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Original Article

Korean J healthc assoc Infect Control Prev 2023; 28(1): 113-125

Published online June 30, 2023 https://doi.org/10.14192/kjicp.2023.28.1.113

Copyright © Korean Society for Healthcare-associated infection Control and Prevention

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Epidemiology of Catheter-related Bloodstream Infections in Neonatal Intensive Care Units: A Rapid Systematic Literature Review

Erdenetuya Bolormaa1*, Choryok Kang2*, Young June Choe3,4 , Joo Seon Heo3,5, Hannah Cho3

Department of Preventive Medicine, Korea University College of Medicine1, College of Nursing, Seoul National University2, Department of Pediatrics, Korea University Anam Hospital3, Allergy and Immunology Center, Korea University4, Institute of Nano, Regeneration, Reconstruction, Korea University College of Medicine, Korea University5, Seoul, Korea

Correspondence to: Young June Choe
E-mail: choey@korea.ac.kr
ORCID: https://orcid.org/0000-0003-2733-0715

*Equally contributed to the manuscript.

Received: March 15, 2023; Revised: April 28, 2023; Accepted: May 8, 2023

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0).

Abstract

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Background: Catheter-related bloodstream infections (CRBSIs) are serious complications in neonatal intensive care units (NICUs). We aimed to assess the incidence of CRBSIs in NICUs worldwide and describe the causative organisms.
Methods: We searched PubMed, EMBASE, Cochrane, and KoreaMed databases. We included studies on CRBSIs in NICU settings with data on bacteremia. We performed a random-effects meta-analysis on CRBSI incidence in NICUs, stratified the data according to WHO regions. We compiled data on underlying organisms.
Results: Of the 692 studies identified, 71 published between 2011 and 2022 were considered eligible. The pooled incidence of CRBSI per 1000 catheter days in NICUs was 8.66 (95% confidence interval [CI], 7.19; 10.12). Stratifying by WHO regions, the CRBSI incidence per 1000 catheter days was 10.38 (95% CI, 3.86; 16.90) in the Eastern Mediterranean Region (EMR), 11.77 (95% CI, 9.20; 14.35) in the European Union Region (EUR), 5.94 (95% CI, 3.87; 8.00) in the Western Pacific Region (WPR), and 6.71 (95% CI, 4.39; 9.03) in the Region from the Americas (AMR). Of the 2887 bacterial strains, 73.4% (n=2118) were gram-positive bacteria, 18.9% (n=547) were gram-negative bacteria, and 7.8% (n=225) were fungi. Coagulasenegative Staphylococci (n=1380, 65.2%) were the most common pathogen among the grampositive types, followed by Staphylococcus aureus (n=318, 15%). Among the CRBSI gramnegative cultures, Klebsiella spp. (n=201, 36.7%) was the primary pathogen.
Conclusion: We found a substantial burden of CRBSIs in NICUs across the globe. Our findings highlight the need to improve the implementation of global and local strategies to reduce CRBSIs in NICUs.

Keywords: Neonate, Bacteremia, Catheters, Infection control, Systematic review

INTRODUCTION

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Central venous catheters are commonly used to administer medications and parenteral nutrition to vulnerable neonates in neonatal intensive care units (NICUs) [1]. A common and serious complication of central venous catheters is a catheter-related bloodstream infection (CRBSI), which is the most common cause of late-onset sepsis and has an estimated mortality rate of 70% in infants [2]. Neonates are highly vulnerable to CRBSIs in NICUs; however, incidence estimates are lacking in many countries.

A previous systematic review and meta-analysis investigated the incidence of neonatal sepsis [3]; however, no systematic review on the global incidence of CRBSIs limited to NICU settings has been reported to date. The study sought to review neonatal sepsis and mortality across low- and middle-income countries; however, this is not specific to CRBSIs in the NICU [3]. Furthermore, no regional comparative study has investigated the incidence of CRBSIs in NICUs.

We conducted a systematic literature review to assess the incidence of CRBSIs in NICUs worldwide and describe the causative organisms. We aimed to assess the global incidence of CRBSI, particularly in NICUs, and compile data on causative pathogens.

