Abstract
Background
This project aimed to study resource utilization and surgical outcomes after hepaticojejunostomy (HJ) for biliary injuries utilizing data from ACS NSQIP.
Methods
Data from the Participant Use Data File containing surgical patients submitted to the ACS NSQIP during the period of 1/1/2005–12/31/2014 were analyzed.
Results
During the study period, 320 patients underwent HJ. Mean age was 50 years, and 109 (34%) were male. Forty-four percent of patients met criteria for ASA class III–V. Forty patients (12.5%) developed one or more critical care complications (CCC). Eighty-one patients (25%) experienced morbidity with a perioperative mortality rate of 1.9%. The mean age of these patients was 52 years, and 62% were male. Age and preoperative elevated alkaline phosphatase were independent predictors of CCC (p < 0.001 and 0.042, OR 1.035, OR 4.337, respectively). Patients ASA class III, age, and preoperative hypoalbuminemia were found to increase risk for prolonged LOS (OR 1.87, p = 0.041, OR 1.02, p = 0.049, OR 2.63, p = 0.001).
Discussion
The most significant predictors of morbidity and increased resource utilization after HJ include increasing age, ASA class III or above, and preoperative hypoalbuminemia. Age and ASA class are the strongest predictors of CCC in these patients.
Introduction
Iatrogenic biliary duct injury (IBDI) is an important and serious complication of abdominal surgery, most commonly occurring during laparoscopic cholecystectomy (LC). LC is one of the most common surgical procedures performed in the United States with approximately 750,000 performed annually.1 The incidence of IBDI increased to 0.9% after the introduction of LC.2 Unrecognized or improperly treated IBDI can lead to further complications such as secondary biliary cirrhosis and liver dysfunction, need for further surgical intervention, or even death.3 This leads to increased healthcare costs, time off work, and decreased quality of life.4, 5 Short and long term outcomes are generally correlated with the severity and grade of the IBDI.
The goal of operative treatment of IDBI is to reestablish bile flow into the gastrointestinal tract and prevent cholangitis, biliary sludge, biliary stones, stricture or biliary cirrhosis. Hepaticojejunostomy (HJ) is the most commonly used and recommended means of IBDI repair.2, 6, 7 HJ is the preferred treatment for many reasons including absence of intestinal reflux into bile ducts and a lower occurrence of postoperative stricture.2, 8 However, HJ does have considerable risk of longterm complications, most notably a stricture of the HJ and need for repeat HJ.9
The aim of this project was to study resource utilization and short term surgical outcomes after HJ for biliary injury utilizing the data from ACS NSQIP.
Methods
A study that investigated patients undergoing hepaticojejunostomy for biliary injuries was performed. The ACS NSQIP database was used to collect pre-, intra-, and postoperative variables. The data were analyzed using the Participant Use Data File containing all surgical patients submitted to the ACS NSQIP during the study period of 1/1/2005–12/31/2014. The ACS NSQIP collects preoperative risk factors including preoperative laboratory data, intraoperative variables, and 30-day postoperative morbidity and mortality outcomes for a systematic and prospective sample of patients undergoing surgical procedures in both the inpatient and outpatient setting.
In 2011 readmitted data was added to the to the ACS NSQIP dataset. Therefore, readmission data between 2011 and 2014 were collected and analyzed. Readmitted patients were stratified into planned readmissions, unplanned readmissions related to the index procedure (UPRR), and unrelated readmissions. Planned readmissions were defined as those indicated at the time of the index procedure. Unrelated readmissions were defined as those in which the readmission was associated with a pathology unrelated to the initial procedure. Morbidity was defined as previously published by the presence of surgical site infection, wound dehiscence, pneumonia, unplanned intubation, extended ventilator use, sepsis or septic shock, urinary tract infection, renal failure or insufficiency, pulmonary embolism/deep vein thrombosis, myocardial infarction, stroke, any readmission, and any reoperation.10 Critical care complications (CCC) was defined as the presence of organ space infection as a surrogate for intraabdominal abscess, pneumonia, unplanned intubation, ventilator use beyond 48 h, sepsis or septic shock, renal failure or insufficiency, pulmonary embolism/deep vein thrombosis, myocardial infarction, and stroke. Resource utilization outcome variables were defined as operative time greater than the median, length of stay greater than median, and readmission requirement.
