Patency of splenic vessels after laparoscopic spleen and splenic vessel-preserving distal pancreatectomy

Original article

Patency of splenic vessels after laparoscopic spleen andsplenic vessel-preserving distal pancreatectomy

Y.-S. Yoon1, K. H. Lee2, H.-S. Han1, J. Y. Cho1 and K. S. Ahn1

Departments of 1Surgery and 2Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 166 Gumi-ro,Bundang-gu, Seongnam-si, Gyeonggi-do, 463-707, KoreaCorrespondence to: Professor H.-S. Han (e-mail: [email protected])

Background: This study evaluated the short- and long-term patency of preserved splenic vessels afterlaparoscopic spleen-preserving distal pancreatectomy (SPDP) with preservation of the splenic vessels.Methods: This single-centre retrospective study included all patients who had undergone splenic vessel-preserving laparoscopic SPDP between 2004 and 2007. The patency of the splenic vessels was assessedby abdominal computed tomography and classified into three grades according to the degree of stenosis.Results: Twenty-two patients were included. The preoperative patency of the splenic artery and veinwas normal in 20 and 19 patients respectively. Normal patency of the splenic artery and vein was observedin 16 and five patients respectively within 1 month of surgery, and in 19 and nine patients 6 months ormore after operation. Nine of ten patients with complete splenic vein occlusion developed a collateralcirculation in the late postoperative phase. Splenic perfusion was well preserved in all patients.Conclusion: Splenic vessel-preserving laparoscopic SPDP has the short-term benefit of good perfusionto the spleen. In the long term, there is a risk of left-sided portal hypertension if the splenic vein becomesoccluded after surgery.

Paper accepted 11 February 2009Published online in Wiley InterScience (www.bjs.co.uk). DOI: 10.1002/bjs.6609

Introduction

Laparoscopic distal pancreatectomy is a reliable and safeoperation for selected patients with benign and low-grade malignant lesions in the body and tail of thepancreas. It is associated with a shorter hospital stayand fewer postoperative complications than open distalpancreatectomy1–4.

Although laparoscopic distal pancreatectomy can bedone with or without preservation of the spleen, laparo-scopic spleen-preserving distal pancreatectomy (SPDP) ispreferred to avoid the risk of postoperative infectious com-plications after splenectomy5–8. SPDP can be carried outeither with preservation or division of the splenic ves-sels (Warshaw’s method9). The spleen vessel-preservingmethod is more demanding because it requires meticu-lous dissection of the pancreas from the splenic vessels.The method with division of the splenic vessels is eas-ier but carries a risk of spleen-related morbidity such asinfarction and abscess owing to insufficient splenic bloodsupply9–11. To reduce this risk, efforts have been madeto preserve adequate blood supply to the spleen. With

the refinement of laparoscopic skills, laparoscopic SPDPcan be performed safely with preservation of the splenicvessels11–15.

However, it is not clear whether the patency ofthe preserved splenic vessels is well maintained in theimmediate and late postoperative phases after splenicvessel-preserving laparoscopic SPDP. In this retrospectivestudy, the early and late patency of splenic vessels aftersplenic vessel-preserving laparoscopic SPDP was analysedand the clinical significance of this surgical procedure wasevaluated.

Methods

All patients undergoing splenic vessel-preserving laparo-scopic SPDP between June 2004 and August 2007 atthe Department of Surgery, Seoul National UniversityBundang Hospital, were enrolled in this retrospectivestudy. These patients were selected from a larger cohortundergoing laparoscopic distal pancreatectomy with orwithout preservation of the spleen and splenic vessels in

Copyright 2009 British Journal of Surgery Society Ltd British Journal of Surgery 2009; 96: 633–640Published by John Wiley & Sons Ltd

634 Y.-S. Yoon, K. H. Lee, H.-S. Han, J. Y. Cho and K. S. Ahn

the same period. Indications for laparoscopic distal pancre-atectomy were tumours in the pancreatic body and tail thatwere presumed to be benign or low-grade malignanciesaccording to preoperative radiological studies. Writteninformed consent was obtained from all patients beforesurgery.

The operative strategy for laparoscopic distal pancre-atectomy was to preserve the spleen and splenic vessels,unless the tumour was very close to the splenic hilum, ormalignancy was suspected from preoperative radiologicalstudies or during the laparoscopic procedure. Postoper-ative patency of the splenic vessels and clinical outcomewas studied in patients who had splenic vessel-preservinglaparoscopic SPDP.

