ARTICLE IN PRESS

American Journal of Infection Control 000 (2021) 1−6

Contents lists available at ScienceDirect

American Journal of Infection Control

journal homepage: www.ajicjournal.org

Major Article

Risk factors for nosocomial methicillin resistant Staphylococcus aureus

(MRSA) colonization in a neonatal intensive care unit: A Case-control
study
Archana Balamohan MD a,*, Joanna Beachy MD, PhD a,b, Nina Kohn MBA, MA c, Lorry G. Rubin MD a,b
a
Cohen Children’s Medical Center of New York, New York, NY
b
Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY
c
Biostatistics Unit, Feinstein Institute of Medical Research, Manhasset, NY

Key Words: Aim: To determine risk factors for MRSA colonization in a Level IV Neonatal Intensive Care Unit (NICU) inde-
Epidemiology pendent of length of stay and gestational age in the context of a persistently circulating MRSA clone.
NICU Design: Retrospective matched case-control study.
Outbreak Setting: Level IV NICU
Risk factors
Patients: Infants admitted between April 4,2017- March 31,2018.
Methods: Based on weekly surveillance cultures, infants who acquired MRSA were matched 1:1 with MRSA-
negative control infants by duration of exposure (length of stay) and gestational age to determine risk factors
for acquisition.
Results: Fifty case infants were matched with controls. Isolates from 45 of the 50 cases were mupirocin-resis-
tant and related by pulse-field gel electrophoresis. On matched univariable analysis, the following were sig-
nificantly associated with a risk for MRSA acquisition: 1.Bed location in the acute area(P = 0.03), 2.
Requirement of any level of respiratory support during the week prior to MRSA detection(P = 0.04), 3.Higher
ATP pass rate (a measure of effectiveness of cleaning) during the week of and week prior(P = 0.01), 4.Higher
MRSA colonization pressure during the week of and week prior(P< 0.0001), 5.Not having a hearing test dur-
ing the time between the previous negative culture and MRSA acquisition(P = 0.01). A multivariable condi-
tional logistic regression model (that excluded ATP pass rate) found that only colonization pressure was
associated with acquisition of MRSA colonization.
Conclusions: In an outbreak setting, MRSA colonization pressure is significantly associated with MRSA acqui-
sition in the NICU independent of length of stay and gestational age.
© 2021 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All
rights reserved.

INTRODUCTION
Staphylococcus aureus (SA) is a leading pathogen in infants in a
neonatal intensive care unit (NICU).1-4 SA infections are associated
with significant mortality5 and morbidity, including high rates of
neurodevelopmental sequelae and growth impairment.6,7 Neonatal
methicillin-resistant SA (MRSA) colonization is a demonstrated risk
factor for invasive MRSA infection.8,9 In a study conducted in a NICU,
* Address Correspondence to: Archana Balamohan, MD, Arkansas Children’s Hospi-
tal, 1 Children’s Way, Little Rock, AR 72202
E-mail address: abalamohan@uams.edu (A. Balamohan).
Conflicts of interest: Drs. Balamohan, Beachy and Rubin and Nina Kohn do not have
any conflicts of interest.
Funding : None.
the risk of MRSA infection among colonized infants was 10.2% com-
pared to a 2.3% risk of infection among non-colonized infants.9 In a
study of both MRSA and methicillin-susceptible SA (MSSA) in a
Hawaiian NICU, SA-colonized infants were 82-fold more likely to
become infected with SA than non-colonized infants.10
Previously described risk factors for MRSA colonization within a
NICU include prematurity, low birth weight,11-13 length of stay
(LOS),11,14 outborn status and admission to the NICU after 24 hours of
age, presence of central venous device, lower cumulative exposure to
systemic antibiotic, and colonization pressure.12,14 However, LOS
may confound some of the aforementioned risk factors. To minimize
LOS as a possible confounding factor, Washam et al15 evaluated risk
factors for SA acquisition independent of LOS and found that infant
placement in a single-bed room was associated with a lower risk of
SA colonization than placement in a multi-bedded room.

