ORIGINAL ARTICLE
A Case-matched Comparative Study of Laparoscopic Versus Open Distal Pancreatectomy Yazan S. Khaled, MPhil, MBChb, BSc,*w Deep J. Malde, FRCS,* Jessica Packer, MRCS,* Nicola De Liguori Carino, FRCS,* Rahul Deshpande, FRCS,* Derek A. O’Reilly, FRCS,*w David J. Sherlock, FRCS,* and Basil J. Ammori, FRCS, MD*w
Introduction: Although the laparoscopic approach to distal pancreatectomy for benign and malignant diseases is largely replacing open surgery in some centers, well-designed studies comparing these approaches are limited. We present a case-matched study that compares the outcomes of laparoscopic distal pancreatectomy (LDP) to open distal pancreatectomy (ODP). Methods: Of 112 patients (51 female) who underwent surgery between January 2002 and December 2011, 44 patients were matched on a 1:1 basis (22 LDP, 22 ODP) according to age, sex, and tumor size. Outcomes were compared on an intention-to-treat basis. Data shown represent median where appropriate. Results: The laparoscopic and open groups were comparable for age (57 vs. 59.9 y, P = 0.980), sex distribution (P = 1.000), tumor size (3 vs. 4 cm, P = 0.904), and the frequency of benign versus malignant disease (P = 0.920). LDP was associated with significantly lower blood loss (100 vs. 500 mL, P = 0.001), higher spleen preservation rate (45% vs. 18%, P = 0.029), as well as shorter high dependency unit stay (1 vs. 5 d, P = 0.001) and postoperative hospital stay (5 vs. 14 d, P = 0.017). There was no significant difference in operating time (245 vs. 240 min, P = 0.602) and postoperative morbidity (13.6% vs. 27.2%, P = 0.431). In patients with malignant disease, there were no differences in R0 resection margin status (90% vs. 85.7%, P = 0.88), the numbers of lymph nodes retrieved (12.7 vs. 14.1, P = 0.82), the 1- and 2-year survival rates (89% vs. 81%, P = 0.54 and 74.2% vs. 71.5%, P = 0.63, respectively), and the mean duration of survival (45 vs. 31 mo, P = 0.157). Conclusions: The laparoscopic approach to distal pancreatectomy offers advantages over open surgery in terms of reductions in operative trauma and duration of postoperative recovery without compromising the oncologic resection. Key Words: distal pancreatectomy, pancreatic ductal adenocarcinoma, pancreatic neuroendocrine tumors, laparoscopic pancreatectomy, pancreatic fistula
(Surg Laparosc Endosc Percutan Tech 2015;25:363–367)
T
he advances in minimally invasive technology and operative techniques in the last decade have yielded an increase in popularity of the laparoscopic approach to
Received for publication December 8, 2014; accepted April 6, 2015. From the *The Hepato-Pancreato-Biliary Unit, North Manchester General Hospital; and wInstitute of Cardiovascular Sciences, The University of Manchester, Manchester, UK. The author declares no conflicts of interest. Reprints: Basil J. Ammori, FRCS, MD, The Hepato-Pancreato-Biliary Unit, North Manchester General Hospital, Delaunays Road, Crumpsall, Manchester, M8 5RB, United Kingdom (e-mail: [email protected]). Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
Surg Laparosc Endosc Percutan Tech
pancreatic resections, and this is particularly adapted to distal pancreatectomy (DP) wherein no reconstruction is required. Several retrospective studies have demonstrated the safety and feasibility of laparoscopic distal pancreatectomy (LDP).1–6 Although technically demanding, the laparoscopic approach to DP benefits from the avoidance of a large incision to access this deep-seated retroperitoneal organ, an enhanced operative vision and access, and the relatively small specimen to retrieve.7 Although some authors advocate that the laparoscopic approach should become the gold standard for the treatment of lesions in the distal pancreas,2 no randomized controlled trials comparing LDP with open distal pancreatectomy (ODP) have been conducted. However, a limited number of well-designed comparative studies exist,1,8–12 and further evidence is needed. We report a comparative study of LDP versus ODP within a casematched cohort design in an attempt to better elucidate whether the laparoscopic approach offers advantages over open surgery and whether this could be accomplished without oncologic drawbacks.
MATERIALS AND METHODS Patient Population All patients who underwent DP for pancreatic pathology by surgeons at our tertiary referral unit were considered for the study. Patients who underwent LDP from the beginning of our learning curve in 2002 were included, whereas patients who underwent ODP from 2002 were considered. One surgeon (B.J.A.) performed LDP in all comers, whereas others were either selective or performed ODP in all patients. Patients were excluded if they had DP for nonpancreatic pathology or other forms of pancreatic resections such as enucleation, median pancreatectomy, or total pancreatectomy.
Surgical Principles The operative technique, especially that of LDP, has been discussed in detail in a previous publication by Ammori and Ayiomamitis.13 Briefly, for lesions in the tail of the pancreas, the patient is placed in the right lateral or semilateral position, whereas the supine French position is adopted for lesions in the body of the pancreas. For lesions in the tail of the gland, a distal-to-proximal approach was adopted. The body and tail of the pancreas were exposed, the location of the lesion confirmed with laparoscopic ultrasound, and the potential presence of further lesions explored. The dissection proceeded from the tail of the pancreas toward the body. For lesions in the body of the
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pancreas, a proximal to distal approach was adopted. Whenever the resection was destined, on preoperative imaging, to involve transection of the neck of the pancreas, the superior mesenteric vein and portal vein were dissected and the junction with the splenic vein identified. The pancreas was then transected with an endo-GIA (Ethicon Endo-Surgery) or with an ultrasonically activated scalpel and the stump is oversewn with 3-0 Prolene suture if bleeding was encountered. An attempt was made to conserve the spleen in patients with benign pathology or low-grade malignancy. Although splenic conservations in the majority of patients involved preservation of the splenic artery and vein, splenic conservation with the sacrifice of splenic artery, splenic vein, or both vessels (the Warshaw technique14) was also performed in some patients. In case of DP with splenectomy, division of the splenic artery preceded that of the vein whenever possible. Once the pancreas was also transected, a medial to lateral dissection posterior to the splenic vein along the retroperitoneal plane was facilitated and the spleen was finally detached from its ligamentous attachments en bloc. Open surgery was carried through a bilateral subcostal or upper transverse abdominal incision, and similar operative technique and principles were applied as described above.
