1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54
IJSU1365_proof ■ 25 May 2014 ■ 1/4
International Journal of Surgery xxx (2014) 1e4
Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center Q2
Antonio Sciuto, Roberta Abete, Stefano Reggio, Felice Pirozzi, Anna Settembre, Francesco Corcione* Department of Laparoscopic and Robotic Surgery, “Azienda Ospedaliera dei Colli” e Monaldi Hospital, Via Leonardo Bianchi s.n.c., 80131 Naples, NA, Italy
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 March 2014 Accepted 3 May 2014 Available online xxx
Background: Spleen-preserving laparoscopic distal pancreatectomy is gaining acceptance for treatment of insulinomas of the pancreatic body and tail. The aim of this report is to evaluate feasibility, safety and outcomes of this procedure in a retrospective series. Methods: From May 2004 to November 2013, 9 patients underwent laparoscopic spleen-preserving distal pancreatectomy for benign insulinomas in our department. Tumors were single and sporadic in eight patients, while the remaining patient had insulinomas in the setting of multiple endocrine neoplasia 1. Tumors were located by preoperative imaging in all cases. Laparoscopic ultrasound was always performed to guide the surgical procedure. Results: All the operations were carried out laparoscopically with a mean operative time of 110 min (range 90e210 min) and a mean blood loss of 50 ml (range 30e120 ml). One patient (11.1%) died on the 22nd post-operative day for massive intra-abdominal bleeding associated with pancreatitis of the stump. Two patients (22.2%) developed pancreatic fistula that healed conservatively. Mean postoperative hospital stay was 7.1 days (range 5e18 days). All alive patients were free from recurrence after a mean follow-up of 45 months (range 11e72 months). Conclusion: Laparoscopic spleen-preserving distal pancreatectomy is safe and feasible for the management of benign insulinomas. Definition of the tumor with preoperative imaging and laparoscopic ultrasound is essential to achieve high cure rate with minimal conversion. © 2014 Published by Elsevier Ltd on behalf of Surgical Associates Ltd.
Keywords: Laparoscopic distal pancreatectomy Spleen-preserving Insulinoma Laparoscopic ultrasound Pancreatic benign tumors
1. Introduction Pancreatic insulinomas (PIs) are the most common functioning neuroendocrine tumors, with an incidence of approximately one to four cases per million persons [1]. Surgical resection is the treatment of choice for PIs, with cure being achieved in more than 90% of patients [2,3]. Surgical approaches include enucleation, partial or total pancreatic resection, and pancreaticoduodenectomy. Distal pancreatectomy is indicated for non-enucleable lesions of the pancreatic body and tail and can be performed with or without spleen preservation [4]. The general features of PIs, including small size, high benignity rate, usually sporadic nature and elective localization in the pancreatic body and tail, make these tumors well suitable for laparoscopic treatment [5,6]. With advances in techniques and equipment, including the availability of laparoscopic
* Corresponding author. E-mail address: [email protected] (F. Corcione).
ultrasound, the minimally invasive approach to distal pancreatectomy has become a feasible and safe option over the last few years [7,8]. The aim of this paper is to report our experience with laparoscopic spleen-preserving distal pancreatectomy for insulinomas, evaluating the feasibility, safety and the outcomes of this procedure. 2. Methods From May 2004 to November 2013, 9 patients underwent laparoscopic spleen-preserving distal pancreatectomy for insulinoma in our department. They were identified by a search of a prospective maintained operating room database. Data were retrospectively collected from hospital charts and operative reports. There were five women and four men with a mean age of 36 years (range 28e59 years). Three patients were ASA1, 4 were ASA 2 and 2 were ASA 3. All tumors were located preoperatively by a combination of imaging techniques, including computed tomography, magnetic resonance imaging, 111In-pentetreotide
http://dx.doi.org/10.1016/j.ijsu.2014.05.023 1743-9191/© 2014 Published by Elsevier Ltd on behalf of Surgical Associates Ltd.
