SURGICAL INFECTIONS

Volume 18 Number 4, 2017

ª Mary Ann Liebert, Inc.
DOI: 10.1089/sur.2017.058

Patients at High-Risk for Surgical Site Infection

Krislynn M. Mueck and Lillian S. Kao

Abstract

Background: Surgical site infections (SSIs) are a significant healthcare quality issue, resulting in increased
morbidity, disability, length of stay, resource utilization, and costs. Identification of high-risk patients may
improve pre-operative counseling, inform resource utilization, and allow modifications in peri-operative
management to optimize outcomes.
Methods: Review of the pertinent English-language literature.
Results: High-risk surgical patients may be identified on the basis of individual risk factors or combinations of
factors. In particular, statistical models and risk calculators may be useful in predicting infectious risks, both in
general and for SSIs. These models differ in the number of variables; inclusion of pre-operative, intra-operative,
or post-operative variables; ease of calculation; and specificity for particular procedures. Furthermore, the
models differ in their accuracy in stratifying risk. Biomarkers may be a promising way to identify patients at
high risk of infectious complications.
Conclusions: Although multiple strategies exist for identifying surgical patients at high risk for SSIs, no one
strategy is superior for all patients. Further efforts are necessary to determine if risk stratification in combination
with risk modification can reduce SSIs in these patient populations.

Keywords: high risk patients; prevention; risk stratification; surgical site infection

S urgical site infections (SSIs) are a significant health-

care problem in the United States and globally [1]. Such
infections are associated with increased morbidity, mortality,
hospital length of stay, resource utilization, and costs [2–5]. A
2012 analysis using American College of Surgeons (ACS)
National Surgical Quality Improvement Project (NSQIP) data
found that SSIs were the most common reason for unplanned
readmissions [4]. A 2013 meta-analysis noted that SSIs con-
tribute the most to overall costs (33.7% of $9.8 billion per year,
or $3.6 billion annually) for common healthcare-acquired in-
fections [5]. The estimated cost of each SSI was estimated to be
$20,785 [5]. Furthermore, a population-based study in Europe
reported that the attributable burden of an SSI is 11.6 disability-
adjusted life years per 100,000 population [6]. Thus, SSIs have
a significant impact on healthcare costs and patient outcomes,
both short- and long-term.
Multiple evidence-based interventions exist for the prevention
of SSIs [7, 8]. Although a systematic review of healthcare-
associated infection-prevention programs in general showed a
favorable cost-benefit ratio [9], the number and quality of eco-
nomic evaluations of specific interventions (surgical hand and
skin antisepsis and wound dressings) to prevent SSIs are poor
[10]. Furthermore, compliance with multi-faceted prevention
programs or prevention bundles can be difficult [11, 12]. Thus, it
may be more practical to reserve more expensive, complex, or
resource-intensive interventions for patients at high risk of SSI.
In addition to optimizing resource utilization, other
benefits of accurate risk stratification include better pre-
operative counseling regarding expectations and risks,
peri-operative risk modification in order to reduce SSIs, and
increased post-operative surveillance to detect and treat
SSIs early. Multiple methods have been used for stratifying
patients’ SSI risk. One method is to target patients having a
specific risk factor. Another is to utilize risk calculators or
scoring systems in order to predict the risk of SSI and other
complications. A third method is to utilize biomarkers
predictive of clinical outcomes such as SSIs. This paper
reviews the evidence for and implications of using each of
these methods to identify patients at high risk of SSIs.
Specific Risk Factors
Factors at the patient, operative, and institutional levels
can affect a patient’s risk of SSI (Table 1) [13]. All should
be considered in determining a patient’s overall risk and
for devising strategies to mitigate that risk. Because this
review is about the high-risk patient, only patient-level
factors will be discussed. Furthermore, the focus is on
whether these factors predict risk accurately and if so, how
that risk can be reduced. Lastly, this is not intended to be a
comprehensive review, so not all risk factors will be dis-
cussed in detail.