Categorical variables were compared using chi-squared test and continuous variables using Mann–Whitney U test. Multivariable logistic regression was performed to determine independent demographic, preoperative clinical and intraoperative risk factors for perioperative mortality and morbidity, LOS, BPU, prolong ventilation, operative time, UPRR. Statistically significant variables in the univariate analysis were included in the multivariate analysis. A p < 0.05 was considered the threshold for statistical significance. Statistical analysis was performed using SPSS software, version 21.0 (SPSS Inc, Chicago, Illinois).
Results
A total of 320 patients underwent hepaticojejunostomy (HJ) for biliary tract injury during the study period.
Eighty-one patients (25%) experienced morbidity. Six (1.8%) patients died within 30 days of operation with a mortality rate 1.8%. Univariate analysis of variables associated with morbidity and mortality are shown in Table 1, Table 2, respectively. Independent predictors of morbidity were age, elevated preoperative alkaline phosphatase (OR (95%CI) 1.04 (1.02–1.05), p < 0.001, OR (95%CI) 2.04 (1.10–3.92), p = 0.028, respectively). Only age was shown to be independent predictor of mortality (OR (95%CI) 1.03 (1.01–1.05), p = 0.005).
Table 1.
Major morbidity among patients undergoing biliary reconstruction for IBDIa
| Variable | All patients | No. major morbidities | At least 1 major morbidity | Significance |
|---|---|---|---|---|
| All patients | N = 320 | n = 239 | n = 81 | |
| Age, mean (SD) | 50 (18) | 47 (17) | 57 (17) | <0.001 |
| Age | ||||
| <=35 | 88 | 74 | 11 | 0.001 |
| 36–45 | 48 | 43 | 7 | |
| 46–55 | 68 | 48 | 20 | |
| 56–65 | 52 | 36 | 17 | |
| 66+ | 64 | 38 | 26 | |
| Female | 211 | 170 | 42 | 0.003 |
| BMI | ||||
| <18.5 | 23 | 16 | 7 | 0.158 |
| 18.5–25 | 80 | 55 | 24 | |
| 25–30 | 104 | 81 | 25 | |
| 30–35 | 64 | 50 | 13 | |
| 35–40 | 40 | 33 | 7 | |
| 40+ | 9 | 4 | 5 | |
| ASA class | ||||
| I–II | 179 | 148 | 31 | 0.001 |
| III | 131 | 86 | 45 | |
| IV–V | 10 | 5 | 5 | |
| Diabetes mellitus | 45 | 26 | 19 | 0.010 |
| Congestive heart failure | 3 | 2 | 1 | 1.000 |
| Anticoagulation or bleeding disorder | 11 | 7 | 4 | 0.479 |
| Renal insufficiency or failure | 1 | 0 | 1 | 0.253 |
| Smoking | 57 | 46 | 10 | 0.179 |
| Presence of ascites | 7 | 5 | 2 | 1.000 |
| Dialysis | 2 | 2 | 0 | 0.621 |
| Albumin <3 g/dl | 93 | 62 | 30 | 0.098 |
| Bilirubin >1 | 150 | 110 | 39 | 0.793 |
| Creatinine >1.2 | 27 | 14 | 12 | 0.017 |
| Alkaline phosphatase >125 | 208 | 148 | 60 | 0.072 |
A major morbidity is defined as one of the following events: SSI (superficial, deep incisional, or organ/space), wound dehiscence, pneumonia, unplanned intubation, on ventilator >48 h, sepsis/septic shock, UTI, renal failure/insufficiency, pulmonary embolism, DVT, myocardial infarction, stroke/CVA, any readmission, or any reoperation.
