Pasricha et al. Antimicrobial Resistance and Infection Control 2013, 2:17
http://www.aricjournal.com/content/2/1/17
SHORT REPORT
Open Access
Methicillin-resistant Staphylococcus aureus risk
profiling: who are we missing?
Janet Pasricha1,5, Stephan Harbarth1*, Thibaud Koessler2, Veronique Camus1, Jacques Schrenzel3, Gilles Cohen4,
Didier Pittet1, Arnaud Perrier2 and Anne Iten1
Abstract
Background: Targeted screening of patients at high risk for methicillin-resistant Staphylococcus aureus (MRSA)
carriage is an important component of MRSA control programs, which rely on prediction tools to identify those
high-risk patients. Most previous risk studies reported a substantial rate of patients who are eligible for screening,
but failed to be enrolled. The characteristics of these missed patients are seldom described. We aimed to determine
the rate and characteristics of patients who were missed by a MRSA screening programme at our institution to see
how the failure to include these patients might impact the accuracy of clinical prediction tools.
Findings: From March-June 2010 all patients admitted to 13 internal medicine wards at the University of Geneva
Hospital (HUG) were prospectively screened for MRSA carriage. Of 1968 patients admitted to the ward, 267 patients
(13.6%) failed to undergo appropriate MRSA screening. Forty-one (2.4%) screened patients were MRSA carriers at
admission. On multivariate regression, patients who were missed by screening were more likely to be aged < 50 years
(OR 2.4 [1.4-3.9]), transferred to internal medicine from another ward in the hospital (OR 2.8 [1.1-7.1]), and have a history
of malignancy (OR 3.2[2.1-5.1]). There was no significant difference in the rate of previous MRSA carriage between
screened and unscreened patients.
Conclusions: Our findings highlight the potential bias that “missed” patients may introduce into MRSA risk scores.
Reporting on the proportions and characteristics of missed patients is essential for accurate interpretation of MRSA
prediction tools.
Keywords: Carrier state, Epidemiology, MRSA, Prevalence, Probability, Predictive value of tests, Staphylococcal infection,
Switzerland
Findings
Introduction
Prevention and control of MRSA cross infection is among
the most important challenges of infection control. Surveillance of all patients for MRSA carriage on admission
to hospital allows those patients colonised with MRSA to
be isolated and contact precautions undertaken, with the
aim of minimising spread to other patients. As patients
with MRSA evident on routine clinical specimens represents a small fraction of the burden of MRSA, surveillance
is needed to identify the reservoir of colonised but not
infected patients [1,2]. However, universal surveillance utilises significant healthcare resources, and its effectiveness
* Correspondence: stephan.harbarth@hcuge.ch
1
Infection Control Program, University of Geneva Hospitals and Faculty of
Medicine, 4 Rue Gabrielle Perret-Gentil, Geneva 1211, Switzerland
Full list of author information is available at the end of the article
is debatable [3-5]. Despite this, screening is increasingly
utilised in hospital MRSA control programs, and is still
legislated in the United Kingdom and some states of the
USA [6,7]. To mitigate costs without sacrificing the effectiveness of surveillance, many MRSA screening programs
rely on clinical prediction tools to target patients at high
risk of MRSA carriage [5]. Several epidemiological studies
form the basis of these tools in which the major risk factors for MRSA carriage have been identified, including: a
history of MRSA colonization, admission to intensive care,
hospitalization in the previous 12 months, extensive contact with health care, previous receipt of antibiotic therapy
and skin or soft tissue infection at admission [8-12]. However, these studies report 5-83% of patients who were eligible for study, but not screened. The characteristics of
these missed patients are seldom described [11]. We examined the characteristics of patients who were missed
© 2013 Pasricha 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.
