Pathogen-Specific Clustering of
Nosocomial Blood Stream Infections
in Very Preterm Infants
Felix Reichert, MD,a Brar Piening, MD,b Christine Geffers, MD,b Petra
Gastmeier, MD,b Christoph Bührer, MD,a Frank Schwab, PhDb
BACKGROUND AND OBJECTIVES: Nosocomial infections in NICUs tend to cluster, sometimes as
abstract
devastating outbreaks, but pathogen-specific transmission probabilities are unknown. We
aimed to quantify the pathogen-specific risk of a blood stream infection (BSI) in preterm
infants after an index case with that pathogen in the same department.
METHODS: Data of 44 818 infants below 1500 g birth weight of the German NICU surveillance
system (2000–2011) were used to calculate the probability of a BSI in the presence or
absence of another infant in the same unit with a same-pathogen BSI.
RESULTS: The relative risk was similar for the more common pathogens, Enterococcus
spp (4.3; 95% confidence interval: 2.7–6.9; n = 243), Enterobacter spp (7.9, 5.4–11.4; n
= 246), Escherichia coli (7.9; 5.1–12.1; n = 210), Candida albicans (8.7; 5.0–15.4; n = 138),
Staphylococcus aureus (9.5; 7.6–12.1; n = 407) and Klebsiella spp (13.1; 9.0–19.1; n = 190) but
markedly elevated for Serratia spp (77.5; 41.1–146.1; n = 58) and Pseudomonas aeruginosa
(64.5; 25.7–162.1; n = 38). Rates of BSI per 100 exposed infants ranged between 2.21
(Enterococcus) and 8.15 (Serratia). The same pattern emerged after adjustments were made
for patients’ characteristics or when the analysis was restricted to positive blood cultures
during the preceding 30 days.
CONCLUSIONS: Although BSIs with P aeruginosa or Serratia spp in preterm infants are rare,
they are associated with a markedly elevated risk of secondary same-pathogen BSI and
should prompt intensified active surveillance and infection control measures.
aDepartment of Neonatology, and bInstitute for Hygiene and Environmental Medicine, Charité University Medical
Center, Berlin, Germany
Dr Reichert drafted the initial manuscript, scrutinized the literature, and critically reviewed
the manuscript; Drs Piening and Geffers coordinated and supervised the data collection, were
involved in the design of the study, and critically reviewed the manuscript; Dr Gastmeier designed
the data collection instruments, supervised the nosocomial infection surveillance system,
was involved in the conceptualization of the study, and critically reviewed the manuscript; Dr
Bührer was involved in the extension of the study, suggested methods to analyze the data,
and wrote the manuscript; Dr Schwab conceptualized and designed the study, carried out the
statistical calculations, and critically reviewed the manuscript; and all authors approved the final
manuscript as submitted.
WHAT’S KNOWN ON THIS SUBJECT: Nosocomial
infections in neonatal intensive care tend to run in
clusters. Calculating pathogen-specific transmission
probabilities requires large databases.
WHAT THIS STUDY ADDS: The relative risk for a
same-pathogen blood stream infection after an
index case in the same unit is markedly elevated
for Pseudomonas aeruginosa and Serratia spp, as
compared with other pathogens.
DOI: 10.1542/peds.2015-2860
Accepted for publication Jan 5, 2016
Address correspondence to Christoph Bührer, MD, Klinik für Neonatologie, Charité
Universitätsmedizin Berlin, D-13344 Berlin, Germany. E-mail: [email protected]
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
To cite: Reichert F, Piening B, Geffers C, et al. PathogenSpecific Clustering of Nosocomial Blood Stream Infections
in Very Preterm Infants. Pediatrics. 2016;137(4):e20152860
Copyright © 2016 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant
to this article to disclose.
PEDIATRICS Volume 137, number 4, April 2016:e20152860
ARTICLE
In very low birth weight preterm
infants, nosocomial blood stream
infections (BSIs) are associated with
substantial morbidity and mortality.
