Surg Endosc DOI 10.1007/s00464-015-4349-9
and Other Interventional Techniques
Risk factors for postoperative sepsis in laparoscopic gastric bypass L. J. Blair1 • C. R. Huntington1 • T. C. Cox1 • T. Prasad1 • A. E. Lincourt1 K. S. Gersin1 • B. T. Heniford1 • V. A. Augenstein1
•
Received: 15 February 2015 / Accepted: 17 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Introduction Postoperative sepsis is a rare but serious complication following elective surgery. The purpose of this study was to identify the rate of postoperative sepsis following elective laparoscopic gastric bypass (LGBP) and to identify patients’ modifiable, preoperative risk factors. Methods The American College of Surgeons National Surgical Quality Improvement Program database was queried from 2005 to 2013 for factors associated with the development of postoperative sepsis following elective LGBP. Patients who developed sepsis were compared to those who did not. Results were analyzed using the Chisquare test for categorical variables and Wilcoxon twosample test for continuous variables. A multivariate logistic regression analysis was utilized to calculate adjusted odds ratios for factors contributing to sepsis. Results During the study period, 66,838 patients underwent LGBP. Of those, 546 patients developed postoperative sepsis (0.82 %). The development of sepsis was associated with increased operative time (161 ± 77.8 vs. 135.10 ± 56.5 min; p \ 0.0001) and a greater number of preoperative comorbidities, including diabetes (39.6 vs. 30.6 %; p \ 0.0001), hypertension requiring medication
Presented at the SAGES 2015 Annual Meeting, April 15–18, 2015, Nashville, Tennessee. & V. A. Augenstein [email protected] L. J. Blair [email protected] 1
Division of Gastrointestinal and Minimally Invasive Surgery, Department of Surgery, Carolinas Medical Center, 1025 Morehead Medical Drive, Suite 300, Charlotte, NC 28204, USA
(65.2 vs. 54 %; p \ 0.0001), current tobacco use (16.7 vs. 11.5 %; p = 0.0002), and increased pack-year history of smoking (8.6 ± 18.3 vs. 5.6 ± 14.2; p = 0.0006), and the Charlson Comorbidity Index (0.51 ± 0.74 vs. 0.35 ± 0.57, p \ 0.0001). Sepsis resulted in an increased length of stay (10.1 ± 14.4 vs. 2.4 ± 4.8 days; p \ 0.0001) and a 30 times greater chance of 30-day mortality (4.03 vs. 0.11 %, p \ 0.0001). Multivariate logistic regression analysis showed that current smokers had a 63 % greater chance of developing sepsis compared to non-smokers, controlling for age, race, gender, BMI, and CCI score (OR 1.63, 95 % CI 1.23–2.14; p = 0.0006). Conclusions Laparoscopic gastric bypass is uncommonly associated with postoperative sepsis. When it occurs, it portends a 30 times increased risk of death. A patient history of diabetes, hypertension, and increasing packyears of smoking portend an increased risk of sepsis. Current smoking status, a preoperative modifiable risk factor, is independently associated with the chance of postoperative sepsis. Preoperative patient optimization and risk reduction should be a priority for elective surgery, and patients should be encouraged to stop smoking prior to gastric bypass. Keywords Bariatric surgery Gastric bypass NSQIP Complications Mortality Smoking
Currently, obesity affects over 35 % of adults in the USA, with 69 % of the population reported to be overweight [1]. The obesity epidemic has continued to increase dramatically in more recent years with no signs of improvement, which makes this health issue one of the largest associated preventable causes of death facing the US population today [2]. When compared to supervised medical weight-loss
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programs, bariatric surgery has been shown to be the only treatment option that has provided sustainable, long-term weight loss [3]. Worldwide, bariatric surgery is commonly performed and rates are increasing annually. In 2008, 344,221 bariatric surgery operations were performed by 4680 bariatric surgeons across the globe, with 60 % of these operations being performed in North America [4]. With the increasing prevalence of obesity and its surgical correction, it is important to monitor the operative complication and mortality rates to maintain rigorous standards of quality and safety for this elective procedure. Reported rates of morbidity and mortality of this complex surgery range from 9 to 25 % and 0.1 to 2 %, respectively, and have decreased significantly since the first reports of laparoscopic gastric bypass [5]. Kelles et al. [6] estimated that 53.7 % of deaths following bariatric surgery were attributable to early or late complications, and among these, the most common cause of mortality was postoperative sepsis at 42.7 %. While postoperative sepsis and death are now rare, study of their source and control of those causes that are preventable remains important. Considering the infrequency with which these complications occur, a large, multi-institutional patient source would be required to adequately discern possible common, preventable factors. A nationwide study would be appropriate, and, to our knowledge, an epidemiologic review focusing on postoperative sepsis following laparoscopic gastric bypass has not been described. If patient risk factors can be identified, this list can be utilized by surgeons to preoperatively identify patients who may require further optimization and counseling. The purpose of this study was to identify the rate of postoperative sepsis following elective laparoscopic gastric bypass and to identify pertinent and modifiable risk factors for the development of sepsis.
Methods Data collection The American College of Surgeons National Surgical Quality Improvement Program (NSQIP) database was queried from 2005 to 2013. This database includes prospectively collected data from over 400 hospitals across the USA entered by trained reviewers beginning in the preoperative period and continuing 30 days postoperatively (acsnsqip.org). Demographic information, comorbidities, procedural data, and postoperative complications within 30 days are collected by trained data abstractors, supplemented as necessary with additional questions addressed to treating physicians and follow-up calls to patients.
