Colonization with Methicillin-Resistant Staphylococcus

aureus After Liver Transplantation

Guilherme Santoro-Lopes, Erika Ferraz de Gouvea, Rodrigo Carreira M. Monteiro,
Rodrigo Castelo Branco, Jose Rodolfo Rocco, Marcia Halpern,
Adriana Lucia Pires Ferreira, Elaine Gama Pessoa de Araujo, Samanta T. Basto,
Vinicius Gomes Silveira, and Joaquim Ribeiro-Filho
Methicillin-resistant Staphylococcus aureus (MRSA) is a
frequent cause of infection after orthotopic liver transplantation (OLT). Colonization with MRSA is associated
with a higher risk of infection. Previous studies have
shown a high prevalence of MRSA colonization among
OLT candidates. However, the risk of colonization with
MRSA after OLT is still unclear. The objective of this
study was to estimate the incidence and the factors associated with colonization with MRSA after OLT. This was
a prospective cohort study including patients submitted
to OLT between the years 2000 and 2002. Surveillance
cultures of nasal swab specimens were performed within
the 1st 72 hours of hospital admission and, subsequently,
on weeks 2, 6, 13, and 26. Patients whose baseline cultures
revealed nasal carriage of MRSA were excluded. A total of
60 patients were included in the study. The median follow-up was 72 days. A total of 9 patients (15%) became
colonized. In multiple logistic regression analyses, the use
of a urinary catheter for >5 days (P .006), postoperative bleeding at the surgical site (P .009), and preoperative use of uoroquinolones (P .08) were associated
with a higher risk of colonization. Patients without any of
these risk factors did not become colonized. In conclusion, nasal carriage of MRSA is frequently acquired after
OLT. Periodic postoperative screening for MRSA carriage
should be an integral component in programs designed to
reduce nosocomial MRSA transmission in these patients.
Further studies are needed to set up and validate a predictive model that could allow targeting postoperative
screening to high-risk OLT recipients. (Liver Transpl
2005;11:203209.)

nfections with methicillin-resistant Staphylococcus

aureus (MRSA) have been associated with prolongation of hospital stay and higher hospital charges.1 3
Some studies have also suggested that MRSA infections
may be associated with higher mortality when compared with methicillin-sensitive Staphylococcus aureus
infections.4 7
MRSA infections frequently complicate the postoperative course of orthotopic liver transplant (OLT)
recipients.8 11 In some centers, MRSA has become the
leading multidrug resistant pathogen causing infection
after OLT.12 Different studies have reported that OLT
recipients that were colonized with MRSA on admission for transplantation had a high incidence of MRSA
infection, ranging from 31 to 88%.9 11 Nonetheless, in

these studies, the incidence of MRSA infection among

patients who were not nasal carriers at admission,
although signicantly lower as compared with patients
with preoperative colonization, was also high, ranging
from 9 to 24%.9 11 These data suggest that transmission of MRSA to a relevant proportion of OLT recipients occurs in the postoperative period. However, to
our knowledge, no study has specically assessed the
risk of postoperative acquisition of MRSA carriage in
these patients.
The aim of this study was to determine the incidence
of nasal colonization with MRSA after OLT and to
assess the factors associated with it.

Patients and Methods

This prospective cohort study was carried out at Hospital
Universitario Clementino Fraga Filho, a 350-bed teaching
hospital, afliated to the Federal University of Rio de Janeiro,
Brazil. All patients who underwent OLT between October
2000 and June 2002 were eligible for the study. The exclusion
criteria were the isolation of MRSA in the baseline surveillance culture, and death transfer to another hospital within
the 1st postoperative week. The study protocol was approved
by the Institutional Research Board. Only patients who
signed an informed consent were included in the study.
Baseline nasal swab specimens were routinely collected
within the 1st 72 hours of hospital admission for OLT. Follow-up nasal specimens were collected at postoperative weeks
2, 6, 13, and 26, and at each new hospital admission within
the 1st 6 postoperative months. Swabs were moistened with

