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    Laparoscopic distal pancreatectomy with or without splenectomy:spleen-preservation does not increase morbidity

    2012-06-11 08:05:56

    Beijing,China

    Introduction

    Laparoscopic surgery is one of the greatest revolutions in modern medicine; its prominent advantages of smaller incision,faster recovery,and reduced pain make it more and more popular all over the world.In the past ten years,with the advancement in surgical technology and accumulation of laparoscopic skills,pancreatic laparoscopic surgery has been gaining recognition and increased in practice,including explorative laparoscopy for cancer staging,diagnostic laparoscopic biopsy,external and internal pancreatic drainage,enucleation,distal pancreatectomy,and even pancreaticoduodenectomy.Among these,laparoscopic distal pancreatectomy was the first and most rapidly developed for its comparative technical simplicity.[1-4]

    Laparoscopic distal pancreatectomy is accepted for benign and low-malignancy tumors located in the distal pancreas.[2-6]However,irrespective of open or laparoscopic procedures for distal pancreatectomy,the indications for spleen preservation are ill-defined.Whether splenectomy can cause a series of adverse consequences such as postoperative abscesses and sepsis has been widely debated in the literature and remains controversial.[7-10]Furthermore,to date,there are few reports extensively comparing laparoscopic spleen-preserving distal pancreatectomy (LSPDP) with laparoscopic distal pancreatectomy with splenectomy(LDPS),although many comparisons in open procedures have been conducted.This study aimed to share our indications for spleen-preservation and surgical experience in laparoscopic procedures,and compare the safety and outcome of LSPDP with LDPS.

    Methods

    We searched for all patients for whom LDPS or LSPDP had been performed at our hospital between July 2002 and April 2010 (including all successful and converted cases).Only patients with a preoperative diagnosis of benign or low-degree malignant tumors by CT or endoscopic ultrasound were considered for laparoscopic surgery and all of them had given informed consent.The indications for LDPS at our institution included 1)tumor size >5 cm; 2) appearance of dense adhesions between tumor and splenic vessels; and 3) malignancy not excluded.For benign tumors <5 cm,LSPDP was the first recommended choice for patients.Medical records of these patients were reviewed retrospectively in terms of patient characteristics,preoperative investigations,operative procedures,splenic preservation,tumor size,blood loss,intra- and post-operative complications,pathologic diagnosis,and outcome.

    Surgical procedures

    We used 4 trocars.The first one was 10 mm and inserted into the umbilicus for location of a 30° telescope,two 5-mm trocars at the right upper quadrant and left midclavicular line below the costal arch,and one 12-mm trocar at the anterior axillary line of the left lower quadrant.The gastrocolic and gastrosplenic ligaments were divided by a ultrasonic dissection of 10-mm,the adhesion between the posterior gastric wall and surface of the pancreas was released,then the inferior border of the pancreas and adhesion between the retroperitoneum and posterior aspect of the pancreas were mobilized.The splenic artery was identified and dissected at the upper border of the pancreas body (Fig.1).During LDPS,the pancreas was transected with Endo-GIA staplers (Tyco Healthcare,Norwalk,CT,USA) (Fig.2) and splenic vessels were ligated with Endo-GIA staplers or clips.Bleeding from the stump or pancreatic vessels was controlled by additional sutures or clips (Fig.3).During LSPDP,the splenic artery and vein were dissected gently from the pancreas; a window was created with a right angle and enlarged until the Endo-GIA linear stapler could be placed between the pancreas and splenic vein.After transection of the pancreas,starting from the cut end of the pancreas which was grasped and retracted anteriorly,the dissection was made continuously towards the tail until the pancreas was freed (Fig.4).Finally,the rinsed and aspirated operationalfield was carefully inspected for hemostasis (Fig.5).The whole specimen was placed in a bag and extracted through the enlarged trocar site on the left side or umbilicus.A rubber drainage tube was routinely placed in the pancreatic stump.

    Fig.1.Mobilizing the inferior border of the pancreas and revealing the splenic vessel.

    Fig.2.Firing the stapler to transect the pancreas.

    Fig.3.Bleeding control of the stump.

    Fig.4.Dissection continued towards the tail until the pancreas is totally freed.

    Fig.5.Inspection of proximal pancreatic stump for hemostasis.

