Surg Endosc DOI 10.1007/s00464-015-4265-z
and Other Interventional Techniques
Binding pancreaticogastrostomy in laparoscopic central pancreatectomy: a novel technique in laparoscopic pancreatic surgery Defei Hong1 • Yingbin Liu2 • Shuyou Peng1 • Xiaodong Sun1 • Zhifei Wang1 Jian Cheng1 • Guoliang Shen1 • Yuanbiao Zhang1 • Dongsheng Huang1
•
Received: 4 March 2015 / Accepted: 8 May 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Even though more and more cases of laparoscopic central pancreatectomy (LCP) are reported (Machado et al. in Surg Laparosc Endosc Percutan Tech 23(6):486–490, 2013; Hong et al. in World J Surg Oncol 10:223, 2012; Gonzalez et al. in JOP 14(3):273–276, 2013, Zhang et al. in J Laparoendosc Adv Surg Tech A 23(11):912–918, 2013; Sucandy et al. in N Am J Med Sci 2(9):438–441, 2010; Sa Cunha et al. in Surgery 142(3):405–409, 2007), the management for pancreatic stumps remains the most technically challenging part which is the same as in pancreatoduodenectomy (PD), making it the bottleneck for laparoscopic pancreatic surgery. In open surgery, various pancreatic reconstruction techniques designed for either pancreaticojejunostomy (PJ) or pancreaticogastrostomy (PG) have been attempted to reduce the postoperative pancreatic fistula (POPF), including the binding anastomosis, invented by our team, i.e., binding PG (BPG) and binding PJ, which have been proved to be effective to reduce the POPF (Hong et al. 2012; Peng et al. in Ann Surg 245(5):692–698, 2007; Peng et al. in Updates Surg 63(2):69–74, 2011). However, despite of this, few reports are seen addressing such technique for
& Zhifei Wang [email protected] & Dongsheng Huang [email protected] 1
Department of Hepatobiliary and Pancreatic Surgery and Minimally Invasive Surgery, Zhejiang Provincial People’s Hospital, Hangzhou, China
2
Department of General Surgery, Xin Hua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
laparoscopic surgery even though laparoscopic pancreatic surgery is more performed. After a previous successful laparoscopic BPG in a case of laparoscopic CP (LCP; Hong et al. 2012) and more than 50 cases of open PD and CP (Peng et al. 2011), we further performed laparoscopic BPG in 10 consecutive cases of LCP with satisfactory outcomes. Objective To explore the feasibility and efficacy of LCP with BPG. Methods Between October 2011 and July 2014, LCP with laparoscopic BPG was performed in ten consecutive patients with lesions of benign or low malignancy at the pancreatic neck. Operative and pathological data, complications, hospital stay and details on the surgical techniques were introduced. Results The operations were successfully performed in all the ten cases, with no conversions. The tumor size ranged from 2.0–3.0 to 2.5–3.0 cm, average (2.50 ± 0.35) to (2.66 ± 0.35) cm, and the diameter of pancreatic duct was (1.6–2.1) mm, average (1.71 ± 0.17) mm. Operation time was 170–250 (198.50 ± 25.82) min, and blood loss was 20–300 (125 ± 107.31) mL. Three cases had grade A pancreatic fistula (PF), and one case had delayed gastric emptying, which were all managed with conservative treatment. Upper GI bleeding occurred in one case which was cured with second operation, time for the recovery of bowl movement was 3–5 (4.2 ± 0.8) days, the time for semifluid dieting was 6–10 (8.2 ± 1.5) days, and the hospital stay was 8–20 (12.8 ± 4.63) days. The postoperative fast blood sugar was (6.3 ± 1.6) mmol/L with the normal diet, which was not significantly different from the preoperative data (5.3 ± 0.5) mmol/L (P [ 0.05). The postoperative pathology was as follows: five cases of cystic serous adenoma, one case of intraductal papillary mucinous neoplasm, two cases of neuroendocrine tumor, and two cases of solid pseudopapillary tumor of pancreas. All the
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patients were followed up for 7–40 months, no recurrence happened, and no new incidence of diabetes or insufficiency of pancreatic exocrine function occurred. Conclusions LCP with BPG is feasible and safe; the advantages lie in its minimal invasiveness, the efficacy for avoiding PF, and the preservation of the pancreatic endocrine and exocrine function insufficiency, making it an ideal procedure for the benign or low-malignant lesions at the pancreatic neck. Keywords Central pancreatectomy Binding pancreaticogastrostomy Pancreatic fistula
CP has been gradually accepted as a choice of surgery for lesions at the pancreatic neck which are of either benign or low malignancy and with the involvement of main pancreatic duct, or they are too close to the pancreatic duct. The advancement of CT, MR and endoscopic ultrasound (combined with biopsy) has helped to identify such cases; the intraoperative ultrasound and frozen section of cutting edge help to ensure the radical resection. The advantages of CP lie in the preservation of pancreatic function maximally as it conserves far more innocent pancreatic tissue than distal pancreatectomy (DP) and pancreatoduodenctomy (PD) [1, 2]. Controversies for such procedure mainly lie in two concerns: the required management for two pancreatic stumps with the postoperative rate of PF as high as 40–70 %, and the pancreatic reconstruction, making it more complicated than DP [1–4]. Such procedure has been attempted both laparoscopically and robotically as alternative to open surgery. However, the technical limitation of laparoscopic surgery makes the pancreatic reconstruction under laparoscope extremely difficult, as it has long been for laparoscopic PD. The biggest concern is the risk of serious complication due to the postoperative pancreatic fistula (POPF) coming from a failure in the management for the remnant pancreatic stump that remains technically challenging, which has been regarded as the most frequent major complication and potentially serious, life-threatening event. Technical difficulties in laparoscopic pancreatic reconstruction lie mainly in pancreatic anastomosis, and the reasons contribute to such difficulties are the reduced tactile and preciseness during laparoscopic surgery due to the lack of flexibility of the long and rigid laparoscopic instruments, in contrast to the limited space and fixed angle, largely complicate the suture maneuver during anastomosis, especially when the pancreas tissue rather soft and the very small pancreatic duct, making both pancreaticojejunostomy (PJ) and pancreaticogastrostomy (PG) much technically challenging, thus increasing the risk of leakage [3, 5–8]. On the other hand, among the various invention and modification for the pancreatic reconstructions, the binding
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maneuver has been proved to be effective in open surgery for pancreatic reconstructions [9, 10]. As members of the team who invented the binding PJ (BPJ) and binding PG (BPG), we initially applied it in LPG [5], finding that using binding other than suturing made the procedure rather simple and greatly facilitated the operation maneuvers under laparoscope. After we continuously performed such technique in ten cases of laparoscopic central pancreatectomy (LCP) with satisfactory results from October 2011 to July 2014, we summarized the data and reported our experience, the short-term outcomes and technical aspects, or both LCP and LPG are introduced. Our objective was to demonstrate that LCP with LBPG is a valid technique.