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
IJSU1365_proof ■ 25 May 2014 ■ 2/4
2
A. Sciuto et al. / International Journal of Surgery xxx (2014) 1e4
scintigraphy (octreoscan) and endoscopic ultrasound. Mean size of the lesions was 18 mm (range 15e32 mm) and all were suspected to be benign. One patient was affected by multiple endocrine neoplasia type 1 and had two 25-mm insulinomas located in the pancreatic tail and other smaller tumors in the body. The remaining 8 patients underwent surgery for a single and sporadic insulinoma. Five tumors were located in the tail of the pancreas and 3 in the body. 2.1. Surgical technique The patient is placed supine in a reverse Trendelenburg position with 10-degree right lateral tilt and legs abducted. The surgeon stood between the patient's legs with the two assistants on each side. Pneumoperitoneum is created via the open Veres-assisted technique [9] and insufflation pressures are set at 12 mmHg. A 30 telescope is used. Four trocars are used: a 10- to 12-mm telescope trocar (T1) in the midline above the umbilical scar; one 10- to 12-mm trocar along the left (T2) and one 5-mm trocar along the right (T3) midclavear lines, lateral to the rectus muscles, 3 cm above T1; one 5-mm trocar (T4) in the midline below the xiphoid process. At first intraoperative ultrasonography is performed to confirm location and size of the insulinoma and to exclude additional tumors. The gastrocolic ligament is opened to allow entry into the lesser sac and to expose the anterior surface of the pancreas. The inferior short gastric vessels are divided only if necessary to retract the stomach and improve exposure. At this time, laparoscopic ultrasound is newly performed to obtain precise information about the anatomic relation of the tumor with the Wirsung duct and major vessels and to determine the pancreatic resection margin. The anterior inferior surface of the pancreas is dissected free from the attachment of the transverse mesocolon, and the splenocolic ligament is divided to reflect the colon inferiorly. Sharp and blunt dissection of the inferior pancreatic margin proceeds from medial to lateral towards the splenic hilum, where then the splenic vein is identified. Then the vein is dissected free from the posterior surface of the pancreas using a lateral-to-medial approach, with dissection moving from the splenic hilum to the pancreatic section margin. The pancreatic branches of the vein are sequentially identified and ligated using bipolar forceps, ultrasound scalpel or clips. The pancreatic body and tail is further elevated to visualize the splenic artery, which runs just superior to the vein and is dissected free in a similar fashion. Once an adequate mobilization of the pancreas has been achieved, a linear stapler covered by a staple line reinforcement is applied across the pancreatic parenchima sparing the main splenic vessels. The pancreatic remnant is then covered by a hemostatic patch. A drain is placed at the stapled pancreas and the surgical specimen is removed through a minimal enlargement of the T1 site using a retrieval bag. Amylase content in the drain fluid was determined on postoperative days 1,3 and 5. Pancreatic fistula was defined as an amylase value more than 2000 UI/l. 3. Results Successful laparoscopic resection was carried out in all patients without need for conversion or resection of the spleen. Mean operative time was 110 min (range 90e210 min). No intraoperative mortality was recorded. Intraoperative complications included a bleeding from a pancreatic branch of the splenic vein that was controlled by clip placement. Mean intraoperative blood loss was 50 ml (range 30e120 ml). Postoperative mortality was 11.1%. One patient was discharged after a 6-day uneventful postoperative course. He was readmitted on the 22nd postoperative day and underwent reoperation for massive intra-abdominal bleeding
associated with pancreatitis of the stump. Unfortunately, he died shortly after surgery. Postoperative complications included two pancreatic fistulas, accounting for an incidence rate of 22.2%. They were low-output fistulas with associated pleural collections that healed with conservative management, including total parenteral nutrition, persisting drainage and octreotide perfusion. Transient hyperamilasemia was recorded in two patients. Mean postoperative hospital stay was 7.1 days (range 5e18 days). All insulinomas were benign at the final pathologic examination. All alive patients were free from recurrence after a mean follow-up of 45 months (range 11e72 months). 4. Discussion Since the first description by Gagner in 1996 [10], the laparoscopic treatment of PIs in gaining wide acceptance. However, feasibility and safety of this approach has been reported only in a small number of patients, mainly due to the rarity of this tumor and to the need of very skilled surgeons [11e15]. A recent meta-analysis including seven studies with a total of 452 patients found that the laparoscopic approach for PIs is associated with reduction of hospital stay and similar rates of postoperative complications compared to open surgery [6]. Patients with benign tumors located in the body or tail of the pancreas can better benefit from the laparoscopic approach. For this location, either distal pancreatectomy or tumor enucleation can be correctly employed [11]. The size of the tumor and the relationship with the pancreatic duct and splenic vessels as well as the occurrence of multiple lesions are crucial in determining the surgical procedure [4,16,17]. Laparoscopic intraoperative ultrasonography is the most effective technique to assess these issues [18,19]. Furthermore, it is essential to precisely determine the pancreatic resection line, in order to assure a complete tumor excision. For these reasons, the availability of intraoperative ultrasound should be considered essential for guidance of the laparoscopic approach [19]. The use of this