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Study design The NSQIP database was queried for all elective laparoscopic gastric bypasses performed from 2005 to 2013 as determined by current procedural terminology codes 43644 and 43645. Patients under age 18 and cases coded as ‘‘emergent’’ were excluded. Variables are clearly described in the ACS NSQIP data dictionary. Smokers are defined as patients who have smoked cigarettes in the year prior to admission for surgery and do not include other tobacco products (NSQIP Data Dictionary, acsnsqip.org). NSQIP variables and outcomes NSQIP records over 30 patient comorbidities but does not include a global comorbidity scale on which to rate patients such as the Charlson Comorbidity Index (CCI) [7]. The CCI is one such scoring system that has been extensively validated in surgery patients [8–10]. The authors used available NSQIP data to create a NSQIP Charlson Comorbidity Index which has previously been published [11], where comorbidities are scored as points according to the original CCI. Previous studies have verified that CCI adapted to large administrative databases have had similar sensitivity in stratifying mortality [12, 13], and this strategy has been used in NSQIP in previous studies [14, 15]. The primary outcome of interest for this study was postoperative sepsis. Statistical analysis Patients who developed sepsis following this procedure were compared to those who did not using the Chi-square test for categorical variables and Wilcoxon two-sample test for continuous variables. Primary risk factors for developing sepsis were identified from univariate analyses. These risk factors were each then used as the primary predictor in separate multiple logistic regression models for estimating the odds of developing sepsis while controlling for age, race, gender, BMI, and CCI score. The Hosmer–Lemeshow test was used to check the goodness of fit of the multiple logistic regression models. Statistical significance was set at p B 0.05, and all reported p values are two-tailed. All data were analyzed using Statistical Analysis Software, version 9.4 (SAS Institute, Inc., Cary, NC).
Results During the study period, 66,838 patients underwent laparoscopic gastric bypass. Of those, 546 patients developed postoperative sepsis overall (0.82 %). The rates of the
Surg Endosc
development of sepsis gradually but significantly declined over the study period p \ 0.0001 (Table 1). Patient demographics and comorbidities are compared and demonstrated in Table 2. Specifically, the development of sepsis was associated with increased age (47.5 ± 11.4 vs. 44.9 ± 11.5 years; p \ 0.0001) and operative time (161 ± 77.8 vs. 135.10 ± 56.5 min; p \ 0.0001), and greater number of preoperative comorbidities including diabetes (39.6 vs. 30.6 %; p \ 0.0001), hypertension requiring medication (65.2 vs. 54 %; p \ 0.0001), current tobacco use (16.7 vs. 11.5 %; p = 0.0002), and increased pack-year smoking history (8.6 ± 18.3 vs. 5.6 ± 14.2; p = 0.0006). CCI was also strongly associated with the incidence of postoperative sepsis (0.51 ± 0.74 vs. 0.35 ± 0.57, p \ 0.0001). As would be expected, the rate of reoperation was dramatically higher in the septic patients (58.6 vs. 2.2 %, p \ 0.0001). Rates of other postoperative complications were significantly elevated in the sepsis group including wound infection, UTI, pneumonia, myocardial infarction, DVT, and PE (p \ 0.0001). There was over a 30 times greater chance of 30-day mortality for patients who developed sepsis (4.03 vs. 0.11 %, p \ 0.0001). Length of stay was also significantly greater in the sepsis group (10.1 ± 14.4 vs. 2.4 ± 4.8 days; p \ 0.0001) as was the incidence of readmission (63.7 vs. 5.8 %, p \ 0.0001). Multiple logistic regression analysis showed that current smokers had a 63 % greater chance of developing sepsis compared to non-smokers, controlling for age, race, gender, BMI, and CCI score (OR 1.63, 95 % CI 1.23–2.14; p value = 0.0006) (Table 3). Although statistical analysis did not reveal a direct association between smoking and mortality, the development of postoperative sepsis was found to have a 38 times greater chance of 30-day mortality (OR 38.08, 95 % CI 23.46–61.81; p value \ 0.0001). Moreover, as pack-year smoking history increased, patients were at increased risk of sepsis (OR 1.007, 95 % CI 1.001–1.013; p value = 0.0307); interestingly, there was a 1 % increased risk of sepsis for each additional pack-year. Hypertensive patients who require medication to control Table 1 Percentage of patients developing sepsis following laparoscopic gastric bypass by year
their disease (OR 1.315, 95 % CI 1.030–1.677; p value = 0.0277) and diabetic patients were at an increased risk of developing sepsis (OR 1.281, 95 % CI 1.053–1.557; p value = 0.0133). Increased operative time was also a predictor for sepsis (OR 1.006, 95 % CI 1.004–1.007; p value \ 0.0001). An incremental increase in postoperative sepsis risk was seen with every 30 min of additional operative time; each half hour added an 18 % risk (p \ 0.0001).
