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Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a meta-analysis
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Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a meta-analysis Jintang Ning , Jimei Wang , Songzhen Zhang , Xiaojuan Sha PII: DOI: Reference:
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Please cite this article as: Jintang Ning , Jimei Wang , Songzhen Zhang , Xiaojuan Sha , Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a metaanalysis, The Spine Journal (2019), doi: https://doi.org/10.1016/j.spinee.2019.10.009
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Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a meta-analysis
Running title: Meta-analysis on nasal colonization and SSI
Authors: Jintang Ning 1*, Jimei Wang 1*, Songzhen Zhang 1, and Xiaojuan Sha 2 *, these authors contributed equally to this work
Affiliations: 1, Department of Pharmacy, Dongying People’s Hospital, Dongying 257091, China 2, Department of Public Health, Qingdao Sanatorium, Qingdao 266000, China
Corresponding author: Dr. Jimei Wang, Department of Pharmacy, Dongying People’s Hospital, No. 317 Nanyi Road, Dongying 257091, China; Telephone: +86-0546-8331577; Fax: +86-0546-8331577; Email: [email protected]
Funding Disclosure(s) Statement The authors received no funding for this study.
1
Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a meta-analysis
Running title: Meta-analysis on nasal colonization and SSI
2
1
Abstract
2 3
Background context: Nasal colonization of Staphylococcus aureus (SA) may increase the risk
4
of surgical site infection (SSI) after spine surgeries, although the results of previous studies
5
were inconsistent.
6
Purpose: To evaluate the influences of nasal colonization of SA, methicillin-susceptible SA
7
(MSSA), and methicillin-resistant SA (MRSA) on the incidence of SSI after spine surgery.
8
Study design/setting: systematic review and meta-analysis.
9
Patient sample: Seven studies including 10,650 patients who underwent nasal swab
10
examination before spine surgeries were included, and 221 patients had nasal colonization of
11
MRSA at baseline.
12
Outcome measures: Association between baseline nasal colonization of SA, MRSA and SSI
13
after spine surgery.
14
Methods: Relevant follow-up studies were identified through systematic searches of the
15
PubMed, Embase, and Cochrane Library databases. A random effects model was applied to
16
pool the results. Subgroup analyses were performed according to whether MRSA
17
decolonization was applied.
18
Results: During follow-up, a total of 244 SSI events occurred, including 57 MRSA-SSI
19
events. Pooled results showed that nasal SA (risk ratio [RR]=0.75, p=0.22) or MSSA
20
colonization (RR=0.60, p=0.22) did not significantly affect the risk of overall SSI after
21
surgeries. However, nasal MRSA colonization was associated with significantly increased
3
1
risks of overall SSI and MRSA-SSI (RR=2.52 and 6.21 respectively, both p<0.001).
2
Interestingly, the associations between nasal MRSA colonization and increased risks of
3
overall and MRSA-SSI remained significant in studies without MRSA decolonization, but
4
became insignificant in studies with MRSA decolonization.
5
Conclusions: Nasal MRSA colonization may be associated with increased risks of overall SSI
6
and MRSA-SSI after spine surgeries, and nasal MRSA decolonization may be associated with
7
a reduction of SSI in these patients.
8 9 10
Keywords: Staphylococcus aureus; Nasal colonization; Spine surgery; Surgical site infection; Meta-analysis
11 12 13 14 15
4
1
Introduction
2 3
With continuous improvements of surgical instrumentation and techniques, many spinal
4
procedures that were unable to be performed previously have become feasible and increasing
5
numbers of spine surgeries are being performed [1, 2]. However, the complexity of the spine
6
surgical procedures has also resulted in a high incidence of surgical site infection (SSI) [3].
7
According to previous reports, the risk of SSI associated with spine surgeries is higher than
8
that with general orthopedic surgeries [4]. In a report from the National Nosocomial
9
Infections Surveillance System, the incidence of SSI among patients who have undergone
10
spinal fusion surgery ranged between 2.4% and 8.5% [5]. Because the incidence of SSI after
11
spine surgery contributes to increased patient mortality and medical costs [6, 7], early
12
identification of patients at high risk for the development of SSI after spine surgery is of
13
clinical significance.
14 15
The pathogenesis of SSI is complicated which may involve many clinical factors [8]. Recent
16
evidence from studies in patients treated with cardiac or orthopedic surgeries indicated that
17
nasal colonization of Staphylococcus aureus (SA), particularly of the methicillin-resistant SA
18
(MRSA), may increase the risk of SSI after surgeries [9, 10]. However, pilot studies
19
investigating the role of nasal colonization of SA in patients who have undergone spine
20
surgeries have produced inconsistent results [11-17]. Although some early studies confirmed
21
the potential predictive role of nasal MRSA colonization for SSI after spine surgeries [11, 12,
5
1
15], others did not support that nasal MRSA colonization is associated with the risk of SSI in
2
these patients [13, 14, 16, 17]. Because the numbers of patients included in these pilot studies
3
are generally small, especially for the groups with nasal MRSA colonization, it is possible
4
that the limited study scales may be statistically inadequate to provide a significant result.
5
Therefore, in the present study, we aimed to pool the results of the previous studies in a
6
meta-analysis to systematically evaluate the influences of nasal colonization of SA,
7
methicillin-susceptible SA (MSSA), and MRSA on the incidence of SSI after spine surgeries.
8 9 10
Methods
11 12
This study was performed in accordance with the MOOSE (Meta-analysis of Observational
13
Studies in Epidemiology) [18] and Cochrane’s Handbook [19] guidelines.
14 15
Database search
16
We searched the PubMed, Embase, and Cochrane Library databases for relevant studies,
17
using combinations of the following terms: (1) "staphylococcus"; (2) "nasal" OR "nose"; (3)
18
"spine" OR "spinal" OR "vertebral" OR "vertebrate"; and (4) "surgery" OR "surgical" OR
19
"procedure" OR "operation" OR" operative". We limited the search to human studies
20
published in English. A manual analysis of the reference lists of original and review articles
21
was performed as a supplementation. The final search was performed on May 05, 2019.