imaging modality may also help to significantly reduce the need for conversion. Inability to localize the tumor has been reported as the main reason for conversion together with technical difficulties in performing pancreatic resection [19,20]. Conversion rates in the literature vary from 20 to 33% [6], but in our series no conversion occurred. Distal pancreatectomy is the procedure of choice for insulinomas of the pancreatic body and tail located deeply in the parenchima and close to the main pancreatic duct [15]. Recent literature confirms that laparoscopic distal pancreatectomy is a feasible and safe procedure in patients with benign or low grade malignancies [7]. Two major issues related to this procedure are preserving the spleen and controlling the leak from the pancreatic stump. As with open surgery, spleen preservation is encouraged whenever it is technically feasible, although reported experiences are limited [15,21,22]. It is advocated given the lack of oncologic reasons for removing the lymphatics along the splenic vessels and the lymph nodes in the splenic hilum [22]. Moreover, spleen preservation has been reported to be associated with a reduction in perioperative infections and severe complications [23]. Preservation of the spleen with distal pancreatectomy can be achieved by carefully dissecting the pancreas off the splenic vessels or by maintaining the blood to the spleen via short gastric vessels, with resection of the splenic artery and vein (Warshaw's technique). The latter procedure may shorten operative time and reduce blood loss as well as the incidence of massive bleeding from injury to the splenic vessels [24,25]. Although Warshaw's technique has been reported for PIs [26], these advantages may be less evident for patients with small and benign tumors like PIs, especially if not located close to the splenic vessels. Moreover, this procedure may
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
IJSU1365_proof ■ 25 May 2014 ■ 3/4
A. Sciuto et al. / International Journal of Surgery xxx (2014) 1e4
be associated with postoperative splenic infarction requiring splenectomy as well as long-term complications, including bleeding from gastric and perigastric varices [22,27,28]. Preservation of the splenic vessels should be always attempted, and a careful blunt dissection together with the appropriate use of modern technologies is the key to achieve it. The short gastric vessels should be preserved during the operation, in order to allow a “conversion” to Warshaw's technique in case of a very difficult dissection or accidental bleeding [29]. In our experience, we performed this procedure only twice for large pancreatic cistoadenoma close to the splenic vessels. In both cases, the postoperative course was complicated by splenic infarction. Pancreatic fistula is the other major issue regarding distal pancreatectomy. It remains the most common postoperative complication, with an incidence rate up to more than 27% [30]. Recent comparative studies and meta-analysis found that the laparoscopic approach is associated with a similar rates of fistula compared to open surgery [6,31,32]. However, a limitation is that variation exists in the definition of pancreatic fistula among the studies. Several surgical techniques and devices for management of the pancreatic stump have been proposed to prevent leakage, including stapler, sutures, radiofrequency or ultrasonic devices, fibrin glue, sealants and patches, but without any significant improvement [33e35]. The incidence of pancreatic fistula seems to be related neither to the method of stamp closure nor to underlying pathologic process [36]. In our series fistula occurred in 22.2% of patients and none of them required reoperation. In conclusion, spleen-preserving laparoscopic pancreatectomy can be safely performed in most patients with benign insulinomas. Definition of the tumor with preoperative imaging and laparoscopic ultrasound is essential to achieve high cure rate with minimal conversion. Additional researches are needed to reduce the incidence of pancreatic fistula. Ethical approval This is a retrospective study based only on the analyses of recorded data and then no Ethical Approval was necessary. Q1
Author contribution Antonio Sciuto: Participated substantially in conception and design of the study, collection and analysis of data; also participated substantially in the drafting and editing of the manuscript. Roberta Abete: Participated substantially in conception and design of the study, collection and analysis of data; also participated substantially in the drafting and editing of the manuscript. Stefano Reggio: Participated substantially in conception and design of the study, collection and analysis of data; also participated substantially in the drafting and editing of the manuscript. Felice Pirozzi: Participated substantially in conception and design of the study, analysis of data and critical revision of the manuscript. Anna Settembre: Participated substantially in conception and design of the study, analysis of data and critical revision of the manuscript. Francesco Corcione: Participated substantially in conception and design of the study, analysis of data and critical revision of the manuscript. All the authors approved the final version of the manuscript. Funding No funding has been received for this paper.
3