Table 2.
Perioperative mortality among patients undergoing biliary reconstruction for IBDI
| Variable | All patients | Mortality within 30 days of operation | No mortality | Significance |
|---|---|---|---|---|
| All patients | N = 320 | n = 6 | n = 314 | |
| Age, mean (SD) | 50 (18) | |||
| Age | ||||
| <=35 | 86 | 0 | 85 | 0.004 |
| 36–45 | 48 | 0 | 50 | |
| 46–55 | 67 | 1 | 66 | |
| 56–65 | 51 | 0 | 53 | |
| 66+ | 64 | 5 | 60 | |
| Female | 211 | 2 | 210 | 0.105 |
| BMI | ||||
| <18.5 | 23 | 1 | 22 | 0.536 |
| 18.5–25 | 80 | 2 | 75 | |
| 25–30 | 105 | 3 | 104 | |
| 30–35 | 64 | 0 | 63 | |
| 35–40 | 42 | 0 | 41 | |
| 40+ | 9 | 0 | 9 | |
| ASA class | ||||
| I–II | 179 | 0 | 179 | <0.001 |
| III | 131 | 3 | 128 | |
| IV–V | 10 | 3 | 7 | |
| Diabetes mellitus | 45 | 2 | 44 | |
| Congestive heart failure | 3 | 2 | 1 | |
| Anticoagulation or bleeding disorder | 11 | 1 | 10 | 0.191 |
| Renal insufficiency or failure | 1 | 0 | 1 | 0.981 |
| Smoking | 57 | 1 | 57 | 1.000 |
| Presence of ascites | 7 | 1 | 6 | 0.125 |
| Dialysis | 2 | 0 | 2 | 1.000 |
| Albumin <3 g/dl | 93 | 6 | 88 | 0.002 |
| Bilirubin >1 | 150 | 6 | 144 | 0.021 |
| Creatinine >1.2 | 26 | 1 | 25 | 0.408 |
| Alkaline phosphatase >125 | 208 | 6 | 204 | 0.167 |
Critical care complications (CCC)
Forty patients (12.5%) developed one or more critical care complications (Table 3). Of the total patient population, 12 patients developed organ space infection, 8 developed pneumonia, 10 experienced extended ventilator use, 7 underwent unplanned reintubation, 17 developed sepsis, 4 developed septic shock, 6 developed renal failure, 3 developed DVT/PE, 2 experienced cardiac arrest and 2 experienced myocardial infarction. Some patients experienced more than 1 CCC in this study. Multivariate regression analysis demonstrated factors associated with one or more critical care complication (Table 4).
Table 3.