Patients and methods Patient selection A retrospective study of ten patients with histologically proven benign or low-malignant tumors at the pancreatic neck underwent LCP at our center from October 2011 to July 2014 was conducted. There were ten patients (four male patients and six female patients with the medium age of (53.80 ± 9.36) (range 33–67 year)). The tumor size ranged from (2.0–3.0) to (2.5–3.0) cm, average (2.50 ± 0.35) to (2.66 ± 0.35) cm, and the diameter of pancreatic duct was 1.6–2.1 mm, average (1.71 ± 0.17) mm. The cases that high malignancy could not be ruled out (high tumor marker). Preoperative workup comprised: chest, abdominal and pancreas enhanced CT and MRI, endoscopic ultrasound, magnetic resonance (MRI) or both. Preoperative data, archived prospectively in our database, included general patient characteristics, tumor size and location and body mass index (BMI). The intraoperative results included trocar and patient positions and time of operation excluding time for intraoperative biopsy. The postoperative results included days to passing first flatus, the time for recovery of feeding, length of hospital stay and postoperative complications. Pathological data included intraoperative and postoperative findings. All operations were performed by one surgeon (H.D.F) who had performed over 100 of open PD with binding BPG and 8 cases of laparoscopic PD with BPG.
Laparoscopic surgical techniques The patient was in a supine position under general anesthesia. A 10-mm incision was made below the umbilicus, and pneumoperitoneum of 12–15 mmHg was established using Hasson’s technique. The abdominal was explored to
Surg Endosc
rule out metastasis; incisions of 5, 12 and 5 mm were made at the right upper quadrant, left upper quadrant and left lumbar region, respectively. First, the pancreatic body was exposed by dividing the gastrocolic ligament and opening of the lesser sac, and then, the pancreas was further exposed by hanging the stomach with an 8# urine catheter, which was anchored from outside the abdomen. The peritoneum along the inferior edge of the pancreas around the middle colic vein is dissected until the superior mesenteric vein (SMV) is identified. A blunt dissection is continued cephaladly separating the pancreas from the SMV posteriorly to the pancreatic neck, until the post-pancreatic tunnel was established; the splenic vein and its confluence with SMV to portal vein were exposed. Then, the dissection moved to the superior edge of the pancreas, and blunt dissection was continued to expose the splenic vein and splenic artery off the pancreas for a 2 cm distance at the pancreatic neck. The pancreatic neck is then lifted, and the branches of splenic vessels to the pancreas were secured with Hem-o-lok about 2 cm distally from the pancreatic neck. Tumor’s borderline was confirmed under laparoscopic ultrasound. A 60 cm liner stapler was applied to cut the pancreatic neck at its proximal side. The distal pancreatic stump is lifted for further dissection along its superior and inferior boarders and branches of vessels to the splenic vessels, and inferior peripancreatic veins are identified and secured with Hem-o-lok, facilitating the mobilization of the pancreas distally until the sufficient margin is reached, followed by a transection at distal side of the pancreas with harmonic. The sample was then sent for intraoperative frozen biopsy to confirm pathology to be benign or of low malignancy. The distal pancreas stump was further freed by dissecting it from the splenic artery and splenic vein for about 3 cm as preparation for anastomosis, followed by closing the cutting surface with stitch suture with 4-0 prolene. A pancreatic duct tube was place after identifying the orifice of the pancreatic duct. About 3 cm opening was made on the posterior wall of the stomach, which is approximate to the diameter to the pancreatic stump before it was sterilized with PVP iodine, an additional 3–5 cm opening was made on the anterior gastric wall, a full-layer purse suture was made at the opening of posterior wall of the stomach with a 3-0 prolene, and the pancreatic stump was dragged into the stomach for about 2 cm under direct observation. By tying the purse suture, the gastric wall was binded to the pancreatic stump followed by closing the anterior gastric wall. Definition of complications Based on International Study Group on Pancreatic Fistula Definition (ISGPF), the diagnosis of postoperative complications was defined as follows [11]:
1.
2. 3. 4. 5.
Pancreatic fistula: Drain output of any measurable volume of fluid on or after postoperative day 3 with an amylase content [3 times the serum amylase activity. Delayed gastric emptying: Continuous decompression [10 days. Postoperative hemorrhage: PRBC transfusion [3U 24 h after surgery. Biliary fistula: Output of biliary-rich fluid [5 days or confirmed by cholangiography or fistula angiography. Abdominal collection: Intraperitoneal fluid [5 cm confirmed by CT or ultrasound with or without clinical symptoms.
Statistical analysis The statistical analysis of the data was performed using SPSS 13.0 statistical software and Microsoft Excel software. One-sample t test was used when the data were normally distributed, or nonparametric test was applied when the data were abnormally distributed. Chi-square tests or Fisher’s tests were used for frequency data.