Discussion Postoperative sepsis is a rare but devastating complication of elective surgery that leads to a significantly increased risk of 30-day mortality. This study, which examines the outcomes of over 66,000 patients undergoing LGBP over an 8-year time period, found that the incidence of sepsis has continually decreased during that time period. However, it also demonstrated a number of factors associated with and predicting postoperative sepsis. While gender and preoperative BMI were not associated with poor outcomes, increased age and preoperative hypertension, diabetes, smoking, and the lifetime quantity of smoking were significantly linked to postoperative sepsis. Patients having postoperative sepsis also had a higher Charlson Comorbidity Index. The treatment or prevention of many of these factors, specifically hypertension, diabetes, and the related CCI, is the reason that many patients actually undergo the operation. While these comorbidities increase a patient’s risk of surgery, they are also related to morbidity and mortality if no surgery is performed and they are not treated. Preoperative patient optimization and risk reduction should be a priority for patients and surgeons, especially for elective surgery. Although there is no direct link between hypertension and sepsis reported in the surgical literature, there is a multitude of evidence that comorbid patients are at increased risk of postoperative complications [2–4, 16]. In our study, hypertensive patients requiring anti-hypertensive
Year
Lap gastric bypass patients (n)
% of patients developing sepsis
2006
4546
1.36
2007
6297
0.95
2008
8215
0.83
2009
9728
0.90
2010
9786
0.79
2011
9477
0.71
2012 2013
9635 9154
0.64 0.68
The number of patients developing sepsis decreased significantly (p \ 0.001). Lap laparoscopic
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Surg Endosc Table 2 Characteristics of the postoperative sepsis and no sepsis groups following laparoscopic gastric bypass
Sepsis (n = 546)
No sepsis (n = 66,292)
p value
Age (years)
47.5 ± 11.4
44.9 ± 11.5
\0.0001*
Male gender
23 %
20.3 %
BMI (kg/m )
47.4 ± 8.9
46.7 ± 8.2
Diabetes
39.6 %
30.6 %
\0.0001*
Hypertension
65.2 %
54 %
\0.0001*
Smokers
16.7 %
11.5 %
0.0002
Pack-years
8.6 ± 18.3
5.6 ± 14.2
0.0006*
CCI score
0.51 ± 0.74
0.35 ± 0.57
\0.0001*
Operative time (minutes) Length of stay (days)
161 ± 78 10.8 ± 14.7
135 ± 56 2.4 ± 4.8
\0.0001* \0.0001*
30-day mortality
4.03 %
0.11 %
\0.0001*
Demographics
2
0.1173 0.0880
Operative details
Postoperative complications Superficial wound infection
12.3 %
1.61 %
\0.0001*
UTI
12.27 %
0.78 %
\0.0001*
Pneumonia
18.86 %
0.34 %
\0.0001*
Myocardial infarction
1.28 %
0.06 %
\0.0001*
DVT
0.92 %
0.06 %
\0.0001*
PE
1.83 %
0.19 %
\0.0001*
Readmission
63.68 %
5.83 %
\0.0001*
Return to OR
58.61 %
2.17 %
\0.0001*
* Represents significant p value \0.05
Table 3 Multivariate logistic regression analysis for sepsis predictors
Smoking
Odds ratio
95 % Confidence interval
1.625
1.233–2.142
p value 0.0006*
Pack-years
1.007
1.001–1.013
0.0307*
Diabetes
1.281
1.053–1.557
0.0133*
Hypertension requiring medication
1.315
1.030–1.677
0.0277*
Operative time (per minute)
1.006
1.004–1.007
\0.0001*
* Represents significant p value \ 0.05. * Controlling for age, race, gender, BMI, and CCI score. For diabetics, CCI was omitted and age, race, gender, BMI, smoking status, hypertension and COPD were used
therapy had a 32 % increased risk of developing postoperative sepsis, which is likely a representation of these comorbid patients’ increased risk of complications (p = 0.02). This finding is supported by the work of Gupta et al., they found that preoperative hypertension increased the risk of postoperative complications by 34 % in bariatric surgery patients (OR 1.34, 95 % CI 1.10–1.63) [4]. Additionally, diabetes was found to be an independent risk factor for the development of sepsis. In our study, diabetics had a 28 % increased risk of developing postoperative sepsis when compared to non-diabetics, again a reflection of the complexity of these comorbid patients (p = 0.0133). A multitude of publications in the general surgery literature have supported this conclusion,
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namely that patients with diabetes are at increased risk of postoperative complications including wound infection and sepsis [5, 17]. Sanni et al. [5] performed an analysis of patient data from 2010 to 2011 and demonstrated that patients with diabetes doubled their risk of postoperative complications following bariatric surgery (OR 2.044, 95 % CI 1.552–2.693). A Blue Cross and Blue Shield patient database study performed using data for over 22,000 bariatric surgery patients by Steele et al. [18] found that diabetics were at increased risk of cardiac (OR 1.7, p = 0.001), infectious (OR 1.8, p = 0.001), and renal complications (OR 4.6, p = 0.01) when compared to case-matched controls in the year following their bariatric procedure. NSQIP does not include a variable for measuring
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HbA1C; therefore, it is not possible to investigate the impact of preoperative glycemic control on surgical outcomes in this dataset. There are data suggesting that close preoperative glucose control can improve infection and wound complication outcomes [19] with a HbA1C of\7.2 marking a goal for patients with a resultant significant decrease in postsurgical morbidity. Further research will be necessary to assess the influence of tight glycemic control and management of hypertension on bariatric surgical outcomes. Smoking is another controllable comorbid factor that has been linked to many poor surgical outcomes including increased length of stay, wound complications, and sepsis in bariatric surgery patients [20–22]. Padwal et al. [20] were able to link smoking to increased risk of 10-year all-cause mortality in obese patients eligible for bariatric surgery (OR 1.62, 95 % CI 1.28–2.06; p value \ 0.05). Marchini et al. [21] demonstrated that smoking was a predictor for increased length of stay following bariatric surgery (p \ 0.01). Our data revealed that smokers were at 63 % increased risk of postoperative sepsis (OR 1.625, 95 % CI 1.2330–2.142, p = 0.0006). As pack-year smoking history increased, patients were at increased risk of sepsis (OR 1.007, 95 % CI 1.001–1.013; p value = 0.0307); interestingly, there was a 1 % increased risk of sepsis for each additional pack-year. It is evident that smoking and lifetime quantity of smoking prior to elective surgery lead to an increased risk of complications, and smoking must therefore be strongly discouraged. NSQIP defines an active smoker as someone who has smoked cigarettes within the past year. This definition raises an interesting question of the optimal timing for preoperative smoking cessation. Traditionally, surgeons have recommended smoking cessation for a 30- to 90-day preoperative time period; however, this recommendation is largely anecdotal [23]. One randomized controlled trial conducted on colorectal surgery patients revealed that there was no difference in outcomes for patients who successfully engaged in short-term smoking cessation (defined as \3 weeks) [24]. In another randomized controlled trial of smoking cessation 6–8 weeks prior to surgery in hip and knee replacement patients, wound-related complications decreased from 31 to 5 % in the smoking cessation intervention group (p = 0.001) [25]. Reinbold et al. [26] suggested that urine cotinine testing should be considered for all smokers attempting preoperative smoking cessation as up to 10 % of patients may continue to smoke despite proclaiming abstinence and will need more time to attempt cessation prior to scheduling surgery. The ASMBS guidelines state that cigarette smoking is linked to increased risk of postoperative marginal ulceration and pneumonia and recommend cessation of smoking at any time before surgery even it is within 6 weeks of the operation (https:// asmbs.org/resources/clinical-practice-guidelines-for-the-