6
1 2
Inclusion and exclusion criteria
3
The aim of the study was to answer the following four questions in patients who underwent
4
spine surgeries: (1) Is the incidence of overall SSI higher among SA-colonized patients than
5
among noncolonized patients? (2) Is the incidence of overall SSI higher among
6
MSSA-colonized patients higher than among noncolonized patients? (3) Is the incidence of
7
overall SSI higher among MRSA-colonized patients than among noncolonized patients? and
8
(4) Is the incidence of MRSA-SSI higher among MRSA-colonized patients than among
9
noncolonized patients? Accordingly, articles were included if they met the following criteria:
10
(1) full-length article in English; (2) reported data from longitudinal follow-up; (3) included
11
patients scheduled for spine surgery for non-infectious diseases; (4) reported results of nasal
12
swab performed before surgery to screen for colonization of SA, MSSA, or MRSA; and (5)
13
documented the incidence of total SSI events and/or MRSA-SSI events according to the
14
status of nasal SA colonization. The SSI events were defined based on the 2017 Centers for
15
Disease Control criteria for wound surveillance as previously described [20]. Reviews, letters,
16
editorials, and studies without longitudinal follow-up were excluded.
17 18
Data extraction and quality evaluation
19
Database searching, data extraction, and quality assessment were performed by two authors
20
independently, and discrepancies were resolved by consultation with the corresponding
21
author. The data extracted included: (1) first author, location, and study design characteristics;
7
1
(2) procedure characteristics and number, mean age, and gender of patients; (3) methods for
2
screening of nasal SA colonization, proportions of patients with nasal SA and MRSA
3
colonization before surgeries, and strategies for decolonization for nasal MRSA carriers; (4)
4
follow-up durations and SSI outcomes reported; and (5) total numbers of SA-, MSSA-, and
5
MRSA-colonized patients and noncolonized patients according to the results of nasal swab
6
examination and the number of patients with overall SSI and MRSA-SSI in each group after
7
spine surgeries. Study quality evaluation was performed with the Newcastle-Ottawa Scale
8
(NOS) [21], which ranks studies from 1 to 9 stars and judges each study with regard to three
9
aspects: selection of study groups; comparability of groups; and ascertainment of the outcome
10
of interest.
11 12
Statistical analyses
13
We used risk ratios (RRs) with 95% confidence interval (CIs) to estimate the risk of SSI
14
events in patients with various nasal colonization statuses after spine surgeries [19]. The
15
Cochrane’s Q test and I2 test were performed to evaluate the heterogeneity among studies
16
[22]. An I2 > 50% indicated significant heterogeneity. A random effects model was applied to
17
pool the data, because this model incorporates the potential heterogeneity to generate a more
18
generalized result [19]. Sensitivity analyses in which individual studies were removed one at
19
a time were performed to evaluate the stability of the results [23]. A predefined subgroup
20
analysis was performed to evaluate whether nasal decolonization affects the association
21
between nasal MRSA colonization and SSI after spine surgery. Potential publication bias was
8
1
assessed by funnel plots with the Egger regression asymmetry test [24]. RevMan (Version 5.1;
2
Cochrane Collaboration, Oxford, UK) software was used for the statistical analyses.
3 4 5
Results
6 7
Results of literature search
8
The process of the literature search is shown in Figure 1. Overall, 293 studies were obtained
9
after the initial literature search, and 277 were excluded based on the screening of titles and
10
abstracts primarily because of irrelevance to the aim of the meta-analysis. Finally, seven
11
follow-up studies [11-17] were included.
12 13
Study characteristics and quality evaluation
14
The characteristics of the included studies are presented in Table 1. Overall, 10,650 patients
15
who underwent nasal swab examination before spine surgeries were included, and 221
16
patients had nasal colonization of MRSA at baseline. During follow-up, a total of 244 SSI
17
events occurred, including 57 MRSA-SSI events. The studies were published between 2014
18
and 2018 and performed in the United States [11-13, 17], Japan [14, 15], and France [16].
19
Five were retrospective studies [11-14, 17], whereas two were prospectively designed [15,
20
16]. All of the studies included patients who underwent spine surgeries for non-infectious
21
diseases, with nasal swab performed before surgery to identify nasal SA colonization. The
9
1
timing of nasal screening varied from one week to 12 months before surgery. The times of
2
nasal culture required to confirm nasal colonization were not reported in all of the included
3
studies. At baseline, 18.8%–35.6% of the patients were colonized with SA, and 1.1%–5.9%
4
of the patients were colonized with MRSA. For patients with nasal colonization with MRSA,
5
decolonization with topical mupirocin and/or intravenous (i.v.) vancomycin was applied in
6
four studies [12, 13, 15, 16], while decolonization was not applied in the other three studies
7
[11, 14, 17]. The patients were followed for up to 1 year. The outcomes of overall SSI events
8
were reported in all of the included studies, while five studies reported MRSA-SSI events [11,
9
12, 15-17]. The qualities of the included studies were moderate, with NOS scores varying
10
between six and seven points.
11 12
Nasal SA or MSSA colonization and the risk of SSI after spine surgery
13
The pooled results from four studies [11-13, 16] showed that nasal SA colonization was not
14
likely to affect the risk of overall SSI in patients after spine surgery (RR=0.75, 95% CI:
15
0.47–1.19; p=0.22; Figure 2A). No significant heterogeneity was detected (p for Cochrane’s
16
Q test =0.37, I2=5%). Sensitivity analyses with one study excluded at a time produced the
17
same results (RR=0.60–0.82, all p>0.05). Similarly, the pooled results from four studies
18
[11-13, 16] showed that nasal MSSA colonization was also unlikely to affect the risk of
19
overall SSI in patients after spine surgery (RR=0.66, 95% CI: 0.34–1.29; p=0.22; Figure 2B).
20
No significant heterogeneity was detected (p for Cochrane’s Q test =0.32, I2=31%).
21
Sensitivity analyses with one study excluded at a time returned consistent results (RR: 0.49–
10
1
0.77, all p>0.05).
2 3
Nasal MRSA colonization and the risk of overall SSI after spine surgery
4
The pooled results from seven studies [11-17] showed that nasal MRSA colonization may be
5
associated with a significantly increased risk of overall SSI in patients after spine surgery
6
(RR=2.52, 95% CI: 1.36–4.67; p=0.003; Figure 3A). No significant heterogeneity was
7
detected (p for Cochrane’s Q test =0.30, I2=17%). Sensitivity analyses with one study
8
excluded produced the same results (RR: 2.03–3.15, all p<0.05). Subgroup analyses showed
9
that nasal MRSA colonization may also be associated with an increased risk of overall SSI in
10
studies in which decolonization of MRSA was not applied (RR=3.04, 95% CI: 1.22–7.62;
11
p=0.02), but the association became insignificant in the analysis of studies in which
12
decolonization of MRSA was applied (RR=1.98, 95% CI: 0.75–5.02; p=0.15). These results
13
suggest that decolonization of MRSA may be associated with a reduction in the overall risk
14
of SSI in patients with nasal MRSA colonization after spine surgeries.