https://doi.org/10.1016/j.ajic.2021.04.082
0196-6553/© 2021 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
 ARTICLE IN PRESS
2 A. Balamohan et al. / American Journal of Infection Control 00 (2021) 1−6
During the first quarter of 2017, a cluster of 3 cases of MRSA bacter-
emia was observed in our Level IV NICU, a rate of 0.806 infections per
1,000 hospital days that was much higher than the baseline rate of
0.164 infections per 1,000 hospital days during the previous two years.
This prompted the initiation of surveillance cultures, revealing
that 45% of infants were MRSA colonized. New cases of colonization
continued to occur despite use of a mupirocin decolonization regi-
men, leading to recognition of a mupirocin-resistant clone. A
renewed emphasis on standard infection prevention precautions was
implemented along with additional measures including intensified
education and observation of hand hygiene, increased environmental
cleaning, and instituting a limitation on the NICU census. However,
despite these measures, newly colonized infants continued to accrue
for over a year (Fig 1).
To support efforts to control the spread of this MRSA clone and to
address the concern of a potentially contributing reservoir, we con-
ducted a study of risk factors for MRSA acquisition.
METHODS
Setting
This study was a retrospective matched case-control study con-
ducted at a quaternary NICU at Cohen Children’s Medical Center
(CCMC) of Northwell Health. The NICU is a 57 beds unit divided into
an acute care section (24 beds) and a special care nursery (“step-
down”) section. The acute care section is divided into 12 rooms (2
beds per rooms that are adjoined to an adjacent room to form a 4 bed
pod). The special care nursery section is divided into 5 multibed
rooms with 6-8 beds per room. In March 2017 an active surveillance
screening program was implemented to identify infants colonized
Fig 1. Epidemic curve of weekly number of new (black bars) and repeatedly positive (grey bars) infants with MRSA colonization in a neonatal intensive care unit during the study
period. The x-axis indicates month and year and the y-axis indicates number of infants.
with SA among infants with an anticipated NICU stay of greater than
48 hours. On a designated day each week, these infants were sub-
jected to a combined surface swab of the anterior nares, umbilicus,
and inguinal region on a weekly basis that was cultured for SA, both
MSSA and MRSA. If a culture grew either MRSA or MSSA, the infant
was considered to be colonized. A decolonization treatment consist-
ing of 2% mupirocin ointment applied to both nares, umbilicus
(unless an umbilical catheter was present), and abraded skin, if pres-
ent, twice a day for a five day period was initiated. The treatment pro-
tocol was repeated once if the infant had a persistently positive
culture. Chlorhexidine baths were not utilized. Pulse field gel electro-
phoresis on MRSA isolates were performed at the New York State
Public Health Laboratories. This study was approved by the Institu-
tional Review Board at CCMC with waiver of consent.
Design
Infants who were inpatients of the NICU between April 4, 2017,
and March 31, 2018 on the designated day of weekly surveillance cul-
tures were eligible for inclusion as case or control infants. Infants
who had a surveillance culture growing MRSA with at least one pre-
vious negative surveillance culture were eligible for inclusion as case
infants, including those previously MSSA colonized with subsequent
MRSA colonization provided the infant had at least two negative
weekly surveillance cultures between the MSSA- and MRSA-positive
surveillance cultures. Infants were excluded as case subjects if a sur-
veillance culture was positive for MRSA before hospital day 4. The
exposure time was defined as the time, in days, between NICU admis-
sion and the date of the initial positive MRSA surveillance culture.
Gestational age brackets were defined as follows: ≤ 26 weeks, 27 −
29 weeks, 30 − 33 weeks, 34 − 36 weeks, and ≥ 37 weeks. Controls
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A. Balamohan et al. / American Journal of Infection Control 00 (2021) 1−6
were randomly selected for each case from infants within the same
gestational age bracket provided they had the same or greater expo-
sure-time as did the case patient. Potential controls were excluded if
they were previously MRSA-colonized. If a potential control had a
history of MSSA colonization, at least two negative surveillance cul-
tures were required to be eligible. Infants with a prior stay in the
Pediatric Intensive Care Unit were eligible to be included as a case or
control patient if they had at least one negative surveillance culture
after transfer to the NICU prior to detection of SA on a surveillance
culture. After random matching, if more than one infant from a set of
twin or triplet siblings was eligible for the study, one of the twin/trip-
let infants was randomly selected to be removed from the study as
was the patient matched to them.
Data collection
Data on potential risk factors were abstracted from the electronic
medical records for the case and control patients. Extracted data
included:
Infant demographics: sex, ethnicity, race, and single/multiple
gestation
Maternal factors, specifically substance abuse, known MRSA coloni-
zation, prolonged rupture of membranes, and peripartum antibi-
otics (defined as during the week prior to delivery and including