    Pancreaticfistula

    The definition of pancreaticfistula was based on the criteria of Bassi et al,[11]as a the drain output of any measurable volume of fluid on or after the third postoperative day,with amylase content greater than three times the serum amylase activity.The grading system for pancreaticfistula was according to the definition by the International Study Group of Pancreatic Fistula (ISGPF),which considers grade A to be subclinical,whereas grades B and C are defined as clinical pancreaticfistula.

    Statistical analysis

    Statistical software package SPSS 13.0 (SPSS Inc.,Chicago,IL.,USA) was used for all analyses.Data were presented as mean±SD or median (range).Statistical analyses were performed by the independent-sample t test for continuous variables and the Chi-square test or Fisher's exact test (two-sided) where appropriate for categorical variables to reveal differences.P<0.05 was considered statistically significant.

    Results

    Altogether 46 patients (15 males and 31 females; aged 15-73 years,average 48±16) were identified.LDPS and LSPDP were performed successfully in 16 and 21 patients respectively,whereas both were converted to open surgery in 9 patients.The most common chief complaints were epigastric discomfort or pain,incidental findings during regular physical examinations,and recurrent headache,lethargy,and blurred vision inthe patients with insulinoma.All patients were found to have a mass in the body or tail of the pancreas by CT or endoscopic ultrasound and were preoperatively diagnosed as having benign or low-degree malignant tumors.

    Table 1.Cause of conversion to open surgery in 9 patients

    Table 2.Preoperative and intra-operative data for LDPS and LSPDP groups

    The mean tumor size was 3.4±1.9 cm (range 1.0-8.5),and the mean operation time was 272.2±72.3 minutes(range 90-430).Median blood loss was 331 mL (range 10-2300).Other laparoscopic procedures were combined in 7 patients:laparoscopic cholecystectomy (4 patients),hepatic nodule biopsy (2),and liver cyst fenestration (1).The causes of conversion in 9 patients are listed in Table 1.Dense adhesions and intra-operative bleeding were the major reasons to abandon laparoscopic surgery in this series.The total conversion rate was 19.6%.

    In the LDPS and LSPDP groups for whom the procedures werefinally performed successfully,there were no significant differences in average age,average operation time,average blood loss,gender and conversion rate,but the mean tumor size was greater in the LDPS than in the LSPDP group (Table 2).

    Pancreaticfistula was the most frequent postoperative complication.Based on the ISGPF definition,clinical pancreaticfistula developed in 2 patients in the LDPSgroup and 4 in the LSPDP group.Other complications included postoperative bleeding in the LDPS group and abdominal fluid collection,abdominal infection and pulmonary infection in the LSPDP group.The differences in all these complications and total morbidity rate between the two groups were not significant.Moreover,there were no splenic infarction or mortality (Table 3).

    Table 3.Postoperative complications in LDPS and LSPDP groups

    Table 4.Final diagnosis of LDPS and LSPDP by pathologic examination

    All the patients were diagnosed pathologically and were confirmed to have an R0 resection (Table 4).Benign tumors and low-degree malignant tumors were identified in 22 and 13 patients respectively,whereas 2 patients who had undergone LDPS were confirmed to have malignant neuroendocrine carcinomas.Follow-up for a median of 35 months showed that all the patients were alive without recurrence,and the symptoms of hypoglycemia in patients with insulinoma disappeared.

    Discussion

    In 1994 Soper et al[12]first performed laparoscopic distal pancreatectomy in a pig model to document its safety and feasibility.Since then,accumulating case reports or small series have appeared reported.Until 2009,more than 800 patients have received laparoscopic distal pancreatectomies worldwide.[4]In the past,surgeons preferred to remove the spleen simultaneously since the intimate relationship between splenic vessels and the pancreas made separation difficult.In recent years,however,the immunological role of the spleen has been increasingly emphasized and many adverse consequences have been reported after splenectomy.More importantly,in patients with benign and lowdegree malignant tumors,a long-term survival is expected and the quality of life needs to be considered.Therefore,spleen-preservation is desirable.

    There are many clinical trials and series reports which compare open distal pancreatectomy with or without spleen-preservation.Most studies[7-9]documented a remarkable decrease in postoperative infection and complications in spleen-preservation groups over splenectomy groups,whereas others had contradictory findings.[10,13]To our knowledge,few reports concentrated on such comparisons of laparoscopic procedures.At our hospital we have performed laparoscopic distal pancreatectomy and tumor enucleation since 2002.When the tumor size was <5 cm and presented as benign,LSPDP was recommended.Otherwise,an en bloc distal pancreatectomy along with splenectomy was considered.In this series,there was no significant difference in age and gender between the LDPS and LSPDP groups.In the LSPDP group,the tumor size,the operation time and blood loss were less than those in the LDPS group.Selection bias may be one of the major causes of this finding since the indications for the two procedures are different.In the early stage of LSPDP,surgeons inevitably prefer to choose relatively simple cases.