Abbreviations: MRSA, methicillin-resistant Staphylococcus

aureus; OLT, orthotopic liver transplant; ICU, intensive care unit.
From the Hospital Universitario Clementino Fraga Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
Supported in part by Conselho Nacional de Pesquisa (CNPq)
(470550 / 2001-5) and by CAPES.
Address reprint requests to Guilherme Santoro-Lopes, Rua Justiniano
da Rocha 201 / 302, Vila Isabel , Rio de Janeiro, CEP: 20551-010,
Brazil. Telephone: 55-21-25622725; Fax: 55-21-25901615; E-mail:
santorolopes@hucff.ufrj.br
Copyright 2005 by the American Association for the Study of
Liver Diseases
Published online in Wiley InterScience (www.interscience.wiley.com).
DOI 10.1002/lt.20338

Liver Transplantation, Vol 11, No 2 (February), 2005: pp 203 209

203

204

Santoro-Lopes et al.

physiologic saline and gently rotated in the right and left

anterior nares. Specimens were sent to the laboratory within
30 minutes and plated onto mannitol salt agar. Staphylococcus
aureus was identied by means of standard microbiological
methods. Resistance to oxacillin was determined by use of the
disk diffusion test performed on Muller-Hinton agar after
incubation for 24 48 hours.
Contact precautions were taken in every patient in whom
nasal carriage of MRSA was detected. Decolonization with
intranasal mupirocin (3 times per day) and daily chlorhexidine baths, both for 5 days, was prescribed only after surgical
wounds were healed. Therefore, in most cases, decolonization
was attempted only after hospital discharge. Patients who
were not effectively decolonized had their medical chart
agged and contact precautions were routinely used in these
cases at the time of readmission.
The end of follow-up for patients who became colonized
was dened as the date of the diagnosis of colonization with
MRSA. For all other patients, the end of follow-up was
dened as the last date a nasal swab specimen was collected
within the 1st 180 days after OLT.
Additional baseline and follow-up data collected in each
patient included: 1) demographic and preoperative clinical
data (gender, age, Child-Turcotte-Pugh score, etiology of the
underlying hepatic disease, the presence of diabetes mellitus,
hospital admissions, and the use of antibiotics within the
previous 6 months); 2) transplant surgery-related data (operation time, number of red blood cell concentrates, and plasma
units transfused); 3) data associated with postoperative care
(acute physiology and chronic health evaluation [APACHE
II13], simplied acute physiology score [SAPS II14], and sepsis-related organ failure assessment [SOFA15] scores, immunosuppressive therapy, number of antimicrobial drugs used
for 72 hours, length of use of invasive devices, length of
hospital and intensive care unit (ICU) stay; and 4) data on
postoperative complications (rejection, hepatic artery or portal vein thrombosis, bleeding at the surgical site, new operation, maximum serum levels of creatinine, and liver function
tests observed during follow-up). APACHE II, SAPS, and
SOFA scores were recorded within the 1st 24 hours after
admission to the ICU.

Postoperative Management Protocol

Perioperative antimicrobial prophylaxis consisted of ampicillin plus sulbactam for 48 hours. Patients who reported allergy
to penicillin received clindamycin and ciprooxacin during
the same period. Immediately after transplantation, patients
were admitted to an 8-bed surgical ICU, where they remained
until they could be weaned from mechanical ventilation. After
ICU discharge, patients were transferred to small single or
double rooms. Prophylaxis for Pneumocystis carinii infections
consisted of 160 mg of trimethoprim plus 800 mg of sulfametoxazol daily, for 1 year. Immunosuppression for patients
who had chronic infection with hepatitis B or C viruses consisted of corticosteroids and a calcineurin inhibitor (tacroli-

mus or cyclosporin). Azathioprine was additionally used for

the immunosuppression of patients with other indications for
OLT.

