American Journal of Infection Control xxx (2015) 1-4

Contents lists available at ScienceDirect

American Journal of Infection Control

American Journal of
Infection Control

journal homepage: www.ajicjournal.org

Major article

Risk factors for surgical site infections after neurosurgery: A focus

on the postoperative period
Nadim Cassir MD a, *,1, Silvestre De La Rosa MD b,1, Anthony Melot MD b,
Adamou Touta MD b, Lucas Troude MD c, Anderson Loundou PhD c,
Herv Richet PhD a, Pierre-Hugues Roche PhD b
a
Unit de Recherche sur les Maladies Infectieuses Tropicales et Emergentes, UM63, CNRS 7278, IRD 198, Inserm 1095, Institut Hospitalo-Universitaire
Mditerrane-Infection, Aix-Marseille-Universit, Marseille, France
b
Service de Neurochirurgie, CHU Nord, Marseille, France
c
Unit de Recherche de Sant Publique et Maladies Chroniques, Universit Aix-Marseille, Marseille, France

Key Words:
Surgical site infections
Neurosurgery
Infection control
Intensive care unit
Risk factors

Background: Surgical site infection (SSI) after neurosurgery has potentially devastating consequences.
Methods: A prospective cohort study was conducted over a period of 24 months in a university center. All
adult patients undergoing neurosurgical procedures, with exception of open skull fractures, were
included. Multivariate logistic regression analysis was used to identify independent risk factors.
Results: We included 949 patients. Among them, 43 were diagnosed with SSI (4.5%). A signicant
reduction in postneurosurgical SSI from 5.8% in 2009 to 3.0% in 2010 (P .04) was observed. During that
period, an active surveillance with regular feedback was established. The most common microorganisms
isolated from SSI were Staphylococcus aureus (23%), Enterobacteriaceae (21%), and Propionibacterium acnes
(12%). We identied the following independent risk factors for SSI postcranial surgery: intensive care unit
(ICU) length of stay 7 days (odds ratio [OR] 6.1; 95% condence interval [CI], 1.7-21.7), duration of
drainage 3 days (OR 3.3; 95% CI, 1.1-11), and cerebrospinal uid leakage (OR 5.6; 95% CI, 1.1-30).
For SSIs postspinal surgery, we identied the following: ICU length of stay 7 days (OR 7.2; 95% CI,
1.6-32.1), coinfection (OR 9.9; 95% CI, 2.2-43.4), and duration of drainage 3 days (OR 5.7; 95% CI,
1.5-22).
Conclusion: Active surveillance with regular feedback proved effective in reducing SSI rates. The postoperative period is associated with overlooked risk factors for neurosurgical SSI. Infection control
measures targeting this period are therefore promising.
Copyright 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc.
Published by Elsevier Inc. All rights reserved.

Surgical site infections (SSIs) are the most common and serious
complications among surgically treated patients, resulting in
increased rates of morbidity and mortality, length of stay in hospital, and costs.1,2 SSIs are now recognized as the most common and
most costly health careeassociated (HA) infections in the United
States.3 Reported rates of SSI are relatively variable, ranging from
1%-8% in published series after cranial surgery and from 0.5%-18.8%
after spine surgery.4,5 Such wide-ranging results from different
reports may be caused by signicant variations in operative factors,
* Address correspondence to Nadim Cassir, MD, Unit de Recherche sur les
Maladies Infectieuses Tropicales et Emergentes (URMITE), UM63, CNRS 7278, IRD
198, Inserm U1095, Institut Hospitalo-Universitaire Mditerrane-Infection, AixMarseille-Universit, 27 Boulevard Jean Moulin, 13385 Marseille cedex 05, France.
E-mail address: cassirnadim@gmail.com (N. Cassir).
Conicts of interest: None to report.
1
These authors contributed equally to this work.

