Implementation of central line-associated bloodstream infection prevention bundles in a surgical intensive care unit using peer tutoring
Park et al. Antimicrobial Resistance and Infection Control
Implementation of central line-associated bloodstream infection prevention bundles in a surgical intensive care unit using peer tutoring
Sang-Won Park 0 1
Suhui Ko 1
Hye-sun An 1
Ji Hwan Bang 0 1
Woo-Young Chung 0 2
0 Department of Internal Medicine, Boramae Medical Center, Seoul National University College of Medicine , 20 Boramae-ro 5-Gil, Dongjak-gu, Seoul 07061 , Republic of Korea
1 Infection Control Office, Boramae Medical Center , Seoul , Republic of Korea
2 Intensive Care Units, Boramae Medical Center , Seoul , Republic of Korea
Background: Central line-associated bloodstream infections (CLABSIs) can be prevented through well-coordinated, multifaceted programs. However, implementation of CLABSI prevention programs requires individualized strategies for different institutional situations, and the best strategy in resource-limited settings is uncertain. Peer tutoring may be an efficient and effective method that is applicable in such settings. Methods: A prospective intervention was performed to reduce CLABSIs in a surgical intensive care unit (SICU) at a tertiary hospital. The core interventions consisted of implementation of insertion and maintenance bundles for CLABSI prevention. The overall interventions were guided and coordinated by active educational programs using peer tutoring. The CLABSI rates were compared for 9 months pre-intervention, 6 months during the intervention and 9 months post-intervention. The CLABSI rate was further observed for three years after the intervention. Results: The rate of CLABSIs per 1000 catheter-days decreased from 6.9 infections in the pre-intervention period to 2.4 and 1.8 in the intervention (6 m; P = 0.102) and post-intervention (9 m; P = 0.036) periods, respectively. A regression model showed a significantly decreasing trend in the infection rate from the pre-intervention period (P < 0.001), with incidence-rate ratios of 0.348 (95% confidence interval [CI], 0.98-1.23) in the intervention period and 0.257 (95% CI, 0.07-0.91) in the post-intervention period. However, after the 9-month post-intervention period, the yearly CLABSI rates reverted to 3.0-5.4 infections per 1000 catheter-days over 3 years. Conclusions: Implementation of CLABSI prevention bundles using peer tutoring in a resource-limited setting was useful and effectively reduced CLABSIs. However, maintaining the reduced CLABSI rate will require further strategies.
Central line-associated bloodstream infection; Intensive care unit; Education; Intervention; Learning by teaching; Peer tutoring
Central line-associated bloodstream infection (CLABSI)
is one of serious healthcare-associated infections that
cause increased medical costs, morbidity and mortality;
however, CLABSIs have been prevented in many
developed and developing countries using multifaceted
]. Several guidelines for the prevention of
CLABSIs are available, but the core contents of the
evidence-based recommendations are shared in common
]. Although the objectives of the CLABSI prevention
guidelines are evident and simple, the implementation of
these guidelines in clinical practices requires many
factors to be well-coordinated. Heterogeneity in compliance
or performance with the guidelines exists worldwide,
and interventions have not always been successful .
The importance of infection control in healthcare
settings for patient safety and quality of care cannot be
emphasized enough, but the available resources
including expert personnel, reimbursement systems and
managerial support are not always sufficient to deal
with many active issues in most healthcare facilities.
Different strategies for different regional or
institutional situations are needed for the successful
implementation of CLABSI prevention guidelines.