Statistical Analysis
Quantitative variables are described by their median and
interquartile range. Categorical variables are described by
their absolute counts and percents. The possible association of
nasal colonization with MRSA and the studied covariates was
analyzed with the Mann-Whitney test (for quantitative variables) and with the 2 or Fishers exact test (for categorical
variables). Forward stepwise logistic multiple regression analysis was used to determine which factors were independently
associated with postoperative MRSA colonization. Covariates
associated with a P .1 in the univariate analyses were
included in the logistic regression analyses. The nal regression model included covariates associated with a P .25 in
the adjusted analysis. All tests were 2-tailed. SPSS for Windows 9.0 (SPSS, Chicago, IL) was used in the statistical analyses.

Results
A total of 80 OLTs were performed during the study
period. A total of 13 patients did not sign the informed
consent and, thus, were not included in the study. Of
the 67 patients who were enrolled in the study, 7 were
eventually excluded. Reasons for exclusion were: nasal
colonization by MRSA diagnosed in the baseline culture (n 2; 3%), death (n 4; 6%), or transfer to
another hospital (n 1;, 1.5%) within the 1st postoperative week.
A total of 60 patients were included in the study.
Perioperative prophylaxis with clindamycin and ciprooxacin were used for perioperative prophylaxis in 5
patients (8%) who were allergic to penicillin. In 17
patients (28%) methicillin-sensitive Staphylococcus
aureus was isolated in the baseline culture. A total of 7
(41%) methicillin-sensitive Staphylococcus aureus carriers and 12 (28%) of the noncolonized patients had used
a uoroquinolone within the previous 6 months (P
.32).
The median follow-up was 72 days (interquartile
range: 17-178 days). Nasal colonization with MRSA
was detected in 9 patients (15%; 95% condence interval: 6 24%). The median time for MRSA acquisition
was 24 days (range 8-119 days). In 5 cases (56%) colonization was only detected after discharge from the
ICU.
The results of the univariate analyses assessing the
association between MRSA colonization and demo-

205

MRSA Colonization After OLT

Table 1. Association Between Colonization With MRSA Colonization After Liver Transplantation and Demographic and
Preoperative Variables*

Variables

Colonized patients
(n 9)

Noncolonized patients
(n 51)

60 (48 63)
6 (67)
7 (78)
7 (78)
2 (22)
6 (67)
7 (78)

52 (41 58)
32 (63)
31 (61)
30 (59)
5 (11)
14 (28)
12 (24)

.09
1.0
.46
.46
.28
.05
.003

Age (years)
Male gender
Child-Turcotte-Pugh score 10
Chronic HCV infection
Diabetes mellitus
Hospital admission within the previous 6 months
Preoperative use of a uoroquinolone
Abbreviations: HCV, hepatitis C virus.
*Results of univariate analyses.
Median (interquartile range).
n (percent).

graphic and preoperative covariates are shown Table 1.

MRSA colonization was signicantly associated with
the use of a uoroquinolone (P .003) in the previous

6 months. There was also a trend for an association

between postoperative colonization and hospital admission within 6 months before OLT (P .05). Table 2

Table 2. Association Between MRSA Colonization After Liver Transplantation and Perioperative and Postoperative Variables

Variables
Operation time (hours)
Transfusions during OLT surgery
Packed red blood cells (units)
Plasma (units)
Length of use of devices (days)
Endotracheal tube
Central venous catheter
Indwelling urinary catheter
Swan-Ganz catheter
Arterial catheter
Maximum serum creatinine (mg%)
Maximum total bilirubin (mg%)
Maximum ALT U/mL
Maximum AST U/mL
Maximum Gama-GT U/mL
Apache II score
SAPS II score
SOFA score
Tacrolimus (vs. cyclosporin)*
Length of stay in ICU (days)
Length of hospital stay (days)
Bleeding at the surgical site*
New laparotomy*
Acute rejection*
Hepatic artery/portal vein thrombosis*
Number of antibiotics used for 72 hours