Splenic vessel-preserving laparoscopicspleen-preserving distal pancreatectomy

Under general anaesthesia, the patient was placed ina supine, 30° reverse Trendelenburg position with leftside-up adjustment. After creation of a carbon dioxidepneumoperitoneum via a 10-mm infraumbilical port,three additional trocars (12- and 5–10-mm trocars forthe surgeon, and a 5-mm trocar for the assistant) wereinserted. The positions of the two operator workingports varied according to tumour location. If theanticipated pancreatic resection line was near the superiormesenteric–portal–splenic vein confluence, two trocarswere placed in the right upper abdomen. If the anticipatedpancreatic resection line was not close to the confluence,they were inserted in the epigastric area and the left upperabdomen. A 5-mm trocar for the assistant was inserted atthe left anterior axillary line.

After trocar placement, the greater omentum was dividedusing ultrasonic shears (Harmonic scalpel, Ethicon,Cincinnati, USA; Sonosurg, Olympus, Tokyo, Japan)from the midline towards the spleen. With the stomachelevated, the retroperitoneum was opened along theinferior pancreatic border and further dissection wasperformed on the avascular plane posterior to the pancreasuntil the splenic vein and artery were identified. In theinitial patients in this series, a retrograde pancreatectomywas performed in which pancreatic transection was the finalstep after the pancreas had been freed completely from thesplenic vessels. Subsequently, an antegrade pancreatectomywas performed in which proximal pancreatic transectionwas done as an initial step, followed by dissection ofthe pancreas from the splenic vessels towards the spleen.Small branches of the splenic vessels encountered duringdissection were divided using endoclips or ultrasonicshears. Pancreatic transection was achieved using oneor two 45-mm Endo-GIA staplers (Tyco Healthcare,

Norwalk, Connecticut, USA). The type of cartridge (white,2·5 mm; blue, 3·5 mm) was selected according to thethickness and texture of the pancreas. No additional sutureswere placed on the pancreatic stump, but fibrin glue wasapplied. The surgical specimen was retrieved in a vinyl bagand extracted through a small incision created by extendinga port-site incision. A Jackson–Pratt drain was placed nearthe pancreatic stump.

Computed tomography

All patients underwent computed tomography in theearly (within 1 month) and late (after at least 6 months)postoperative periods. The examinations were performedusing 16- or 64-detector row scanners (Brilliance; PhilipsMedical Systems, Cleveland, Ohio, USA). The CTprotocol comprised early arterial and portal venous phasescans using bolus-tracking software to trigger scanning15 s after the aortic enhancement had reached a thresholdof 200 Hounsfield units. The portal venous phase scanwas obtained 70 s after the injection of contrast material.Transverse images 2 mm thick were reconstructed at 1-mmintervals from the raw data of the scans.

Assessment of patency of the splenic vessels andperfusion of the spleen

The postoperative status of the splenic vessels and splenicperfusion were assessed by examining the abdominalCT images. Two radiologists specializing in the hep-atopancreatobiliary system retrospectively reviewed thescans by working together in consensus. The scans werereviewed using an interactive sliding slab ray sum technique(AquariusNET; TeraRecon, San Mateo, California, USA)with a maximum slab thickness of 3 mm. This review-ing technique16 is available in many commercial CTworkstations, and accurately depicts pathology in smalltubular structures such as vessels17,18. To evaluate vascularpatency, the radiologists used appropriate magnification,and changed the viewing plane such that it was parallel orperpendicular to the target segment of vessel being anal-ysed. All postoperative CT images were compared withpreoperative images to evaluate postoperative changes invascular patency, and to determine whether the analysedvessel was native or a collateral that developed after surgeryfollowing occlusion of the original splenic artery or vein.

Patency of the splenic vessels was classified into threegrades according to the degree of stenosis: intact (grade0), partial occlusion or thrombosis (grade 1) and totalocclusion or not identified (grade 2). Splenic perfusion wasgrouped into four grades on the basis of the percentagesplenic infarction: intact (grade 0), less than 50 per cent

Copyright 2009 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2009; 96: 633–640Published by John Wiley & Sons Ltd

Laparoscopic spleen and splenic vessel-preserving distal pancreatectomy 635

infarction of total splenic volume (grade 1), 50 per centor more infarction (grade 2) and 100 per cent infarction(grade 3).

