Factors Associated with Surgical Site Infection in Colorectal Surgery: The Japan Nosocomial Infections Surveillance Author(s): Keita Morikane MD PhD, Hitoshi Honda MD PhD, Takuya Yamagishi MD PhD, Satowa Suzuki MD PhD and Mayumi Aminaka RN PhD Source: Infection Control and Hospital Epidemiology, Vol. 35, No. 6 (June 2014), pp. 660-666 Published by: Cambridge University Press on behalf of Society for Healthcare Epidemiology of America Stable URL: http://www.jstor.org/stable/10.1086/676438 Accessed: 01-12-2015 09:43 UTC
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infection control and hospital epidemiology
june 2014, vol. 35, no. 6
original article
Factors Associated with Surgical Site Infection in Colorectal Surgery: The Japan Nosocomial Infections Surveillance Keita Morikane, MD, PhD;1 Hitoshi Honda, MD, PhD;2 Takuya Yamagishi, MD, PhD;3 Satowa Suzuki, MD, PhD;4 Mayumi Aminaka, RN, PhD5
objective. Surgical site infection (SSI) is one of the most common healthcare-associated infections (HAIs). This study aims to assess factors associated with SSI after colorectal surgery in Japan, using a Japanese national database for HAIs. design. setting.
A retrospective nationwide surveillance-based study. Japanese healthcare facilities.
methods. Data on colon and rectal surgeries performed from 2008 through 2010 were extracted from a national monitoring system for healthcare-associated infections, the Japan Nosocomial Infections Surveillance (JANIS). Factors associated with SSI after colon and rectal surgery were assessed using multivariate logistic regression. results. The cumulative incidence of SSI for colon and rectal surgery was 15.0% (6,691 of 44,751) and 17.8% (3,230 of 18,187), respectively. Traditional risk factors included in the National Nosocomial Infections Surveillance (NNIS) modified risk index were significant in predicting SSI in the final model for both colon and rectal surgery. Among the additional variables routinely collected in JANIS were factors independently associated with the development of SSI, such as male sex (adjusted odds ratio [aOR], 1.20 [95% confidence interval (CI), 1.14–1.27]), ileostomy or colostomy placement (aOR, 1.13 [95% CI, 1.04–1.21]), emergency operation (aOR, 1.40 [95% CI, 1.29– 1.52]), and multiple procedures (aOR, 1.22 [95% CI, 1.13–1.33]) for colon surgery as well as male sex (aOR, 1.43 [95% CI, 1.31–1.55]), ileostomy or colostomy placement (aOR, 1,63 [95% CI, 1.51–1.79]), and emergency operation (aOR, 1.43 [95% CI, 1.20–1.72]) for rectal surgery. conclusions. For colorectal operations, inclusion of additional variables routinely collected in JANIS can more accurately predict SSI risk than can the NNIS risk index alone. Infect Control Hosp Epidemiol 2014;35(6):660-666
Surgical site infection (SSI) is one of the most common healthcare-associated infections (HAI).1 The incidence of SSI is estimated to be 240,000 cases per year in the United States on the basis of recent epidemiological data.2 SSI occurs in 2%–5% of all patients who have undergone inpatient surgery.3 SSI also accounts for up to $10 billion of additional costs annually.4,5 In response to the substantial burden caused by SSI, the Centers for Disease Control and Prevention (CDC) published guidelines for the prevention of SSI in 1999.1 These guidelines incorporate the National Nosocomial Infections Surveillance (NNIS) risk index, which includes wound class, duration of operation, and the American Society of Anesthesiologists (ASA) score, originally suggested by Culver et al.6 Laparoscopic surgery was later added to the NNIS risk
index.7 The NNIS risk index is used for assessing the risk of SSI outside the United States as well. Recent data from the National Healthcare Safety Network (NHSN) indicate that the incidence of SSI ranges from 4% to 9% in colon surgery and 3% to 27% in rectal surgery.8 Besides the risk factors assessed in the NNIS risk index, various other factors were associated in previous studies with the development of SSI.9-11 In Japan, a national surveillance system for HAI, called the Japan Nosocomial Infections Surveillance (JANIS), was established in 2000 by the Ministry of Health, Labor and Welfare of Japan.12 Surveillance for SSI using the definition of NNIS surveillance with some modifications was begun in 2002. JANIS currently collects SSI surveillance data from
Affiliations: 1. Division of Infection Control and Clinical Laboratory, Yamagata University Hospital, Yamagata, Japan; 2. Department of Infection Prevention, Tokyo Metropolitan Tama Medical Center, Fuchu, Tokyo, Japan; 3. Infectious Disease Surveillance Center, National Institute of Infectious Diseases, Tokyo, Japan; 4. Department of Bacteriology II, National Institute of Infectious Diseases, Tokyo, Japan; 5. National College of Nursing, Japan, Tokyo, Japan. Received October 30, 2013; accepted January 30, 2014; electronically published April 22, 2014. 䉷 2014 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2014/3506-0005$15.00. DOI: 10.1086/676438
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table 1. Incidence of Surgical Site Infection (SSI) after Colorectal Surgery, 2008–2010 Incidence of SSI, % (no. of SSIs/no. of procedures) Procedure COLO REC note.
