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Risk Factors for Surgical Site Infections after
Colorectal Resection in Diabetic Patients
Rishabh Sehgal, MB, BCh, Arthur Berg, PhD, Rafael Figueroa, MD, Lisa S Poritz, MD,
Kevin J McKenna, MD, David B Stewart, MD, Walter A Koltun, MD, FACS
Surgical site infections (SSIs) are a well known complication of gastrointestinal surgery and
associated with an increased morbidity, mortality and overall cost. Diabetes mellitus (DM) is a
risk factor for SSI. However, there is no clear consensus as to which other risk factors play a
significant role. The goal of this study was to identify risk factors associated with SSI in patients
with DM undergoing colorectal resection.
STUDY DESIGN: A retrospective review was conducted of DM patients who underwent colorectal resection from
June 2000 to June 2009 at Milton S Hershey Medical Center, Division of Colorectal Surgery.
Individual measures were analyzed using chi-square, t-test, and Mann-Whitney U tests, and
statistical significance was confirmed using a multiple logistical regression model.
RESULTS:
There were 183 DM patients included in the study, 28 (15%) of whom developed SSI. Glucose
levels were significantly higher in the SSI group for each time interval, 0 to 6 hours (211 mg/dL,
p ⫽ 0.03), 0 to 48 hours (176 mg/dL, p ⫽ 0.001), and 48 to 96 hours (167 mg/dL, p ⫽ 0.012)
postoperatively. Other measures significantly associated with SSI included the use of drains
(p ⫽ 0.05) and the use of prophylactic antibiotics for more than 24 hours (p ⫽ 0.02). Body
mass index and stoma creation approached statistical significance (p ⫽ 0.08, 0.07, respectively).
The type of hypoglycemic regimen, immunosuppression, and emergency surgery were not
associated with an increased rate of SSI.
CONCLUSIONS: Higher than normal glucose control at all postoperative time intervals was associated with SSI.
The majority of glucose levels were below the American Diabetes Association recommended
level of 200 mg/dL, but patients still developed SSI. Type of perioperative glucose control did
not affect the incidence of SSI. These data suggest that DM patients undergoing colectomy
should have glucose tightly controlled, avoid placement of drains, and receive antibiotics for less
than 24 hours. (J Am Coll Surg 2011;212:29–34. © 2011 by the American College of
Surgeons)
BACKGROUND:
Surgical site infections (SSI) pose an ongoing problem in
surgical practice. They lead to patient dissatisfaction, delayed wound healing, increased risk of incisional hernias,
extended length of hospital stay (LOS), and an increased
risk of other nosocomial complications. Furthermore,
there is an increased expense associated with SSI. The CDC
estimates an additional cost of $2,734 to $26,019 to the
American health care system per SSI, with an annual figure
estimated between $130 million and $845 million.1 Therefore, reducing the incidence of SSIs is important in improving both the individual patient’s health and reducing the
overall cost of health care.
Patients undergoing colorectal resection are at an increased risk for developing SSI due to the bacterial load of
the colon. The incidence of SSIs after colorectal resection
ranges from 3% to 30%.2 A wide variety of risk factors
thought to play a role in the pathogenesis of SSIs have been
studied. Obesity, steroid use, anemia, bowel preparation,
hypothermia, nutritional status, and blood transfusion
are some of the factors considered to be associated with
development of an SSI. The Center for Medicare and
Medicaid Services (CMS) has implemented protocols
for prophylactic antibiotic choice, timing of administration, and duration of use aimed at reducing SSI, but as
Disclosure Information: Nothing to disclose.
Presented at the American College of Surgeons 95th Clinical Congress, Chicago, IL, October 2009.
Received July 15, 2010; Revised September 7, 2010; Accepted September 10,
2010.
From the Division of Colon and Rectal Surgery, Department of Surgery
(Sehgal, Berg, Figueroa, Poritz, McKenna, Stewart, Koltun), and Department
of Public Health Sciences (Berg), Penn State Milton S Hershey Medical
Center, Hershey, PA.