1
2 MUECK AND KAO

Table 1. Examples of Risk Factors for Surgical Site Frailty is defined as increased vulnerability to everyday or
Infection on the Basis of Patient, Operative, acute stressors resulting from a decline in physiologic reserve
and Institutional-Level Factors and function across multiple organ systems [15]. The ACS
NSQIP and the American Geriatrics Society have devised
Patient-level factors
recommendations for optimal pre-operative assessment of
Characteristics geriatric patients [16]. They recommend that all geriatric
Sex patients have a baseline frailty assessment, given that it is a
Age risk factor for poor surgical outcomes [17]. Multiple scoring
Frailty systems for frailty have been developed, and several have
Patient dependence been correlated with SSIs and other complications after
Socioeconomic factors surgery [18–20]. Interventions that have been employed to
Lifestyle prevent or reduce frailty have included physical activity,
Smoking status nutrition, home modifications, comprehensive geriatric as-
Alcohol abuse sessment, or a combination of these [21]. However, not all of
Co-morbidities these methods are effective [21], nor is it known what the
Diabetes mellitus optimal methods are for implementing these interventions
Chronic obstructive pulmonary disease (i.e., for increasing physical activity) [22]. For example,
Congestive heart failure current systematic reviews of the effect of pre-habilitation,
Acute myocardial infarction
which can include pre-operative physical or nutritional
Renal insufficiency
Hypertension therapy or both, on surgical outcomes describe a paucity of
Osteoporosis high-quality studies, as well as inconclusive results [23,24].
Multiple co-morbidities Moreover, most of the trials have focused on overall com-
(i.e., Charlson Co-Morbidity Score) plications, length of stay, and mortality rate rather than on
Medications specific complications such as SSI. Further research is re-
Immunosuppression quired to determine whether short-term interventions that
Prior environment ameliorate frailty can reduce surgical complications, in-
Pre-operative length of stay cluding SSIs.
Admission from a long-term healthcare facility
Risk calculators or scoring systems Lifestyle characteristics
National Nosocomial Infections Surveillance Smoking and alcohol abuse have both been reported to be
American Society of Anesthesiologists (ASA) risk factors for SSIs [13]. Smoking in particular has been
Operative-level factors found to be a risk factor for both impaired wound healing and
SSIs for many procedures [8,13,25–28]. Smoking is included
Procedure characteristics in risk prediction models such as the Surgical Site Infection
Incision class Risk Score (SSIRS) [29]. A systematic review of studies
Type of surgery evaluating the pathophysiology of smoking suggests three
Elective versus emergency procedure mechanisms by which this practice impairs wound healing
Case complexity and increases infections: Reduction of tissue oxygenation and
Duration of operation perfusion, impairment of the inflammatory response and
Blood loss/blood transfusions
Medical device implantation bactericidal mechanisms, and decrease in site cell prolifera-
tion and remodeling [30]. A meta-analysis of almost 500,000
Institutional-level factors patients suggested that smoking increases the odds of SSI
by 79% (odds ratio [OR] 1.79; 95% confidence interval
Current environment [CI] 1.57–2.07) [31]. Furthermore, based on four randomized
Safety culture controlled trials, cessation of smoking is associated with a
Hospital characteristics 57% relative risk reduction in SSIs (OR 0.43; 95% CI 0.21–
Size 0.85) [31]. The optimal timing of pre-operative smoking
Experience cessation and its impact on both incision healing and other
Physician problems, such as respiratory complications, is controversial
Hospital [32, 33]. However, the ACS and Surgical Infection Society
(SIS) 2016 guidelines recommend smoking cessation four to
six wks prior to surgery as a way to prevent SSIs [8].
Patient characteristics
Patient co-morbidities
Multiple studies have identified patient characteristics
such as age and sex as risk factors for SSI [13,14]. Although Multiple patient co-morbidities have been associated with
acknowledgement of these risk factors may improve pre- SSIs (Table 1). In a scoping review of risk factors, diabetes
operative counseling and peri-operative management, many mellitus was the co-morbidity most frequently studied in
of these factors are not modifiable. Therefore, more recently, association with SSIs [13]. Poor glycemic control, both long
there has been greater emphasis on potentially modifiable and short term, has been linked to SSIs, and multiple studies
patient characteristics such as frailty, which can be associated have demonstrated an association between peri-operative
with age and disability but that is not a surrogate for either. hyperglycemia, regardless of diabetes mellitus status, and
PATIENTS AT HIGH RISK FOR SSI 3