Incidence ratio (95% CI)
Cumulative
2008
2009
2010
2008 vs 2009
2008 vs 2010
15.0 (6,691/44,751) 17.8 (3,230/18,187)
15.9 (2,055/12,946) 18.3 (965/5,268)
14.8 (2,321/15,672) 18.1 (1,124/6,209)
14.3 (2,315/16,133) 17.0 (1,141/6,710)
0.93 (0.88–0.98) 0.99 (0.91–1.07)
0.90 (0.85–0.95) 0.93 (0.86–1.00)
CI, confidence interval; COLO, colon surgery; REC, rectal surgery; SSI, surgical site infection.
more than 400 institutions (as of February 2013) and is the largest SSI database in Japan. The aim of this study is to describe the incidence of SSI and identify the risk factors associated with SSI in patients who underwent colorectal surgery between 2008 and 2010 in Japan, using the large Japanese national HAI database.
methods Data on SSI in patients who underwent colorectal surgery, coded as COLO (colon surgery) and REC (rectal surgery), between 2008 and 2010 were extracted from the JANIS database. A total of 44,751 cases of COLO and 18,187 cases of REC were included in the study. Approval for data extraction was granted by the Ministry of Health, Labour and Welfare of the Japanese government. The institutional review board at Yamagata University School of Medicine gave their approval for this project. JANIS recruits hospitals on a voluntary basis each year. Participating hospitals are required to report SSI surveillance data for colorectal surgery patients electronically on a biannual basis. Variables collected include the NNIS modified risk index (wound class, ASA score, duration of operation,
figure 1. Incidence of surgical site infection (SSI) after colorectal surgery by quartile of duration of surgery. The upper cutoff points of duration in the first, second, and third quartiles were 121, 167, and 220 minutes, respectively, for colon surgery (COLO) and 160, 220, and 296 minutes, respectively, for rectal surgery (REC).
and laparoscopic surgery), age, sex, multiple surgical procedures, emergency operation (emergency status), ileostomy or colostomy placement, device implantation, trauma surgery, general anesthesia, and 1-day surgery. The type of surgery was coded according to NNIS operative procedure categories. However, colorectal surgery was coded in the same way as in the NHSN system; COLO was defined as a “procedure with resection, incision, or anastomosis of colon without including rectal procedure,” and REC was defined as a “procedure with resection, incision or anastomosis of rectum.”13 Because of the small number of cases, the following variables were excluded from statistical analysis: trauma surgery (0.3% [128 of 44,751 cases] for COLO and 0.2% [41 of 18,187 cases] for REC), 1-day surgery (0.3% [155 of 44,751 cases] for COLO and 0.2% [38 of 18,187 cases] for REC), and device-implanted surgery (1.0% [450 of 44,751 cases] for COLO and 1.0% [182 of 18,187 cases] for REC). General anesthesia was also excluded from analysis, because general anesthesia was performed in the vast majority of colorectal surgical procedures registered with JANIS (99.1% [44,358 of 44,751 cases] for COLO and 97.9% [17,796 of 18,187 cases] for REC). Before performing statistical analysis for the factors associated with SSI in colorectal surgery, the association between the incidence of SSI and selected continuous or categorical variables was examined and modified to fit the statistical model. Continuous variables, such as duration of operation and age, were divided into 4 quartiles, and the SSI rates were compared in each quartile. If there was a definite cutoff point at which it was possible to rationalize dichotomization of the variable, we dichotomized it at the cutoff point. If there was none, we simply divided the value by 10 and regarded it as a continuous variable. Categorical variables, such as ASA and wound class, were examined in the same way as the continuous variables that were categorized into quartiles. Potential risk factors associated with SSI in each type of procedure were first assessed using univariate modeling analysis. Comparison between categorical variables was done using x2 test. Variables with a P value of less than .25 in the univariate modeling analysis were considered potential independent variables and were entered into the logistic regression model. The multivariate model was developed using forward stepwise logistic regression. Variables were retained in the final model if the 2-tailed P value was less than .05.
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to 68 years or less than 68 years in REC. The incidence of SSI for both operative procedures after stratification by ASA score is shown in Table 2. There was a considerable difference in SSI rate between each ASA score group. However, because the percentages of COLO with an ASA score of 5 and of REC with an ASA score of 4 and 5 were very small (less than 0.1% of cases), the ASA score was categorized differently for COLO and REC (ie, ASA score 1, 2, 3, and 4 or greater in COLO and ASA score 1, 2, and 3 or greater in REC). Wound class contained 4 ordered categories (ie, class I to IV). The SSI rates in each group were considerably different. Because each group was sufficiently large, we retained the class I to class IV categorization without modification. Risk Factors for SSI in Colorectal Surgery figure 2. Incidence of surgical site infection (SSI) after colorectal surgery by quartile of age. The upper cutoff points of age in the first, second, and third quartiles were 61, 70, and 78 years, respectively, for colon surgery (COLO) and 59, 67, and 75 years, respectively, for rectal surgery (REC).
All of the statistical analyses were performed using SAS, version 9.0 (SAS).
results
The risk factors associated with SSI in COLO and REC by univariate modeling analysis are shown in Table 3. All collected variables except age for REC were statistically significant on univariate modeling analysis and were entered into the multivariate logistic regression models. In the final model, all variables except age were retained in COLO, whereas all variables except multiple procedures were retained in REC (Table 4). The c-index of multivariate logistic regression models for COLO and REC were 0.667 and 0.686, respectively.
discussion
Incidence of SSI and Trends over Time Cumulative incidences of SSI in COLO and REC during the study period were 15.0% (6,691 of 44,751 cases) and 17.8% (3,230 of 18,187 cases), respectively. In both of the procedures, the incidence decreased over time during the study period (Table 1). The decrease in SSI incidence in 2009 and 2010 compared with 2008 was statistically significant for COLO but not for REC. Modification of Variables Other than Dichotomous Variables We found no definite cutoff point at which to rationalize dichotomization of the duration of operation (Figure 1). We therefore divided the value by 10 and regarded it as continuous variable. There was a significant difference in the incidence of SSI between the second and third quartile of the variable “age” (Figure 2). On the basis of this finding, we dichotomized the age variable as greater than or equal to 71 years or less than 71 years in COLO and greater than or equal
Since the beginning of SSI surveillance in the NNIS system, the NNIS risk index, which initially consisted of 3 variables (duration of operation, wound class, and ASA score), has been used to adjust the risk for SSI to enable comparison of SSI incidence. Laparoscopy was incorporated as a fourth factor into the NNIS risk index for certain gastrointestinal procedures, including colon and rectal surgery. The risk adjustment model, which was published in 2010 by the CDC, changed the risk stratification of SSI significantly.14 Although previous studies analyzed risk factors for individual operative procedures, findings were mainly based on small numbers of operations in small numbers of hospitals and lacked statistical power. Like the study by Mu et al,15 our study demonstrated that risk factors for SSI differed according to the type of operative procedure. However, the number of rectal surgical procedures in the study by Mu et al15 was quite low compared with that of colon surgical procedures. The reason for this discrepancy between the number of colon and rectal surgical procedures
table 2. Incidence of Surgical Site Infection (SSI) after Colorectal Surgery by American Society of Anesthesiologists (ASA) Score SSI incidence by ASA score, % (no. of SSIs/no. of procedures) Procedure COLO REC note.