Conflict of interest The authors have no conflicts of interest to disclose. References [1] A. Mathur, P. Gorden, S.K. Libutti, Insulinoma, Surg. Clin. North Am. 89 (2009) 1105e1121. [2] B.D. Matthews, T.I. Smith, K.W. Kercher, W.D. Holder Jr., B.T. Heniford, Surgical experience with functioning pancreatic neuroendocrine tumor, Am. Surg. 68 (2002) 660e665. [3] E. Finlayson, O.H. Clark, Surgical treatment of insulinomas, Surg. Clin. North Am. 84 (2004) 775e785. [4] H. Liu, C. Peng, S. Zhang, et al., Strategy for the surgical management of insulinomas: analysis of 52 cases, Dig. Surg. 24 (2007) 463e470. [5] J.J. Shin, P. Gorden, S.K. Libutti, Insulinoma: pathophysiology, localization and management, Future Oncol. 6 (2010) 229e237. [6] A.P. Su, N.W. Ke, Y. Zhang, et al., Is laparoscopic approach for pancreatic insulinomas safe? Results of a systematic review and meta-analysis, J. Surg. Res. 186 (2014) 126e134. [7] M. Iacobone, M. Citton, D. Nitti, Laparoscopic distal pancreatectomy: up-todate and literature review, World J. Gastroenterol. 18 (2012) 5329e5337. [8] F. Corcione, E. Marzano, D. Cuccurullo, V. Caracino, F. Pirozzi, A. Settembre, Distal pancreas surgery: outcome for 19 cases managed with a laparoscopic approach, Surg. Endosc. 20 (2006) 1729e1732. [9] F. Corcione, L. Miranda, A. Settembre, et al., Open Veress assisted technique. Results in 2700 cases, Minerva Chir. 62 (2007) 443e446. [10] M. Gagner, A. Pomp, M.F. Herrera, Early experience with laparoscopic resections of islet cell tumors, Surgery 120 (1996) 1051e1054. [11] A. Toniato, F. Meduri, M. Foletto, A. Avogaro, M. Pelizzo, Laparoscopic treatment of benign insulinomas localized in the body and tail of the pancreas: a single-center experience, World J. Surg. 30 (2006) 1916e1919. [12] A. Isla, J.D. Arbuckle, P.B. Kekis, et al., Laparoscopic management of insulinomas, Br. J. Surg. 96 (2009) 185e190. [13] C.Y. Lo, W.F. Chan, C.M. Lo, S.T. Fan, P.K. Tam, Surgical treatment of pancreatic insulinomas in the era of laparoscopy, Surg. Endosc. 18 (2004) 297e302. [14] M. Hu, G. Zhao, Y. Luo, R. Liu, Laparoscopic versus open treatment for benign pancreatic insulinomas: an analysis of 89 cases, Surg. Endosc. 25 (2011) 3831e3837. [15] Y. Luo, R. Liu, M.G. Hu, Y.M. Mu, L.C. An, Z.Q. Huang, Laparoscopic surgery for pancreatic insulinomas: a single-institution experience of 29 cases, J. Gastrointest. Surg. 13 (2009) 945e950. ndez-Cruz, G. Cesar-Borges, Laparoscopic strategies for resection of [16] L. Ferna insulinomas, J. Gastrointest. Surg. 10 (2006) 752e760. [17] Y.P. Zhao, H.X. Zhan, T.P. Zhang, et al., Surgical management of patients with insulinomas: result of 292 cases in a single institution, J. Surg. Oncol. 103 (2011) 169e174. [18] C.Y. Lo, C.M. Lo, S.T. Fan, Role of laparoscopic ultrasonography in intraoperative localization of pancreatic insulinoma, Surg. Endosc. 14 (2000) 1131e1135. te Française de Chirurgie [19] A. Ayav, L. Bresler, L. Brunaud, P. Boissel, SFCL (Socie Laparoscopique); AFCE (association Francophone de Chirurgie Endocrinienne). Laparoscopic approach for solitary insulinoma: a multicentre study, Langenbecks Arch. Surg. 390 (2005) 134e140. [20] A. Sa Cunha, C. Beau, A. Rault, B. Catargi, D. Collet, B. Masson, Laparoscopic versus open approach for solitary insulinoma, Surg. Endosc. 21 (2007) 103e108. [21] X. Ding, J. Tan, J. Qian, Laparoscopic spleen-preserving distal pancreatectomy (LSPDP), Hepatogastroenterology 60 (2013) 605e610. [22] G. Butturini, M. Inama, G. Malleo, et al., Perioperative and long-term results of laparoscopic spleen-preserving distal pancreatectomy with or without splenic vessels conservation: a retrospective analysis, J. Surg. Oncol. 105 (2012) 387e392. [23] M. Shoup, M.F. Brennan, K. McWhite, D.H. Leung, D. Klimstra, K.C. Conlon. The value of splenic preservation with distal pancreatectomy. Arch. Surg. 137: 164e168. [24] A.L. Warshaw, Distal pancreatectomy with preservation of the spleen, J. Hepatobiliary Pancreat. Sci. 17 (2010) 808e812. [25] A. Pryor, J.R. Means, T.N. Pappas, Laparoscopic distal pancreatectomy with splenic preservation, Surg. Endosc. 21 (2007) 2326e2330. [26] S. Shimizu, M. Tanaka, H. Konomi, T. Tamura, K. Mizumoto, K. Yamaguchi, Spleen-preserving laparoscopic distal pancreatectomy after division of the splenic vessels, J. Laparoendosc. Adv. Surg. Tech. A 14 (2004) 173e177. [27] F. Miura, T. Takada, T. Asano, et al., Hemodynamic changes of splenogastric circulation after spleen-preserving pancreatectomy with excision of splenic artery and vein, Surgery 138 (2005) 518e522. [28] G.Y. Lv, G.Y. Wang, C. Jiang, et al., Laparoscopic spleen-preserving distal pancreatectomy with or without splenic vessel conservation: a retrospective study of 20 cases, Hepatogastroenterology 60 (2013) 1785e1788. ndez-Cruz, I. Martínez, R. Gilabert, G. Cesar-Borges, E. Astudillo, [29] L. Ferna S. Navarro, Laparoscopic distal pancreatectomy combined with preservation of the spleen for cystic neoplasms of the pancreas, J. Gastrointest. Surg. 8 (2004) 493e501.
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9
IJSU1365_proof ■ 25 May 2014 ■ 4/4
4
A. Sciuto et al. / International Journal of Surgery xxx (2014) 1e4
[30] Y. Nakamura, E. Uchida, T. Aimoto, S. Matsumoto, H. Yoshida, T. Tajiri, Clinical outcome of laparoscopic distal pancreatectomy, J. Hepatobiliary Pancreat. Surg. 16 (2009) 35e41. [31] B.W. Eom, J.Y. Jang, S.E. Lee, H.S. Han, Y.S. Yoon, S.W. Kim, Clinical outcomes compared between laparoscopic and open distal pancreatectomy, Surg. Endosc. 22 (2008) 1334e1338. [32] S.S. Mehta, G. Doumane, T. Mura, D. Nocca, J.M. Fabre, Laparoscopic versus open distal pancreatectomy: a single-institution case-control study, Surg. Endosc. 26 (2012) 402e407. €pfer, A. Thiede, S. Timm, Analysis of closure [33] U. Lorenz, M. Maier, U. Steger, C. To of the pancreatic remnant after distal pancreatic resection, HPB 9 (2007) 302e307.
[34] T.I. Carter, Z.V. Fong, T. Hyslop, et al., A dual-institution randomized controlled trial of remnant closure after distal pancreatectomy: does the addition of a falciform patch and fibrin glue improve outcomes? J. Gastrointest. Surg. 17 (2013) 102e109. [35] U.F. Wellner, F. Makowiec, O. Sick, U.T. Hopt, T. Keck, Arguments for an individualized closure of the pancreatic remnant after distal pancreatic resection, World J. Gastrointest. Surg. 4 (2012) 114e120. [36] M.K. Sheehan, K. Beck, S. Creech, J. Pickleman, G.V. Aranha, Distal pancreatectomy: does the method of closure influence fistula formation? Am. Surg. 68 (2002) 264e267.