Correspondence address: Rishabh Sehgal, MB, BCh, Division of Colon and
Rectal Surgery, Penn State Milton S Hershey Medical Center, PO Box 850,
Hershey, PA 17033. email: [email protected] or [email protected]
© 2011 by the American College of Surgeons
Published by Elsevier Inc.
29
ISSN 1072-7515/11/$36.00
doi:10.1016/j.jamcollsurg.2010.09.011
30
Sehgal et al
Colorectal Resection and Surgical Site Infection
J Am Coll Surg
Table 1. Criteria for Defining a Surgical Site Infection
Abbreviations and Acronyms
BMI
DM
LOS
SSI
⫽
⫽
⫽
⫽
body mass index
diabetes mellitus
length of stay
surgical site infection
of yet it is unclear if these interventions have had a
significant impact.
Diabetes mellitus (DM) has been shown to play a significant predisposing role for SSIs in many surgical disciplines
such as orthopaedic, cardiac, and general surgery.3-6 Poor
glycemic control, especially in the immediate postoperative
period, has been associated with an increased incidence of
SSI.6 The American Diabetes Association (ADA) has recommended that perioperative blood glucose levels be kept
below 200 mg/dL to minimize SSI.7 However, in this
higher risk group of DM patients, it is unclear what other
factors play a role in SSI occurrence. For example, whether
severity of DM defined by the need for insulin versus oral
agents, or whether prolonged use of prophylactic antibiotics might alter SSI incidence is unknown. The purpose of
this study was to investigate other potential risk factors in
the development of SSIs in this high risk diabetic group
undergoing colorectal resection.
Superficial incisional surgical site infection
Infection occurs within 30 days after the operation and infection
involves only skin or subcutaneous tissue of the incision and at
least one of the following:
1. Purulent drainage, with or without laboratory confirmation,
from the superficial incision.
2. Organisms isolated from an aseptically obtained culture of fluid
or tissue from the superficial incision.
3. At least one of the following signs or symptoms of infection:
pain or tenderness, localized swelling, redness, or heat and
superficial incision is deliberately opened by surgeon, unless
incision is culture-negative.
4. Diagnosis of superficial incisional surgical site infection by the
surgeon or attending physician.
All patients with DM who underwent colorectal resection
(segmental colectomy, total proctocolectomy, anterior resection, or abdominal perineal resection) by the Division of
Colon and Rectal Surgery at the Milton S Hershey Medical
Center, Penn State College of Medicine, between June 2000
and June 2009, were identified. Patients who underwent a
simple colostomy closure without segmental resection and patients who did not have a primary closure of their wound were
excluded. Data were collected from patient hospital records,
clinic notes, operative records, and electronic medical records.
The study was approved by the Milton S Hershey Medical
Center Institutional Review Board.
did or did not develop an SSI according to the definition
set by the CDC (Table 1).
Postoperative glucose levels were divided into 3 time
intervals. The first postoperative glucose (within 6 hours
of operation) was a single value. The second and third
time values were a mean of all the glucose readings taken
between 0 and 48 hours (including the first glucose) and
48 and 96 hours, respectively. The 0- to 6-hour time
period was in part chosen because intraoperative blood
sugars were infrequently measured, so this 0- to 6-hour
period was effectively the first glucose after operation, so
it was the best available measure of intraoperative glucose control. The 0- to 48-hour measurement is thought
to be an indicator of early postoperative glucose control
and by definition, included the first glucose value as
well.
Operative factors analyzed included creation of a stoma,
approach (open, laparoscopic, including hand assisted, or
laparoscopic converted to open), mode of skin closure (staples vs subcutaneous closure), use of intra-abdominal or
pelvic drains, preoperative bowel preparation, prophylactic
antibiotic use, preoperative steroid or immunosuppression
use, evidence of intra-abdominal infection at operation,
use of antibiotics longer than 24 hours, requirement for
blood products, estimated blood loss, core intraoperative
body temperature, and operative time.
