Per-Jonas Blind, Bodil Andersson, Bobby Tingstedt, Magnus Bergenfeldt, Roland Andersson, Gert Lindell, Christian Sturesson

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1 2326 LIVER Per-Jonas Blind, Bodil Andersson, Bobby Tingstedt, Magnus Bergenfeldt, Roland Andersson, Gert Lindell, Christian Sturesson Department of Surgery, Clinical Sciences Lund, Skåne University Hospital and Lund University, Sweden Corresponding author: Christian Sturesson, Department of Surgery, Skåne University Hospital, S Lund, Sweden; Tel.: ; Fax: ; Liver resection, Fast track, Length of stay, Morbidity, Complications. : Fast-track programs involving multi-modal measures to enhance recovery after surgery, reduce morbidity and decrease hospital length of stay (LOS) are used for different major surgical pro- within a fast-track program have been studied only to a limited extent, which was the aim of the present study. The present study comprises for liver resections introduced in March Patient outcomes were compared to a historical cohort of patients (n=62) operated in Factors prolonging LOS was analyzed by uni- and multivariate analysis. Median LOS was 6 days (range 3-42 days) within the fast-track program as compared with 8 days (range 5-47 days) in the historical cohort (P=0.004). On multivariate analysis, factors increasing LOS in the fast-track group were found to be the presence of complication (P=0.018), extent of resection (major as compared to minor) (P=0.001) and inability to drink > 1250 ml on the day after surgery (P=0.002). - Patients who can only drink limited amounts of patients that should be given special attention within a fast-track program. Fast-track programs with evidence-based multimodal measures to accelerate recovery, decrease morbidity and decrease hospital length of stay (LOS) have been implemented for different major surgical procedures (1, 2, 3, 4, 5). In recent years, the concept has also been applied to liver resectional surgery (6, 7, 8, 9, 10). Important aspects of fast-track programs include preoperative patient information, avoidance of preoperative fasting, limited use of drains and catheters, early postoperative mobilization and immediate postoperative oral nutrition. In liver surgery, introducing a fast-track program has consistently shortened LOS, which has been interpreted as an enhanced recovery. The more widespread use of fast-track clinical pathways for liver resections calls for identification of factors predicting delayed recovery, to pin point patients needing special actions for enhancing recuperation. For liver resections, factors increasing LOS with traditional care have been shown to be major versus minor resections (11), reduced pre-operative liver function (12), obesity, diabetes and smoking (13). To our knowledge, no such analysis has been made in the context of a fast-track program for liver resection, which was the aim of the present study. In March 2012, a fast-track program for liver resection was introduced at our institution Patient data was prospectively collected and the present analysis includes patients (n=64) consecutively operated up to November 2012 with liver resection, with or without the addition of intraoperative radiofrequency ablation. Patients excluded from the analysis were patients with Hepato-Gastroenterology 2014; 61: doi /hge13687 H.G.E. Update Medical Publishing S.A., Athens-Stuttgart liver cirrhosis (n=2), patient undergoing resection of hilar cholangiocarcinoma (n=1), patient not receiving preoperative protocol information (n=1) and patients undergoing exploration only without liver resection (n=4). Patients received information on the planned operation as well as information on the fast-track program by a hepatobiliary surgeon in the outpatient clinic. At the same visit, complementary information on the fast-track program was given orally and in writing by a project nurse. The information included the chosen criteria for discharge, being normal or decreasing bilirubin values, no need for intravenous (i.v.) fluids, acceptable pain relief on oral analgetics (defined as max 3 at rest and max 5 at movement on a 100-mm visual analogue scale (14), tolerance to normal food, fully mobilized or mobilized to preoperative level with respect to activities of daily living (15) and the patient being willing to be discharged. Patients were informed that they could expect a hospital stay of 5-6 days. The perioperative care principles of the fast-track program are shown in. Patients were sent from the postoperative high-dependency unit to the ward the day of surgery for uncomplicated minor resections (here defined as resection of <3 Couinaud s segments), and the day after surgery in case of major re- Approximately 4 weeks after discharge, patients were seen in the outpatient clinic by a surgeon for information on the histopathological report and to register patient-reported complications. In case of hospital readmission within 30 days following discharge, the charts of that admission were scrutinized for time and reason for admission, treatment given and additional LOS. Mor-