The education of and feedback from healthcare
workers are core components of implementing an
intervention program. The education component should be
organized in a manner that allows the healthcare
workers to collaborate, learn from, and support each
other. We used ‘learning by teaching method’-based
education to implement CLABSI prevention bundles in
a surgical intensive care unit (SICU) with a high CLABSI
rate. This peer tutoring approach was intended to
motivate the healthcare workers to actively participate in
their own workplace problems and to develop a safety
culture in the unit through the sharing of a common
Setting and subjects
This study was conducted in a surgical intensive care
unit at a 767-bed tertiary hospital. The SICU had 15
beds, and most of the beds were occupied by patients
from the neurosurgery and thoracic surgery
departments. The patient to nurse ratio was 3:1. The SICU did
not have a full-time intensivist responsible for overall
clinical care but instead had a medical director whose
main responsibility was administrative. All patients
admitted to the SICU during the study period were
included. The infection control office at the hospital
comprised one infectious diseases physician who
concurrently served as the director and one full-time and one
Study design and data collection
The primary goals of the intervention were to reduce
CLABSIs in a SICU and to maintain the reduced rate. The
secondary goals were to improve the perception of core
knowledge related to CLABSI prevention and to retain
compliance with the use of insertion and maintenance bundles.
This study consisted of three periods, a pre-intervention
period of 9 months (August 2011 to April 2012), an
intervention period of 6 months (May 2012 to October 2012),
and a post-intervention period of 9 months (November
2012 to July 2013). In addition, long-term follow-up of
CLABSIs was performed for 3 years after 2013, and the
infection control office intervened minimally during this
period as specified in the ‘Intervention Program’ section
below. The insertion bundle included hand hygiene,
maximal barrier precautions, chlorhexidine skin antisepsis, and
optimal catheter site selection with the subclavian vein
identified as the preferred site for insertion that were explained
in detail in previous reports [
1, 9, 10
]. The maintenance
bundle included hand hygiene, catheter site dressing, hub
care, and daily review of central line necessity [
1, 9, 10
catheter site dressing, either sterile gauze or transparent
semipermeable dressing was used and replaced every 2 days
and 1 week respectively if not otherwise indicated. The site
was disinfected with 2% chlorhexidine tincture. Before
accessing catheter hubs, 70% alcohol was used for cleansing
to reduce contamination.
Hand hygiene performance in the SICU was
monitored weekly by an infection control nurse using the
World Health Organization hand hygiene guide as a part
of hospital-wide surveillance [
]. As the monitoring has
a role of both measuring the performance and educating
the healthcare workers on the spot, feedback about the
hand hygiene performance was given to the health care
workers immediately on the spot and monthly to each
department. We only irregularly audit the hand hygiene
performance by pre-trained unrelated external personnel
to estimate the magnitude of Hawthorne effect for
reference only. The perception of core knowledge was
assessed for all nurses in the SICU. The survey consisted
20 questions total and was performed three times during
the intervention period of 6 months. Residents or
physicians in charge inserted catheter. The nurse in charge of
each patient assisted the procedure and before the
insertion, the nurse explained the checklist of insertion
bundle and checked the adherence. The default of bundle
was pointed out by the nurse in the middle of procedure
and the persistence of default was recorded in the
checklist. However, the nurse did not have the authority to
stop the procedure.
CLABSIs were defined as laboratory-confirmed
bloodstream infections in which a central line was in
place for >2 calendar days on the date of event, and
the line was in place on the date of the event or the
day before [
]. To capture data for infections
acquired during hospitalization only, the designation of
CLABSI was considered valid only if the positive
blood culture and clinical signs/symptoms of infection
occurred at least 48 h after admission. The infection
control office monitored the CLABSI events as well
as compliance with use of the central line bundles.
The number of pairs of blood cultures per 1000
patient-days was calculated during the study period to
monitor the appropriate ordering practices of blood
Regular team meetings between the infection control
office and the SICU were held to implement and
coordinate the CLABSI prevention bundles. The SICU team
included the director of the unit, the head nurse and all
of the working nurses. The infection control office
designed the overall CLABSI prevention bundles and
working programs and adjusted them based on the
feedback received at the regular meetings.
Implementation of the insertion and maintenance
bundles was initiated through education, which provided
working knowledge of the bundles, as well as individual
and group feedback related to bundle use adherence. The
educational sessions were conducted for all of the nurses
in the SICU and were taught using the ‘learning by
teaching’ or peer tutoring method in which the nurses
themselves prepared and delivered the lecture contents (Fig. 1).