labor)
Neonatal risk factors from the time of admission: days of various
types of respiratory support, antimicrobial use, and presence of
central venous catheter
Neonatal risk factors during the week prior to detection of MRSA col-
onization (or persistently negative surveillance culture in con-
trols): bed location, number of bed location changes, presence of
central venous catheter, cardiac or radiographic imaging, and
MRSA colonization pressure (calculated as point prevalence of
MRSA-colonized infants in the NICU) during the week prior and
week of first detection in each case patient.
During the study period, CCMC Infection Prevention, Quality
teams, and Environmental Services Teams provided data on hand
hygiene and on the effectiveness of equipment and surface cleaning
by post-cleaning testing of swabbed surfaces using adenosine tri-
phosphate (ATP) surface testing. ATP is a chemical compound found
in living cells, including microbes that should be reduced by effective
cleaning. A ‘pass’ is favorable, indicating a low ATP level and indicates
effective cleaning.
Statistical analysis
In the primary analysis, MRSA cases were matched 1:1 with nega-
tive controls. For each categorical factor, McNemar’s test was used to
compare the proportion of cases (MRSA+) with that risk factor to the
proportion of controls with that risk factor. For each continuous fac-
tor, the Wilcoxon signed-rank test was used to compare cases to con-
trols. Factors that were significantly associated with MRSA culture
results on univariable analysis, (P < 0.05), were included in a multi-
variable conditional logistic regression model. Backward elimination
was used to remove effects that did not contribute significant infor-
mation to the model. Unit on day of culture (acute, step-down), respi-
ratory support (yes, no), hearing test (yes, no), and colonization
pressure (%) during week of and the week prior were significantly
associated with MRSA culture result, either positively or negatively,
in the univariable analyses. Hearing test was not included in the mul-
tivariable model, due to the presence of sparse data points. Coloniza-
tion pressure (%) during the week of new colonization or control was
not included, as it was correlated with colonization pressure (%)
3
during the week prior. Based on logic, colonization pressure during
the week prior would be more likely than colonization pressure dur-
ing the week of detection to contribute to new colonization; hence, it
was decided a priori, to use colonization during the week prior in
multivariable analyses. Therefore, bed location on day of culture,
respiratory support, and colonization pressure (%) during week prior
were included in the multivariable conditional logistic model.
RESULTS
Based on eligibility criteria, 495 infants met criteria for inclusion
as a case or control. An additional 41 infants who would have been
eligible were excluded because a surveillance culture was not
obtained, indicating that 82.8% of eligible infants were included. Sev-
enty-two (14.5%) infants became MRSA colonized during the study
period. Of these, 63 MRSA cases were eligible as cases and were
matched with 63 controls. After excluding infants who had a twin
sibling in the study as well as their corresponding case or control as
described in the Methods section, 50 MRSA cases and their matched
controls were analyzed.
Forty-five of the 50 MRSA cases were colonized with mupirocin-
resistant isolates (90%) that were clonally related as assessed by simi-
lar or identical pulse-field gel electrophoresis patterns of bacterial
DNA.
The results of the matched case-control univariate analyses (Table
I) revealed a significantly greater risk of acquiring MRSA was associ-
ated with infants who were located in the acute area on the day of
detection of MRSA colonization, required respiratory support in the
week prior to detection of colonization, and were exposed to higher
colonization pressure (%) in the NICU during the week of or week
prior to detection of colonization. A higher ATP bioburden pass rate
and having had a hearing test during the prior week were negatively
associated with MRSA colonization. There were no significant differ-
ences between cases and controls in birth weight, number of bed
location changes, surgical operations performed, central venous cath-
eter presence, systemic antibiotic usage, radiologic studies, or num-
ber of consultant interactions (Table I). Bed location (acute unit vs
step down unit) on the day of culture, respiratory support, and colo-
nization pressure during the week prior were included in the multi-
variable conditional logistic model. After backward elimination, only
colonization pressure (%) during the week prior was significantly
associated with MRSA colonization.
DISCUSSION
A major finding of this study is that, in addition to birth weight,
gestational age, length of stayand outborn status11-14 that have previ-
ously have been established to be independent risk factors for MRSA
colonization in NICUs, in the setting of a MRSA outbreak, MRSA colo-
nization pressure was independently associated with risk of new
MRSA colonization. Colonization pressure in a NICU as a risk factor of
MRSA colonization is generally supported by available literature.
Pierce et al16 found that every person-day increase in exposure to
untreated MRSA carriage lead to a 6% increase in MRSA acquisition