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
10 11 12 13 14 15 16 17 18
IJSU1365_proof ■ 25 May 2014 ■ 1/4
International Journal of Surgery xxx (2014) 1e4
Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center Q2
Antonio Sciuto, Roberta Abete, Stefano Reggio, Felice Pirozzi, Anna Settembre, Francesco Corcione* Department of Laparoscopic and Robotic Surgery, “Azienda Ospedaliera dei Colli” e Monaldi Hospital, Via Leonardo Bianchi s.n.c., 80131 Naples, NA, Italy
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 March 2014 Accepted 3 May 2014 Available online xxx
Background: Spleen-preserving laparoscopic distal pancreatectomy is gaining acceptance for treatment of insulinomas of the pancreatic body and tail. The aim of this report is to evaluate feasibility, safety and outcomes of this procedure in a retrospective series. Methods: From May 2004 to November 2013, 9 patients underwent laparoscopic spleen-preserving distal pancreatectomy for benign insulinomas in our department. Tumors were single and sporadic in eight patients, while the remaining patient had insulinomas in the setting of multiple endocrine neoplasia 1. Tumors were located by preoperative imaging in all cases. Laparoscopic ultrasound was always performed to guide the surgical procedure. Results: All the operations were carried out laparoscopically with a mean operative time of 110 min (range 90e210 min) and a mean blood loss of 50 ml (range 30e120 ml). One patient (11.1%) died on the 22nd post-operative day for massive intra-abdominal bleeding associated with pancreatitis of the stump. Two patients (22.2%) developed pancreatic fistula that healed conservatively. Mean postoperative hospital stay was 7.1 days (range 5e18 days). All alive patients were free from recurrence after a mean follow-up of 45 months (range 11e72 months). Conclusion: Laparoscopic spleen-preserving distal pancreatectomy is safe and feasible for the management of benign insulinomas. Definition of the tumor with preoperative imaging and laparoscopic ultrasound is essential to achieve high cure rate with minimal conversion. © 2014 Published by Elsevier Ltd on behalf of Surgical Associates Ltd.
Keywords: Laparoscopic distal pancreatectomy Spleen-preserving Insulinoma Laparoscopic ultrasound Pancreatic benign tumors
1. Introduction Pancreatic insulinomas (PIs) are the most common functioning neuroendocrine tumors, with an incidence of approximately one to four cases per million persons [1]. Surgical resection is the treatment of choice for PIs, with cure being achieved in more than 90% of patients [2,3]. Surgical approaches include enucleation, partial or total pancreatic resection, and pancreaticoduodenectomy. Distal pancreatectomy is indicated for non-enucleable lesions of the pancreatic body and tail and can be performed with or without spleen preservation [4]. The general features of PIs, including small size, high benignity rate, usually sporadic nature and elective localization in the pancreatic body and tail, make these tumors well suitable for laparoscopic treatment [5,6]. With advances in techniques and equipment, including the availability of laparoscopic
* Corresponding author. E-mail address: [email protected] (F. Corcione).
ultrasound, the minimally invasive approach to distal pancreatectomy has become a feasible and safe option over the last few years [7,8]. The aim of this paper is to report our experience with laparoscopic spleen-preserving distal pancreatectomy for insulinomas, evaluating the feasibility, safety and the outcomes of this procedure. 2. Methods From May 2004 to November 2013, 9 patients underwent laparoscopic spleen-preserving distal pancreatectomy for insulinoma in our department. They were identified by a search of a prospective maintained operating room database. Data were retrospectively collected from hospital charts and operative reports. There were five women and four men with a mean age of 36 years (range 28e59 years). Three patients were ASA1, 4 were ASA 2 and 2 were ASA 3. All tumors were located preoperatively by a combination of imaging techniques, including computed tomography, magnetic resonance imaging, 111In-pentetreotide
http://dx.doi.org/10.1016/j.ijsu.2014.05.023 1743-9191/© 2014 Published by Elsevier Ltd on behalf of Surgical Associates Ltd.
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
IJSU1365_proof ■ 25 May 2014 ■ 2/4
2
A. Sciuto et al. / International Journal of Surgery xxx (2014) 1e4
scintigraphy (octreoscan) and endoscopic ultrasound. Mean size of the lesions was 18 mm (range 15e32 mm) and all were suspected to be benign. One patient was affected by multiple endocrine neoplasia type 1 and had two 25-mm insulinomas located in the pancreatic tail and other smaller tumors in the body. The remaining 8 patients underwent surgery for a single and sporadic insulinoma. Five tumors were located in the tail of the pancreas and 3 in the body. 2.1. Surgical technique The patient is placed supine in a reverse Trendelenburg position with 10-degree right lateral tilt and legs abducted. The surgeon stood between the patient's legs with the two assistants on each side. Pneumoperitoneum is created via the open Veres-assisted technique [9] and insufflation pressures are set at 12 mmHg. A 30 telescope is used. Four trocars are used: a 10- to 12-mm telescope trocar (T1) in the midline above the umbilical scar; one 10- to 12-mm trocar along the left (T2) and one 5-mm trocar along the right (T3) midclavear lines, lateral to the rectus muscles, 3 cm above T1; one 5-mm trocar (T4) in the midline below the xiphoid process. At first