perioperative-nutritional-metabolic-and-nonsurgical-supportof-the-bariatric-surgery-patient). In our practice, we often perform preoperative cotinine testing prior to elective surgery in active smokers. Further investigation is necessary to prove the validity of optimal timing required for preoperative smoking cessation. Operative time is related to the incidence of sepsis; even when controlling for other factors with multivariate analysis, it remains strongly associated. Indeed, for every 30 min of operative time, the risk of sepsis increases by 19 % (p \ 0.0001). This particular finding has not been previously reported, though increased operative time can serve as a general marker for increased overall complications [27, 28]. While anesthesia time may play some role in outcomes, sepsis may not be the result of the actual surgical time. Longer operative time may be related to the events in the operative room that require additional effort to complete the surgery. Efficiency in the OR and ability to avoid technical complications are important. Access to care and availability of surgical services for highly comorbid patients is becoming more difficult as insurance companies are pushing toward outcome-based reimbursement [29, 30]. There is a debate concerning whether smokers should be refused elective surgery all together. Bariatric surgery is particularly fraught with controversy as many patients are being offered surgery specifically to correct their preoperative comorbidities. As reported above, LGBP surgery has demonstrated successful and sustained reduction in diabetes and hypertension postoperatively. Some authors suggest that in order to reconcile the increased risk of surgical complications in this comorbid patient population, surgery should be offered earlier to morbidly obese patients prior to the development of diabetes, hypertension, and their resultant complications [31]. Surgeons must balance tighter control of diabetes and hypertension preoperatively with the risks and benefits of surgery in an effort to best control these comorbidities over the life of the patient. While this requires a very delicate balance, it is evident that smoking cessation must be encouraged and possibly mandatory in bariatric patients both pre- and postoperatively to further improve surgical outcomes.
Conclusion Postoperative sepsis develops after 0.82 % of elective laparoscopic gastric bypass procedures. When it occurs, it portends a 30 times greater chance of death. Current smoking status, hypertension requiring medication, diabetes, increased operative time, and stepwise increase in pack-years are independently associated with an increased chance of postoperative sepsis. Modifiable risk factors
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contribute significantly to morbidity in bariatric surgery; therefore, cessation of smoking and optimization of other risk factors should be strongly advocated before elective bariatric surgery. Compliance with Ethical Standards Disclosures Drs. Heniford, Augenstein, and Lincourt have previously been awarded surgical research and education grants from W.L. Gore and Associates, Ethicon, Novadaq, Bard/Davol, and LifeCell Inc. Vedra A. Augenstein MD, FACS, has previously been awarded surgical research and education grants from Bard, Ethicon and Lifecell. L. J. Blair, C. R. Huntington, T. C. Cox, T. Prasad, A. E. Lincourt, and K. S. Gersin have no potential conflict or disclosures relevant to this work.
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12. Sundararajan V, Henderson T, Perry C, Muggivan A, Quan H, Ghali WA (2004) New ICD-10 version of the Charlson comorbidity index predicted in-hospital mortality. J Clin Epidemiol 57(12):1288–1294 13. D’Hoore W, Bouckaert A, Tilquin C (1996) Practical considerations on the use of the Charlson comorbidity index with administrative data bases. J Clin Epidemiol 49(12): 1429–1433 14. Ehlert BA, Durham CA, Parker FM, Bogey WM, Powell CS, Stoner MC (2011) Impact of operative indication and surgical complexity on outcomes after thoracic endovascular aortic repair at National Surgical Quality Improvement Program Centers. J Vasc Surg 54(6):1629–1636 15. Bergman S, Martelli V, Monette M, Sourial N, Deban M, Hamadani F et al (2013) Identification of quality of care deficiencies in elderly surgical patients by measuring adherence to process-based quality indicators. J Am Coll Surg 217(5):858–866 16. Cawley J, Sweeney MJ, Kurian M, Beane S (2007) Predicting complications after bariatric surgery using obesity-related comorbidities. Obes Surg 17(11):1451–1456 17. Ramos M, Khalpey Z, Lipsitz S, Steinberg J, Panizales MT, Zinner M et al (2008) Relationship of perioperative hyperglycemia and postoperative infections in patients who undergo general and vascular surgery. Ann Surg 248(4):585–591 18. Steele KE, Prokopowicz GP, Chang HY, Richards T, Clark JM, Weiner JP et al (2012) Risk of complications after bariatric surgery among individuals with and without type 2 diabetes mellitus. Surg Obes Relat Dis Off J Am Soc Bariatr Surg 8(3):305–330 19. Colavita PD, Zemlyak AY, Burton PV, Dacey KT, Walters AL, Lincourt AE, Tsirline VE, Kercher KW, Heniford BT (eds) (2013) The expansive cost of wound complications after ventral hernia repair. American College of Surgeons, Washington 20. Padwal RS, Klarenbach SW, Wang X, Sharma AM, Karmali S, Birch DW et al (2013) A simple prediction rule for all-cause mortality in a cohort eligible for bariatric surgery. JAMA Surg 148(12):1109–1115 (Epub 2013/10/18) 21. Marchini JF, Souza FL, Schmidt A, Cunha SF, Salgado W Jr, Marchini JS et al (2012) Low educational status, smoking, and multidisciplinary team experience predict hospital length of stay after bariatric surgery. Nutr Metab Insights 5:71–76 (Epub 2012/01/01) 22. Lent MR, Hayes SM, Wood GC, Napolitano MA, Argyropoulos G, Gerhard GS et al (2013) Smoking and alcohol use in gastric bypass patients. Eat Behav 14(4):460–463 (Epub 2013/11/05) 23. Lindstrom D, Sadr Azodi O, Wladis A, Tonnesen H, Linder S, Nasell H et al (2008) Effects of a perioperative smoking cessation intervention on postoperative complications: a randomized trial. Ann Surg 248(5):739–745 (Epub 2008/10/25) 24. Sørensen LT, Jørgensen T (2003) Short-term pre-operative smoking cessation intervention does not affect postoperative complications in colorectal surgery: a randomized clinical trial. Colorectal Dis 5(4):347–352 25. Moller AM, Villebro N, Pedersen T, Tonnesen H (2002) Effect of preoperative smoking intervention on postoperative complications: a randomised clinical trial. Lancet 359(9301):114–117 (Epub 2002/01/26) 26. Reinbold C, Rausky J, Binder JP, Revol M (2014) Urinary cotinine testing as pre-operative assessment of patients undergoing free flap surgery. Ann Chir Plast Esthet. 2Epub pii: S02941260(14)00191-5. doi:10.1016/j.anplas.2014.10.002. (Epub ahead of print) 27. Catanzarite T, Saha S, Pilecki MA, Kim JY, Milad MP (2015) Longer operative time during benign laparoscopic and robotic hysterectomy is associated with increased 30-day perioperative
