Epidemiology and outcomes associated with surgical site infection following
Teena Chopra MD, MPH*, Dror Marchaim MD, Ylinne Lynch BS, Chris Kosmidis MD,
Jing J. Zhao PharmD, Sorabh Dhar MD, Naasha Gheyara MD, Deborah Turner BS, Don Gulish,
Michael Wood MD, FACS, George Alangaden MD, Keith S. Kaye MD, MPH
Detroit Medical Center and Wayne State University, Detroit, Michigan
Roux-en-Y gastric bypass surgery
Risk adjusted score
Background: Surgical site infection (SSI) is a frequent problem complicating bariatric surgery. However,
the potential risk factors, risk stratification, and outcomes of SSIs in this patient population remain poorly
defined. The aim of this prospective case-control study was to characterize better the risk factors and to
improve risk stratification for SSIs following bariatric surgery.
Methods: Patients studied had SSI following Roux-en-Y gastric bypass surgery (RYGBS) between
November 2006 and March 2009 at Harper University Hospital and were each matched with 3 controls
based on type of operative procedure, surgeon, and year of surgery. Thirty-day outcomes included
mortality, hospital readmissions, outpatient procedures, and emergency room visits. A scoring system
(BULCS score) was compared with the National Nosocomial Infections Surveillance system risk index
using logistic regression.
Results: In multivariate analysis, duration of surgery (odds ratio [OR], 3.3; 95% confidence interval [CI]:
1.62-6.74), diagnosis of bipolar disorder (OR, 3.341; 95% CI: 1.0-12.27), use of prophylactic antibiotics
other than cefazolin (OR, 4.2; 95% CI: 1.47-11.69), and sleep apnea (OR, 1.8; 95% CI: 1.05-2.97) were
significantly associated with SSI. Patients with SSI were more likely to have return emergency visits (OR,
4.96; 95% CI: 2.9-8.48), readmission (OR, 6.53; 95% CI: 3.44-12.42), and outpatient procedures following
surgery (OR, 4.75; 95% CI: 1.32-17.14) than were controls without SSI. The BULCS score was a stronger
predictor of SSI than the National Nosocomial Infections Surveillance system (C-statistic, ?0.62 vs 0.55,
Conclusion: SSI following bariatric surgery was associated with receipt of antibiotic prophylaxis other
than cefazolin and comorbid conditions including sleep apnea and bipolar disorder. The BULCS score
performed favorably as a predictor and risk adjuster for SSI following bariatric surgery. SSI was associated
with increased health care resource utilization.
Copyright ? 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc.
Published by Elsevier Inc. All rights reserved.
The global epidemic of obesity has become a major public health
problem. According to the latest National Health and Nutrition
Examination Survey, over 30% of adults in the United States are
obese (body mass index [BMI] > 30 [kg/m2]), and over 60% are
either overweight (BMI, 25-30) or obese.1It has been estimated
that, by the year 2030, the prevalence of individuals who are
overweight or obese in the United States will be greater than 80% in
adults and greater than 30% in adolescents.2Obesity has been
linked to many chronic problems, including hypertension, diabetes
mellitus type 2, coronary artery disease, sleep apnea, and osteoar-
thritis.3If the rise in obesity continues as predicted, by 2030,
approximately 1 in 6 health care dollars spent, or approximately
900 billion dollars annually, would be directly attributable to
problems associated with obesity and overweight.2
Medical management of obesity has been effective only in
certain instances. Bariatric surgery, a type of “weight loss” surgery,
has been a revolutionary breakthrough in the management of
obesity. A 2009 Cochrane Review reported that, in obese patients,
surgical approaches were more effective weight loss interventions
compared with nonsurgical approaches.4Patients who are eligible
* Address correspondence to Teena Chopra, MD, Assistant Professor of Medicine,
Division of Infectious Diseases, University Health Center, 4201 St Antoine Street,
Suite 2B, Detroit, MI 48201.
E-mail address: email@example.com (T. Chopra).