Colonized patients
(n 9) Median (IQR)

Non-colonized patients
(n 51) Median (IQR)

16 (9.5 17)

12 (11 15)

.38

6 (2.5 16)
5 (1 10.5)

4 (2 7)
3 (0 6)

.18
.27

3 (1 6.5)
8 (7 10)
6 (5 8)
3 (1.5 4.5)
3 (1.5 5)
1.6 (1.2 2.8)
2.6 (1.3 13.0)
363 (130 572)
170 (93 525)
603 (287 1052)
13 (9 16)
27 (23 41)
7 (6 13)
6 (67)
6 (4 11.5)
17 (11 25.5)
4 (44)
4 (44)
1 (11)
3 (33)
2 (1 3)

1 (.5 2)
4 (3 7)
3 (2 4)
2 (1 3)
1 (1 2)
1.8 (1.4 2.4)
7.3 (1.7 12.4)
272 (193 595)
191 (98 426)
798 (498 1489)
9 (11 13)
19 (13 25)
7 (6 8)
25 (49)
3 (2 4)
14 (10 25)
3 (6)
5 (10)
12 (24)
7 (14)
0 (0 2)

.024
.007
.003
.085
.03
.56
.34
.81
.90
.42
.31
.006
.62
.27
.023
.53
.007
.09
.67
.16
.018

Abbreviations: IQR, interquartile range; OLT, orthotopic liver transplantation; ICU, intensive care unit; AST, aspartate aminotransferase; ALT, alanine aminotransferase.
*Categorical data presented as absolute count (percent).

Results of univariate analyses.

206

Santoro-Lopes et al.

Table 3. Variables Associated With MRSA Colonization After Liver Transplantation*

Variables
Urinary catheter 5 days
Bleeding at the surgical site
Preoperative use of a uoroquinolone

Odds ratio (95% condence interval)

22.58 (1.48 345)

26.0 (1.46 464)
8.38 (0.57 123)

.006
.009
.08

*Results of multiple logistic regression analyses.

presents the results of the univariate analyses that

assessed the association between nasal colonization with
MRSA and the variables related to transplant surgery
and postoperative care. MRSA colonization was significantly associated with: longer stay in ICU (P .023),
longer use of invasive devices such as endotracheal tube
(P .024), indwelling urinary catheter (P .003),
central venous catheter (P .007), arterial catheter
(P .03), the number of antibiotics used (P .018),
the simplied acute physiology score recorded on
admission to the ICU (P .006), and the occurrence of
postoperative bleeding at the surgical site (P .007).
Nasal colonization with MRSA also tended to be associated with older age (P .09), the longer use of SwanGanz catheters (P .085) and the performance of a
new laparotomy (P .09). Nasal carriage of MRSA was
detected in 4 of 18 patients (22%) treated with a uoroquinolone after OLT and in 5 (12%) other patients
(P .3).
In the multivariate analyses (Table 3), the use of a
urinary catheter for 5 days (P .006) and bleeding at
the surgical site (P .009) independently predicted
colonization with MRSA. Preoperative use of a quinolone (P .08) also tended to be associated with a higher
risk of colonization. There was also a signicant correlation between the number of these risk factors that
were found in each patient and the probability of
acquiring nasal carriage of MRSA (Spearmans rank
correlation coefcient .59; P .001). MRSA colonization was not observed among the 32 patients in
whom these 3 factors were absent, but it occurred in 1
of the 11 patients with 1 risk factor, 6 of the 14 patients
with 2 risk factors, and in the 2 patients with 3 risk
factors.
MRSA infections were diagnosed in 2 patients who
acquired nasal colonization (22%) and in 1 of the noncolonized patients (2%) (P .076). Hepatic abscesses
occurred in the 2 MRSA carriers and peritonitis was
diagnosed in the noncolonized patient.