such as the use of implants or drains, the surgical approach itself,

and population heterogeneity.5 Because of the potentially devastating consequences of infectious complications, studying their
specic risk factors remains of major importance for determining
accurate preventive strategies, especially because up to 60% of SSIs
are estimated to be preventable when using evidence-based
guidelines.6
Although advances have been made in infection control preand perioperative practices, including improved operating room
ventilation, sterilization methods, barriers, surgical technique, and
availability of antimicrobial prophylaxis, SSIs remain a substantial
concern in neurosurgery.7 Several studies have documented the
efcacy of preoperative showers at reducing skin microbial
counts, but the evidence of their effect on infection rates is less
compelling.8 Additionally, Young et al showed that errors in individual antibiotic prophylaxis measures were not signicantly

0196-6553/$36.00 - Copyright 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ajic.2015.07.005

N. Cassir et al. / American Journal of Infection Control xxx (2015) 1-4

associated with SSI.9 On the other side, risk factors for SSI in the
postoperative period have been scarcely studied.
In this study, we analyze the rates, types, and main risk factors
for SSIs after neurosurgical procedures with a focus on the postoperative period.
MATERIALS AND METHODS
We conducted a prospective cohort study of SSI among adult
neurosurgical patients at the 694-bed, University Nord Hospital in
Marseille (France). All patients undergoing neurosurgical procedure (brain or spine surgery) from January 1, 2009-December 31,
2010, were eligible for inclusion. We excluded patients already
diagnosed with an SSI, patients with open skull fracture, and those
for whom the follow-up was incomplete. A neurosurgeon and a
member of the infection control team systematically reviewed the
medical records of each surgical patient. Postsurgical follow-up
was performed for all included patients after at least 30 days (or
1 year if an implant was left in place after the procedure). All
patients underwent the same skin preparation protocol before
surgery. No modications in infection control measures were
observed during the study period. The use of prophylactic antibiotics was performed according to the French Society of Anaesthesia and Intensive Care (Societ Franaise dAnesthsie
Ranimation) guidelines.10
The denitions for SSI used by the Centers for Disease Control
and Prevention were used in this study.11 SSIs were separated into 2
groups (supercial SSIs limited to the suppuration of wounds,
disunion of scars, and abscess of the scalp or wall and deep SSIs,
such as organ or space SSIs, such as meningitis, ventriculitis, osteomyelitis, or abscess) depending on the site and extent of infection.
The Altemeier score used by the American College of Surgeons
wound classication schema was divided into 4 classes: clean,
clean-contaminated, contaminated, and dirty.12 The National
Nosocomial Infections Surveillance (NNIS) score (composed of the
American Society of Anesthesiologists score, Altemeier score, and
surgery duration) was applied for all surgeries, on a scale of 0-3
points. Permanent prosthetic implants included cranioplasty kit,
synthetic dura, and spinal anterior or posterior osteosynthesis.
Transient material included ventriculoperitoneal or external ventricular shunts and subcutaneous drains. Cerebrospinal uid
leakage was recorded on the basis of otorrhea, rhinorrhea, or
leakage from the surgical wound.
The following data were recorded age, comorbid conditions,
length of preoperative stay, reason for the surgery, type of operative
procedure, previous surgery at the same site, SSI classication,
causative microorganisms, permanent prosthetic implant or transient material used, emergency or scheduled surgery, NNIS score,
length of drainage, cerebrospinal uid leakage, postoperative
length of stay in the intensive care unit (ICU), coinfections (postoperative infections documented at another site) and coinfection
causative microorganisms.
PASW Statistics 17.0 (SPSS, Inc., Hong-Kong, China) was used
for the statistical analysis. Mean  SD or median with minimum
and maximum was used to describe continuous variables. Percentage and number of events were used for quantitative variables. Student t test or Mann-Whitney U test was used to perform
2-group comparisons for quantitative variables. The c2 test was
used to perform 2-group comparisons for qualitative variables, or
the Fisher exact test was used when the expected count was <5. A
multivariate analysis using logistic regression was performed to
identify independent risk factors for SSI. Variables clinically relevant and associated (P < .10) with SSI in univariate analysis were
used in the model. A signicance threshold of .05 was adopted for
all statistical analyses.