SSIs [34]. Furthermore, data from a multi-center quality-
improvement initiative suggest that better glycemic control
reduces SSIs [35]. However, whether tight glycemic control,
traditionally defined as a serum glucose concentration below
110 mg/dL, is a feasible, effective, and safe method for re-
ducing SSIs is still controversial [34,36]. The ACS/SIS guide-
lines recommend a target of 110–150 mg/dL or <180 mg/dL in
patients undergoing cardiac surgery [8]. With regard to long-
term glycemic control prior to surgery, the data are conflicting.
Although multiple retrospective studies have demonstrated an
association between an elevated hemoglobin A1c (HbA1c) and
SSIs [37–39], other investigators have reported no correlation
[40]. Furthermore, a systematic review suggested that an ele-
vated HbA1c was not definitely associated with SSIs.(41) Other
studies that have examined hemoglobin A1c and hyperglycemia
together suggest that both are associated with SSIs [42–44].
However, high-quality, randomized trial data on whether tar-
geting a specific HbA1c value pre-operatively reduces SSIs are
lacking. The ACS/SIS guidelines recommend that ‘‘optimal’’
blood glucose control be obtained pre-operatively but ac-
knowledge the evidence gap [8].
Multiple co-morbidities clearly increase the risk of SSIs
[13]. Therefore, another approach to identifying the high-risk
patient is to use prediction models or risk calculators that
incorporate multiple co-morbidities and other characteristics.
Models for Predicting SSI Risk
Multiple scores and models have been developed to predict
the outcomes of surgery (Table 2), and choosing the right
model can be challenging [45,46]. The ideal model should be
accurate, objective, and easy to use. Although no model is
perfect, these tools can be useful in risk-stratifying surgical
patients in order to determine whether pre-operative modi-
fication of risk factors or changes in surgical approach should
be considered. The available models differ in several re-
spects. First, some models are specific to SSIs or infectious
complications, whereas others predict all complications or
death. Some models can be applied broadly across multiple
types of surgical procedures, whereas others are procedure
specific. Some models utilize only pre-operative variables,
whereas others incorporate pre-operative and intra-operative
factors. Lastly, models differ in the number of variables in-
cluded. Several popular models for predicting SSI risk are
discussed below. However, a comprehensive description of
all published models is beyond the scope of this paper.
Incision class
The Association of periOperative Registered Nurses
(AORN) incision classification system is used frequently to
stratify patients on the basis of SSI risk [47]. There are four
classes: Clean (I), clean-contaminated (II), contaminated
(III), and dirty (IV). The risk of SSI increases with the extent
of site contamination. However, recent analyses of multi-
institutional datasets suggest that the absolute risk of infec-
tion with each incision class may be less than previously
estimated [48,49]. Furthermore, results differ regarding
whether incision class predicts overall SSI risk accurately
[50,51]. The lack of association between incision class and
SSI may be attributable in part to misclassification. Several
studies in pediatric surgery have demonstrated inaccuracies
in the documentation of incision class, even after multi-
faceted educational interventions [48,52–55]. Nonetheless,
site classification continues to be used in many models pre-
dicting SSIs and other post-operative outcomes.

