Risk Factors of Surgical Site Infection after Hepatic Resection Author(s): Tian Yang, MD; Ping-An Tu, MD; Han Zhang, MD; Jun-Hua Lu, MD; Yi-Nan Shen, MD; Shou-Xin Yuan, MD; Wan Yee Lau, MD, FRCS, FACS, FRACS (Hon); Eric C. H. Lai, MBChB, MRCSEd, FRACS; Chong-De Lu, MD; Meng-Chao Wu, MD; Jie-Wei Li, MD, PhD; Feng Shen, MD, PhD Source: Infection Control and Hospital Epidemiology, Vol. 35, No. 3 (March 2014), pp. 317-320 Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiology of America
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infection control and hospital epidemiology
march 2014, vol. 35, no. 3
concise communication
Risk Factors of Surgical Site Infection after Hepatic Resection Tian Yang, MD;1,a Ping-An Tu, MD;1,a Han Zhang, MD;1,a Jun-Hua Lu, MD;1 Yi-Nan Shen, MD;1 Shou-Xin Yuan, MD;1 Wan Yee Lau, MD, FRCS, FACS, FRACS (Hon);1,2 Eric C. H. Lai, MBChB, MRCSEd, FRACS;1,2 Chong-De Lu, MD;1 Meng-Chao Wu, MD;1 Jie-Wei Li, MD, PhD;1 Feng Shen, MD, PhD1
A study of 7,388 consecutive patients after hepatic resection between 2011 and 2012 identified hepatolithiasis, cirrhosis, and intraoperative blood transfusion as the only independent risk factors of both incisional and organ/space surgical site infection (SSI). Patients with these conditions should be cared for with caution to lower SSI rates. Infect Control Hosp Epidemiol 2014;35(3):317-320
Advances in surgical techniques and devices as well as improvements in perioperative care have significantly reduced in-hospital mortality after hepatic resection, whereas postoperative morbidity remains high.1,2 Surgical site infection (SSI), including incisional and organ/space SSI,3 is the most common but potentially preventable complication after hepatic resection.4-8 SSI following hepatic resection can be devastating, requiring surgical debridement(s), aggravating postoperative hepatic failure, and occasionally leading to postoperative mortality. Early identification of risk factors of SSI after hepatic resection is the first step to help improve perioperative outcomes. Hepatic resection is the most effective treatment method for hepatolithiasis,9,10 which is prevalent in Southeast Asia but rare in Western countries. However, SSI is the most common postoperative complication for it.9,11 Thus, it is worthwhile to determine whether hepatolithiasis is an independent risk factor of SSI after hepatic resection. This prospective study was conducted on a large cohort of patients undergoing hepatic resection to study the risk factors of overall, incisional, and organ/space SSI.
attack of bacterial cholangitis or cholecystitis or liver abscess within 2 weeks prior to the operation. Data were prospectively collected and entered into a computer database. Approval for this study was obtained from the ethics committee of the hospital. Perioperative Care and Surgical Procedures The criteria used for hepatic resection and perioperative care were consistent throughout the study period and have been reported in a previous study.12 There was no preoperative shaving. Abdominal incisions were closed with nonabsorbable sutures. Local antibiotics and subcutaneous drains were not used on the wounds. Intravenous prophylactic antibiotic, either broad-spectrum penicillin or first- or second-generation cephalosporins, were uniformly given at a dosage of 1–2 g intravenously at induction of anesthesia, followed by an additional dose intravenously at a 3-hour intervals, as recommended by the Centers for Disease Control and Prevention guidelines.13 Postoperative prophylaxis antibiotics were continued for 1–3 days after surgery. Other perioperative cares were practically standardized. Diagnosis of SSI The standardized surveillance criteria for defining SSI—as developed by the National Nosocomial Infections Surveillance System of the Centers for Disease Control and Prevention—were used, with SSIs classified as either incisional (superficial or deep) or organ/space.3 The risk factors for SSI were collected using a standardized data collection form. Statistical Analysis The primary outcomes were incisional SSI and organ/space SSI. Statistical analysis was done using SPSS software (ver. 18.0; SPSS). Comparison between patients who developed SSI (overall, incisional, and organ/space SSI) and those who did not was done using a x2 test with Yates correction or a Fisher exact test as appropriate. For the risk factors for SSI, significant variables (P ! .10) in the univariate analyses were entered into a multivariate logistic regression model using a criterion of P ≤ .05. A level of P ! .05 was considered statistically significant.