Postoperative Management Nasogastric tubes, when used, were removed as early as possible. Free oral fluids and subsequently light diet were introduced postoperatively as early as deemed appropriate and tolerable by the patient. A specimen from the drain fluid was sent for measurement of amylase concentration after 72 hours, and the drain was removed if no fistula was detected. Octreotide was administered routinely until removal of the drain. All patients were followed up regularly in the surgical clinic and regular cross-sectional imaging was undertaken as appropriate.
Study Design Patients who underwent DP between January 2002 and December 2011 were identified through screening the theater register and our prospective hospital database, and their clinical records were reviewed for data collection. Patients who underwent LDP were matched to those who have had ODP on a 1:1 basis. The matching criteria included age (±5 y), tumor size (±2 cm), and sex. When >1 subject met the matching criteria, controls were chosen at random. Clinicopathologic characteristics and perioperative outcomes were recorded. We reviewed each patient’s history for age, sex, body mass index, American Society of Anaesthesiologists’ grade, pathologic diagnosis, tumor size, and concomitant operations. Comparisons between the 2 surgical approaches included operative parameters (operative time, intraoperative blood loss, and blood transfusion rate), postoperative recovery (length of hospital stay, overall complications, postoperative pancreatic fistula (POPF) rate, and mortality), as well as oncologic safety (margin status) and survival in patients with malignant pathology.
Definitions Postoperative mortality was defined as the number of deaths that occurred for any reason within 30 days after surgery or in-hospital regardless of duration of hospital stay. Postoperative morbidity rate included all complications within 30 days of surgery. Complications were graded
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according to the Dindo-Clavien classification.15,16 The criteria of the International Study Group on Pancreatic Fistula were used to define and grade POPF.17 The length of hospital stay was defined as the interval from the day of surgery to discharge. Operative time was defined as the interval (minutes) from first incision to closure of the last skin wound.
Statistical Analysis Categorical variables were presented in proportions and continuous variables as median (range). Data were analyzed using the software package SPSS version 17 (Chicago, IL). Comparison between groups was performed on intention-totreat basis using the Mann-Whitney U test, the independent t test, and the w2 test as appropriate. Significance was accepted at the 5% level. Survival after resection for malignant disease was compared using the Kaplan-Meier survival analysis with the log rank significance test.
RESULTS Patient Characteristics Of 112 patients who underwent DP, 74 (24 LDP, 50 DP) had complete data for analysis during the study period. The case-matched cohort consisted of 44 patients (22 LDP vs. 22 ODP). Patients who underwent LDP were comparable to those who underwent ODP with regard to age, sex, American Society of Anaesthesiologists score, and body mass index (Table 1).
Intraoperative Characteristics These are shown in Table 2. LDP was associated with significantly lower blood loss but there was no difference in the intraoperative transfusion requirements between the 2 groups. Although the median operating time of LDP was shorter than that of ODP, the difference was not statistically significant. There was 1 conversion (4.5%) to open surgery due to bleeding from the splenic vein. The overall splenic preservation rate was significantly higher in the laparoscopic group.
Pathologic Characteristics Table 3 shows the histopathologic results. There was no significant difference in the distribution of benign, intermediate, and malignant disease and no difference in the maximum diameter of the resected lesion on histology. The R0 resection margins for the neuroendocrine tumors and the ductal adenocarcinoma and the numbers of lymph nodes that were retrieved showed no significant differences between the laparoscopic and open groups.
Postoperative Outcomes These are shown in Table 4. There was no significant difference in the postoperative morbidity, and the frequency TABLE 1. Patient Characteristics Sex: F/M Age* ASA grade* BMI (kg/m2)*
LDP (n = 22)
ODP (n = 22)
P
14/8 57 (34-78) 2 26.5 (21.5-70.2)
14/8 59.9 (32-78) 2 28.3 (24-36.6)
1 0.98 0.9 0.4
*Data shown represent median (range). ASA indicates American Society of Anesthesiologists; BMI, body mass index; LDP, laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
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TABLE 2. Operative Outcomes
TABLE 4. Postoperative Outcomes
LDP (n = 22)
ODP (n = 22)
LDP (n = 22) ODP (n = 22) P
Operating time (min)* 245 (105-400) 240 (120-405) 0.602 Blood loss (mL)* 100 (50-800) 500 (150-1700) 0.001 Intraoperative blood 0 (0-2) 0 (0-8) 0.163 transfusion (U)* Spleen preservation [n (%)] 10 (45) 4 (18) 0.029 Conversion to open surgery 1 (4.5) Not applicable [n (%)] *Data shown represent median (range). LDP indicates laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
of grades A and B POPF; there were no grade C fistulae in either cohort. LDP was associated with significantly shorter durations of postoperative stay on high dependency unit/ intensive therapy unit and total hospital stay. The postoperative complications are listed in Table 5. There were 2 deaths in the entire cohort of patients. A 56-yearold man, who underwent ODP for a neuroendocrine tumor succumbed to septic complications on the eighth postoperative day after re-laparotomy for small bowel obstruction. Another 73-year-old man, who underwent LDP for neuroendocrine tumor, developed acute liver failure secondary to metastatic liver disease on the seventh postoperative day. There were 4 patients who needed re-laparotomy in the ODP cohort for small bowel perforation (n = 1), small bowel obstruction (n = 1), and bleeding (n = 2).