Conflicts of interest: None to report.
Contents lists available at ScienceDirect
American Journal of Infection Control
journal homepage: www.ajicjournal.org
American Journal of
0196-6553/$36.00 - Copyright ? 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
American Journal of Infection Control 40 (2012) 815-9
for bariatric surgery include those with a BMI greater than 40 as
well as thosewith a BMI between 35 and 40 with existing comorbid
conditions such as sleep apnea, severe diabetes mellitus, or other
obesity-related illnesses that pose a serous risk of cardiopulmonary
disease. Bariatric surgery has been shown to decrease overall
mortality,5increase quality of life,6and diminish or eliminate some
comorbid conditions associated with obesity, such as diabetes,
osteoarthritis, and sleep apnea.7
There are several types of bariatric surgery performed in the
United States. One of the most common types of bariatric surgery is
the Roux-en-Y gastric bypass (RYGBS). In this procedure, a section
of the stomach and small intestine are bypassed to create weight
loss secondary to malabsorption. This surgery can be performed
using an open or laparoscopic approach. As with any surgical
procedure, surgical site infection (SSI) is a potentially devastating
problem. The severity of SSI can range froma relatively mild surface
incisional infection to a severe infection, such as intra-abdominal
abscess involving the deep organ space. SSI is associated with
late-onset complications, including incisional hernias.8Although
bariatric surgery itself has not been shown to carry a rate of
infection above that for obese patients undergoing some types of
nonbariatric surgery,9obese patients have an increased incidence
of SSIs compared with nonobese patients for many types of
procedures. There are scant data pertaining to risk factors for SSI
followingbariatric surgery, and published literature consists onlyof
small single-center studies.8In addition, there exists a need for risk
adjustment metrics for SSI following bariatric surgery to facilitate
meaningful comparison of SSI rates among centers and surgeons.
The National Nosocomial Infections Surveillance (NNIS) system risk
index is currently used for risk adjustment but has not been
analyzed specifically for SSI following bariatric surgery. This study
analyzed the epidemiology of and outcomes associated with SSI
following bariatric surgery in a large patient cohort. The results
were used to develop a model for scoring SSI risk in bariatric
MATERIALS AND METHODS
Study design and setting
A case-control study was performed at Harper University
Hospital, which is a 500-bed, tertiary care referral hospital in
Detroit, MI. Approximately 900 bariatric surgeries are performed
annually, including w 300 RYGBs, of which the majority are lapa-
roscopic. The average number of open RYGBs per year during the
study period was 50, and no open procedures were performed in
the last year of the study period. The study was approved by the
Wayne State University Human Investigation Committee.
Study definitions and data collection
Study patients were patients who underwent either “open” or
laparoscopic RYGBS at Harper University Hospital between
November 2006 and March 2009. Cases were patients who devel-
oped a SSI following RYGB surgery during the study period. All
cases of SSI were identified prospectively by infection control
preventionists. SSIs were classified as superficial incisional SSI,
deep incisional SSI, or organ/space SSI based on the Centers for
Disease Control and Prevention definitions.10
patients who underwent bariatric surgery during the study period
but who did not develop SSI. Controls were matched to cases in
a 3:1 ratio. Matching criteria included (1) type of procedure, (2)
year that the procedure was performed, and (3) surgeon. We did
not match based on age, gender, or BMI because we wanted to
study those factors as potential risk factors for SSIs. All matching
requirements for each case were met without a problem.
Clinical information for study subjects was obtained from the
database maintained by the Michigan Bariatric Surgery Collabora-
tive.11These data were collected prospectively and included
comorbid conditions; functional status; perioperative information
such as duration of surgery, prophylactic antibiotics used, and
American Society of Anesthesiologists (ASA) score, laboratory
values, and outcomes at 30 days. Thirty-day outcomes included
additional outpatient procedures related to the bariatric surgery,
emergency department visits, readmission to the hospital, and
mortality. A scoring system, called the BULCS score, was constructed
to predict SSI following RYGBS based on the multivariate model.