methods
results
The study was carried out in a university-based hepatobiliary center in Shanghai, which is the largest hepatobiliary surgical center in China. Consecutive patients who underwent open hepatic resection between January 2010 and December 2011 were included in this study. Excluded from the study were patients who received laparoscopic hepatic resection, hepatic resection with concomitant biliary reconstruction or gastrointestinal surgical procedures, or those who had an acute
Patient Population Of the 7,388 consecutive patients in the study cohort, there were 5,447 men (73.7%) and 1,941 women (26.3%), with a mean age of 55.8 years (range, 2–88 years). Obesity was found in 2,016 (27.3%) patients, and 410 (5.5%) patients were underweight. The patients’ hepatobiliary diseases that required hepatic resection were hepatecellular carcinoma (5,174;
This content downloaded from 146.203.126.115 on Sat, 15 Feb 2014 09:37:02 AM All use subject to JSTOR Terms and Conditions
table 1. Univariate Analysis of Risk Factors for Surgical Site Infection (SSI) after Hepatic Resection Variable Age, years !50 ≥50 Sex Male Female Obese (BMI ≥30) Underweight (BMI !18) Comorbid illness Diabetes mellitus Cardiovascular disease Hypertension COPD Renal dysfunction Active tobacco use Repeat hepatectomy ASA score !2 ≥2 Cirrhosis Preoperative ascites HbsAg (⫹) Anti-HCV (⫹) Child-Pugh score A B⫹C Platelets !100 # 109/L ≥100 # 109/L Prothrombin time, seconds !3 ≥3 Albumin, g/L !35 ≥35 Hepatobiliary diseases Hepatolithiasis Nonhepatolithiasis Type of hepatectomya Major Minor Additional surgical procedures Cholecystotomy Splenectomy Pericardial devascularization Hilar lymph node dissection Pringle maneuver Intraoperative blood loss, mL !800 ≥800 Operative time, minutes !240 ≥240 Intraoperative blood transfusion Postoperative bile leakage Postoperative bleeding requiring reoperation Use of abdominal drainageb Length of abdominal drainage, days (n p 7,206) !5 ≥5 Postoperative antibiotic prophylaxis No Yes
No.
Overall SSI
P
Incisional SSI
P
Organ/space SSI
P
3,314 4,074
295 (8.9) 403 (9.9)
.15
166 (5.0) 243 (6.0)
.07
155 (4.7) 206 (5.0)
.45
5,447 1,941 2,016 410 1,250 571 186 489 162 65 914 711
532 166 262 45 126 73 18 48 15 6 104 83
(9.8) (8.6) (13.0) (11.0) (10.0) (12.8) (9.7) (9.8) (9.3) (9.2) (11.4) (11.7)
.12
305 104 177 32 75 49 12 28 8 4 66 60
(5.6) (5.4) (8.8) (7.8) (6.0) (8.6) (6.5) (5.7) (4.9) (6.2) (7.2) (8.4)
.69
270 91 115 22 69 34 9 25 9 3 50 37
(5.0) (4.7) (5.7) (5.4) (5.5) (6.0) (5.1) (5.1) (5.6) (4.6) (5.5) (5.2)
.64
4,802 2,586 3,885 243 4,915 185
423 275 443 27 486 18
(8.8) (10.6) (11.8) (11.1) (9.9) (9.7)
245 164 253 18 285 11
(5.1) (6.3) (6.5) (7.4) (5.8) (5.9)
211 150 242 13 250 10
(4.4) (5.8) (6.2) (5.3) (5.1) (5.4)
!.01
6,654 734
618 (9.3) 80 (10.9)
.16
356 (5.4) 53 (7.2)
.04
313 (4.7) 48 (6.5)
.03
1,595 5,793
163 (10.2) 535 (9.2)
.23
100 (6.3) 309
.15
94 (5.9) 267 (4.6)
.04
6,001 1,387
564 (9.4) 134 (9.7)
.76
330 (5.5) 79 (5.7)
.77
295 (4.9) 66 (4.8)
.81
485 6,903
58 (12.0) 640 (9.3)
.05
43 (8.9) 366 (5.3)
!.01
27 (5.5) 334 (4.8)
.47
498 6,890
92 (18.5) 606 (8.8)
!.01
64 (12.9) 345 (5.0)
!.01
55 (11.0) 306 (4.4)
1,699 5,689
161 (9.5) 537 (9.4)
.96
105 (6.2) 304 (5.3)
.19
88 (5.2) 273 (4.8)
.52
2,106 173 118 491 6,810
202 18 16 48 636
(9.6) (10.4) (13.6) (9.8) (9.3)
.79 .66 .12 .80 .27
122 11 9 34 372
.54 .63 .12 .16 .34
110 12 9 27 330
(5.2) (6.9) (7.6) (5.5) (4.8)
.40 .21 .16 .52 .58
5,855 1,533
530 (9.0) 168 (11.0)
.02