RESULTS
A total of 949 neurosurgical patients were prospectively
included during a 24-month period. Their age ranged from 1890 years (mean  SD, 55.9  18 years); 533 (56.5%) of them were
men. The procedures were divided into cranial surgery (n 526;
55.4%) and spinal surgery (n 423; 44.6%). The general combined
SSI rate was 4.5% (43 SSIs), corresponding primarily to deep or
organ-space SSI (n 37; 86%). It was divided into 25 SSIs (4.7%) for
cranial surgery and 18 SSIs (4.2%) for spinal surgery. The general
rate decreased from 5.8% in 2009 to 3.0% in 2010 (P .04). During
the study period, quarterly feedback of SSI incidence was shared
with the surgical team.
The predominantly isolated organisms in patients with SSI were
Staphylococcus aureus (23%), Enterobacteriaceae (21%), and Propionibacterium acnes (12%) (Table 1). After brain surgery, S aureus (24%)
were most frequently isolated, whereas Enterobacteriaceae (33%)
was most frequently isolated after spinal surgery. Coinfections
during the postoperative period corresponded to HA bloodstream
infections (n 6; 14%), HA urinary tract infections (UTIs) (n 5;
11.6%), and HA pneumonia (n 2; 4.6%). In 6 cases of SSI (14%), the
same microorganism was isolated from coinfection sites (2 UTIs
caused by Klebsiella pneumonia, 1 UTI caused by Escherichia coli, 2
catheter-related infections caused by S aureus, 1 ventilatorassociated pneumonia caused by Pseudomonas aeruginosa).
Risk factors independently associated with SSI after cranial
surgery were a NNIS score 2 (odds ratio [OR] 9.6; 95%
condence interval [CI], 3.7-23.9), previous surgery at the
same site (OR 6.8; 95% CI, 1.6-29.4), postoperative ICU length
of stay 7 days (OR 6.1; 95% CI, 1.7-21.7), duration of
drainage 3 days (OR 3.3; 95% CI, 1.1-11), and cerebrospinal uid
leakage (OR 5.6; 95% CI, 1.1-30) (Table 2). Risk factors independently associated with SSI after spinal surgery were a NNIS score 2
(OR 8.5; 95% CI, 2.2-32.5), postoperative ICU length of
stay 7 days (OR 7.2; 95% CI, 1.6-32.1), postoperative coinfection
(OR 9.9; 95% CI, 2.2-43.4), and duration of drainage 3 days
(OR 5.7; 95% CI, 1.5-22) (Table 3).
DISCUSSION
In this study we observed a signicant decrease of the SSI
incidence rate during a 2-year surveillance period. Implementation
of an active surveillance with quarterly feedback to the surgical
staff may have contributed to it.13 As noted by Heipel et al, active
surveillance by an infection control practitioner together with
neurosurgeons may enhance signicantly the sensitivity for
detecting SSI.14 Moreover, in a French national-based surveillance
program, the SSI rate decrease was associated with survey implementation and regular feedback.15 The percentage decrease, however, was lower after the rst 3 years, probably because of
difculties in maintaining the resources needed to constantly
monitor all surgical patients.15 In addition, it has recently been
shown that each episode of wound infection after a spine procedure contributed to a mean increase in the cost of care by $4,067
compared with a noncomplicated case.16 These ndings highlight
the need for permanent signicant infection control resources to
limit the global burden of SSI.
Our multivariate analysis led us to identify independent risk
factors for neurosurgical SSI during the postoperative period,
especially an ICU length of stay 7 days. Previous studies have
already identied the ICU length of stay as an independent risk
factor for neurosurgical SSI in general.17,18 This could be in part
explained by the fact that ICU patients are more vulnerable to
skin colonization and HA infections and that manipulation of
different devices represents a risk for cross-transmission in the

N. Cassir et al. / American Journal of Infection Control xxx (2015) 1-4

Table 1
Causative microorganisms of the 43 surgical site infections

Microorganisms
Staphylococcus aureus
CoNS
Enterococcus spp
Enterobacteriaceae
Pseudomonas aeruginosa
Propionibacterium acnes
Other anaerobes
Multibacteria
Undocumented

Brain surgery
(n 25)
6
0
2
3
2
4
1
4
3

Table 3
Factors associated with SSI after spinal surgery

Spinal surgery
(n 18)

(24)
(0)
(8)
(12)
(8)
(16)
(4)
(16)
(12)

4
2
0
6
0
1
3
1
1

(22.2)
(11.1)
(0)
(33.3)
(0)
(5.5)
(16.6)
(5.5)
(5.5)

Total
(N 43)
10
2
2
9
2
5
4
5
4

(23.2)
(4.6)
(4.6)
(20.9)
(4.6)
(11.6)
(9.2)
(11.6)
(9.2)

NOTE. Values are n (%).

