Journal of Hospital Infection 96 (2017) 1e15

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Journal of Hospital Infection

journal homepage: www.elsevierhealth.com/journals/jhin

Review

Impact of surgical site infection on healthcare costs and

patient outcomes: a systematic review in six European
countries
J.M. Badia a, A.L. Casey b, N. Petrosillo c, P.M. Hudson d, S.A. Mitchell d,
C. Crosby e, *
a
Hospital Universitari de Granollers, Universitat Internacional de Catalunya, Granollers, Spain
b
Department of Clinical Microbiology, University Hospitals Birmingham NHS Foundation Trust, Edgbaston, Birmingham, UK
c
National Institute for Infectious Diseases ‘L. Spallanzani’, IRCCS, Rome, Italy
d
DRG Abacus, Bicester, UK
e
Becton Dickinson & Co., Franklin Lakes, NJ, USA

A R T I C L E I N F O S U M M A R Y

Article history: Background: Surgical site infections (SSIs) are associated with increased morbidity and
Received 15 November 2016 mortality. Furthermore, SSIs constitute a financial burden and negatively impact on pa-
Accepted 1 March 2017 tient quality of life (QoL).
Available online 8 March 2017 Aim: To assess, and evaluate the evidence for, the cost and health-related QoL (HRQoL)
burden of SSIs across various surgical specialties in six European countries.
Keywords: Methods: Electronic databases and conference proceedings were systematically searched
Surgical site infection to identify studies reporting the cost and HRQoL burden of SSIs. Studies published post
Surgery 2005 in France, Germany, the Netherlands, Italy, Spain, and the UK were eligible for data
Europe extraction. Studies were categorized by surgical specialty, and the primary outcomes were
Economic burden the cost of infection, economic evaluations, and HRQoL.
Quality of life Findings: Twenty-six studies met the eligibility criteria and were included for analysis.
There was a paucity of evidence in the countries of interest; however, SSIs were consis-
tently associated with elevated costs, relative to uninfected patients. Several studies
reported that SSI patients required prolonged hospitalization, reoperation, readmission,
and that SSIs increased mortality rates. Only one study reported QoL evidence, the results
of which demonstrated that SSIs reduced HRQoL scores (EQ-5D). Hospitalization reportedly
constituted a substantial cost burden, with additional costs arising from medical staff,
investigation, and treatment costs.
Conclusion: Disparate reporting of SSIs makes direct cost comparisons difficult, but this
review indicated that SSIs are extremely costly. Thus, rigorous procedures must be

* Corresponding author. Address: CareFusion, Becton Dickinson, Procedural Solutions, 3750 Torrey View Court, San Diego, CA 92130, USA.
Tel.: þ1 913 485 1597.
E-mail address: cynthia.crosby@CareFusion.com (C. Crosby).