1
2
3
4
5
11.8 (1,182/10,012) 14.4 (7,21/4,994)
14.4 (3,745/26,080) 18.1 (1,950/10,777)
19.8 (1,575/7,940) 23.0 (524/2,283)
26.1 (174/667) 28.1 (34/121)
28.6 (14/49) 8.3 (1/12)
COLO, colon surgery; REC, rectal surgery.
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table 3. Univariate Modeling Analysis for Risk Factors for Surgical Site Infection (SSI) in Colorectal Surgery COLO (n p 44,751) Variable
REC (n p 18,187)
No. of procedures
No. of SSI
Incidence of SSI (%)
No. of procedures
No. of SSI
Incidence of SSI (%)
22,072 22,679 ... ...
3,407 3,284 ... ...
15.4 14.5 ... ...
... ... 9,056 9,131
... ... 1,635 1,595
... ... 18.1 17.5
10,012 26,080 7,940 719 ...
1,182 3,745 1,575 189 ...
11.8 14.4 19.8 26.3 ...
4,994 10,777 ... ... 2,416
721 1,950 ... ... 559
14.4 18.1 ... ... 23.1
11,281 11,201 11,127 11,142
1,430 1,650 1,713 1,898
12.7 14.7 15.4 17.0
4,609 4,568 4,474 4,536
544 743 807 1,136
11.8 16.3 18.0 25.0
6,499 38,252
1,716 4,975
26.4 13.0
880 17,303
291 2,939
33.1 17.0
24,973 19,741
4,042 2,641
16.2 13.4
11,386 6,778
2,276 948
20.0 14.0
6,353 38,398
1,453 5,238
22.9 13.6
5,815 12,372
1,574 1,656
27.1 13.4
10,406 34,345
838 5,863
8.05 17.0
3,997 14,190
456 2,774
11.4 19.6
4,584 40,167
982 5,709
21.4 14.2
1,945 16,242
440 2,790
22.6 17.2
1,350 37,888 3,505 2,008
132 4,777 1,009 773
9.8 12.6 28.8 38.5
476 15,955 1,351 405
56 2,573 444 157
11.8 16.1 329 38.8
a
Age, years ≥71 !71 ≥68 !68 ASA scoreb 1 2 3 (COLO) 4, 5 (COLO) 3, 4, 5 (REC) Duration of operation First quartile Second quartile Third quartile Fourth quartile Emergent operation Yes No Sex Male Female Ileostomy/colostomy placement Yes No Laparoscopic surgery Yes No Multiple procedures Yes No Wound class I II III IV
P .0046
P .30
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
note. ASA, American Society of Anesthesiologists; COLO, colon surgery; REC, rectal surgery. a Age was classified as greater than or equal to 71 or less than 71 for COLO and greater than or equal to 68 or less than 68 for REC, respectively. See “Methods” for details. b ASA score was classified as 1, 2, 3, or greater than or equal to 4 (4 and 5) for COLO and 1, 2, or greater than or equal to 3 (3, 4, and 5) for REC. See “Methods” for details.
reported to the NHSN system is unclear. In contrast, although the JANIS database is a surveillance program that is based on voluntary reporting, the surveillance data for COLO and REC were separately reported to assess risk factors associated with each type of surgical procedure more precisely. As a result, the total number of colon and rectal surgical procedures in this study was approximately 44,000 and 18,000, respectively. Separate assessment of risk factors associated with each type of surgical procedure using a large cohort is a chief strength of our study.
The 4 variables included in the NNIS modified risk index (duration, wound class, ASA score, and laparoscopy) remained significant in the multiple regression model, as did other factors, such as sex, undergoing multiple procedures, and the placement of ileostomies and colostomies. The SSI incidence was significantly higher among male patients than among female patients. The differences in SSI incidence (male vs female patients, 16.2% vs 13.4% in COLO and 20.0% vs 14.0% in REC) were also far larger than expected. Previous studies have demonstrated variable associ-
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table 4. Multivariate Analysis for Factors Independently Associated with Surgical Site Infection in Colorectal Surgery Characteristic, by procedure
Adjusted odds ratio (95% CI)
COLO Factors in the NNIS risk index ASA score (≥4 vs 3 vs 2 vs 1) Duration of operation (per 10-minute increase) Wound class (IV vs III vs II vs I) Laparoscopic surgery Factors not in the NNIS risk index Male sex Ileostomy/colostomy placement Emergent operation Multiple procedures REC Factors in the NNIS risk index ASA score (≥4 vs 3 vs 2 vs 1) Duration of operation (increase in 10 minutes) Wound class (IV vs III vs II vs I) Laparoscopic surgery Factors not in the NNIS risk index Male sex Ileostomy/colostomy placement Emergent operation
1.12 (1.07–1.16) 1.03 (1.03–1.03) 1.77 (1.69–1.86) 0.47 (0.43–0.51) 1.20 1.13 1.40 1.22
(1.14–1.27) (1.04–1.21) (1.29–1.52) (1.13–1.33)
1.17 1.03 1.67 0.56
(1.10–1.25) (1.03–1.03) (1.53–1.84) (0.50–0.62)
1.43 (1.31–1.55) 1.63 (1.51–1.79) 1.43 (1.20–1.72)
note. ASA, American Society of Anesthesiologists; CI, confidence interval; COLO, colon surgery; NNIS, National Nosocomial Infections Surveillance; REC, rectal surgery.