MATERIALS AND METHODS

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1. Search strategy

We searched PubMed, EMBASE, Cochrane, and KoreaMed databases using the following keywords: “catheter-related infection”, “CVC infection”, “CVC-related infection”, “CVC associated infection”, “central line infection”, “central line related infection”, “central line-associated infection”, “bacteremia”, “bloodstream infection”, “neonatal intensive care”, “NICU”, “infant”, “neonate”, “newborn”, “newly born infant”, “neonatal infant”, “premature infant”, “preterm infant”, “low birth weight infant”, “LBW infant”, and “CRBSI”. We combined these terms with “AND” or “OR” when searching the databases. The search was performed on December 9, 2022.

2. Selection criteria

Studies were reviewed by their titles and abstracts in the first screening and by full-textarticles in the second screening. The inclusion criteria were as follows: (1) the research participants included patients with CRBSIs, (2) all patients must have been admitted to the NICU, (3) the research participants had received no prior interventions, (4) the research was about microorganisms, and (5) the study was published in English. The exclusion criteria were as follows: (1) the study was duplicated, (2) the data could not be extracted or converted for useful data, (3) the studies were case reports, roundtable meeting reports, conference reports, or reviews, (4) the study was published in languages other than English, and (5) the results were incomplete.

3. Data extraction

The information about the first author, published year, research time, country, data collection method, total patients in NICUs, total patients with CRBSIs, total catheter days, and total distribution of species and types of microorganisms was extracted by the review investigator with Microsoft Office Excel 2010.

4. Statistical analysis

The proportion of extracted data, the proportion of pathogens, and the pooled incidence and its 95% confidence intervals were analyzed using a meta package of R 4.2.2. A random effects model was chosen based on the heterogeneity and significance tests (P<.05, I2>50%). A subgroup analysis of regions divided by the World Health Organization (WHO) was conducted.

RESULTS

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1. Study selection

A total of 692 studies were first screened by their titles and abstracts. and 331 were selected for the next full-text screening. Among those, 97 studies did not involve patients with CRBSIs in NICUs, 9 recruited intervention participants, 2 studies were reviews, 9 were written in French and Chinese languages, and 143 did not have useful data for our meta-analysis of CRBSI incidence. Finally, 71 studies [4-74] were eligible for our analysis. We depicted the flowchart of the selection of surveys in Fig. 1.

Figure 1. Flowchart of the study selection.
Abbreviations: NICU, neonatal intensive care unit; CRBSI, catheter-related bloodstream infection.

Table 1 describes the selected studies on CRBSIs in NICUs.