304 (5.0) 105 (7.5)
!.01
277 (4.7) 84 (5.5)
.23
5,917 1,471 1112 221 38 7,206
539 159 139 25 5 685
(9.1) (10.8) (12.5) (10.8) (13.2) (9.5)
!.05
312 97 76 13 3 401
(5.3) (6.6) (6.8) (5.9) (7.9) (5.6)
!.05
271 90 74 17 3 352
.02
5,745 1,461
524 (9.1) 161 (11.0)
.03
309 (5.4) 92 (6.3)
.17
254 (4.4) 98 (6.7)
!.01
184 7,204
17 (9.2) 681 (9.5)
.92
10 (5.4) 399 (5.5)
.95
10 (5.4) 351 (4.9)
.73
!.01
.28 .40 !.10 .91 .77 .93 .95 .03 .03 .01 !.01
.37 .07 .89
!.01
.34 .43 .28
(5.8) (6.4) (7.6) (6.9) (5. 5)
!.01
.04 .43 !.01 .58 .85 .74 .83 .02 !.01 .03 !.01 !.01
.05 .81
.04 .82 .52 .50
(4.6) (6.1) (6.7) (7.2) (7.9) (4.9)
.04 .64 .25 .22 .98 .81 .69 NS .38 .68
!.01
.73 .26 .74
!.01
!.01 !.05
.34 .97
note. Data are no. (%) of patients, unless otherwise indicated. ASA, American Society of Anesthesiologists; BMI, body mass index; COPD, chronic obstructive pulmonary disease; HCV, hepatitis C virus; NS, not significant; SSI, surgical site infection. a Major, resection of 3 or more Couinaud liver segments; minor, resection of fewer than 3 segments. b Drainage with T tube was excluded.
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ssi after hepatectomy
table 2. Multivariate Analysis of Risk Factors of Surgical Site Infection (SSI) after Hepatic Resection
Overall SSI Obesity (BMI ≥30) Diabetes mellitus ASA score ≥2 Cirrhosis Repeat hepatectomy Hepatolithiasis Length of abdominal drainage ≥5 days Intraoperative blood transfusion Incisional SSI Obesity (BMI ≥30) Diabetes mellitus Cirrhosis Hypoalbuminemia Repeat hepatectomy Hepatolithiasis Intraoperative blood transfusion Organ/space SSI ASA score ≥2 Cirrhosis Hepatolithiasis Intraoperative blood transfusion Length of abdominal drainage ≥5 days Postoperative bile leakage
OR
95% CI
P
1.62 1.43 1.35 1.55 1.15 1.75 1.49 1.57
1.25–2.09 1.07–1.90 1.03–1.74 1.34–1.80 1.03–1.31 1.42–2.13 1.34–1.77 1.32–1.98
!.01
1.55 1.35 1.61 1.19 1.17 1.58 1.32
1.30–1.97 1.18–1.65 1.35–1.94 1.03–1.58 1.03–1.32 1.32–1.99 1.10–1.68
!.01
1.42 1.70 1.66 1.71 1.27 1.22
1.14–1.80 1.41–2.12 1.46–1.97 1.45–2.11 1.07–1.54 1.03–1.49
.01 !.01 !.01 !.01 .03 .04
.03 .04 !.01 !.05 !.01 !.01 !.01
.01 !.01
.03 !.05 !.01
.01
note. ASA, American Society of Anesthesiologists; BMI, body mass index; CI, confidence interval; OR, odds ratio.
70.0%), hepatic hemangioma (548; 7.4%), and hepatolithiasis (498; 6.7%). The preoperative liver functional status was Child-Pugh A in 6,654 patients, B in 724 patients, and C in 10 patients. Repeat hepatectomy was carried out for 711 patients (9.6%). Cirrhosis as determined by postoperative histopathological examination was present in 3,885 patients (52.6%). Operative Outcomes and Incidences of SSI Among all, 103 patients died, and the mortality rate was 1.4%. For the 698 patients who developed SSI after hepatic resection, incisional and organ/space SSI was diagnosed in 409 and 361 patients, respectively (72 patients had both incisional and organ/space SSI). The incidences of overall, incisional, and organ/space SSI were 9.4%, 5.5%, and 4.9%, respectively. The median time from operation to the diagnosis of SSI was 7 days. The mean postoperative stay for patients who developed SSI was 13.6 days, which was significantly longer than the 7.2 days in those who did not develop SSI (P ! .01). Univariate and Multivariable Analyses for Risk Factors for SSI The results of univariate analysis of risk factors associated with overall, incisional, and organ/space SSI after hepatic resection are summarized in Table 1.