http://dx.doi.org/10.1016/j.jhin.2017.03.004
0195-6701/ª 2017 The Authors. Published by Elsevier Ltd on behalf of The Healthcare Infection Society. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
2 J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
implemented to minimize SSIs. More economic and QoL studies are required to make
accurate cost estimates and to understand the true burden of SSIs.
on behalf of The Healthcare Infection Society. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Surgical site infection (SSI) is one of the most frequently
reported types of hospital-acquired infection (HAI), consti-
tuting up to 19.6% of all HAIs in Europe in 2011e2012 [1]. The
Centre for Disease Control and Prevention (CDC) [and the
European Centre for Disease Prevention and Control (ECDC)]
defines SSI as postoperative infection occurring within 30 days
of a surgical procedure (or within one year for permanent im-
plants) [2e4].
The development of an SSI causes a substantial increase in
the clinical and economic burden of surgery. The financial
burden of surgery is increased due to the direct costs incurred
by prolonged hospitalization of the patient, diagnostic tests,
and treatment. Certain patients may also require reoperation
after the contraction of an SSI, which is associated with
considerable additional costs [5]. Indeed, Broex et al.
demonstrated that in European hospitals patients who develop
an SSI constitute a financial burden approximately double that
of patients who do not develop an SSI [6]. The same review also
reported that the length of hospitalization was more than
twice as long for patients with an SSI relative to uninfected
patients [6]. SSIs may therefore represent an opportunity cost
to hospitals by displacing hospital resources that would
otherwise be spent elsewhere, as well as delaying subsequent
patients’ surgery. Following discharge from hospital, SSI pa-
tients may also rely on healthcare from other community care
services, which will further contribute to the economic burden
of infection.
SSIs negatively impact on patient physical and mental
health. Increased patient morbidity, mortality, and loss of
earnings during recovery are some of the indirect costs asso-
ciated with infection. Intangible costs may also be incurred by
the patient, such as pain and anxiety. In addition, patients
may experience delayed wound healing and be more suscep-
tible to secondary complications, such as bacteraemia [7,8].
Distress may also be caused to the patient and family mem-
bers if the patient is absent from home and work for a pro-
longed period. Accordingly, prolonged hospitalization and
increased morbidity as a result of developing an SSI have been
shown to negatively impact on patient health-related quality
of life (HRQoL) [9].
There is limited evidence reporting the costs incurred
following the development of an SSI, and few recent data
comparing overall costs across surgical specialties. Thus, the
aim of this systematic review was to assess, and evaluate the
evidence for, the cost and HRQoL burden of SSI across various
surgical specialties in Europe. The six countries included in the
review were the ‘big five’ European nations (France, Germany,
Italy, Spain, the UK), as well as the Netherlands.
Methods
The following electronic databases were interrogated on
September 12th, 2015, to identify relevant studies: Embase,
ª 2017 The Authors. Published by Elsevier Ltd
Medline, and the Cochrane Library. Supplementary data
sources included reference lists of included publications and
the following conference proceedings over the last three years’
availability: the International Society for Pharmacoeconomics
and Outcomes Research (ISPOR), the European Society of
Clinical Microbiology and Infectious Diseases (ESCMID), the In-
ternational Conference on Prevention and Infection Control
(ICPIC), and the Healthcare Infection Society (HIS).
National studies reporting SSI economic and/or quality of
life (QoL) evidence in patients who underwent surgery in a
hospital setting met the inclusion criteria. The review
included studies published in English post 2005 that reported
data for France, Germany, the Netherlands, Italy, Spain, and
the UK. The population, interventions, comparators, out-
comes, study design (PICOS) statement is summarized in
Supplementary Appendix A. Titles and abstracts of publica-
tions yielded by the electronic searches were screened ac-
cording to the eligibility criteria, and non-relevant studies
were excluded. Full publications of potentially relevant pub-
lications were assessed by a single reviewer, and verified by a
second reviewer. Eligible studies were represented multiple
times if they reported on more than one European country or
operation type. See the PRISMA flow diagram (Figure 1), which
illustrates the number of eligible papers identified by the
systematic review.
Included studies were stratified by surgical specialty into
the following groups: cardiothoracic surgery, general surgery,
neurosurgery, orthopaedic and trauma surgery, otolaryngology,
urology, and multiple or unspecified surgery.
No. of records identified through database; n=9066
Embase=5339; Medline=2520; Cochrane=1207
Duplicates; n=1693
No. of records screened (by title and
Exclusion 1st pass; n=6997 abstract); n=7373
Disease/indication, n=1734
Review/editorial, n=1574
Study design, n=1237
Copy/duplicate, n=807
Country, n=904
Outcomes, n=411
Patient population, n=228
Animal/in vitro study, n=81
Treatment, n=12
Protocol only, n=6
No. of articles assessed for
eligibility (by full paper); n=360
Language, n=3
Exclusion 2nd pass; n=337
Abstract only, n=101
Outcomes, n=223
Country, n=8
Disease/indication, n=3
Copy/duplicate, n=2
Additional records identified
through hand searching; n=3
Included studies; n=26
Figure 1. Systematic review PRISMA flow diagram.
 J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
Economic evaluations (including costeutility, cost-
minimization, costeeffectiveness, and costebenefit ana-
lyses) and studies reporting relevant cost of illness and/or QoL
data were considered for inclusion. The primary outcomes of