intraoperative ultrasonography is performed to confirm location and size of the insulinoma and to exclude additional tumors. The gastrocolic ligament is opened to allow entry into the lesser sac and to expose the anterior surface of the pancreas. The inferior short gastric vessels are divided only if necessary to retract the stomach and improve exposure. At this time, laparoscopic ultrasound is newly performed to obtain precise information about the anatomic relation of the tumor with the Wirsung duct and major vessels and to determine the pancreatic resection margin. The anterior inferior surface of the pancreas is dissected free from the attachment of the transverse mesocolon, and the splenocolic ligament is divided to reflect the colon inferiorly. Sharp and blunt dissection of the inferior pancreatic margin proceeds from medial to lateral towards the splenic hilum, where then the splenic vein is identified. Then the vein is dissected free from the posterior surface of the pancreas using a lateral-to-medial approach, with dissection moving from the splenic hilum to the pancreatic section margin. The pancreatic branches of the vein are sequentially identified and ligated using bipolar forceps, ultrasound scalpel or clips. The pancreatic body and tail is further elevated to visualize the splenic artery, which runs just superior to the vein and is dissected free in a similar fashion. Once an adequate mobilization of the pancreas has been achieved, a linear stapler covered by a staple line reinforcement is applied across the pancreatic parenchima sparing the main splenic vessels. The pancreatic remnant is then covered by a hemostatic patch. A drain is placed at the stapled pancreas and the surgical specimen is removed through a minimal enlargement of the T1 site using a retrieval bag. Amylase content in the drain fluid was determined on postoperative days 1,3 and 5. Pancreatic fistula was defined as an amylase value more than 2000 UI/l. 3. Results Successful laparoscopic resection was carried out in all patients without need for conversion or resection of the spleen. Mean operative time was 110 min (range 90e210 min). No intraoperative mortality was recorded. Intraoperative complications included a bleeding from a pancreatic branch of the splenic vein that was controlled by clip placement. Mean intraoperative blood loss was 50 ml (range 30e120 ml). Postoperative mortality was 11.1%. One patient was discharged after a 6-day uneventful postoperative course. He was readmitted on the 22nd postoperative day and underwent reoperation for massive intra-abdominal bleeding
associated with pancreatitis of the stump. Unfortunately, he died shortly after surgery. Postoperative complications included two pancreatic fistulas, accounting for an incidence rate of 22.2%. They were low-output fistulas with associated pleural collections that healed with conservative management, including total parenteral nutrition, persisting drainage and octreotide perfusion. Transient hyperamilasemia was recorded in two patients. Mean postoperative hospital stay was 7.1 days (range 5e18 days). All insulinomas were benign at the final pathologic examination. All alive patients were free from recurrence after a mean follow-up of 45 months (range 11e72 months). 4. Discussion Since the first description by Gagner in 1996 [10], the laparoscopic treatment of PIs in gaining wide acceptance. However, feasibility and safety of this approach has been reported only in a small number of patients, mainly due to the rarity of this tumor and to the need of very skilled surgeons [11e15]. A recent meta-analysis including seven studies with a total of 452 patients found that the laparoscopic approach for PIs is associated with reduction of hospital stay and similar rates of postoperative complications compared to open surgery [6]. Patients with benign tumors located in the body or tail of the pancreas can better benefit from the laparoscopic approach. For this location, either distal pancreatectomy or tumor enucleation can be correctly employed [11]. The size of the tumor and the relationship with the pancreatic duct and splenic vessels as well as the occurrence of multiple lesions are crucial in determining the surgical procedure [4,16,17]. Laparoscopic intraoperative ultrasonography is the most effective technique to assess these issues [18,19]. Furthermore, it is essential to precisely determine the pancreatic resection line, in order to assure a complete tumor excision. For these reasons, the availability of intraoperative ultrasound should be considered essential for guidance of the laparoscopic approach [19]. The use of this imaging modality may also help to significantly reduce the need for conversion. Inability to localize the tumor has been reported as the main reason for conversion together with technical difficulties in performing pancreatic resection [19,20]. Conversion rates in the literature vary from 20 to 33% [6], but in our series no conversion occurred. Distal pancreatectomy is the procedure of choice for insulinomas of the pancreatic body and tail located deeply in the parenchima and close to the main pancreatic duct [15]. Recent literature confirms that laparoscopic distal pancreatectomy is a feasible and safe procedure in patients with benign or low grade malignancies [7]. Two major issues related to this procedure are preserving the spleen and controlling the leak from the pancreatic stump. As with open surgery, spleen preservation is encouraged whenever it is technically feasible, although reported experiences are limited [15,21,22]. It is advocated