Follow-up The overall median (range) follow-up was 22 (0 to 72) and 18 (0 to 84) months for the laparoscopic and open groups, respectively (P = 0.731). Among patients with malignant disease, 15 of 18 patients in the LDP group and 11 of 16 patients in the ODP group were alive at the time of reporting. Comparable outcomes were observed after LDP
TABLE 3. Histopathologic Results
Tumour diameter (cm)* Pathology Benign Serous cystadenoma Mucinous cystadenoma Pancreatitis/pseudocyst Malignant IPMN NET Adenocarcinoma Other Resection margins (R0) [n (%)] No. nodes retrieved
LDP (n = 22)
ODP (n = 22)
3 (0.7-12)
4 (1.5-8.3)
4 0 2 2/0 18 0 9 4 5 18/20 (90)
6 2 2 1/1 16 1 8 5 2 17/20 (85)
0.88
12.7
14.1
0.82
P 0.904 0.92
r
Complications [n (%)] Dindo-Clavien classification 1 2 3a 3b 4a 4b Pancreatic fistula [n (%)] A B C HDU/ITU stay (d)* Total hospital stay (d)* Mortality [n (%)]
P
3 (13.6)
6 (27.2)
0.431
0 2 0 0 1 0 6 (27.2) 2 4 0 1 (0-7) 5 (2-20) 1 (4.2)
0 2 0 3 0 1 5 (22.7) 3 2 0 5 (0-33) 14 (4-154) 1 (4.2)
0.82
0.001 0.017 1
*Data shown represent median (range). HDU indicates high dependency unit; ITU, intensive therapy unit; LDP, laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
and ODP for malignant disease in terms of survival rates at 1 and 2 years (89% vs. 81%, P = 0.54 and 74.2% vs. 71.5%, P = 0.63, respectively) and the mean duration of survival (45 vs. 31 mo, P = 0.157) (Fig. 1).
DISCUSSION This case-matched comparative study of LDP versus ODP demonstrated that the laparoscopic approach offered advantages in terms of reductions in blood loss and lengths of intensive care and postoperative hospital stay as well as a higher spleen preservation rate, while offering comparative oncologic resections and outcomes in the subgroup of patients with malignant disease. The feasibility and safety of LDP was demonstrated by the low rate of conversion to open surgery and comparative postoperative morbidity and mortality to those observed with open surgery. A recent review of published comparative studies of LDP versus ODP showed similar findings as the laparoscopic approach was associated with significantly reduced blood loss (mean, 237 vs. 562 mL, P < 0.001), shorter postoperative hospital stay (mean, 9.1 vs. 14.7 d, P < 0.001), and lower morbidity (30.5% vs. 38.4%, P = 0.007).18 Our overall morbidity rate after LDP was lower than that of ODP (13.6% vs. 27.2%); however, the difference was not statistically significant. Although our relatively small series does not
TABLE 5. Details of Postoperative Complications
*Data shown represent median (range). IPMN indicates intraductal papillary neoplasm; LDP, laparoscopic distal pancreatectomy; NET, neuroendocrine tumor; ODP, open distal pancreatectomy.
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Pancreatic fistula Liver failure Cardiac Respiratory Hemorrhage Small bowel obstruction Re-laparotomy
LDP (n = 22)
ODP (n = 22)
6 1 1 1 0 0 0
5 0 2 0 2 1 4*
*Re-laparotomy for small bowel perforation (n = 1), small bowel perforation (n = 1), and postoperative hemorrhage (n = 2). LDP indicates laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
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FIGURE 1. Kaplan-Meier survival curve for laparoscopic versus open distal pancreatectomy (LDP vs. ODP) in patients with malignant pathology: the mean survival was 45 versus 31 months, P = 0.157 (log rank test).
allow for a meaningful comparison of operative mortality, the literature review of previously published comparative studies of LDP versus ODP found no differences between the 2 approaches in this regard (0.6% vs. 0.5%).18 The rates of POPF after LDP reported in the literature ranged from 0% to 50%.5,9,10,18 The rates of POPF after LDP were comparable to those seen after ODP both in this report (27.5% vs. 22.7%) and in the recent literature review (16.1% vs. 19.5%, P = 0.154)18; all POPFs in our series were of grades A and B that resolved with conservative management and none of the patients had grade C POPF. The factors associated with the development of POPF were not evaluated in this study. The operating time of LDP was comparable to that of ODP in this study and was not dissimilar from that reported in the literature review in which no differences were observed between the 2 approaches (mean, 220 vs. 209 min).18 Preservation of the spleen prolongs operating time as Eom et al19 demonstrated during laparoscopic DP (mean, 194 vs. 251 min, P = 0.020). The spleen preservation rate in various series of LDP ranged between 32% and 84%.3,10,20,21 Our spleen preservation rate after LDP significantly exceeded that accomplished after ODP (45% vs. 18%) in this case-matched study design with comparable tumor size and pathology. These findings are similar to those reported in the recent literature review of LDP versus ODP (median, 37.8% vs. 8.0%, P < 0.001).18 The higher spleen preservation rate therefore appears to be a true advantage of the laparoscopic approach and this could be attributed to the better vision afforded by the magnification used in laparoscopy that aids the fine dissection of the pancreas off the splenic vessels and the splenic hilum. The oncologic clearance achieved with laparoscopic surgery appears comparable to that observed after ODP. In