Table 2. Scoring Systems

Inclusion
No. of of intra-operative
System Year variables variables Outcomes predicted
Pre-operative
American Society of Anesthesiologists (ASA) 1941 Unlimited No None
Charlson Comorbidity Index 1987 19 No Death
Surgical Risk Scale(76) 2002 3 No Death
Surgical Outcome Risk Tool (SORT)(77) 2014 6 No Death
Post-operative
Portsmouth Physiological and Operative Severity 1998 18 6 Morbidity and death
Score for the enumeration of Mortality and morbidity
(P-POSSUM)(78)
American College of Surgeons National Surgical 1997 72 15 Morbidity and death
Quality Improvement Project (ACS NSQIP)(60)
Surgical Apgar Score (SAS)(79) 2007 3 3 Morbidity and death
National Nosocomial Infection Surveillance 1991 3 Yes SSI
(NNIS)(56)
Contamination, Obesity, Laparotomy, 2012 4 Yes Colorectal SSI
and ASA (COLA)(80)
Preventie Ziekenhuisinfecties door Surveillance 2006 4 Noa SSI
(PREZIES)(81)
Ventral Hernia Risk Score(58) 2013 5 Yes Ventral hernia SSI
a
Includes discharge diagnosis.
Multiple scoring systems exist to predict death, morbidity, and infectious complications such as SSIs. They differ in terms of variables
included, specificity to procedures, and accuracy.
Modified from Sobol and Wunsch [45].
4 MUECK AND KAO
National Nosocomial Infections Surveillance (NNIS)
The National Nosocomial Infections Surveillance (NNIS)
system builds on incision classification. Using this system,
the American Society of Anesthesiologists (ASA) physical
status classification, and the duration of the operative pro-
cedure beyond the 75th percentile, the NNIS system stratifies
patients into three classes of risk for SSI [56]. However, the
predictive ability of NNIS is poor, with one study reporting
only 57% accuracy for SSIs prediction after colorectal re-
sections [57]. In another study, NNIs had 64% accuracy in
predicting SSIs after open ventral hernia repair [58]. Lastly,
in a study of valvular and coronary artery bypass grafting
surgery, NNIS had accuracies of 62% and 60%, respectively,
for predicting SSIs [59].
American College of Surgeons National Surgical
Quality Improvement Project (ACS NSQIP)
The ACS NSQIP database provides risk- and reliability-
adjusted data that allow hospitals and surgeons to compare
their outcomes, including SSIs. They also have a risk cal-
culator that utilizes multiple variables to calculate patients’
morbidity and likelihood of death after surgery [60]. This
calculator is not specific for types of surgery or complica-
tions. Several studies have suggested that the risk calculator
is inaccurate for predicting SSIs [49,61,62]. A study by the
Ventral Hernia Outcomes Collaborative compared multiple
risk calculators, including the ACS NSQIP tool, for their
ability to stratify patients for SSIs after open ventral hernia
repair [49]. The investigators found that the ACS NSQIP risk
calculator had modest ability to predict SSIs (73% accuracy).
The accuracy of any of the calculators ranged from 55% to
81%. Despite the limitations of the risk calculator, ACS
NSQIP can be used to identify risk factors for SSI in specific
procedures or subspecialties [63–66].
Other models
Many other models for predicting SSIs build on the inci-
sion classification and NNIS systems (Table 2).
Accuracy. The utility of predictive models, scoring sys-
tems, and risk calculators depends on their accuracy. As al-
ready noted, the accuracy of different models for predicting
SSI after open ventral hernia repair is only modest [49]. This
finding was replicated in a study comparing models for pre-
dicting SSI after colorectal surgery. Bergquist et al. com-
pared the performance of four models in predicting SSIs in
2,300 colorectal surgery patients from a single institution:
NNIS; Contamination, Obesity, Laparotomy, and ASA score
(COLA); Preventie Ziekenhuisinfecties door Surveillance
(PREZIES); and NSQIP [57]. The authors found that the c-
statistic for all four models ranged from 0.57 to 0.61. The c-
statistic is equivalent to the area under the receiver operating
characteristic (ROC) curve and represents the predictive ac-
curacy of a model; a c-statistic of 0.50 indicates that the
model is no more accurate than flipping a coin. A systematic
review of 16 risk scores for predicting SSIs or peri-prosthetic
joint infections after joint arthroplasty found that only three
scores had a discriminative ability greater than 0.70 [67].
These studies demonstrate the limited accuracy of the
available models for predicting SSIs.
Biomarkers. Biomarkers are ‘‘objective, quantifiable char-
acteristics of biological processes’’ that can correlate with pa-
tients’ clinical outcomes [68]. Both pre-operative and post-