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30. Hong CS, Atlas SJ, Chang Y, Subramanian SV, Ashburner JM, Barry MJ et al (2010) Relationship between patient panel characteristics and primary care physician clinical performance rankings. JAMA 304(10):1107–1113 31. Sugerman HJ, Wolfe LG, Sica DA, Clore JN (2003) Diabetes and hypertension in severe obesity and effects of gastric bypass-induced weight loss. Ann Surg 237(6):751–756 (discussion 7–8)
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and Other Interventional Techniques
Risk factors for postoperative sepsis in laparoscopic gastric bypass L. J. Blair1 • C. R. Huntington1 • T. C. Cox1 • T. Prasad1 • A. E. Lincourt1 K. S. Gersin1 • B. T. Heniford1 • V. A. Augenstein1
•
Received: 15 February 2015 / Accepted: 17 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Introduction Postoperative sepsis is a rare but serious complication following elective surgery. The purpose of this study was to identify the rate of postoperative sepsis following elective laparoscopic gastric bypass (LGBP) and to identify patients’ modifiable, preoperative risk factors. Methods The American College of Surgeons National Surgical Quality Improvement Program database was queried from 2005 to 2013 for factors associated with the development of postoperative sepsis following elective LGBP. Patients who developed sepsis were compared to those who did not. Results were analyzed using the Chisquare test for categorical variables and Wilcoxon twosample test for continuous variables. A multivariate logistic regression analysis was utilized to calculate adjusted odds ratios for factors contributing to sepsis. Results During the study period, 66,838 patients underwent LGBP. Of those, 546 patients developed postoperative sepsis (0.82 %). The development of sepsis was associated with increased operative time (161 ± 77.8 vs. 135.10 ± 56.5 min; p \ 0.0001) and a greater number of preoperative comorbidities, including diabetes (39.6 vs. 30.6 %; p \ 0.0001), hypertension requiring medication
Presented at the SAGES 2015 Annual Meeting, April 15–18, 2015, Nashville, Tennessee. & V. A. Augenstein [email protected] L. J. Blair [email protected] 1
Division of Gastrointestinal and Minimally Invasive Surgery, Department of Surgery, Carolinas Medical Center, 1025 Morehead Medical Drive, Suite 300, Charlotte, NC 28204, USA
(65.2 vs. 54 %; p \ 0.0001), current tobacco use (16.7 vs. 11.5 %; p = 0.0002), and increased pack-year history of smoking (8.6 ± 18.3 vs. 5.6 ± 14.2; p = 0.0006), and the Charlson Comorbidity Index (0.51 ± 0.74 vs. 0.35 ± 0.57, p \ 0.0001). Sepsis resulted in an increased length of stay (10.1 ± 14.4 vs. 2.4 ± 4.8 days; p \ 0.0001) and a 30 times greater chance of 30-day mortality (4.03 vs. 0.11 %, p \ 0.0001). Multivariate logistic regression analysis showed that current smokers had a 63 % greater chance of developing sepsis compared to non-smokers, controlling for age, race, gender, BMI, and CCI score (OR 1.63, 95 % CI 1.23–2.14; p = 0.0006). Conclusions Laparoscopic gastric bypass is uncommonly associated with postoperative sepsis. When it occurs, it portends a 30 times increased risk of death. A patient history of diabetes, hypertension, and increasing packyears of smoking portend an increased risk of sepsis. Current smoking status, a preoperative modifiable risk factor, is independently associated with the chance of postoperative sepsis. Preoperative patient optimization and risk reduction should be a priority for elective surgery, and patients should be encouraged to stop smoking prior to gastric bypass. Keywords Bariatric surgery Gastric bypass NSQIP Complications Mortality Smoking
Currently, obesity affects over 35 % of adults in the USA, with 69 % of the population reported to be overweight [1]. The obesity epidemic has continued to increase dramatically in more recent years with no signs of improvement, which makes this health issue one of the largest associated preventable causes of death facing the US population today [2]. When compared to supervised medical weight-loss
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programs, bariatric surgery has been shown to be the only treatment option that has provided sustainable, long-term weight loss [3]. Worldwide, bariatric surgery is commonly performed and rates are increasing annually. In 2008, 344,221 bariatric surgery operations were performed by 4680 bariatric surgeons across the globe, with 60 % of these operations being performed in North America [4]. With the increasing prevalence of obesity and its surgical correction, it is important to monitor the operative complication and mortality rates to maintain rigorous standards of quality and safety for this elective procedure. Reported rates of morbidity and mortality of this complex surgery range from 9 to 25 % and 0.1 to 2 %, respectively, and have decreased significantly since the first reports of laparoscopic gastric bypass [5]. Kelles et al. [6] estimated that 53.7 % of deaths following bariatric surgery were attributable to early or late complications, and among these, the most common cause of mortality was postoperative sepsis at 42.7 %. While postoperative sepsis and death are now rare, study of their source and control of those causes that are preventable remains important. Considering the infrequency with which these complications occur, a large, multi-institutional patient source would be required to adequately discern possible common, preventable factors. A nationwide study would be appropriate, and, to our knowledge, an epidemiologic review focusing on postoperative sepsis following laparoscopic gastric bypass has not been described. If patient risk factors can be identified, this list can be utilized by surgeons to preoperatively identify patients who may require further optimization and counseling. The purpose of this study was to identify the rate of postoperative sepsis following elective laparoscopic gastric bypass and to identify pertinent and modifiable risk factors for the development of sepsis.
