Giuffrè et al. BMC Pediatrics 2012, 12:64
http://www.biomedcentral.com/1471-2431/12/64
RESEARCH ARTICLE
Open Access
Epidemic spread of ST1-MRSA-IVa in a neonatal
intensive care unit, Italy
Mario Giuffrè1, Domenico Cipolla1, Celestino Bonura2, Daniela Maria Geraci2,3, Aurora Aleo2, Stefania Di Noto1,
Federica Nociforo1, Giovanni Corsello1 and Caterina Mammina2*
Abstract
Background: Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) has recently emerged as
an important pathogen in neonatal intensive care units (NICUs). The purposes of this study were to characterize
methicillin-resistant isolates from an outbreak in a NICU, to examine the genetic traits and clonality of CA-MRSA,
and to review the characteristics and outcomes of the neonatal cases and investigate the routes of entry and
transmission of the MRSA outbreak strain in the NICU under study.
Methods: The study NICU practiced an active surveillance program for multidrug-resistant organisms, including
weekly cultures for detection of MRSA from nasal swabs among all the admitted neonates. All first isolates from
surveillance cultures and all clinical isolates were submitted for susceptibility testing and genotyping. Data from
each infant’s medical records were prospectively included in a database, and the clinical features and outcomes of
the colonized/infected infants were assessed.
Results: A total of 14 infants were colonized or infected by a strain of ST1-MRSA-IVa between April and August
2011. The CA-MRSA strain appeared to have been introduced to the NICU by an infected infant transferred from
another hospital. The outbreak was successfully contained by multifaceted infection control interventions.
Conclusions: The results of this study confirm that NICU is a healthcare setting with a critical permeability to
CA-MRSA. Active surveillance including molecular typing can help to detect and monitor the spread of
antimicrobial drug-resistant organisms, and thus trigger timely control interventions.
Keywords: CA-MRSA, NICU, Epidemiology, Infection control
Background
Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) has recently emerged as an important pathogen. CA-MRSA was first identified in
infection cases with no previous contact with the healthcare system or other well-recognized risk factors, such
as recent antimicrobial drug use [1]. However, it has
recently become increasingly identified as a healthcareassociated (HA) pathogen [2]. Neonatal intensive care
units (NICUs), nurseries and maternity settings are
involved in these CA-MRSA events with alarming frequencies, and as many as 12 out of 18 recent outbreaks
in healthcare facilities have occurred in these settings,
with seven outbreaks affecting NICUs [3].
* Correspondence: caterina.mammina@unipa.it
2
Department of Sciences for Health Promotion “G. D’ Alessandro”, University
of Palermo, Via del Vespro 133, I-90127 Palermo, Italy
Full list of author information is available at the end of the article
CA-MRSA outbreaks have usually been traced to the
infiltration of a single strain in a healthcare setting [4].
However, their epidemiological patterns are increasingly
difficult to understand, as their occurrence and dissemination routes in the community are largely unknown. The
boundaries between CA and HA infections have become
blurred, casting doubt on some previously defined criteria for distinguishing between CA- and HA-MRSA [5].
CA-MRSA has generally been considered to be susceptible to most non-β-lactam antibiotics, to carry small
staphylococcal chromosomal cassette (SCC)mec cassettes (types IV or V), and to frequently produce the
Panton-Valentine leucocidin (PVL). These attributes are
detected in most strains of USA300, the most successful
CA-MRSA strain, which is now endemic in the US, but
occur infrequently in other geographical areas, such as
Europe [4, 6]. Nonetheless, some increasingly resistant
CA-MRSA strains have been described [4]. Moreover,
© 2012 Giuffrè et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Giuffrè et al. BMC Pediatrics 2012, 12:64
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the light IV and V SCCmec types have proven to be
peculiar to some epidemic HA-MRSA clones, 4 such as
ST22-MRSA-IV (EMRSA-15) [3, 5]. Additionally, PVLnegative CA-MRSA strains have been shown to cause
not only community infections, but also healthcare outbreaks [3, 5]. Consequently, highly discriminative molecular typing systems are needed to understand the
epidemiology of MRSA.
In this study, we report an outbreak of infection/
colonization by an ST1-MRSA-IVa strain in a NICU in
Palermo, Italy. The aim of the study was to characterize
the bacterial isolates, determine the genetic traits and
clonality of CA-MRSA, and to review the characteristics
and outcomes of the neonatal cases and investigate the
routes of entry and transmission of the MRSA strain in
the NICU under study.