given the lack of oncologic reasons for removing the lymphatics along the splenic vessels and the lymph nodes in the splenic hilum [22]. Moreover, spleen preservation has been reported to be associated with a reduction in perioperative infections and severe complications [23]. Preservation of the spleen with distal pancreatectomy can be achieved by carefully dissecting the pancreas off the splenic vessels or by maintaining the blood to the spleen via short gastric vessels, with resection of the splenic artery and vein (Warshaw's technique). The latter procedure may shorten operative time and reduce blood loss as well as the incidence of massive bleeding from injury to the splenic vessels [24,25]. Although Warshaw's technique has been reported for PIs [26], these advantages may be less evident for patients with small and benign tumors like PIs, especially if not located close to the splenic vessels. Moreover, this procedure may
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
IJSU1365_proof ■ 25 May 2014 ■ 3/4
A. Sciuto et al. / International Journal of Surgery xxx (2014) 1e4
be associated with postoperative splenic infarction requiring splenectomy as well as long-term complications, including bleeding from gastric and perigastric varices [22,27,28]. Preservation of the splenic vessels should be always attempted, and a careful blunt dissection together with the appropriate use of modern technologies is the key to achieve it. The short gastric vessels should be preserved during the operation, in order to allow a “conversion” to Warshaw's technique in case of a very difficult dissection or accidental bleeding [29]. In our experience, we performed this procedure only twice for large pancreatic cistoadenoma close to the splenic vessels. In both cases, the postoperative course was complicated by splenic infarction. Pancreatic fistula is the other major issue regarding distal pancreatectomy. It remains the most common postoperative complication, with an incidence rate up to more than 27% [30]. Recent comparative studies and meta-analysis found that the laparoscopic approach is associated with a similar rates of fistula compared to open surgery [6,31,32]. However, a limitation is that variation exists in the definition of pancreatic fistula among the studies. Several surgical techniques and devices for management of the pancreatic stump have been proposed to prevent leakage, including stapler, sutures, radiofrequency or ultrasonic devices, fibrin glue, sealants and patches, but without any significant improvement [33e35]. The incidence of pancreatic fistula seems to be related neither to the method of stamp closure nor to underlying pathologic process [36]. In our series fistula occurred in 22.2% of patients and none of them required reoperation. In conclusion, spleen-preserving laparoscopic pancreatectomy can be safely performed in most patients with benign insulinomas. Definition of the tumor with preoperative imaging and laparoscopic ultrasound is essential to achieve high cure rate with minimal conversion. Additional researches are needed to reduce the incidence of pancreatic fistula. Ethical approval This is a retrospective study based only on the analyses of recorded data and then no Ethical Approval was necessary. Q1
Author contribution Antonio Sciuto: Participated substantially in conception and design of the study, collection and analysis of data; also participated substantially in the drafting and editing of the manuscript. Roberta Abete: Participated substantially in conception and design of the study, collection and analysis of data; also participated substantially in the drafting and editing of the manuscript. Stefano Reggio: Participated substantially in conception and design of the study, collection and analysis of data; also participated substantially in the drafting and editing of the manuscript. Felice Pirozzi: Participated substantially in conception and design of the study, analysis of data and critical revision of the manuscript. Anna Settembre: Participated substantially in conception and design of the study, analysis of data and critical revision of the manuscript. Francesco Corcione: Participated substantially in conception and design of the study, analysis of data and critical revision of the manuscript. All the authors approved the final version of the manuscript. Funding No funding has been received for this paper.
3
Conflict of interest The authors have no conflicts of interest to disclose. References [1] A. Mathur, P. Gorden, S.K. Libutti, Insulinoma, Surg. Clin. North Am. 89 (2009) 1105e1121. [2] B.D. Matthews, T.I. Smith, K.W. Kercher, W.D. Holder Jr., B.T. Heniford, Surgical experience with functioning pancreatic neuroendocrine tumor, Am. Surg. 68 (2002) 660e665. [3] E. Finlayson, O.H. Clark, Surgical treatment of insulinomas, Surg. Clin. North Am. 84 (2004) 775e785. [4] H. Liu, C. Peng, S. Zhang, et al., Strategy for the surgical management of insulinomas: analysis of 52 cases, Dig. Surg. 24 (2007) 463e470. [5] J.J. Shin, P. Gorden, S.K. Libutti, Insulinoma: pathophysiology, localization and management, Future Oncol. 6 (2010) 229e237. [6] A.P. Su, N.W. Ke, Y. Zhang, et al., Is laparoscopic approach for pancreatic insulinomas safe? Results of a systematic review and meta-analysis, J. Surg. Res. 186 (2014) 126e134. [7] M. Iacobone, M. Citton, D. Nitti, Laparoscopic distal pancreatectomy: up-todate and literature review, World J. Gastroenterol. 18 (2012) 5329e5337. [8] F. Corcione, E. Marzano, D. Cuccurullo, V. Caracino, F. Pirozzi, A. Settembre, Distal pancreas surgery: outcome for 19 cases managed with a laparoscopic approach, Surg. Endosc. 