All critical care complications in patients undergoing biliary reconstruction for IBDIa
| Variable | All patients | No. critical care complications | At least 1 critical care complication | Significance |
|---|---|---|---|---|
| All patients | N = 320 | n = 280 | n = 40 | |
| Age, mean (SD) | 50 (18) | 48 (17) | 52 (16) | <0.001 |
| Age | ||||
| ≤35 | 88 | 84 | 3 | <0.001 |
| 36–45 | 48 | 46 | 3 | |
| 46–55 | 68 | 63 | 7 | |
| 56–65 | 52 | 46 | 8 | |
| 66+ | 64 | 41 | 19 | |
| Female | 211 | 196 | 15 | <0.001 |
| BMI | ||||
| <18.5 | 22 | 8 | 0 | 0.987 |
| 18.5–25 | 80 | 73 | 11 | |
| 25–30 | 104 | 95 | 15 | |
| 30–35 | 64 | 59 | 7 | |
| 35–40 | 41 | 37 | 6 | |
| 40+ | 9 | 8 | 1 | |
| ASA class | ||||
| I–II | 179 | 168 | 10 | <0.001 |
| III | 131 | 106 | 26 | |
| IV–V | 10 | 6 | 4 | |
| Diabetes mellitus | 45 | 36 | 10 | <0.001 |
| Congestive heart failure | 3 | 2 | 1 | 0.331 |
| Anticoagulation or bleeding disorder | 11 | 8 | 3 | 0.147 |
| Renal insufficiency or failure | 1 | 0 | 1 | 0.125 |
| Smoking | 57 | 50 | 6 | 0.824 |
| Presence of ascites | 7 | 5 | 2 | 0.214 |
| Dialysis | 2 | 2 | 0 | 1.000 |
| Albumin <3 g/dl | 93 | 70 | 23 | <0.001 |
| Bilirubin >1 | 150 | 126 | 24 | 0.099 |
| Creatinine >1.2 | 26 | 17 | 10 | <0.001 |
| Alkaline phosphatase >125 | 208 | 173 | 34 | 0.011 |
A critical care complication is defined as one of the following events: organ space/SSI, pneumonia, unplanned intubation, on ventilator >48 h, sepsis/septic shock, renal failure/insufficiency, pulmonary embolism, DVT, cardiac arrest, myocardial infarction, or stroke/CVA.
Table 4.
Multivariate logistic regression for any critical care complication after biliary surgerya
| Variable | Estimated odds ratio | 95% Confidence interval for estimated odds ratio | Significance |
|---|---|---|---|
| Patient ageb | 1.035 | (1.011, 1.062) | 0.005 |
| Gender, male vs. female | 3.107 | (1.391, 7.172) | 0.006 |
| Preoperative albumin <3 | 3.522 | (1.586, 7.958) | 0.002 |
| Preoperative alkaline phosphatase >125 | 4.337 | (1.716, 12.816) | 0.004 |
A critical care complication is defined as one of the following events: organ/space SSI, pneumonia, unplanned intubation, on ventilator >48 h, sepsis/septic shock, renal failure/insufficiency, pulmonary embolism, DVT, cardiac arrest, myocardial infarction, or stroke/CVA.
Age, ASA class and BMI were used as continuous variables.
Resource utilization outcomes
Length of stay greater than median
The median length of stay (LOS) for patients undergoing HJ was 8 days. Independent factors associated with prolonged LOS included age and preoperative hypoalbuminemia (OR (95% CI) 1.02 (1.01–1.04), p = 0.002, OR (95% CI) 3.8 (2.16–6.8), p < 0.001, respectively).
Operation time greater than median
The median operative time for patients undergoing HJ was 233 min. Preoperative alkaline phosphatase was an independent variable associated with longer operation duration (OR (95% CI) 1.66 (1.02–2.7), p = 0.04).
Readmission
Of the 103 patients in whom readmission data was available, 13 required readmission. Independent predictors of readmission were preoperative hyperbilirubinemia, ASA class III and ASA class IV–V compared to class I–II (OR (95% CI) 8.79 (1.86–56.46), p = 0.011, OR (95% CI) 11.02 (2.07–97.64), p = 0.012 and OR (95% CI) 75.79 (3.93–2369.15), p = 0.006, respectively).
Discussion
Iatrogenic biliary duct injury (IBDI) is a feared and serious complication of abdominal surgery. Hepaticojejunostomy (HJ) is the most commonly performed procedure to reestablish biliary continuity. However, HJ is a complex surgery and is associated with many risks that can lead to further complications and resource utilization. AbdelRafee et al. demonstrated an 88% success rate and 29% incidence of long term complications after HJ for biliary injuries.11 Despite the gravity of this operation and its impact on patients, analysis of predictors for complications and healthcare costs after HJ for biliary injuries is lacking in the current medical literature. This study is the first to retrospectively analyze predictors for critical care complications, resource utilization, and perioperative morbidity and mortality using the ACS NSQIP national database for patients with biliary injuries undergoing HJ.