319
Multivariate logistic regression analysis (Table 2) identified the following 8 independent risk factors for overall SSI: obesity, diabetes mellitus, American Society of Anesthesiologists (ASA) score of 2 or greater, cirrhosis, repeat hepatectomy, hepatoliathiasis, length of abdominal drainage 5 days or longer, and intraoperative blood transfusion. The factor associated with the highest odds ratio was hepatolithiasis. In addition, obesity, diabetes mellitus, cirrhosis, hypoalbuminemia, repeat hepatectomy, hepatolithiasis, and intraoperative blood transfusion significantly predicted incisional SSI, while ASA score of 2 or greater, cirrhosis, hepatolithiasis, intraoperative blood transfusion, length of abdominal drainage 5 days or longer, and postoperative bile leakage significantly predicted organ/space SSI. Among these independent risk factors, hepatolithiasis, cirrhosis, and intraoperative blood transfusion were the only factors that were associated with both incisional and organ/space SSI.
discussion One highlight of this study is the finding that SSI after hepatic resection for hepatolithiasis is more common than for other hepatobiliary diseases on multivariate analysis. Possible explanations are recurrent attacks of acute cholangitis with bacterial colonization in the biliary system in intrahepatic lithiasis14 and the more common occurrence of postoperative bile leakage, which was identified as a risk factor for organ/space SSI by this and other studies.4,5,15,16 Another interesting and important finding in this study is the identification of cirrhosis as an independent risk factor of both incisional and organ/space SSI after hepatic resection. As far as we know, this is the first study to reveal the relationship between cirrhosis and postoperative SSI after hepatic resection. In this study, 443 (11.8%) of 3,885 cirrhotic patients developed postoperative SSI. This high prevalence of SSI in cirrhotic patients can be explained by the presence of various dysfunctions in the mechanisms of defense against infection: a decrease in function of the reticuloendothelial system and granulocytes, a decrease in complement concentrations, and a change in cell-mediated immunity.17,18 This study also found that intraoperative blood transfusion was the only surgical-related risk factor shared by both incisional and organ/space SSI after hepatic resection, which is consistent with previous studies on a variety of other operations.19,20 However, the underlying mechanism remains obscure. Measures to decrease blood loss and avoid intraoperative blood transfusions are important strategies in decreasing postoperative SSI. In conclusion, postoperative SSI was common in patients undergoing hepatic resection. High-risk groups of patients and operations were identified. In order to reduce SSI after hepatic resection, patients with hepatolithiasis or cirrhosis should be cared for with caution, and intraoperative blood loss should be kept to an absolute minimum.
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320
infection control and hospital epidemiology
march 2014, vol. 35, no. 3
acknowledgments Financial support. This work was supported by the National Natural Science Foundation of China (81000166 and 81172020), the Shanghai Program for Excellent Talents in Health System (XYQ2011033), the Foundation for Outstanding Young Scholar of Second Military Medical University, the Shanghai Rising-Star Science Foundation for Youths (12QA1404800), and the State Key Project on Infectious Diseases of China (2012ZX10002-016). 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. Affiliations: 1. Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China; 2. Faculty of Medicine, Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China; a. These authors contributed equally to this work. Address correspondence to Feng Shen, MD, PhD, Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China ([email protected]) or to Jie-Wei Li, MD, PhD, Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China ([email protected]). Received August 19, 2013; accepted November 9, 2013; electronically published January 31, 2014. 䉷 2014 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2014/3503-0019$15.00. DOI: 10.1086/675278
references 1. Cescon M, Vetrone G, Grazi GL, et al. Trends in perioperative outcome after hepatic resection: analysis of 1500 consecutive unselected cases over 20 years. Ann Surg 2009;249:995–1002. 2. Taketomi A, Kitagawa D, Itoh S, et al. Trends in morbidity and mortality after hepatic resection for hepatocellular carcinoma: an institute’s experience with 625 patients. J Am Coll Surg 2007; 204:580–587. 3. National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004;32:470–485. 4. Togo S, Matsuo K, Tanaka K, et al. Perioperative infection control and its effectiveness in hepatectomy patients. J Gastroenterol Hepatol 2007;22:1942–1948. 5. Okabayashi T, Nishimori I, Yamashita K, et al. Risk factors and predictors for surgical site infection after hepatic resection. J Hosp Infect 2009;73:47–53. 6. Kobayashi S, Gotohda N, Nakagohri T, Takahashi S, Konishi M, Kinoshita T. Risk factors of surgical site infection after hepatectomy for liver cancers. World J Surg 2009;33:312–317.