interest were direct and indirect healthcare costs, cost
drivers, and proxy outcomes for which a cost could be applied
such as length of stay (LOS), readmissions, the number of
additional procedures required, and mortality. Both generic
and condition-specific questionnaires describing the QoL
associated with SSI and utilities derived from generic
preference-based instruments (e.g. the EQ-5D) were of in-
terest for the review. Quality assessment (QA) of cost of
illness/burden studies were assessed by a checklist adapted to
cost of illness (COI) by Molinier et al. [10].
Results
Search results
A total of 9066 papers were identified via the electronic
database searches. Upon the removal of duplicate papers,
7373 titles and abstracts were reviewed. A total of 360
potentially relevant publications were ordered for full paper
review. Twenty-six studies were identified that reported costs
and/or QoL associated with SSI; 24 were full publications and
two were abstracts only (Figure 1) [5,9,11e34]. Countries
from which the cost and QoL evidence was derived included
France (N ¼ 4), Germany (N ¼ 2), Italy (N ¼ 1), Spain (N ¼ 3),
and the UK (N ¼ 16) [5,9,11e34]. The surgical specialties
considered by the studies were cardiothoracic (N ¼ 4), general
(N ¼ 3), neurosurgery (N ¼ 2), orthopaedic and trauma (N ¼
7), otolaryngology (N ¼ 1), and urology (N ¼ 1)
[5,9,17,14,16,18e22,24,27e31,33,34]. Seven studies consid-
ered multiple surgical specialties and one study did not
specify the surgical specialty considered (Tables IeV)
[11e13,15,23,25,26,32].
France
Four full publication studies were identified for France
[14,15,25,27]. Two studies were cost analyses and two studies
were prospective cohort studies. The surgical specialties
considered in the studies included cardiothoracic surgery (N ¼
1), otolaryngology surgery (N ¼ 1), multiple surgical specialties
(N ¼ 1), and one study did not specify the surgical specialty.
The outcomes reported included the study incidence of SSIs
(N ¼ 3), direct costs (N ¼ 4), cost drivers (N ¼ 2), LOS (N ¼ 3),
mortality (N ¼ 2), and the requirement for additional proced-
ures (N ¼ 1) (Table I).
Germany
Two full SSI cost publications reporting the results of a
matched caseecontrol study were identified for Germany
[20,21]. It should be noted that the two publications for Ger-
many report equivalent data, but present the findings in dif-
ference currencies. The surgical specialty considered was
cardiothoracic surgery (N ¼ 2). The endpoints reported were
the direct costs of infection (N ¼ 2), cost drivers (N ¼ 2), LOS
(N ¼ 2), and mortality (N ¼ 2) (Table II).
The Netherlands
The systematic review identified no eligible studies for the
Netherlands.
3
Italy
One study reported the results of an SSI cost analysis in Italy
[33]. This study was detailed in an abstract and reported the
direct costs associated with SSIs following orthopaedic and
trauma surgery (Table III).
Spain
Three full publications investigating the burden of SSIs were
available for Spain, including a nested caseecontrol study, a
retrospective observational study, and an open-label compar-
ative clinical study [11,12,19]. The surgical specialties
considered in the studies were urology surgery (N ¼ 1) and
multiple surgical specialties (N ¼ 2). Outcomes reported across
the Spanish studies included study incidence of SSIs (N ¼ 3),
direct costs (N ¼ 3), indirect costs (N ¼ 1), LOS (N ¼ 3), mor-
tality (N ¼ 2), and resource consumption (N ¼ 1) (Table IV).
UK
Sixteen of the eligible studies were based in the UK; 15 were
full publications and one was an abstract
[5,9,13,16e18,22e24,26,28e32,34]. Study designs included
caseecontrol studies (N ¼ 2), surveillance studies (N ¼ 2),
randomized control trials (N ¼ 2), prospective cohort studies
(N ¼ 3), retrospective cohort studies (N ¼ 3), and cost analyses
(N ¼ 4). Surgical specialties considered in the studies were
cardiothoracic surgery (N ¼ 1), general surgery (N ¼ 3),
neurosurgery (N ¼ 2), orthopaedic and trauma surgery (N ¼ 6),
and multiple surgical specialties (N ¼ 4). Outcomes reported
across the UK-based studies included study incidence of SSIs
(N ¼ 10), direct costs associated with SSI (N ¼ 14), cost drivers
(N ¼ 5), HRQoL (N ¼ 1), LOS (N ¼ 12), mortality (N ¼ 5),
readmissions (N ¼ 3), additional procedures (N ¼ 2), and
resource use (N ¼ 1) (Table V).
Costs
France
The four studies available for France reported substantial
additional costs due to SSIs. Penel et al. reported that following
head and neck cancer surgery, patients who developed an SSI
constitute a total per-patient medical cost V17,434 higher than
those patients who did not develop an SSI. The total cost
estimation considered the additional laboratory testing, pro-
longed hospitalization, medication costs and medical staff
costs (Table I) [27].
Germany
The matched caseecontrol study in Germany demonstrated
that the total medical cost per patient was significantly
elevated in patients who contracted an SSI [$49,449 vs $18,218
(V36,261 vs V13,356) for SSI patients and uninfected patients,
respectively]. The results indicated that for patients who
developed an SSI, intensive care unit (ICU) and ward-care costs
accounted for the largest costs (27.7% and 24.7%, respec-
tively), whereas costs associated with laboratory tests and
other hospital costs were not higher for infected patients
compared with controls (Table II) [20,21].
Italy
Nobile et al. reported that in orthopaedic and trauma sur-
gery patients, the development of an SSI was associated with
additional total medical costs of V32,000, relative to
 4
Table I
Burden of surgical site infection in France
Study, publication type, study type No. of patients Epidemiology results Costs Proxy outcomes
(incidence/prevalence)
Cardiothoracic surgery (N ¼ 1)
Cossin et al. [14] N ¼ 8569 Rate of SSI: Total additional cost of SSI Mean duration of
Cost analysis study over four years: post-surgery hospital
Year 1 (2008): 52 (2.5%) stay (days):
Year 2 (2009): 35 (1.9%) With reimbursement: SSI: 23
Year 3 (2010): 45 (2.2%) V291,000 for 94 patients No SSI: 10 (P < 0.01)