Among critical care complications the most common risk factors were increasing age followed by ASA class. Patients developing major complications were all classified as ASA class III or above in 75% of patients.
Preoperative optimization of patients' underlying health conditions is generally strived for patients undergoing surgery. Zafar et al. reported on a single center experience that the most common predictors of early complications after biliary reconstruction for biliary injuries are hypoalbuminemia and ASA class.12 As such, this study also found ASA classification to be associated with increased risk of CCC and morbidity. Eskander et al. in a large study of biliary surgery for multiple indications reported a perioperative death rate of 4.2% versus 1.9% in this series, finding reconstruction for malignancy as the strongest predictor of perioperative mortality.13 Optimizing the management of significant comorbidities such as diabetes, hypertension and others can change the patient's preoperative ASA class to a lower grade decreasing the risk of developing critical care complications and general morbidity after surgery.
ASA classification and hypoalbuminemia were the most notable risk factors for increased resource utilization in these patients. ASA class III or above was a strong predictor for extended ventilator use and unplanned readmissions. All patients requiring extended ventilatory support were ASA class III or above. Patients with ASA class III or above had greater than 11 fold increased risk of readmission in this cohort. In a study on resource use for repair of biliary injuries after cholecystectomy, Bauer et al. reported a mean LOS of 17 days and a readmission rate higher than the one found in this series (38% vs. 12%).14 Preoperative hypoalbuminemia predicted increased risk of extended ventilator use almost 8 fold and risk of prolonged LOS 3.9 fold. Preoperative hyperbilirubinemia showed a significant increased risk for extended ventilator use (OR = 18.1) and readmissions (OR = 8.79). Elevated preoperative alkaline phosphatase was associated with increased operative time (OR = 1.66).
Some strengths of the ACS NSQIP system used in this study include stringent definition of each variable analyzed and homogeneity of the data series within a fixed timeframe across multiple healthcare institutions. There are limitations to this study that should be acknowledged. The NSQIP dataset was not developed to study this specific patient population and some important variables such severity of injury information, antibiotic treatment, length of antibiotic treatment, fistula formation, output, time of closure, timing of the HJ (early vs. late) among others are not captured. Only the larger academic centers that are accustomed to complicated cases are captured in NSQIP which could contribute to selection bias. NSQIP dataset collects data from 30 days after the surgical procedure, and 90-day perioperative morbidity and mortality that are frequently reported are not collected. Arterial injury data that is important in regard to biliary complications is limited and the codes may not accurately reflect the correct number of patients with synchronous injuries.
In summary, this study identified various predictors of complications and increased resource utilization in patients undergoing HJ for biliary injuries. Among others, the most significant predictors of morbidity and increased resource utilization after major biliary surgery for injuries of the biliary system included age, ASA class III or above, and hypoalbuminemia. ASA class and hyperbilirubinemia are the most significant factors associated with increased risk of unplanned readmissions related to the procedure. Age was found as the only independent predictor of perioperative death in this cohort. Every effort should be attempted to correct potential modifiable risk factors, such as tighter glucose control, abstinence from alcohol and tobacco, weight loss and hypertension management to optimize patients prior to surgery, when feasible. This could potentially decrease the rates of critical care complications and resource utilization in patients undergoing biliary reconstruction for biliary injuries.
Funding
No funding resources to disclose.
Authorship
Designed research: NJ, AD, DD, RG.
Collected data: AD, DD.
Analyzed data: NJ, AD, DD, RG.
Wrote the manuscript: NJ, AD, MD, MS, JB, DD, RG.
Critical editing of content: NJ, AD, MD, MS, JB, DD, RG.
Approval of final version: all authors.
Conflicts of interest
None to declare.
