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Abstract
Background and Purpose: Each year, as many as two million operations are complicated by surgical site infections in the United States, and surgical patients account for 30% of patients with sepsis. The purpose of this
study was to determine recent trends in sepsis incidence, severity, and mortality rate after surgical procedures
and to evaluate changes in the pattern of septicemia pathogens over time.
Methods: Analysis of the 19902006 hospital discharge data from the Healthcare Cost and Utilization Project
(HCUP) State Inpatient Databases (SID) for New Jersey. Patients 18 years who developed sepsis after surgery
were identified using International Classification of Diseases, Ninth Revision, Clinical Modification codes as
defined by the Patient Safety Indicator Postoperative Sepsis developed by the Agency for Healthcare Research and Quality (AHRQ). Severe sepsis was defined as sepsis complicated by organ dysfunction.
Results: A total of 1,276,451 surgery discharges (537,843 elective [42.1%] and 738,608 non-elective [57.9%] procedures) were identified. After elective surgery, 5,865 patients (1.09%) developed postoperative sepsis, of whom
2,778 (0.52%) had severe sepsis. The incidence of postoperative sepsis after elective surgery increased from
0.67% to 1.74% (p 0.0001) and severe sepsis after elective surgery from 0.22% to 1.12% (p 0.0001). The sepsis mortality rate for elective procedures showed no significant change over time. The proportion of severe sepsis after elective cases increased from 32.9% to 64.6% (p 0.0002). The rates of postoperative sepsis (4.24%) and
severe sepsis (2.28%) were significantly greater for non-elective than for elective procedures (p 0.0002). Nonelective surgical procedures had a significant increase in the rates of postoperative sepsis (3.74% to 4.51%) and
severe sepsis (1.79% to 3.15%) over time (p 0.0001) with the proportion of severe sepsis increasing from 47.7%
to 69.9% (p 0.0002). The in-hospital mortality rate after non-elective surgery decreased from 37.9% to 29.8%
(p 0.0001).
Conclusions: Sepsis and death were more likely after non-elective than elective surgery. Sepsis and severe sepsis has increased significantly after elective and non-elective procedures over the last 17 years. The hospital
mortality rate was reduced significantly after non-elective surgery, but no improvements were found for elective surgery patients who developed sepsis. Disparities in age, sex, and ethnicity and the development of postoperative surgical sepsis were found. Population-based studies may assist in defining temporal trends, disparities, and outcomes in sepsis not elucidated in smaller studies.
substantially by perioperative bacterial infection, hemorrhage, blood transfusion, or anesthesia up to severe suppression that promotes sepsis [48].
In the United States, the incidence of sepsis during the last
decades has increased considerably and has been accompanied by a significant increase in the disease severity [911].
Despite the reduction in the disease case fatality rate over
time, sepsis remains one of the leading causes of death in the
United States [12]. Surgical patients account for approxi-
ORE THAN 40 MILLION major surgical operations are performed annually in the United States of which 800,000
to two million are complicated by surgical site infections
[13]. Sepsis is an extreme manifestation of the infectious
process that is associated with increased resource utilization
and poor outcome. Surgery patients can be defined as a highrisk group for developing sepsis, as procedures evoke substantial metabolic, hematologic, and immunologic responses
[4]. The immune function after surgery may be transformed
The Surgical Outcomes Research Group, Department of Surgery, Robert Wood Johnson Medical School, New Brunswick, New Jersey.
*Presented at the 28th Annual Meeting of the Surgical Infection Society, Hilton Head Island, South Carolina, May 8, 2008.
71
72
mately 30% of all sepsis patients [13], and epidemiologic investigation of sepsis incidence and death after surgical procedures may help to define patient populations at greatest
risk and characterize temporal changes in sepsis and outcomes. Most of the current data on post-surgical sepsis are
based on analysis from single institutions and small geographic areas, which makes their generalizability difficult
[1420]. We evaluated trends in incidence, severity, mortality rate, and associated pathogens of sepsis after surgical procedures on a population level.