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the current study, the rates of positive resection margin in patients with malignant disease for LDP and ODP (10% vs. 15%) and the number of lymph nodes retrieved (median, 12.7 vs. 14.1) were comparable with no statistically significant difference in their overall survival after a median follow-up of 22 and 18 months, respectively. In their multicenter comparative analysis of LDP versus ODP for pancreatic ductal adenocarcinoma, Kooby et al found no difference in the rates of positive resection margin (27% vs. 26%), the number of nodes retrieved (mean, 13.8 vs. 12.5), and the overall survival (median, 16 mo in each group).20 Kooby et al conducted a multivariate analysis of factors predictive of poor survival and found that the surgical approach (laparoscopic or open surgery) did not have an impact, but advanced age, large tumors, positive margins, and node positive disease were independently associated with worse survival.20 In another report of LDP in 27 patients with malignancy, Ferna´ndez-Cruz et al7 were able to achieve R0 resection in 90% of ductal adenocarcinoma patients with a mean lymph node count of 14.5. A recent meta-analysis of LDP versus ODP reported no differences in terms of the extent of oncologic clearance.21 In contrast, the single-institution study by Baker et al5 reported a significantly lower lymph node retrieval rate with LDP compared with ODP (mean, 5.2 vs. 9.4, P = 0.4), but their rates were rather low in both groups. The role of LDP for malignancy, nonetheless, still remains controversial, and some surgeons perform open surgery on all patients with preoperative22 or intraoperative23 diagnosis of malignancy, whereas others performed laparoscopic resection if judged technically feasible.1,5,10 Malignancy was one of the reasons in some studies for conversion from laparoscopic to open surgery, either for technical difficulties8 or on principle.23 It is useful to note, however, that comparative studies that included fairly similar proportions of malignant resections in the laparoscopic and open groups found no evidence of increased operative morbidity with the laparoscopic approach.1,10,19 The 2 largest meta-analyses comparing LDP versus ODP reported a shorter length of hospital stay, lower blood loss, and risk of postoperative morbidity, without difference in operative time, margin positivity, incidence of postoperative pancreatic fistula, and mortality.4,21 A potential drawback of laparoscopic surgery is the likelihood of higher cost compared with open surgery. In a comparative study of LDP versus ODP, Hilal et al24 showed that LDP did not have a negative impact on cost. Although we did not examine cost, the shorter operating time and the significantly shorter intensive care and hospital stays that we observed with LDP would undoubtedly have had a favorable impact on the overall cost of that surgical episode. There are limitations to the current study. Although we attempted to circumvent selection bias through cohort matching, a certain degree of bias is inherent within any study outside of a randomized controlled design. However, the relative infrequency of pancreatic diseases that require DP renders the conduction of a randomized trial with sufficient sample size and statistical power challenging, although potentially achievable in a multicenter multinational setting. There is an operator bias regarding the selection of surgical approach among the 5 surgeons involved in the study, with some routinely performing either laparoscopic or open surgery in all comers, whereas others adopted a highly selective approach toward laparoscopy; this limits generalizability of the findings of this study. In addition, tumors were a little larger in the open group (median, 4 vs. 3.2 cm) and the study
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was not powered enough to identify this as a statistically significant difference.
CONCLUSIONS In conclusion, the findings of this case-matched comparative study suggest that the laparoscopic approach to DP offered advantages over open surgery in terms of operative trauma and postoperative recovery as well as the ability to preserve the spleen when indicated, and this was achieved without compromising the oncologic resection. However, the effectiveness of the laparoscopic approach to DP should be evaluated in an adequately powered randomized controlled trial. REFERENCES 1. Vijan SS, Ahmed KA, Harmsen WS, et al. Laparoscopic vs open distal pancreatectomy: a single-institution comparative study. Arch Surg. 2010;145:616–621. 2. Teh SH, Tseng D, Sheppard BC. Laparoscopic and open distal pancreatic resection for benign pancreatic disease. J Gastrointest Surg. 2007;11:1120–1125. 3. DiNorcia J, Schrope BA, Lee MK, et al. Laparoscopic distal pancreatectomy offers shorter hospital stays with fewer complications. J Gastrointest Surg. 2010;14:1804–1812. 4. Venkat R, Edil BH, Schulick RD, et al. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg. 2012;255:1048–1059. 5. Baker MS, Bentrem DJ, Ujiki MB, et al. A prospective single institution comparison of peri-operative outcomes for laparoscopic and open distal pancreatectomy. Surgery. 2009;146:635–645. 6. Taylor C, O’rourke N, Nathanson L, et al. Laparoscopic distal pancreatectomy: the Brisbane experience of forty-six cases. HPB (Oxford). 2008;10:38–42. 7. Ferna´ndez-Cruz L, Blanco L, Cosa R, et al. Is laparoscopic resection adequate in patients with neuroendocrine pancreatic tumors? World J Surg. 2008;32:904–917. 8. Velanovich V. Case-control comparison of laparoscopic versus open distal pancreatectomy. J Gastrointest Surg. 2006;10:95–98. 9. Matsumoto T, Shibata K, Ohta M, et al. Laparoscopic distal pancreatectomy and open distal pancreatectomy: a nonrandomized comparative study. Surg Laparosc Endosc Percutan Tech. 2008;18:340–343.