BSI with the most commonly isolated
organisms in BSI, coagulase-negative
staphylococci (CoNS) display a
rather benign clinical course.1,
2 CoNS are part of the normal
skin flora, and rates of BSI with
CoNS have been found to decline
after implementation of improved
handling of central venous lines.2,3
In contrast, BSIs with Staphylococcus
aureus, gram-negative rods, or fungi
have a high mortality risk,4 with
Pseudomonas aeruginosa and Serratia
marcescens figuring prominently.2,
3,5,6 Horizontal transmissions of
these pathogens in NICUs may cause
difficult-to-control outbreaks.
BSIs and outbreaks with nonCoNS pathogens, while potentially
devastating for the affected infants
or units, respectively,7–11 still occur
mostly in a sporadic fashion. Thus,
there is a need for a sufficiently large
database to calculate and compare
the BSI clustering probability for
specific pathogens. We used the data
from the German national neonatal
infections surveillance system1,10,
12,13 to estimate the probability of a
hospitalized very low birth weight
(<1500 g) infant to develop a BSI
with a particular pathogen when
another infant previously diagnosed
with a BSI of the same pathogen was
being cared for in the same unit. We
also calculated the probability of
contracting a BSI with a particular
pathogen after an index case during
the preceding 30 days in the same
department.
METHODS
Methods and definitions employed
by the German national neonatal
infection surveillance system have
been described previously.1,10,
12,13 It has become the preferred
surveillance system for neonatal
nosocomial infections after
2
participation in an infection
surveillance system was made
mandatory for all NICUs in Germany
caring for infants below 1500 g birth
weight. All analyses are done using
anonymized data within the legal
framework of quality improvement,
obviating the need for ethical
approval and informed consent.
The surveillance records pneumonia,
necrotizing enterocolitis, and BSI
beyond 72 hours of age in all preterm
infants with a birth weight <1500
g until discharge, until death, or
until they reach 1800 g. Trained
hospital nurses and physicians collect
demographic and obstetric data of
all infants surveyed, and an array of
clinical data of infected neonates.12
Non-CoNS BSIs are being defined as
any case with a positive blood and/
or cerebrospinal fluid culture with
a recognized pathogen, unrelated to
an infection at another site, in the
presence of at least 2 clinical signs
of systemic infection (increased
[>38°C] or decreased [<36.5°C]
body temperature or temperature
instability, tachycardia, increased
rates of apnea/bradycardia episodes,
prolonged capillary refill, metabolic
acidosis, hyperglycemia, apathy, or
seizures). Pathogens isolated from
cerebrospinal fluid are included in
the BSI definition as most cases of
meningitis in preterm infants result
from hematogenous dissemination,
and microbiological findings in
cerebrospinal fluid may identify
pathogens missed when culturing
inadequate amounts of blood.
For the purpose of this analysis,
exposure to a particular pathogen
was defined in 2 ways:
1. An infant was considered exposed
to a pathogen if a BSI with that
particular species had caused
a BSI in another infant (index
case) cared for simultaneously
in the same department (date of
admission of the exposed infant
preceding the date of discharge of
the index case, date of BSI of the
index case preceding the date of
discharge of the exposed infant,
and date of BSI of the index case
preceding the date of BSI of the
exposed infant).
2. An infant was considered exposed
to a pathogen if a BSI with that
particular species had been
diagnosed in an index case cared
for in the same department during
the length of stay of the exposed
infant or up to 30 days before
admission of the exposed infant,
with the date of BSI of the index
case preceding the date of BSI of
the exposed infant.
The analysis was restricted to
pathogens implicated in >30 BSIs
during the study period. As CoNS
are part of the normal skin flora
of virtually every infant and often
considered contaminations when
grown from blood cultures, no
calculations were carried out for
CoNS.
Statistical Methods
For the various pathogens, adjusted
odds ratios (ORs) were calculated
by using multivariable logistic
regression models. The patient-based
parameters birth weight (<500/500–
749/750–999/1000–1249/1250–
1499 g), gestational age (≤26/27–
28/29–30/≥31 weeks), gender
(boy/girl), delivery mode (planned
cesarean, vaginal delivery, emergency
cesarean), multiple birth (no/yes),
and length of stay were considered
in all models as confounders. Missing
values were considered as a separate
category. Furthermore, generalized
estimating equations (GEEs) were
calculated to consider clustering
effects within a department by
exchangeable correlation structure.