Association between patency and clinical variables

To determine the clinical factors affecting patency ofthe splenic vessels, the association between splenic vesselpatency and various clinical factors was analysed. Clinicalfactors included age, sex, body mass index (BMI), oper-ating time, intraoperative blood loss, tumour size, lengthof resected pancreas and postoperative intra-abdominalcomplications, including pancreatic fistulas and intra-abdominal fluid collections. Postoperative complicationswere graded according to the modified Clavien system19.Pancreatic fistulas were defined according to the Interna-tional Study Group on Pancreatic Fistula20 as output, viaa drain placed at surgery or a percutaneous drain placedafter operation, of any measurable volume of drained fluidon or after postoperative day 3, with an amylase con-tent greater than three times the upper normal serumvalue.

Statistical analysis

Data are presented as median (range). Univariable analyseswere performed to identify clinical risk factors for poorpostoperative patency of the splenic vessels, followingbinary classification of vascular patency into intact (grade0) and stenotic (grades 1–2). Categorical variables werecompared using Fisher’s exact test and continuous variablesby means of the non-parametric Mann–Whitney U test.P < 0·050 was considered statistically significant. SPSS

version 15.0 for Windows (SPSS, Chicago, Illinois, USA)was used for all analyses.

Results

Thirty-five patients underwent laparoscopic distal pancre-atectomy, of whom ten also had splenectomy because oftumour proximity to the splenic hilum (five) and suspicionof malignancy (five). Preservation of the spleen and splenicvessels was attempted in 25 patients and the splenic ves-sels were preserved successfully in 22. The splenic vesselswere sacrificed in the remaining three patients because ofaccidental injury during dissection; the splenic artery wasinjured in one patient, and both the splenic artery and veinin two patients.

The 22 patients who were enrolled in this study includedsix men and 16 women, with a median age of 41 (10–79)years and BMI 21·6 (18·4–25·2) kg/m2. Nine patients

had at least one underlying disease (hypertension in five,diabetes mellitus in four and chronic hepatitis B in one).The indications for splenic vessel-preserving laparoscopicSPDP were pancreatic tumour (21 patients) and partialpancreatic transection owing to trauma (one). The finalpathological diagnoses of the tumours are detailed inTable 1. Two patients were reported to have carcinomain situ on pathological analysis of the surgical specimen.The median size of the tumours was 4·0 (1·5–12·0) cmand the median length of resected pancreas was 10·0(3·0–18·0) cm.

Perioperative clinical outcome

Median operating time was 250 (70–325) min. Medianestimated blood loss was 300 (200–1000) ml; intraoperativetransfusion was required in one patient (4·5 per cent).There were no perioperative deaths. Eleven patientsexperienced 15 postoperative complications (Table 2). Theonly spleen-related complication was focal infarction,which occurred in four patients. Median postoperativehospital stay was 10 (5–44) days. One patient wasdischarged at 44 days after surgery owing to therequirement for repeated percutaneous drainage for apancreatic fistula.

Patency of the splenic artery

The patency of the splenic artery, as assessed bypreoperative CT, was classified as grade 0 in 20 patients andgrade 1 in two. In the early postoperative phase patency wasclassified as grade 0 in 16 patients and grade 1 in six (Figs 1and 2). Two patients with grade 1 patency before surgeryimproved to grade 0 in the early postoperative period. Aftera median follow-up of 15·0 (4·4–35·2) months from theinitial postoperative scan, patency improved from grade 1

Table 1 Postoperative pathological findings in the 21 patientswith pancreatic tumours

No. of patients

Solid pseudopapillary neoplasm 7Intraductal papillary mucinous neoplasm 4

Adenoma 2Borderline 1Carcinoma in situ 1

Mucinous cystic neoplasm 4Adenoma 2Borderline 1Carcinoma in situ 1

Endocrine neoplasm 4Serous cystadenoma 1Lymphoepithelial cyst 1



Table 2 Postoperative complications

No. ofcomplications Management

Grade I 11Focal splenic infarction (< 10%) 4 ObservationPancreatic fistula* 5 ObservationIntra-abdominal fluid collection 2 Observation

Grade IIIa 4Pancreatic fistula* 2 Drain repositionIntra-abdominal fluid collection 1 Drain repositionPleural effusion 1 Sonographically

guidedaspiration

Grade I complication: any deviation from the normal postoperativecourse without the need for pharmacological treatment or surgical,endoscopic and radiological interventions; grade IIIa: surgical,endoscopic or radiological intervention required, not performed undergeneral anaesthesia19. *Defined according to the International StudyGroup on Pancreatic Fistula20. Two complications occurredsimultaneously in four patients: focal splenic infarction andintra-abdominal fluid collection (two patients), splenic infarction andpancreatic fistula (one), and pancreatic fistula and pleural effusion (one).

to grade 0 in three of six patients, and patency was preservedin all patients with grade 0 patency at the first scan (Fig. 2).Therefore, 19 of 22 patients showed normal patency ofthe splenic artery in the late postoperative period. Nopatient had grade 2 patency of the splenic artery aftersurgery.