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10. Casadei R, Ricci C, D’Ambra M, et al. Laparoscopic versus open distal pancreatectomy in pancreatic tumours: a case– control study. Updates Surg. 2010;62:171–174. 11. Mehta SS, Doumane G, Mura T, et al. Laparoscopic versus open distal pancreatectomy: a single-institution casecontrol study. Surg Endosc. 2012;26:402–407. 12. Rehman S, John S, Lochan R, et al. Oncological feasibility of laparoscopic distal pancreatectomy for adenocarcinoma: a single-institution comparative study. World J Surg. 2014; 38:476–483. 13. Ammori BJ, Ayiomamitis GD. Laparoscopic pancreaticoduodenectomy and distal pancreatectomy: a UK experience and a systematic review of the literature. Surg Endosc. 2011;25: 2084–2099. 14. Warshaw AL. Conservation of the spleen with distal pancreatectomy. Arch Surg. 1988;123:550–553. 15. Clavien P-A, Sanabria JR, Strasberg SM. Proposed classification of complications of surgery with examples of utility in cholecystectomy. Surgery. 1992;111:518–526. 16. Dindo D, Demartines N, Clavien P-A. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–213. 17. Bassi C, Dervenis C, Butturini G, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138:8–13. 18. Jusoh AC, Ammori BJ. Laparoscopic versus open distal pancreatectomy: a systematic review of comparative studies. Surg Endosc. 2012;26:904–913. 19. Eom B, Jang J-Y, Lee S, et al. Clinical outcomes compared between laparoscopic and open distal pancreatectomy. Surg Endosc. 2008;22:1334–1338. 20. Kooby DA, Gillespie T, Bentrem D, et al. Left-sided pancreatectomy: a multicenter comparison of laparoscopic and open approaches. Ann Surg. 2008;248:438–446. 21. Sui C-J, Li B, Yang J-M, et al. Laparoscopic versus open distal pancreatectomy: a meta-analysis. Asian J Surg. 2012;35:1–8. 22. Tang C, Tsui K, Ha J, et al. Laparoscopic distal pancreatectomy: a comparative study. Hepatogastroenterology. 2007;54: 265–271. 23. Nakamura Y, Uchida E, Aimoto T, et al. Clinical outcome of laparoscopic distal pancreatectomy. J Hepatobiliary Pancreat Surg. 2009;16:35–41. 24. Hilal MA, Hamdan M, Di Fabio F, et al. Laparoscopic versus open distal pancreatectomy: a clinical and cost-effectiveness study. Surg Endosc. 2012;26:1670–1674.
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367
A Case-matched Comparative Study of Laparoscopic Versus Open Distal Pancreatectomy Yazan S. Khaled, MPhil, MBChb, BSc,*w Deep J. Malde, FRCS,* Jessica Packer, MRCS,* Nicola De Liguori Carino, FRCS,* Rahul Deshpande, FRCS,* Derek A. O’Reilly, FRCS,*w David J. Sherlock, FRCS,* and Basil J. Ammori, FRCS, MD*w
Introduction: Although the laparoscopic approach to distal pancreatectomy for benign and malignant diseases is largely replacing open surgery in some centers, well-designed studies comparing these approaches are limited. We present a case-matched study that compares the outcomes of laparoscopic distal pancreatectomy (LDP) to open distal pancreatectomy (ODP). Methods: Of 112 patients (51 female) who underwent surgery between January 2002 and December 2011, 44 patients were matched on a 1:1 basis (22 LDP, 22 ODP) according to age, sex, and tumor size. Outcomes were compared on an intention-to-treat basis. Data shown represent median where appropriate. Results: The laparoscopic and open groups were comparable for age (57 vs. 59.9 y, P = 0.980), sex distribution (P = 1.000), tumor size (3 vs. 4 cm, P = 0.904), and the frequency of benign versus malignant disease (P = 0.920). LDP was associated with significantly lower blood loss (100 vs. 500 mL, P = 0.001), higher spleen preservation rate (45% vs. 18%, P = 0.029), as well as shorter high dependency unit stay (1 vs. 5 d, P = 0.001) and postoperative hospital stay (5 vs. 14 d, P = 0.017). There was no significant difference in operating time (245 vs. 240 min, P = 0.602) and postoperative morbidity (13.6% vs. 27.2%, P = 0.431). In patients with malignant disease, there were no differences in R0 resection margin status (90% vs. 85.7%, P = 0.88), the numbers of lymph nodes retrieved (12.7 vs. 14.1, P = 0.82), the 1- and 2-year survival rates (89% vs. 81%, P = 0.54 and 74.2% vs. 71.5%, P = 0.63, respectively), and the mean duration of survival (45 vs. 31 mo, P = 0.157). Conclusions: The laparoscopic approach to distal pancreatectomy offers advantages over open surgery in terms of reductions in operative trauma and duration of postoperative recovery without compromising the oncologic resection. Key Words: distal pancreatectomy, pancreatic ductal adenocarcinoma, pancreatic neuroendocrine tumors, laparoscopic pancreatectomy, pancreatic fistula
(Surg Laparosc Endosc Percutan Tech 2015;25:363–367)
T
he advances in minimally invasive technology and operative techniques in the last decade have yielded an increase in popularity of the laparoscopic approach to
Received for publication December 8, 2014; accepted April 6, 2015. From the *The Hepato-Pancreato-Biliary Unit, North Manchester General Hospital; and wInstitute of Cardiovascular Sciences, The University of Manchester, Manchester, UK. The author declares no conflicts of interest. Reprints: Basil J. Ammori, FRCS, MD, The Hepato-Pancreato-Biliary Unit, North Manchester General Hospital, Delaunays Road, Crumpsall, Manchester, M8 5RB, United Kingdom (e-mail: [email protected]). Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
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pancreatic resections, and this is particularly adapted to distal pancreatectomy (DP) wherein no reconstruction is required. Several retrospective studies have demonstrated the safety and feasibility of laparoscopic distal pancreatectomy (LDP).1–6 Although technically demanding, the laparoscopic approach to DP benefits from the avoidance of a large incision to access this deep-seated retroperitoneal organ, an enhanced operative vision and access, and the relatively small specimen to retrieve.7 Although some authors advocate that the laparoscopic approach should become the gold standard for the treatment of lesions in the distal pancreas,2 no randomized controlled trials comparing LDP with open distal pancreatectomy (ODP) have been conducted. However, a limited number of well-designed comparative studies exist,1,8–12 and further evidence is needed. We report a comparative study of LDP versus ODP within a casematched cohort design in an attempt to better elucidate whether the laparoscopic approach offers advantages over open surgery and whether this could be accomplished without oncologic drawbacks.
MATERIALS AND METHODS Patient Population All patients who underwent DP for pancreatic pathology by surgeons at our tertiary referral unit were considered for the study. Patients who underwent LDP from the beginning of our learning curve in 2002 were included, whereas patients who underwent ODP from 2002 were considered. One surgeon (B.J.A.) performed LDP in all comers, whereas others were either selective or performed ODP in all patients. Patients were excluded if they had DP for nonpancreatic pathology or other forms of pancreatic resections such as enucleation, median pancreatectomy, or total pancreatectomy.