J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15

Year 4 (2011): 62 (2.3%) Without reimbursement: Mortality during four-
V1,034,000 (patients NR) year study period:
SSI: 9 (5.4%)
No SSI: 205 (2.4%)

Otolaryngology (N ¼ 1)
Penel et al. [27] N ¼ 261 Incidence of SSI: Total medical cost per Mean hospital LOS
Prospective cohort study patient (SD): [days (SD)]:
94 (36%)
SSI: V39,957 (29,802) SSI: 35.02 (26.12)
No SSI: V22,523 (10,679) No SSI: 19.74 (9.36)

Multiple or unspecified surgical specialties (N ¼ 2)

Defez et al. [15] N ¼ 300 (SSI cases, n ¼ 30; NR Total additional cost per SSI NR
Prospective cohort study controls, n ¼ 30) patient by expenditure (SD):
V1,814 (4,226)
Total additional cost of SSI
by site: V386,297
Lamarsalle et al. [25] NR: 520,715 surgical Total incidence of SSI: 3.0% Total additional cost Overall mean LOS
Cost analysis study procedures were included associated with SSI following [days (range)]:
surgery in 2010:
SSI: 32 (13e62)
Public hospitals: No SSI: 14 (3e42)
V43,019,936 Mortality during 1
Private hospitals: year study period [%
V14,872,779 (range)]:

SSI: 8.3% (0.4e16.0)

No SSI: 2.0% (0.0
e13.1) (P < 0.001)

LOS, length of stay; NR, not reported; SD, standard deviation; SSI, surgical site infection.
 J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15 5
uninfected patients, corresponding to an average cost per SSI
of V9,560 [33]. It was noted that the abstract did not specify
which resources and costs were considered in the estimation of

Mortality during 27-month study

the total cost of SSIs (Table III).

LOS in hospital, days (95% CI): Spain

No SSI: 16.5 (14.0, 17.5)

Surgical site infections were associated with elevated costs

No SSI: 8.8% (P ¼ 0.03)

Proxy outcomes

SSI: 34.4 (30.1, 38.6) in the three studies available for Spain [11,12,19]. Alfonso et al.
reported that across multiple surgical specialties, the direct
(P ¼ 0.0006) total healthcare cost of developing an SSI was $1,084,639,
which was mainly attributable to prolonged hospitalization

SSI: 17.6%
period: (37%) and other hospital costs (43%). Primary healthcare costs
and antibiotic costs accounted for 14% and 6%, respectively.
When indirect costs such as SSI-related morbidity/mortality and
societal costs were also considered, healthcare costs only
accounted for about 10.5% of the total financial burden. Inter-
estingly, Alfonso et al. also demonstrated that SSI-related costs
were positively correlated with increasing age, with SSI
patients >80 years representing the largest financial burden
No SSI: $18,218 (16,520, 24,561);

(Table IV) [11].