7. Uchiyama K, Ueno M, Ozawa S, et al. Risk factors for postoperative infectious complications after hepatectomy. J Hepatobiliary Pancreat Sci 2011;18:67–73. 8. Shiba H, Ishii Y, Ishida Y, et al. Assessment of blood-products use as predictor of pulmonary complications and surgical-site infection after hepatectomy for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 2009;16:69–74. 9. Yang T, Lau WY, Lai EC, et al. Hepatectomy for bilateral primary hepatolithiasis: a cohort study. Ann Surg 2010;251:84–90. 10. Tabrizian P, Jibara G, Shrager B, Schwartz ME, Roayaie S. Hepatic resection for primary hepatolithiasis: a single-center Western experience. J Am Coll Surg 2012;215:622–626. 11. Chen DW, Tung-Ping PR, Liu CL, Fan ST, Wong J. Immediate and long-term outcomes of hepatectomy for hepatolithiasis. Surgery 2004;135:386–393. 12. Yang T, Zhang J, Lu JH, et al. A new staging system for resectable hepatocellular carcinoma: comparison with six existing staging systems in a large Chinese cohort. J Cancer Res Clin Oncol 2011; 137:739–750. 13. 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. 14. Fan ST, Lai EC, Wong J. Hepatic resection for hepatolithiasis. Arch Surg 1993;128:1070–1074. 15. Arikawa T, Kurokawa T, Ohwa Y, et al. Risk factors for surgical site infection after hepatectomy for hepatocellular carcinoma. Hepatogastroenterology 2011;58:143–146. 16. Sadamori H, Yagi T, Shinoura S, et al. Risk factors for organ/ space surgical site infection after hepatectomy for hepatocellular carcinoma in 359 recent cases. J Hepatobiliary Pancreat Sci 2013; 20:186–196. 17. Schindl MJ, Millar AM, Redhead DN, et al. The adaptive response of the reticuloendothelial system to major liver resection in humans. Ann Surg 2006;243:507–514. 18. Fernandez J, Gustot T. Management of bacterial infections in cirrhosis. J Hepatol 2012;56(suppl):S1–S12. 19. Olsen MA, Lefta M, Dietz JR, et al. Risk factors for surgical site infection after major breast operation. J Am Coll Surg 2008;207: 326–335. 20. Talbot TR, D’Agata EM, Brinsko V, Lee B, Speroff T, Schaffner W. Perioperative blood transfusion is predictive of poststernotomy surgical site infection: marker for morbidity or true immunosuppressant. Clin Infect Dis 2004;38:1378–1382.
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Stable URL: http://www.jstor.org/stable/10.1086/675278 . Accessed: 15/02/2014 09:37 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp
. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].
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The University of Chicago Press and The Society for Healthcare Epidemiology of America are collaborating with JSTOR to digitize, preserve and extend access to Infection Control and Hospital Epidemiology.
http://www.jstor.org
This content downloaded from 146.203.126.115 on Sat, 15 Feb 2014 09:37:02 AM All use subject to JSTOR Terms and Conditions
infection control and hospital epidemiology
march 2014, vol. 35, no. 3
concise communication
Risk Factors of Surgical Site Infection after Hepatic Resection Tian Yang, MD;1,a Ping-An Tu, MD;1,a Han Zhang, MD;1,a Jun-Hua Lu, MD;1 Yi-Nan Shen, MD;1 Shou-Xin Yuan, MD;1 Wan Yee Lau, MD, FRCS, FACS, FRACS (Hon);1,2 Eric C. H. Lai, MBChB, MRCSEd, FRACS;1,2 Chong-De Lu, MD;1 Meng-Chao Wu, MD;1 Jie-Wei Li, MD, PhD;1 Feng Shen, MD, PhD1
A study of 7,388 consecutive patients after hepatic resection between 2011 and 2012 identified hepatolithiasis, cirrhosis, and intraoperative blood transfusion as the only independent risk factors of both incisional and organ/space surgical site infection (SSI). Patients with these conditions should be cared for with caution to lower SSI rates. Infect Control Hosp Epidemiol 2014;35(3):317-320
Advances in surgical techniques and devices as well as improvements in perioperative care have significantly reduced in-hospital mortality after hepatic resection, whereas postoperative morbidity remains high.1,2 Surgical site infection (SSI), including incisional and organ/space SSI,3 is the most common but potentially preventable complication after hepatic resection.4-8 SSI following hepatic resection can be devastating, requiring surgical debridement(s), aggravating postoperative hepatic failure, and occasionally leading to postoperative mortality. Early identification of risk factors of SSI after hepatic resection is the first step to help improve perioperative outcomes. Hepatic resection is the most effective treatment method for hepatolithiasis,9,10 which is prevalent in Southeast Asia but rare in Western countries. However, SSI is the most common postoperative complication for it.9,11 Thus, it is worthwhile to determine whether hepatolithiasis is an independent risk factor of SSI after hepatic resection. This prospective study was conducted on a large cohort of patients undergoing hepatic resection to study the risk factors of overall, incisional, and organ/space SSI.