et al14 had similar findings, identifying colonization pres-
risk. Giuffre
sure as a strong independent risk factor for MRSA acquisition: for
every day and percent unit of increment, the odds ratio of becoming
colonized with MRSA increased by 4% and 5%, respectively. However,
more recently, Washam et al15 studied risk factors for MRSA acquisi-
tion in an endemic setting and did not find that colonization pressure
was a risk factor for MRSA colonization. This difference with our find-
ing may be related to the large range of weekly colonization preva-
lence (5-50%) we observed; this may have allowed for an increased
likelihood of detecting an effect of colonization pressure compared to
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4 A. Balamohan et al. / American Journal of Infection Control 00 (2021) 1−6

Table 1
Univariate analyses of possible risk factors for MRSA colonization

A. Discrete factors

Cases (N = 50), Controls (N = 50), P-value

Number (%) Number (%)

Sex: Male 30 (60%) 34 (68%) 0.3711

Ethnicity
Hispanic/Latino 10 (20%) 10 (20%) 0.8470
Not Hispanic 32 (64%) 35 (70%)
Other/Unknown 8 (16%) 5 (10%)
Race
Asian 5 (10%) 5 (10%) 0.9494
Black/African American 17 (34%) 15 (30%)
White 11 (22%) 15 (30%)
Other 17 (34%) 15 (30%)
Multiple gestation? Yes 4 (8%) 9 (18%) 0.1317
Intrapartum maternal antibiotics? Yes* 27 (61%) 31 (70%) 0.3458
Prolonged rupture of membranes (>18h): Yes 12 (24%) 9 (18%) 0.4054
Mode of Delivery: C section 37 (74%) 36 (72%) 0.8084
Inborn vs transfer: transfer 13 (26%) 9 (18%) 0.3458
Surgery during hospitalization? Yes 19 (38%) 24 (48%) 0.1655
Surgery in OR: Yes 12 (24%) 12 (24%) 1.000
Prior cardiac surgery: Yes 5 (10%) 4 (8%) 0.6547
Unit on day of culture: acute 36 (72%) 26 (52%) -0.0330
Bed adjacent to room door 18 (36) 19 (38%) 0.8348
Change in bed (prior negative to culture) 19 (38%) 19 (38%) 1.00
Change in bed (past week) 20 (40%) 18 (36%) 0.6698
Respiratory support (invasive and non-invasive) 42 (84%) 33 (66%) -0.0389
Receiving donor breast milk (from milk bank) 10 (20%) 9 (18%) 0.7815
Central venous catheter present during prior 7 days 33 (67%) 33 (67%) 1.000
Central venous catheter present at any point prior 44 (88%) 41 (82%) 0.3657
MSSA colonization prior to 1st MRSA-detection (or control) 4 (8%) 3 (6%) 0.7055
Treatment with an antibiotic with MRSA activity 9 (18%) 4 (8%) 0.1655
at prior negative culture: Yes
Treatment with an antibiotic with MRSA activity 5 (10%) 7 (14%) 0.5271
at case/control culture: Yes
Antibiotic use (from time of admission to time of culture): Yes 41 (82%) 44 (88%) 0.3657
Anti-staphylococcal b-lactams (anti-staphylococcal 41 (82%) 43 (86%) 0.5637
penicillin, penicillin
plus b-lactamase inhibitor combination,
cephalosporins, carbapenems)
Non−anti-staphylococcal b-lactams (e.g., penicillin, 41 (82%) 43 (86%) 0.5367
ampicillin, amoxicillin)
Anti-MRSA (e.g., vancomycin, clindamycin) 14 (28%) 18 (36%) 0.3173
Aminoglycosides 36 (72%) 39 (78%) 0.4386
Prior topical mupirocin treatment course 4 (9%) 4 (9%) 1.00
Prior PICU Stay 1 (2%) 1 (2%) 1.00
Echocardiogram during the prior 7 days 12 (24%) 13 (26%) 0.7815
EKG during prior 7 days 4 (8%) 6 (12%) 0.4795
EEG during the prior 7 days 0 (0%) 0 (0%) ———
Ultrasound (other than cardiac) during the prior 7 days 22 (44%) 25 (50%) 0.5316
Radiograph during the prior 7 days 30 (60%) 32 (64%) 0.6374
Glucometer glucose resulted during the prior 7 days 36 (72%) 38 (76%) 0.5930
Hearing test prior to MRSA colonization or control 8 (17%) 17 (35%) 0.0126
Eye exam prior to MRSA colonization or control 8 (17%) 8 (17%) 1.0000
Seen by one or more subspecialists 40 (80%) 41 (80%) 0.7815