Results Of all the ten cases, pancreatic duct was found in nine cases, with the diameters \2 mm in all, and the textures of the pancreas were all soft. LCP was successfully completed in all ten cases. Operation time was 170–250 (198.50 ± 25.82) min, and blood loss was 20–300 (125 ± 107.31) mL. Three cases had grade A pancreatic fistula (PF); one case had delayed gastric emptying, which were all managed with conservative treatment. Upper GI bleeding occurred in one case which was cured with second operation; time for the recovery of bowl movement was 3–5 (4.2 ± 0.8) days; the time for semifluid dieting was 6–10 (8.2 ± 1.5) days; the hospital stay was 8–20 (12.8 ± 4.63) days. The postoperative fast blood sugar was (6.3 ± 1.6) mmol/L with the normal diet, which was not significantly different from the preoperative data (5.3 ± 0.5) mmol/L (P [ 0.05). The postoperative pathology was as follows: five cases of cystic serous adenoma, one case of intraductal papillary mucinous neoplasm, two cases of neuroendocrine tumor, and two cases of solid pseudopapillary tumor of pancreas. All the patients were followed up for 7–40 months, no recurrence happened, and no new incidence of diabetes or insufficiency of pancreatic exocrine function occurred. All the intraoperative pathology was identical to the postoperative pathological findings. One case was reoperated in emergency due to upper GI bleeding 6 h postoperatively, a vascular bleeding at pancreatic stump was confirmed by gastroscopy, and emergency surgery was
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performed. 4-0 prolene sutures the bleeding site. Delayed gastric empty occurred in one case, which was managed by conservative treatment.
Discussion Low-grade malignancies or benign lesions of the central pancreas present a surgical dilemma between preserving pancreatic endocrine function and resecting sufficient parenchyma to minimize the risk of recurrence. Although enucleation is accepted as an appropriate management for selected benign lesions, low-grade malignancies and benign lesions without involvement of the main pancreatic duct, for the cases with lesions at pancreatic neck with involvement of main pancreatic duct or close to it, PD or DP is always indicated. Despite of the two challenges, the sufficient margin from the concern of surgical oncology and theoretically more risk of POPF due to two pancreatic stumps, CP is an alternative choice and has been applied more recently. Guillemin and Bessot firstly reported central pancreatectomy in 1957 [12], such technique has been reported more recently, even the experience with data of more than 50 cases [2, 13–16], the largest series of cases at the single center with a 12-year experience confirmed its benefit, saying the procedure is best indicated for benign or low-grade lesions in young and fit patients who can sustain a significant postoperative morbidity and could benefit from the excellent longterm results. Such procedure mainly has theoretic benefit: The preservation of the pancreatic parenchyma can remain its endocrine and exocrine function, and the exempt of PD can remain the anatomy of the digestive tract thus avoiding the related complications. However, CP brings several concerns also: The risk of POPF is higher theoretically due to the double cutting ends of pancreas, the possible insufficient margins in case of malignancy. Localizing the tumor in the pancreas usually requires tactile feedback to assess the site and size of the tumor. Intraoperative frozen biopsy for the cutting edge is important, local lymph node biopsy was need for neuroendocrine tumor or IPMN; the close or even resection of distal pancreas will be decided when the remnant pancreas is atrophy or \5 cm, or with inflammation or fibrosis. Intraoperative laparoscopic ultrasound helps to identify the cutting margins therefore securing the sufficient cutting edge. Even though there are two pancreatic stumps after CP, making it seem logical that CP carries a higher overall risk of pancreatic fistula than other pancreatectomy procedures, the POPF is closely related to pancreatic reconstruction, which is another focus of discussion considering the various types of operations. Even though there are many classic approaches for the reconstruction of pancreas, such as the duct to mucosa as in PJ, the two layer anastomosis [2, 9–11, 17], they are not
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suitable for laparoscopic manipulation. Plus, for those pancreatic ducts is\3 mm in diameter and those locate at the edge of the pancreas, such types of reconstruction are extremely technically difficult by laparoscopy with a significantly higher risk of PF; in our ten cases, the diameter of pancreatic duct was 1.6–2.1 mm, average (1.71 ± 0.17) mm. Plus, CP is performed mainly for benign lesions—that is, with a soft pancreas and a nondilated main pancreatic duct, which are consequently at higher risk of pancreatic fistula. From the recent literature, PG is more preferred over PJ as for CP, which is due to several reasons: the reduced anastomosis simplifying the operation, the reduced rate of POPF, and no interference on pancreatic endocrine and exocrine functions [2, 4]; the advantages of PG also lie in the avoidance of activation of pancreatic enzyme, the sufficient blood supply of gastric wall, and the proximity of the stomach and pancreatic stump. Furthermore, gastric and pancreatic secretion is easily diverted with a nasogastric tube after PG, and PG reconstruction may divert potential pancreatic fistulas away from major blood vessels [17]. Also, the duct-to-mucosa anastomosis technique, though accepted as a very reliable technique, is extremely technically challenging technique not applicable and reliable in laparoscopic surgery but in only a few surgeons’ hands. Therefore, despite of some controversies, we prefer PG laparoscopic scenario based on our experience of more than 50 cases of open PD and CP with the BPG [10]. Furthermore, binding PG technique spares the need for suturing anastomosis by simply drawing the purse suture, making it much easier to perform on the gastric wall. In the first case, other than the above-described technique for BPG, we sutured the stump with a straight needle which was first penetrating through the anterior gastric wall and then the abdominal wall, followed by the anchoring the suture from outside of the abdomen, to facilitate the anastomosis. However, when dragging the pancreatic stump into the stomach, it is risky for a possible tearing of the vessels of the pancreatic stump, and the problem lies in that such possible bleeding might not be found after the binding anastomosis. Such incidence happened on the first case of LCP, when upper GI bleeding was emergent within 6 h and arterial active bleeding at the pancreatic stump was confirmed with emergency upper GI endoscopic. The patient was reoperated in emergency, laparotomy with a small ventral midline incision was made, the anterior gastric wall was opened, and the bleeding site was secured with 4-0 prolene suture. An intraoperative upper GI endoscope was applied to rule out such complication in the rest of nine cases. In addition, a full-layer closure of pancreatic stump was performed, and caution should be paid to avoid the pancreatic duct. The delayed gastric emptying has been one major concern for PG, while occurred in one case in this series and was proved to be gastroparesis, which was managed with conservative therapy for 15 days.