Table 1 . The characteristics of studies included in this systematic review

Ref No.StudyNo. of subjectsStudy designCountryStudy yearStudy populationCLABSI preventionIncidence/1000 catheter-days
[4]Al-Mousa et al.671Prospective cohortKuwait2013-2015Neonatal patientsNone15.3
[5]Almeida et al.*1194RetrospectivePortugal2007-2010Newborn infantsPreventive bundle14.1
[6]Arnts et al.*45Prospective observationalNetherland2009-2010Newborn infantsPreventive bundle12.9
[7]Bannatyne et al.*406Retrospective cohortAustralia2011-2013Newborn infantsPreventive bundle8.8
[8]Bierlaire et al.*140ProspectiveBelgium2019NeonatesPreventive bundle8.4
[9]Blanchard et al.Retrospective cohortCanada2007-2011Neonatal patientsNone4
[10]Bolat et al.569Prospective, cohortTurkey2009-2011Neonatal patientsNone3.64
[11]Boutaric et al.*111ProspectiveFrance2004-2006Premature infantsPreventive protocol16
[12]Bunni et al.*311RetrospectiveUK2009NeonatesPreventive bundle22.4
[13]Cabrera et al.167ProspectivePeru2017-2018NeonatesNone8
[14]Callejas et al.689RetrospectiveCanada2010-2013NeonatesNone5.6
[15]Chandonnet et al.*ProspectiveUSA2011Neonatal patientsPreventive bundle2.6
[16]Cheng et al.123Retrospective cohortChina2011-2012NeonatesNone4.99
[17]Cheong et al.39RetrospectiveJapan2013VLBW infantsNone3.57
[18]Cleves et al.1246Retrospective, quasi-experimentalUSA2012-2014NeonatesChlorhexidine baths8.64
[19]Dumpa et al.*68Retrospective reviewUSA2009-2010Neonatal patientsPreventive bundle4.4
[20]Erdei et al.*ProspectiveUSA2009Newborn infantsPreventive bundle4.1
[21]Ereno et al.107RetrospectiveSingaporeNeonatal patientsNone5.9
[22]Flidel-Rimon et al.*141ProspectiveIsrael2011-2012InfantsPreventive bundle15.2
[23]Fontela et al.Retrospective dynamic cohortAustralia2003-2009Neonatal patientsNone4.4
[24]Freeman et al.*285RetrospectiveUSA2005-2012Neonatal patientsPrevention protocol1.69
[25]Freitas et al.1560Prospective cohortBrazil2014-2016NeonatesNone18.6
[26]Gadallah et al.434Prospective cohortEgypt2012NeonatesNone158.3
[27]Gerver et al.RetrospectiveUK2016-2017NeonatesNone1.5
[28]Greenhalgh et al.176Retrospective cohortAustralia2012NeonatesNone11.5
[29]Hei et al.131ProspectiveChina2008-2011Neonatal patientsNone13.7
[30]Helder et al.*537Prospective, observationalNetherland2014-2016InfantsAntiseptic protocol3.1
[31]Hocevar et al.RetrospectiveUSA2006-2008NeonatesNone3.9
[32]Holzmann-Pazgal et al.*RetrospectiveUSA2006-2008NeonatesLine team11.6
[33]Hussain et al.301ProspectivePakistan2016Neonatal patientsPreventive bundle17.1
[34]Hussain et al.2046RetrospectivePakistan2011-2015Neonatal patientsNone8.9
[35]Jansen et al.180Retrospective cohortNetherland2015-2019Preterm neonatesNone14
[36]Jansen et al.891Retrospective cohortNetherland2012-2020Preterm neonatesNone13.4
[37]Jeong et al.*326RetrospectiveKorea2011-2013Neonatal patientsPreventive bundle6.6
[38]Kim et al.Retrospective reviewKorea2016-2020InfantsNone2.85
[39]Kinoshita et al.2383Prospective observationalJapan2014-2017VLBW infantsNone2.1
[40]Kleinlugtenbeld et al.*75ProspectiveNetherland2007Premature newbornPreventive bundle20.1
[41]Kourkouni et al.ProspectiveGreeceNeonatal patientsNone6.58
[42]Kulali et al.*70Prospective cohortTurkey2016-2017Neonatal patientsPreventive bundle12.4
[43]Leblebicioglu et al.3430ProspectiveTurkey2003-2012Neonatal patientsNone21
[44]Leistner et al.5586Prospective cohortGermany2008-2009VLBW infantsNone8.3
[45]Leveillee et al.1577Retrospective cohortCanada2011-2016NeonatesNone8.4
[46]Milstone et al.3967Retrospective cohortUSA2005-2010NeonatesNone1.66
[47]Mohamed Cassim et al.*350UK2010-2011Newborn infantsPreventive bundle4.3
[48]Nercelles et al.4704ProspectiveChile2005-2011Newborn infantsNone0.9
[49]Nielsen et al.382RetrospectiveDenmark2019-2020Neonatal patientsNone13.41
[50]Oh et al.429RetrospectiveKorea2017InfantsPreventive bundle1.89
[51]Patrick et al.*Prospective cohortUSA2007-2012Neonatal patientsNone2.1
[52]Pavcnik-Arnol et al.Prospective cohortSlovenia2011-2012Neonatal patientsNone5.5
[53]Pharande et al.*13731ProspectiveAustralia2002-2016Newborn infantsPreventive bundle12.04
[54]Piazza et al.RetrospectiveUSA2011Neonatal patientsNone1.333
[55]Ponnusamy et al.189Prospective observationalUK2009-2010InfantsNone16.9
[56]Rallis et al.*94ProspectiveGreece2012NeonatesPreventive bundle12
[57]Resende et al.*551ProspectiveBrazil2010-2011InfantsPreventive bundle23
[58]Rosenthal et al.*2009Prospective surveillanceEl Salvador, Mexico, Philippines, Tunisia2003Neonatal patientsPreventive bundle21.4
[59]Salm et al.*3028Prospective cohortGermany2007-2009VLBW infantsPreventive bundle13.47
[60]Sanderson et al.4248ProspectiveAustralia2007-2009InfantsNone10.6
[61]Shalabi et al.540Retrospective matched cohortCanada2010-2013InfantsNone8.5
[62]Shepherd et al.*USA2003-2006InfantsPreventive bundle6
[63]Sinha et al.*152RetrospectiveUK2007Preterm neonatesPreventive bundle26.5
[64]Soares et al.251Retrospective cohortPortugal2014-2016Neonatal patientsNone12.4
[65]Steiner et al.*526ProspectiveGermany2010-2012VLBW infantsPreventive bundle8.96
[66]Taylor et al.83Retrospective, quasi-experimentalAustralia2013-2017InfantsNone13.8
[67]Ting et al.*Retrospective observationalCanada2007-2008NeonatesPreventive bundle7.9
[68]Wen et al.301ProspectiveChina2010-2014Premature infantsNone1.9
[69]Wilder et al.*USA2011Neonatal patientsPreventive bundle3.9
[70]Worth et al.ProspectiveAustralia2008-2016Neonatal patientsNone2.2
[71]Yalaz et al.1200ProspectiveTurkey2008-2010Newborn infantsNone4.1
[72]Yumani et al.369RetrospectiveNetherland2007Neonatal patientsNone18.1
[73]Zachariah et al.Cross-sectionalUSA2011Neonatal patientsNone1.52
[74]Zhou et al.29ProspectiveChina2008-2010NewbornsPreventive bundle16.7

