number of corrections required. Make the results

known to providers and enlist the providers in developing methods for improvement.

Enlist administrative leadership as sponsors to help remove or mitigate barriers

> Enlist an executive sponsor who recognizes the value of preventing CLABSI to the organization and your

patients. The sponsor can help engage key stakeholders, the board, and staff in seeing the big picture

of the importance of eliminating harm caused by CLABSI.

> The sponsor must have the authority and ability to provide solutions in overcoming barriers and

resources needed to facilitate implementation.

> Utilize respected senior physicians as “opinion leaders” who can test these changes in their local units,

and then advocate for organization-wide adoption of successful best practices.

Change not only “The Practice,” but also “The Culture”

> Instituting the CLABSI insertion and maintenance bundles will require a change in culture, particularly

among physicians, who will be asked to evolve their practice of individualizing management for each

patient toward a more standardized, multidisciplinary approach. Physicians may be concerned about the

perceived risks of loss of control and shared responsibility. Encourage physicians to actively monitor the

effectiveness of these multidisciplinary interventions to reduce CLABSI rates.

> Many physicians prefer to learn from peers rather than by following theoretical “expert advice.” Use lead

physicians as peer educators to advocate for the adoption of improvements such as a CVC insertion

bundle and to model the new practices.

> Begin the trial with a small test of change in one unit or area and then disseminate successful

results more widely across the organization. The ideal outcome is the development of team-based

care wherein each member of the team (physician, nurse, technicians) contributes to improved

quality of patient care.

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PART 4: CONCLUSION AND ACTION PLANNING

CLABSI prevention is complex and challenging. However, there are many evidence-based strategies

and tools to use to reduce CLABSI. This effort requires a multidisciplinary approach that includes

physicians, leaders, and front-line staff. Continual monitoring of compliance to bundles assists

in data-driven decision making. Utilizing data to drive practice and process changes as well as

communication to clinical staff on bundle performance and CLABSI rates is imperative.

> Multidisciplinary approach: Assemble a team with physician champions, front-line staff leaders, and

key leadership persons. Determine and define roles that the leader has the energy to lead a dynamic

process improvement project. Assess the composition of the team and the support from key strategic

partners such as the quality leader, chief medical officer, nursing director, infection prevention, etc.

Create strategies and/or allocate resources to engage front-line staff in designing new care processes.

> Ongoing monitoring: Use the data to drive decision making for determining practice and process

changes. Use the Top Ten Checklist (Appendix I) to assess current efforts in CLABSI prevention.

Ask, “Do we have this element in place? If so, how well are we doing it? Have we had practice drift?”

Enlist physician and nursing champions on the team to assist in data analysis, determine potential

interventions and conduct small tests of change.

> Communication: Establish clear lines of communication with physicians, staff, other stakeholders, and

supporting leadership. Communication should include bundle compliance performance, CLABSI rates,

and annotated with interventions to show effect of improvement efforts.

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APPENDIX I: TOP TEN CHECKLIST

Associated Hospital/Organization: HRET HIIN Purpose of Tool: A checklist to review current or initiate new interventions for CLABSI prevention in your facility

Reference: www.hret-hiin.org

PART 5: APPENDICES

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Created February 2017 www.hret-hiin.org

>>> PROMOTE SAFETY ACROSS THE BOARD

DATE OF LAST CLABSI:

Implement the insertion bundle: Procedural pause, hand hygiene, aseptic technique for insertion and care, site selection of subclavian (preferred) or internal jugular (acceptable), avoidance of femoral vein in adults, maximal sterile precautions, and skin prep with two percent chlorhexidine.

Implement an insertion checklist to promote compliance and monitoring.

Implement a “stop the line” approach to the insertion bundle. If there is an observed violation of infection control practices (e.g., maximal sterile barrier precaution, break in sterile technique), line placement should stop and the violation should be corrected.

Adopt the maintenance bundle with dressing changes (every seven days for transparent dressings), line changes, and IV fluid changes. Incorporate dressing changes into daily assessment and review. Can be part of charge nurse’s checklist along with the daily review of line necessity.

Incorporate a daily review of line necessity and maintenance bundle into workflow (e.g., charge nurse rounds). Use an electronic health care record prompt.

Use a chlorhexidine impregnated sponge dressing.

Use two percent chlorhexidine impregnated cloths for daily skin cleansing.

Do not routinely replace CVCs, PICCs, hemodialysis catheters, or pulmonary artery catheters.

Use a suture-less securement device.

Use ultrasound guidance to place lines if this technology is available.