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Laparoscope provides a specific observation angle, i.e., from to caudal to cephral; some avascular plane thus could be utilized, e.g., the post-pancreatic tunnel behind the pancreatic neck, when the SMV is identified. We previously introduced a specific binding technique and accumulated our experience both in binding PJ and binding PG (BPG) which was initially invented by Dr. Peng and Dr. Hong, which is widely accepted for their significant advantages in teams of reducing the rate of POPF [9, 10]. Such technique, with its name binding, emphasizes the advantages of binding other than suturing; the underlining advantages are the simplified anastomosis procedure and the reduced risk related to suturing, such as the potential leakage between the adjacent stitches and possibility of the needle hole which penetrates into the small branches of pancreatic duct [5, 10]. We further proved BPG to be safe and effective in open surgery by our previous RCT study with 53 cases in the BPJ group and 62 in the BPG group. In the BPJ group, pancreatic fistulae occurred in six cases (11.3 %), DGE in five, hemorrhage in one, biliary fistulae in two and an abdominal abscess in one. One patient died of MOF caused by an abdominal abscess on the 5th day postoperatively. In the BPG group, pancreatic fistulae developed in four cases(6.5 %), DGE in 11, hemorrhage in three, bililary fistulae in five and abdominal abscesses in two. There were no operative mortalities in the BPG group. No statistical difference was found between the two groups with respect to PF rate. We concluded from that study that both BPJ and BPG are safe and reliable procedures for reconstructing pancreatic digestive continuity after PD. Interestingly, such advantage of exempting suturing is greatly suitable for laparoscopic surgery, because all the reconstructions, either running suture, in which the long thread often tangles, or the stitch suturing, in which the suture cannot be otherwise prepared one by one, often make the most critical step both timeconsuming and not secured. On the other hand, the binding technique often requires a few purses suturing, which has a much requirement for the suturing as required more strictly for anastomosis, e.g., the tension free, clear visionalization and appropriate angle, which are harder to achieve in laparoscopic surgery compared with open surgery. Based on such presumption, we applied modified Peng’s BPG, i.e., the one-layer BPG and applied it in ten laparoscopic CP (LCP) cases, which simplified the laparoscopic procedure with satisfactory results; only three cases had A grade pancreatic fistula. The time for BPG anastomosis in this LBPG series was (20.3 ± 2.6) min, indicating that the learning curve is not long, while the time for laparoscopic pancreatic anastomosis is known lengthy and these types of procedures require extensive experience in open pancreatic surgery combined with a high level of laparoscopic skill.
There are several key steps for such techniques. First, the pancreatic stump needs to be mobilized for at least 3 cm for anastomosis; Second, the opening in the gastric wall should be the most approximated to the pancreatic stump, a fulllayer purse suture with 3-0 prolene on the opening of the gastric wall, in order to reduce the risk of gastric wall bleeding and to provide sufficient strength for suturing. Unlike the open surgery, even though the purse suturing on the gastric wall is not technically challenging under laparoscope, the laparoscopic binding does raise some concerns regarding the strength that is needed during the binding maneuver under laparoscope, when the tactile is much compromised. However, this can be compensated with the visualization of the tissue’s distortion, while the binding thread is tied, and to our experience, the strength should be enough and the binding secured when the thread is sacking into the gastric wall surface. It can be concluded that LCP is feasible and LBPG is a simplified technique facilitating LCP. To our knowledge, this is the first report on binding at the anastomosis under laparoscope. Even though open BPG and BPJ were proved to be effective in our previous RCT study, the binding technique may also have contributed to the low POPF rate of both laparoscopic and open PJ, so a comparative study taking the binding technique as a single factor to rule out other influences thus to valid its validity. Acknowledgments This work was supported by the fund of the Key Project of the Science and Technology Department of Zhejiang Province: the establishment, evaluation and personalized application of binding pancreatojejunostomy/binding pancreatogastrostomy, Fund No: 2013C03046, the Key Funds for the Platform of Medicine of the Health and Family Planning Commission of Zhejiang Province, Nos: 2013ZDA004 and 2015127995, the fund from the Science and Technology Department of Zhejiang Province, No: 2015C33112 and the fund from the Education Department of Heilongjiang Province Government, No: 12511245. Disclosures Drs. Defei Hong, Yingbin Liu, Shuyou Peng, Xiaodong Sun, Zhifei Wang, Jian Cheng, Guoliang Shen, Yuanbiao Zhang and Dongsheng Huang have no conflict of interest or financial ties to disclose.
References 1. Machado MA, Surjan RC, Epstein MG, Makdissi FF (2013) Laparoscopic central pancreatectomy: a review of 51 cases. Surg Laparosc Endosc Percutan Tech 23(6):486–490 2. Goudard Y, Gaujoux S, Dokmak S, Cros J, Couvelard A, Palazzo M (2014) Reappraisal of central pancreatectomy: a 12 year-Single center experience. JAMA Surg 149(4):356–363 3. Gonzalez F, Mesleh MG, Lukens FJ, Wallace MB, Asbun HJ, Stauffer JA (2013) Laparoscopic central pancreatectomy and pancreaticogastrostomy for the management of a proximally migrated pancreatic stent. JOP 14(3):273–276 4. Michael JG, Jared T, John AC (2004) Pancreaticogastrostomy: a novel application after central pancreatectomy. J Am Coll Surg 198:871–876
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Surg Endosc 5. Hong DF, Xin Y, Cai XJ, Peng SY (2012) Application of binding pancreatogastrostomy in laparoscopic central pancreatectomy. World J Surg Oncol 10:223 6. Zhang R, Xu X, Yan J, Wu D, Ajoodhea H, Mou Y (2013) Laparoscopic central pancreatectomy with pancreaticojejunostomy: preliminary experience with 8 cases. J Laparoendosc Adv Surg Tech A 23(11):912–918 7. Sucandy I, Pfeifer CC, Sheldon DG (2010) Laparoscopic assisted central pancreatectomy with pancreaticogastrostomy reconstruction—an alternative surgical technique for central pancreatic mass resection. N Am J Med Sci 2(9):438–441 8. Cunha AS, Rault A, Beau C, Collet D, Masson B (2007) Laparoscopic central pancreatectomy: single institution experience of 6 patients. Surgery 142(3):405–409 9. Peng SY, Wang JW, Lau WY, Cai XJ, Mou YP, Liu YB, Li JT (2007) Conventional versus binding pancreaticojejunostomy after pancreaticoduodenectomy: a prospective randomized trial. Ann Surg 245(5):692–698 10. Peng SY, Wang JW, Hong DF, Liu YB, Wang YF (2011) Binding pancreaticoenteric anastomosis: from binding pancreaticojejunostomy to binding pancreaticogastrostomy. Updates Surg 63(2):69–74 11. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138(1):8–13