    The indications for laparoscopic surgery of the pancreas are generally benign or low-degree malignant tumors by preoperative identification and chronic pancreatitis with symptoms.As reported,malignant cases are all limited to unexpected postoperative pathologic diagnosis.In this situation,whether a second operation should be undertaken remains controversial.In our series,all the patients were subjected to examinations including CT and endoscopic ultrasound,and were all diagnosed as having benign or low-degree malignant tumors preoperatively.However,two patients who underwent LDPS were confirmed pathologically as having neuroendocrine carcinoma.Since this kind of tumor has a much better prognosis than ductal adenocarcinoma and both patients had negative resection margins,further surgical procedures were not necessary.Follow-up for 14 and 21 months revealed no evidence of tumor relapse in these two patients.

    The two methods for spleen-preservation have been described.The first is to preserve the splenic artery and vein by separating the pancreas and splenic vessels near the splenic pedicle.The alternative technique was described by Warshaw in 1988.[14]The main splenic vessels are divided at the pancreatic neck and near the splenic pedicle,and the distal pancreas associated with the splenic vessels is transected,leaving the short gastric vessels and the left gastroepiploic vessels to feed the spleen.Many authors reported serious complications when using Warshaw's technique,such as entire splenic necrosis or abscess which needed re-operation for splenectomy.[15-18]We performed 6 spleen-preserving distal pancreatectomies with splenic vessel ligations due to bleeding of splenic vessels or difficulty in separating a tumor from vessels.We reserved at least half of the short gastric artery to feed the spleen.Fortunately,no splenic infarctions or abscesses developed after operation.

    Bleeding,obesity,dense adhesions and the presence of malignancy are reported to be the major causes of conversions.[4,19,20]In our study,9 patients did not complete laparoscopic procedure.The causes of conversions were oncological or technical.Dense adhesion was the major cause for conversion to an open surgery in 3 of the 9 patients.Sometimes,adhesions between tumor and adjacent tissues or vessels make separation extremely difficult,and dense adhesions between the mass and the posterior stomach or colon may suggest a malignant disease.Therefore,under this condition,conversion to open surgery is unavoidable.Intra-operative bleeding is the second cause of conversion,especially in spleenpreservation.In our series,two patients suffered from this intra-operative complication because of injury of branches of the splenic vessels.Hence,the following points for prevention of bleeding should be emphasized.First,the operative method should be chosen cautiously on the basis of preoperative radiologic examinations.The splenic vessels are more likely to be spared when a thin fat plane can be seen between the vessels and the pancreas.Second,during LSPDP,we preferred to use the suction apparatus as a blunt dissection instrument to separate the pancreas and splenic vessels.Accompanied by aspiration,this can afford a clear view at the anatomical level.Third,generally a thin loose connective tissue occurs between the pancreas and splenic vessels,and dissection along this level can minimize intraoperative bleeding.

    Comparison of postoperative complications revealed no significant differences between the two groups in our series.Pancreaticfistula was still the most common complication.The texture of the pancreas and the management of pancreatic stump have proven to be key risk factors for pancreaticfistula.Hilal et al[20]reported that suturing the pancreatic remnant with PDS 3.0 interrupted stitches rather than a staple line gave an encouraging result,reducing afistula rate from 50% to 9%.We often used the Endo-GIA with 3.5-mm staples to close the primary stump of the pancreas.If its texture was hard and thick,we preferred to suture the stump.The total pancreaticfistula rate was 37.8%,and most pancreaticfistulas were cured by drainage,only 2 patients in the LDPS group and 4 in the LSPDP group developed grade B and Cfistulas,which needed fasting or antibiotics to control the infection.

    Our results showed that LSPDP is a feasible,safe and efficient technique.Spleen-preservation should be done for patients with benign or low-degree malignant tumors in the distal pancreas.The Warshaw's technique of spleen preservation is safe when dissection between the splenic vessels and distal pancreas is hard to achieve.