Central Line-Associated Bloodstream Infections (CLABSI) Top Ten Checklist

Created August 2016

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APPENDIX II: PATIENT LABEL – CENTRAL LINE PROCEDURAL CHECKLIST

Associated Hospital/Organization: Institute for Healthcare Improvement

Purpose of Tool: To document procedural practices in the CCU related to insertion technique for CVP lines, dialysis access ports, and central lines (including PICC)

Reference: IHI CLABSI Insertion Checklist. Retrieved from http://www.ihi.org/knowledge/Pages/Tools/ CentralLineInsertionChecklist.aspx

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APPENDIX III: EXAMPLE OF A CVC MAINTENANCE AUDIT/MONITORING FORM

Associated Hospital/Organization: University of Kansas Hospital in Kansas City, Kansas

Purpose of Tool: Can be used to audit CVC maintenance practice

Reference: N/A

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APPENDIX IV: EXAMPLE OF A SCRUB THE HUB FLIER

Associated Hospital/Organization: University of Kansas Hospital in Kansas City, Kansas

Purpose of Tool: To promote line access disinfecting

Reference: N/A

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PART 6: REFERENCES

1. Marshall, J., et al. (2014). Strategies to prevent central line-associated bloodstream infections in acute care hospitals: 2014 update. Infection Control & Hospital Epidemiology, 29(7), 753-771.

2. Centers for Disease Control and Prevention. (2015). Bloodstream infection event (central line-associated bloodstream infection and non-central line-associated bloodstream infection).

3. Centers for Disease Control and Prevention. (2011). Vital signs: central line-associated blood stream infections – United States, 2001, 2008, and 2009. Annals of Emergency Medicine, 58(5), 447-450.

4. Scott, R.D. (2009). The direct medical costs of healthcare-associated infections in U.S. hospitals and the benefits of prevention.

5. Centers for Disease Control and Prevention. (2014). National and state healthcare-associated infections progress report. Retrieved from http://www.cdc.gov/hai/progress-report/

6. Institute for Healthcare Improvement. (2012). How-to guide: Prevent central line-associated bloodstream infections. Cambridge, MA. Retrieved from www.ihi.org

7. AHA/HRET Final Project Report. Retrieved from www.hret-hen.org

8. Grady, N.P., Alexander, M., Burns, L.A., Dellinger, P., Graland, J., Heard, S.O., et al. (2011). Guidelines for the prevention of intravascular catheters-related infections, 2011. Retrieved from http://www.cdc.gov/hicpac/pdf/guidelines/bsi- guidelines-2011.pdf

9. Southworth, S.L., Jenamn, L.J., Kinder, L.A., Sell, J.L. (2012). The journey to zero central catheter-associated bloodstream infections: Culture change in an intensive care unit. Critical Care Nurse, 32(2), 49-54.

10. Gozu, A., Clay, C., Younus, F. (2001). Hospital-wide reduction in central line-associated bloodstream infections: A tale of two small community hospitals. Infection Control & Hospital Epidemiology , 32(6), 619-622.

11. Marshall, J., et al. (2014). Strategies to prevent central line-associated bloodstream infections in acute care hospitals: 2014 update. Infection Control & Hospital Epidemiology, 29(7), 753-771.

12. Institute for Healthcare Improvement. (2012). How-to guide: Prevent central line-associated bloodstream infections. Cambridge, MA. Retrieved from http://www.ihi.org/knowledge/Pages/Tools HowtoGuidePreventCentralLineAssociatedBloodstreamInfection.aspx

13. Grady, N.P., Alexander, M., Burns, L.A., Dellinger, P., Graland, J., Heard, S.O., et al. (2011). Guidelines for the prevention of intravascular catheters-related infections, 2011. Retrieved from http://www.cdc.gov/hicpac/pdf/guidelines/bsi- guidelines-2011.pdf

14. Marshall, J., et al. (2014). Strategies to prevent central line-associated bloodstream infections in acute care hospitals: 2014 update. Infection Control & Hospital Epidemiology, 29(7), 753-771.

15. Southworth, S.L., Jenamn, L.J., Kinder, L.A., Sell, J.L. (2012). The journey to zero central catheter-associated bloodstream infections: Culture change in an intensive care unit. Critical Care Nurse, 32(2), 49-54.

16. Agency for Healthcare Research and Quality. (2015). TeamSTEPPS®: Strategies and tools to enhance performance and patient safety. Retrieved from http://www.ahrq.gov/professionals/education/curriculum-tools/teamstepps/index.html

17. Goetz, A.M., Wagener, M.M., Miller, J.M., Muder, R.R. (1998). Risk of infection due to central venous catheters: Effect of site placement and catheter type. Infection Control & Hospital Epidemiology, 19, 842-845.

18. Parienti, J.J., Thirion, M., Magarben, B., et al. (2008). Femoral versus jugular central catheterization in patients requiring renal replacement therapy: A randomized controlled study. JAMA, 299, 2413-2422.

19. Merrer, J., Jonghe, B.D., Golliot, F., et al. (2001). Complications of femoral and subclavian venous catheterization in critically ill patients: A randomized controlled trial. JAMA, 286, 700.

20. Marshall, J., et al. (2014). Strategies to prevent central line-associated bloodstream infections in acute care hospitals: 2014 update. Infection Control & Hospital Epidemiology, 29(7), 753-771.

21. Grady, N.P., Alexander, M., Burns, L.A., Dellinger, P., Graland, J., Heard, S.O., et al. (2011). Guidelines for the prevention of intravascular catheters-related infections, 2011. Retrieved from http://www.cdc.gov/hicpac/pdf/guidelines/bsi- guidelines-2011.pdf

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22. Parienti, J.J., du Cheryron, D., Timisit, J.F., Traore, O., Kalfon, P., Mimoz, O., Mermel, L.A. (2012). Meta-analysis of subclavian insertion and nontunneled central venous catheter-associated infection risk reduction in critically ill adults. Critical Care Medicine, 40(5), 1627-1634.