*Estimated only pre-intervention period CLABSI rate.

Abbreviation: VLBW, very low birth weight.

2. Study characteristics

The 71 eligible studies were published from 2011-2022, mainly concentrated in 2012-2016. The surveys were conducted between 2002 and 2020. Dividing the studies by WHO regions, 22 (30.9%) were from the Region from the Americas (AMR) [9,13-15,18-20,24,25,31,32,45,46, 48,51,54,57,61,62,67,69,73], 5 (7.0%) from the Eastern Mediterranean Region (EMR) [4,26,33,34,58], 27 (38.0%) from the European Union Region (EUR) [5,6,8, 10-12,22,27,30,35,36,40-44,47,49,52,55,56,59,63-65,71,72], and 17 (23.9%) from the Western Pacific Region (WPR) [7,16,17,21,23,28,29,37-39,50,53,60,66,68, 70,74].

Most studies were from the United States (n=13, 18.3%) [15,18-20,24,31,32,46,51,54,62,69,73], Australia (n=7, 9.9%) [7,23,28,53,60,66,70], and the Netherlands (n=6, 8.5%) [6,30,35,36,40,72]. Regarding the methodology, 50.7% (n=36) were retrospective and 45.1% (n=32) were prospective studies. We included 63 082 patients in NICUs, except for 17 studies that did not provide information on the total number of patients with catheters.

3. The incidence of CRBSI

We estimated the pooled incidence of CRBSI per 1000 catheter days in NICUs by dividing the regions into subgroups. The CRBSI incidence per 1000 catheter days was 10.38 in the EMR (95% CI, 3.86; 16.90), 11.77 (95% CI, 9.20; 14.35) in the EUR, 5.94 (95% CI, 3.87; 8.00) in the WPR, and 6.71 (95% CI, 4.39; 9.03) in the AMR, and the total weighted CRBSI incidence per 1000 catheter days was 8.66 (95% CI, 7.19; 10.12) (Fig. 2).

Figure 2. Forest plot for catheter-related bloodstream infections per 1000 catheter days in the different World Health Organization regions, 2002-2020. (A) Eastern Mediterranean, Europe, (B) Western Pacific and Americas.
Abbreviations: EMR, Eastern Mediterranean Region; EUR, European Union Region; WPR, Western Pacific Region; AMR, Region from America.