operative markers have been evaluated for their correlation with
the development of SSI or other infectious complications [69–
75]. However, if the intent is to modify treatment to prevent
SSIs, pre-operative biomarkers would be more useful.
The pre-operative biomarkers most commonly studied in-
clude measures of nutritional status such as serum pre-albumin
or albumin concentrations and pre-operative systemic inflam-
mation markers such as C-reactive protein (CRP). Multiple
studies of spine surgery patients have identified a low pre-
albumin concentration as a predictor of SSI [73–75]. Whereas
the ACS/SIS guidelines do not mention pre-operative nutri-
tional support to prevent SSIs, the World Health Organization
states that oral or enteral multiple nutrient-enhanced formulas
should be considered in underweight patients undergoing major
surgical procedures [7]. The WHO performed their own meta-
analyses and determined that multiple nutrient-enhanced nu-
tritional formulas resulted in a 47% reduction in the odds of an
SSI (OR 0.53; 95% CI 0.30–0.91) compared with standard
formula in randomized controlled trials [7]. However, the
quality of the evidence was rated very low. Single nutrient-
enhanced formulas did not have any effect on SSIs [7]. Fur-
thermore, it is not clear whether nutritional support yielding a
specified pre-albumin target or a change in the pre-albumin
concentration reduces SSIs.
Pre-operative inflammation, represented by elevated
CRP and hypoalbuminemia, has been associated with more
post-operative infections in patients undergoing gastrointes-
tinal surgery [69–71]. In a multi-center study of patients
having elective gastrointestinal cancer surgery, the Glasgow
Prognostic Score (GPS), which is a measure of systemic in-
flammation based on albumin and CRP, was associated with
post-operative infection [70]. However, the GPS was not
correlated with SSI specifically by univariate or multivariate
analyses. In another multi-center prospective study of patients
undergoing elective colorectal surgery, the areas under the
ROC curves for pre-operative albumin and CRP concentra-
tions were 0.62 and 0.57, respectively, for any infectious
complication [69]. Further studies are necessary to determine
if pre-operative systemic inflammation can be modified as a
risk factor.
Pre-operative biomarkers are promising as adjuncts to
other clinical tools for risk stratifying surgical patients. Risk
scores utilizing only biomarkers, such as the GPS, are not
specific for SSIs. Prospective trials are necessary to deter-
mine if modification of these pre-operative risk factors can
reduce SSIs.
Implications
Although multiple studies have evaluated the prognostic
accuracy of models and biomarkers to predict SSIs, many
conclusions are based on a specific cohort of patients or on a
single-center study. Only a few models have been validated
externally [67]. Variations in defining risk factors and dif-
ferent risk-adjustment strategies can cause significant dis-
cordance between prediction methods. Misclassification and
measurement errors can lead to inaccurate risk prediction
even if the model is robust. Furthermore, unanswered ques-
tions remain regarding: (1) Whether changes in care based on
PATIENTS AT HIGH RISK FOR SSI
risk stratification can reduce SSIs; (2) at what risk thresh-
old(s) interventions should be implemented; and (3) at what
risk threshold(s) it is cost-effective to recommend additional
interventions to mitigate SSI risk.
Conclusions
Prevention of SSIs is a complex problem that requires a
multi-faceted approach. Identification of high-risk patients
and of other complications may result in interventions for
pre-operative risk modification, change in operative strategy,
triage of patients to a higher level of care post-operatively, or
utilization of more resources for prevention and surveillance.
However, no single approach for stratifying risk is accurate
uniformly in all patients and for all procedures, and all
methods of risk stratification have advantages and disad-
vantages. Furthermore, it is unknown at which threshold
changes in management should occur to obtain effectiveness
and cost-effectiveness.
Author Disclosure Statement
Neither of the authors has any competing financial interests.
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Address correspondence to:
Dr. Krislynn M. Mueck
Department of Surgery
Center for Surgical Trials and
Evidence-Based Practice (C-STEP)
John P. and Katherine G. McGovern Medical School
at the University of Texas Health Science Center
6431 Fannin
Houston, TX 77030
E-mail: Krislynn.M.Mueck@uth.tmc.edu