15 16
Nasal MRSA colonization and the risk of MRSA-SSI after spine surgery
17
The pooled results from five studies [11, 12, 15-17] showed that nasal MRSA colonization
18
may be associated with an increased risk of MRSA-SSI in patients after spine surgery
19
(RR=6.21, 95% CI: 2.37–16.25; p<0.001; Figure 3B). No significant heterogeneity was
20
detected (p for Cochrane’s Q test =0.56, I2=0%). Sensitivity analyses with one study excluded
21
at a time returned consistent results (RR: 4.47–8.27, all p<0.05). Subgroup analyses showed
11
1
that nasal MRSA colonization may be associated with an increased risk of MRSA-SSI in
2
studies in which decolonization of MRSA was not applied (RR=15.02, 95% CI: 3.69–61.19;
3
p<0.001), but the association became insignificant in the analysis of studies in which
4
decolonization of MRSA was applied (RR=2.85, 95% CI: 0.76–10.66; p=0.12). These results
5
suggest that decolonization of MRSA may be associated with a reduced risk of MRSA-SSI in
6
patients with nasal MRSA colonization after spine surgery.
7 8
Publication bias
9
Funnel plots for the associations between nasal SA, MSSA, and MRSA colonization and
10
overall SSI risk as well as the association between nasal MRSA colonization and MRSA-SSI
11
risk are shown in Figure 4A-D. The funnel plots were symmetric on visual inspection.
12
Egger’s regression tests were not performed due to the limited number of studies included.
13 14
Discussion
15
In this meta-analysis of pooled results from seven follow-up studies, we found that nasal
16
colonization of SA or MSSA was unlikely to be associated with a significantly increased risk
17
of SSI after spine surgery. However, nasal colonization of MRSA may be associated with
18
increased risks for overall SSI and MRSA-SSI after spine surgery. Interestingly, subgroup
19
analyses showed that the association between nasal MRSA colonization and the increased
20
risk of SSI seemed to be mainly driven by studies in which nasal MRSA decolonization was
21
not applied. In the subgroup analysis of studies in which nasal MRSA decolonization was
12
1
applied, the associations between nasal MRSA colonization and increased risks of overall SSI
2
and MRSA-SSI became insignificant. These results suggest that nasal MRSA colonization
3
may be associated with an increased risk of overall SSI and MRSA-SSI after spine surgery,
4
while nasal MRSA decolonization may be associated with a reduction in the risk of SSI in
5
these patients.
6 7
The association between nasal carriage of SA and SSI has been suggested by studies of
8
patients receiving orthopedic surgeries. In an early meta-analysis of six studies, Levy et al
9
demonstrated that nasal carriage of SA is a major risk factor for SSI after general orthopedic
10
surgeries (pooled odds ratio [OR]=5.92, p=0.03). However, these results were based on direct
11
pooling of the ORs from individual studies, and considerable heterogeneity was detected
12
(I2=90%). As mentioned by the authors, the considerable heterogeneity among the included
13
studies was reflective of the different study characteristics and methodology of the included
14
studies, which makes the interpretation of the results difficult [25]. Also, the authors were
15
unable to determine which strains of SA (MSSA or MRSA) contributed to the potential
16
association between nasal colonization of SA and SSI after orthopedic surgeries. Moreover,
17
the previous hypothesis that nasal SA colonization is the major acquisition pathway for SSI
18
after orthopedic surgery has been challenged by the inconsistent results of some studies.
19
Berthelot et al. investigated a total of 3,908 consecutive patients undergoing orthopedic
20
surgery [26]. For 22 patients with SSI related to SA, only nine were nasal SA carriers before
21
surgery [26]. Moreover, among the nine nasal SA carriers who developed SSI, three had
13
1
different pairs of SA strains on nasal swabs and at the infection site, suggesting that the
2
association between nasal SA colonization and SA-related SSI may not be as close as
3
previously considered [26]. In our study, by pooling the results of all available follow-up
4
studies of patients who received spine surgeries, nasal colonization of SA or MSSA was
5
unlikely to be associated with increased risks of SSI. These findings also support the
6
uncertainty of the association between SA (primarily MSSA) and the affected SSI risk after
7
spine surgeries. Another potential mechanism, from our perspective, perhaps is that the
8
intensive administration of perioperative antibiotics for patients scheduled to undergo spine
9
surgery may block the potential acquisition of MSSA from endogenous colonization to the
10
surgical sites.
11 12
Another finding of our meta-analysis is that nasal colonization of MRSA seemed to be
13
associated with increased risks of overall SSI and MRSA-SSI after spine surgery. These
14
results may indicate the importance of screening for nasal colonization of MRSA, rather than
15
MSSA, for the identification of patients at higher risk for development of SSI. Further
16
subgroup analyses showed that the association between nasal MRSA colonization and an
17
increased risk of SSI was mainly driven by studies in which nasal MRSA decolonization was
18
not applied. From the subgroup analysis of studies in which nasal MRSA decolonization was
19
applied, the associations between nasal MRSA colonization and increased risk of overall and
20
MRSA-SSI became insignificant. These results suggest that nasal MRSA colonization may be
21
a risk factor for the development of SSI after spine surgery, and effective decolonization of
14
1
nasal MRSA may help to prevent SSI. This is consistent with the findings of a previous
2
meta-analysis of patients treated with cardiac or general orthopedic procedures. The previous
3
meta-analysis included 39 studies of patients who underwent cardiac or total joint
4
replacement procedures and demonstrated that application of glycopeptide prophylaxis with
5
or without nasal decolonization significantly reduced the risk of MRSA-SSI [27]. In another
6
recently published meta-analysis of patients who received total knee and hip arthroplasty,
7
Sadigursky et al. found that the use of a prophylaxis protocol for decolonization of MRSA
8
significantly reduced the incidence of SSI by 39% in these patients. These findings, together
9
with ours, demonstrate that nasal colonization of MRSA may be a risk factor of SSI after
10
surgery, and screening and decolonization of nasal MRSA may be effective at reducing the
11
incidence of SSI after spine surgery.