Surgical Principles The operative technique, especially that of LDP, has been discussed in detail in a previous publication by Ammori and Ayiomamitis.13 Briefly, for lesions in the tail of the pancreas, the patient is placed in the right lateral or semilateral position, whereas the supine French position is adopted for lesions in the body of the pancreas. For lesions in the tail of the gland, a distal-to-proximal approach was adopted. The body and tail of the pancreas were exposed, the location of the lesion confirmed with laparoscopic ultrasound, and the potential presence of further lesions explored. The dissection proceeded from the tail of the pancreas toward the body. For lesions in the body of the
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pancreas, a proximal to distal approach was adopted. Whenever the resection was destined, on preoperative imaging, to involve transection of the neck of the pancreas, the superior mesenteric vein and portal vein were dissected and the junction with the splenic vein identified. The pancreas was then transected with an endo-GIA (Ethicon Endo-Surgery) or with an ultrasonically activated scalpel and the stump is oversewn with 3-0 Prolene suture if bleeding was encountered. An attempt was made to conserve the spleen in patients with benign pathology or low-grade malignancy. Although splenic conservations in the majority of patients involved preservation of the splenic artery and vein, splenic conservation with the sacrifice of splenic artery, splenic vein, or both vessels (the Warshaw technique14) was also performed in some patients. In case of DP with splenectomy, division of the splenic artery preceded that of the vein whenever possible. Once the pancreas was also transected, a medial to lateral dissection posterior to the splenic vein along the retroperitoneal plane was facilitated and the spleen was finally detached from its ligamentous attachments en bloc. Open surgery was carried through a bilateral subcostal or upper transverse abdominal incision, and similar operative technique and principles were applied as described above.
Postoperative Management Nasogastric tubes, when used, were removed as early as possible. Free oral fluids and subsequently light diet were introduced postoperatively as early as deemed appropriate and tolerable by the patient. A specimen from the drain fluid was sent for measurement of amylase concentration after 72 hours, and the drain was removed if no fistula was detected. Octreotide was administered routinely until removal of the drain. All patients were followed up regularly in the surgical clinic and regular cross-sectional imaging was undertaken as appropriate.
Study Design Patients who underwent DP between January 2002 and December 2011 were identified through screening the theater register and our prospective hospital database, and their clinical records were reviewed for data collection. Patients who underwent LDP were matched to those who have had ODP on a 1:1 basis. The matching criteria included age (±5 y), tumor size (±2 cm), and sex. When >1 subject met the matching criteria, controls were chosen at random. Clinicopathologic characteristics and perioperative outcomes were recorded. We reviewed each patient’s history for age, sex, body mass index, American Society of Anaesthesiologists’ grade, pathologic diagnosis, tumor size, and concomitant operations. Comparisons between the 2 surgical approaches included operative parameters (operative time, intraoperative blood loss, and blood transfusion rate), postoperative recovery (length of hospital stay, overall complications, postoperative pancreatic fistula (POPF) rate, and mortality), as well as oncologic safety (margin status) and survival in patients with malignant pathology.
Definitions Postoperative mortality was defined as the number of deaths that occurred for any reason within 30 days after surgery or in-hospital regardless of duration of hospital stay. Postoperative morbidity rate included all complications within 30 days of surgery. Complications were graded
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according to the Dindo-Clavien classification.15,16 The criteria of the International Study Group on Pancreatic Fistula were used to define and grade POPF.17 The length of hospital stay was defined as the interval from the day of surgery to discharge. Operative time was defined as the interval (minutes) from first incision to closure of the last skin wound.
Statistical Analysis Categorical variables were presented in proportions and continuous variables as median (range). Data were analyzed using the software package SPSS version 17 (Chicago, IL). Comparison between groups was performed on intention-totreat basis using the Mann-Whitney U test, the independent t test, and the w2 test as appropriate. Significance was accepted at the 5% level. Survival after resection for malignant disease was compared using the Kaplan-Meier survival analysis with the log rank significance test.
RESULTS Patient Characteristics Of 112 patients who underwent DP, 74 (24 LDP, 50 DP) had complete data for analysis during the study period. The case-matched cohort consisted of 44 patients (22 LDP vs. 22 ODP). Patients who underwent LDP were comparable to those who underwent ODP with regard to age, sex, American Society of Anaesthesiologists score, and body mass index (Table 1).
Intraoperative Characteristics These are shown in Table 2. LDP was associated with significantly lower blood loss but there was no difference in the intraoperative transfusion requirements between the 2 groups. Although the median operating time of LDP was shorter than that of ODP, the difference was not statistically significant. There was 1 conversion (4.5%) to open surgery due to bleeding from the splenic vein. The overall splenic preservation rate was significantly higher in the laparoscopic group.
Pathologic Characteristics Table 3 shows the histopathologic results. There was no significant difference in the distribution of benign, intermediate, and malignant disease and no difference in the maximum diameter of the resected lesion on histology. The R0 resection margins for the neuroendocrine tumors and the ductal adenocarcinoma and the numbers of lymph nodes that were retrieved showed no significant differences between the laparoscopic and open groups.