Data collection
Statistical analyses
Demographic data collected included age at surgery, sex,
diagnosis, procedure performed, length of stay (LOS), readmission for SSI or any other reason, the presence of a
preoperative stoma (ileostomy or colostomy), surgical
wound classification, American Society of Anesthesiology
(ASA) score (I to IV), preoperative hypoglycemic regimen
(diet controlled, oral hypoglycemics, or insulin), and body
mass index (BMI). Patients were subdivided into those who
The R statistical software system (version 2.9.2, http://
www.r-project.org/) was used to perform univariate and
multivariate statistical analyses. The Fisher’s exact test,
2-sample t-test, and Mann-Whitney U test were used to
test the association of individual predictors with SSI. For
the multivariate analysis, logistic regression was performed.
Variable selection for consideration in the multivariate logistic regression was based on statistical significance or
METHODS
Subjects
Vol. 212, No. 1, January 2011
Sehgal et al
Table 2. Patient Characteristics Not Significantly Associated with Surgical Site Infection on Univariate Analysis
Variable
Age, y*, (mean ⫾ SE)
Sex, n (%)
Female
Male
Diagnosis, n (%)
Colorectal cancer
Diverticulitis
Inflammatory bowel
disease
Other
Preoperative stoma, n
(%)
Yes
No
Preoperative
hypoglycemic
regime, n (%)
Diet only
Oral hypoglycemics
Insulin
SSI
(n ⴝ 28, 15%)
No SSI
p
(n ⴝ 155, 85%) Value
63.6 ⫾ 12
65.6 ⫾ 12.8
12 (43)
16 (57)
64 (41)
91 (59)
10 (36)
6 (21)
70 (45)
33 (21)
9 (32)
3 (11)
25 (16)
27 (18)
0.15
0.67
0.29
Table 3. Operative Measures Not Statistically Associated
with Surgical Site Infection on Univariate Analysis
0.14
6 (4)
149 (96)
0.38
4 (14)
14 (50)
10 (36)
31
was done as an elective or emergent colectomy, the patient’s
physical status (ASA grade), and wound classification did
not correlate with SSI. The approach to the colectomy
(open or laparoscopic) and the mode of skin closure also
had no influence on development of SSI (Table 3).
Glucose values at all 3 time points were significantly
higher in the patients who developed an SSI than those
who did not (Table 4, Fig. 1). The largest difference in
glucose values between patients with or without SSI was
Variable
3 (10)
25 (90)
Colorectal Resection and Surgical Site Infection
24 (15)
94 (60)
37 (25)
*Statistical analysis performed using Mann–Whitney test. Statistical analysis
for remaining variables performed using Fisher’s exact test.
SSI, surgical site infection.
marginal statistical significance in the univariate analysis
while also considering the medical relevance of the variables as potential predictors.
RESULTS
A total of 191 diabetic patients were identified who underwent colorectal resection from June 2000 to June 2009 at
the Milton S Hershey Medical Center by the Division of
Colon and Rectal Surgery. Eight patients, none of whom
had a wound infection, had no glucose readings recorded in
the chart and were therefore excluded. Out of the evaluable
183 patients, 28 (15%) patients developed an SSI.
Patient characteristics not significantly associated with
SSI on univariate analysis are listed in Table 2 and included
age, sex, diagnosis (colorectal cancer, diverticulitis, inflammatory bowel disease, or miscellaneous) and the presence
of a preoperative stoma. Interestingly, the type of home
diabetic regimen the patient used, ie, diet controlled versus
oral hypoglycemics versus insulin, did not have any relationship to the development of an SSI.