12 13
It has to be mentioned that the pathogenesis of SSI after spine surgeries is multifactorial [28].
14
Many clinical factors, including patient characteristics (e.g., obesity, diabetes, and smoking),
15
a longer operative time, transfusion during the operation, and other factors have been
16
suggested to be important risk factors for the incidence of SSI after spine surgeries [8, 29].
17
Due to the limited number of cases with SSI in each study and small number of available
18
studies in our meta-analysis, our analysis for the association between nasal MRSA
19
colonization and SSI after surgery was based on univariate findings rather than multivariable
20
adjusted findings. The potential imbalance of these clinical factors related to SSI may
21
confound our finding of the association between nasal MRSA colonization and incidence of
15
1
SSI after spine surgeries. Our results should be confirmed in cohort studies with larger
2
sample sizes that incorporate adequate adjustment of multiple factors that may influence the
3
SSI, such as the prevalence of diabetes between groups, differences in the immune status of
4
patients, and differences in surgical times and procedure characteristics.
5 6
Our study has limitations. First, the number of included studies was small, which prevented
7
us from evaluating the potential influences of patient (e.g., smoking status, with or without
8
diabetes, and hypertension) or procedure characteristics (different types of spine surgeries) on
9
the association between nasal SA colonization and SSI events after spine surgeries. Second,
10
we only included studies published in English, which may lead to additional bias by
11
potentially missing of studies published in other languages. Third, as a meta-analysis of
12
observational studies, a causative association between nasal MRSA colonization and the
13
increased risk of SSI after spine surgeries could not be retrieved based on our results. Fourth,
14
also due to the nature of a meta-analysis of observational studies, we could not exclude the
15
possibility that potential clinical factors for SSI may confound our findings. Moreover,
16
although the potential efficacy of nasal MRSA decolonization for the prevention of SSI after
17
spine surgery should be optimally investigated in randomized controlled trials, due to the
18
ethical reasons, these clinical trials cannot be performed. Finally, the optimal regimens for
19
nasal MRSA decolonization should be evaluated in future studies.
20 21
In conclusion, nasal MRSA colonization may be associated with increased risks of overall
16
1
SSI and MRSA-SSI after spine surgeries, while nasal MRSA decolonization may be
2
associated with a reduction in the risk of SSI in these patients. Further studies are needed to
3
validate our findings and determine whether the association between nasal MRSA
4
colonization and SSI after spine surgery is independent of the characteristics of patients and
5
surgical procedures. Moreover, the optimal regimens for nasal MRSA decolonization remain
6
to be determined.
7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33
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in
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2010;http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. 22. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539-58. 23. Patsopoulos NA, Evangelou E, Ioannidis JP. Sensitivity of between-study heterogeneity in meta-analysis: proposed metrics and empirical evaluation. Int J Epidemiol. 2008;37(5):1148-57. 24. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629-34. 25. Levy PY, Ollivier M, Drancourt M, Raoult D, Argenson JN. Relation between nasal carriage of Staphylococcus aureus and surgical site infection in orthopedic surgery: the role of nasal contamination. A systematic literature review and meta-analysis. Orthop Traumatol Surg Res. 2013;99(6):645-51. 26. Berthelot P, Grattard F, Cazorla C, et al. Is nasal carriage of Staphylococcus aureus the main acquisition pathway for surgical-site infection in orthopaedic surgery? Eur J Clin Microbiol Infect Dis. 2010;29(4):373-82. 27. Schweizer M, Perencevich E, McDanel J, et al. Effectiveness of a bundled intervention of decolonization and prophylaxis to decrease Gram positive surgical site infections after cardiac or orthopedic surgery: systematic review and meta-analysis. BMJ. 2013;346:f2743. 28. Boody B, Vaccaro AR. Point-of-View: Risk Factors for Surgical Site Infection After Posterior Lumbar Spinal Surgery. Spine (Phila Pa 1976). 2018;43(10):738. 29. Fei Q, Li J, Lin J, et al. Risk Factors for Surgical Site Infection After Spinal Surgery: A Meta-Analysis. World Neurosurg. 2016;95:507-15.
18
Figure legends
Figure 1 Diagram of study selection.
19
Figure 2 Forest plots for the meta-analysis of associations of nasal colonization of (A) SA and (B) MSSA with overall SSI risk after spine surgery.
20
Figure 3 Forest plots for the meta-analysis of associations of nasal colonization of MRSA with (A) overall SSI and (B) MRSA-SSI risk after spine surgery.
21
Figure 4 Funnel plots for the associations of nasal colonization of (A) SA, (B) MSSA, and (C) MRSA with the risk of SSI after spine surgery, and for the association of nasal colonization of (D) MRSA with the risk of MRSA-SSI after spine surgery.