2 Fast-track Program for Liver Resection Hepato-Gastroenterology 61 (2014) 2327 classification (16). Perioperative bleeding without the need for any intervention other than blood transfusion was not registered as a complication. The fast-track program cohort of patients was compared to a historical cohort of patients consecutively operated during 2009 with the same exclusion criteria as described above for the fast-track patients. In 2009, there was no written program with the intention of enhancing recovery. At the time we did not use written directives mobilization, analgesia, fluid substitution or removal of urinary catheters. This was done at the discretion of the attending surgeon. Continuous data are expressed as median (range) and categorical variables as number (percentage). Comparison between the fast-track and control groups as well as univariate analysis of variables of importance for LOS in the fast-track group were made using Mann-Whitney test for continuous variables and Fischer s exact test for categorical variables. In the fast-track group, variables with a p<0.20 on univariate analysis with respect to LOS were included in a stepwise multivariate linear regression analysis model. A p-value <0.05 was considered significant. All data analyses were performed using IBM SPSS Statistics 19 software (IBM, Armonk, NY). Patent demographics and perioperative data for the fast-track program and the historical control groups are shown in. Initial LOS was significantly shorter for the fast-track group than the control group (6 vs 8 days, p=0.004), with no change when including readmissions. Readmissions in the fast-track group (n=3) were at 7, 10 and 17 days after discharge and were due to intra-abdominal infection, pyelonephritis on the basis of an obstructing renal stone, and fecaloma, respectively. Another 4 patients in the fast-track group were treated on an out-patient basis due to a superficial surgical site infection (SSI) (n=3) by wound debridement and urinary retention (n=1) treated by reinsertion of a urinary catheter. In total, 6 patients (9%) in the fasttrack group had superficial SSI. The complications in the fast-track group are shown in, where liver failure is defined according to the criteria (17). There was no 30-day mortality in either group. In the fast-track group, 59/64 patients (93%) were able to drink more than 200 ml after surgery on the day of operation. Intravenous analgesia was withdrawn on the morning of POD2 in 60/64 patients (94%). These patients consumed 20(0-75) mg and 20 (0-40) mg of oxycodone on POD2 and POD3, respectively. Antiemetic drugs were given to 17/64 patients (27%) on POD2 and to 12/64 patients (19%) on POD3, reflecting the incidence of postoperative nausea. The urinary catheter was removed on POD2 in 46/64 patients (72%). Weight increase on POD1 was 1.3 (-1.1 8) kg in the fast-track group. shows the results from the univariate analysis of factors influencing LOS in the fast-track group. When performing multivariate analysis, factors predicting prolonged LOS were major liver resection (P=0.001), the occurrence of a complication (P=0.018) and the inability to drink > 1250 ml on POD1 (P=0.002).. Fast-track program principles of perioperative care. Day of surgery Carbohydrate drinks (400 ml) up to 2 h before surgery Right-sided subcostal incision with upward midline extension No abdominal drains No postoperative nasogastric tubes Antiemetics administered 1 h before end of surgery consisting of 4 mg ondasetron and 0.5 mg droperidol Patient sent to recovery ward Patient-controlled analgesia with intravenous morphine and oral paracetamol Restart of free oral intake of drinks Patient assisted out of bed to mobilize for short periods Patients send to surgical ward in case of uncomplicated minor resections Postoperative day 1 Patient sent to surgical ward in case of major resections Resume normal diet Assisted mobilization out of bed >6 h daily Postoperative day 2 Intravenous analgesia stopped Urinary catheter removed Oral analgesia (oxycodone + paracetamol) Laxatives (sodiumpicosulfate) Postoperative day 5 Aim at discharge Day 1-3 after discharge Telephone contact by project nurse The present study showed that by introducing a fasttrack program for liver resections a hospital LOS of 6 days was attained. This finding is in accordance with the results from the study by van Dam et al (9). Recently, the results from the Copenhagen group was presented and showed an even shorter LOS of 5 days after introducing their fast-track