ations between sex and SSI. A study by Kingston et al11 showed results similar to those of our study, whereas male sex was associated with SSI in REC, but not in COLO, in the analysis of the NHSN data.15 Additional research is needed to clarify the effect of sex on the risk of SSI. Approximately 10% of the operations (4,584 of colon cases and 1,945 of rectal cases) were deemed to be “multiple procedures.” We did not have detailed information on the types of procedures, but generally such multiple procedures tend to require more time to perform. Because the duration of the procedures was adjusted for in the model, there seem to be unknown additional factors associated with multiple procedures, possibly related to the complexity of such operations. The placement of an ileostomy or colostomy brings more contamination into the operative field and requires more time than similar surgical procedures that do not involve the creation of a stoma. Our analysis showed the placement of ileostomy or colostomy to be a significant risk factor for SSI, in keeping with the results of the study by Blumetti et al,10 who proposes adding the creation, revision, or closure of an ileostomy or colectomy as a risk factor in SSI surveillance. Because this variable has not been incorporated into the NNIS and NHSN system, placement of an ileostomy or colostomy should be considered as a risk factor for SSI in these types of procedures. Age was insignificant in the univariate modeling analysis of REC. In COLO, age was a significant predictor of SSI in univariate modeling analysis, although it did not remain so
in the multiple regression model. This result was generally consistent with the research using NHSN data, in which age was not a risk factor in REC but showed an inverted relationship with risk of SSI in COLO.15 Kaye et al16 also investigated the relationship between age and SSI incidence and found that, although the risk for SSI increased with age, beyond the age of 65 years the relationship became inverse. This inverse U-shaped trend made it difficult to evaluate the contribution that age makes to the risk of SSI. Age is a significant risk factor in few of the other operative procedures.15 Older patients may show a decreased risk for SSI, because they might be selected on the basis of indications for operation, and surgeons might also tend to avoid invasive techniques in treating older individuals. These factors may cancel out the risk, if any, associated with age. The overall incidence of SSI in our database is considerably higher than that in the NHSN data. The incidence of SSI after colon operations in the NHSN database is 5.6% (3,453 SSIs among 62,140 operations), which is approximately onethird of the incidence in the JANIS database.8 Although unmeasured factors (eg, perioperative antimicrobial use and skin antisepsis) might be associated with the difference in incidence of SSI between the JANIS and NHSN databases, this difference may be explained in part by the difficulty of postdischarge surveillance in the United States, where up to 70% of the SSI cases occur after patients are discharged from the hospital.17 In contrast, the postoperative length of stay in Japanese hospitals (typically 2 weeks or longer after COLO
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risk factors for surgical site infection in colorectal surgery
and REC) is sufficient to enable detection of most cases of SSI during hospitalization. This study has a number of limitations. Like the NHSN database, JANIS is a national surveillance program reliant on voluntary reporting, and data were reported from approximately 400 Japanese hospitals with more than 200 beds. Although the data in JANIS were robust, the findings of this study may not be generalizable to smaller Japanese hospitals. Data used in the research were collected through the national surveillance system in Japan, and the validation of data has yet to be performed. However, the overall SSI rates in JANIS are similar to the validated rates of its predecessor, the Japanese Healthcare-Associated Infections Surveillance database.18 Furthermore, another study also demonstrated similar SSI rates based on SSI surveillance with careful and timely evaluation of suspected SSI cases at a Japanese hospital.19 Therefore, we believe that data used in this study have been accurately collected and provide a good estimate of the true occurrence of SSI in Japan. As with other national databases, the number of collected variables was restricted, and even with adjustment for known predisposing factors, other unmeasured factors, including obesity, diabetes, and smoking, were not evaluated in the study. For example, body mass index has been identified as a risk factor in several studies,9,10,20,21 and medical school affiliation and hospital bed size have been identified in the research using NHSN data.15 In conclusion, we investigated the risk factors for SSI in colorectal surgery in Japan. Besides the factors that are currently used in the NNIS risk index for stratification, there are others that should be incorporated into the stratification to better adjust the risk and allow meaningful comparisons of SSI incidence between hospitals.
acknowledgments We thank all hospitals participating in the JANIS system. Financial support. This work was supported by grants H24-ShinkouIppan-010 from the Ministry of Health, Labour and Welfare, Japan. Potential conflicts of interest. All authors report no conflicts of interest relevant to this article. All authors submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and the conflicts that the editors consider relevant to this article are disclosed here. Address correspondence to Keita Morikane, MD, PhD, Division of Infection Control and Clinical Laboratory, Yamagata University Hospital, 2–2–2 Iida-Nishi, Yamagata 990–9585, Japan ([email protected]). Presented in part: IDWeek 2012; San Diego, California; October 20, 2012.