Patients and Methods
Data sources
Data for this study were collected from the New Jersey
State Inpatient Databases (SID) from 1990 to 2006. The SID
is a publicly available database, developed as a part of the
Healthcare Cost and Utilization Project (HCUP) and sponsored by the Agency for Healthcare Research and Quality
(AHRQ) [21]. The New Jersey SID includes inpatient discharge abstracts from the acute care community hospitals in
the state that are collected annually by the state Department
of Health and Senior Services. They contain clinical and nonclinical information on hospitalized patients with all types
of insurance and the uninsured, and cover annually more
than one million hospitalizations with several hundred characteristics.
Study population
We selected patients 18 years and older who were admitted to the hospital for surgical procedures. To identify surgical patients, we used all International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM)
operating room procedure codes and surgical discharge Diagnosis-Related Groups (DRGs).
To identify surgical patients developing sepsis, the Patient
Safety Indicator Postoperative Sepsis (PSI 13) was utilized
[22]. Patient Safety Indicator 13 was designed to identify sepsis as a complication. The AHRQ and the Stanford-University of California-San Francisco Evidence-based Practice
Center have developed Patient Safety Indicators (PSIs).
These indicators were developed after a comprehensive literature review, analysis of ICD-9-CM codes, review by a
clinician panel, implementation of risk adjustment, and empirical analyses. The PSIs focus on potentially preventable
instances of complications and other iatrogenic events during hospitalization. They are tools to identify potential adverse events and are screening tools for highlighting areas
in which quality should be investigated and for case finding
and tracking and monitoring patient safety events. Among
20 hospital-level indicators, eight are related to surgical discharges. One of these indicators, PSI 13 was utilized to identify sepsis as a complication. Patient Safety Indicators are
particularly applicable to surgical patients, as they are more
homogeneous than medical patients, making it easier to account for case mix.
Observations with postoperative sepsis had the following
ICD-9-CM diagnosis codes in any secondary position (suggesting a complication from the surgical procedure) for the
diagnosis codes: Streptococcal septicemia (038.0), staphylococcal septicemia unspecified (038.10), Staphylococcus aureus
VOGEL ET AL.
septicemia (038.11), Other staphylococcal septicemia
(038.19), pneumococcal septicemia (038.2), septicemia due to
anaerobes (038.3), gram-negative organism unspecified
(038.40), Haemophilus influenzae (038.41), Escherichia coli
(038.42), Pseudomonas (038.43), Serratia (038.44), septicemia
due to other gram-negative organisms (038.49), other specified septicemias (038.8), unspecified septicemia (038.9), septic shock (785.52), other shock without mention of trauma
(785.59), systemic inflammatory response syndrome due to
infectious process without organ dysfunction (995.91), or systemic inflammatory response syndrome due to infectious
process with organ dysfunction (995.92).
To identify major organ dysfunction, the following ICD9-CM diagnosis codes in any secondary position for the diagnosis code were used: cardiovascular failure (785.50,
785.51, 785.59, 458.0, 458.8, 458.9, 796.3, 427.5), respiratory
failure (518.81, 518.82, 786.09, 799.1), acute renal failure
(584.5, 584.6, 584.7, 584.8, 584.9), acute hepatic failure (570,
572.2, 573.4), coagulation failure (286.6, 286.9, 287.4, 287.5),
and central nervous system failure (293.0, 348.1, 348.3,
780.01).
In accordance with the PSI 13 requirements, we excluded
from the analysis all patients with preexisting sepsis or infection, with any ICD-9-CM code for immunocompromised
state or cancer, with the Major Diagnostic Categories (MDC)
code 14 (Pregnancy and Childbirth), and with hospital length
of stay of less than four days. These restrictions increase the
chance that a person developed sepsis as a result of the surgical procedure. In addition, among all septic patients, we
selected a subgroup of those with severe sepsis defined as
sepsis complicated by organ dysfunction [23]. Classification
of an operation as elective or non-elective was based on the
HCUP variable for admission type.