Methods
Setting
The NICU of the university teaching hospital (Azienda
Ospedaliero-Universitaria Policlinico “P. Giaccone”),
Palermo, Italy, admits 250 infants annually, of all gestational ages (mean 37 weeks, range 26–42). This NICU is
associated with the regional reference centre for genetic
diseases, and therefore has a high prevalence of neonates
with malformations (approximately 20%), as well as of
admissions of infants born elsewhere (outborn) (approximately 35%). The NICU includes one intensive care
room containing of eight beds and one intermediate care
room containing an additional eight beds. The average
nurse-to-patient ratios are 1:3 and 1:4 in the two sections, respectively.
MRSA surveillance
A microbiological surveillance screening program for
MRSA has been in place since June 2009 for all infants
staying in the NICU. Surveillance specimens from the
anterior nares were obtained weekly (each Tuesday) and
sent for MRSA detection and typing. Sampling at admission was discontinued after the first 6 months because
of a low yield rate. All first isolates from surveillance
cultures and all clinical isolates, i.e. those from diagnostic samples submitted to the clinical microbiology
laboratory, were genotyped and compared weekly. No
routine surveillance cultures were obtained from healthcare workers (HCWs). MRSA-colonized infants were
labeled, but not physically segregated, after careful consideration of facility design and ward staffing issues.
However, cohort care was implemented by designated
HCWs. The NICU had experienced endemic circulation
of ST22-MRSA-IVA (EMRSA-15) since 2009. Strict
infection control measures had been implemented,
including contact precautions, reinforcement of hand
hygiene and compliance monitoring by direct observation,
Page 2 of 7
but they were unable to definitively interrupt the spread
of this clone.
A prospective database was routinely maintained for
patients from whom multidrug resistant organisms, including MRSA, were isolated. Data from medical records
included demographic characteristics, delivery history,
complications of prematurity, use of parenteral nutrition
and invasive devices, clinical presentation if any, antimicrobial susceptibility pattern of MRSA isolates, therapeutic interventions, and outcome.
For the purpose of this study, any infant who had one
or more screening nasal specimens that yielded MRSA
was considered to be colonized, and infected cases were
considered to be those with a clinical isolate of MRSA
from one or more non-nasal or pharyngeal specimens, or
clinical signs/symptoms requiring antimicrobial therapy.
The ST1-MRSA outbreak period was defined as the
time between admission of the first ST1-MRSA case and
the discharge of the last case (April 3 to August 12,
2011). The study protocol was approved by the Ethics
Committee of the Azienda Ospedaliero-Universitaria
Policlinico “P. Giaccone”, Palermo, Italy, and informed
consent was sought in accordance with the principles of
the Declaration of Helsinki. Written informed consent
was obtained from the parents of each patient.
Laboratory methods
Surveillance specimens for MRSA culture were obtained
with cotton swabs and processed within 4 h. Swabs were
incubated overnight in Brain Heart Infusion broth, and
then inoculated onto mannitol salt agar, incubated in air
at 37°C and examined at 24 and 48 h. Presumptive
S. aureus isolates were identified according to standard
methods [7]. MRSA isolates were searched for by colony
screening onto oxacillin agar (Mueller-Hinton with oxacillin 6 mg/L) and confirmed using cefoxitin disks. Susceptibility testing of clinical isolates was carried out
using the Phoenix™ Automated Microbiology System
(Becton Dickinson Diagnostic Systems, Sparks, MD,
US). Antibacterial drug susceptibility of surveillance
isolates was routinely performed using the disk diffusion method by determining the susceptibility of each
isolate to erythromycin, clindamycin, sulfamethoxazoletrimethoprim, tetracycline, ciprofloxacin, gentamicin,
tobramycin, linezolid, rifampicin, vancomycin and teicoplanin [8]. S. aureus ATCC 25923 was used as the quality control strain.
Molecular typing
Polymerase chain reaction (PCR)-based strategies were
used to identify the structural type of the SCCmec element and the PVL genes (lukS-PV, lukF-PV) [4, 9, 10].
Multilocus sequence typing (MLST) was performed, as
previously described [11]. The MLST allelic profiles and
Giuffrè et al. BMC Pediatrics 2012, 12:64
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sequence types were assigned by submission to the S.
aureus MLST database (www.mlst.net).
Genotypic characterization of the MRSA isolates was
performed by multilocus variable number tandem repeat
analysis (MLVA) [12]. Patterns were digitized and analyzed using Bio-Numerics software (Applied Maths,
Ghent, Belgium).