Pasricha et al. Antimicrobial Resistance and Infection Control 2013, 2:17
http://www.aricjournal.com/content/2/1/17
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during a MRSA surveillance study at our institution to ascertain whether their exclusion might introduce bias and
affect the accuracy of clinical prediction tools and risk
profiling. Specifically, we hypothesised that an important
proportion of patients would be missed by our MRSA
screening programme, and that these patients would differ
from those patients who were not missed.
screened and 39 (2.0%) patients underwent screening
but not within 48 hours of admission. Therefore, 267 patients (13.6%) failed to undergo appropriate MRSA screening. Forty-one (2.4%) screened patients were MRSA
carriers at admission. Patients who were missed during
MRSA screening were younger (57.1 years vs 61.6 years;
P < 0.0001) and a greater percentage had been transferred
to internal medicine from another hospital ward (7.0% vs
2.7%; P < 0.0001). The proportions of patients identified as
previous MRSA carriers was not significantly different between the screened and unscreened groups (9.6% vs
13.2%, respectively, P = 0.308). There was no significant
difference in the proportion of patients missed by screening on weekends as compared to weekdays. The results of
uni- and multivariate regression analysis of factors potentially associated with being missed for MRSA screening
are shown in the Table 1. On multivariate regression,
patients who were missed by screening were more likely
to be aged < 50 years, admitted to internal medicine from
another hospital, and have a history of malignancy.
Setting and methods
The University of Geneva Hospitals (HUG) are a 2200bed tertiary hospital network providing in- and outpatient
care to the Canton of Geneva. From March to June 2010 a
universal MRSA surveillance program was undertaken to
prospectively screen all patients consecutively admitted to
13 internal medicine wards. The primary aim of this study
was to determine the rate of MRSA carriage amongst patients admitted to internal medicine. Secondary aims included: to formulate a clinical prediction tool that would
accurately predict those patients at high risk of MRSA carriage on admission to internal medicine, and to: determine
the effectiveness of our programme to capture all patients
for screening. Over the study period, all patient admissions
to internal medicine were recorded and basic demographic and clinical data was collected. Further clinical
data were obtained by retrospectively accessing electronic
medical records. All patients >18 years of age were eligible
for screening and were screened for MRSA by pooled nose
and groin swabs. Trained ward nurses conducted the
screening seven days a week. Pooled samples were streaked
onto MRSAid agar (bioMérieux, Lyon, France) and then inoculated into a colistin-salt (CS) broth. When no MRSA
was detected on chromogenic agar at day 1, a second
MRSAid plate was inoculated using the overnight enrichment in the CS broth. Suspect colonies were confirmed by
a duplex polymerase chain reaction to assess the presence
of the mecA gene [13].
The proportion of patients who were eligible for, but did
not have MRSA screening was determined. Wilcoxon rank
sum tests and chi2-tests were used to assess differences
between screened and unscreened groups. Factors potentially associated with failure to screen were first evaluated
using univariate logistic regression. Variables with a
P value <0.2 were retained. Multivariate models were then
developed and variables were eliminated in a stepwise
fashion using likelihood ratio tests to compare each model
to the previous one (STATA 11.2; StataCorp, College
Station, Texas, USA).
Results
Of 1968 patients admitted to internal medicine, 1740
(88.4%) underwent admission screening within 48 hours
of admission. 228 (11.6%) admitted patients were not
Discussion
Screening patients for MRSA carriage on admission to
hospital is an increasingly important component of hospital MRSA control programs. Many programs rely on
prediction tools so that patients at high risk of MRSA carriage may be targeted for selective screening rather than
to utilise universal screening which is costly and resource
intensive. Ideally, prediction tools are formulated using
local epidemiological data from (universal) surveillance
studies. However, many of these studies report a substantial rate of patients who are eligible for screening, but fail
to be enrolled by the surveillance programme. The characteristics of these patients are seldom described.