Statistical analysis
Data were analyzed with SAS 9.1 software (SAS Institute,
Cary, NC). We used demographic characteristics of patients
(age, sex, and race), principal and eight secondary diagnoses,
principal and seven secondary procedures, admission source
and type, disposition of patient at discharge, and calendar
year. The rate of postoperative sepsis was defined as the
number of postoperative sepsis cases divided by the number of patients with surgical procedures, expressed as a percentage. To evaluate the severity of the disease, we calculated the percentage of severe sepsis cases among all sepsis
cases. The rate of hospital mortality for postoperative sepsis
was calculated as the number of fatal surgical sepsis cases in
the hospitals divided by the total number of hospitalized
surgical patients with sepsis expressed as a percentage. To
test the difference in estimates between various groups we
used the Student t-test for continuous variables and chisquare analysis for categorical variables. The z ratio with p
value for the difference between two independent proportions was utilized to compare two groups with results presented as percentages. The Cochran-Armitage trend test was
employed initially to analyze changes in the rates of postoperative sepsis and its mortality rate from 19902006. Taking into account the changes in the age structure of population in the country over the study period, we adjusted the
rates of sepsis incidence and death with the method of direct standardization and computed direct standardized rate
73
with the standard error (SE) of this rate [24]. The structure
of the population of hospitalized surgical patients in the State
of New Jersey in 2000 was used as a standard in computing
standardized rates of sepsis incidence. Calculating the standardized rates of death, we used for the same purpose a
structure of septic surgical patients hospitalized in the year
2000. Trends in age-adjusted rates were evaluated with linear regression analysis. All reported p values are two-sided;
p 0.05 was considered significant.
Results
A total of 1,276,451 surgery discharges that met the inclusion and exclusion criteria for our study were identified in
the New Jersey acute care hospitals from 1990 to 2006.
Among all surgical patients, 42.1% were admitted to the hospital electively and 57.9% non-electively. Demographic and
clinical characteristics of patients undergoing surgical procedures of both categories, including those who developed
sepsis, are displayed in Table 1. Overall, 2.9% of all surgical
procedures were complicated by sepsis. Patients undergoing
non-elective procedures developed sepsis more often than
those having elective procedures (4.2% and 1.1%, respectively; p 0.0002).
From 1990 to 2006, the rates of postoperative sepsis in New
Jersey increased significantly (Table 2; Fig. 1) for both nonelective (from 3.74% to 4.51%; p 0.0001) and elective (from
0.67% to 1.74%; p 0.0001) surgery. The proportion of cases
of severe sepsis after non-elective procedures increased from
47.7% to 69.9% (p 0.0002) and almost doubled after elec-
TABLE 1.
CHARACTERISTICS
OF
SURGICAL PATIENTS
Elective
Non-elective
Sepsis (%)
Sepsis
Sepsis
1,276,451
37,171 (2.9)
537,843
5,865 (1.1)
738,608
31,306 (4.2)
599,867
676,557
27
18,938 (3.2)
18,233 (2.7)
0
243,700
294,133
11
3,112 (1.3)
2,753 (0.9)
0
356,167
382,424
17
15,826 (4.4)
15,480 (4.0)
0
308,668
286,053
451,365
230,365
5,398
7,131
14,946
9,696
(1.8)
(2.5)
(3.3)
(4.2)
145,847
137,656
202,450
51,890
888
1,285
2,670
1,022
(0.6)
(0.9)
(1.3)
(2.0)
162,821
148,397
248,915
178,475
4,510
5,846
12,276
8,674
(2.8)
(3.9)
(4.0)
(4.9)
947,487
152,247
88,646
47,703
40,368
26,215
5,822
2,613
1,485
1,036
19,597
(2.8)
(3.8)
(3.0)
(3.1)
(2.6)
(52.7)
403,572
60,741
35,695
18,879
18,956
4,233
735
408
264
225
2,778
(1.1)
(1.2)
(1.1)
(1.4)
543,915
91,506
52,951
28,824
21,412
(47.4)
21,982
5,087
2,205
1,221
811
16,819
(4.0)
(5.6)
(4.2)
(4.2)
(3.8)
(53.7)
1,041
964
1,109
173
103
478
1,559
1,177
(37.5)
(34.7)
(39.9)
(6.2)
(3.7)
(17.2)
(26.6)
(42.4)
8,096
6,462
5,881
1,040
539
2,222
10,234
7,777
(48.1)
(38.4)
(35.0)
(6.2)
(3.2)
(13.2)
(32.7)
(46.2)
9,137
7,246
6,990
1,213
642
2,700
11,793
8,954
(46.6)
(37.0)
(35.7)
(6.2)
(3.3)
(13.8)
(31.7)
(45.7)
74
VOGEL ET AL.