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3. Cruse P. Wound infection surveillance. Rev Infect Dis 1981;3: 734–737. 4. Engemann JJ, Carmeli Y, Cosgrove SE, et al. Adverse clinical and economic outcomes attributable to methicillin resistance among patients with Staphylococcus aureus surgical site infection. Clin Infect Dis 2003;36:592–598. 5. Kirkland KB, Briggs JP, Trivette SL, Wilkinson WE, Sexton DJ. The impact of surgical-site infections in the 1990s: attributable mortality, excess length of hospitalization, and extra costs. Infect Control Hosp Epidemiol 1999;20:725–730. 6. Culver DH, Horan TC, Gaynes RP, et al. Surgical wound infection rates by wound class, operative procedure, and patient risk index. Am J Med 1991;91:152S–157S. 7. Gaynes RP, Culver DH, Horan TC, et al. Surgical site infection rates in the United States, 1992–1998: the National Nosocomial Infections Surveillance System basic SSI risk index. Clin Infect Dis 2001;33:S69–S77. 8. Edwards JR, Peterson KD, Mu Y, et al. National Healthcare Safety Network (NHSN) report, data summary for 2006 through 2008, issued December 2009. Am J Infect Control 2009;37:783– 805. 9. de Oliveira AC, Ciosak SI, Ferraz EM, et al. Surgical site infection in patients submitted to digestive surgery: risk prediction and the NNIS risk index. Am J Infect Control 2006;34:201–207. 10. Blumetti J, Luu M, Sarosi G, et al. Surgical site infections after colorectal surgery: do risk factors vary depending on the type of infection considered? Surgery 2007;142:704–711. 11. Kingston RD, Walsh S, Robinson C. Significant risk factors in elective colorectal surgery. Ann R Coll Surg Engl 1995;77:369– 371. 12. Japan Nosocomial Infections Surveillance. http://www.nih -janis.jp/english/about/index.html. Accessed January 25, 2014. 13. Centers for Disease Control and Prevention. Surveillance for Surgical Site Infection Events, National Healthcare Safety Network. http://www.cdc.gov/nhsn/acute-care-hospital/ssi/index .html. Accessed January 25, 2014. 14. Centers for Disease Control and Prevention. National Healthcare Safety Network newsletter. http://www.cdc.gov/nhsn/PDFs /Newsletters/NHSN_NL_OCT_2010SE_final.pdf. Published October 2010. Accessed January 25, 2014. 15. Mu Y, Edwards JR, Horan TC, Berrios-Torres SI, Fridkin SK. Improving risk-adjusted measures of surgical site infection for the National Healthcare Safety Network. Infect Control Hosp Epidemiol 2011;32:970–986. 16. Kaye KS, Schmit K, Pieper C, et al. The effect of increasing age on the risk of surgical site infection. J Infect Dis 2005;191:1056– 1062. 17. Holtz TH, Wenzel RP. Postdischarge surveillance for nosocomial wound infection: a brief review and commentary. Am J Infect Control 1992;20:206–213. 18. Morikane K, Harihara Y, Konishi T. Ten years of experience in nationwide surgical site infection surveillance in Japan. In: Program and abstracts of the 49th Annual Meeting of the Infectious Disease Society of America (IDSA). Boston, MA: IDSA, 2011. Abstract 689. 19. Morikane K, Nishioka M, Tanimura H, Noguchi H, Konishi T, Kobayashi H. Using surveillance data to direct infection control efforts to reduce surgical-site infections following clean abdominal operations in Japan. Infect Control Hosp Epidemiol 2002;23: 404–406.
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infection control and hospital epidemiology
june 2014, vol. 35, no. 6
original article
Factors Associated with Surgical Site Infection in Colorectal Surgery: The Japan Nosocomial Infections Surveillance Keita Morikane, MD, PhD;1 Hitoshi Honda, MD, PhD;2 Takuya Yamagishi, MD, PhD;3 Satowa Suzuki, MD, PhD;4 Mayumi Aminaka, RN, PhD5
objective. Surgical site infection (SSI) is one of the most common healthcare-associated infections (HAIs). This study aims to assess factors associated with SSI after colorectal surgery in Japan, using a Japanese national database for HAIs. design. setting.
A retrospective nationwide surveillance-based study. Japanese healthcare facilities.
methods. Data on colon and rectal surgeries performed from 2008 through 2010 were extracted from a national monitoring system for healthcare-associated infections, the Japan Nosocomial Infections Surveillance (JANIS). Factors associated with SSI after colon and rectal surgery were assessed using multivariate logistic regression. results. The cumulative incidence of SSI for colon and rectal surgery was 15.0% (6,691 of 44,751) and 17.8% (3,230 of 18,187), respectively. Traditional risk factors included in the National Nosocomial Infections Surveillance (NNIS) modified risk index were significant in predicting SSI in the final model for both colon and rectal surgery. Among the additional variables routinely collected in JANIS were factors independently associated with the development of SSI, such as male sex (adjusted odds ratio [aOR], 1.20 [95% confidence interval (CI), 1.14–1.27]), ileostomy or colostomy placement (aOR, 1.13 [95% CI, 1.04–1.21]), emergency operation (aOR, 1.40 [95% CI, 1.29– 1.52]), and multiple procedures (aOR, 1.22 [95% CI, 1.13–1.33]) for colon surgery as well as male sex (aOR, 1.43 [95% CI, 1.31–1.55]), ileostomy or colostomy placement (aOR, 1,63 [95% CI, 1.51–1.79]), and emergency operation (aOR, 1.43 [95% CI, 1.20–1.72]) for rectal surgery. conclusions. For colorectal operations, inclusion of additional variables routinely collected in JANIS can more accurately predict SSI risk than can the NNIS risk index alone. Infect Control Hosp Epidemiol 2014;35(6):660-666
Surgical site infection (SSI) is one of the most common healthcare-associated infections (HAI).1 The incidence of SSI is estimated to be 240,000 cases per year in the United States on the basis of recent epidemiological data.2 SSI occurs in 2%–5% of all patients who have undergone inpatient surgery.3 SSI also accounts for up to $10 billion of additional costs annually.4,5 In response to the substantial burden caused by SSI, the Centers for Disease Control and Prevention (CDC) published guidelines for the prevention of SSI in 1999.1 These guidelines incorporate the National Nosocomial Infections Surveillance (NNIS) risk index, which includes wound class, duration of operation, and the American Society of Anesthesiologists (ASA) score, originally suggested by Culver et al.6 Laparoscopic surgery was later added to the NNIS risk
index.7 The NNIS risk index is used for assessing the risk of SSI outside the United States as well. Recent data from the National Healthcare Safety Network (NHSN) indicate that the incidence of SSI ranges from 4% to 9% in colon surgery and 3% to 27% in rectal surgery.8 Besides the risk factors assessed in the NNIS risk index, various other factors were associated in previous studies with the development of SSI.9-11 In Japan, a national surveillance system for HAI, called the Japan Nosocomial Infections Surveillance (JANIS), was established in 2000 by the Ministry of Health, Labor and Welfare of Japan.12 Surveillance for SSI using the definition of NNIS surveillance with some modifications was begun in 2002. JANIS currently collects SSI surveillance data from
Affiliations: 1. Division of Infection Control and Clinical Laboratory, Yamagata University Hospital, Yamagata, Japan; 2. Department of Infection Prevention, Tokyo Metropolitan Tama Medical Center, Fuchu, Tokyo, Japan; 3. Infectious Disease Surveillance Center, National Institute of Infectious Diseases, Tokyo, Japan; 4. Department of Bacteriology II, National Institute of Infectious Diseases, Tokyo, Japan; 5. National College of Nursing, Japan, Tokyo, Japan. Received October 30, 2013; accepted January 30, 2014; electronically published April 22, 2014. 䉷 2014 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2014/3506-0005$15.00. DOI: 10.1086/676438
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table 1. Incidence of Surgical Site Infection (SSI) after Colorectal Surgery, 2008–2010 Incidence of SSI, % (no. of SSIs/no. of procedures) Procedure COLO REC note.