In this study, 13.6% of patients failed to have admission
MRSA screening swabs performed. This rate of “missed”
screening opportunities is comparable to that found in
other MRSA risk profiling studies [8-11,14]. Patients who
were not screened differed from those who were in several
ways. Firstly, younger patients (<50 years) were more likely
to be missed during MRSA screening. A possible explanation for this is that nurses perceived younger patients to
be at low risk for MRSA carriage and were thus less inclined to pursue screening. Although older age is frequently identified as a risk factor for MRSA carriage
[8,10,12], it is possible that the tendency to miss younger
patients from screening may contribute to this finding and
inflate effect estimates. Transfer to internal medicine from
another hospital department (intra-hospital transfer) was
also a risk factor for being missed during screening. Intrahospital transfer has been previously identified as a risk
factor for MRSA admission carriage [10]; missing this
group of patients could result in an underestimation of
Pasricha et al. Antimicrobial Resistance and Infection Control 2013, 2:17
http://www.aricjournal.com/content/2/1/17
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Table 1 Results of uni- and multi-variate regression analyses of factors associated with failure to have an admission
MRSA swab performed1
Proportions (n)
Variable
Univariate regression Multivariate regression
Swabs missed (n = 267) Swabs done (n = 1740) OR [95%CI] P value Adjusted OR [95%CI] P value
Male sex
55.9 (148)
58.6 (997)
0.9 [0.7-1.1]
0.402
Age < 50 years old
30.3 (81)
19.9 (339)
1.7 [1.3-2.3]
<0.001
Admitted from ICU
4.5(12)
7.6(129)
0.6 [0.3-1.1]
0.074
Admitted from another ward
7.1(19)
2.7(45)
2.8 [1.6-4.9]
<0.001
88.3(235)
89.7(1526)
0.9 [0.6-1.3]
0.484
Uncomplicated diabetes mellitus
10.4(12
18.7(126)
0.5 [0.3-0.9]
0.034
Acute renal failure
10.4(12
21.8(147)
0.4 [0.2-0.8]
0.006
Chronic renal failure
6.1(7)
13.8(93)
0.4 [0.2-0.9]
0.026
End stage renal failure
4.3(5)
2.4(16)
1.9 [0.7-5.2]
0.231
Admitted from home
Complicated diabetes mellitus
5.2(6)
9.8(66)
0.5 [0.2-1.2]
0.122
Peripheral vascular disease
2.6(3)
4.3(29)
0.6 [0.2-2.0]
0.400
Chronic obstructive pulmonary disease
9.6(11)
14.4(97)
0.6 [0.3-1.2]
0.167
Dementia
0.9(1)
1.5(10)
0.6 [0.07-4.6] 0.608
Stroke
0
0.9(6)
Omitted
1.0(1)
0.4(3)
2.0 [0.2-19.0] 0.561
Congestive cardiac failure
11.3(13)
24.8(167)
0.4 [0.2-0.7]
0.002
Ischaemic heart disease
10.4(12)
11.3(76)
0.9 [0.5-1.8]
0.791
Haematological malignancy
10.4(12)
5.8(39)
1.9 [1.0-3.7]
0.065
0
1.2(8)
Omitted
Cerebral haemorrhage
Carotid artery stenosis
2.4 [1.4-3.9]
<0.001
2.8 [1.1-7.1]
0.028
Parkinsons disease
0.9(1)
0.7(5)
1.2 [0.1-10.2] 0.884
Connective tissue disease
0.9(1)
2.2(15)
0.4 [0.05-2.9] 0.358
Liver failure
1.0(1)
1.8(12)
0.5 [0.06-3.8] 0.488
0
1.0(7)
Omitted
Solid organ cancer
35.7(41)
15.4(104)
3.0 [1.9-4.7]
<0.001
3.2[2.1-5.1]
<0.001
Metastatic cancer
12.6(13)
7.3(50)
1.8 [0.3-3.9]
0.866
2.6 [1.4-4.8]
0.004
Peptic ulcer disease
1.9(2)
2.5(17)
1.1 [0.3-3.9]
0.866
Infection
1.9(2)
0.7(5)
2.4 [0.5-12.5] 0.301
Monday
8.90(35)
91.10(358)
0.8[0.4-1.4]
0.355
Tuesday
16.02(62)
83.98(325)
1.5[0.9-2.5]
0.140
Wednesday
15.93(54)
84.07(285)
1.5[0.9-2.5]
0.155
Respiratory failure
Day of the week
Thursday
16.08(46)
83.92(240)
1.5[0.9-2.6]
0.153
Friday
15.49(35)
84.51(191)
1.4[0.8-2.6]
0.226
Saturday
8.61(13)
91.39(138)
0.7[0.4-1.5]
0.408
Sunday
11.35(21)
88.65(164)
0.8[0.5-1.3]
0.365
1.