SSI: $49,449 (42,505, 65,835);

No SSI: $1,599; V1,167 (ns)

UK
Cost per patient (95% CI):

V36,261 (31,028, 48,060)

V13,356 (12,060, 17,930)

Multiple studies reported that various surgical specialties

Cost per patient day:

were associated with elevated costs following the develop-

SSI: $1,385; V1,011

ment of an SSI [5,9,13,16e18,22e24,26,28e32,34]. For

example, Tanner et al. reported that general surgery patients
Costs

who contracted an SSI constituted an additional healthcare

(P < 0.0001)

CI, confidence interval; LOS, length of stay; ns, not significant; NR, not reported; SSI, surgical site infection.

financial burden of £10,523 per patient [29]. Cost drivers

identified in this study included prolonged LOS, treatment
costs and readmission costs. Several studies demonstrated that
the primary cost driver was prolonged postoperative hospital-
ization of infected patients, relative to uninfected patients
The 2010 publication reported costs in V and the 2011 publication reported costs in US$.

[13,29,30,32]. Additional expenditure was also attributed to

operative costs, medical staff costs, and investigation and
treatment costs [13,18,23,29,30,32]. For example, Jenks et al.
(incidence/prevalence)

reported that operating theatre and medical staff costs

Epidemiology results

accounted for 11% and 18% of the total additional costs asso-
ciated with infection, respectively [23]. Notably, the cost
burden was greater for patients who developed deep SSIs
NR

compared with superficial infections (Table V) [23,31].

Proxy outcomes
n ¼ 17; controls,

Proxy outcomes for which a cost could be applied included

No. of patients

N ¼ 51 (cases,

LOS, mortality, readmissions, and the number of additional

procedures required. Length of stay in hospital was higher
among patients who developed an SSI relative to uninfected
Burden of surgical site infection in Germany

n ¼ 34)

patients; this was true for all studies in the six European
countries and across all surgical specialties. The highest num-
ber of days required in hospital following the development of
Study, publication type, study type

an SSI was recorded after orthopaedic and trauma surgery in

Cardiothoracic surgery (N ¼ 2)

the UK (an additional 54 days with an SSI) [18]. Conversely,

prolonged hospitalization was lowest for one study in Spain,
Matched caseecontrol

which reported an additional LOS of 2.1 days among patients

Graf et al. [20,21] a

who develop SSIs after multiple or unspecified surgical

specialties [12]. However, variability existed between LOS
reported in studies in the same country as well for the same
surgical specialty (Figure 2) [11,12].
study
Table II

France
All three studies reporting LOS demonstrated that hospi-
a

talization was prolonged in patients who developed an SSI

6 J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
Table III
Burden of surgical site infection in Italy
Study, publication type, No. of patients Epidemiology results
study type (incidence/prevalence)
Orthopaedic and
trauma surgery (N ¼ 1)
Nobile et al. [33] N¼7 NR
Cost analysis study
NR, not reported; SSI, surgical site infection.
compared with uninfected patients [14,25,27]. Indeed, Penel
et al. reported that the mean duration of hospitalization for
patients who develop an SSI following head and neck cancer
surgery was 15.3 days longer than for uninfected patients [27].
Cossin et al. reported that the mean duration of post-surgery
hospitalization among patients who contracted an SSI after
cardiothoracic surgery was 2.3 times higher than for those who
did not. In addition, Lamarsalle et al. reported that mortality
during a one-year study period was significantly higher in SSI
patients relative to controls (8.3% vs 2.0%, respectively)
(Table I) [25].
Germany
The development of an SSI following cardiothoracic surgery
necessitated prolonged hospitalization. Graf et al. reported
that mean LOS in SSI patients was 17.9 days longer than for
those who did not contract an infection. In addition, the per-
centage mortality rate was double in patients who developed
an SSI compared with that of uninfected patients (Table II)
[20,21].
Spain
All three studies consistently reported that SSIs are
responsible for prolonged hospitalization relative to uninfected
patients. Accordingly, Gili-Ortiz et al. reported that mean LOS
was 17.8 days longer among patients who contracted an SSI
following radical cystectomy surgery, compared with unin-
fected patients [19]. This study also highlighted that the per-
centage mortality rate among SSI patients after surgery was
about 2.4 times higher than among those who did not develop
an SSI (Table IV).
UK
Multiple studies demonstrated that the length of hospi-
talization was greater in patients who contracted an SSI
following surgery, compared with uninfected patients
[5,18,23,24,28,29,31,34]. Interestingly, Coello et al. high-
lighted that the additional LOS after contraction of an SSI
varied between surgical specialties, ranging from 3.3 days
Costs Proxy outcomes
Direct cost associated with SSI: NR
Total extra cost of SSI: V32,000
Average cost per SSI: V9,560
Cost of hospital admissions: V3,411
eV22,273
Cost borne by regional health service:
V57,419
Average cost per case: V8,202
Cost borne by hospital: V8,513
Average cost per case: V1,216
(abdominal hysterectomy) to 21.0 days (limp amputation)
[13]. The length of hospitalization following the development
of an SSI also varied between surgical specialties in other UK
studies, ranging from an additional 11.93 days following knee
prosthesis surgery, to 54 additional days after hip fracture
surgery [18,24]. It was also noted that hospitalization was
longer for patients who developed a deep SSI compared with
a superficial infection [23,31]. SSIs were reported to result in
increased hospital readmissions and reoperations compared
with uninfected patients [5,22,29,31]. Notably, patients who
underwent orthopaedic and trauma surgery and developed a
deep SSI (N ¼ 8) had a total of 14 reoperations in addition to
their index procedure [31]. Furthermore, Tanner et al. re-
ported that three out of 29 patients who contracted an SSI
after general surgery were readmitted following hospital
discharge. Increased mortality rates among SSI patients were
also reported relative to those who did not contract an SSI
(Table V) [13].
Quality of life
Eligible studies reporting SSI QoL data were only available
for one study in the UK. The study was a full publication de-
tailing the results of a randomized control study conducted in
2013 [9]. EQ-5D scores demonstrated that SSIs negatively
impact on patient HRQoL, demonstrated by a statistically sig-
nificant reduction in HRQoL scores (11%) at 30 days in patients
who underwent laparotomy surgery, relative to patients who
did not develop an SSI [9]. It is noteworthy that the results of
this study were also included in a recent systematic review by
Gheorghe et al., who reported that the SSI utility decrement in
patients who developed an SSI after laparotomy surgery was
0.05 at 7 days and 0.12 at 30 days (Table V) [35].
Discussion
This systematic review confirms that a significant number of
SSIs occur following various surgical specialties in European
Table IV
Burden of surgical site infection in Spain
Study, publication type, study
type
Urology (N ¼ 1)
Gili-Ortiz et al. [19]
Retrospective observational
study
Multiple surgical specialties (N ¼ 2)
Alfonso et al. [11]
Nested caseecontrol study
Arroyo et al. [12]
Open-label comparative
clinical study
HR, hazard ratio; LOS, length of stay; NR, not reported; SD, standard deviation; SSI, surgical site infection.
No. of patients Epidemiology results (incidence/
prevalence)
N ¼ 4377 SSI incidence: 859 (19.4%)
N ¼ 1962 Rates of SSI for all surgical
patients:
Overall: 177 (9.02%)
In-hospital: 93 (4.74%)
Post-discharge: 84 (4.28%)
N ¼ 416 (gauze/tape group, Incidence of SSI:
n ¼ 199; polyurethane
group, n ¼ 217) Gauze/tape group: 13 (6.6%)
Polyurethane group: 3 (1.4%)
(P ¼ 0.006)
Costs
Overruns attributable to SSI:
SSI: V33,533.4
No SSI: V18,657.7
Total cost of prolonged LOS
with SSI:
Total cost: $397,828
Per patient: $3,753
Direct healthcare cost of
patients with SSI:
Total cost: $1,084,639
Per patient: $10,232
Total cost of SSI including
indirect costs:
Total cost: $10,353,444
Per patient: $97,433
Total cost of postoperative
management of superficial SSI:
Gauze/tape group: V59,400
Polyurethane group: V22,400
Proxy outcomes
Mean hospital LOS (days):
SSI: 37.4
No SSI: 19.6
J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
Mortality rate among radical
cystectomy patients during
three-year study period:
SSI: 10.2%
No SSI: 4.2%
HR: 2.5 (95% CI: 1.9, 3.2) (P
< 0.0001)
Mean LOS [days (SD)]:
SSI patients: 23.73 (19.89)
SSI post-discharge: 12.99
(4.09)
No SSI: 9.45 (2.51)
Mortality during 4.5-year
study period:
Overall: NR (1.1%)
SSI-attributable: 21 (11.9%)
Hospital LOS, days (SD)
SSI: 9.5 (5.4)
No SSI: 7.4 (3.3) (P ¼ 0.016)
7