Methods Data collection The American College of Surgeons National Surgical Quality Improvement Program (NSQIP) database was queried from 2005 to 2013. This database includes prospectively collected data from over 400 hospitals across the USA entered by trained reviewers beginning in the preoperative period and continuing 30 days postoperatively (acsnsqip.org). Demographic information, comorbidities, procedural data, and postoperative complications within 30 days are collected by trained data abstractors, supplemented as necessary with additional questions addressed to treating physicians and follow-up calls to patients.
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Study design The NSQIP database was queried for all elective laparoscopic gastric bypasses performed from 2005 to 2013 as determined by current procedural terminology codes 43644 and 43645. Patients under age 18 and cases coded as ‘‘emergent’’ were excluded. Variables are clearly described in the ACS NSQIP data dictionary. Smokers are defined as patients who have smoked cigarettes in the year prior to admission for surgery and do not include other tobacco products (NSQIP Data Dictionary, acsnsqip.org). NSQIP variables and outcomes NSQIP records over 30 patient comorbidities but does not include a global comorbidity scale on which to rate patients such as the Charlson Comorbidity Index (CCI) [7]. The CCI is one such scoring system that has been extensively validated in surgery patients [8–10]. The authors used available NSQIP data to create a NSQIP Charlson Comorbidity Index which has previously been published [11], where comorbidities are scored as points according to the original CCI. Previous studies have verified that CCI adapted to large administrative databases have had similar sensitivity in stratifying mortality [12, 13], and this strategy has been used in NSQIP in previous studies [14, 15]. The primary outcome of interest for this study was postoperative sepsis. Statistical analysis Patients who developed sepsis following this procedure were compared to those who did not using the Chi-square test for categorical variables and Wilcoxon two-sample test for continuous variables. Primary risk factors for developing sepsis were identified from univariate analyses. These risk factors were each then used as the primary predictor in separate multiple logistic regression models for estimating the odds of developing sepsis while controlling for age, race, gender, BMI, and CCI score. The Hosmer–Lemeshow test was used to check the goodness of fit of the multiple logistic regression models. Statistical significance was set at p B 0.05, and all reported p values are two-tailed. All data were analyzed using Statistical Analysis Software, version 9.4 (SAS Institute, Inc., Cary, NC).
Results During the study period, 66,838 patients underwent laparoscopic gastric bypass. Of those, 546 patients developed postoperative sepsis overall (0.82 %). The rates of the
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development of sepsis gradually but significantly declined over the study period p \ 0.0001 (Table 1). Patient demographics and comorbidities are compared and demonstrated in Table 2. Specifically, the development of sepsis was associated with increased age (47.5 ± 11.4 vs. 44.9 ± 11.5 years; p \ 0.0001) and operative time (161 ± 77.8 vs. 135.10 ± 56.5 min; p \ 0.0001), and greater number of preoperative comorbidities including diabetes (39.6 vs. 30.6 %; p \ 0.0001), hypertension requiring medication (65.2 vs. 54 %; p \ 0.0001), current tobacco use (16.7 vs. 11.5 %; p = 0.0002), and increased pack-year smoking history (8.6 ± 18.3 vs. 5.6 ± 14.2; p = 0.0006). CCI was also strongly associated with the incidence of postoperative sepsis (0.51 ± 0.74 vs. 0.35 ± 0.57, p \ 0.0001). As would be expected, the rate of reoperation was dramatically higher in the septic patients (58.6 vs. 2.2 %, p \ 0.0001). Rates of other postoperative complications were significantly elevated in the sepsis group including wound infection, UTI, pneumonia, myocardial infarction, DVT, and PE (p \ 0.0001). There was over a 30 times greater chance of 30-day mortality for patients who developed sepsis (4.03 vs. 0.11 %, p \ 0.0001). Length of stay was also significantly greater in the sepsis group (10.1 ± 14.4 vs. 2.4 ± 4.8 days; p \ 0.0001) as was the incidence of readmission (63.7 vs. 5.8 %, p \ 0.0001). Multiple logistic regression analysis showed that current smokers had a 63 % greater chance of developing sepsis compared to non-smokers, controlling for age, race, gender, BMI, and CCI score (OR 1.63, 95 % CI 1.23–2.14; p value = 0.0006) (Table 3). Although statistical analysis did not reveal a direct association between smoking and mortality, the development of postoperative sepsis was found to have a 38 times greater chance of 30-day mortality (OR 38.08, 95 % CI 23.46–61.81; p value \ 0.0001). Moreover, as pack-year smoking history increased, patients were at increased risk of sepsis (OR 1.007, 95 % CI 1.001–1.013; p value = 0.0307); interestingly, there was a 1 % increased risk of sepsis for each additional pack-year. Hypertensive patients who require medication to control Table 1 Percentage of patients developing sepsis following laparoscopic gastric bypass by year
their disease (OR 1.315, 95 % CI 1.030–1.677; p value = 0.0277) and diabetic patients were at an increased risk of developing sepsis (OR 1.281, 95 % CI 1.053–1.557; p value = 0.0133). Increased operative time was also a predictor for sepsis (OR 1.006, 95 % CI 1.004–1.007; p value \ 0.0001). An incremental increase in postoperative sepsis risk was seen with every 30 min of additional operative time; each half hour added an 18 % risk (p \ 0.0001).