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12. Guillemin P, Bessot M (1957) Chronic calcifying pancreatitis in renal tuberculosis: pancreatojejunostomy using an original technic. Mem Acad Chir (Paris) 83(27–28):869–871 13. DiNorcia J, Ahmed L, Lee MK, Reavey PL, Yakaitis EA, Lee JA (2010) Better preservation of endocrine function after central versus distal pancreatectomy for mid-gland lesions. Surgery 148(6):1247–1256 14. Adham M, Giunippero A, Hervieu V, Courbie`re M, Partensky C (2008) Central pancreatectomy: single-center experience of 50 cases. Arch Surg 143(2):175–181 15. Crippa S, Bassi C, Warshaw AL, Falconi M, Partelli S, Thayer SP (2007) Middle pancreatectomy: indications, short- and long-term operative outcomes. Ann Surg 246(1):69–76 16. Sauvanet A, Partensky C, Sastre B, Gigot JF, Fagniez GL, Tuech JJ, Millat B, Berdah S, Dousset B, Jaeck D, Treut YP, Letoublon C (2002) Medial pancreatectomy: a multi-institutional retrospective study of 53 patients by the French Pancreas Club. Surgery 132(5):836–843 17. Menahem B, Guittet L, Mulliri A, Alves A, Lubrano J (2015) Pancreaticogastrostomy is superior to pancreaticojejunostomy for prevention of pancreatic fistula after pancreaticoduodenectomy: an updated meta-analysis of randomized controlled trials. Ann Surg 261(5):882–887
and Other Interventional Techniques
Binding pancreaticogastrostomy in laparoscopic central pancreatectomy: a novel technique in laparoscopic pancreatic surgery Defei Hong1 • Yingbin Liu2 • Shuyou Peng1 • Xiaodong Sun1 • Zhifei Wang1 Jian Cheng1 • Guoliang Shen1 • Yuanbiao Zhang1 • Dongsheng Huang1
•
Received: 4 March 2015 / Accepted: 8 May 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Even though more and more cases of laparoscopic central pancreatectomy (LCP) are reported (Machado et al. in Surg Laparosc Endosc Percutan Tech 23(6):486–490, 2013; Hong et al. in World J Surg Oncol 10:223, 2012; Gonzalez et al. in JOP 14(3):273–276, 2013, Zhang et al. in J Laparoendosc Adv Surg Tech A 23(11):912–918, 2013; Sucandy et al. in N Am J Med Sci 2(9):438–441, 2010; Sa Cunha et al. in Surgery 142(3):405–409, 2007), the management for pancreatic stumps remains the most technically challenging part which is the same as in pancreatoduodenectomy (PD), making it the bottleneck for laparoscopic pancreatic surgery. In open surgery, various pancreatic reconstruction techniques designed for either pancreaticojejunostomy (PJ) or pancreaticogastrostomy (PG) have been attempted to reduce the postoperative pancreatic fistula (POPF), including the binding anastomosis, invented by our team, i.e., binding PG (BPG) and binding PJ, which have been proved to be effective to reduce the POPF (Hong et al. 2012; Peng et al. in Ann Surg 245(5):692–698, 2007; Peng et al. in Updates Surg 63(2):69–74, 2011). However, despite of this, few reports are seen addressing such technique for
& Zhifei Wang [email protected] & Dongsheng Huang [email protected] 1
Department of Hepatobiliary and Pancreatic Surgery and Minimally Invasive Surgery, Zhejiang Provincial People’s Hospital, Hangzhou, China
2
Department of General Surgery, Xin Hua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
laparoscopic surgery even though laparoscopic pancreatic surgery is more performed. After a previous successful laparoscopic BPG in a case of laparoscopic CP (LCP; Hong et al. 2012) and more than 50 cases of open PD and CP (Peng et al. 2011), we further performed laparoscopic BPG in 10 consecutive cases of LCP with satisfactory outcomes. Objective To explore the feasibility and efficacy of LCP with BPG. Methods Between October 2011 and July 2014, LCP with laparoscopic BPG was performed in ten consecutive patients with lesions of benign or low malignancy at the pancreatic neck. Operative and pathological data, complications, hospital stay and details on the surgical techniques were introduced. Results The operations were successfully performed in all the ten cases, with no conversions. The tumor size ranged from 2.0–3.0 to 2.5–3.0 cm, average (2.50 ± 0.35) to (2.66 ± 0.35) cm, and the diameter of pancreatic duct was (1.6–2.1) mm, average (1.71 ± 0.17) mm. Operation time was 170–250 (198.50 ± 25.82) min, and blood loss was 20–300 (125 ± 107.31) mL. Three cases had grade A pancreatic fistula (PF), and one case had delayed gastric emptying, which were all managed with conservative treatment. Upper GI bleeding occurred in one case which was cured with second operation, time for the recovery of bowl movement was 3–5 (4.2 ± 0.8) days, the time for semifluid dieting was 6–10 (8.2 ± 1.5) days, and the hospital stay was 8–20 (12.8 ± 4.63) days. The postoperative fast blood sugar was (6.3 ± 1.6) mmol/L with the normal diet, which was not significantly different from the preoperative data (5.3 ± 0.5) mmol/L (P [ 0.05). The postoperative pathology was as follows: five cases of cystic serous adenoma, one case of intraductal papillary mucinous neoplasm, two cases of neuroendocrine tumor, and two cases of solid pseudopapillary tumor of pancreas. All the
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patients were followed up for 7–40 months, no recurrence happened, and no new incidence of diabetes or insufficiency of pancreatic exocrine function occurred. Conclusions LCP with BPG is feasible and safe; the advantages lie in its minimal invasiveness, the efficacy for avoiding PF, and the preservation of the pancreatic endocrine and exocrine function insufficiency, making it an ideal procedure for the benign or low-malignant lesions at the pancreatic neck. Keywords Central pancreatectomy Binding pancreaticogastrostomy Pancreatic fistula