Discussion
In this study, 15% of the OLT recipients acquired nasal
colonization with MRSA during the 1st 6 months of
follow-up after transplantation. To our knowledge, the
risk of postoperative colonization with MRSA among
OLT recipients had not been previously assessed. Similar studies carried out among other groups of patients
admitted to ICUs have yielded variable results. The
incidence of MRSA colonization in these studies ranged
from 5 to 56%.16 19 Most of this wide variation is
probably explained by differences among institutions
with regards to the endemicity of MRSA and to the
infection control strategies employed. The present
study was uncontrolled, thus we could not determined
if the rate of colonization among OLT recipients was
signicantly different from that observed in other
patients admitted to the same surgical ICU.
As in most studies that assessed the colonization of
OLT recipients with MRSA,8 10 we restricted the
screening to cultures of nasal specimens. The additional
collection of cutaneous (from wounds, axilla, and
groin)11 and rectal20 samples have been associated with
an increase in the sensitivity for detection of MRSA
colonization that ranged from 8 to 21% among OLT
recipients and other patients admitted to a surgical
ICU. Therefore, it is probable that the incidence of
colonization was underestimated in this study. On the
other hand, the cost-effectiveness of the use of a more
extensive screening routine for OLT recipients that
included the collection of other specimens in addition
to nasal swabs has not yet been established.
Preoperative colonization with MRSA has been
associated with increased risk for MRSA infection after
transplantation.8 11 A similar trend was observed in
this study, but the small number of cases of infection
that occurred in this sample did not allow any conclusion about the risk for MRSA infection among OLT
recipients who became nasal carriers after transplantation. Although decolonization with intranasal mupiro-

MRSA Colonization After OLT

cin has been shown to reduce the incidence of postoperative infections in other groups of surgical patients
who were nasal carriers of Staphylococcus aureus,21
results of a similar study carried out in liver transplant
candidates and recipients were disappointing.22 Despite
the documentation of successful decolonization in 87%
of the patients in the study of Paterson et al.,22 the
incidence of S. aureus infections, most of them caused
by MRSA, was not reduced in comparison with the
results those authors observed in a historical cohort.
Persistence of S. aureus carriage at sites that were not
affected by the use of intranasal mupirocin may have
inuenced the results of that study. Nonetheless, the
frequent hand carriage of MRSA among health care
workers, the fact that 2 strains of MRSA were shared by
multiple patients, and the frequent occurrence of
MRSA infections in patients who were not nasal carriers
suggested that persistence of unabated nosocomial
transmission of MRSA might also explain the lack of a
benecial effect of decolonization in that study.22
Studies carried out in other groups of patients have
shown that the implementation of control measures
aimed at the reduction of MRSA transmission has been
followed by a signicant reduction in the rate of MRSA
infection.23 The spread of MRSA occurs mainly from
person to person via contact with contaminated health
care workers hands and clothes or contaminated equipment. Patients with unrecognized colonization are
important reservoirs for MRSA transmission.24,25 Successful programs of containment of MRSA dissemination are based on the screening of high risk patients for
the early identication of reservoirs and the timely institution of control measures, such as barrier precautions
and reinforcement of hand hygiene. On-admission
screening targeted to high risk patients, including organ
transplant recipients, has been demonstrated to be the
most cost-effective procedure for detection of occult
MRSA carriage in acute care endemic settings.26
Although this procedure has been routinely in use in
our institution during the time this study was performed, the incidence of postoperative colonization
with MRSA among OLT recipients who had negative
surveillance cultures on admission was high. In approximately 50% of the cases, colonization was detected by
surveillance cultures only after discharge from the ICU.
This nding suggests that OLT recipients should be
periodically screened for MRSA carriage along all their
hospital stay and not only at admission.
In this study, the use of a urinary catheter for 5
days and the occurrence of postoperative bleeding at the
surgical were independently associated with MRSA colonization. These factors are probably surrogate markers