Discussion Postoperative sepsis is a rare but devastating complication of elective surgery that leads to a significantly increased risk of 30-day mortality. This study, which examines the outcomes of over 66,000 patients undergoing LGBP over an 8-year time period, found that the incidence of sepsis has continually decreased during that time period. However, it also demonstrated a number of factors associated with and predicting postoperative sepsis. While gender and preoperative BMI were not associated with poor outcomes, increased age and preoperative hypertension, diabetes, smoking, and the lifetime quantity of smoking were significantly linked to postoperative sepsis. Patients having postoperative sepsis also had a higher Charlson Comorbidity Index. The treatment or prevention of many of these factors, specifically hypertension, diabetes, and the related CCI, is the reason that many patients actually undergo the operation. While these comorbidities increase a patient’s risk of surgery, they are also related to morbidity and mortality if no surgery is performed and they are not treated. Preoperative patient optimization and risk reduction should be a priority for patients and surgeons, especially for elective surgery. Although there is no direct link between hypertension and sepsis reported in the surgical literature, there is a multitude of evidence that comorbid patients are at increased risk of postoperative complications [2–4, 16]. In our study, hypertensive patients requiring anti-hypertensive
Year
Lap gastric bypass patients (n)
% of patients developing sepsis
2006
4546
1.36
2007
6297
0.95
2008
8215
0.83
2009
9728
0.90
2010
9786
0.79
2011
9477
0.71
2012 2013
9635 9154
0.64 0.68
The number of patients developing sepsis decreased significantly (p \ 0.001). Lap laparoscopic
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Surg Endosc Table 2 Characteristics of the postoperative sepsis and no sepsis groups following laparoscopic gastric bypass
Sepsis (n = 546)
No sepsis (n = 66,292)
p value
Age (years)
47.5 ± 11.4
44.9 ± 11.5
\0.0001*
Male gender
23 %
20.3 %
BMI (kg/m )
47.4 ± 8.9
46.7 ± 8.2
Diabetes
39.6 %
30.6 %
\0.0001*
Hypertension
65.2 %
54 %
\0.0001*
Smokers
16.7 %
11.5 %
0.0002
Pack-years
8.6 ± 18.3
5.6 ± 14.2
0.0006*
CCI score
0.51 ± 0.74
0.35 ± 0.57
\0.0001*
Operative time (minutes) Length of stay (days)
161 ± 78 10.8 ± 14.7
135 ± 56 2.4 ± 4.8
\0.0001* \0.0001*
30-day mortality
4.03 %
0.11 %
\0.0001*
Demographics
2
0.1173 0.0880
Operative details
Postoperative complications Superficial wound infection
12.3 %
1.61 %
\0.0001*
UTI
12.27 %
0.78 %
\0.0001*
Pneumonia
18.86 %
0.34 %
\0.0001*
Myocardial infarction
1.28 %
0.06 %
\0.0001*
DVT
0.92 %
0.06 %
\0.0001*
PE
1.83 %
0.19 %
\0.0001*
Readmission
63.68 %
5.83 %
\0.0001*
Return to OR
58.61 %
2.17 %
\0.0001*
* Represents significant p value \0.05
Table 3 Multivariate logistic regression analysis for sepsis predictors
Smoking
Odds ratio
95 % Confidence interval
1.625
1.233–2.142
p value 0.0006*
Pack-years
1.007
1.001–1.013
0.0307*
Diabetes
1.281
1.053–1.557
0.0133*
Hypertension requiring medication
1.315
1.030–1.677
0.0277*
Operative time (per minute)
1.006
1.004–1.007
\0.0001*
* Represents significant p value \ 0.05. * Controlling for age, race, gender, BMI, and CCI score. For diabetics, CCI was omitted and age, race, gender, BMI, smoking status, hypertension and COPD were used
therapy had a 32 % increased risk of developing postoperative sepsis, which is likely a representation of these comorbid patients’ increased risk of complications (p = 0.02). This finding is supported by the work of Gupta et al., they found that preoperative hypertension increased the risk of postoperative complications by 34 % in bariatric surgery patients (OR 1.34, 95 % CI 1.10–1.63) [4]. Additionally, diabetes was found to be an independent risk factor for the development of sepsis. In our study, diabetics had a 28 % increased risk of developing postoperative sepsis when compared to non-diabetics, again a reflection of the complexity of these comorbid patients (p = 0.0133). A multitude of publications in the general surgery literature have supported this conclusion,
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namely that patients with diabetes are at increased risk of postoperative complications including wound infection and sepsis [5, 17]. Sanni et al. [5] performed an analysis of patient data from 2010 to 2011 and demonstrated that patients with diabetes doubled their risk of postoperative complications following bariatric surgery (OR 2.044, 95 % CI 1.552–2.693). A Blue Cross and Blue Shield patient database study performed using data for over 22,000 bariatric surgery patients by Steele et al. [18] found that diabetics were at increased risk of cardiac (OR 1.7, p = 0.001), infectious (OR 1.8, p = 0.001), and renal complications (OR 4.6, p = 0.01) when compared to case-matched controls in the year following their bariatric procedure. NSQIP does not include a variable for measuring