attack of bacterial cholangitis or cholecystitis or liver abscess within 2 weeks prior to the operation. Data were prospectively collected and entered into a computer database. Approval for this study was obtained from the ethics committee of the hospital. Perioperative Care and Surgical Procedures The criteria used for hepatic resection and perioperative care were consistent throughout the study period and have been reported in a previous study.12 There was no preoperative shaving. Abdominal incisions were closed with nonabsorbable sutures. Local antibiotics and subcutaneous drains were not used on the wounds. Intravenous prophylactic antibiotic, either broad-spectrum penicillin or first- or second-generation cephalosporins, were uniformly given at a dosage of 1–2 g intravenously at induction of anesthesia, followed by an additional dose intravenously at a 3-hour intervals, as recommended by the Centers for Disease Control and Prevention guidelines.13 Postoperative prophylaxis antibiotics were continued for 1–3 days after surgery. Other perioperative cares were practically standardized. Diagnosis of SSI The standardized surveillance criteria for defining SSI—as developed by the National Nosocomial Infections Surveillance System of the Centers for Disease Control and Prevention—were used, with SSIs classified as either incisional (superficial or deep) or organ/space.3 The risk factors for SSI were collected using a standardized data collection form. Statistical Analysis The primary outcomes were incisional SSI and organ/space SSI. Statistical analysis was done using SPSS software (ver. 18.0; SPSS). Comparison between patients who developed SSI (overall, incisional, and organ/space SSI) and those who did not was done using a x2 test with Yates correction or a Fisher exact test as appropriate. For the risk factors for SSI, significant variables (P ! .10) in the univariate analyses were entered into a multivariate logistic regression model using a criterion of P ≤ .05. A level of P ! .05 was considered statistically significant.
methods
results
The study was carried out in a university-based hepatobiliary center in Shanghai, which is the largest hepatobiliary surgical center in China. Consecutive patients who underwent open hepatic resection between January 2010 and December 2011 were included in this study. Excluded from the study were patients who received laparoscopic hepatic resection, hepatic resection with concomitant biliary reconstruction or gastrointestinal surgical procedures, or those who had an acute
Patient Population Of the 7,388 consecutive patients in the study cohort, there were 5,447 men (73.7%) and 1,941 women (26.3%), with a mean age of 55.8 years (range, 2–88 years). Obesity was found in 2,016 (27.3%) patients, and 410 (5.5%) patients were underweight. The patients’ hepatobiliary diseases that required hepatic resection were hepatecellular carcinoma (5,174;
This content downloaded from 146.203.126.115 on Sat, 15 Feb 2014 09:37:02 AM All use subject to JSTOR Terms and Conditions
table 1. Univariate Analysis of Risk Factors for Surgical Site Infection (SSI) after Hepatic Resection Variable Age, years !50 ≥50 Sex Male Female Obese (BMI ≥30) Underweight (BMI !18) Comorbid illness Diabetes mellitus Cardiovascular disease Hypertension COPD Renal dysfunction Active tobacco use Repeat hepatectomy ASA score !2 ≥2 Cirrhosis Preoperative ascites HbsAg (⫹) Anti-HCV (⫹) Child-Pugh score A B⫹C Platelets !100 # 109/L ≥100 # 109/L Prothrombin time, seconds !3 ≥3 Albumin, g/L !35 ≥35 Hepatobiliary diseases Hepatolithiasis Nonhepatolithiasis Type of hepatectomya Major Minor Additional surgical procedures Cholecystotomy Splenectomy Pericardial devascularization Hilar lymph node dissection Pringle maneuver Intraoperative blood loss, mL !800 ≥800 Operative time, minutes !240 ≥240 Intraoperative blood transfusion Postoperative bile leakage Postoperative bleeding requiring reoperation Use of abdominal drainageb Length of abdominal drainage, days (n p 7,206) !5 ≥5 Postoperative antibiotic prophylaxis No Yes
No.
