Abstract
This study evaluated the short- and long-term patency of preserved splenic vessels after laparoscopic spleen-preserving distal pancreatectomy (SPDP) with preservation of the splenic vessels.
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 assessed by abdominal computed tomography and classified into three grades according to the degree of stenosis.
Twenty-two patients were included. The preoperative patency of the splenic artery and vein was normal in 20 and 19 patients respectively. Normal patency of the splenic artery and vein was observed in 16 and five patients respectively within 1 month of surgery, and in 19 and nine patients 6 months or more after operation. Nine of ten patients with complete splenic vein occlusion developed a collateral circulation in the late postoperative phase. Splenic perfusion was well preserved in all patients.
Splenic vessel-preserving laparoscopic SPDP has the short-term benefit of good perfusion to the spleen. In the long term, there is a risk of left-sided portal hypertension if the splenic vein becomes occluded after surgery.
Introduction
Laparoscopic distal pancreatectomy is a reliable and safe operation for selected patients with benign and low-grade malignant lesions in the body and tail of the pancreas. It is associated with a shorter hospital stay and fewer postoperative complications than open distal pancreatectomy1–4.
Although laparoscopic distal pancreatectomy can be done with or without preservation of the spleen, laparoscopic spleen-preserving distal pancreatectomy (SPDP) is preferred to avoid the risk of postoperative infectious complications after splenectomy5–8. SPDP can be carried out either with preservation or division of the splenic vessels (Warshaw's method9). The spleen vessel-preserving method is more demanding because it requires meticulous dissection of the pancreas from the splenic vessels. The method with division of the splenic vessels is easier but carries a risk of spleen-related morbidity such as infarction and abscess owing to insufficient splenic blood supply9–11. To reduce this risk, efforts have been made to preserve adequate blood supply to the spleen. With the refinement of laparoscopic skills, laparoscopic SPDP can be performed safely with preservation of the splenic vessels11–15.
However, it is not clear whether the patency of the preserved splenic vessels is well maintained in the immediate and late postoperative phases after splenic vessel-preserving laparoscopic SPDP. In this retrospective study, the early and late patency of splenic vessels after splenic vessel-preserving laparoscopic SPDP was analysed and the clinical significance of this surgical procedure was evaluated.
Methods
All patients undergoing splenic vessel-preserving laparoscopic SPDP between June 2004 and August 2007 at the Department of Surgery, Seoul National University Bundang Hospital, were enrolled in this retrospective study. These patients were selected from a larger cohort undergoing laparoscopic distal pancreatectomy with or without preservation of the spleen and splenic vessels in the same period. Indications for laparoscopic distal pancreatectomy were tumours in the pancreatic body and tail that were presumed to be benign or low-grade malignancies according to preoperative radiological studies. Written informed consent was obtained from all patients before surgery.
The operative strategy for laparoscopic distal pancreatectomy was to preserve the spleen and splenic vessels, unless the tumour was very close to the splenic hilum, or malignancy was suspected from preoperative radiological studies or during the laparoscopic procedure. Postoperative patency of the splenic vessels and clinical outcome was studied in patients who had splenic vessel-preserving laparoscopic SPDP.
Splenic vessel-preserving laparoscopic spleen-preserving distal pancreatectomy
Under general anaesthesia, the patient was placed in a supine, 30° reverse Trendelenburg position with left side-up adjustment. After creation of a carbon dioxide pneumoperitoneum via a 10-mm infraumbilical port, three additional trocars (12- and 5–10-mm trocars for the surgeon, and a 5-mm trocar for the assistant) were inserted. The positions of the two operator working ports varied according to tumour location. If the anticipated pancreatic resection line was near the superior mesenteric–portal–splenic vein confluence, two trocars were placed in the right upper abdomen. If the anticipated pancreatic resection line was not close to the confluence, they were inserted in the epigastric area and the left upper abdomen. A 5-mm trocar for the assistant was inserted at the left anterior axillary line.
After trocar placement, the greater omentum was divided using ultrasonic shears (Harmonic scalpel®, Ethicon, Cincinnati, USA; Sonosurg®, Olympus, Tokyo, Japan) from the midline towards the spleen. With the stomach elevated, the retroperitoneum was opened along the inferior pancreatic border and further dissection was performed on the avascular plane posterior to the pancreas until the splenic vein and artery were identified. In the initial patients in this series, a retrograde pancreatectomy was performed in which pancreatic transection was the final step after the pancreas had been freed completely from the splenic vessels. Subsequently, an antegrade pancreatectomy was performed in which proximal pancreatic transection was done as an initial step, followed by dissection of the pancreas from the splenic vessels towards the spleen. Small branches of the splenic vessels encountered during dissection were divided using endoclips or ultrasonic shears. Pancreatic transection was achieved using one or 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 the thickness and texture of the pancreas. No additional sutures were placed on the pancreatic stump, but fibrin glue was applied. The surgical specimen was retrieved in a vinyl bag and extracted through a small incision created by extending a port-site incision. A Jackson–Pratt drain was placed near the pancreatic stump.
Computed tomography
All patients underwent computed tomography in the early (within 1 month) and late (after at least 6 months) postoperative periods. The examinations were performed using 16- or 64-detector row scanners (Brilliance; Philips Medical Systems, Cleveland, Ohio, USA). The CT protocol comprised early arterial and portal venous phase scans using bolus-tracking software to trigger scanning 15 s after the aortic enhancement had reached a threshold of 200 Hounsfield units. The portal venous phase scan was obtained 70 s after the injection of contrast material. Transverse images 2 mm thick were reconstructed at 1-mm intervals from the raw data of the scans.