(The BULCS score ranged from 0-12 and consisted of four variables:
Bipolar illness prior to surgery [4 points], presence of pre-operative
Urinary incontinence [2 points], Long surgical duration [>180
minutes] [4 points], use of an antibiotic other than Cefazolin as
prophylaxis [5 points], and history of Sleep apnea [2 points].) The
BULCS score was derived from a multivariate model that predicted
SSI. Point values were assigned according the odds ratio (OR) for
each variable in the final multivariate model. The final BULCS score
was broken in tertiles and compared with the NNIS risk index score.
The NNIS risk index score was also calculated for each patient to
gauge their SSI risk.12One point was assigned for each of the
following: (1) wounds classified as contaminated, (2) ASA physical
classification ?3, and (3) surgery duration > 180 minutes.
All analyses were performed by using the SAS software (version
9.2; SAS Institute, Cary, NC). The t test and Wilcoxon rank-sum test
were used to analyze continuous variables, and conditional logistic
regressionanalysiswasusedfor matched bivariateandmultivariate
analyses, respectively. For the multivariate model building, vari-
ables with a P value of <.10 in the bivariate analyses were included
as candidate variables. Conditional logistic regression with back-
wards selection was used to select for variables in the final model.
Final models included variables with an adjusted P value <.05. All
candidate variables were checked for confounding. Confounders
variables by >10% when added back to the model. Confounding
variables were incorporated into the final model. All P values were
Characteristics of the study subjects
n ¼ 91
50.4 (44-58) 49.2 (44-54)
46.1 ? 11.5 45.8 ? 10.5
n ¼ 273
Female sex, n (%)
Age (mean ? SD), yr
Type 2 DM, n (%)
CPAP, n (%)
Sleep apnea, n (%)
Cefoxitin, n (%)
Clindamycin, n (%)
Cefazolin, n (%)
Ciprofloxacin 400 mg, n (%)
Vancomycin 1 g, n (%)
BULCS score (median,
DM, diabetes mellitus.
T. Chopra et al. / American Journal of Infection Control 40 (2012) 815-9
2-sided. Conditional logistic regression was used to analyze the
association between risk scores and SSI following RYGB. The
predictive ability of each score was gauged using the C-statistic.
A total of 751 RYGBS was performed during the study period.
Ninety-four percent (n ¼ 701) were laparoscopic procedures, and
6.1% (n ¼ 46) were open procedures. Ninety-one case patients with
SSI were identified (SSI rate,12%). Sixty-five (71.4%) of the SSIs were
superficial incisional, 18 (19.8%) were deep incisional, and 8 (9.9%)
were organ/space. The infections occurred at a mean of 10.7 ? 6.62
days after surgery. Two hundred seventy-three matched controls
As displayed in Table 1, both the cases and controls were
predominantly female. The cases weremore likely to have a slightly
higher BMI as compared with the controls. Cases were significantly
more likely to have had longer surgery (median, 200.5 minutes;
interquartile range, 123-256 minutes) than the matched controls
(median, 152.5 minutes; interquartile range, 100-225; P ¼ .002),
and 50.6% of the cases (n ¼ 46) were in surgery for over 180
minutes, whereas only 36.6% of the controls (n ¼ 100) had a surgery
lasting longer than 180 minutes (P ¼.001). Both cases and controls
had a median ASA score of 3.
Of the comorbid conditions reported in Table 1, 41.8% of the
cases had type 2 diabetes mellitus (n ¼ 38), compared with 28.6%
(n ¼ 78) of controls (P ¼ .02, OR, 1.8; 95% confidence interval [CI]:
1.09-2.96). Compared with controls, cases were significantly more
likely to report a history of sleep apnea (46% vs 63%, respectively;
P ¼ .006; OR, 1.92; 95% CI: 1.19-3.1) as well as use of continuous
positive airway pressure (CPAP) during sleep at the time of surgery
(30% vs 48.4%, respectively; P ¼ .001; OR, 2.11; 95% CI: 1.31-3.4).