Overall SSI
P
Incisional SSI
P
Organ/space SSI
P
3,314 4,074
295 (8.9) 403 (9.9)
.15
166 (5.0) 243 (6.0)
.07
155 (4.7) 206 (5.0)
.45
5,447 1,941 2,016 410 1,250 571 186 489 162 65 914 711
532 166 262 45 126 73 18 48 15 6 104 83
(9.8) (8.6) (13.0) (11.0) (10.0) (12.8) (9.7) (9.8) (9.3) (9.2) (11.4) (11.7)
.12
305 104 177 32 75 49 12 28 8 4 66 60
(5.6) (5.4) (8.8) (7.8) (6.0) (8.6) (6.5) (5.7) (4.9) (6.2) (7.2) (8.4)
.69
270 91 115 22 69 34 9 25 9 3 50 37
(5.0) (4.7) (5.7) (5.4) (5.5) (6.0) (5.1) (5.1) (5.6) (4.6) (5.5) (5.2)
.64
4,802 2,586 3,885 243 4,915 185
423 275 443 27 486 18
(8.8) (10.6) (11.8) (11.1) (9.9) (9.7)
245 164 253 18 285 11
(5.1) (6.3) (6.5) (7.4) (5.8) (5.9)
211 150 242 13 250 10
(4.4) (5.8) (6.2) (5.3) (5.1) (5.4)
!.01
6,654 734
618 (9.3) 80 (10.9)
.16
356 (5.4) 53 (7.2)
.04
313 (4.7) 48 (6.5)
.03
1,595 5,793
163 (10.2) 535 (9.2)
.23
100 (6.3) 309
.15
94 (5.9) 267 (4.6)
.04
6,001 1,387
564 (9.4) 134 (9.7)
.76
330 (5.5) 79 (5.7)
.77
295 (4.9) 66 (4.8)
.81
485 6,903
58 (12.0) 640 (9.3)
.05
43 (8.9) 366 (5.3)
!.01
27 (5.5) 334 (4.8)
.47
498 6,890
92 (18.5) 606 (8.8)
!.01
64 (12.9) 345 (5.0)
!.01
55 (11.0) 306 (4.4)
1,699 5,689
161 (9.5) 537 (9.4)
.96
105 (6.2) 304 (5.3)
.19
88 (5.2) 273 (4.8)
.52
2,106 173 118 491 6,810
202 18 16 48 636
(9.6) (10.4) (13.6) (9.8) (9.3)
.79 .66 .12 .80 .27
122 11 9 34 372
.54 .63 .12 .16 .34
110 12 9 27 330
(5.2) (6.9) (7.6) (5.5) (4.8)
.40 .21 .16 .52 .58
5,855 1,533
530 (9.0) 168 (11.0)
.02
304 (5.0) 105 (7.5)
!.01
277 (4.7) 84 (5.5)
.23
5,917 1,471 1112 221 38 7,206
539 159 139 25 5 685
(9.1) (10.8) (12.5) (10.8) (13.2) (9.5)
!.05
312 97 76 13 3 401
(5.3) (6.6) (6.8) (5.9) (7.9) (5.6)
!.05
271 90 74 17 3 352
.02
5,745 1,461
524 (9.1) 161 (11.0)
.03
309 (5.4) 92 (6.3)
.17
254 (4.4) 98 (6.7)
!.01
184 7,204
17 (9.2) 681 (9.5)
.92
10 (5.4) 399 (5.5)
.95
10 (5.4) 351 (4.9)
.73
!.01
.28 .40 !.10 .91 .77 .93 .95 .03 .03 .01 !.01
.37 .07 .89
!.01
.34 .43 .28
(5.8) (6.4) (7.6) (6.9) (5. 5)
!.01
.04 .43 !.01 .58 .85 .74 .83 .02 !.01 .03 !.01 !.01
.05 .81
.04 .82 .52 .50
(4.6) (6.1) (6.7) (7.2) (7.9) (4.9)
.04 .64 .25 .22 .98 .81 .69 NS .38 .68
!.01
.73 .26 .74
!.01
!.01 !.05
.34 .97
note. Data are no. (%) of patients, unless otherwise indicated. ASA, American Society of Anesthesiologists; BMI, body mass index; COPD, chronic obstructive pulmonary disease; HCV, hepatitis C virus; NS, not significant; SSI, surgical site infection. a Major, resection of 3 or more Couinaud liver segments; minor, resection of fewer than 3 segments. b Drainage with T tube was excluded.
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ssi after hepatectomy
table 2. Multivariate Analysis of Risk Factors of Surgical Site Infection (SSI) after Hepatic Resection
Overall SSI Obesity (BMI ≥30) Diabetes mellitus ASA score ≥2 Cirrhosis Repeat hepatectomy Hepatolithiasis Length of abdominal drainage ≥5 days Intraoperative blood transfusion Incisional SSI Obesity (BMI ≥30) Diabetes mellitus Cirrhosis Hypoalbuminemia Repeat hepatectomy Hepatolithiasis Intraoperative blood transfusion Organ/space SSI ASA score ≥2 Cirrhosis Hepatolithiasis Intraoperative blood transfusion Length of abdominal drainage ≥5 days Postoperative bile leakage
OR
95% CI
P
1.62 1.43 1.35 1.55 1.15 1.75 1.49 1.57
1.25–2.09 1.07–1.90 1.03–1.74 1.34–1.80 1.03–1.31 1.42–2.13 1.34–1.77 1.32–1.98
!.01
1.55 1.35 1.61 1.19 1.17 1.58 1.32
1.30–1.97 1.18–1.65 1.35–1.94 1.03–1.58 1.03–1.32 1.32–1.99 1.10–1.68
!.01
1.42 1.70 1.66 1.71 1.27 1.22
1.14–1.80 1.41–2.12 1.46–1.97 1.45–2.11 1.07–1.54 1.03–1.49
.01 !.01 !.01 !.01 .03 .04
.03 .04 !.01 !.05 !.01 !.01 !.01
.01 !.01
.03 !.05 !.01
.01
note. ASA, American Society of Anesthesiologists; BMI, body mass index; CI, confidence interval; OR, odds ratio.