Table V
Burden of surgical site infection in the UK
Study, publication type, study
type
Cardiothoracic surgery (N ¼ 1)
Dhadwal et al. [16]
Randomized control trial
General surgery (N ¼ 3)
Dholakia et al. [17]
Prospective cohort study
Pinkney et al. [9]
Randomized control trial
No. of patients
N ¼ 186 (study group, n ¼ 87;
control group, n ¼ 99)a
N ¼ 64
N ¼ 760 (wound edge
protection, n ¼ 382;
standard intraoperative care,
n ¼ 378)
Epidemiology results
(incidence/prevalence)
Incidence of sternal wound
infection at 90 days:
Study group: 8 (9.2%)
Control group: 25 (25.2%)
Overall incidence of SSI: 5
(7.81%)
Incidence of SSI within
30 days of surgery:
Wound edge protection: 91
(24.7%)
Standard intraoperative
care: 93 (25.4%) (P ¼ 0.85)
Costs
Mean cost of antibiotic use,
cost (range):
Study group: $358 (31e12,714)
Control group: $454 (9e21,316)
Mean hospital cost, $1000
(range):
Study group: $14.8 (5.7e126.8)
Control group: $18.6 (5.7e97.3)
Additional hospital cost of SSI
per patient: £243
NR
8
Proxy outcomes
Mean postoperative hospital
LOS [days (range)]:
J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
Study group: 9.1 (4e73)
Control group: 12.0 (4e69)
Infection-related mortality
during one-year study period:
Study group: 0
Control group: 2 (2.0%)
NR
Mean hospital LOS [days (IQR)]:
Wound edge protection: 9 (6
e15)
SSI: 10 (7e20)
No SSI: 8 (6e14)
Standard intraoperative care: 9
(6e14) (P ¼ 0.82):
SSI: 10 (7e22)
No SSI: 9 (6e13)
Number of deaths within 30
days of surgery:
Wound edge protection: 8/382
Standard intraoperative care:
12/378
 Tanner et al. [29]
Surveillance study
Neurosurgery (N ¼ 2)
Atkinson et al. [34]
Caseecontrol study
O’Keeffe et al. [5]
Cost analysis study
Orthopaedic and trauma surgery (N ¼ 6)
Edwards et al. [18]
Prospective cohort study
Hahnel et al. [22]
Prospective cohort study
N ¼ 105 Incidence of SSI within Additional costs of SSI patients:
30 days of surgery: 29
(27.6%) Total: £305,173
Inpatient: £259,835 (85%)
Post discharge: £45,338 (15%)
Mean cost per patients: £10,523
Inpatient: £8,959.80
Post discharge: £1,563
N ¼ 17 NR: 17 patients experienced Direct costs (currency NR):
SSI but total number of patients
was NR
Costs were 2.5-fold higher in
patients with SSI than in unin-
fected patients
N ¼ 236 (245 craniotomy Incidence of SSI: Total additional cost associated
procedures) with craniotomy infections:
Overall, 20 (8.4%)
Cost per infection: £9,283
Overall cost: £185,660
N ¼ 3563 Incidence of SSI: Mean total cost:
Overall, 80 (2.3%) SSI: £25,940
No SSI: £8,979
N ¼ 535 NR NR
Mean LOS: on average 14 days
longer for patients with an SSI,
relative to those without
Readmissions due to SSI: 3
patients
J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
Mean inpatient LOS for patients
with SSI [days (SD)]:
Overall: 32 (15.4)
Mean LOS [days (SD)]:
SSI: 34 (27.9)
No SSI: 9.4 (6.1) (P < 0.001)
Mean LOS:
SSI: 76
No SSI: 22 (P ¼ 0.001)
One-year mortality:
SSI: 26 (32.5%)
No SSI: 1116 (33.5%) (P ¼ 0.954)
Number of emergency
readmissions due to superficial
SSI:
Overall, 2 (2.4%)
(continued on next page)
9
Table V (continued )
Study, publication type, study
type
Kallala et al. [24]
Retrospective cohort study
Pollard et al. [28]
Retrospective cohort study
Vanhegan et al. [30]
Retrospective cohort study
Wijeratna et al. [31]
Case-control study
Multiple or unspecified surgical specialties (N ¼ 4)
Coello et al. [13]
Surveillance study
No. of patients
N ¼ 168
Infected cases, N ¼ 61
Controls, N ¼ 122
N ¼ 286
N ¼ 525(hip hemi-arthroplasty,
n ¼ 415; total hip replacement,
n ¼ 110)
NR: 67,410 surgical procedures
were reported by the 140
participating hospitals
Epidemiology results
(incidence/prevalence)
NR
Incidence of deep wound
infection over 6 years: 61 (2.5%)
NR
Overall incidence of SSI: 17
(3.2%)
Incidence of SSI per 100
operations (95% CI):
Limb amputation: 14.3 (12.3,
16.4)
Small bowel surgery: 10.0 (7.7,
12.8)
Large bowel surgery: 10.0 (9.3,
10.8)
Vascular surgery: 7.7 (6.8, 8.6)
Costs
Mean total costs of revision
surgery [£ (SD)]:
SSI: £30,011 (4,514)
No SSI: £9,655 (599.7) (P <
0.0001)
Median cost of treatment per
patient (IQR)
SSI: £24,410 (15,130e38,670)
No SSI: £7,210 (4290e10,780)
(P < 0.001)
Mean total costs [£ (SD)]:
Deep infection: 21,937 (10,965)
Aseptic loosening: 11,897
(4,629)
Per-prosthetic fracture: 18,185
(9,124)
Dislocation: 10,893 (5,476)
Mean total cost of inpatient
stay
SSI: £15,576
No SSI: £6,922 (P < 0.00005)
Additional cost per SSI:b
Limb amputation: £6,103
Small bowel surgery: £3,836
Large bowel surgery: £2,732
Vascular surgery: £3,545
CABG: £3,894
Open reduction of long bone
fracture: £2,877
10
Proxy outcomes
Mean LOS [days (SD)]:
SSI: 21.49 (3.062%)
No SSI: 9.56 (0.71%) (P <
0.0001)
Median LOS [days (IQR)]
J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
SSI: 80 (43e146)
No SSI: 28 (13e53)
Mortality at 6 months after
initial fracture surgery:
SSI: 23 (37.7%)
No SSI: 32 (26.2%) (P ¼ 0.111)
Mean LOS [days (SD)]:
Deep infection: 16.8 (22.3)
Aseptic loosening: 9.3 (8.6)
Per-prosthetic fracture: 17.1
(17.8)
Dislocation: 9.1 (4.2)
Mean hospital LOS [days]
SSI: 39
No SSI: 16 (P < 0.001)
Additional mean LOS for
patients with SSI [days (95%
CI)]:
Limb amputation: 21.0 (13.2,
31.1)
Small bowel surgery: 13.2 (6.5,
22.4)
Vascular surgery: 12.2 (9.8,
15.0)
 CABG: 4.2 (3.8, 4.6)
Open reduction of long bone
fracture: 4.4 (3.7, 5.3)
Hip prosthesis: 3.1 (2.8, 3.3)
Knee prosthesis: 1.9 (1.7, 2.2)
Abdominal hysterectomy: 2.5
(2.1, 2.9)
Jenks et al. [23] NR: 14,870 surgical episodes Incidence of all SSI:
Cost analysis study were followed
SSI during admission: 162 (1.1%)
SSI on readmission: 120 (0.8%)
SSI post-discharge: 451 (3.2%)
Total SSI over 2 years: 733
(5.1%)
Leaper et al. [26] NR: analysis was per 1000 Estimated incidence of SSI per
Cost analysis study operations 1000 operations:
Postoperative film dressings:
100
Antimicrobial barrier dressing:
65
Hip prosthesis: £3,342
Knee prosthesis: £3,168
Abdominal hysterectomy: £959
Median cost attributable to SSI
(95% CI):
All surgical categories: £5,239
(4,622, 6,719)
2-year costs attributable to SSI
(range):
2-year total cost of SSI:
£2,491,424 [£19,469 (cholecys-
tectomy) to £722,537 (cardiac)]
2-year overall loss for SSI pa-
tients: £1,083,726
Cost per 1000 operations at an
efficacy of 35%:
Postoperative film dressing:
Total cost: £320,600
Cost per procedure: £320.60
Antimicrobial barrier dressing:
Total cost: £239,710
Cost per procedure: £239.70
Large bowel surgery: 9.4 (8.1,
10.8)
CABG: 13.4 (12.4, 14.6)
Long bone fracture open
reduction: 9.9 (6.1, 14.6)
Hip prosthesis: 11.5 (10.3, 12.8)
Knee prosthesis: 10.9 (9.0,
13.0)
Abdominal hysterectomy: 3.3
(2.7, 4.0)
Mortality, range across surgical
categories between October
1997 and June 2001:
J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
SSI: 0.4e13.0
No SSI: 0.2e8.1
LOS in all surgical categories,
days:
Total LOS attributable to SSI
over 2 years: 4694
Median postoperative LOS, days
(95% CI):
Non-SSI: 5 (5, 5)
SSI: 19 (17, 21)
Mortality during 2-year study
period:
SSI: 21 deathsc
Non-SSI: 490 deathsc
Infection-attributable bed-days
per 1000 operations:
Postoperative film dressing:
1100
Antimicrobial barrier dressing:
715
11
(continued on next page)
12 J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15