Compared with controls, cases also reported significantly higher
rates of bipolar disorder (2.2% vs 6.6%, respectively; P ¼.03; OR, 3.4;
95% CI: 1.01-11.47).
The species most commonly cultured from the wound were
Streptococcus spp (n ¼ 27), Enterococcus spp (9), coagulase-negative
staphylococci (9), Enterobacteriaceae (5), Staphylococcus aureus (5),
and Eikenella (3). In 25 cases, anaerobic cultures weresent, of which
15 cultures grew anaerobes. They were Prevotella (n ¼ 10), Pep-
tostreptococcus (5, including 1 case of bacteremia), Bacteroides (1),
and Veillonella (1).
Surgical antimicrobial prophylaxis was analyzed (Table 1).
Cefoxitin was the most common perioperative agent used in 60
case patients (65.9%) and 180 (65.9%) control patients. The most
common dose of cefoxitin was 2 g parenterally. Clindamycin was
the second most commonly used agent (usuallygiven at a dose of at
900 mg parenterally) and used significantly more frequently in
cases (n ¼ 23, 25.3%) than controls (n ¼ 42,15.4%, P ¼.02). Cefazolin
(at 2 g intravenous piggyback) was used in significantly fewer cases
(n ¼ 8, 8.8%) than controls (n ¼ 49, 17.9%, P ¼ .007).
In multivariate analysis (Table 2), the following independent
predictors of SSI were identified: sleep apnea (OR,1.8; 95% CI: 1.05-
2.97), bipolar disorder (OR, 3.4; 95% CI: 1.0-12.27), duration of
surgery longer than 180 minutes (OR, 3.3; 95% CI: 1.62-6.74), and
preoperative urinary incontinence (OR,1.5; 95% CI: 0.74-3.04). This
model was controlled for the confounding effects of urinary
Based on this model, the BULCS score was derived. As previously
mentioned, the variables used in the BULCS score and their
assigned point value were as follows: Bipolar illness prior to
surgery (4 points), presence of preoperative Urinary incontinence
(2 points), Long surgical duration (>180 minutes) (4 points), use of
an antibiotic other than Cefazolin as prophylaxis (5 points), and
history of Sleep apnea (2 points). The median BULCS score of cases
was 9 (interquartile range,7-11) and of controls was 7 (interquartile
range, 5-9; P < .001). The BULCS score was divided into the
following tertiles: first tertile, BULCS 0-4; second tertile, BULCS 5-8;
third tertile, BULCS ?9. An increase in tertile ranking was correlated
with an increase in the rate of SSI (BULCS tertile 1 ¼8.3% SSI, BULCS
tertile 2 ¼ 21% SSI; P value ¼ .04; and BULCS tertile 3 ¼ 36% SSI; P
value ¼ .0009) (Fig 1). In analysis of the NNIS risk index and SSI risk,
SSI rate increase correlated with higher NNIS score (NNIS score
0 ¼ 22% SSI, NNIS score 1 ¼ 23% SSI; P value ¼ .9; and NNIS score
2 ¼ 32%; P value ¼ .08).
The associations between SSI risk and BULCS score and NNIS risk
index were compared. One model was constructed using the BULCS
tertiles score. With each increase in tertile, the risk for SSI increased
in a stepwise fashion. Using lowest tertile as reference, the second
BULCS tertile score was associated with an OR of 4.8 for develop-
ment of SSI (95% CI: 1.0-23.6), and the third tertile score was
associated with an ORof 16.2 (95% CI: 3.1-82.8). When the NNIS risk
index was analyzed, there was no statistically significant increase in
Thirty-day postoperative outcome
(n ¼ 91), n (%)
(n ¼ 273), n (%)
ED, emergency department.