20 (2006) 1729e1732. [9] F. Corcione, L. Miranda, A. Settembre, et al., Open Veress assisted technique. Results in 2700 cases, Minerva Chir. 62 (2007) 443e446. [10] M. Gagner, A. Pomp, M.F. Herrera, Early experience with laparoscopic resections of islet cell tumors, Surgery 120 (1996) 1051e1054. [11] A. Toniato, F. Meduri, M. Foletto, A. Avogaro, M. Pelizzo, Laparoscopic treatment of benign insulinomas localized in the body and tail of the pancreas: a single-center experience, World J. Surg. 30 (2006) 1916e1919. [12] A. Isla, J.D. Arbuckle, P.B. Kekis, et al., Laparoscopic management of insulinomas, Br. J. Surg. 96 (2009) 185e190. [13] C.Y. Lo, W.F. Chan, C.M. Lo, S.T. Fan, P.K. Tam, Surgical treatment of pancreatic insulinomas in the era of laparoscopy, Surg. Endosc. 18 (2004) 297e302. [14] M. Hu, G. Zhao, Y. Luo, R. Liu, Laparoscopic versus open treatment for benign pancreatic insulinomas: an analysis of 89 cases, Surg. Endosc. 25 (2011) 3831e3837. [15] Y. Luo, R. Liu, M.G. Hu, Y.M. Mu, L.C. An, Z.Q. Huang, Laparoscopic surgery for pancreatic insulinomas: a single-institution experience of 29 cases, J. Gastrointest. Surg. 13 (2009) 945e950. ndez-Cruz, G. Cesar-Borges, Laparoscopic strategies for resection of [16] L. Ferna insulinomas, J. Gastrointest. Surg. 10 (2006) 752e760. [17] Y.P. Zhao, H.X. Zhan, T.P. Zhang, et al., Surgical management of patients with insulinomas: result of 292 cases in a single institution, J. Surg. Oncol. 103 (2011) 169e174. [18] C.Y. Lo, C.M. Lo, S.T. Fan, Role of laparoscopic ultrasonography in intraoperative localization of pancreatic insulinoma, Surg. Endosc. 14 (2000) 1131e1135. te Française de Chirurgie [19] A. Ayav, L. Bresler, L. Brunaud, P. Boissel, SFCL (Socie Laparoscopique); AFCE (association Francophone de Chirurgie Endocrinienne). Laparoscopic approach for solitary insulinoma: a multicentre study, Langenbecks Arch. Surg. 390 (2005) 134e140. [20] A. Sa Cunha, C. Beau, A. Rault, B. Catargi, D. Collet, B. Masson, Laparoscopic versus open approach for solitary insulinoma, Surg. Endosc. 21 (2007) 103e108. [21] X. Ding, J. Tan, J. Qian, Laparoscopic spleen-preserving distal pancreatectomy (LSPDP), Hepatogastroenterology 60 (2013) 605e610. [22] G. Butturini, M. Inama, G. Malleo, et al., Perioperative and long-term results of laparoscopic spleen-preserving distal pancreatectomy with or without splenic vessels conservation: a retrospective analysis, J. Surg. Oncol. 105 (2012) 387e392. [23] M. Shoup, M.F. Brennan, K. McWhite, D.H. Leung, D. Klimstra, K.C. Conlon. The value of splenic preservation with distal pancreatectomy. Arch. Surg. 137: 164e168. [24] A.L. Warshaw, Distal pancreatectomy with preservation of the spleen, J. Hepatobiliary Pancreat. Sci. 17 (2010) 808e812. [25] A. Pryor, J.R. Means, T.N. Pappas, Laparoscopic distal pancreatectomy with splenic preservation, Surg. Endosc. 21 (2007) 2326e2330. [26] S. Shimizu, M. Tanaka, H. Konomi, T. Tamura, K. Mizumoto, K. Yamaguchi, Spleen-preserving laparoscopic distal pancreatectomy after division of the splenic vessels, J. Laparoendosc. Adv. Surg. Tech. A 14 (2004) 173e177. [27] F. Miura, T. Takada, T. Asano, et al., Hemodynamic changes of splenogastric circulation after spleen-preserving pancreatectomy with excision of splenic artery and vein, Surgery 138 (2005) 518e522. [28] G.Y. Lv, G.Y. Wang, C. Jiang, et al., Laparoscopic spleen-preserving distal pancreatectomy with or without splenic vessel conservation: a retrospective study of 20 cases, Hepatogastroenterology 60 (2013) 1785e1788. ndez-Cruz, I. Martínez, R. Gilabert, G. Cesar-Borges, E. Astudillo, [29] L. Ferna S. Navarro, Laparoscopic distal pancreatectomy combined with preservation of the spleen for cystic neoplasms of the pancreas, J. Gastrointest. Surg. 8 (2004) 493e501.
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9
IJSU1365_proof ■ 25 May 2014 ■ 4/4
4
A. Sciuto et al. / International Journal of Surgery xxx (2014) 1e4
[30] Y. Nakamura, E. Uchida, T. Aimoto, S. Matsumoto, H. Yoshida, T. Tajiri, Clinical outcome of laparoscopic distal pancreatectomy, J. Hepatobiliary Pancreat. Surg. 16 (2009) 35e41. [31] B.W. Eom, J.Y. Jang, S.E. Lee, H.S. Han, Y.S. Yoon, S.W. Kim, Clinical outcomes compared between laparoscopic and open distal pancreatectomy, Surg. Endosc. 22 (2008) 1334e1338. [32] S.S. Mehta, G. Doumane, T. Mura, D. Nocca, J.M. Fabre, Laparoscopic versus open distal pancreatectomy: a single-institution case-control study, Surg. Endosc. 26 (2012) 402e407. €pfer, A. Thiede, S. Timm, Analysis of closure [33] U. Lorenz, M. Maier, U. Steger, C. To of the pancreatic remnant after distal pancreatic resection, HPB 9 (2007) 302e307.
[34] T.I. Carter, Z.V. Fong, T. Hyslop, et al., A dual-institution randomized controlled trial of remnant closure after distal pancreatectomy: does the addition of a falciform patch and fibrin glue improve outcomes? J. Gastrointest. Surg. 17 (2013) 102e109. [35] U.F. Wellner, F. Makowiec, O. Sick, U.T. Hopt, T. Keck, Arguments for an individualized closure of the pancreatic remnant after distal pancreatic resection, World J. Gastrointest. Surg. 4 (2012) 114e120. [36] M.K. Sheehan, K. Beck, S. Creech, J. Pickleman, G.V. Aranha, Distal pancreatectomy: does the method of closure influence fistula formation? Am. Surg. 68 (2002) 264e267.
Please cite this article in press as: A. Sciuto, et al., Laparoscopic spleen-preserving distal pancreatectomy for insulinoma: Experience of a single center, International Journal of Surgery (2014), http://dx.doi.org/10.1016/j.ijsu.2014.05.023
10 11 12 13 14 15 16 17 18