References
- 1.Flum D.R., Cheadle A., Prela C., Dellinger E.P., Chan L. Bile duct injury during cholecystectomy and survival in medicare beneficiaries. JAMA. 2003;290:2168–2173. doi: 10.1001/jama.290.16.2168. [DOI] [PubMed] [Google Scholar]
- 2.Jablonska B., Lampe P. Iatrogenic bile duct injuries: etiology, diagnosis and management. World J Gastroenterol. 2009;15:4097–4104. doi: 10.3748/wjg.15.4097. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Truant S., Boleslawski E., Lebuffe G., Sergent G., Pruvot F.R. Hepatic resection for post-cholecystectomy bile duct injuries: a literature review. HPB (Oxford) 2010;12:334–341. doi: 10.1111/j.1477-2574.2010.00172.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Andersson R., Eriksson K., Blind P.J., Tingstedt B. Iatrogenic bile duct injury–a cost analysis. HPB (Oxford) 2008;10:416–419. doi: 10.1080/13651820802140745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Landman M.P., Feurer I.D., Moore D.E., Zaydfudim V., Pinson C.W. The long-term effect of bile duct injuries on health-related quality of life: a meta-analysis. HPB (Oxford) 2013;15:252–259. doi: 10.1111/j.1477-2574.2012.00586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Ahrendt S.A., Pitt H.A. Surgical therapy of iatrogenic lesions of biliary tract. World J Surg. 2001;25:1360–1365. doi: 10.1007/s00268-001-0124-2. [DOI] [PubMed] [Google Scholar]
- 7.Jabłońska B., Lampe P., Olakowski M., Górka Z., Lekstan A., Gruszka T. Hepaticojejunostomy vs. end- to-end biliary reconstructions in the treatment of iatrogenic bile duct injuries. J Gastrointest Surg. 2009;13:1084–1093. doi: 10.1007/s11605-009-0841-7. [DOI] [PubMed] [Google Scholar]
- 8.Mercado M.A., Chan C., Salgado-Nesme N., López-Rosales F. Intrahepatic repair of bile duct injuries. A comparative study. J Gastrointest Surg. 2008;12:364–368. doi: 10.1007/s11605-007-0428-0. [DOI] [PubMed] [Google Scholar]
- 9.Stilling N.M., Fristrup C., Wettergren A., Ugianskis A., Nygaard J., Holte K. Long-term outcome after early repair of iatrogenic bile duct injury. A national Danish multicentre study. HPB (Oxford) 2015;17:394–400. doi: 10.1111/hpb.12374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Raval M.V., Hamilton B.H., Ingraham A.M., Ko C.Y., Hall B.L. The importance of assessing both inpatient and outpatient surgical quality. Ann Surg. 2011;253:611–618. doi: 10.1097/SLA.0b013e318208fd50. [DOI] [PubMed] [Google Scholar]
- 11.AbdelRafee A., El-Shobari M., Askar W., Sultan A.M., El Nakeeb A. Long-term follow-up of 120 patients after hepaticojejunostomy for treatment of post-cholecystectomy bile duct injuries: a retrospective cohort study. Int J Surg. 2015;18:205–210. doi: 10.1016/j.ijsu.2015.05.004. [DOI] [PubMed] [Google Scholar]
- 12.Zafar S.N., Khan M.R., Raza R., Khan M.N., Kasi M., Rafiq A. Early complications after biliary enteric anastomosis for benign diseases: a retrospective analysis. BMC Surg. 2011;11:19. doi: 10.1186/1471-2482-11-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Eskander M.F., Bliss L.A., Yousafzai O.K., de Geus S.W., Ng S.C., Callery M.P. A nationwide assessment of outcomes after bile duct reconstruction. HPB (Oxford) 2015;17:753–762. doi: 10.1111/hpb.12436. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Bauer T.W., Morris J.B., Lowenstein A., Wolferth C., Rosato F.E., Rosato E.F. The consequences of a major bile duct injury during laparoscopic cholecystectomy. J Gastrointest Surg. 1998;2:61–66. doi: 10.1016/s1091-255x(98)80104-2. [DOI] [PubMed] [Google Scholar]