Denominators used to calculate proportions were adjusted for the number of patients in whom data were available. OR odds ratio, CI confidence interval.
the true MRSA carriage rate and a failure to recognise
intra-hospital transfer as an important risk factor for
MRSA carriage. Patients with malignancy were more likely
to be missed during screening in our study. This was due
to logistic difficulties (e.g. frequent readmissions for
chemotherapy; ultra-short hospitalizations) within our
hospital oncology ward that impeded their regular
participation in screening, and was therefore a problem
specific to our institution.
To our knowledge, the study by Furano et al. is the
only one to report detailed characteristics of patients
missed by MRSA screening [11]. In this study, 83.7% of
eligible patients were not enrolled in screening. Unenrolled patients were older, less likely to have had a
Pasricha et al. Antimicrobial Resistance and Infection Control 2013, 2:17
http://www.aricjournal.com/content/2/1/17
hospital admission in the previous year, and had a higher
in-hospital mortality than those patients who were enrolled [11]. The present study will help to further elucidate the importance and magnitude of misclassification
bias in MRSA risk profiling studies.
Our study has several limitations. Firstly, it is likely that
the effectiveness of hospital surveillance programmes to
enrol patients on admission may be heavily influenced by
institutional and local factors. Therefore, the generalizability
of our findings may be limited. Secondly, some of our data
was collected retrospectively from medical records and is
therefore subject to the inaccuracies inherent to data collected in this way.
Nevertheless, we believe that our findings highlight
some of the potential misclassification biases that may
occur in MRSA risk profiling studies due to patients
missed from screening. This could have important implications for the accuracy of MRSA risk scores developed
to target MRSA screening. Clear reporting on patient recruitment and the proportions and characteristics of
those patients missed is essential for accurate interpretation of clinical prediction tools identifying patients at
high risk for carriage of antibiotic-resistant bacteria.
Competing interests
S. H. has received a peer-reviewed MRSA research grant funded by Pfizer,
and is a member of the speakers’ bureau of bioMérieux, and a member of
the advisory boards of Destiny Pharma, bioMérieux, and DaVolterra. JS is a
consultant for bioMérieux, Biocartis, and Spinomix, and has received research
grants and conference support from Abbott, Becton-Dickinson and Bruker.
Authors’ contributions
AI, TK, AP and DP designed the study, supervised the data collection and
contributed to the data analysis. AP and DP provided financial support. JS
supervised the laboratory work. VC and GC led data collection and validation.
JP performed the data analysis and prepared the manuscript. SH and AI
supervised and led the data analysis and manuscript preparation. All authors
contributed and approved the final manuscript.
Acknowledgements
We would like to extend our thanks to F. Maitre, J. Maurin, and G. Renzi for
their help with this study, and Rosemary Sudan for editorial assistance.
During this study, research activities on MRSA by SH were supported by the
European Community, 6th Framework Programme (MOSAR network contract
LSHP-CT-2007-037941).
Author details
1
Infection Control Program, University of Geneva Hospitals and Faculty of
Medicine, 4 Rue Gabrielle Perret-Gentil, Geneva 1211, Switzerland.
2
Department of General Internal Medicine, University of Geneva Hospitals
and Faculty of Medicine, Geneva, Switzerland. 3Central Laboratory of
Bacteriology, University of Geneva Hospitals and Faculty of Medicine,
Geneva, Switzerland. 4Direction of Medico-Economic Analysis, University of
Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland. 5Current
affiliation: The Jenner Institute, Oxford University, Oxford, UK.
Received: 4 March 2013 Accepted: 26 May 2013
Published: 30 May 2013
Page 4 of 4
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doi:10.1186/2047-2994-2-17
Cite this article as: Pasricha et al.: Methicillin-resistant Staphylococcus
aureus risk profiling: who are we missing?. Antimicrobial Resistance and
Infection Control 2013 2:17.
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