CP has been gradually accepted as a choice of surgery for lesions at the pancreatic neck which are of either benign or low malignancy and with the involvement of main pancreatic duct, or they are too close to the pancreatic duct. The advancement of CT, MR and endoscopic ultrasound (combined with biopsy) has helped to identify such cases; the intraoperative ultrasound and frozen section of cutting edge help to ensure the radical resection. The advantages of CP lie in the preservation of pancreatic function maximally as it conserves far more innocent pancreatic tissue than distal pancreatectomy (DP) and pancreatoduodenctomy (PD) [1, 2]. Controversies for such procedure mainly lie in two concerns: the required management for two pancreatic stumps with the postoperative rate of PF as high as 40–70 %, and the pancreatic reconstruction, making it more complicated than DP [1–4]. Such procedure has been attempted both laparoscopically and robotically as alternative to open surgery. However, the technical limitation of laparoscopic surgery makes the pancreatic reconstruction under laparoscope extremely difficult, as it has long been for laparoscopic PD. The biggest concern is the risk of serious complication due to the postoperative pancreatic fistula (POPF) coming from a failure in the management for the remnant pancreatic stump that remains technically challenging, which has been regarded as the most frequent major complication and potentially serious, life-threatening event. Technical difficulties in laparoscopic pancreatic reconstruction lie mainly in pancreatic anastomosis, and the reasons contribute to such difficulties are the reduced tactile and preciseness during laparoscopic surgery due to the lack of flexibility of the long and rigid laparoscopic instruments, in contrast to the limited space and fixed angle, largely complicate the suture maneuver during anastomosis, especially when the pancreas tissue rather soft and the very small pancreatic duct, making both pancreaticojejunostomy (PJ) and pancreaticogastrostomy (PG) much technically challenging, thus increasing the risk of leakage [3, 5–8]. On the other hand, among the various invention and modification for the pancreatic reconstructions, the binding
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maneuver has been proved to be effective in open surgery for pancreatic reconstructions [9, 10]. As members of the team who invented the binding PJ (BPJ) and binding PG (BPG), we initially applied it in LPG [5], finding that using binding other than suturing made the procedure rather simple and greatly facilitated the operation maneuvers under laparoscope. After we continuously performed such technique in ten cases of laparoscopic central pancreatectomy (LCP) with satisfactory results from October 2011 to July 2014, we summarized the data and reported our experience, the short-term outcomes and technical aspects, or both LCP and LPG are introduced. Our objective was to demonstrate that LCP with LBPG is a valid technique.
Patients and methods Patient selection A retrospective study of ten patients with histologically proven benign or low-malignant tumors at the pancreatic neck underwent LCP at our center from October 2011 to July 2014 was conducted. There were ten patients (four male patients and six female patients with the medium age of (53.80 ± 9.36) (range 33–67 year)). The tumor size ranged from (2.0–3.0) to (2.5–3.0) cm, average (2.50 ± 0.35) to (2.66 ± 0.35) cm, and the diameter of pancreatic duct was 1.6–2.1 mm, average (1.71 ± 0.17) mm. The cases that high malignancy could not be ruled out (high tumor marker). Preoperative workup comprised: chest, abdominal and pancreas enhanced CT and MRI, endoscopic ultrasound, magnetic resonance (MRI) or both. Preoperative data, archived prospectively in our database, included general patient characteristics, tumor size and location and body mass index (BMI). The intraoperative results included trocar and patient positions and time of operation excluding time for intraoperative biopsy. The postoperative results included days to passing first flatus, the time for recovery of feeding, length of hospital stay and postoperative complications. Pathological data included intraoperative and postoperative findings. All operations were performed by one surgeon (H.D.F) who had performed over 100 of open PD with binding BPG and 8 cases of laparoscopic PD with BPG.
Laparoscopic surgical techniques The patient was in a supine position under general anesthesia. A 10-mm incision was made below the umbilicus, and pneumoperitoneum of 12–15 mmHg was established using Hasson’s technique. The abdominal was explored to
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rule out metastasis; incisions of 5, 12 and 5 mm were made at the right upper quadrant, left upper quadrant and left lumbar region, respectively. First, the pancreatic body was exposed by dividing the gastrocolic ligament and opening of the lesser sac, and then, the pancreas was further exposed by hanging the stomach with an 8# urine catheter, which was anchored from outside the abdomen. The peritoneum along the inferior edge of the pancreas around the middle colic vein is dissected until the superior mesenteric vein (SMV) is identified. A blunt dissection is continued cephaladly separating the pancreas from the SMV posteriorly to the pancreatic neck, until the post-pancreatic tunnel was established; the splenic vein and its confluence with SMV to portal vein were exposed. Then, the dissection moved to the superior edge of the pancreas, and blunt dissection was continued to expose the splenic vein and splenic artery off the pancreas for a 2 cm distance at the pancreatic neck. The pancreatic neck is then lifted, and the branches of splenic vessels to the pancreas were secured with Hem-o-lok about 2 cm distally from the pancreatic neck. Tumor’s borderline was confirmed under laparoscopic ultrasound. A 60 cm liner stapler was applied to cut the pancreatic neck at its proximal side. The distal pancreatic stump is lifted for further dissection along its superior and inferior boarders and branches of vessels to the splenic vessels, and inferior peripancreatic veins are identified and secured with Hem-o-lok, facilitating the mobilization of the pancreas distally until the sufficient margin is reached, followed by a transection at distal side of the pancreas with harmonic. The sample was then sent for intraoperative frozen biopsy to confirm pathology to be benign or of low malignancy. The distal pancreas stump was further freed by dissecting it from the splenic artery and splenic vein for about 3 cm as preparation for anastomosis, followed by closing the cutting surface with stitch suture with 4-0 prolene. A pancreatic duct tube was place after identifying the orifice of the pancreatic duct. About 3 cm opening was made on the posterior wall of the stomach, which is approximate to the diameter to the pancreatic stump before it was sterilized with PVP iodine, an additional 3–5 cm opening was made on the anterior gastric wall, a full-layer purse suture was made at the opening of posterior wall of the stomach with a 3-0 prolene, and the pancreatic stump was dragged into the stomach for about 2 cm under direct observation. By tying the purse suture, the gastric wall was binded to the pancreatic stump followed by closing the anterior gastric wall. Definition of complications Based on International Study Group on Pancreatic Fistula Definition (ISGPF), the diagnosis of postoperative complications was defined as follows [11]:
1.