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HbA1C; therefore, it is not possible to investigate the impact of preoperative glycemic control on surgical outcomes in this dataset. There are data suggesting that close preoperative glucose control can improve infection and wound complication outcomes [19] with a HbA1C of\7.2 marking a goal for patients with a resultant significant decrease in postsurgical morbidity. Further research will be necessary to assess the influence of tight glycemic control and management of hypertension on bariatric surgical outcomes. Smoking is another controllable comorbid factor that has been linked to many poor surgical outcomes including increased length of stay, wound complications, and sepsis in bariatric surgery patients [20–22]. Padwal et al. [20] were able to link smoking to increased risk of 10-year all-cause mortality in obese patients eligible for bariatric surgery (OR 1.62, 95 % CI 1.28–2.06; p value \ 0.05). Marchini et al. [21] demonstrated that smoking was a predictor for increased length of stay following bariatric surgery (p \ 0.01). Our data revealed that smokers were at 63 % increased risk of postoperative sepsis (OR 1.625, 95 % CI 1.2330–2.142, p = 0.0006). As pack-year smoking history increased, patients were at increased risk of sepsis (OR 1.007, 95 % CI 1.001–1.013; p value = 0.0307); interestingly, there was a 1 % increased risk of sepsis for each additional pack-year. It is evident that smoking and lifetime quantity of smoking prior to elective surgery lead to an increased risk of complications, and smoking must therefore be strongly discouraged. NSQIP defines an active smoker as someone who has smoked cigarettes within the past year. This definition raises an interesting question of the optimal timing for preoperative smoking cessation. Traditionally, surgeons have recommended smoking cessation for a 30- to 90-day preoperative time period; however, this recommendation is largely anecdotal [23]. One randomized controlled trial conducted on colorectal surgery patients revealed that there was no difference in outcomes for patients who successfully engaged in short-term smoking cessation (defined as \3 weeks) [24]. In another randomized controlled trial of smoking cessation 6–8 weeks prior to surgery in hip and knee replacement patients, wound-related complications decreased from 31 to 5 % in the smoking cessation intervention group (p = 0.001) [25]. Reinbold et al. [26] suggested that urine cotinine testing should be considered for all smokers attempting preoperative smoking cessation as up to 10 % of patients may continue to smoke despite proclaiming abstinence and will need more time to attempt cessation prior to scheduling surgery. The ASMBS guidelines state that cigarette smoking is linked to increased risk of postoperative marginal ulceration and pneumonia and recommend cessation of smoking at any time before surgery even it is within 6 weeks of the operation (https:// asmbs.org/resources/clinical-practice-guidelines-for-the-
perioperative-nutritional-metabolic-and-nonsurgical-supportof-the-bariatric-surgery-patient). In our practice, we often perform preoperative cotinine testing prior to elective surgery in active smokers. Further investigation is necessary to prove the validity of optimal timing required for preoperative smoking cessation. Operative time is related to the incidence of sepsis; even when controlling for other factors with multivariate analysis, it remains strongly associated. Indeed, for every 30 min of operative time, the risk of sepsis increases by 19 % (p \ 0.0001). This particular finding has not been previously reported, though increased operative time can serve as a general marker for increased overall complications [27, 28]. While anesthesia time may play some role in outcomes, sepsis may not be the result of the actual surgical time. Longer operative time may be related to the events in the operative room that require additional effort to complete the surgery. Efficiency in the OR and ability to avoid technical complications are important. Access to care and availability of surgical services for highly comorbid patients is becoming more difficult as insurance companies are pushing toward outcome-based reimbursement [29, 30]. There is a debate concerning whether smokers should be refused elective surgery all together. Bariatric surgery is particularly fraught with controversy as many patients are being offered surgery specifically to correct their preoperative comorbidities. As reported above, LGBP surgery has demonstrated successful and sustained reduction in diabetes and hypertension postoperatively. Some authors suggest that in order to reconcile the increased risk of surgical complications in this comorbid patient population, surgery should be offered earlier to morbidly obese patients prior to the development of diabetes, hypertension, and their resultant complications [31]. Surgeons must balance tighter control of diabetes and hypertension preoperatively with the risks and benefits of surgery in an effort to best control these comorbidities over the life of the patient. While this requires a very delicate balance, it is evident that smoking cessation must be encouraged and possibly mandatory in bariatric patients both pre- and postoperatively to further improve surgical outcomes.
Conclusion Postoperative sepsis develops after 0.82 % of elective laparoscopic gastric bypass procedures. When it occurs, it portends a 30 times greater chance of death. Current smoking status, hypertension requiring medication, diabetes, increased operative time, and stepwise increase in pack-years are independently associated with an increased chance of postoperative sepsis. Modifiable risk factors
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contribute significantly to morbidity in bariatric surgery; therefore, cessation of smoking and optimization of other risk factors should be strongly advocated before elective bariatric surgery. Compliance with Ethical Standards Disclosures Drs. Heniford, Augenstein, and Lincourt have previously been awarded surgical research and education grants from W.L. Gore and Associates, Ethicon, Novadaq, Bard/Davol, and LifeCell Inc. Vedra A. Augenstein MD, FACS, has previously been awarded surgical research and education grants from Bard, Ethicon and Lifecell. L. J. Blair, C. R. Huntington, T. C. Cox, T. Prasad, A. E. Lincourt, and K. S. Gersin have no potential conflict or disclosures relevant to this work.
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