CABG, coronary artery bypass graft; CI, confidence interval; IQR, interquartile range; LOS, length of stay; NR, not reported; OR, odds ratio; PFF, proximal femoral fracture; SD, standard

The study group received a single dose of gentamicin 2 mg/kg, rifampicin 600 mg and vancomycin 15 mg/kg, with three further doses of 7.5 mg/kg at 12 h intervals. The control group
countries. The incidence of SSI was as high as 36% in one of the
studies reviewed, demonstrating that infections constitute a
persistent complication of surgery [27]. Analysis of the 26
eligible studies confirmed that the financial burden of surgery
Proxy outcomes

is consistently higher in patients who develop an SSI, relative to

uninfected patients [5,9,13e24,26e34]. Indeed, Edwards et al.
NR

reported that in England, the mean total cost of orthopaedic

and trauma surgery in those who developed an SSI was about
2.9 times higher than the costs associated with patients who
did not [18].
Several studies consistently demonstrated that hospitali-
zation was prolonged for patients who developed an
SSI following surgery compared with uninfected patients
Infected patient (ASEPSIS >10):
Mean cost according to ASEPSIS

[5,9,11e14,18e21,23e25,27e29,31,32]. This is exemplified in

Uninfected patients (ASEPSIS

a French study by Cossin et al. who reported that following

cardiothoracic surgery, the mean duration of post-surgery
hospitalization for patients who developed an SSI was 2.3
times higher than that of uninfected patients [14]. Prolonged
Costs

LOS on general wards and in the ICU as a result of contracting

an SSI was reported to constitute a major cost burden in
<10): £3,700

multiple studies [5,11,18,20,21,28e30,32]. The number of

days of hospitalization varied between countries and surgical
£7,718
score:

specialties; however, comparable LOS following the develop-

ment of an SSI after cardiothoracic surgery was reported be-
tween studies, with an average of 15.5 days [14,20,21]. It
should also be noted that the cost per day of hospitalization
differed between studies and countries; for example, whereas
infections (SSI criteria): 382
Overall incidence of wound
(incidence/prevalence)

Penel et al. estimated the cost per day of hospitalization at

Epidemiology results

V1,140 per day, Arroyo et al. estimated it at V350 per day

[12,27]. This variation is likely attributable to the inclusion of
different parameters in the defined daily hospitalization cost
(e.g. overhead, laboratory, diagnosis, healthcare professional
costs).
received cefuroxime 1.5 g at induction and three further doses of 750 mg at 8 h intervals.

In addition to prolonged hospitalization, expenditure was

also attributed to investigation and treatment costs, operative
(9.9%)

costs, and medical staff costs [11,13,20,21,29,32]. Alfonso

et al. reported that whereas LOS accounted for 37% of total
Total number of patients in the SSI and non-SSI groups was not reported.

costs associated with SSIs after multiple surgical specialties,

primary healthcare costs (14%), antibiotic costs (6%), and other
hospital costs (43%) were also incurred. Furthermore, several
studies reported that SSIs were associated with an increased
No. of patients

requirement for reoperation, readmission, and increased mor-

tality rates [11,14,19e21,25,34]. For example, nine out of 20
patients who developed an infection after neurosurgery in the
UK required reoperation, amounting to an overall cost of more
Based on costs derived from Plowman et al. [44].
N ¼ 15,548

than £7,000 [5]. The need for costly reoperations as a result of

infection has subsequently fuelled consideration of cost-
effective non-surgical treatments in high-risk patients [36].
There was considerable heterogeneity between the identi-
fied SSI studies, with a number of data gaps in the economic
deviation; SSI, surgical site infection.

and HRQoL evidence available, and so a quantitative analysis of

the studies (meta-analysis) was not deemed appropriate. This
Study, publication type, study

highlights the ongoing need for well-designed studies that use a

common approach to patient selection, definition of endpoints,
Cost analysis study

and follow-up. First, no economic or HRQoL evidence was

Wilson et al. [32]
Table V (continued )

found for the Netherlands, and, with the exception of the UK,
only a limited number of studies were identified for the other
countries. It is also noteworthy that the generalizability of
economic evidence between countries is unknown due to the
varying healthcare systems, finance structures, and currencies.
type

Additionally, the evidence available according to surgical

c
b
a

specialty was not evenly distributed across the six European

 J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15 13

60
Cardiothoracic surgery

50
Otolaryngology
Additional LOS, days

40
Multiple or unspecified sugical
specialties
30
Urology

20
Neurosurgery

10 Orthopaedic and trauma

surgery

0 General surgery
1 2 3 4 5 6 7 8 9 10111213

France Germany Spain UK

Additional LOS (days)