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Preoperative Early postoperative Late postoperative

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Fig. 2 Changes in splenic artery patency over time

Patency of the splenic vein

The splenic vein was completely patent before surgery(grade 0) in 19 patients, grade 1 in two patients andgrade 2 in one (Fig. 3). In two patients with grade 1patency before surgery, the splenic vein recovered to grade0 patency, one within a month and the other by late follow-up after 6 months. One patient with grade 2 patency did notimprove but developed extensive collaterals. The patencyof the splenic vein in the early postoperative period wasgrade 0 in five of 22 patients, grade 1 in ten and grade 2 inseven (Fig. 4). Among ten patients with grade 1 patency inthe early postoperative period, patency improved to grade0 in four patients and deteriorated to grade 2 in three(Fig. 4). There was no change in patency from grade 0 or2 early after operation. Nine of the 22 patients had normalpatency of the splenic vein 6 months or more after surgery.

a Grade 0 patency b Grade 1 patency

Fig. 1 Splenic artery patency. a Coronal volume rendering image showing an intact (grade 0) splenic artery (arrows). b Oblique axialmaximum intensity projection image showing that the proximal segment of the splenic artery (black arrow) is stenotic (grade 1),compared with the distal segment (white arrow). Arrowhead indicates the splenic vein overlapped in the image. S, spleen; K, left kidney



a Grade 0 patency b Grade 1 patency

c Grade 2 patency

Fig. 3 Splenic vein patency. a Oblique axial reformation image showing intact (grade 0) splenic vein (arrows). b Transverse computedtomography image showing stenotic (grade 1) splenic vein (arrows). Arrowheads indicate the perivascular cuffing, which probablycorresponds to a thickened venous wall or perivascular inflammation. c Oblique axial reformation image showing thrombosis (grade 2)of the splenic vein (arrows). Arrowhead indicates the intact segment of the splenic vein. P, remnant pancreas; I, postoperativeinflammation; S, focal infarction of the spleen

Risk factors for poor patency of the splenic vessels

In the early postoperative period, postoperative intra-abdominal complications, including pancreatic fistulas andintra-abdominal fluid collections, were identified as sig-nificant risk factors for poor patency of the splenic vein.None of the patients with grade 0 patency experiencedany intra-abdominal complications, whereas ten of 17 withgrade 1 or 2 patency had intra-abdominal complications

(P = 0·040). Although patients with poor patency of thesplenic vein in the early and late periods had greater intra-operative blood loss, this difference did not reach statisticalsignificance (P = 0·101 and P = 0·082 respectively).

Collateral circulation

At late follow-up CT, collateral vessels of splenic venousflow were identified in nine of the ten patents who had



total occlusion (grade 2) of the splenic vein. One ofthese patients had minor collateral vessels (short gastricvessels) associated with total occlusion of the splenic veinbefore surgery, which developed into gastric varices afteroperation. Collaterals were located in the short gastric vein(three), gastroepiploic vein (five), coronary vein (three),left adrenal vein (one) and retroperitoneal vein (two); fourpatients had at least two collaterals (Fig. 5). No patienthad bleeding from the gastric varices and there was nosplenomegaly or thrombocytopenia. No collateral vesselswere observed in patients with grade 0 or 1 patency.

Perfusion of the spleen

Grade 0 splenic perfusion was observed in 18 of 22 patientswithin a month of surgery and in 21 after 6 months. Fourpatients had focal splenic infarction affecting less than10 per cent of splenic volume within a month of operation,which was asymptomatic and had disappeared in threepatients by the late follow-up.

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Preoperative Early postoperative Late postoperative

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Fig. 4 Changes in splenic vein patency over time

Discussion

This study has shown that the patency of the splenicvessels cannot always be preserved even after splenicvessel-preserving laparoscopic SPDP. In particular, thepatency of the splenic vein was more often compromisedthan that of the splenic artery. Only nine of 22 patientsshowed normal patency of the splenic vein at least6 months after surgery, whereas 19 patients had a fullypatent splenic artery. Most previous studies on splenicvessel-preserving laparoscopic SPDP have focused on thefeasibility and safety of the procedure, with results basedon early postoperative outcome. Splenic blood supply hasbeen investigated previously after splenic vessel-sacrificinglaparoscopic SPDP21,22, but not in detail after the splenicvessel-preserving procedure.