program (6). The present study, as well as previous reports, has demonstrated that fasttrack liver surgery is safe with respect to morbidity and without increasing readmission rate (6, 7). Concerning colorectal surgery, a complete fast-track program has been proposed to include 17 elements covering the perioperative phase, where implementation of a least 4 of these elements results in a reduction of both LOS and morbidity rates (4). Our program includes 13 of these elements. In our fast-track program, we chose patient-controlled analgesia with i.v. morphine for the first two postoperative days. Most previous fast-track programs have relied on epidural catheters for postoperative analgesia. Compared with i.v. morphine, epidural analgesia carries the advantages of superior analgesia (18) and faster resolution of postoperative ileus (19). However, in clinical practice a failure rate of epidural analgesia of as high as 30% occurs (20). Moreover, the use of epidural analgesia after liver resections has been associated with an increased frequency of perioperative blood transfusions not attributable to increased blood loss (21), which potentially could offset the benefit of better pain control (22, 23). In addition, postoperative coagulopathy could delay catheter removal, leading to an increased LOS (24). In our study i.v. analgesia was

3 2328 Hepato-Gastroenterology 61 (2014) Blind PJ, Andersson B, Tingstedt B, et al. Patient characteristics P Age, years, median (range) 65 (35-81) 68 (26-82) Male gender, n (%) 36 (56) 36 (58) ASA grade I or II, n (%) 51 (80) 44 (71) BMI, median (range) 26 (19-39) 25 (19-41) Diagnosis, malignant, n (%) 59 (92) 59 (95) Colorectal metastases, n (%) 53 (83) 42 (68) Other malignancy, n (%) 6 (9) 17 (27) Benign, n (%) 5 (8) 3 (5) Preoperative chemotherapy, n (%) Intraoperative data 32 (50) 23 (37) Major resections, n (%) 22 (34) 26 (42) Blood loss, median (range) 300 ( ) 500 ( ) Unilateral incision, n (%) 53 (83) 23(37) Operation duration, median (range) Postoperative data Demographics and perioperative data for the fast-track program and historic control groups. Patients with in-hospital complications, n (%) Patients with complications within 30 days of initial hospital discharge, n (%) Highest Dindo-Clavien s 250 (60-660) 340 ( ) (25) 14 (23) (38) 20 (32) Grade 0 40 (62) 42 (68) I 10 (16) 13 (21) II 9 (14) 6 (10) III 4 (6) 0 1 (1) 1 (1) Initial length-of-stay, days median (range) 6 (3-42) 8 (5-47) Readmissions, n (%) 3 (5) 6 (10) BMI body mass index, ASA American society of Anesthesiologists. stopped on POD2 in the great majority of patients and oral oxycodone was offered in addition to paracetamol. Studies have shown that postoperative oral analgesia without any morphine-analogues after liver resections is possible (6, 9), which would potentially reduce the incidence of nausea and postoperative ileus. Using the surrogate marker of administered antiemetic drugs for measuring the incidence of nausea, the incidence was fairly low in the present study. In colorectal surgery the introduction of fast-track programs has been shown to reduce morbidity (25), but no such effect has been found for liver resections. In the present study, morbidity rates did not differ between patients in the fast-track and control groups (). Several factors that have been found to increase morbidity after liver resection are difficult to influence. To minimize complications, minor resections may be preferred if possible for oncological reasons. In case of colorectal liver metastases, no oncological difference has been found between anatomical and more parenchyma-saving atypical resections (11, 26). However, anatomical resections are oncologically superior to atypical resections in case of hepatocellular carcinoma (27, 28). It has been shown that a bilateral subcostal incision is a risk factor for pulmonary complications after liver resections (29). In our series, a unilateral right-sided J-shaped incision was used for the majority of patients in the fast-track group (). This can be compared with the historical group, where a majority of patients were operated through a bilateral subcostal incision with a midline extension. This fact illustrates the problem of comparing with historical control; not everything changes abruptly with the implementation of a program but rather builds up with time and experience. Another example is the reduced blood loss and operation time in the fast-track group as compared with the historical control group, which reasonably enough depends on increased experience by the operating surgeons collaborating with the anesthesiologists. SSI occurred in 11% in the fast-track group, which is in accordance with previous results (30). Prevention of SSI is important to reduce patient morbidity and thereby reducing LOS and readmissions (31). In case of colorectal liver metastases, SSI may delay the initiation of adjuvant chemotherapy. There is a relationship between SSI and longer operative time (32) as well as poor perioperative glycemic control (33). Postoperative blood glucose levels were not analyzed in the present study. It has been argued that the parameter hospital LOS may relate more to a change in the organization of care than to an enhanced recovery (34) and that this parameter should be complemented with statistics of true functional recovery. Indeed, is can be assumed that functional recovery was attained earlier than hospital discharge in the present study in some patients. For example, patients were discharged only to a very limited extent during weekends. As shown in, the day of operation significantly influenced LOS on univariate analysis, most probably due to the fact that discharge during weekend was not encouraged. From the results of the present study, we cannot distinguish if the decrease in LOS found between the fasttrack and control groups is due to enhanced recovery, change in organization of care or increased operative experience, given the reduced blood loss and shorter operative time in the fast-track group as compared to of all three factors. Another weakness of our study is the relative small number of patients included. Discharge criteria in fast-track programs usually include only functional recovery largely neglecting psychological recovery. For liver resections, many patients are elderly which increases the incidence of postoperative confusion (35). In our study, postoperative confusion postponed hospital discharge in 2/64 patients in the fast-track group. In fast-track colorectal surgery, age, comorbidity and failure to mobilize have been shown to increase LOS (36, 37). At multivariate analysis LOS was found to depend on the extent of liver resection, the occurrence of a complication and the inability of the patient to drink >1250 ml on POD1. It is well known that major liver resections increase the rate of complications (11). The finding that

4 Fast-track Program for Liver Resection Hepato-Gastroenterology 61 (2014) 2329 the extent of liver resections and the occurrence of complications were independent predictors of increased LOS could be related to the fact that the great majority of patients subjected to major resections stayed overnight in the perioperative department. The mobilization and nutrition scheme was in this way somewhat delayed as more effort on this could be put in the ward. The result that the occurrence of a complication influences LOS is hardly surprising. However, the severity of the complication was less important than the mere incidence of any complication. One could imagine that minor complications (Dindo-Clavien grade I) should have a negligible impact on LOS. It can be speculated that the occurrence of a complication decreased the will of the patient as well as the attending physician for discharge. The reason why a significant number of patients were unable to drink an arbitrary chosen amount of >1250 ml on POD1, which was found to predict an increased LOS, is unknown. Most probable the cause is multifactorial. The observation of limited oral intake on POD1 should lead to a closer monitoring of these patients in order to detect any correctable underlying cause. In conclusion, the implementation of a fast-track program for liver resections resulted in hospital LOS in accordance with other studies on the subject. The novel findings are that in the context of fast-track surgery, factors prolonging LOS is the presence of complication, major resection as compared to minor and if the patient drinks less than 1250 ml on the first postoperative day. In-hospital complications for the fast-track program patients (n=64). 7 Postoperative ileus/ early postoperative small bowel obstruction requiring reinsertion of nasogastric tube 3 Urinary retention requiring reinsertion of urinary catheter Postoperative confusion prolonging length-of-stay 2 Intra-abdominal infection 1 Pneumonia 1 Urinary tract infection 1 Esophagitis 1 Renal failure requiring dialysis 1 Liver failure Anaesthesia, surgery, and challenges in postoperative recovery. Lancet 2003; : Enhanced recovery after surgery: a consensus review of clinical care for patients undergoing colonic resection. Clin Nutr 2005; : Evidence-based surgical care and the evolution of fast-track surgery. Ann Surg 2008; : The enhanced recovery after surgery (ERAS) pathway for patients undergoing major elective open colorectal surgery: a meta-analysis of randomized controlled trials. Clin Nutr 2010; : Fast tracking after Ivor Lewis esophagogastrectomy. Chest 2004; : Evaluation of a fasttrack programme for patients undergoing liver resection. Br J Surg 2013; : Fast-track programmes for