Incidence ratio (95% CI)
Cumulative
2008
2009
2010
2008 vs 2009
2008 vs 2010
15.0 (6,691/44,751) 17.8 (3,230/18,187)
15.9 (2,055/12,946) 18.3 (965/5,268)
14.8 (2,321/15,672) 18.1 (1,124/6,209)
14.3 (2,315/16,133) 17.0 (1,141/6,710)
0.93 (0.88–0.98) 0.99 (0.91–1.07)
0.90 (0.85–0.95) 0.93 (0.86–1.00)
CI, confidence interval; COLO, colon surgery; REC, rectal surgery; SSI, surgical site infection.
more than 400 institutions (as of February 2013) and is the largest SSI database in Japan. The aim of this study is to describe the incidence of SSI and identify the risk factors associated with SSI in patients who underwent colorectal surgery between 2008 and 2010 in Japan, using the large Japanese national HAI database.
methods Data on SSI in patients who underwent colorectal surgery, coded as COLO (colon surgery) and REC (rectal surgery), between 2008 and 2010 were extracted from the JANIS database. A total of 44,751 cases of COLO and 18,187 cases of REC were included in the study. Approval for data extraction was granted by the Ministry of Health, Labour and Welfare of the Japanese government. The institutional review board at Yamagata University School of Medicine gave their approval for this project. JANIS recruits hospitals on a voluntary basis each year. Participating hospitals are required to report SSI surveillance data for colorectal surgery patients electronically on a biannual basis. Variables collected include the NNIS modified risk index (wound class, ASA score, duration of operation,
figure 1. Incidence of surgical site infection (SSI) after colorectal surgery by quartile of duration of surgery. The upper cutoff points of duration in the first, second, and third quartiles were 121, 167, and 220 minutes, respectively, for colon surgery (COLO) and 160, 220, and 296 minutes, respectively, for rectal surgery (REC).
and laparoscopic surgery), age, sex, multiple surgical procedures, emergency operation (emergency status), ileostomy or colostomy placement, device implantation, trauma surgery, general anesthesia, and 1-day surgery. The type of surgery was coded according to NNIS operative procedure categories. However, colorectal surgery was coded in the same way as in the NHSN system; COLO was defined as a “procedure with resection, incision, or anastomosis of colon without including rectal procedure,” and REC was defined as a “procedure with resection, incision or anastomosis of rectum.”13 Because of the small number of cases, the following variables were excluded from statistical analysis: trauma surgery (0.3% [128 of 44,751 cases] for COLO and 0.2% [41 of 18,187 cases] for REC), 1-day surgery (0.3% [155 of 44,751 cases] for COLO and 0.2% [38 of 18,187 cases] for REC), and device-implanted surgery (1.0% [450 of 44,751 cases] for COLO and 1.0% [182 of 18,187 cases] for REC). General anesthesia was also excluded from analysis, because general anesthesia was performed in the vast majority of colorectal surgical procedures registered with JANIS (99.1% [44,358 of 44,751 cases] for COLO and 97.9% [17,796 of 18,187 cases] for REC). Before performing statistical analysis for the factors associated with SSI in colorectal surgery, the association between the incidence of SSI and selected continuous or categorical variables was examined and modified to fit the statistical model. Continuous variables, such as duration of operation and age, were divided into 4 quartiles, and the SSI rates were compared in each quartile. If there was a definite cutoff point at which it was possible to rationalize dichotomization of the variable, we dichotomized it at the cutoff point. If there was none, we simply divided the value by 10 and regarded it as a continuous variable. Categorical variables, such as ASA and wound class, were examined in the same way as the continuous variables that were categorized into quartiles. Potential risk factors associated with SSI in each type of procedure were first assessed using univariate modeling analysis. Comparison between categorical variables was done using x2 test. Variables with a P value of less than .25 in the univariate modeling analysis were considered potential independent variables and were entered into the logistic regression model. The multivariate model was developed using forward stepwise logistic regression. Variables were retained in the final model if the 2-tailed P value was less than .05.
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to 68 years or less than 68 years in REC. The incidence of SSI for both operative procedures after stratification by ASA score is shown in Table 2. There was a considerable difference in SSI rate between each ASA score group. However, because the percentages of COLO with an ASA score of 5 and of REC with an ASA score of 4 and 5 were very small (less than 0.1% of cases), the ASA score was categorized differently for COLO and REC (ie, ASA score 1, 2, 3, and 4 or greater in COLO and ASA score 1, 2, and 3 or greater in REC). Wound class contained 4 ordered categories (ie, class I to IV). The SSI rates in each group were considerably different. Because each group was sufficiently large, we retained the class I to class IV categorization without modification. Risk Factors for SSI in Colorectal Surgery figure 2. Incidence of surgical site infection (SSI) after colorectal surgery by quartile of age. The upper cutoff points of age in the first, second, and third quartiles were 61, 70, and 78 years, respectively, for colon surgery (COLO) and 59, 67, and 75 years, respectively, for rectal surgery (REC).