Although the direct cause of vascular occlusion couldnot be determined in this study, there are several plausibleexplanations for the higher occlusion rate of the splenicvein compared with the splenic artery. First, dissection ofthe splenic vein from the pancreas is more demandingtechnically; the procedure requires more manipulationbecause the splenic vein is densely adherent to the pancreas,and small branches are encountered more frequentlythan with the splenic artery. Although not statisticallysignificant, the greater intraoperative blood loss in patientswith poor patency of the splenic vein after operationseems to support this concept. Second, the vein hasfewer muscle and elastic fibres, and it transports bloodunder lower pressure and at a lower speed than theartery. These structural and functional properties may

b Gastric varicesa Engorged gastroepiploic vein

Fig. 5 Collateral veins. a Coronal volume rendering image showing an engorged gastroepiploic vein (arrows). b Coronal reformationimage showing varices (V) at the gastric wall (G). S, spleen; K, left kidney



make the splenic vein more susceptible to thrombosisand inflammation23–26. In the present study, patients withpoor vascular patency of the splenic vein experienced morepostoperative intra-abdominal complications than patientswith normal vascular patency in the month after operation.However, the effects of intra-abdominal complications onvessel patency were reversed in some patients in the latepostoperative period.

Despite compromised patency of the preserved splenicvessels, splenic perfusion was well maintained in mostpatients. More than three-quarters of the patients had nor-mal splenic perfusion and the remainder had asymptomaticsplenic infarction affecting less than 10 per cent of the totalvolume. Sato and colleagues22 reported that the splenicblood supply decreased to half of its previous level aftersplenic vessel-sacrificing SPDP, although it had recoveredto the preoperative level by 10 days after operation. There-fore, after splenic vessel-sacrificing SPDP, there is a risk ofspleen-related complications such as splenic infarction andabscess until splenic perfusion normalizes.

The potential advantage of maintaining perfusion tothe spleen in splenic vessel-preserving SPDP should bebalanced against the possibility of splenic vein occlusionand the potential risk of left-sided portal hypertension27,28.In the present study, nine of ten patients with completesplenic vein occlusion developed a collateral circulation.However, none experienced gastrointestinal bleeding. Inone patient, minor collateral vessels associated with totalocclusion of the splenic vein before operation developedinto gastric varices. Therefore, the preoperative patencyof the splenic vessels should be evaluated carefully whenselecting patients for splenic vessel-preserving laparoscopicSPDP. If total occlusion of the splenic vessels is evident, asplenic vessel-preserving procedure may not be indicatedbecause total vascular occlusion may not recover even afterresection and left-sided portal hypertension may ensue.Interestingly, disturbance of the splenogastric circulationhas also been reported after splenic vessel-sacrificingSPDP, but reasons for the increased gastric venous flowthat resulted in gastric varices were not clear29. Toconfirm the clinical significance of the venous collateralsand varices that develop after laparoscopic SPDP with orwithout preservation of the splenic vessels, further long-term follow-up and a comparative study between the twooperative procedures are needed.

A possible limitation of the present study is thewide variation in follow-up, from 4·4 to 35·2 months.This was a consequence of the retrospective nature ofthis investigation. The results for vascular patency andformation of collaterals may vary depending on theduration of follow-up. However, although partial vascular

occlusion may change over time, total vascular occlusionis less likely to improve, irrespective of the follow-uptime. In this study, none of the ten patients with totalvascular occlusion experienced improvement in splenicvenous patency, and nine of them developed collaterals.

Splenic vessel-preserving laparoscopic SPDP has theshort-term benefit of good perfusion to the spleen, butthere is a risk of postoperative occlusion of the splenicvein and left-sided portal hypertension in the long term.Patency of the splenic vessels should be checked withina month of operation, and long-term follow-up is neededespecially for those with poor splenic vein patency. A largerstudy is needed to confirm the clinical significance of theshort- and long-term outcomes after this operation.

Acknowledgements

This study was supported by a grant from the KoreaHealthcare Technology Research and DevelopmentProject, Ministry of Health and Welfare, Korea (A060299).The authors declare no conflict of interest.

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Patency of splenic vessels after laparoscopic spleen and splenic vessel-preserving distal pancreatectomy