In the GEE models, only birth weight
and gender were considered in all
models because the limited number
of events restricted adjusting for
more confounders.
P values < .05 were considered
significant. Calculations were carried
out using SPSS 22.0 (IBM SPSS
REICHERT et al
6.90 (4.83–9.86)
3.06 (2.13–4.38)
4.89 (2.66–9)
4.24 (2.01–8.94)
9.21 (5.23–16.2)
53.08 (18.91–149.02)
33.75 (7.02–162.17)
4.37 (2.35–8.14)
9.54 (7.55–12.06)
4.34 (2.73–6.90)
7.88 (5.45–11.41)
7.88 (5.14–12.07)
13.06 (8.96–19.05)
77.46 (41.08–146.09)
64.52 (25.69–162.05)
8.74 (4.97–15.37)
We also looked at numbers of BSI
when a same-pathogen BSI was
observed in the same unit during
the preceding 30 days (Table 2). By
this definition, rates of BSI per 100
exposed infants varied between
1.4 (C albicans) and 6.5 (Serratia
spp). The RR for acquiring a BSI
while a same pathogen-BSI had
been diagnosed in the preceding 30
b
a
Methicillin-sensitive.
Vancomycin-sensitive.
c Cefotaxime-sensitive.
83
19
31
23
31
11
5
13
1172 (2.6)
859 (1.9)
805 (1.8)
689 (1.5)
659 (1.5)
135 (0.3)
105 (0.2)
527 (1.2)
407
243
246
210
190
58
38
138
Staphylococcus aureusa
Enterococcus sppb
Enterobacter spp
Escherichia colic
Klebsiella pneumoniaec
Serratia spp
Pseudomonas aeruginosa
Candida albicans
7.08 (5.72–8.66)
2.21 (1.38–3.37)
3.85 (2.68–5.36)
3.34 (2.13–4.89)
4.7 (3.26–6.53)
8.15 (4.36–13.72)
4.76 (1.77–10.24)
2.47 (1.38–4.08)
Number of BSI in
Exposed Infants
Infants exposed,
n (%)
RR (95% CI)
7.96 (6.11–10.37)
2.41 (1.58–3.67)
5.32 (3.58–7.91)
4.58 (2.91–7.20)
8.82 (5.84–13.31)
63.34 (30.32–132.35)
35.32 (12.71–98.20)
3.69 (2.03–6.69)
GEE Adjusted OR (95% CI)
Records of 44 818 infants with a
birth weight <1500 g born between
January 1, 2000, and December
31, 2011, and being cared for in
229 hospitals across Germany
revealed a total of 2004 non-CoNS
culture-positive BSIs. Pathogens
identified (in descending order) were
methicillin-sensitive S aureus (n =
407), Enterobacter spp (n = 246),
vancomycin-sensitive Enterococcus
spp (n = 243), cefotaximesensitive Escherichia coli (n = 210),
cefotaxime-sensitive Klebsiella spp
(n = 190), Candida albicans (n =
138), Serratia spp (n = 58), and P
aeruginosa (n = 38). Pathogens with
30 or less BSIs not analyzed further
included Citrobacter spp (n = 17),
Acinetobacter baumannii (n = 28),
and Group B Streptococcus (n = 30).
Number of BSI
Rate of BSI per 100 Exposed
Infants (95% CI)
Logistic Regression
Adjusted OR (95% CI)
RESULTS
Numbers of BSI acquired while
another infant with a same-pathogen
BSI was being cared for in the unit
are shown in Table 1. Rates of BSI
per 100 exposed infants varied
between 2.2 (Enterococcus spp)
and 8.2 (Serratia spp). The relative
risk (RR) for acquiring a BSI in the
presence or absence of an infant
with a preceding same-pathogen BSI
varied between 4.3 (Enterococcus)
and 77.5 (Serratia). In logistic
regression analysis, adjusted ORs
varied between 2.4 (Enterococcus)
and 63.3 (Serratia). Adjusted OR
did not differ substantially with
the results calculated by using GEE
models (Table 1).
Pathogen
TABLE 1 BSI in the Presence or Absence of an Infant Cared for Simultaneously in the Same Department With a Same Pathogen-BSI
Statistics, IBM Corporation) and SAS
9.3 (SAS Institute, Inc, Cary, NC).