After an initial introductory overview of the CLABSI
bundles by the infection control office, these 30-min weekly
educational sessions were held for 6 months (May 2012 –
Oct 2012). The content of the lecture given by each nurse
consisted of a repetitive summary of the core contents of
the CLABSI bundles followed by a detailed review of one
section of the published guidelines for the prevention of
intravascular catheter-related infections, which was
allocated to each lecturer [
]; a self-assessment of the
current departmental problems in view of the reviewed
content; and suggestions for possible solutions to these
problems. The educational sessions were designed such
that all of the SICU nurses served as lecturer, and the
nurses had the opportunity to actively study and discuss
the CLABSI-related problems. The framework of the
lecture was suggested by the infection control office. The
review sections included the guideline references to share
their scientific basis. All of the participants were
encouraged to discuss their problems or suggestions during every
session. To educate doctors and encourage their
cooperative compliance with the prevention bundles, separate
monthly meetings were held between the infection control
office and representative doctors from every clinical
department that used the SICU because there was no
intensivist or physician dedicated to patient care in the SICU.
Indirect education for all of the doctors in clinical
departments was performed through these representative
doctors using presentation materials created by the infection
control office. Regular group feedback and instant
individual feedback were given pertaining to the performance of
the CLABSI prevention checklists. The checklists used in
the insertion and maintenance bundles were incorporated
into the electronic medical record (EMR) system during
the interventional period, and then automatic data
collection in the infection control office and a short message
alert service for the removal of central catheters were
implemented. An all-in-one cart that had all of the necessary
items for central line insertion was prepared.
After the intervention period, systematically fixed
programs continued. There was weekly hand hygiene
monitoring. The performance of checklists in the insertion and
maintenance bundles of CLABSI prevention checked by
the nurses in the SICU was monitored through EMR by
the infection office, and the feedback for violation was
provided to individual healthcare workers daily and
clinical departments monthly. However, active educational
meetings were not held any more. There was no
systematic educational program about CLABSI bundle for new
nurses of SICU, but they were expected to learn from their
colleagues and fixed work pattern like daily checklists
embedded in the EMR system. For new residents or
physicians, educational material illustrated in a PowerPoint file
was provided monthly through their e-mail. Active audit
for the individual component of checklists on the spot
was not performed.
Comparisons of the CLABSI incidence rates during and
after the intervention period with that of the baseline
were analyzed by Poisson regression and are presented
with 95% confidence intervals (CIs). All statistical tests
were two-tailed, and P values <0.05 were considered
significant (SPSS 22.0; SPSS Inc., Chicago, IL, USA).
The rate of CLABSIs per 1000 catheter-days decreased
from 6.9 infections in the pre-intervention period to 2.4
and 1.8 in the intervention (6 m; P = 0.102) and
postintervention (9 m; P = 0.036) periods, respectively (Table 1
and Fig. 2). The regression model showed a significantly
decreasing trend in the infection rate from the
preintervention period (P < 0.001) with incidence-rate ratios of
0.348 (95% confidence interval [CI], 0.98–1.23) in the
intervention period and 0.257 (95% CI, 0.07–0.91) in the
post-intervention period. However, after the 9 months
post-intervention period, the yearly CLABSI rates reverted
to 3.0–5.4 per 1000 catheter-days (Table 1).