22
Table 1 Characteristics of the included studies. Study
Design
Country
Patients and
Number
procedures
of patients
Mean age years
Thakkar 2014
RC
USA
Male
Screening method
%
Patients
Nasal
underwent spine
swab,
surgeries for
519
59
48
within 30
arthrodesis and
days before
decompression
surgery
Nasal
Nasal
Decolonization
SA
MRSA
methods for
positive
positive
MRSA
%
%
26.0
4.8
Follow-up duration
SSI outcomes reported
NOS score
months MRSA-SSI NA
12
and overall
6
SSI
Patients Ramos 2016
underwent spine RC
USA
surgeries for
Nasal swab 3556
51
52
primary spinal
before
Topical 18.8
2.7
admission
mupirocin and
12
Overall SSI
7
i.v. vancomycin
fusion Pediatric Luhmann 2016
RC
USA
patients who had spine surgery
Nasal swab 339
13
NA
1-4 weeks before
22.1
5.9
Topical mupirocin
MRSA-SSI 12
Kobayashi 2018
PC
Japan
underwent instrumental
Nasal swab 132
45
50
2018
PC
France
Patients underwent
35.6
3.8
admission
spine surgery Mallet
before
331
16
17
Nasal swab for twice
23
22.7
3
Topical mupirocin Topical mupirocin and
6
SSI
surgery Patients
and overall
MRSA-SSI 12
and overall
6
SSI 11
MRSA-SSI and overall
7
adolescent
within 12
idiopathic
months
scoliosis surgery
i.v. vancomycin
SSI
before surgery
Patients Nielsen 2018
RC
USA
underwent posterior spinal
Nasal swab 1200
14
36
fusion
2018
RC
Japan
underwent elective spine surgery
MRSA-SSI NR
2.8
NA
12
surgery
Patients Kawabata
before
and overall
6
SSI
Nasal swab 4573
61
60
before
NR
1.1
NA
12
Overall SSI
7
surgery
SA, Staphylococcus aureus; MRSA, methicillin-resistant Staphylococcus aureus; SSI, surgical site infection; NOS, Newcastle-Ottawa Scale; RC, retrospective cohort; PC, prospective cohort; NR, not reported; NA, not applied; i.v., intravenous
24
Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a meta-analysis Jintang Ning , Jimei Wang , Songzhen Zhang , Xiaojuan Sha PII: DOI: Reference:
S1529-9430(19)31055-1 https://doi.org/10.1016/j.spinee.2019.10.009 SPINEE 58043
To appear in:
The Spine Journal
Received date: Revised date: Accepted date:
13 August 2019 18 October 2019 18 October 2019
Please cite this article as: Jintang Ning , Jimei Wang , Songzhen Zhang , Xiaojuan Sha , Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a metaanalysis, The Spine Journal (2019), doi: https://doi.org/10.1016/j.spinee.2019.10.009
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Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a meta-analysis
Running title: Meta-analysis on nasal colonization and SSI
Authors: Jintang Ning 1*, Jimei Wang 1*, Songzhen Zhang 1, and Xiaojuan Sha 2 *, these authors contributed equally to this work
Affiliations: 1, Department of Pharmacy, Dongying People’s Hospital, Dongying 257091, China 2, Department of Public Health, Qingdao Sanatorium, Qingdao 266000, China
Corresponding author: Dr. Jimei Wang, Department of Pharmacy, Dongying People’s Hospital, No. 317 Nanyi Road, Dongying 257091, China; Telephone: +86-0546-8331577; Fax: +86-0546-8331577; Email: [email protected]
Funding Disclosure(s) Statement The authors received no funding for this study.
1
Nasal colonization of Staphylococcus aureus and the risk of surgical site infection after spine surgery: a meta-analysis
Running title: Meta-analysis on nasal colonization and SSI
2
1
Abstract
2 3
Background context: Nasal colonization of Staphylococcus aureus (SA) may increase the risk
4
of surgical site infection (SSI) after spine surgeries, although the results of previous studies
5
were inconsistent.
6
Purpose: To evaluate the influences of nasal colonization of SA, methicillin-susceptible SA
7
(MSSA), and methicillin-resistant SA (MRSA) on the incidence of SSI after spine surgery.
8
Study design/setting: systematic review and meta-analysis.
9
Patient sample: Seven studies including 10,650 patients who underwent nasal swab
10
examination before spine surgeries were included, and 221 patients had nasal colonization of
11
MRSA at baseline.
12
Outcome measures: Association between baseline nasal colonization of SA, MRSA and SSI
13
after spine surgery.
14
Methods: Relevant follow-up studies were identified through systematic searches of the
15
PubMed, Embase, and Cochrane Library databases. A random effects model was applied to
16
pool the results. Subgroup analyses were performed according to whether MRSA
17
decolonization was applied.
18
Results: During follow-up, a total of 244 SSI events occurred, including 57 MRSA-SSI
19
events. Pooled results showed that nasal SA (risk ratio [RR]=0.75, p=0.22) or MSSA
20
colonization (RR=0.60, p=0.22) did not significantly affect the risk of overall SSI after
21
surgeries. However, nasal MRSA colonization was associated with significantly increased
3
1
risks of overall SSI and MRSA-SSI (RR=2.52 and 6.21 respectively, both p<0.001).
2
Interestingly, the associations between nasal MRSA colonization and increased risks of
3
overall and MRSA-SSI remained significant in studies without MRSA decolonization, but
4
became insignificant in studies with MRSA decolonization.
5
Conclusions: Nasal MRSA colonization may be associated with increased risks of overall SSI
6
and MRSA-SSI after spine surgeries, and nasal MRSA decolonization may be associated with
7
a reduction of SSI in these patients.
8 9 10
Keywords: Staphylococcus aureus; Nasal colonization; Spine surgery; Surgical site infection; Meta-analysis
11 12 13 14 15
4
1
Introduction
2 3
With continuous improvements of surgical instrumentation and techniques, many spinal
4
procedures that were unable to be performed previously have become feasible and increasing
5
numbers of spine surgeries are being performed [1, 2]. However, the complexity of the spine
6
surgical procedures has also resulted in a high incidence of surgical site infection (SSI) [3].
7
According to previous reports, the risk of SSI associated with spine surgeries is higher than
8
that with general orthopedic surgeries [4]. In a report from the National Nosocomial
9
Infections Surveillance System, the incidence of SSI among patients who have undergone
10
spinal fusion surgery ranged between 2.4% and 8.5% [5]. Because the incidence of SSI after
11
spine surgery contributes to increased patient mortality and medical costs [6, 7], early
12
identification of patients at high risk for the development of SSI after spine surgery is of
13
clinical significance.
14 15
The pathogenesis of SSI is complicated which may involve many clinical factors [8]. Recent
16
evidence from studies in patients treated with cardiac or orthopedic surgeries indicated that
17
nasal colonization of Staphylococcus aureus (SA), particularly of the methicillin-resistant SA
18
(MRSA), may increase the risk of SSI after surgeries [9, 10]. However, pilot studies
19
investigating the role of nasal colonization of SA in patients who have undergone spine
20
surgeries have produced inconsistent results [11-17]. Although some early studies confirmed
21
the potential predictive role of nasal MRSA colonization for SSI after spine surgeries [11, 12,
5
1
15], others did not support that nasal MRSA colonization is associated with the risk of SSI in
2
these patients [13, 14, 16, 17]. Because the numbers of patients included in these pilot studies
3
are generally small, especially for the groups with nasal MRSA colonization, it is possible
4
that the limited study scales may be statistically inadequate to provide a significant result.
5
Therefore, in the present study, we aimed to pool the results of the previous studies in a
6
meta-analysis to systematically evaluate the influences of nasal colonization of SA,
7
methicillin-susceptible SA (MSSA), and MRSA on the incidence of SSI after spine surgeries.
8 9 10
Methods
11 12
This study was performed in accordance with the MOOSE (Meta-analysis of Observational
13
Studies in Epidemiology) [18] and Cochrane’s Handbook [19] guidelines.