B. Continuous Factors

Cases (N = 50), Controls (N = 50), P-value

Median (Q1, Q3) Median (Q1, Q3)

Birthweight (g) 1407.5 (885.0, 2230.0) 1335.0 (860.0, 2109.0) 0.6307

Age on admission (days) 0.0 (0.0, 0.0) 0.0 (0.0, 0.0) 0.9878
Average census week of MRSA colonization 55 (51,57) 55 (51,58) 0.8082
Average census week prior to MRSA colonization 55 (51,56) 55 (51,57) 0.4591
Number of room moves since prior negative culture 0 (0,1) 0 (0,1) 0.8036
Number of moves during prior week 0 (0,1) 0 (0,1) 0.9449
Number of subspecialist services that visited 2 (1,3) 2 (1,3) 0.4555
infant during prior week
Total days respiratory support: CPAP 2 (0, 6) 0 (0, 4) 0.1184
Colonization pressure (%) during week of new 26.5 (13.0, 45.0) 9.0 (8.0, 15.0) <0.0001
colonization or control
Colonization pressure (%) during week prior to 29.5 (9.0, 45.0) 10.0 (8.0, 16.0) <0.0001
new colonization or control
ATP pass rate, week of colonization detection (n = 36) 96.5 (86, 99.5) 98 (96, 99.5) 0.0091
ATP pass rate, week prior to colonization detection (n = 36) 94 (83, 98) 98.5 (93, 100) 0.0128