Adherence to each component in the insertion bundle
reached 100% in the 5th month. Adherence to each
component in the maintenance bundle reached 100% in
the 2nd month. The absolute amount of central line use
increased gradually but central line utilization ratio
taking patient-days into account has been steadily
decreasing since the initial rise during intervention period from
0.58 to 0.48 (Table 1). The places of central line
insertion during intervention (6 m) and post-intervention
(9 m) periods were operating room (58.6%),
interventional radiology (20.8%), SICU (16.4%), emergency room
(3.5%) and general ward (0.7%). The awareness of core
knowledge about CLABSI prevention practices during
the interventional period of 6 months increased, with
scores of 15.8 (1st month), 17.1 (3rd month), and 18.9
(6th month) points out of a total of 20 points for the
20question assessment. The performance of hand hygiene
which was monitored weekly were 93.4% (range, 92–96),
89.7% (range, 79–97) and 90.9% (range, 83–96) during
the pre-intervention, intervention and post-intervention
Twenty pathogens were responsible for the CLABSIs
during the 3 study periods, which totaled 24 months
(Table 2). In the pre-interventional period, the
predominant causative organisms were Enterococcus
species (20%), Acinetobacter baumannii (20%), and
coagulase-negative staphylococci (10%); one case each (5%)
of Staphylococcus aureus, viridans streptococci, Pseudomonas
aeruginosa and Stenotrophomonas maltophilia also occurred.
In the intervention and post-intervention periods, Candida
was the most common pathogen (4/6, 66.7%) of the 6 total
causative agents, though the total number of infections was
small. The Candida cases were not related to neutropenia.
The mean pairs of blood cultures per 1000 patient-days
during study periods were 201 (pre-intervention), 190
(intervention), and 196 (post-intervention).
Our intervention to reduce CLABSIs by implementing
CLABSI prevention bundles using peer tutoring was
effective during the interventional period of 6 months and
a post-interventional period of approximately 1 year.
However, without continuous active interactions and
dominating internal governance, the virtuous reduction
of CLABSIs was not sustained. Our educational method
had several advantages. Each healthcare worker had the
opportunity to voice her/his own work-related problems,
to hear from other colleagues, to understand the
principles behind their routine activities and to receive
responses to their problems. These factors minimized
resistance to the introduction of a new job pattern. The
purpose of the educational sessions was to motivate the
healthcare workers, to provide them with expert
knowledge for practical use and to improve knowledge
retention over longer time periods. Determining the most
effective educational method has been an area of utmost
interest for a long time. Generally, active participatory
education is more effective than passive learning.
‘Learning by teaching’ or peer tutoring is one of the
active participatory educational methods in which the core
idea is to have a pair or group of students teaching the
majority of topics to their classmates in a way that
encourages their classmates’ active participation and
communication in the best possible way [
Pyramids’ have shown that learners can retain
Central line utilization ratio
aCLABSI central line-associated bloodstream infection
bCLABSI rate CLABSI events per 1000 central line-days
approximately 90% of the content of a subject matter
when they teach the material to someone else.
The commitment of the infection control staffs to
coordinate the overall program and the presence of
governing leadership in the unit to maintain a level of practice
quality were basic components of the intervention.
aTwo cases were polymicrobial with A. baumannii + S. aureus and A.
baumannii + coagulase-negative staphylococci, respectively
Regardless of the strong positive aspects of our
educational approach, the intervention failed to sustain a
reduced CLABSI rate beyond 9 months post-intervention.
Several complex factors seem to be responsible for this
lack of sustainability. High job turnover in the unit
coupled with the lack of a continuing education system
for new nurses and doctors after the intervention period
likely weakened the effectiveness of the prevention
protocols. The turnover rates of nurses in the SICU were 24.9%
and 59.5% due to resignation, leave of absence and
rotation during intervention (6 m) and post-intervention
(9 m) periods. Thereafter, the rate was 39.1% - 46.8%
annually for 3 years. Interns or residents had a rotational
program every 1 or 2 months among 3 affiliated family
hospitals. The patient-to-nurse ratio of 1:3 was much
higher than the previously reported rate of 1:2 which was
a risk factor for CLABSIs [
]. Moreover, there was no
dedicated intensivist in the SICU who could have led and
maintained the program at the hospital.