Fig. 3 shows the trend of CRBSI per 1000 catheter days by an identified period of surveillance. The incidence of CRBSI per 1000 catheter days was 0.0-26.5, 1.9-23, and 1.5-17.1 in 2006-2010, 2011-2015, and 2016-2020, respectively.

Figure 3. Trend of catheter-related bloodstream infections per 1000 catheter days in neonatal intensive units by surveillance periods.

4. Distribution of pathogenic microorganisms

A total of 2887 bacterial strains were isolated from CRBSI samples. Among these, 73.4% (n=2118) were gram-positive bacteria, 18.9% (n=547) were gram-negative bacteria, and 7.8% (n=225) were fungi. Coagulase-negative Staphylococci (n=1380, 65.2%) was the most common pathogen among the gram-positive type, followed by Staphylococcus aureus (n=318, 15%), Enterococcus spp. (n=166, 7.8%), Staphylococcus epidermidis (n=88, 4.2%), and Enterococcus faecalis (n=64, 3%). Among the CRBSI gram-negative cultures, Klebsiella spp. (n=201, 36.7%) was the primary pathogen, followed by Escherichia coli (n=96, 17.6%) and Enterobacter spp. (n=64, 11.9%). Candida species (n=170, 75.6%) was primarily isolated among the fungi, and Candida albicans (n=33, 14.7%) and Candida parapsilosis (n=10, 4.4%) were most frequent among the CRBSI fungi isolates (Table 2).

Table 2 . The proportion of pathogen related to catheter-related bloodstream infection in neonatal intensive care unit (2006-2020)

Total pathogens (n=2887)Frequency (%)
Gram-positive (n=2118)
Coagulase-negative Staphylococci1380 (65.2)
Staphylococcus epidermidis88 (4.2)
Staphylococcus capitis14 (0.7)
Staphylococcus aureus333 (15.7)
Methicillin-resistant Staphylococcus aureus14 (0.7)
Methicillin-sensitive Staphylococcus aureus10 (0.5)
Enterococcus spp.166 (7.8)
Enterococcus faecalis64 (3)
Streptococcus spp.19 (0.9)
Bacillus spp.11 (0.5)
Other gram-positive19 (0.9)
Gram-negative (n=547)
Klebsiella spp.201 (36.7)
Klebsiella pneumoniae37 (6.8)
Escherichia coli96 (17.6)
Enterobacter spp.65 (11.9)
Enterobacter cloacae6 (1.1)
Pseudomonas aeruginosa32 (5.9)
Acinetobacter baumannii24 (4.4)
Serratia marcescens19 (3.5)
Citrobacter freundii5 (0.9)
Burkholderia cepacia3 (0.5)
Pseudomonas fluorescens2 (0.4)
Stenotrophomonas maltophilia2 (0.4)
Citrobacter koseri2 (0.4)
Other gram-negative53 (9.7)
Fungi (n=225)
Candida spp.170 (75.6)
Candida albicans33 (14.7)
Candida parapsilosis10 (4.4)
Candida guillermondii5 (2.2)
Candida lusitaniae3 (1.3)
Candida tropicalis2 (0.9)
Candida glabrata2 (0.9)


Gram-positive species were the most common pathogen type among CRBSI incidences in all three regions in our study, with proportions of 70% in the AMR, 76% in the WPR, and 84% in the EUR. Fig 4 describes the proportions of pathogen types among the subgroups of WHO regions. Among the EMR region surveys, no survey isolated pathogenic species. Approximately 20%, 21%, and 14% of the strains were gram-negative in the AMR, WPR, and EUR, respectively. Fungi was isolated in only 2% in EUR, 10% in AMR, and 3% in WPR.

Figure 4. The proportions of pathogens identified from catheter-related bloodstream infections in different World Health Organization regions, 2006-2016.
Abbreviations: AMR, Region from America; WPR, Western Pacific Region; EUR, European Union Region.