14 15
Database search
16
We searched the PubMed, Embase, and Cochrane Library databases for relevant studies,
17
using combinations of the following terms: (1) "staphylococcus"; (2) "nasal" OR "nose"; (3)
18
"spine" OR "spinal" OR "vertebral" OR "vertebrate"; and (4) "surgery" OR "surgical" OR
19
"procedure" OR "operation" OR" operative". We limited the search to human studies
20
published in English. A manual analysis of the reference lists of original and review articles
21
was performed as a supplementation. The final search was performed on May 05, 2019.
6
1 2
Inclusion and exclusion criteria
3
The aim of the study was to answer the following four questions in patients who underwent
4
spine surgeries: (1) Is the incidence of overall SSI higher among SA-colonized patients than
5
among noncolonized patients? (2) Is the incidence of overall SSI higher among
6
MSSA-colonized patients higher than among noncolonized patients? (3) Is the incidence of
7
overall SSI higher among MRSA-colonized patients than among noncolonized patients? and
8
(4) Is the incidence of MRSA-SSI higher among MRSA-colonized patients than among
9
noncolonized patients? Accordingly, articles were included if they met the following criteria:
10
(1) full-length article in English; (2) reported data from longitudinal follow-up; (3) included
11
patients scheduled for spine surgery for non-infectious diseases; (4) reported results of nasal
12
swab performed before surgery to screen for colonization of SA, MSSA, or MRSA; and (5)
13
documented the incidence of total SSI events and/or MRSA-SSI events according to the
14
status of nasal SA colonization. The SSI events were defined based on the 2017 Centers for
15
Disease Control criteria for wound surveillance as previously described [20]. Reviews, letters,
16
editorials, and studies without longitudinal follow-up were excluded.
17 18
Data extraction and quality evaluation
19
Database searching, data extraction, and quality assessment were performed by two authors
20
independently, and discrepancies were resolved by consultation with the corresponding
21
author. The data extracted included: (1) first author, location, and study design characteristics;
7
1
(2) procedure characteristics and number, mean age, and gender of patients; (3) methods for
2
screening of nasal SA colonization, proportions of patients with nasal SA and MRSA
3
colonization before surgeries, and strategies for decolonization for nasal MRSA carriers; (4)
4
follow-up durations and SSI outcomes reported; and (5) total numbers of SA-, MSSA-, and
5
MRSA-colonized patients and noncolonized patients according to the results of nasal swab
6
examination and the number of patients with overall SSI and MRSA-SSI in each group after
7
spine surgeries. Study quality evaluation was performed with the Newcastle-Ottawa Scale
8
(NOS) [21], which ranks studies from 1 to 9 stars and judges each study with regard to three
9
aspects: selection of study groups; comparability of groups; and ascertainment of the outcome
10
of interest.
11 12
Statistical analyses
13
We used risk ratios (RRs) with 95% confidence interval (CIs) to estimate the risk of SSI
14
events in patients with various nasal colonization statuses after spine surgeries [19]. The
15
Cochrane’s Q test and I2 test were performed to evaluate the heterogeneity among studies
16
[22]. An I2 > 50% indicated significant heterogeneity. A random effects model was applied to
17
pool the data, because this model incorporates the potential heterogeneity to generate a more
18
generalized result [19]. Sensitivity analyses in which individual studies were removed one at
19
a time were performed to evaluate the stability of the results [23]. A predefined subgroup
20
analysis was performed to evaluate whether nasal decolonization affects the association
21
between nasal MRSA colonization and SSI after spine surgery. Potential publication bias was
8
1
assessed by funnel plots with the Egger regression asymmetry test [24]. RevMan (Version 5.1;
2
Cochrane Collaboration, Oxford, UK) software was used for the statistical analyses.
3 4 5
Results
6 7
Results of literature search
8
The process of the literature search is shown in Figure 1. Overall, 293 studies were obtained
9
after the initial literature search, and 277 were excluded based on the screening of titles and
10
abstracts primarily because of irrelevance to the aim of the meta-analysis. Finally, seven
11
follow-up studies [11-17] were included.
12 13
Study characteristics and quality evaluation
14
The characteristics of the included studies are presented in Table 1. Overall, 10,650 patients
15
who underwent nasal swab examination before spine surgeries were included, and 221
16
patients had nasal colonization of MRSA at baseline. During follow-up, a total of 244 SSI
17
events occurred, including 57 MRSA-SSI events. The studies were published between 2014
18
and 2018 and performed in the United States [11-13, 17], Japan [14, 15], and France [16].
19
Five were retrospective studies [11-14, 17], whereas two were prospectively designed [15,
20
16]. All of the studies included patients who underwent spine surgeries for non-infectious
21
diseases, with nasal swab performed before surgery to identify nasal SA colonization. The
9
1
timing of nasal screening varied from one week to 12 months before surgery. The times of
2
nasal culture required to confirm nasal colonization were not reported in all of the included
3
studies. At baseline, 18.8%–35.6% of the patients were colonized with SA, and 1.1%–5.9%
4
of the patients were colonized with MRSA. For patients with nasal colonization with MRSA,
5
decolonization with topical mupirocin and/or intravenous (i.v.) vancomycin was applied in
6
four studies [12, 13, 15, 16], while decolonization was not applied in the other three studies
7
[11, 14, 17]. The patients were followed for up to 1 year. The outcomes of overall SSI events
8
were reported in all of the included studies, while five studies reported MRSA-SSI events [11,
9
12, 15-17]. The qualities of the included studies were moderate, with NOS scores varying
10
between six and seven points.
11 12
Nasal SA or MSSA colonization and the risk of SSI after spine surgery
13
The pooled results from four studies [11-13, 16] showed that nasal SA colonization was not
14
likely to affect the risk of overall SSI in patients after spine surgery (RR=0.75, 95% CI:
15
0.47–1.19; p=0.22; Figure 2A). No significant heterogeneity was detected (p for Cochrane’s
16
Q test =0.37, I2=5%). Sensitivity analyses with one study excluded at a time produced the
17
same results (RR=0.60–0.82, all p>0.05). Similarly, the pooled results from four studies
18
[11-13, 16] showed that nasal MSSA colonization was also unlikely to affect the risk of
19
overall SSI in patients after spine surgery (RR=0.66, 95% CI: 0.34–1.29; p=0.22; Figure 2B).