Successful large-scale interventions with sustained
reductions in CLABSIs have been reported worldwide
2, 3, 5, 16, 17
]. In South Korea, there have been a few
single center or small-scale trials to reduce CLABSIs
]. The only recent multicenter interventional
study involving 58 ICUs in 26 hospitals funded by the
Korea Centers for Disease Control and Prevention
resulted in a CLABSI rate of 2.23 infections per 1000
catheter-days, which did not significantly improve the
preinterventional rate of 2.09 infections per 1000
catheterdays . There have been no reports about sustaining a
reduced CLABSI rate in South Korea. The distribution of
CLABSI pathogens in the pre-interventional period was
similar to recent Korean National Healthcare-associated
Infections Surveillance System (KONIS) data from 166
ICUs, which showed A. baumannii (14.6%) as second
most common pathogen of CLABSI in 2013 [
high number of A. baumannii infections in our study
might reflect high A. baumannii infection/colonization in
the SICU. Regarding relatively higher frequency of
candida infection during the intervention and the
immediate post-intervention periods, there were no changes of
antibiotics prophylaxis or strategies of treatment of
surgical site infection. The only systematic change was a use of
2% chlorhexidine tincture for skin disinfection before
catheter insertion and catheter site dressing instead of
10% povidone-iodine as a CLABSI bundle component.
Whether the chlorhexidine had weaker effect on candida
that on other bacterial pathogens requires further data
due to the small absolute number of candida infections in
our study, but previous studies about CLABSI have not
supported the role of chlorhexidine in candida infections.
There are diverse institutional situations and cultures
that deal with infection control programs and patient
safety issues. Although standard CLABSI prevention
guidelines are well-known, their translation into clinical
practice needs to be individualized according to regional
or institutional feasibility. Our educational method was
efficient in the initial implementation of the program
and effectively reduced the CLABSI rate for a short time
period of approximately one year. To maintain the
reduced rate, a multifaceted integrative approach must be
]. Intra-departmental or intra-unit effort
hardly maintained the effects of the program over a
longer time period. Our approach may not be effective in
certain situations, but it deserves to be considered by
institutions implementing a CLABSI prevention program
for the first time, especially in resource-limited settings.
Our study has some limitations. First, as this was a
single-center study, the effectiveness of our approach
may not be generalizable. However, one institutional
success may provide a good model for generalization, as
has been shown previously [
]. Second, we did not
perform a comparative study to prove the effectiveness
of the peer tutoring method. However, from a practical
point of view, it was a useful tool to guide the program
as it received the cooperation of the participants and
improved the understanding between healthcare workers.
Third, the indirect educational approach implemented
for doctors in the SICU might have weakened the effect
of the intervention. As residents from each clinical
department who were mainly involved in the insertion
procedure in the SICU rotated at 1 or 2 months interval
among 3 family hospitals, integrative successive group
education and follow-up assessment were impractical.
And maintenance bundles were mainly related to the
nurses. So, we decided to educate indirectly the doctors
through preceptors in each department who had regular
meetings with infection control office. The doctors had
individual feedbacks on the spot in the SICU for their
performance. Fourth, the performance of insertion
bundle might be incomplete. Operating room was the most
frequent place of central line insertion, but fully adopted
the insertion bundle only after intervention period. They
had been using a similar protocol except for skin
disinfection with 10% povidone-iodine and a small sized
drape. Emergency room (3.5%) and general ward (0.7%)
had no insertion bundle though the number was small.
A peer tutoring educational method was useful for the
implementation of CLABSI prevention bundles in a
SICU and effectively reduced infection rates for a short
time period of approximately 1 year. This approach is
applicable for hospitals with limited resources that are
trying to initiate prevention bundles. However, to
maintain the reduced CLABSI rates, resources support and
multifaceted cooperative approaches may be essential.
CIs: Confidence intervals; CLABSI: Central line-associated bloodstream
infection; EMR: Electronic medical record; SICU: Surgical intensive care unit
This work was supported by a clinical research grant-in-aid from the Seoul
Metropolitan Government - Seoul National University (SMG-SNU) Boramae
Medical Center (03–2012-3).