hepatopancreatic resections: where do we stand? HPB 2011; : Implementation of a fast-track clinical pathway decreases postoperative length of stay and hospital charges for liver resection. Cell Biochem Biophys 2011; : Initial experience with a multimodal enhanced recovery programme in patients undergoing liver resection. Br J Surg 2008; : Randomized clinical trial of laxatives and oral nutritional supplements within an enhanced recovery after surgery protocol following liver resection. Br J Surg 2010; : The ex- colorectal liver metastases. Eur J Surg Oncol 2004; : Predictors of periopertative morbidity and liver dysfunction after hepatic resection in patients with chronic liver disease. HPB (Oxford) 2011; : Obesity, diabetes, and smoking are important determinants of resource utilization in liver resection: a multicenter analysis of 1029 patients. Ann Surg 2009; : Measures of Rating Scale for Pain (NRS Pain), McGill Pain Questionnaire (MPQ), Short-Form McGill Pain Questionnaire (SF-MPQ), Chronic Pain Grade Scale (CPGS), Short Form-36 Bodily Pain Scale (SF-36 BPS), and Measure of Intermittent and Constant Osteoarthritis Pain (ICOAP). Arthritis Care Res (Hoboken) 2011; :S gery patients. J Am Coll Surg 2011; : complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004; : The "50-50 criteria" on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg 2005; :824-8, discussion 8-9. trolled opiate analgesia vs. epidural analgesia following liver resection surgery. HPB (Oxford) 2012; : Effect of postoperative analgesia on major postoperative complications: a systematic update of the evidence. Anesth Analg 2007; : Failed epidural: causes and management. Br J Anaesth 2012; : Epidural analgesia in hepatic resection. J Am Coll Surg 2008; : Impact of blood loss on outcome after liver resection. Dig Surg 2007; : fusions on perioperative and long-term outcome in patients following hepatic resection for colorectal metastases. Ann Surg 2003; :860-9; discussion Epidural analgesia and liver resection: postoperative coagulation disorders and epidural catheter removal. Minerva Anestesiol 2011;77: A systematic review of enhanced recovery protocols in colorectal surgery. Ann R

5 2330 Hepato-Gastroenterology 61 (2014) Blind PJ, Andersson B, Tingstedt B, et al. BMI body mass index, ASA American society of anesthesiologists, POD postoperative day. *Kruskal-Wallis test. Age 32 5 (3-20) >65 years 32 7 (4-42) Gender male 36 6 (3-42) female 28 6 (3-20) Marital status married 45 6 (4-11) single 19 6 (3-42) BMI < (3-42) > (3-8) Diabetes yes (6-14) no 54 6 (3-42) Smoking yes 8 5 (4-9) no 56 6 (3-42) ASA grade I/II 49 6(3-42) Preoperative chemotherapy III 15 6 (3-14) yes 32 7 (3-20) no 32 6 (3-42) Day of operation Monday (3-11) Tuesday 25 6 (6-42) Wednesday 19 6 (3-19) Extent of resection major (4-20) Intraoperative blood loss Operation time (min) minor 42 6 (3-42) 49 6 (3-20) >500 ml 15 7 (4-42) 47 6 (3-14) >360 min 17 7 (6-42) Oral intake POD (4-42) >1250 ml (3-8) Complication yes 16 8 (6-42) Dindo-Clavien > grade 1 no 48 6 (3-14) yes (6-42) no 54 6 (3-14) * Coll Surg Engl 2011; : Resection margin with anatomic or nonanatomic hepatectomy for liver metastasis from colorectal cancer. J Gastrointest Surg 2012; : Risk factors of postoperative recurrence and adequate surgical approach to improve long-term outcomes of hepatocellular carcinoma. HPB (Oxford) 2013; :31-9. Anatomic resection independently improves long-term survival in patients with T1-T2 hepatocellular carcinoma. Ann Surg Oncol 2007; : Multivariate analysis of risk factors for pulmonary complications after hepatic resection. Ann Surg 2012; : Predictors of surgical site infection after liver resection: a multicentre analysis using National Surgical Quality Improvement Program data. HPB (Oxford) 2012; : The impact of surgical-site infections in the 1990s: attributable mortality, excess length of hospitalization, and extra costs. Infect Control Hosp Epidemiol 1999; : Predictive factors for surgical site infection in general surgery. Surgery 2008; : ; discussion -3. Poor postoperative blood glucose control increases surgical site infections after surgery for hepato-biliary-pancreatic cancer: a prospective study in a high-volume institute in Japan. J Hosp Infect 2008; : Length of stay: an inappropriate readout of the success of enhanced recovery programs. World J Surg 2008; : Safety of liver resection in the elderly: how important is age? Ann Surg Oncol 2011; : Factors predicting deviation from an enhanced recovery programme and delayed discharge after laparoscopic colorectal surgery. Colorectal Dis 2012; :e Hospital stay amongst patients undergoing major elective colorectal surgery: predicting prolonged stay and readmissions in NHS hospitals. Colorectal Dis 2011; :

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