DISCUSSION

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We analyzed a total of 71 studies and showed a substantial burden of CRBSIs in NICUs globally; however, our review was limited by a vast difference in terms of incidence rate, necessitating a standardized investigative method to report CRBSIs in NICUs. According to the National Healthcare Safety Network in the United States, only CLABSI in children ≤1 year is defined, which may not be suitable for neonates due to differences in the symptoms of infection [75]. This should motivate global researchers to define local NICU CRBSI definitions according to the standardized recommendations and sustainably implement such preventive measures. In this context, a modified case definition for CRBSI in NICU settings should be adapted from the previously defined “catheter-related bloodstream infection” or “central line-associated bloodstream infection” [76].

This systematic literature review is the first to investigate the global incidence of CRBSIs in NICUs. We estimated the CRBSI incidence with stratification according to WHO regions and identified regional differences in CRBSI incidence. In this study, incidence estimates were higher in the EMR and EUR than in the WPR and AMR. This finding indicates that the need to reduce CRBSIs in NICUs is greater in the EMR and EUR. Data from the African and Southeast Asian regions were not included in this study, which might lead to knowledge gaps on the global incidence of CRBSIs in NICUs. The incidence of neonatal sepsis is reported to be very high in the African region; however, the majority of hospital-wide and ICU-based studies have been conducted in high-income regions such as the European and American WHO regions [77]. Therefore, further studies are required to investigate the data from the African and Southeast Asian regions.

Furthermore, we found a downward trend in the incidence of CRBSIs in NICUs across countries. This may be explained by the adoption of CRBSI prevention bundles at multiple sites; however, this could not be determined from the current dataset. We propose a longitudinal analysis in defined clinical settings to investigate the role of prevention bundles in the incidence of CRBSIs in NICUs at different times.

In our study, the most common causative pathogens of CRBSIs in NICUs were coagulase-negative Staphylococci, Staphylococcus aureus, and Klebsiella spp. Our findings are consistent with a relevant study that estimated the global incidence of neonatal sepsis. This systematic review reported that the most commonly identified pathogens of neonatal sepsis were Staphylococcus aureus and Klebsiella spp. [3]. However, this review did not focus on NICU-based studies, and our study is the first to report the causative pathogens of CRBSI in NICUs worldwide.

Reducing neonatal mortality is an important component of the third Sustainable Development Goal. It is essential to understand the wide variability in neonatal health outcomes, particularly in NICUs across the globe. A recent systematic review showed that West and Central Africa and South Asia had the highest neonatal mortality rates in 2017, despite improvements from the 1990s [78]. A vast difference in neonatal mortality due to infectious causes between high- and low-income countries and regions is an important issue since the regionalization of neonatal healthcare is emphasized [79]. In this context, our study showed that neonatal CRBSI incidence was variable across countries, particularly in different settings. Higher incidences were observed in the Eastern Mediterranean and European regions compared to those of the Western Pacific and American regions. This difference may be explained by the access to facilities for newborns, as previously described [80].

Our study was limited by the variability among individual studies, resulting in heterogeneity of the synthesized data, which required careful interpretation. Despite our broad search strategy with a focus on CRBSIs in NICUs, data from the African and Southeast Asian regions were not included in our study. This may be explained by a lack of epidemiological data, deficiencies in healthcare organizations and resources, and institutional obstacles to delivering critical care in the resource-limited settings of low-income countries. A recent systematic review showed that West and Central Africa and South Asia had the highest neonatal mortality rates in 2017, despiteimprovements from the 1990s [81]. Reducing neonatal mortality is an important component of the third Sustainable Development Goal. It is essential to understand the wide variability in neonatal health outcomes, particularly in NICUs across the globe.

We found a variable incidence of CRBSIs in NICUs globally, with a downward trend over the past 15 years; however, the substantialdisease burden remains among newborns. Our findings highlight the need to improve the implementation of global and local strategies to reduce CRBSIs in NICUs. Future research is required to address the knowledge gaps identified by our study.

ACKNOWLEDGEMENTS

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This study was supported by the Korean Society for Healthcare-Associated Infection Control and Prevention in 2021.

DISCLOSURE OF CONFLICT OF INTEREST

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The authors have no potential conflict of interest to disclose.

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