TABLE 2.
INCIDENCE
AND
MORTALITY RATE
FOR
POSTOPERATIVE SEPSIS
IN
Incidence, %
Sepsis
Severe sepsis
Sepsis
Severe sepsis
Year
Elective
N/elective
Elective
N/elective
Elective
N/elective
Elective
N/elective
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
0.67
0.83
0.75
0.88
0.87
0.96
1.04
1.24
1.19
1.33
1.26
1.36
1.21
1.47
1.50
1.74
1.74
3.74
4.09
4.14
3.79
3.69
3.95
3.92
4.31
4.18
4.39
4.57
4.60
4.61
4.67
4.71
4.53
4.51
0.22
0.31
0.27
0.36
0.34
0.41
0.44
0.52
0.54
0.58
0.58
0.72
0.67
0.89
0.84
1.15
1.12
1.79
1.91
1.90
1.78
1.69
1.95
1.91
2.17
2.18
2.28
2.45
2.52
2.69
2.75
2.97
3.11
3.15
27.11
27.01
25.56
29.17
29.08
28.21
25.76
25.98
25.95
26.84
27.39
27.87
28.53
29.16
21.49
23.53
23.88
37.94
36.18
35.20
33.51
33.88
34.04
32.83
31.48
33.20
34.38
31.30
30.48
31.71
29.93
29.09
30.81
29.77
52.21
50.98
46.88
54.79
53.72
48.15
46.43
47.02
41.96
44.22
44.14
38.80
39.89
38.12
31.28
31.58
34.35
55.42
54.89
52.83
51.89
51.40
49.04
48.70
47.01
47.26
48.98
45.59
42.14
43.44
40.42
39.87
40.56
38.00
N/elective non-elective.
togenarians had a rate of sepsis of 4.21% (p 0.0002). Interestingly, this trend predominated among patients having
elective procedures (3.2-fold increase: From 0.61% to 1.97%;
p 0.0002) whereas after non-elective surgical procedures,
the increase was less extensive (1.7-fold: From 2.77% to
4.86%; p 0.0002) and in patients 6579 years of age, the
rates of postoperative sepsis did not differ from that in octogenarians.
Male patients were more likely to have postoperative sepsis than female patients (odds ratio [OR] 1.17; 95% confidence interval [CI] 1.15, 1.20), and this difference was greater
after elective procedures (OR 1.37; 95% CI 1.30, 1.44) than
after non-elective surgery (OR 1.10; 95% CI 1.08, 1.13).
Racial disparities in the occurrence of postoperative sepsis
were noted. We found the lowest rate of surgical sepsis in
white patients (2.77%), whereas black patients had the high-
FIG. 1.
Age-adjusted rates of postoperative sepsis in New Jersey, 19902006. Error bar standard error.
FIG. 2.
Age-adjusted rates of postoperative severe sepsis in New Jersey, 19902006. Error bar standard error.
FIG. 3.
75
Age-adjusted rates of mortality for postoperative sepsis in New Jersey, 19902006. Error bar standard error.
76
FIG. 4.
error.
VOGEL ET AL.
Age-adjusted rates of mortality for postoperative severe sepsis in New Jersey, 19902006. Error bar standard
77
11.
12.
13.
14.
15.
16.
17.
18.
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