70.0%), hepatic hemangioma (548; 7.4%), and hepatolithiasis (498; 6.7%). The preoperative liver functional status was Child-Pugh A in 6,654 patients, B in 724 patients, and C in 10 patients. Repeat hepatectomy was carried out for 711 patients (9.6%). Cirrhosis as determined by postoperative histopathological examination was present in 3,885 patients (52.6%). Operative Outcomes and Incidences of SSI Among all, 103 patients died, and the mortality rate was 1.4%. For the 698 patients who developed SSI after hepatic resection, incisional and organ/space SSI was diagnosed in 409 and 361 patients, respectively (72 patients had both incisional and organ/space SSI). The incidences of overall, incisional, and organ/space SSI were 9.4%, 5.5%, and 4.9%, respectively. The median time from operation to the diagnosis of SSI was 7 days. The mean postoperative stay for patients who developed SSI was 13.6 days, which was significantly longer than the 7.2 days in those who did not develop SSI (P ! .01). Univariate and Multivariable Analyses for Risk Factors for SSI The results of univariate analysis of risk factors associated with overall, incisional, and organ/space SSI after hepatic resection are summarized in Table 1.
319
Multivariate logistic regression analysis (Table 2) identified the following 8 independent risk factors for overall SSI: obesity, diabetes mellitus, American Society of Anesthesiologists (ASA) score of 2 or greater, cirrhosis, repeat hepatectomy, hepatoliathiasis, length of abdominal drainage 5 days or longer, and intraoperative blood transfusion. The factor associated with the highest odds ratio was hepatolithiasis. In addition, obesity, diabetes mellitus, cirrhosis, hypoalbuminemia, repeat hepatectomy, hepatolithiasis, and intraoperative blood transfusion significantly predicted incisional SSI, while ASA score of 2 or greater, cirrhosis, hepatolithiasis, intraoperative blood transfusion, length of abdominal drainage 5 days or longer, and postoperative bile leakage significantly predicted organ/space SSI. Among these independent risk factors, hepatolithiasis, cirrhosis, and intraoperative blood transfusion were the only factors that were associated with both incisional and organ/space SSI.
discussion One highlight of this study is the finding that SSI after hepatic resection for hepatolithiasis is more common than for other hepatobiliary diseases on multivariate analysis. Possible explanations are recurrent attacks of acute cholangitis with bacterial colonization in the biliary system in intrahepatic lithiasis14 and the more common occurrence of postoperative bile leakage, which was identified as a risk factor for organ/space SSI by this and other studies.4,5,15,16 Another interesting and important finding in this study is the identification of cirrhosis as an independent risk factor of both incisional and organ/space SSI after hepatic resection. As far as we know, this is the first study to reveal the relationship between cirrhosis and postoperative SSI after hepatic resection. In this study, 443 (11.8%) of 3,885 cirrhotic patients developed postoperative SSI. This high prevalence of SSI in cirrhotic patients can be explained by the presence of various dysfunctions in the mechanisms of defense against infection: a decrease in function of the reticuloendothelial system and granulocytes, a decrease in complement concentrations, and a change in cell-mediated immunity.17,18 This study also found that intraoperative blood transfusion was the only surgical-related risk factor shared by both incisional and organ/space SSI after hepatic resection, which is consistent with previous studies on a variety of other operations.19,20 However, the underlying mechanism remains obscure. Measures to decrease blood loss and avoid intraoperative blood transfusions are important strategies in decreasing postoperative SSI. In conclusion, postoperative SSI was common in patients undergoing hepatic resection. High-risk groups of patients and operations were identified. In order to reduce SSI after hepatic resection, patients with hepatolithiasis or cirrhosis should be cared for with caution, and intraoperative blood loss should be kept to an absolute minimum.
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320
infection control and hospital epidemiology
march 2014, vol. 35, no. 3
acknowledgments Financial support. This work was supported by the National Natural Science Foundation of China (81000166 and 81172020), the Shanghai Program for Excellent Talents in Health System (XYQ2011033), the Foundation for Outstanding Young Scholar of Second Military Medical University, the Shanghai Rising-Star Science Foundation for Youths (12QA1404800), and the State Key Project on Infectious Diseases of China (2012ZX10002-016). 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. Affiliations: 1. Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China; 2. Faculty of Medicine, Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China; a. These authors contributed equally to this work. Address correspondence to Feng Shen, MD, PhD, Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China ([email protected]) or to Jie-Wei Li, MD, PhD, Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China ([email protected]). Received August 19, 2013; accepted November 9, 2013; electronically published January 31, 2014. 䉷 2014 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2014/3503-0019$15.00. DOI: 10.1086/675278
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