2. 3. 4. 5.
Pancreatic fistula: Drain output of any measurable volume of fluid on or after postoperative day 3 with an amylase content [3 times the serum amylase activity. Delayed gastric emptying: Continuous decompression [10 days. Postoperative hemorrhage: PRBC transfusion [3U 24 h after surgery. Biliary fistula: Output of biliary-rich fluid [5 days or confirmed by cholangiography or fistula angiography. Abdominal collection: Intraperitoneal fluid [5 cm confirmed by CT or ultrasound with or without clinical symptoms.
Statistical analysis The statistical analysis of the data was performed using SPSS 13.0 statistical software and Microsoft Excel software. One-sample t test was used when the data were normally distributed, or nonparametric test was applied when the data were abnormally distributed. Chi-square tests or Fisher’s tests were used for frequency data.
Results Of all the ten cases, pancreatic duct was found in nine cases, with the diameters \2 mm in all, and the textures of the pancreas were all soft. LCP was successfully completed in all ten cases. Operation time was 170–250 (198.50 ± 25.82) min, and blood loss was 20–300 (125 ± 107.31) mL. Three cases had grade A pancreatic fistula (PF); one case had delayed gastric emptying, which were all managed with conservative treatment. Upper GI bleeding occurred in one case which was cured with second operation; time for the recovery of bowl movement was 3–5 (4.2 ± 0.8) days; the time for semifluid dieting was 6–10 (8.2 ± 1.5) days; the hospital stay was 8–20 (12.8 ± 4.63) days. The postoperative fast blood sugar was (6.3 ± 1.6) mmol/L with the normal diet, which was not significantly different from the preoperative data (5.3 ± 0.5) mmol/L (P [ 0.05). The postoperative pathology was as follows: five cases of cystic serous adenoma, one case of intraductal papillary mucinous neoplasm, two cases of neuroendocrine tumor, and two cases of solid pseudopapillary tumor of pancreas. All the patients were followed up for 7–40 months, no recurrence happened, and no new incidence of diabetes or insufficiency of pancreatic exocrine function occurred. All the intraoperative pathology was identical to the postoperative pathological findings. One case was reoperated in emergency due to upper GI bleeding 6 h postoperatively, a vascular bleeding at pancreatic stump was confirmed by gastroscopy, and emergency surgery was
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performed. 4-0 prolene sutures the bleeding site. Delayed gastric empty occurred in one case, which was managed by conservative treatment.
Discussion Low-grade malignancies or benign lesions of the central pancreas present a surgical dilemma between preserving pancreatic endocrine function and resecting sufficient parenchyma to minimize the risk of recurrence. Although enucleation is accepted as an appropriate management for selected benign lesions, low-grade malignancies and benign lesions without involvement of the main pancreatic duct, for the cases with lesions at pancreatic neck with involvement of main pancreatic duct or close to it, PD or DP is always indicated. Despite of the two challenges, the sufficient margin from the concern of surgical oncology and theoretically more risk of POPF due to two pancreatic stumps, CP is an alternative choice and has been applied more recently. Guillemin and Bessot firstly reported central pancreatectomy in 1957 [12], such technique has been reported more recently, even the experience with data of more than 50 cases [2, 13–16], the largest series of cases at the single center with a 12-year experience confirmed its benefit, saying the procedure is best indicated for benign or low-grade lesions in young and fit patients who can sustain a significant postoperative morbidity and could benefit from the excellent longterm results. Such procedure mainly has theoretic benefit: The preservation of the pancreatic parenchyma can remain its endocrine and exocrine function, and the exempt of PD can remain the anatomy of the digestive tract thus avoiding the related complications. However, CP brings several concerns also: The risk of POPF is higher theoretically due to the double cutting ends of pancreas, the possible insufficient margins in case of malignancy. Localizing the tumor in the pancreas usually requires tactile feedback to assess the site and size of the tumor. Intraoperative frozen biopsy for the cutting edge is important, local lymph node biopsy was need for neuroendocrine tumor or IPMN; the close or even resection of distal pancreas will be decided when the remnant pancreas is atrophy or \5 cm, or with inflammation or fibrosis. Intraoperative laparoscopic ultrasound helps to identify the cutting margins therefore securing the sufficient cutting edge. Even though there are two pancreatic stumps after CP, making it seem logical that CP carries a higher overall risk of pancreatic fistula than other pancreatectomy procedures, the POPF is closely related to pancreatic reconstruction, which is another focus of discussion considering the various types of operations. Even though there are many classic approaches for the reconstruction of pancreas, such as the duct to mucosa as in PJ, the two layer anastomosis [2, 9–11, 17], they are not
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suitable for laparoscopic manipulation. Plus, for those pancreatic ducts is\3 mm in diameter and those locate at the edge of the pancreas, such types of reconstruction are extremely technically difficult by laparoscopy with a significantly higher risk of PF; in our ten cases, the diameter of pancreatic duct was 1.6–2.1 mm, average (1.71 ± 0.17) mm. Plus, CP is performed mainly for benign lesions—that is, with a soft pancreas and a nondilated main pancreatic duct, which are consequently at higher risk of pancreatic fistula. From the recent literature, PG is more preferred over PJ as for CP, which is due to several reasons: the reduced anastomosis simplifying the operation, the reduced rate of POPF, and no interference on pancreatic endocrine and exocrine functions [2, 4]; the advantages of PG also lie in the avoidance of activation of pancreatic enzyme, the sufficient blood supply of gastric wall, and the proximity of the stomach and pancreatic stump. Furthermore, gastric and pancreatic secretion is easily diverted with a nasogastric tube after PG, and PG reconstruction may divert potential pancreatic fistulas away from major blood vessels [17]. Also, the duct-to-mucosa anastomosis technique, though accepted as a very reliable technique, is extremely technically challenging technique not applicable and reliable in laparoscopic surgery but in only a few surgeons’ hands. Therefore, despite of some controversies, we prefer PG laparoscopic scenario based on our experience of more than 50 cases of open PD and CP with the BPG [10]. Furthermore, binding PG technique spares the need for suturing anastomosis by simply drawing the purse suture, making it much easier to perform on the gastric wall. In the first case, other than the above-described technique for BPG, we sutured the stump with a straight needle which was first penetrating through the anterior gastric wall and then the abdominal wall, followed by the anchoring the suture from outside of the abdomen, to facilitate the anastomosis. However, when dragging the pancreatic stump into the stomach, it is risky for a possible tearing of the vessels of the pancreatic stump, and the problem lies in that such possible bleeding might not be found after the binding anastomosis. Such incidence happened on the first case of LCP, when upper GI bleeding was emergent within 6 h and arterial active bleeding at the pancreatic stump was confirmed with emergency upper GI endoscopic. The patient was reoperated in emergency, laparotomy with a small ventral midline incision was made, the anterior gastric wall was opened, and the bleeding site was secured with 4-0 prolene suture. An intraoperative upper GI endoscope was applied to rule out such complication in the rest of nine cases. In addition, a full-layer closure of pancreatic stump was performed, and caution should be paid to avoid the pancreatic duct. The delayed gastric emptying has been one major concern for PG, while occurred in one case in this series and was proved to be gastroparesis, which was managed with conservative therapy for 15 days.