Availability of data and materials
The raw datasets analyzed during the current study period are available from
the authors of this article upon reasonable request.
SWP, SHK, and WYC designed the study. SWP, SHK, HAS, JHB and WYC
performed the intervention as well as collected and analyzed the data. SWP
and SHK wrote the manuscript. All of the authors read and approved the
Ethics approval and consent to participate
This study was approved by the Institutional Review Board at Boramae
Medical Center (06–2012-105). Collection of informed consent was waived
because this study was conducted as part of an institutional policy to
improve internal infection control and was retrospective in nature. All
personal identifiers were anonymized for confidentiality before data
processing. This research was in compliance with the Helsinki Declaration.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Submit your next manuscript to BioMed Central
and we will help you at every step:
1. Pronovost P , Needham D , Berenholtz S , Sinopoli D , Chu H , Cosgrove S , Sexton B , Hyzy R , Welsh R , Roth G , et al. An intervention to decrease catheter-related bloodstream infections in the ICU . N Engl J Med . 2006 ; 355 : 2725 - 32 .
2. Bion J , Richardson A , Hibbert P , Beer J , Abrusci T , McCutcheon M , Cassidy J , Eddleston J , Gunning K , Bellingan G , et al. ' Matching Michigan': a 2-year stepped interventional programme to minimise central venous catheter-blood stream infections in intensive care units in England . BMJ Qual Saf . 2013 ; 22 : 110 - 23 .
3. Berenholtz SM , Lubomski LH , Weeks K , Goeschel CA , Marsteller JA , Pham JC , Sawyer MD , Thompson DA , Winters BD , Cosgrove SE , et al. Eliminating central line-associated bloodstream infections: a national patient safety imperative . Infect Control Hosp Epidemiol . 2014 ; 35 : 56 - 62 .
4. Yaseen M , Al-Hameed F , Osman K , Al-Janadi M , Al-Shamrani M , Al-Saedi A , Al-Thaqafi A . A project to reduce the rate of central line associated bloodstream infection in ICU patients to a target of zero . BMJ Qual Improv Rep . 2016 . https://doi.org/10.1136/bmjquality.u212545. w4986 .
5. Marsteller JA , Sexton JB , Hsu YJ , Hsiao CJ , Holzmueller CG , Pronovost PJ , Thompson DA . A multicenter, phased, cluster-randomized controlled trial to reduce central line-associated bloodstream infections in intensive care units . Crit Care Med . 2012 ; 40 : 2933 - 9 .
6. Latif A , Halim MS , Pronovost PJ . Eliminating infections in the ICU: CLABSI . Curr Infect Dis Rep . 2015 ; 17 : 491 .
7. Ling ML , Apisarnthanarak A , Jaggi N , Harrington G , Morikane K , Thu le TA , Ching P , Villanueva V , Zong Z , Jeong JS , Lee CM . APSIC guide for prevention of central line associated bloodstream infections (CLABSI) . Antimicrob Resist Infect Control . 2016 ; 5 : 16 .
8. Valencia C , Hammami N , Agodi A , Lepape A , Herrejon EP , Blot S , Vincent JL , Lambert ML . Poor adherence to guidelines for preventing central lineassociated bloodstream infections (CLABSI): results of a worldwide survey . Antimicrob Resist Infect Control . 2016 ; 5 : 49 .
9. Marschall J , Mermel LA , Classen D , Arias KM , Podgorny K , Anderson DJ , Burstin H , Calfee DP , Coffin SE , Dubberke ER , et al. Strategies to prevent central line-associated bloodstream infections in acute care hospitals . Infect Control Hosp Epidemiol . 2008 ; 29 ( Suppl 1 ): S22 - 30 .
10. O 'Grady NP , Alexander M , Burns LA , Dellinger EP , Garland J , Heard SO , Lipsett PA , Masur H , Mermel LA , Pearson ML , et al. Guidelines for the prevention of intravascular catheter-related infections . Clin Infect Dis . 2011 ; 52 : e162 - 93 .