Postoperative Outcomes These are shown in Table 4. There was no significant difference in the postoperative morbidity, and the frequency TABLE 1. Patient Characteristics Sex: F/M Age* ASA grade* BMI (kg/m2)*
LDP (n = 22)
ODP (n = 22)
P
14/8 57 (34-78) 2 26.5 (21.5-70.2)
14/8 59.9 (32-78) 2 28.3 (24-36.6)
1 0.98 0.9 0.4
*Data shown represent median (range). ASA indicates American Society of Anesthesiologists; BMI, body mass index; LDP, laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
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TABLE 2. Operative Outcomes
TABLE 4. Postoperative Outcomes
LDP (n = 22)
ODP (n = 22)
LDP (n = 22) ODP (n = 22) P
Operating time (min)* 245 (105-400) 240 (120-405) 0.602 Blood loss (mL)* 100 (50-800) 500 (150-1700) 0.001 Intraoperative blood 0 (0-2) 0 (0-8) 0.163 transfusion (U)* Spleen preservation [n (%)] 10 (45) 4 (18) 0.029 Conversion to open surgery 1 (4.5) Not applicable [n (%)] *Data shown represent median (range). LDP indicates laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
of grades A and B POPF; there were no grade C fistulae in either cohort. LDP was associated with significantly shorter durations of postoperative stay on high dependency unit/ intensive therapy unit and total hospital stay. The postoperative complications are listed in Table 5. There were 2 deaths in the entire cohort of patients. A 56-yearold man, who underwent ODP for a neuroendocrine tumor succumbed to septic complications on the eighth postoperative day after re-laparotomy for small bowel obstruction. Another 73-year-old man, who underwent LDP for neuroendocrine tumor, developed acute liver failure secondary to metastatic liver disease on the seventh postoperative day. There were 4 patients who needed re-laparotomy in the ODP cohort for small bowel perforation (n = 1), small bowel obstruction (n = 1), and bleeding (n = 2).
Follow-up The overall median (range) follow-up was 22 (0 to 72) and 18 (0 to 84) months for the laparoscopic and open groups, respectively (P = 0.731). Among patients with malignant disease, 15 of 18 patients in the LDP group and 11 of 16 patients in the ODP group were alive at the time of reporting. Comparable outcomes were observed after LDP
TABLE 3. Histopathologic Results
Tumour diameter (cm)* Pathology Benign Serous cystadenoma Mucinous cystadenoma Pancreatitis/pseudocyst Malignant IPMN NET Adenocarcinoma Other Resection margins (R0) [n (%)] No. nodes retrieved
LDP (n = 22)
ODP (n = 22)
3 (0.7-12)
4 (1.5-8.3)
4 0 2 2/0 18 0 9 4 5 18/20 (90)
6 2 2 1/1 16 1 8 5 2 17/20 (85)
0.88
12.7
14.1
0.82
P 0.904 0.92
r
Complications [n (%)] Dindo-Clavien classification 1 2 3a 3b 4a 4b Pancreatic fistula [n (%)] A B C HDU/ITU stay (d)* Total hospital stay (d)* Mortality [n (%)]
P
3 (13.6)
6 (27.2)
0.431
0 2 0 0 1 0 6 (27.2) 2 4 0 1 (0-7) 5 (2-20) 1 (4.2)
0 2 0 3 0 1 5 (22.7) 3 2 0 5 (0-33) 14 (4-154) 1 (4.2)
0.82
0.001 0.017 1
*Data shown represent median (range). HDU indicates high dependency unit; ITU, intensive therapy unit; LDP, laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
and ODP for malignant disease in terms of survival rates at 1 and 2 years (89% vs. 81%, P = 0.54 and 74.2% vs. 71.5%, P = 0.63, respectively) and the mean duration of survival (45 vs. 31 mo, P = 0.157) (Fig. 1).
DISCUSSION This case-matched comparative study of LDP versus ODP demonstrated that the laparoscopic approach offered advantages in terms of reductions in blood loss and lengths of intensive care and postoperative hospital stay as well as a higher spleen preservation rate, while offering comparative oncologic resections and outcomes in the subgroup of patients with malignant disease. The feasibility and safety of LDP was demonstrated by the low rate of conversion to open surgery and comparative postoperative morbidity and mortality to those observed with open surgery. A recent review of published comparative studies of LDP versus ODP showed similar findings as the laparoscopic approach was associated with significantly reduced blood loss (mean, 237 vs. 562 mL, P < 0.001), shorter postoperative hospital stay (mean, 9.1 vs. 14.7 d, P < 0.001), and lower morbidity (30.5% vs. 38.4%, P = 0.007).18 Our overall morbidity rate after LDP was lower than that of ODP (13.6% vs. 27.2%); however, the difference was not statistically significant. Although our relatively small series does not
TABLE 5. Details of Postoperative Complications
*Data shown represent median (range). IPMN indicates intraductal papillary neoplasm; LDP, laparoscopic distal pancreatectomy; NET, neuroendocrine tumor; ODP, open distal pancreatectomy.
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Pancreatic fistula Liver failure Cardiac Respiratory Hemorrhage Small bowel obstruction Re-laparotomy
LDP (n = 22)
ODP (n = 22)
6 1 1 1 0 0 0
5 0 2 0 2 1 4*
*Re-laparotomy for small bowel perforation (n = 1), small bowel perforation (n = 1), and postoperative hemorrhage (n = 2). LDP indicates laparoscopic distal pancreatectomy; ODP, open distal pancreatectomy.
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FIGURE 1. Kaplan-Meier survival curve for laparoscopic versus open distal pancreatectomy (LDP vs. ODP) in patients with malignant pathology: the mean survival was 45 versus 31 months, P = 0.157 (log rank test).