NOTE. Bold values are statistically significant P < .05. ATP, adenosine triphosphate; CPAP, continuous positive airway pressure; EEG, electroencephalogram; EKG, electrocardiogram;
MRSA, methicillin-resistant Staphylococcus aureus; MSSA, methicillin-susceptible Staphylococcus aureus; OR, operating room; PICU, pediatric intensive care unit.
 ARTICLE IN PRESS
A. Balamohan et al. / American Journal of Infection Control 00 (2021) 1−6
the study of Washam et al in which the weekly colonization preva-
lence varied within a more limited range.
In addition to exposure to higher colonization pressure, infants at
higher acuity of care (as evidenced by being housed in the acute unit
or requiring any level of respiratory support) were also significantly
more likely to acquire MRSA colonization in a univariate analysis.
Our finding that the absence of a recent hearing test was associated
with a greater risk of MRSA colonization also suggests that higher
acuity of care is the underlying risk factor; as hearing tests are per-
formed on stable infants and those closer to discharge this may
reflect that control infants were less ill and/or closer to anticipated
discharge than case infants. Although on univariate analysis, our
study found an increased likelihood of MRSA colonization in neonates
requiring any level (non-invasive or invasive) respiratory support,
previous studies have shown varied associations between respiratory
support and colonization.15,17 Ramsing et al17 demonstrated nasal
continuous positive airway pressure (nCPAP) as an independent risk
factor for MRSA acquisition in a Level II NICU. Although this is consis-
tent with our findings, LOS, which was not accounted for in their
study, may have been a confounding factor. Washam et al15 who con-
trolled for LOS, did not find intubation to be a risk factor. With inclu-
sion of both invasive and non-invasive (nCPAP) respiratory support
in our analyses, we found that any level of respiratory support was
associated with acquiring MRSA colonization. Use of respiratory sup-
port may facilitate transmission due to increased handling by health
care personnel (HCP) and/or the presence of a foreign body in the
nasal cavity or airway.
LOS, low birth weight, and low gestational age are interrelated
variables and have been reported to be associated with a risk of
MRSA colonization. It is unclear if young gestational age and low
birth weight are independent risk factors or simply markers for the
risk factor LOS.18 The study design of this current investigation con-
trolled for LOS and gestational age bracket and did not find low birth
weight to be associated with MRSA colonization, suggesting that
birth weight may be a marker for LOS and/or gestational age, and
therefore not adequately address whether or not birth weight is an
independent risk factor for MRSA colonization.
In the setting of a clonal mupirocin-resistant MRSA strain that
persisted for over a year, the concern arose for a reservoir potentially
harboring this resistant organism and playing a role in ongoing trans-
mission. Whether this putative reservoir was hospital equipment,
colonized hospital personnel or environmental contamination was
also explored, as shown by the risk factors analyzed in Table 1. To our
knowledge, this is the first study of MRSA acquisition in a NICU set-
ting that investigated an expanded set of potential risk factors for
transmission, specifically exposure to hospital equipment (including
equipment used for eye examination by an ophthalmologist, or for a
hearing evaluation by audiologists, ultrasound, and radiology equip-
ment) and the personnel who operate the equipment, room changes,
and effectiveness of cleaning in the setting of an MRSA outbreak;
none of these factors were associated with risk of MRSA colonization.
This lack of association makes it less likely that technologists or other
personnel who perform bedside evaluations or imaging studies and
any equipment used in diagnostic procedures contributed to MRSA
transmission.
Prenatal risk factors such as Caesarean delivery, maternal antibi-
otic exposure, and prolonged rupture of membranes were not associ-
ated with risk of MRSA colonization but such factors were unlikely to
be identified because of the design of the study whereby enrollment
criteria required a negative MRSA culture after delivery. In previous
studies, maternal colonization,19 outborn status, and admission to
the NICU after 24 hours of age12 were identified as risk factors for
MRSA colonization. Geraci et al12 found that systemic antibiotic use
was more frequent among non-colonized infants, suggesting this as a
possible protective factor. Infants with longer duration of
5
hospitalization may have undergone an increased number of sus-
pected sepsis evaluations resulting in an increased number of antibi-
otic courses. Eliminating prolonged hospitalization by matching for
LOS may explain why our study did not confirm this finding We also
explored the use of antibiotics with MRSA activity among cases and
controls and did not find administration of such antibiotics either
during the week prior or the week of a positive culture to be a risk
factor for or protective against colonization.
The limitations of this study include the small sample size that
could have reduced sensitivity to identify some risk factors and that
the study was conducted during a MRSA outbreak with the possibility
that these findings may not be applicable to risk factors for endemic
MRSA colonization. Another limitation is that the potential role of
HCP with the most patient contact, (ie, nurses, physicians, and other
advanced care practitioners) was not examined. Given that up to 17%
of HCP may be MRSA-colonized,20-22 and transmission of MRSA by
staff has been documented in adult intensive care units22-24 and neo-
natal intensive care units,26 it is possible that HCP played a role in
transmission.22,24-26 Finally, although a recent study found parents to
be a significant source of SA acquisition in the NICU,27 it is unlikely
that visitors played a major role in transmission because the vast
majority of MRSA isolates were clonally related. However, a role of
visitors in transmission by contact with the NICU environment result-
ing in transient carriage and transmission is possible.
Independent of LOS and gestational age, MRSA colonization pres-
sure, higher acuity of care as noted by location in the acute area of
the NICU and the need for respiratory support, and a lower ATP pass
rate were significantly associated with acquisition of MRSA coloniza-
tion in an outbreak setting. Only colonization pressure remained sig-
nificantly associated in a multivariable model. Evaluation of the
potential role of HCP, families, and visitors may also be important to
identify reservoirs and routes of transmission of MRSA in NICUs in an
outbreak setting but was beyond the scope of this study.
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