Independent predictors of SSI following bariatric surgery
ParameterOR (95% CI)
Use of preoperative antibiotic other than cefazolin
Surgery duration > 180 min
NOTE. The multivariate model was controlled for urinary incontinence, OR 1.5 (95%
Fig 1. Figure shows the risk of SSI associated in this study with each tertile of the
BULCS and NNIS scores. The lowest tertile was used as reference in each scoring
system. The second and third BULCS tertile scores were associated with a statistically
significant increase in SSI (tertile 2: odds ratio [OR], 4.8; 95% confidence interval [CI]:
1.0-23.6; tertlie 3: OR, 16.2; 95% CI: 3.1-82.8). NNIS risk index showed no statistically
significant increase in SSI risk as the NNIS risk score increased (tertile 2: OR, 1; 95% CI:
0.7-1.4 for SSI; tertile 3: OR, 1.2; 95% CI: 0.9-1.5). The C-statistic for the BULCS score
(0.62) was greater than the C-statistic for the NNIS risk index (0.55).
T. Chopra et al. / American Journal of Infection Control 40 (2012) 815-9
SSI risk as the NNIS risk score increased (using NNIS risk index of
0 as a reference, NNIS score 1 associated with an OR of 1 [95% CI:
0.7-1.4] for SSI; NNIS score of 2 associated with an ORof 1.2 [95% CI:
0.9-1.5]) (Fig 1). The C-statistic for the BULCS score (0.62) was
greater than the C-statistic for the NNIS risk index (0.55).
In terms of outcomes in the 30 days following surgery (Table 3),
compared with controls, cases were more likely to return to the
emergency department (20.9% vs 57.1%, respectively; P <.0001; OR,
4.96 [95% CI: 2.9-8.48]); to be readmitted to the hospital (10.3% vs
40.7%, respectively; OR, 6.53 [95% CI: 3.44-12.42]); and to undergo
an outpatient procedure related to their surgery (2.2% vs 8%,
respectively; OR, 4.75 [95% CI: 1.32-17.14]). Cases had a higher
30-day mortality than did controls (3.3% vs 0.7%, respectively),
although this did not reach statistical significance (OR, 4.5 [95% CI:
This is the largest published study reporting risk factors for SSI
following RYGB bariatric surgery. Several important findings are
notable. Risk factors relating to characteristics of the operative
setting, comorbid conditions, and functional status of the patient
were all identified. Based on the risk factors identified, a risk score
specific to SSI following bariatric surgery, the BULCS score, was
developed. This score is unique and is a potentially valuable tool to
assist clinicians in assessing SSI risk in patients prior to bariatric
surgery and has potential to serve as a risk adjustment tool for SSI
following bariatric surgery.
The choice of antimicrobial prophylaxis is very critical in
decreasing the rate of SSIs and should be chosen according to the
local microbial flora of the anatomic site of surgery. A recent study
by Freeman et al reported a higher incidence of SSI following
vancomycin use as a prophylactic agent of choice prior to bariatric
surgical procedures.13Vancomycin prophylaxis was used infre-
quently in our study. However, antimicrobial prophylaxis with
cefazolin was associated with a decreased risk for SSI in our study.
Our group recently recommend that cefazolin be used for preop-
erative prophylaxis for bariatric surgery (as long as there is no ileal
involvement) and cefoxitin or cefazolin plus metronidazole be used
if the ileum is involved.14The findings from this study add support
to this recommendation because use of cefazolin was shown to be
related to decreased risk of developing SSI. This finding can be
explained, in part, by the increased activity of cefazolin against
aerobic gram-positive bacteria than cefoxitin. Of the 60 case
patients with SSI who received cefazolin, 8 (13%) had pathogens
that were aerobic gram-positive bacteria. Of the 57 patients with
SSI who received an agent other than cefazolin, 19 (33.3%) had
aerobic gram-positive pathogens isolated. Cefazolin was active
against these pathogens and would have been an effective anti-
microbial prophylaxis choice.