allow for a meaningful comparison of operative mortality, the literature review of previously published comparative studies of LDP versus ODP found no differences between the 2 approaches in this regard (0.6% vs. 0.5%).18 The rates of POPF after LDP reported in the literature ranged from 0% to 50%.5,9,10,18 The rates of POPF after LDP were comparable to those seen after ODP both in this report (27.5% vs. 22.7%) and in the recent literature review (16.1% vs. 19.5%, P = 0.154)18; all POPFs in our series were of grades A and B that resolved with conservative management and none of the patients had grade C POPF. The factors associated with the development of POPF were not evaluated in this study. The operating time of LDP was comparable to that of ODP in this study and was not dissimilar from that reported in the literature review in which no differences were observed between the 2 approaches (mean, 220 vs. 209 min).18 Preservation of the spleen prolongs operating time as Eom et al19 demonstrated during laparoscopic DP (mean, 194 vs. 251 min, P = 0.020). The spleen preservation rate in various series of LDP ranged between 32% and 84%.3,10,20,21 Our spleen preservation rate after LDP significantly exceeded that accomplished after ODP (45% vs. 18%) in this case-matched study design with comparable tumor size and pathology. These findings are similar to those reported in the recent literature review of LDP versus ODP (median, 37.8% vs. 8.0%, P < 0.001).18 The higher spleen preservation rate therefore appears to be a true advantage of the laparoscopic approach and this could be attributed to the better vision afforded by the magnification used in laparoscopy that aids the fine dissection of the pancreas off the splenic vessels and the splenic hilum. The oncologic clearance achieved with laparoscopic surgery appears comparable to that observed after ODP. In
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the current study, the rates of positive resection margin in patients with malignant disease for LDP and ODP (10% vs. 15%) and the number of lymph nodes retrieved (median, 12.7 vs. 14.1) were comparable with no statistically significant difference in their overall survival after a median follow-up of 22 and 18 months, respectively. In their multicenter comparative analysis of LDP versus ODP for pancreatic ductal adenocarcinoma, Kooby et al found no difference in the rates of positive resection margin (27% vs. 26%), the number of nodes retrieved (mean, 13.8 vs. 12.5), and the overall survival (median, 16 mo in each group).20 Kooby et al conducted a multivariate analysis of factors predictive of poor survival and found that the surgical approach (laparoscopic or open surgery) did not have an impact, but advanced age, large tumors, positive margins, and node positive disease were independently associated with worse survival.20 In another report of LDP in 27 patients with malignancy, Ferna´ndez-Cruz et al7 were able to achieve R0 resection in 90% of ductal adenocarcinoma patients with a mean lymph node count of 14.5. A recent meta-analysis of LDP versus ODP reported no differences in terms of the extent of oncologic clearance.21 In contrast, the single-institution study by Baker et al5 reported a significantly lower lymph node retrieval rate with LDP compared with ODP (mean, 5.2 vs. 9.4, P = 0.4), but their rates were rather low in both groups. The role of LDP for malignancy, nonetheless, still remains controversial, and some surgeons perform open surgery on all patients with preoperative22 or intraoperative23 diagnosis of malignancy, whereas others performed laparoscopic resection if judged technically feasible.1,5,10 Malignancy was one of the reasons in some studies for conversion from laparoscopic to open surgery, either for technical difficulties8 or on principle.23 It is useful to note, however, that comparative studies that included fairly similar proportions of malignant resections in the laparoscopic and open groups found no evidence of increased operative morbidity with the laparoscopic approach.1,10,19 The 2 largest meta-analyses comparing LDP versus ODP reported a shorter length of hospital stay, lower blood loss, and risk of postoperative morbidity, without difference in operative time, margin positivity, incidence of postoperative pancreatic fistula, and mortality.4,21 A potential drawback of laparoscopic surgery is the likelihood of higher cost compared with open surgery. In a comparative study of LDP versus ODP, Hilal et al24 showed that LDP did not have a negative impact on cost. Although we did not examine cost, the shorter operating time and the significantly shorter intensive care and hospital stays that we observed with LDP would undoubtedly have had a favorable impact on the overall cost of that surgical episode. There are limitations to the current study. Although we attempted to circumvent selection bias through cohort matching, a certain degree of bias is inherent within any study outside of a randomized controlled design. However, the relative infrequency of pancreatic diseases that require DP renders the conduction of a randomized trial with sufficient sample size and statistical power challenging, although potentially achievable in a multicenter multinational setting. There is an operator bias regarding the selection of surgical approach among the 5 surgeons involved in the study, with some routinely performing either laparoscopic or open surgery in all comers, whereas others adopted a highly selective approach toward laparoscopy; this limits generalizability of the findings of this study. In addition, tumors were a little larger in the open group (median, 4 vs. 3.2 cm) and the study
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was not powered enough to identify this as a statistically significant difference.
CONCLUSIONS In conclusion, the findings of this case-matched comparative study suggest that the laparoscopic approach to DP offered advantages over open surgery in terms of operative trauma and postoperative recovery as well as the ability to preserve the spleen when indicated, and this was achieved without compromising the oncologic resection. However, the effectiveness of the laparoscopic approach to DP should be evaluated in an adequately powered randomized controlled trial. REFERENCES 1. Vijan SS, Ahmed KA, Harmsen WS, et al. Laparoscopic vs open distal pancreatectomy: a single-institution comparative study. Arch Surg. 2010;145:616–621. 2. Teh SH, Tseng D, Sheppard BC. Laparoscopic and open distal pancreatic resection for benign pancreatic disease. J Gastrointest Surg. 2007;11:1120–1125. 3. DiNorcia J, Schrope BA, Lee MK, et al. Laparoscopic distal pancreatectomy offers shorter hospital stays with fewer complications. J Gastrointest Surg. 2010;14:1804–1812. 4. Venkat R, Edil BH, Schulick RD, et al. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg. 2012;255:1048–1059. 5. Baker MS, Bentrem DJ, Ujiki MB, et al. A prospective single institution comparison of peri-operative outcomes for laparoscopic and open distal pancreatectomy. Surgery. 2009;146:635–645. 6. Taylor C, O’rourke N, Nathanson L, et al. Laparoscopic distal pancreatectomy: the Brisbane experience of forty-six cases. HPB (Oxford). 2008;10:38–42. 7. Ferna´ndez-Cruz L, Blanco L, Cosa R, et al. Is laparoscopic resection adequate in patients with neuroendocrine pancreatic tumors? World J Surg. 2008;32:904–917. 8. Velanovich V. Case-control comparison of laparoscopic versus open distal pancreatectomy. J Gastrointest Surg. 2006;10:95–98. 9. Matsumoto T, Shibata K, Ohta M, et al. Laparoscopic distal pancreatectomy and open distal pancreatectomy: a nonrandomized comparative study. Surg Laparosc Endosc Percutan Tech. 2008;18:340–343.
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