ConS, coagulase-negative staphylococci.

Table 2
Factors associated with SSI after cranial surgery

Factors

SSI
No SSI
Univariate Multivariate
(n 25) (n 501)
P value
P value

Background conditions
Age, median  SD (y)
57  18
Sex (male)
15 (60)
Comorbidities
Tobacco
9 (36)
Alcohol
2 (8)
Corticotherapy
8 (32)
Diabetes
2 (8)
Malignancy
11 (44)
ASA score 3
12 (48)
Operation characteristics
NNIS score 2
16 (64)
Previous surgery same site
6 (24)
Emergency
10 (40)
Pathology
Vascular
4 (16)
Tumoral
9 (36)
Traumatic
10 (40)
Hydrodynamic
2 (8)
Surgical approach
Craniectomy
4 (16)
Craniotomy
20 (80)
Trepan
1 (4)
Foreign body
9 (36)
Type
Cranioplasty (synthetic)
1 (4)
Shunts
1 (4)
Ommaya reservoir
0 (0)
Dural plasty
4 (16)
Aneurysm clip
2 (8)
Gliadel wafers (Elsai, Inc.,
1 (4)
Woodcliff Lake, NJ)
Length of hospitalization
7 (28)
before surgery 2 d
Postoperative period
Length of postoperative stay 11 (44)
in ICU  7 d
Other infection
5 (20)
Duration of drainage 3 d
9 (36)
CSF leakage
3 (12)

60  18
277 (55.3)

.40
.60

NA
NA

115
29
126
47
279
176

.10
.60
.50
.90
.30
.20

NA
NA
NA
NA
NA
NA

(23)
(5.8)
(25.1)
(9.4)
(55.6)
(35.1)

61 (12.2)
33 (6.6)
269 (53.7)

<.0001*
.008*
.20

<.001*
.01*
NA

69
218
167
46

(13.8)
(43.5)
(33.3)
(9.2)

.70
.50
.50
.90

NA
NA
NA
NA

33
393
76
85

(6.6)
(78.4)
(15)
(17)

.10
.90
.10
.03*

NA
NA
NA
.30

1
27
1
36
19
1

(0.2)
(5.4)
(0.2)
(7.2)
(3.8)
(0.2)

.10
.90
NA
.10
.30
.10

NA
NA
NA
NA
NA
NA

.40

NA

106 (21.2)

39 (7.8)

<.0001*

.005*

45 (9)
91 (18.2)
10 (2)

.09
.04*
.02*

.80
.04*
.04*

NOTE. Values are n (%) or as otherwise indicated.

ASA, American Society of Anesthesiologists; CSF, cerebrospinal uid; ICU, intensive
care unit; NA, not applicable; NNIS, National Nosocomial Infections Surveillance; SSI,
surgical site infection.
*P <.05.

postoperative period.19 We have recently demonstrated that

Enterobacteriaceae were transient colonizers of ICU patients skin
and that this was related to the hospital length of stay, therefore
representing an underestimated source of HA infection.20,21 Interestingly, our current study shows that Enterobacteriaceae were the
rst causative microorganisms (33.3%) of SSI after spinal surgery. In
a recent study of SSI after neurosurgery, Acinetobacter baumannii,

Factors
Background conditions
Age, median  SD (y)
Sex (male)
Comorbidities
Tobacco
Alcohol
Corticotherapy
Diabetes
Malignancy
ASA score 2
Operation characteristics
NNIS score 2
Previous surgery same site
Emergency
Pathology
Vascular
Tumoral
Traumatic
Degenerative
Surgical approach
Anterior
Posterior
Percutaneous
Foreign body
Type
Osteosynthesis
Cementoplasty
Length of hospitalization
before surgery 2 d
Postoperative period
Length of postoperative
stay in ICU 7 d
Other infection
Duration of drainage 3 d