207

for the need of a more intense manipulation by health

care workers, which may increase the probability of
MRSA transmission. In fact, Dziekan et al.27 have
observed that the required intensity of care was independently associated with the risk of MRSA transmission during an outbreak at a large university hospital.
The use uoroquinolones in the 6 months preceding
transplantation also tended to be associated with the
risk of MRSA acquisition in the multivariate analyses.
This association was not reported in previous studies
carried out in OLT candidates and recipients.8 11
Nonetheless, this nding is consistent with the results
of other studies that analyzed the factors associated with
the acquisition27,28 or the persistent carriage of
MRSA.29 The mechanisms that may explain the association between uoroquinolone use and the increased
risk of acquisition of MRSA have not been fully elucidated. The possibility that the use of these antimicrobials could be a surrogate of more severe disease27 is not
supported by the nding that there was no signicant
association between the preoperative Child-TurcottePugh score and the incidence of colonization. Eradication of microorganisms susceptible to these drugs that
colonize the skin and mucous membranes may favor the
colonization of these sites with MRSA strains resistant
to uoroquinolones. The possibility that exposure to
subinhibitory concentrations of these drugs may cause
the selection of subpopulations of heteroresistant
MRSA that are resistant to both oxacillin and the quinolones has also been proposed.30 Additionally, it has
been shown that both methicillin-sensitive Staphylococcus aureus and MRSA strains exposed to subinhibitory
concentrations of ciprooxacin exhibited increased
attachment to bronectin-coated surfaces as a result of
the increased expression of the staphylococcal bronectin-binding protein.31 However, opposite results have
been reported by other authors.32 The nonsignicant
trend for a more frequent preoperative exposure to uoroquinolones among patients who were colonized with
methicillin-sensitive Staphylococcus aureus at baseline is
in accordance with the hypothesis of an increase in S.
aureus adhesiveness following exposure to these drugs.
The possibility that low-density preoperative carriage of
MRSA, not detected at the baseline screening, was
already present in some of the patients who used a
uoroquinolone before OLT can not be precluded.
The identication of factors that predict an
increased risk for MRSA carriage after OLT may help to
target screening to patients with higher risk of colonization and, therefore, to increase the cost-effectiveness
of programs designed to limit MRSA spread among
OLT recipients. In this study, patients who did not

208

Santoro-Lopes et al.

present any of the risk factors identied in the multivariate model did not become nasal carriers. In addition, there was a signicant correlation between the
number of risk factors present in each patient and the
probability of acquiring nasal carriage of MRSA. Nevertheless, it must be recognized that the limited statistical power of this study may have precluded the identication of other covariates that could be
independently associated with MRSA colonization in
this population. The wide condence intervals associated with the odds ratio estimates in the logistic regression model also reect this limitation in the statistical
power. These facts may reduce the applicability of our
ndings.
In summary, a high incidence of postoperative
MRSA colonization was observed among OLT recipients in our hospital. This nding suggest that periodic
screening for MRSA colonization during a hospital stay
should be an integral component in programs designed
to reduce MRSA transmission among OLT recipients.
Longer use of indwelling urinary catheter, postoperative bleeding at the surgical site, and the use of uoroquinolones before transplantation were associated with
MRSA colonization in the adjusted logistic regression
model. Patients without any of these risk factors did not
become colonized. These results suggest that it may be
possible to target surveillance cultures to OLT recipients who have risk factors for MRSA colonization and,
consequently, to increase the cost-effectiveness of postoperative screening. However, further studies with
larger samples are needed to set up and validate predictive models for MRSA colonization in these patients.

Acknowledgments

5.

6.

7.

8.

9.

10.

11.

12.

13.

14.

15.

We thank Dr. Carmem Lucia Pessoa-Silva and Dr. Ana Maria

Felix de Pinho for reviewing the manuscript.
16.

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