Operative measures that were not significantly associated with an SSI included the use of perioperative steroids,
LOS, the use of blood products, estimated blood loss, average core body temperature, and the use of preoperative
bowel preparation. Furthermore, whether the procedure
SSI (n ⴝ 28)
No SSI
(n ⴝ 155)
Perioperative steroids, %
Yes
14
13
No
86
87
Length of stay, d*,
(mean ⫾ SD)
8.03 ⫾ 3.75 7.58 ⫾ 4.93
Blood transfusion, %
Yes
27
19
No
73
81
Estimated blood loss, mL*,
(mean ⫾ SD)
388 ⫾ 445
290 ⫾ 353
Core body temperature, oC*,
(mean ⫾ SD)
36.15 ⫾ 0.76 35.96 ⫾ 1.31
Length of operation, min*,
(mean ⫾ SD)
161 ⫾ 81
164 ⫾ 83
Bowel preparation, %
Yes
67
66
No
33
34
Elective, %
81
82
Emergency, %
19
18
ASA grade, %
II
32
32
III
61
58
IV
7
10
Wound classification,%
II
93
91
IV
7
(III–IV) 9
Side of colectomy, %
Left
79
74
Right
21
26
Approach, %
Open
89
87
Laparoscopic to open
7
2
Laparoscopic
4
11
Skin closure
Clips
78
85
Sutures
10
8
p
Value
0.77
0.55
0.28
0.11
0.35
0.77
1
0.43
1
0.72
0.75
0.25
0.33
*Statistical analysis performed using Mann–Whitney test.
Statistical analysis for remaining variables performed using Fisher’s exact test.
ASA, American Society of Anesthesiologists; SSI, surgical site infection.
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Sehgal et al
Colorectal Resection and Surgical Site Infection
J Am Coll Surg
Table 4. Glucose Measurements (Normal 70 to 120 mg/dL)
Time
interval, h
0–6
0 – 48
48 – 96
SSI (n ⴝ 28)
No SSI (n ⴝ 155)
211.11 ⫾ 13.62 g/dL 182.39 ⫾ 4.34 g/dL
176.77 ⫾ 7.41 g/dL 160.44 ⫾ 2.64 g/dL
167.85 ⫾ 5.03 g/dL 155.50 ⫾ 2.43 g/dL
p Value
0.03
0.001
0.012
Glucose measurements are mean ⫾ SE. Statistical analysis performed using
Mann–Whitney test.
SSI, surgical site infection.
seen with the immediate postoperative glucose. Also, this
immediate postoperative glucose was the highest glucose in
both the SSI and non-SSI patient groups, with the highest
value (211 mg/dL) seen in the SSI group.
Measures other than glucose that were significantly associated with SSI on univariate analysis included higher
BMI, use of prophylactic antibiotics greater than 24 hours,
stoma creation and the use of pelvic or intra-abdominal
drains (Table 5). When these significant univariate factors
were put into a multiple logistical regression model, glucose levels, the use of drains, and prophylactic antibiotics
for more than 24 hours remained significantly associated
with SSI; BMI and stoma creation missed absolute statistical significance (Table 6).
DISCUSSION
The aim of this study was to identify potential risk factors
for SSI in diabetic patients undergoing colorectal resection.