Figure 2. Additional lenth of hospital stay (LOS) associated with surgical site infection (SSI) versus no SSI. Additional LOS in hospital (days)
reported among patients who developed an SSI, compared with uninfected patients. Numbers along the x-axis denote the study: 1, Cossin
et al. [14]; 2, Penel et al. [27]; 3, Lamarsalle et al. [25]; 4, Graf et al. [20]; 5, Gili-Ortiz et al. [19]; 6, Alfonso et al. [11]; 7, Arroyo et al.
[12]; 8, O’Keefe et al. [5]; 9, Edwards et al. [18]; 10, Kallala et al. [24]; 11, Wijeratna et al. [31]; 12, Tanner et al. [29]; 13, Atkinson et al.
[34]. LOS, length of stay; SSI, surgical site infection.

countries. Very few studies reported the additional costs
associated with SSI following orthopaedic and trauma surgery,
otolaryngology or urology surgery. Furthermore, studies
grouped into the same surgical specialty may not be directly
comparable due to differences in surgical procedures; this is
especially true for studies assigned to ‘multiple or unspecified
surgery’. The presentation of cost and proxy results also varied
between studies, e.g. LOS was not consistently reported,
making comparisons difficult without manipulation of the data.
Furthermore, the definition used to classify SSI differed,
although the criteria defined by the CDC were the most widely
employed [4]. These variables make accurate cost comparisons
between different studies, surgical specialties, and countries
very challenging, and are similar to those reported elsewhere
in the literature [6,11,14,37,38].
It is noteworthy that the majority of studies reviewed here
do not consider the wider impact of SSI to society. For example,
patients who require absence from work constitute an eco-
nomic cost in terms of lost income and reduced work produc-
tivity. A further consideration is that not all infected patients
will be diagnosed before their discharge from hospital; these
patients may not have the same access to treatment, and
infection may consequently cause more distress than for pa-
tients who are diagnosed in hospital [39]. Infections not
detected in hospital may also result in an underreporting of
SSIs, as well as the costs associated with community healthcare
visits [40,41]. It is therefore highly likely that the results of this
review underestimate the true economic burden of SSI in the
six European countries.
In addition to the economic burden, the development of an
SSI and the subsequent prolonged hospitalization will likely
have a negative impact on patient physical and mental health.
Indeed, Pinkney et al. reported that SSIs negatively affect
patients’ health utilities, relative to patients who do not
develop an SSI [9]. However, this was the only eligible study
identified in the current review, highlighting the lack of QoL
studies in the six European countries of interest. A recent
systematic review by Gheorghe et al. reported that reliable
health utility estimates and comparisons are currently hin-
dered by too few studies, small sample sizes, and implicit re-
cords outlining SSI status at the time of assessment [35].
Notably, the review by Gheorghe et al. also emphasized that
there are fewer health utility studies in Europe, with the ma-
jority of SSI model-based economic evaluations being from an
American perspective. It is therefore highly recommended that
more studies be undertaken in Europe to determine whether,
and to what extent, SSIs are associated with QoL decrements.
Increased costs due to SSI may negate the current efforts to
provide efficient and sustainable healthcare; for example,
increased hospitalization as a result of SSI may delay subse-
quent patients’ surgery. It has also been demonstrated that
there is a growing demand for surgical procedures, which will
further exacerbate the problem of SSI and highlights the need
for prompt action [42]. Whereas it has been suggested that one
current system of reimbursement in an English hospital is a
financial disincentive to reduce SSIs, contradictory findings
suggest that if SSI rates are reduced, hospitals should expect
increases in costs (e.g. due to costly intervention programmes)
as well as revenue (e.g. as a result of increased hospital ad-
missions) [23,43]. The ECDC provides a recognized framework
to standardize reporting of SSIs; however, it may not be used by
all European publications and surveillance schemes, leading to
heterogeneous reporting of SSI rates and costs, and subse-
quently weakening any comparisons between European coun-
tries [37]. There is a need for renewed efforts to standardize
procedures and reporting of SSI across European countries,
14 J.M. Badia et al. / Journal of Hospital Infection 96 (2017) 1e15
with particular focus given to preventive strategies to avoid the
associated costs of infection.
In conclusion, this review has demonstrated that SSIs
represent a substantial financial burden in European countries.
Further evidence using robust and common methodologies is
required to make accurate cost estimations, and there is a
clear need for studies that investigate the impact of con-
tracting an SSI on patient QoL. Generalizability of economic
evidence between studies is difficult due to the varying finance
structures, healthcare systems, and currencies. Nonetheless,
the majority of infection-associated costs arise from prolonged
hospitalization, with additional expenditure attributable to
medical staff and treatment. Furthermore, SSIs negatively
impact on patient outcomes, increasing patient morbidity,
mortality, and HRQoL. As the demand for surgical procedures
rises, the incidence and associated costs of SSIs will likely
escalate. Thus, this review highlights the need for renewed
efforts from European countries to improve quality of care and
consequently reduce the financial burden of SSIs.
Acknowledgements
The authors are grateful to C. Hopley and I. Demeyer, both
of whom are employees of Becton Dickinson and provided
insight that greatly assisted the preparation of the manuscript.
The authors also thank P. White, who is an employee of DRG
Abacus and contributed to the writing and editing of the
manuscript.
Conflict of interest statement
J. Badia, A. Casey and N. Petrosillo were paid consultants to
Becton Dickinson & Co. in connection with the development
of the manuscript. P. Hudson and S. Mitchell are both em-
ployees of DRG Abacus, the medical communication com-
pany that conducted the systematic review and provided
writing services. Work by DRG Abacus was funded by Becton
Dickinson & Co.; C. Crosby is an employee of Becton Dick-
inson & Co.
Funding source
This work was funded by Becton Dickinson & Co.
Appendix A. Supplementary data
Supplementary data related to this article can be found at
http://dx.doi.org/10.1016/j.jhin.2017.03.004.
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