All of the statistical analyses were performed using SAS, version 9.0 (SAS).
results
The risk factors associated with SSI in COLO and REC by univariate modeling analysis are shown in Table 3. All collected variables except age for REC were statistically significant on univariate modeling analysis and were entered into the multivariate logistic regression models. In the final model, all variables except age were retained in COLO, whereas all variables except multiple procedures were retained in REC (Table 4). The c-index of multivariate logistic regression models for COLO and REC were 0.667 and 0.686, respectively.
discussion
Incidence of SSI and Trends over Time Cumulative incidences of SSI in COLO and REC during the study period were 15.0% (6,691 of 44,751 cases) and 17.8% (3,230 of 18,187 cases), respectively. In both of the procedures, the incidence decreased over time during the study period (Table 1). The decrease in SSI incidence in 2009 and 2010 compared with 2008 was statistically significant for COLO but not for REC. Modification of Variables Other than Dichotomous Variables We found no definite cutoff point at which to rationalize dichotomization of the duration of operation (Figure 1). We therefore divided the value by 10 and regarded it as continuous variable. There was a significant difference in the incidence of SSI between the second and third quartile of the variable “age” (Figure 2). On the basis of this finding, we dichotomized the age variable as greater than or equal to 71 years or less than 71 years in COLO and greater than or equal
Since the beginning of SSI surveillance in the NNIS system, the NNIS risk index, which initially consisted of 3 variables (duration of operation, wound class, and ASA score), has been used to adjust the risk for SSI to enable comparison of SSI incidence. Laparoscopy was incorporated as a fourth factor into the NNIS risk index for certain gastrointestinal procedures, including colon and rectal surgery. The risk adjustment model, which was published in 2010 by the CDC, changed the risk stratification of SSI significantly.14 Although previous studies analyzed risk factors for individual operative procedures, findings were mainly based on small numbers of operations in small numbers of hospitals and lacked statistical power. Like the study by Mu et al,15 our study demonstrated that risk factors for SSI differed according to the type of operative procedure. However, the number of rectal surgical procedures in the study by Mu et al15 was quite low compared with that of colon surgical procedures. The reason for this discrepancy between the number of colon and rectal surgical procedures
table 2. Incidence of Surgical Site Infection (SSI) after Colorectal Surgery by American Society of Anesthesiologists (ASA) Score SSI incidence by ASA score, % (no. of SSIs/no. of procedures) Procedure COLO REC note.
1
2
3
4
5
11.8 (1,182/10,012) 14.4 (7,21/4,994)
14.4 (3,745/26,080) 18.1 (1,950/10,777)
19.8 (1,575/7,940) 23.0 (524/2,283)
26.1 (174/667) 28.1 (34/121)
28.6 (14/49) 8.3 (1/12)
COLO, colon surgery; REC, rectal surgery.
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table 3. Univariate Modeling Analysis for Risk Factors for Surgical Site Infection (SSI) in Colorectal Surgery COLO (n p 44,751) Variable
REC (n p 18,187)
No. of procedures
No. of SSI
Incidence of SSI (%)
No. of procedures
No. of SSI
Incidence of SSI (%)
22,072 22,679 ... ...
3,407 3,284 ... ...
15.4 14.5 ... ...
... ... 9,056 9,131
... ... 1,635 1,595
... ... 18.1 17.5
10,012 26,080 7,940 719 ...
1,182 3,745 1,575 189 ...
11.8 14.4 19.8 26.3 ...
4,994 10,777 ... ... 2,416
721 1,950 ... ... 559
14.4 18.1 ... ... 23.1
11,281 11,201 11,127 11,142
1,430 1,650 1,713 1,898
12.7 14.7 15.4 17.0
4,609 4,568 4,474 4,536
544 743 807 1,136
11.8 16.3 18.0 25.0
6,499 38,252
1,716 4,975
26.4 13.0
880 17,303
291 2,939
33.1 17.0
24,973 19,741
4,042 2,641
16.2 13.4
11,386 6,778
2,276 948
20.0 14.0
6,353 38,398
1,453 5,238
22.9 13.6
5,815 12,372
1,574 1,656
27.1 13.4
10,406 34,345
838 5,863
8.05 17.0
3,997 14,190
456 2,774
11.4 19.6
4,584 40,167
982 5,709
21.4 14.2
1,945 16,242
440 2,790
22.6 17.2
1,350 37,888 3,505 2,008
132 4,777 1,009 773
9.8 12.6 28.8 38.5
476 15,955 1,351 405
56 2,573 444 157
11.8 16.1 329 38.8
a
Age, years ≥71 !71 ≥68 !68 ASA scoreb 1 2 3 (COLO) 4, 5 (COLO) 3, 4, 5 (REC) Duration of operation First quartile Second quartile Third quartile Fourth quartile Emergent operation Yes No Sex Male Female Ileostomy/colostomy placement Yes No Laparoscopic surgery Yes No Multiple procedures Yes No Wound class I II III IV
P .0046
P .30
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
!.0001
note. ASA, American Society of Anesthesiologists; COLO, colon surgery; REC, rectal surgery. a Age was classified as greater than or equal to 71 or less than 71 for COLO and greater than or equal to 68 or less than 68 for REC, respectively. See “Methods” for details. b ASA score was classified as 1, 2, 3, or greater than or equal to 4 (4 and 5) for COLO and 1, 2, or greater than or equal to 3 (3, 4, and 5) for REC. See “Methods” for details.
reported to the NHSN system is unclear. In contrast, although the JANIS database is a surveillance program that is based on voluntary reporting, the surveillance data for COLO and REC were separately reported to assess risk factors associated with each type of surgical procedure more precisely. As a result, the total number of colon and rectal surgical procedures in this study was approximately 44,000 and 18,000, respectively. Separate assessment of risk factors associated with each type of surgical procedure using a large cohort is a chief strength of our study.