Use of CPAP or presence of sleep apnea was strongly associated
with risk for SSI in our study. Kaw et al reported a similar associ-
ation for patients with sleep apnea undergoing cardiac surgery.15A
2005 paper by Fleischmann et al demonstrated a need for higher
FIO2 to achieve the same arterial oxygen saturation in obese
patients than in nonobese patients.16It may be that the anatomy of
patients with sleep apnea requiring CPAP further exacerbates the
baseline need for higher FIO2in obese patients.
We also found that presence of bipolar disorder was highly
associated with increased risk for SSI following bariatric surgery.
The association between bipolar disease and SSI has not been re-
ported in the context of SSIs. Although affective disorders are not
generally considered a contraindication to bariatric surgery except
in severe cases,17,18there is some evidence to suggest that
psychiatric comorbidity may have an impact on development of
postsurgical complications, including mortality. A recent study
looking at several psychiatric conditions, including depression,
post-traumatic stress syndrome, bipolar disorder, and anxiety,
showed that patients with these conditions had a higher surgical
mortality rate, particularly after respiratory and digestive proce-
dures, although only anxiety and depression were associated with
higher postsurgical mortality in adjusted analysis.19Similarly,
patients with known schizophrenia have been found to have more
adverse events during medical and surgical hospital admissions,
contributing to higher rates of complications and death,20,21and, in
one study pertaining to appendicitis management, were more
likely to be diagnosed at a later stage of illness than their
nonschizophrenic counterparts.21Some research has suggested
that patients with acute bipolar disorder may have altered
immunity22or may have a proinflammatory physiologic state.23
We also hypothesize that bipolar patients may not have been
able to provide optimal self-care in the perioperative setting,
although data to support this were lacking. More research is war-
ranted to further investigate this association.
Similar to other SSI studies, longer operative time was a risk
factor for SSI following bariatric surgery.24-26Interestingly, diabetes
and hyperglycemia were not risk factors in the current study,
although they have been associated with increased risk in other
types of SSI.27,28
The BULCS score developed in this study utilizes 5 varia-
blesdbipolar disorder, sleep apnea, longer surgery duration, non-
cefazolin prophylaxis, and urinary incontinencedto risk stratify
patients for SSI following bariatric surgery.29An increasing BULCS
score was significantly associated with SSI. Given the availability of
the variables used in the score and the ease of calculation of the
BULCS score, we believe that the BULCS score has excellent
potential to be used, possibly as a supplement, to the NNIS risk
index for risk stratification of patients who are undergoing bariatric
surgery. Of course, the BULCS score needs to be validated in other
bariatric surgery cohorts.
During the 30 days following surgery, the patients in this
study who developed SSI were nearly 5 times as likely to return
to the emergency department, over 6 times as likely to be read-
mitted to the hospital for further care, and nearly 5 times as likely
to require a further outpatient procedure. This indicates an
increase in morbidity and health care costs for these patients
compared with patients who underwent bariatric surgery but did
not develop SSI.30
This study had limitations. Most notable was the lack of
intraoperative serum and tissue drug concentration monitoring,
which made it impossible to correlate infection risk with antimi-
crobial concentration. This was a single-center study, and the
generalizability of results remains unclear. The BULCS score was
fitted to the study data, and this score should be validated and
tested on other cohorts of bariatric surgery patients. Hopefully, the
BULCS score can be used to identify patients at increased risk for
SSI following bariatric surgery and as a supplemental risk-
adjustment tool for SSI rates, both of which will ultimately lead
to improved management and outcomes of patients undergoing
As the population in the US becomes more obese, bariatric
surgery will occur with increasing frequency. Measures to prevent
SSI following bariatric surgery and to optimize the management of
patients at high risk for SSI are necessary, life sustaining, and
potentially cost saving. This study provides key information to
identify patients at increased risk for SSI following bariatric
surgery and also demonstrates that patients who experience SSI
T. Chopra et al. / American Journal of Infection Control 40 (2012) 815-9
following bariatric surgery have increased utilization of health Download full-text
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