Our results concur with those from other studies in the
vascular, cardiothoracic, and orthopaedic literature that
show high perioperative glucose levels to be associated with
an increased risk of developing SSI.6 The American Diabetes Association recommends glucose levels be less than 200
mg/dL perioperatively in order to avoid SSI. However, in
0.006
our cohort, most of the glucose levels measured were below
200 mg/dL in the patients who still developed SSIs. By
dividing our patients’ glucose measurements into 3 time
intervals, we sought to identify if there was a specific time
frame during which hyperglycemia may be more critical in
the development of an SSI. In both groups of our patients,
those with and without SSI, the immediate postoperative
blood glucose was the highest of the 3 time points measured, suggesting this may be a key time point for intervention. Other studies in cardiac patients have also shown that
elevated intraoperative blood glucose is associated with
SSI.8 Our data suggest, however, that the American Diabetes Association recommendation of 200 mg/dL may still be
0.003
Table 6. Significant Factors Associated with Surgical Site
Infection on Multivariate Analysis
Table 5. Significant Factors Associated with Surgical Site
Infection on Univariate Analysis
Factors
BMI, kg/m2*, (mean ⫾ SD)
Prophylactic antibiotics used
⬎24 h, %
Yes
No
Stoma creation, %
Yes
No
Drains, %
Yes
No
SSI
(n ⴝ 28)
No SSI
(n ⴝ 155)
p Value
35 ⫾ 8.6
32 ⫾ 16.5
0.03
70
23
45
55
67
33
Measurement
41
59
0.04
60
40
Figure 1. Postoperative glucose values. The following blood glucose values were recorded: the first postoperative glucose (0 to 6
hours), all glucose between 0 and 48 hours and all glucose between
48 and 96 hours. Patients with and without surgical site infection
(SSI) were compared. At all time points the mean glucose was
significantly higher in the patients with an SSI. Orange bar, SSI;
green bar, no SSI.
42
58
*Statistical analysis performed using Mann–Whitney test. Statistical analysis
for remaining variables performed using Fisher’s exact test.
BMI, body mass index; SSI, surgical site infection.
Glucose
Drains
Antibiotic ⬎24 h
Body mass index, kg/m2
Stoma creation
p Value
0.02
0.05
0.02
0.08
0.07
Logistic regression using enter method and incorporating all variables with
p⬍0.1 on univariate analysis.
Vol. 212, No. 1, January 2011
Sehgal et al
too high, and lower blood sugars should be sought to minimize SSI, because the majority of the measured glucose
levels were below 200 mg/dL in those who developed SSIs.
The majority of the studies in the literature that have
looked at perioperative glucose management have been
done primarily in the critical care and cardiac surgical setting. In 2003, Furnary and colleagues8 published a study
that looked at 3,554 diabetic patients undergoing coronary
artery bypass grafting. All patients were treated with either
intraoperative subcutaneous insulin or with continuous insulin infusion for hyperglycemic control. Observed mortality with continuous insulin infusion was significantly
lower than with subcutaneous insulin. Furthermore, better
postoperative glucose control was also shown to decrease
wound infections.8,9 Data from the critical care and cardiac
literature may be able to be extrapolated to other types of
surgery, but large studies looking at perioperative glycemic
control in patients with diabetes outside of the critical care
and cardiac surgical realm are still limited.
One might postulate that the more severe the diabetes
the higher the risk of SSI. The type of hypoglycemic regimen can be used as a surrogate for disease severity. One can
suggest that diet controlled patients might have the least
severe diabetes, those on oral hypoglycemic medications
have intermediate DM severity, and those with insulin dependent diabetes have the most severe category of disease.
Using these severity categories, our data did not show a
significant difference between these groups in the risk of
developing an SSI. Ideally, hemoglobin A1c levels could be
used to assess longer term glycemic control. However due
to the retrospective nature of this study these values were
unavailable. It appears, however, that absolute perioperative glucose control is more important than severity of DM
as reflected by hypoglycemic regimen.
It can be argued that elevated glucose may be an early
sign of postoperative infection as opposed to a causative
factor. Certainly it is possible that during our 48- to 96hour time point, patients who would ultimately get an SSI
may have already started to develop such an infection that
could have been reflected in increased blood sugars. However, the highest blood glucose levels were found in the
immediate postoperative period within 6 hours of operation, which would be very unlikely to have been caused by
a wound infection at such an early time point.