The 4 variables included in the NNIS modified risk index (duration, wound class, ASA score, and laparoscopy) remained significant in the multiple regression model, as did other factors, such as sex, undergoing multiple procedures, and the placement of ileostomies and colostomies. The SSI incidence was significantly higher among male patients than among female patients. The differences in SSI incidence (male vs female patients, 16.2% vs 13.4% in COLO and 20.0% vs 14.0% in REC) were also far larger than expected. Previous studies have demonstrated variable associ-
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table 4. Multivariate Analysis for Factors Independently Associated with Surgical Site Infection in Colorectal Surgery Characteristic, by procedure
Adjusted odds ratio (95% CI)
COLO Factors in the NNIS risk index ASA score (≥4 vs 3 vs 2 vs 1) Duration of operation (per 10-minute increase) Wound class (IV vs III vs II vs I) Laparoscopic surgery Factors not in the NNIS risk index Male sex Ileostomy/colostomy placement Emergent operation Multiple procedures REC Factors in the NNIS risk index ASA score (≥4 vs 3 vs 2 vs 1) Duration of operation (increase in 10 minutes) Wound class (IV vs III vs II vs I) Laparoscopic surgery Factors not in the NNIS risk index Male sex Ileostomy/colostomy placement Emergent operation
1.12 (1.07–1.16) 1.03 (1.03–1.03) 1.77 (1.69–1.86) 0.47 (0.43–0.51) 1.20 1.13 1.40 1.22
(1.14–1.27) (1.04–1.21) (1.29–1.52) (1.13–1.33)
1.17 1.03 1.67 0.56
(1.10–1.25) (1.03–1.03) (1.53–1.84) (0.50–0.62)
1.43 (1.31–1.55) 1.63 (1.51–1.79) 1.43 (1.20–1.72)
note. ASA, American Society of Anesthesiologists; CI, confidence interval; COLO, colon surgery; NNIS, National Nosocomial Infections Surveillance; REC, rectal surgery.
ations between sex and SSI. A study by Kingston et al11 showed results similar to those of our study, whereas male sex was associated with SSI in REC, but not in COLO, in the analysis of the NHSN data.15 Additional research is needed to clarify the effect of sex on the risk of SSI. Approximately 10% of the operations (4,584 of colon cases and 1,945 of rectal cases) were deemed to be “multiple procedures.” We did not have detailed information on the types of procedures, but generally such multiple procedures tend to require more time to perform. Because the duration of the procedures was adjusted for in the model, there seem to be unknown additional factors associated with multiple procedures, possibly related to the complexity of such operations. The placement of an ileostomy or colostomy brings more contamination into the operative field and requires more time than similar surgical procedures that do not involve the creation of a stoma. Our analysis showed the placement of ileostomy or colostomy to be a significant risk factor for SSI, in keeping with the results of the study by Blumetti et al,10 who proposes adding the creation, revision, or closure of an ileostomy or colectomy as a risk factor in SSI surveillance. Because this variable has not been incorporated into the NNIS and NHSN system, placement of an ileostomy or colostomy should be considered as a risk factor for SSI in these types of procedures. Age was insignificant in the univariate modeling analysis of REC. In COLO, age was a significant predictor of SSI in univariate modeling analysis, although it did not remain so
in the multiple regression model. This result was generally consistent with the research using NHSN data, in which age was not a risk factor in REC but showed an inverted relationship with risk of SSI in COLO.15 Kaye et al16 also investigated the relationship between age and SSI incidence and found that, although the risk for SSI increased with age, beyond the age of 65 years the relationship became inverse. This inverse U-shaped trend made it difficult to evaluate the contribution that age makes to the risk of SSI. Age is a significant risk factor in few of the other operative procedures.15 Older patients may show a decreased risk for SSI, because they might be selected on the basis of indications for operation, and surgeons might also tend to avoid invasive techniques in treating older individuals. These factors may cancel out the risk, if any, associated with age. The overall incidence of SSI in our database is considerably higher than that in the NHSN data. The incidence of SSI after colon operations in the NHSN database is 5.6% (3,453 SSIs among 62,140 operations), which is approximately onethird of the incidence in the JANIS database.8 Although unmeasured factors (eg, perioperative antimicrobial use and skin antisepsis) might be associated with the difference in incidence of SSI between the JANIS and NHSN databases, this difference may be explained in part by the difficulty of postdischarge surveillance in the United States, where up to 70% of the SSI cases occur after patients are discharged from the hospital.17 In contrast, the postoperative length of stay in Japanese hospitals (typically 2 weeks or longer after COLO
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risk factors for surgical site infection in colorectal surgery
and REC) is sufficient to enable detection of most cases of SSI during hospitalization. This study has a number of limitations. Like the NHSN database, JANIS is a national surveillance program reliant on voluntary reporting, and data were reported from approximately 400 Japanese hospitals with more than 200 beds. Although the data in JANIS were robust, the findings of this study may not be generalizable to smaller Japanese hospitals. Data used in the research were collected through the national surveillance system in Japan, and the validation of data has yet to be performed. However, the overall SSI rates in JANIS are similar to the validated rates of its predecessor, the Japanese Healthcare-Associated Infections Surveillance database.18 Furthermore, another study also demonstrated similar SSI rates based on SSI surveillance with careful and timely evaluation of suspected SSI cases at a Japanese hospital.19 Therefore, we believe that data used in this study have been accurately collected and provide a good estimate of the true occurrence of SSI in Japan. As with other national databases, the number of collected variables was restricted, and even with adjustment for known predisposing factors, other unmeasured factors, including obesity, diabetes, and smoking, were not evaluated in the study. For example, body mass index has been identified as a risk factor in several studies,9,10,20,21 and medical school affiliation and hospital bed size have been identified in the research using NHSN data.15 In conclusion, we investigated the risk factors for SSI in colorectal surgery in Japan. Besides the factors that are currently used in the NNIS risk index for stratification, there are others that should be incorporated into the stratification to better adjust the risk and allow meaningful comparisons of SSI incidence between hospitals.
acknowledgments We thank all hospitals participating in the JANIS system. Financial support. This work was supported by grants H24-ShinkouIppan-010 from the Ministry of Health, Labour and Welfare, Japan. Potential conflicts of interest. All authors report no conflicts of interest relevant to this article. All authors submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and the conflicts that the editors consider relevant to this article are disclosed here. Address correspondence to Keita Morikane, MD, PhD, Division of Infection Control and Clinical Laboratory, Yamagata University Hospital, 2–2–2 Iida-Nishi, Yamagata 990–9585, Japan ([email protected]). Presented in part: IDWeek 2012; San Diego, California; October 20, 2012.
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