23. Parienti, J.J., Thirion, M., Mégarbane, B., Souweine, B., Ouchikhe, A., Polito, A., … Members of the Cathedia Study Group. (2008). Femoral vs. jugular venous catheterization and risk of nosocomial events in adults requiring acute renal replacement therapy: A randomized controlled trial. JAMA, 299, 2413-22.

24. Marik, P.E., Flemmer, M., Harrison, W. (2012). The risk of catheter-related infection with femoral venous catheters as compared to sublavin and internal jugular venous catheters: A systematic review of the literature and meta-analysis. Critical Care Medicine, 40(8), 2479-2485.

25. Timsit, J.F., et al. (2013). Jugular versus femoral short-term catheterization and risk of infection in intensive care unit patients. Causal analysis of two randomized trials. American Journal of Respiratory and Critical Care Medicine, 188(10), 1232-1239.

26. Merrer, J., De Jonghe, B., Golliot, F., Lefrant, J.Y., Raffy, B., Barre, E., … French Catheter Study Group in Intensive Care. (2001). Complications of femoral and subclavian venous catheterization in critically ill patients: A randomized controlled trial. JAMA, 286, 700-707.

27. Miller, A.H., Roth, B.A., Mills, T.J., Woody, J.R., Longmoor, C.E., Foster, B. (2002). Ultrasound guidance versus the landmark technique for the placement of central venous catheters in the emergency department. Academic Emergency Medicine, 9(8), 800-805.

28. Froehlich, C.D., Rigby, M.R., Rosenberg, E.S., Li, R., Roerig, P.L., Easley, K.A., Stockwell, J.A. (2009). Ultrasound-guided central venous catheter placement decreases complications and decreases placement attempts compared with the landmark technique in patients in pediatric intensive care unit. Critical Care Medicine, 37(3), 1090-1096.

29. Karakitsos, D., Labropoulos, N., de Groot, E., Patrianakos, A.P., Kouraklis, G., Poularas, J., … Karabinis, A. (2006). Real-time ultrasound-guided catheterization of the internal jugular vein: A prospective comparison with the landmark technique in critical care patients. Critical Care, 10(6), R162.

30. Institute for Healthcare Improvement. (2012). How-to guide: Prevent central line-associated bloodstream infections. Cambridge, MA. Retrieved from http://www.ihi.org/knowledge/Pages/Tools/HowtoGuidePreventCentralLineAssociatedBloodstreamInfection.aspx

31. Grady, N.P., Alexander, M., Burns, L.A., Dellinger, P., Graland, J., Heard, S.O., et al. (2011). Guidelines for the prevention of intravascular catheters-related infections, 2011. Retrieved from http://www.cdc.gov/hicpac/pdf/guidelines/bsi- guidelines-2011.pdf

32. Hu, K.K., Lipsky, B.A., Veenstra, D.L., Saint, S. (2004). Using maximal sterile barriers to prevent central venous catheter- related infection: A systematic evidence-based review. American Journal of Infection Control, 32, 142-146.

33. Grady, N.P., Alexander, M., Burns, L.A., Dellinger, P., Graland, J., Heard, S.O., et al. (2011). Guidelines for the prevention of intravascular catheters-related infections, 2011. Retrieved from http://www.cdc.gov/hicpac/pdf/guidelines/bsi- guidelines-2011.pdf

34. Marshall, J., Mermel, L.A., Classen, D., Arias, K.M., Podgorny, K., Anderson, D.J. (2008). Strategies to prevent central line- associated bloodstream infections in acute care hospitals. Infection Control & Hospital Epidemiology, 29, S22-S30.

35. Lederle, F.A., Parenti, C.M., Berskow, L.C., Ellingson, K.J. (1992). The central intravenous catheter. Annals of Internal Medicine, 116, 737-738.

36. Parenti, C.M., Lederle, F.A., Impola, C.L., Peterson, L.R. (1994). Reduction of unnecessary intravenous catheter use: Internal medicine house staff participate in a successful quality improvement project. Archives of Internal Medicine, 154, 1829-1832.

37. Grady, N.P., Alexander, M., Burns, L.A., Dellinger, P., Graland, J., Heard, S.O., et al. (2011). Guidelines for the prevention of intravascular catheters-related infections, 2011. Retrieved from http://www.cdc.gov/hicpac/pdf/guidelines/bsi- guidelines-2011.pdf

38. Marshall, J., Mermel, L.A., Classen, D., Arias, K.M., Podgorny, K., Anderson, D.J. (2008). Strategies to prevent central line- associated bloodstream infections in acute care hospitals. Infection Control & Hospital Epidemiology, 29, S22-S30.

39. Miller, S.E., Maragakis, L.L. (2012). Central line-associated bloodstream infection prevention. Current Opinion in Infectious Diseases, 25(4), 412-422.

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