    Contributors:ZYP proposed the study.DX and CL wrote the first draft.GJC and CG collected and analyzed the data.DMH and LQ contributed to the interpretation of the study and to further drafts.ZTP reviewed the manuscript for intellectual content.ZYP is the guarantor.

    Funding:None.

    Ethical approval:Not needed.

    Competing interest:No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

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    2 Karaliotas C,Sgourakis G.Laparoscopic versus open enucleation for solitary insulinoma in the body and tail of the pancreas.J Gastrointest Surg 2009;13:1869.

    3 Melotti G,Butturini G,Piccoli M,Casetti L,Bassi C,Mullineris B,et al.Laparoscopic distal pancreatectomy:results on a consecutive series of 58 patients.Ann Surg 2007;246:77-82.

    4 Borja-Cacho D,Al-Refaie WB,Vickers SM,Tuttle TM,Jensen EH.Laparoscopic distal pancreatectomy.J Am Coll Surg 2009;209:758-765.

    5 Teh SH,Tseng D,Sheppard BC.Laparoscopic and open distal pancreatic resection for benign pancreatic disease.J Gastrointest Surg 2007;11:1120-1125.

    6 Mabrut JY,Fernandez-Cruz L,Azagra JS,Bassi C,Delvaux G,Weerts J,et al.Laparoscopic pancreatic resection:results of a multicenter European study of 127 patients.Surgery 2005;137:597-605.

    7 Shoup M,Brennan MF,McWhite K,Leung DH,Klimstra D,Conlon KC.The value of splenic preservation with distal pancreatectomy.Arch Surg 2002;137:164-168.

    8 Dulucq JL,Wintringer P,Stabilini C,Feryn T,Perissat J,Mahajna A.Are major laparoscopic pancreatic resections worthwhile? A prospective study of 32 patients in a single institution.Surg Endosc 2005;19:1028-1034.

    9 Carrère N,Abid S,Julio CH,Bloom E,Pradère B.Spleenpreserving distal pancreatectomy with excision of splenic artery and vein:a case-matched comparison with conventional distal pancreatectomy with splenectomy.World J Surg 2007;31:375-382.

    10 Rodríguez JR,Madanat MG,Healy BC,Thayer SP,Warshaw AL,Fernández-del Castillo C.Distal pancreatectomy with splenic preservation revisited.Surgery 2007;141:619-625.

    11 Bassi C,Dervenis C,Butturini G,Fingerhut A,Yeo C,Izbicki J,et al.Postoperative pancreaticfistula:an international study group (ISGPF) definition.Surgery 2005;138:8-13.

    12 Soper NJ,Brunt LM,Dunnegan DL,Meininger TA.Laparoscopic distal pancreatectomy in the porcine model.Surg Endosc 1994;8:57-61.

    13 Holdsworth RJ,Irving AD,Cuschieri A.Postsplenectomy sepsis and its mortality rate:actual versus perceived risks.Br J Surg 1991;78:1031-1038.

    14 Warshaw AL.Conservation of the spleen with distal pancreatectomy.Arch Surg 1988;123:550-553.

    15 Vezakis A,Davides D,Larvin M,McMahon MJ.Laparoscopic surgery combined with preservation of the spleen for distal pancreatic tumors.Surg Endosc 1999;13:26-29.

    16 Shimizu S,Tanaka M,Konomi H,Tamura T,Mizumoto K,Yamaguchi K.Spleen-preserving laparoscopic distal pancreatectomy after division of the splenic vessels.J Laparoendosc Adv Surg Tech A 2004;14:173-177.

    17 Fernández-Cruz L,Martínez I,Gilabert R,Cesar-Borges G,Astudillo E,Navarro S.Laparoscopic distal pancreatectomy combined with preservation of the spleen for cystic neoplasms of the pancreas.J Gastrointest Surg 2004;8:493-501.

    18 Pryor A,Means JR,Pappas TN.Laparoscopic distal pancreatectomy with splenic preservation.Surg Endosc 2007;21:2326-2330.

    19 Tagaya N,Kasama K,Suzuki N,Taketsuka S,Horie K,Furihata M,et al.Laparoscopic resection of the pancreas and review of the literature.Surg Endosc 2003;17:201-206.

    20 Abu Hilal M,Jain G,Kasasbeh F,Zuccaro M,Elberm H.Laparoscopic distal pancreatectomy:critical analysis of preliminary experience from a tertiary referral centre.Surg Endosc 2009;23:2743-2747.

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