20
No significant heterogeneity was detected (p for Cochrane’s Q test =0.32, I2=31%).
21
Sensitivity analyses with one study excluded at a time returned consistent results (RR: 0.49–
10
1
0.77, all p>0.05).
2 3
Nasal MRSA colonization and the risk of overall SSI after spine surgery
4
The pooled results from seven studies [11-17] showed that nasal MRSA colonization may be
5
associated with a significantly increased risk of overall SSI in patients after spine surgery
6
(RR=2.52, 95% CI: 1.36–4.67; p=0.003; Figure 3A). No significant heterogeneity was
7
detected (p for Cochrane’s Q test =0.30, I2=17%). Sensitivity analyses with one study
8
excluded produced the same results (RR: 2.03–3.15, all p<0.05). Subgroup analyses showed
9
that nasal MRSA colonization may also be associated with an increased risk of overall SSI in
10
studies in which decolonization of MRSA was not applied (RR=3.04, 95% CI: 1.22–7.62;
11
p=0.02), but the association became insignificant in the analysis of studies in which
12
decolonization of MRSA was applied (RR=1.98, 95% CI: 0.75–5.02; p=0.15). These results
13
suggest that decolonization of MRSA may be associated with a reduction in the overall risk
14
of SSI in patients with nasal MRSA colonization after spine surgeries.
15 16
Nasal MRSA colonization and the risk of MRSA-SSI after spine surgery
17
The pooled results from five studies [11, 12, 15-17] showed that nasal MRSA colonization
18
may be associated with an increased risk of MRSA-SSI in patients after spine surgery
19
(RR=6.21, 95% CI: 2.37–16.25; p<0.001; Figure 3B). No significant heterogeneity was
20
detected (p for Cochrane’s Q test =0.56, I2=0%). Sensitivity analyses with one study excluded
21
at a time returned consistent results (RR: 4.47–8.27, all p<0.05). Subgroup analyses showed
11
1
that nasal MRSA colonization may be associated with an increased risk of MRSA-SSI in
2
studies in which decolonization of MRSA was not applied (RR=15.02, 95% CI: 3.69–61.19;
3
p<0.001), but the association became insignificant in the analysis of studies in which
4
decolonization of MRSA was applied (RR=2.85, 95% CI: 0.76–10.66; p=0.12). These results
5
suggest that decolonization of MRSA may be associated with a reduced risk of MRSA-SSI in
6
patients with nasal MRSA colonization after spine surgery.
7 8
Publication bias
9
Funnel plots for the associations between nasal SA, MSSA, and MRSA colonization and
10
overall SSI risk as well as the association between nasal MRSA colonization and MRSA-SSI
11
risk are shown in Figure 4A-D. The funnel plots were symmetric on visual inspection.
12
Egger’s regression tests were not performed due to the limited number of studies included.
13 14
Discussion
15
In this meta-analysis of pooled results from seven follow-up studies, we found that nasal
16
colonization of SA or MSSA was unlikely to be associated with a significantly increased risk
17
of SSI after spine surgery. However, nasal colonization of MRSA may be associated with
18
increased risks for overall SSI and MRSA-SSI after spine surgery. Interestingly, subgroup
19
analyses showed that the association between nasal MRSA colonization and the increased
20
risk of SSI seemed to be mainly driven by studies in which nasal MRSA decolonization was
21
not applied. In the subgroup analysis of studies in which nasal MRSA decolonization was
12
1
applied, the associations between nasal MRSA colonization and increased risks of overall SSI
2
and MRSA-SSI became insignificant. These results suggest that nasal MRSA colonization
3
may be associated with an increased risk of overall SSI and MRSA-SSI after spine surgery,
4
while nasal MRSA decolonization may be associated with a reduction in the risk of SSI in
5
these patients.
6 7
The association between nasal carriage of SA and SSI has been suggested by studies of
8
patients receiving orthopedic surgeries. In an early meta-analysis of six studies, Levy et al
9
demonstrated that nasal carriage of SA is a major risk factor for SSI after general orthopedic
10
surgeries (pooled odds ratio [OR]=5.92, p=0.03). However, these results were based on direct
11
pooling of the ORs from individual studies, and considerable heterogeneity was detected
12
(I2=90%). As mentioned by the authors, the considerable heterogeneity among the included
13
studies was reflective of the different study characteristics and methodology of the included
14
studies, which makes the interpretation of the results difficult [25]. Also, the authors were
15
unable to determine which strains of SA (MSSA or MRSA) contributed to the potential
16
association between nasal colonization of SA and SSI after orthopedic surgeries. Moreover,
17
the previous hypothesis that nasal SA colonization is the major acquisition pathway for SSI
18
after orthopedic surgery has been challenged by the inconsistent results of some studies.
19
Berthelot et al. investigated a total of 3,908 consecutive patients undergoing orthopedic
20
surgery [26]. For 22 patients with SSI related to SA, only nine were nasal SA carriers before
21
surgery [26]. Moreover, among the nine nasal SA carriers who developed SSI, three had
13
1
different pairs of SA strains on nasal swabs and at the infection site, suggesting that the
2
association between nasal SA colonization and SA-related SSI may not be as close as
3
previously considered [26]. In our study, by pooling the results of all available follow-up
4
studies of patients who received spine surgeries, nasal colonization of SA or MSSA was
5
unlikely to be associated with increased risks of SSI. These findings also support the
6
uncertainty of the association between SA (primarily MSSA) and the affected SSI risk after
7
spine surgeries. Another potential mechanism, from our perspective, perhaps is that the
8
intensive administration of perioperative antibiotics for patients scheduled to undergo spine
9
surgery may block the potential acquisition of MSSA from endogenous colonization to the
10
surgical sites.