PEDIATRICS Volume 137, number 4, April 2016
days in the same department varied
between 2.3 (Enterococcus) and
59.5 (Serratia). Adjusted ORs using
logistic regression analysis or GEE
are shown in Table 2.
DISCUSSION
This analysis of 2004 BSIs in 44 818
very low birth weight infants
demonstrates that the probability
of an infant developing a BSI with
a particular pathogen increases
while another infant cared for in the
same department has a BSI with the
same pathogen. Rates of pathogenspecific BSI in exposed infants
ranged from 0.022 for Enterococcus
spp to 0.082 for Serratia spp. The
RR of contracting a BSI in exposed
versus nonexposed infants reveals
even more variation. Judged by
overlapping 95% confidence
intervals (CIs), a pattern with 2
groups emerges. The first 1 contains
C albicans, Enterococcus, S aureus,
Enterobacter, E coli, and Klebsiella,
whereas the second group comprises
Serratia spp and P aeruginosa.
The same pattern emerged when
calculating the probabilities of
contracting a BSI with a particular
pathogen in a neonatal department
within 30 days after that pathogen
had been isolated from a blood
culture in another infant cared for in
that department.
There are several limitations to this
study. First, the reporting system
made no distinction between
various strains of Enterococcus,
Enterobacter, or Serratia, and
there was no genotyping of the
pathogens involved. Thus, 2
temporally related BSIs in the
same department might well be
a coincidence. Even in outbreaks,
genotyping has revealed unexpected
polyclonality of the pathogens
isolated.14–19 The likelihood of this
type of error increases alongside the
incidence density, overestimating
the transmission probabilities of
more common pathogens such
3
3.58 (2.28–5.63)
3.19 (2.08–4.89)
3.99 (2.07–7.7)
2.75 (1.19–6.35)
5.53 (2.62–11.64)
39.17 (14.04–109.24)
24.68 (3.76–162.15)
2.14 (0.88–5.24)
5.87 (4.42–7.78)
2.32 (1.24–4.35)
5.89 (3.94–8.79)
5.53 (3.34–9.15)
8.47 (5.37–13.37)
59.47 (29.80–118.67)
35.82 (11.19–114.7)
4.55 (2.02–10.26)
53
10
26
16
20
9
4
6
Methicillin-sensitive.
Vancomycin-sensitive.
c Cefotaxime-sensitive.
b
a
Staphylococcus aureusa
Enterococcus sppb
Enterobacter spp
Escherichia colic
Klebsiella pneumoniaec
Serratia spp
Pseudomonas aeruginosa
Candida albicans
407
243
246
210
190
58
38
138
1115 (2.5)
814 (1.8)
882 (2.0)
659 (1.5)
614 (1.4)
138 (0.3)
109 (0.2)
443 (1.0)
4.75 (3.62–6.13)
1.23 (0.63–2.18)
2.95 (1.98–4.23)
2.43 (1.44–3.83)
3.26 (2.06–4.90)
6.52 (3.23–11.63)
3.67 (1.18–8.61)
1.35 (0.55–2.79)
4.50 (3.31–6.12)
2.56 (1.68–3.91)
4.45 (2.91–6.79)
3.08 (1.82–5.23)
5.43 (3.34–8.83)
47.83 (22.0–104.04)
25.27 (8.39–76.05)
1.77 (0.77–4.09)
GEE Adjusted OR (95% CI)
Logistic Regression
Adjusted OR (95% CI)
RR (95% CI)
Rate of BSI per 100 Exposed
Infants (95% CI)
Number of BSI in
Exposed Infants
Infants Exposed,
n (%)
Number of BSI
Pathogen
TABLE 2 BSI in the Presence of Absence of a Same Pathogen-BSI in the Same Department During the Preceding 30 d
4
as S aureus, and rendering this
kind of analysis virtually pointless
for CoNS, as virtually all preterm
infants become colonized with some
CoNS during the first week of life.20
Retrieval of CoNS from the blood
culture of a sick infant indicates
that the colonization of the infant’s
skin with CoNS has turned into an
invasive disease, usually triggered by
indwelling catheters, but it does not
suggest spread of CoNS from 1 infant
to another infant.20 Rates of BSI
by CoNS but not by gram-negative
pathogens have been found to
decrease following implementation
of improved handling of indwelling
central lines.2,3 Second, while looking
for in-hospital transmissions, we had
no data about the actual physical
proximity of infants contracting
a BSI with the same pathogen.