Apart from glucose control, other measures that were
significantly associated with development of SSIs were the
use of pelvic or intra-abdominal drains and the use of prophylactic broad-spectrum antibiotics for longer than 24
hours. Prolonged use of both of these measures has been
shown to be associated with SSI in other patient populations.10,11 Both prolonged antibiotic use and placement of
Colorectal Resection and Surgical Site Infection
33
drains may have occurred because there were intraoperative
findings that made the operating surgeon concerned about
subsequent infection, suggesting that it was the intraoperative finding, as opposed to the drain or antibiotics themselves, that increased the SSI risk. However, in the SSI
group of patients with drains, only 1 of 18 of those drains
was placed in an abscess cavity. Therefore, the drains in our
patients were primarily placed for reasons other than obvious findings of infection at the time of operation. The
overuse of drains may increase the risk of SSI due to retrograde contamination along the drain, creating a pathway
for subcutaneous soft tissue contamination.
All of our patients received appropriate anerobic and
gram-negative antibiotic coverage on induction of anesthesia. Using a single dose of preoperative antibiotic is considered acceptable in operations lasting up to 3 hours and
without gross soilage during the operation.10 However, use
of antibiotics beyond 24 hours can be indicated in more
complicated operative procedures in which infection is
found. Increasing the length of operation has also been
shown to be a risk factor for SSI.10,12 In theory, prolonging
the length of the operation could potentially increase bacterial exposure to the wound and reduce efficacy of the
antibiotic within the tissues, suggesting the need for prolonged antibiotics.10 However, in our study, the duration of
the procedure was not a significant variable relating to SSI,
although this could be due to the somewhat limited sample
size.
Obesity not only makes the procedure technically more
challenging and potentially longer, but there is also an increased amount of fat or dead space in the wound that may
lead to an increased risk of developing a wound infection. A
study conducted by Itani and associates13 looking at the
association of BMI and the type of antibiotic prophylaxis,
revealed that in patients undergoing elective colorectal surgery there was a higher incidence of SSI in patients with
BMI ⱖ 30 kg/m2 irrespective of the type of prophylactic
antibiotic used. Obesity is already a well known risk factor
for development of SSI.14,15 In our study, increased BMI
was significant on univariate analysis and approached significance on multivariate analysis. This suggests that
weight loss in the obese patient before purely elective procedures may improve overall SSI risk in the DM patient.
Creation of a stoma was also significantly associated with
the development of SSI in this study. These results echo
several results from other similar studies.16 Creation of a
stoma may increase the risk of developing an SSI for 2
reasons. First, the stoma may have been created because of
intraoperative findings that could lead to an increased risk
of infection, and second, the potential for enteric contamination of a fresh abdominal wound from the exposed
34
Sehgal et al
Colorectal Resection and Surgical Site Infection
bowel lumen. Stoma creation should be used judiciously,
and bowel opened or matured only after the incision is
closed and protected from possible contamination.
This study has some limitations. Though suggestive,
tighter glucose control was not definitively shown to prevent wound infection rates. Larger multicenter prospective
trials will be necessary to prove this, but would be worthwhile in order to obtain data that can then be used in
quality control programs. However, based on our findings,
the American Diabetes Association recommendations of
glucose levels being kept less than 200 mg/dL may still be
too high in DM patients undergoing colorectal resection.
Tighter control of perioperative blood glucose levels may
lead to lower SSI rates.
To summarize, in diabetic patients undergoing colorectal surgery, to minimize wound infections, prophylactic
antibiotics should be stopped within 24 hours, and the use
of drains should be kept to a minimum. Weight loss before
purely elective colorectal surgery may also improve SSI risk.
Stomas should be used only when necessary and tight perioperative blood glucose controls may improve the risk of
developing SSI.
4.
5.
6.
7.
8.
9.
10.
11.
Author Contributions
Study conception and design: Sehgal, Figueroa, Poritz, Koltun
Acquisition of data: Sehgal, Figueroa
Analysis and interpretation of data: Berg
Drafting of manuscript: Sehgal, Poritz, Koltun
Critical revision: Stewart, McKenna, Poritz, Koltun
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