11. World Health Organization. WHO Guidelines on hand hygiene in health care . http://apps.who.int/iris/bitstream/10665/44102/1/9789241597906_eng. pdf. 2009. Accessed 1 Aug 2017 .
12. Centers for Disease Control and Prevention. Bloodstream infection event (central line-associated bloodstream infection and non-central lineassociated bloodstream infection) . http://www.cdc.gov/nhsn/pdfs/ pscmanual/4psc_clabscurrent.pdf. 2017. Accessed 1 Aug 2017 .
13. Baron EJ , Weinstein MP , Dunne WM Jr, Yagupsky P , Welch DF , Wilson DM. Cumitech 1C: Blood cultures IV . Washington DC: ASM Press; 2005 .
14. Grzega J , Schöner M. The didactic model LdL (Lernen durch Lehren) as a way of preparing students for communication in a knowledge society . J Educ Teach . 2008 ; 34 : 167 - 75 .
15. Fridkin SK , Pear SM , Williamson TH , Galgiani JN , Jarvis WR . The role of understaffing in central venous catheter-associated bloodstream infections . Infect Control Hosp Epidemiol . 1996 ; 17 : 150 - 8 .
16. Palomar M , Alvarez-Lerma F , Riera A , Diaz MT , Torres F , Agra Y , Larizgoitia I , Goeschel CA , Pronovost PJ , Bacteremia Zero Working G. Impact of a national multimodal intervention to prevent catheter-related bloodstream infection in the ICU: the Spanish experience . Crit Care Med . 2013 ; 41 : 2364 - 72 .
17. Pronovost PJ , Watson SR , Goeschel CA , Hyzy RC , Berenholtz SM . Sustaining reductions in central line-associated bloodstream infections in Michigan intensive care units: a 10-year analysis . Am J Med Qual . 2016 ; 31 : 197 - 202 .
18. Kim OS , Kim SM . Prevention of central venous catheter-related infections . Korean J Nosocomial Infect Control . 1999 ; 4 : 35 - 40 .
19. Yoo S , Ha M , Choi D , Pai H . Effectiveness of surveillance of central catheterrelated bloodstream infection in an ICU in Korea . Infect Control Hosp Epidemiol . 2001 ; 22 : 433 - 6 .
20. Lee DH , Jung KY , Choi YH . Use of maximal sterile barrier precautions and/or antimicrobial-coated catheters to reduce the risk of central venous catheter-related bloodstream infection . Infect Control Hosp Epidemiol . 2008 ; 29 : 947 - 50 .
21. Yoo S , Jung SI , Kim GS , Lim DS , Sohn JW , Kim JY , Kim JE , Jang YS , Jung S , Pai H . Interventions to prevent catheter-associated blood-stream infections: A multicenter study in Korea . Infect Chemother . 2010 ; 42 : 216 - 22 .
22. Yoon YK , Lee SE , Seo BS , Kim HJ , Kim JH , Yang KS , Kim MJ , Sohn JW . Current status of personnel and infrastructure resources for infection prevention and control programs in the Republic of Korea: A national survey . Am J Infect Control . 2016 ; 44 : e189 - 93 .
23. Choi JY , Kwak YG , Yoo H , Lee SO , Kim HB , Han SH , Choi HJ , Kim HY , Kim SR , Kim TH , et al. Trends in the distribution and antimicrobial susceptibility of causative pathogens of device-associated infection in Korean intensive care units from 2006 to 2013: results from the Korean Nosocomial Infections Surveillance System (KONIS) . J Hosp Infect . 2016 ; 92 : 363 - 71 .
24. Berenholtz SM , Pronovost PJ , Lipsett PA , Hobson D , Earsing K , Farley JE , Milanovich S , Garrett-Mayer E , Winters BD , Rubin HR , et al. Eliminating catheter-related bloodstream infections in the intensive care unit . Crit Care Med . 2004 ; 32 : 2014 - 20 .