Infants being cared for in the same
department may or may not have
shared the same room, the same
nurse, or the same ward. Third, the
analysis was restricted to very low
birth weight infants, but NICUs are
being populated also by more mature
infants who are not subjects to this
type of infection surveillance. Fourth,
we only looked at culture-positive
BSI, whereas pathogen transmissions
may involve chains of colonized
or infected infants without clinical
symptoms of systemic infection.21
Focusing on BSI does not take into
account merely colonized infants as
a source of exposure. However, when
we looked at BSI in the presence
or absence of a BSI with the same
pathogen in the same department
during the preceding 30 days, a
highly similar pattern emerged. Fifth,
while the national neonatal infection
surveillance system covers the vast
majority of neonatal intensive units
in Germany, the data are all from the
same country. Therefore, the analysis
presented here calls for similar
studies in elsewhere. Although our
results are thought to be applicable
to hospitals with comparable
resources and hygiene measures,
pathogen-specific transmission rates
might be influenced by different
hygiene standards, use of antibiotics,
and local prevalence of pathogens.22
The differences between the
pathogens analyzed for involvement
in temporally and spatially linked
BSI may reflect differences of
virulence, the ease of spreading
in the NICU environment, or both.
Reported ratios of sterile site
infections to colonizations are 1:6 for
S marcescens, as opposed to 1:27 for
Klebsiella pneumonia.23 Calculated
attack rates, as defined as the ratio
of infants with invasive infections
and all infants positive for a certain
pathogen, have been reported to be
over 20% for P aeruginosa24 and
may exceed 50% for S marcescens
during outbreaks.7 S marcescens
and P aeruginosa have also been
found to figure prominently in NICUacquired bacterial conjunctivitis,
25 emphasizing their potential for
patient-to-patient spreading in this
environment.
In addition to transmission via the
hands of staff,24,26–29 pathogens
may also spread from inanimate
point sources. An increased role for
environmental sources has indeed
been documented for S marcescens
and P aeruginosa, as compared with
other pathogens. Numerous reports
have identified soaps and shampoos
as reservoirs for S marcescens30–33
and P aeruginosa.34,35 Water systems
can act as a source of S marcescens36
and P aeruginosa.19,35,37,38
Although we found P aeruginosa
and Serratia spp to have the highest
rate of BSI in exposed infants of all
pathogens analyzed, they were also
those with the lowest incidence
density. The rate of BSI in exposed
infants, defined by a BSI in another
infant, does not reflect the general
contagiousness of a pathogen but the
risk for a cluster of BSI after an index
case with the specific pathogen. In
contrast to other potential pathogens,
P aeruginosa and Serratia spp are
usually not present in hospitalized
preterm infants, and the advent of a
REICHERT et al
colonized infant in the NICU is pivotal
as a source for further infections.
NICUs should be alerted in any case
of a BSI with P aeruginosa or Serratia,
prompting active surveillance
cultures to detect noninfected
carriers and place them separate
from other infants.39
low birth weight infants. Because
they are also those pathogens with
the highest reported BSI-related
mortality rates,4–6 vigorous attempts
should be made to intensify infection
control measures whenever P
aeruginosa or Serratia spp have been
isolated from a patient in the NICU.
CONCLUSIONS
ACKNOWLEDGMENT
P aeruginosa and Serratia spp are
exceptional in their potential to
spread in the NICU and attack very
The authors thank the health care
and infection control staff for their
continued support of the neonatal
nosocomial infection surveillance
project.
ABBREVIATIONS
BSI: blood stream infection
CI: confidence interval
CoNS: coagulase-negative
staphylococci
GEE: generalized estimating
equation
OR: odds ratio
RR: relative risk
FUNDING: The German National Neonatal Infection Surveillance System is being supported by the Federal Department of Health and intramural funds from the
Charité University Medical Center.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
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