Page 3 of 7
hospitalization and onset of colonization in the 14
cases colonized by ST1-MRSA-IVa, as detected by the
weekly active surveillance culture program, is illustrated
in Figure 3. No attempt was made to decolonize the
infants during the outbreak period. It was also impossible to assess the duration of MRSA colonization,
because 10 neonates remained colonized at discharge.
Two colonized infants died as a result of malformations.
Results
Description of the outbreak
Characterization of MRSA
Two MRSA isolates were identified from blood and the
first surveillance nasal sample of an infant, respectively,
on April 5, 2011. These isolates displayed a different
drug susceptibility pattern from that of the endemic
ST22-MRSA-IVa isolates, and were resistant to gentamicin, erythromycin and clindamycin, unlike the ST22
MRSA isolates. The patient was an extremely-lowbirthweight (ELBW) male infant, who had been transferred the previous day from the NICU of another
hospital in Palermo, Italy, where he was born on February 19. He required surgery because of an intestinal subocclusion (Table 1). Before admission, the patient was
exposed to a high colonization risk because of his prolonged stay in NICU and a previous transfer to a
pediatric surgical division. A further indistinguishable
isolate was detected in an axillary skin swab cultured on
April 26, after the onset of dermatitis. MLVA typing
immediately confirmed the introduction of a new strain
to the study NICU (Figure 1). He was treated empirically
with ampicillin-sulbactam and netilmicin for presumed
sepsis, and then with teicoplanin and meropenem after
the blood culture yielded MRSA. His clinical condition
improved progressively and no further symptoms of
MRSA infection had developed up to discharge.
On May 5, a second MRSA strain resistant to gentamicin, erythromycin and clindamycin was identified
from the nasal swab of another outborn infant who had
been admitted the day before the index case (Table 1).
This was a female ELBW infant who was admitted
to the NICU because of necrotizing enterocolitis with
intestinal perforation. She underwent two laparotomy
interventions on April 4 and 27, respectively, and was
prescribed ampicillin-sulbactam, netilmicin, vancomycin
and meropenem. MRSA with characteristics indistinguishable from the nasal swab isolate was detected from
the endotracheal tube on May 20, and from the weekly
surveillance nasal swab until discharge. Microbiological
cultures yielded no further pathogens and her clinical
condition gradually improved.
An increase in the MRSA isolation rate in the NICU
was observed between May and August 2011 (Figure 2).
A further 12 (15.2%) of 79 neonates who were admitted
during the outbreak period were found to be colonized
by the new MRSA strain. The temporal distribution of
All the MRSA isolates identified by the surveillance
screening program during the ST1-MRSA outbreak period
were submitted to antibiotic susceptibility testing, PCR for
the SCCmec element and PVL genes, MLST and MLVA
typing. Between one and thirteen isolates were available
from each patient, depending on their lengths of stay.
Antimicrobial susceptibility testing of all MRSA isolates
from the 14 infants involved in the outbreak indicated
resistance to β-lactam antibiotics, gentamicin, erythromycin, clindamycin and tetracycline, but susceptibility
to ciprofloxacin, linezolid, rifampicin, sulfamethoxazoletrimethoprim, teicoplanin, tobramycin and vancomycin.
All the isolates carried a SCCmec cassette type IVa
and were negative for the PVL genetic determinants. In
addition, MLST demonstrated that they belonged to
ST1. MLVA showed that all isolates from the 14 infants
had electrophoretic profiles indistinguishable from each
other, but quite different from those of the ST22 isolates
(Figure 1).
Infection control measures
Infection control measures were reviewed and reinforced.
These included special attention to hand disinfection and
environmental cleaning. Anyone caring for an infant
infected/colonized by MRSA was required to wear a facemask, gown and gloves. Infected and colonized infants
were placed under contact precautions and cohorted in
the NICU. All equipment and caring devices in the NICU
were thoroughly cleaned and disinfected. All NICU nursing and medical personnel were informed of the outbreak
and training sessions on infection control practices and
modes of transmission of MRSA were arranged. Outbreak
meetings identified the high prevalence of patients admitted to the NICU for surgery or malformations during the
outbreak period as the likely major triggering factor, with
cross-transmission via the hands of HCWs as the likely
major cause of dissemination of the ST1 strain within the
NICU. No additional factors were identified. The outbreak was considered ended on August 12, when the last
colonized patient was discharged.