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Laparoscope provides a specific observation angle, i.e., from to caudal to cephral; some avascular plane thus could be utilized, e.g., the post-pancreatic tunnel behind the pancreatic neck, when the SMV is identified. We previously introduced a specific binding technique and accumulated our experience both in binding PJ and binding PG (BPG) which was initially invented by Dr. Peng and Dr. Hong, which is widely accepted for their significant advantages in teams of reducing the rate of POPF [9, 10]. Such technique, with its name binding, emphasizes the advantages of binding other than suturing; the underlining advantages are the simplified anastomosis procedure and the reduced risk related to suturing, such as the potential leakage between the adjacent stitches and possibility of the needle hole which penetrates into the small branches of pancreatic duct [5, 10]. We further proved BPG to be safe and effective in open surgery by our previous RCT study with 53 cases in the BPJ group and 62 in the BPG group. In the BPJ group, pancreatic fistulae occurred in six cases (11.3 %), DGE in five, hemorrhage in one, biliary fistulae in two and an abdominal abscess in one. One patient died of MOF caused by an abdominal abscess on the 5th day postoperatively. In the BPG group, pancreatic fistulae developed in four cases(6.5 %), DGE in 11, hemorrhage in three, bililary fistulae in five and abdominal abscesses in two. There were no operative mortalities in the BPG group. No statistical difference was found between the two groups with respect to PF rate. We concluded from that study that both BPJ and BPG are safe and reliable procedures for reconstructing pancreatic digestive continuity after PD. Interestingly, such advantage of exempting suturing is greatly suitable for laparoscopic surgery, because all the reconstructions, either running suture, in which the long thread often tangles, or the stitch suturing, in which the suture cannot be otherwise prepared one by one, often make the most critical step both timeconsuming and not secured. On the other hand, the binding technique often requires a few purses suturing, which has a much requirement for the suturing as required more strictly for anastomosis, e.g., the tension free, clear visionalization and appropriate angle, which are harder to achieve in laparoscopic surgery compared with open surgery. Based on such presumption, we applied modified Peng’s BPG, i.e., the one-layer BPG and applied it in ten laparoscopic CP (LCP) cases, which simplified the laparoscopic procedure with satisfactory results; only three cases had A grade pancreatic fistula. The time for BPG anastomosis in this LBPG series was (20.3 ± 2.6) min, indicating that the learning curve is not long, while the time for laparoscopic pancreatic anastomosis is known lengthy and these types of procedures require extensive experience in open pancreatic surgery combined with a high level of laparoscopic skill.
There are several key steps for such techniques. First, the pancreatic stump needs to be mobilized for at least 3 cm for anastomosis; Second, the opening in the gastric wall should be the most approximated to the pancreatic stump, a fulllayer purse suture with 3-0 prolene on the opening of the gastric wall, in order to reduce the risk of gastric wall bleeding and to provide sufficient strength for suturing. Unlike the open surgery, even though the purse suturing on the gastric wall is not technically challenging under laparoscope, the laparoscopic binding does raise some concerns regarding the strength that is needed during the binding maneuver under laparoscope, when the tactile is much compromised. However, this can be compensated with the visualization of the tissue’s distortion, while the binding thread is tied, and to our experience, the strength should be enough and the binding secured when the thread is sacking into the gastric wall surface. It can be concluded that LCP is feasible and LBPG is a simplified technique facilitating LCP. To our knowledge, this is the first report on binding at the anastomosis under laparoscope. Even though open BPG and BPJ were proved to be effective in our previous RCT study, the binding technique may also have contributed to the low POPF rate of both laparoscopic and open PJ, so a comparative study taking the binding technique as a single factor to rule out other influences thus to valid its validity. Acknowledgments This work was supported by the fund of the Key Project of the Science and Technology Department of Zhejiang Province: the establishment, evaluation and personalized application of binding pancreatojejunostomy/binding pancreatogastrostomy, Fund No: 2013C03046, the Key Funds for the Platform of Medicine of the Health and Family Planning Commission of Zhejiang Province, Nos: 2013ZDA004 and 2015127995, the fund from the Science and Technology Department of Zhejiang Province, No: 2015C33112 and the fund from the Education Department of Heilongjiang Province Government, No: 12511245. Disclosures Drs. Defei Hong, Yingbin Liu, Shuyou Peng, Xiaodong Sun, Zhifei Wang, Jian Cheng, Guoliang Shen, Yuanbiao Zhang and Dongsheng Huang have no conflict of interest or financial ties to disclose.
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