11 12
Another finding of our meta-analysis is that nasal colonization of MRSA seemed to be
13
associated with increased risks of overall SSI and MRSA-SSI after spine surgery. These
14
results may indicate the importance of screening for nasal colonization of MRSA, rather than
15
MSSA, for the identification of patients at higher risk for development of SSI. Further
16
subgroup analyses showed that the association between nasal MRSA colonization and an
17
increased risk of SSI was mainly driven by studies in which nasal MRSA decolonization was
18
not applied. From the subgroup analysis of studies in which nasal MRSA decolonization was
19
applied, the associations between nasal MRSA colonization and increased risk of overall and
20
MRSA-SSI became insignificant. These results suggest that nasal MRSA colonization may be
21
a risk factor for the development of SSI after spine surgery, and effective decolonization of
14
1
nasal MRSA may help to prevent SSI. This is consistent with the findings of a previous
2
meta-analysis of patients treated with cardiac or general orthopedic procedures. The previous
3
meta-analysis included 39 studies of patients who underwent cardiac or total joint
4
replacement procedures and demonstrated that application of glycopeptide prophylaxis with
5
or without nasal decolonization significantly reduced the risk of MRSA-SSI [27]. In another
6
recently published meta-analysis of patients who received total knee and hip arthroplasty,
7
Sadigursky et al. found that the use of a prophylaxis protocol for decolonization of MRSA
8
significantly reduced the incidence of SSI by 39% in these patients. These findings, together
9
with ours, demonstrate that nasal colonization of MRSA may be a risk factor of SSI after
10
surgery, and screening and decolonization of nasal MRSA may be effective at reducing the
11
incidence of SSI after spine surgery.
12 13
It has to be mentioned that the pathogenesis of SSI after spine surgeries is multifactorial [28].
14
Many clinical factors, including patient characteristics (e.g., obesity, diabetes, and smoking),
15
a longer operative time, transfusion during the operation, and other factors have been
16
suggested to be important risk factors for the incidence of SSI after spine surgeries [8, 29].
17
Due to the limited number of cases with SSI in each study and small number of available
18
studies in our meta-analysis, our analysis for the association between nasal MRSA
19
colonization and SSI after surgery was based on univariate findings rather than multivariable
20
adjusted findings. The potential imbalance of these clinical factors related to SSI may
21
confound our finding of the association between nasal MRSA colonization and incidence of
15
1
SSI after spine surgeries. Our results should be confirmed in cohort studies with larger
2
sample sizes that incorporate adequate adjustment of multiple factors that may influence the
3
SSI, such as the prevalence of diabetes between groups, differences in the immune status of
4
patients, and differences in surgical times and procedure characteristics.
5 6
Our study has limitations. First, the number of included studies was small, which prevented
7
us from evaluating the potential influences of patient (e.g., smoking status, with or without
8
diabetes, and hypertension) or procedure characteristics (different types of spine surgeries) on
9
the association between nasal SA colonization and SSI events after spine surgeries. Second,
10
we only included studies published in English, which may lead to additional bias by
11
potentially missing of studies published in other languages. Third, as a meta-analysis of
12
observational studies, a causative association between nasal MRSA colonization and the
13
increased risk of SSI after spine surgeries could not be retrieved based on our results. Fourth,
14
also due to the nature of a meta-analysis of observational studies, we could not exclude the
15
possibility that potential clinical factors for SSI may confound our findings. Moreover,
16
although the potential efficacy of nasal MRSA decolonization for the prevention of SSI after
17
spine surgery should be optimally investigated in randomized controlled trials, due to the
18
ethical reasons, these clinical trials cannot be performed. Finally, the optimal regimens for
19
nasal MRSA decolonization should be evaluated in future studies.
20 21
In conclusion, nasal MRSA colonization may be associated with increased risks of overall
16
1
SSI and MRSA-SSI after spine surgeries, while nasal MRSA decolonization may be
2
associated with a reduction in the risk of SSI in these patients. Further studies are needed to
3
validate our findings and determine whether the association between nasal MRSA
4
colonization and SSI after spine surgery is independent of the characteristics of patients and
5
surgical procedures. Moreover, the optimal regimens for nasal MRSA decolonization remain
6
to be determined.
7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33
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Figure legends
Figure 1 Diagram of study selection.
19
Figure 2 Forest plots for the meta-analysis of associations of nasal colonization of (A) SA and (B) MSSA with overall SSI risk after spine surgery.
20
Figure 3 Forest plots for the meta-analysis of associations of nasal colonization of MRSA with (A) overall SSI and (B) MRSA-SSI risk after spine surgery.
21
Figure 4 Funnel plots for the associations of nasal colonization of (A) SA, (B) MSSA, and (C) MRSA with the risk of SSI after spine surgery, and for the association of nasal colonization of (D) MRSA with the risk of MRSA-SSI after spine surgery.
22
Table 1 Characteristics of the included studies. Study
Design
Country
Patients and
Number
procedures
of patients
Mean age years
Thakkar 2014
RC
USA
Male
Screening method
%
Patients
Nasal
underwent spine
swab,
surgeries for
519
59
48
within 30
arthrodesis and
days before
decompression
surgery
Nasal
Nasal
Decolonization
SA
MRSA
methods for
positive
positive
MRSA
%
%
26.0
4.8
Follow-up duration
SSI outcomes reported
NOS score
months MRSA-SSI NA
12
and overall
6
SSI
Patients Ramos 2016
underwent spine RC
USA
surgeries for
Nasal swab 3556
51
52
primary spinal
before
Topical 18.8
2.7
admission
mupirocin and
12
Overall SSI
7
i.v. vancomycin
fusion Pediatric Luhmann 2016
RC
USA
patients who had spine surgery
Nasal swab 339
13
NA
1-4 weeks before
22.1
5.9
Topical mupirocin
MRSA-SSI 12
Kobayashi 2018
PC
Japan
underwent instrumental
Nasal swab 132
45
50
2018
PC
France
Patients underwent
35.6
3.8
admission
spine surgery Mallet
before
331
16
17
Nasal swab for twice
23
22.7
3
Topical mupirocin Topical mupirocin and
6
SSI
surgery Patients
and overall
MRSA-SSI 12
and overall
6
SSI 11
MRSA-SSI and overall
7
adolescent
within 12
idiopathic
months
scoliosis surgery
i.v. vancomycin
SSI
before surgery
Patients Nielsen 2018
RC
USA
underwent posterior spinal
Nasal swab 1200
14
36
fusion
2018
RC
Japan
underwent elective spine surgery
MRSA-SSI NR
2.8
NA
12
surgery
Patients Kawabata
before
and overall
6
SSI
Nasal swab 4573
61
60
before
NR
1.1
NA
12
Overall SSI
7
surgery
SA, Staphylococcus aureus; MRSA, methicillin-resistant Staphylococcus aureus; SSI, surgical site infection; NOS, Newcastle-Ottawa Scale; RC, retrospective cohort; PC, prospective cohort; NR, not reported; NA, not applied; i.v., intravenous
24