Discussion
MRSA colonization and infection in infants are associated with significant morbidity and economic impact
Case
Gender
Birth date
Admission
date
Inborn/
outborn
Gestational
age at birth
(week)
Weight at
birth (g)
Delivery
Reason for
admission
Length
of stay
(days)
Date of first
isolation of
ST1-MRSA-IVa1
Risk factor(s)
Outcome
1
F
March 28
April 3
outborn
28
760
CS
surgery
45
May 5
CVC, ET, nCPAP, TPN
discharged
22
M
February 19
April 4
outborn
29
960
CS
surgery
35
April 5
CVC, ET, nCPAP
discharged
3
F
May 9
May 9
outborn
35
2240
CS
respiratory distress
19
May 10
CVC
discharged
4
F
May 16
May 16
inborn
39
2770
CS
malformation
41
June 14
CVC, ET
died
5
F
May 4
May 17
outborn
37
2660
VD
malformation
793
June 28
CVC, ET, nCPAP
discharged
6
M
May 17
May 17
inborn
30
1420
CS
preterm care
42
May 24
CVC, nCPAP
discharged
7
F
June 6
June 6
inborn
39
3090
VD
malformation
49
July 12
CVC
discharged
8
F
June 11
June 11
outborn
27
870
CS
preterm care
62
June 28
CVC, ET, nCPAP, TPN
discharged
9
F
June 12
June 13
outborn
30
1450
CS
preterm care
41
July 5
CVC, ET, nCPAP
discharged
10
M
June 19
June 19
inborn
36
2380
CS
respiratory distress
12
June 28
none
discharged
11
F
June 22
June 22
inborn
33
1360
CS19
malformation
26
July 12
CVC, ET, nCPAP, TPN
died
12
F
July 7
July 7
outborn
37
1760
CS
malformation
22
July 12
none
discharged
13
F
July 13
July 13
inborn
39
4220
CS
respiratory distress
7
July 19
none
discharged
14
M
July 17
July 18
inborn
42
1980
VD
respiratory
distress
14
July 19
none
discharged
Giuffrè et al. BMC Pediatrics 2012, 12:64
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Table 1 Characteristics of infants colonized with ST1-MRSA-IVa in an NICU in Palermo, Italy, 2011
CS = caesarian section, VD = vaginal delivery, CVC = central venous catheter, ET = endotracheal tube, nCPAP = nasal continuous positive airway pressure, TPN = total parenteral nutrition.
weekly screening.
index case.
3
transferred to a cardiac surgery ward after 69 days of NICU stay and re-admitted after 6 days.
1
2
Page 4 of 7
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Figure 1 Multilocus variable number tandem repeat analysis
(MLVA) of some representative isolates of methicillin-resistant
Staphylococcus aureus (MRSA) identified during the outbreak
period in the neonatal intensive care unit (NICU) under study.
Lanes: 1 and 10, 500-bp DNA ladder; 2, 4, 5 and 8, ST22-MRSA-IVa
isolates; 3,6,7 and 9, ST1-MRSA-IVa isolates.
[13]. ELBW infants are particularly fragile individuals
who may develop severe diseases. Several possible reservoirs and multiple sources of exposure to MRSA have
been reported for infants hospitalized in nurseries and
NICUs [14], and transmission of the USA300 strain
among postpartum women affected by skin and soft
tissue infections has been described [15]. Cases of CAMRSA transmission associated with breast milk or
carriage by a family member have also been reported
[16, 17]. MRSA skin and soft tissue infections among
full-term newborns were detected in the first 30 days
since their delivery in US hospitals, as well as in neonates
Page 5 of 7
discharged from a nursery [18]. Moreover, previous
studies have identified HCWs as reservoirs [19-21].
In the current study, the index case was an infected infant born elsewhere. A second, long-stay, crosscolonized patient likely became the main reservoir of
MRSA, while subsequent cross-transmission probably
occurred via the hands of staff. MRSA screening at
admission and HCW screening were not in place when
the index case was admitted, but the weekly surveillance
nasal swabs were obtained within 24 h of this patient’s
admission, suggesting that ST1-MRSA-IV was imported
from another healthcare facility on this occasion. However, alternative or concurrent exposure sources, such
as previously colonized infants or HCWs, cannot be
entirely ruled out. Indeed, early acquisition of MRSA
soon after hospitalization has been described previously
[21]. Moreover, because the nares were the only surveillance sampling sites, it is possible that infants colonized
at other sites could have escaped detection. In this
regard, it has been suggested that sampling sites traditionally associated with HA-MRSA, such as the nose,
could lack sensitivity when screening for CA-MRSA
colonization [22].