SSI
(n 18)

No SSI
(n 405)

58  18
52  17
11 (61.1) 245 (60.5)

Univariate Multivariate
P value
P value
.10
.90

NA
NA

.30
NA
NA
.70
NA

NA
NA
NA
NA
NA

7 (38.9)
26 (6.4)
2 (11.1)
33 (8.1)
15 (83.3) 162 (40)

<.0001*
.60
<.001*

.002*
NA
.10

0
0
15
3

(0)
6 (1.5)
(0)
36 (8.9)
(83.3) 130 (32.1)
(16.7) 233 (57.5)

NA
NA
<.0001*
<.001*

NA
NA
.08
NA

1
17
0
16

(5.6)
59 (14.6)
(94.4) 307 (75.8)
(0)
39 (9.6)
(88.9) 178 (44)

.30
.06
NA
<.0001*

NA
NA

16 (88.9) 167 (41.2)

0 (0)
11 ()
3 (16.7)
45 (11.1)

<.0001*
NA
.50

NA
NA
NA

7
0
0
1
0

(38.9) 114 (28.1)

(0)
22 (5.4)
(0)
17 (4.2)
(5.6)
34 (8.4)
(0)
15 (3.7)

.50

7 (38.9)

7 (1.7)

<.0001*

.01*

8 (44.4)
14 (77.8)

10 (2.5)
86 (21.2)

<.0001*
<.0001*

.002*
.01*

NOTE. Values are n (%) or as otherwise indicated.

ASA, American Society of Anesthesiologists; ICU, intensive care unit; NA, not applicable; NNIS, National Nosocomial Infections Surveillance; SSI, surgical site infection.
*P <.05.

which is not considered a skin commensal, was observed as the

second most frequent organism (16.1%).22 Additionally, in a prospective study of postcraniotomy meningitis, gram-negative bacteria (ie, Acinetobacter spp, Klebsiella spp, P aeruginosa, Enterobacter
cloacae, Proteus mirabilis) represented 88% of the pathogens.23
Although identied in other studies as an independent risk
factor for neurosurgical SSI,17,24 a recent review showed that the use
of postoperative drains did not have a secondary effect on infection.25 We identied in this study the duration of drainage 3 days
as an independent risk factor for SSI after both brain and spinal
surgeries. These results suggest that when postoperative drains are
used, the duration of drainage should be limited.
We also identied postoperative coinfections as an independent
risk factor for SSI after spinal surgery. Other studies had already
pointed to the role of coinfections as a risk factor for SSI. Mollman
and Haines, for instance, reported that concurrent noncentral
nervous system infection increased 6-fold the risk of postoperative
neurosurgical infections.26 Recently, Sneh-Arbib et al documented
phenotypically identical isolates from respiratory secretions preSSI to those causing the neurosurgical SSI, in 4 out of 9 patients.27
Kourbeti et al also identied ventilator-associated pneumonia and
UTI as independent risk factors for SSI after neurosurgery procedures.17 Therefore, global HA infection prevention in the postoperative period represents an important measure for the
prevention of SSI.28
Finally, we hypothesize a critical role of postoperative wound
care in SSI prevention. Occlusive dressings have been advocated

N. Cassir et al. / American Journal of Infection Control xxx (2015) 1-4

because they would potentially maintain a sterile barrier for longer

periods postoperatively.29 In a recent study, Le et al showed that a
cranioplasty bundle, including meticulous attention to wound
closure, was associated with reduced SSI rates and lessened the
need for redo cranioplasties.30 Further studies are needed to evaluate the quality of wound care, and measure its impact on SSI rates.
CONCLUSION
Effective infection control programs should include an adequate
number of trained infection control staff and a system for sustained
reporting of SSI rates to surgeons. Infection control measures during the postoperative period represent a window of opportunity to
improve the management of neurosurgical patients and to decrease
their incidence of SSI.
Acknowledgment
We thank Yves Seccia for his technical assistance.
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