The issue of HCWs as a possible exposure source of
MRSA, and especially of CA-MRSA, is widely debated
[23]. Although HCWs have been implicated as the
source of MRSA in many NICU outbreaks, there are
conflicting reports regarding the cost-effectiveness of
HCW screening and decolonization [18, 19, 24]. Evidence of transmission of MRSA from HCWs to patients
in an outbreak setting ranges from 5.8–25.5% of cases,
with an even lower proportion caused by asymptomatic
carriers [25, 26]. Moreover, data about the positive impact of HCW screening and decolonization are difficult
Figure 2 Epidemic curve of methicillin-resistant Staphylococcus aureus (MRSA)positive cases during the outbreak period. Curve shows
the number of infants whose nasal swabs tested positive for ST1-MRSA-IVa and ST22-MRSA-IVa and the number of hospitalized infants by week.
Giuffrè et al. BMC Pediatrics 2012, 12:64
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Page 6 of 7
Figure 3 Time course of hospitalization and onset of ST1-MRSA-IVa colonization, as assessed by the weekly surveillance screening
program, during the outbreak at the NICU under study.
to assess, because both interventions are usually implemented as a part of a composite pattern of infection
control procedures [20, 23, 27]. Decolonization of staff
and patients by mupirocin proved unable to control a
NICU outbreak, according to Lepelletier et al. [28]. In
addition, a decline in the incidence of MRSA infections
in hospital over a 7-year surveillance period was shown
to persist, despite an interruption to routine HCW
screening after the first 4 years [29]. However, the involvement of the HCWs was not assessed in the current
study, which represents a substantial limitation. ST1MRSA carriage by the staff of the NICU was, however,
thought to be unlikely the because transmission chain
was ultimately interrupted without the adoption of
screening and decolonization procedures for HCWs.
Nonetheless, emergence of CA-MRSA strains as HA
pathogens presents a challenge for MRSA control strategies through the increasingly probable reintroduction
of CA-MRSA from the community reservoir [29,30].
Within such an epidemiological framework, HCWs as
well as patient’s visitors could play critical roles as
potential CA-MRSA traders in NICU outbreaks [3].
Consequently, screening and decolonization of HCWs
could be more effective, and should be recommended
when dealing with CA-MRSA.
This study had some limitations. As mentioned above,
HCWs were not screened either as part of the routine
surveillance program or during the outbreak phase.
Moreover, infants were not routinely screened at admission, which could have biased the source attribution of
the ST1-MRSA-IV strain. Finally, the specific NICU setting and local epidemiology of CA-MRSA make it difficult to generalize from the findings.
Conclusions
The present investigation showed that traditional
approaches for the control of HA-MRSA were also
effective in terminating CA-MRSA transmission in the
NICU setting. Molecular typing by MLVA helped to
clarify the epidemiological features of this CA-MRSA
outbreak quickly, by identifying the outbreak ST1MRSA-IVa strains from the background of the endemic
EMRSA-15 colonization cases.
HA transmission of CA-MRSA strains, as well as increasing non-β-lactam resistance in CA-MRSA clones,
present increasingly serious challenges to infection control and the clinical management of infections caused by
these strains. Monitoring of global and local epidemiologies is critical to assess epidemiological trends and to
guide empiric antibiotic options.
Abbreviations
MRSA: Methicillin-resistant Staphylococcus aureus; CA-MRSA: Communityassociated MRSA; ELBW: Extremely-low-birthweight; HA-MRSA: Hospitalassociated MRSA; HCW: Healthcare worker; NICU: Neonatal intensive care
unit; PCR: Polymerase chain reaction; PVL: Panton-Valentine leucocidin;
MLST: Multilocus sequence typing; MLVA: Multilocus variable number
tandem repeat analysis; SCCmec: Staphylococcal chromosomal cassette mec.
Competing interests
The authors declare that they have no competing interests.
Author details
1
Department of Mother and Child, University of Palermo, I-90127 Palermo,
Italy. 2Department of Sciences for Health Promotion “G. D’ Alessandro”,
University of Palermo, Via del Vespro 133, I-90127 Palermo, Italy. 3PhD School
in Food and Human Nutrition, University of Palermo, I-90127 Palermo, Italy.
Authors’ contributions
MG, DC, GC and CM designed and supervised the study and drafted the
manuscript. SD and FN carried out the study in the field, by participating in
the surveillance program, and contributed to the interpretations of results.
DMG was in charge of isolation, identification and susceptibility testing. AA
and CB were in charge of molecular typing. All authors have read and
approved the final manuscript.
Received: 11 January 2012 Accepted: 8 June 2012
Published: 8 June 2012
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doi:10.1186/1471-2431-12-64
Cite this article as: Giuffrè et al.: Epidemic spread of ST1-MRSA-IVa in a
neonatal intensive care unit, Italy. BMC Pediatrics 2012 12:64.
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