Assessment of patency of the splenic vessels and perfusion of the spleen
The postoperative status of the splenic vessels and splenic perfusion were assessed by examining the abdominal CT images. Two radiologists specializing in the hepatopancreatobiliary system retrospectively reviewed the scans by working together in consensus. The scans were reviewed using an interactive sliding slab ray sum technique (AquariusNET; TeraRecon, San Mateo, California, USA) with a maximum slab thickness of 3 mm. This reviewing technique16 is available in many commercial CT workstations, and accurately depicts pathology in small tubular structures such as vessels17,18. To evaluate vascular patency, the radiologists used appropriate magnification, and changed the viewing plane such that it was parallel or perpendicular to the target segment of vessel being analysed. All postoperative CT images were compared with preoperative images to evaluate postoperative changes in vascular patency, and to determine whether the analysed vessel was native or a collateral that developed after surgery following occlusion of the original splenic artery or vein.
Patency of the splenic vessels was classified into three grades according to the degree of stenosis: intact (grade 0), partial occlusion or thrombosis (grade 1) and total occlusion or not identified (grade 2). Splenic perfusion was grouped into four grades on the basis of the percentage splenic infarction: intact (grade 0), less than 50 per cent infarction of total splenic volume (grade 1), 50 per cent or more infarction (grade 2) and 100 per cent infarction (grade 3).
Association between patency and clinical variables
To determine the clinical factors affecting patency of the splenic vessels, the association between splenic vessel patency and various clinical factors was analysed. Clinical factors included age, sex, body mass index (BMI), operating time, intraoperative blood loss, tumour size, length of resected pancreas and postoperative intra-abdominal complications, including pancreatic fistulas and intra-abdominal fluid collections. Postoperative complications were graded according to the modified Clavien system19. Pancreatic fistulas were defined according to the International Study Group on Pancreatic Fistula20 as output, via a drain placed at surgery or a percutaneous drain placed after operation, of any measurable volume of drained fluid on or after postoperative day 3, with an amylase content greater than three times the upper normal serum value.
Statistical analysis
Data are presented as median (range). Univariable analyses were performed to identify clinical risk factors for poor postoperative patency of the splenic vessels, following binary classification of vascular patency into intact (grade 0) and stenotic (grades 1–2). Categorical variables were compared using Fisher's exact test and continuous variables by 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 pancreatectomy, of whom ten also had splenectomy because of tumour proximity to the splenic hilum (five) and suspicion of malignancy (five). Preservation of the spleen and splenic vessels was attempted in 25 patients and the splenic vessels were preserved successfully in 22. The splenic vessels were sacrificed in the remaining three patients because of accidental injury during dissection; the splenic artery was injured in one patient, and both the splenic artery and vein in two patients.
The 22 patients who were enrolled in this study included six 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 laparoscopic SPDP were pancreatic tumour (21 patients) and partial pancreatic transection owing to trauma (one). The final pathological diagnoses of the tumours are detailed in Table 1. Two patients were reported to have carcinoma in situ on pathological analysis of the surgical specimen. The median size of the tumours was 4·0 (1·5–12·0) cm and the median length of resected pancreas was 10·0 (3·0–18·0) cm.
Postoperative pathological findings in the 21 patients with pancreatic tumours
| No. of patients | |
|---|---|
| Solid pseudopapillary neoplasm | 7 |
| Intraductal papillary mucinous neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Mucinous cystic neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Endocrine neoplasm | 4 |
| Serous cystadenoma | 1 |
| Lymphoepithelial cyst | 1 |
| No. of patients | |
|---|---|
| Solid pseudopapillary neoplasm | 7 |
| Intraductal papillary mucinous neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Mucinous cystic neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Endocrine neoplasm | 4 |
| Serous cystadenoma | 1 |
| Lymphoepithelial cyst | 1 |
Postoperative pathological findings in the 21 patients with pancreatic tumours
| No. of patients | |
|---|---|
| Solid pseudopapillary neoplasm | 7 |
| Intraductal papillary mucinous neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Mucinous cystic neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Endocrine neoplasm | 4 |
| Serous cystadenoma | 1 |
| Lymphoepithelial cyst | 1 |
| No. of patients | |
|---|---|
| Solid pseudopapillary neoplasm | 7 |
| Intraductal papillary mucinous neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Mucinous cystic neoplasm | 4 |
| Adenoma | 2 |
| Borderline | 1 |
| Carcinoma in situ | 1 |
| Endocrine neoplasm | 4 |
| Serous cystadenoma | 1 |
| Lymphoepithelial cyst | 1 |
Perioperative clinical outcome
Median operating time was 250 (70–325) min. Median estimated blood loss was 300 (200–1000) ml; intraoperative transfusion was required in one patient (4·5 per cent). There were no perioperative deaths. Eleven patients experienced 15 postoperative complications (Table 2). The only spleen-related complication was focal infarction, which occurred in four patients. Median postoperative hospital stay was 10 (5–44) days. One patient was discharged at 44 days after surgery owing to the requirement for repeated percutaneous drainage for a pancreatic fistula.
Postoperative complications
| No. of complications | Management | |
|---|---|---|
| Grade I | 11 | |
| Focal splenic infarction (< 10%) | 4 | Observation |
| Pancreatic fistula* | 5 | Observation |
| Intra-abdominal fluid collection | 2 | Observation |
| Grade IIIa | 4 | |
| Pancreatic fistula* | 2 | Drain reposition |
| Intra-abdominal fluid collection | 1 | Drain reposition |
| Pleural effusion | 1 | Sonographically guided aspiration |
| No. of complications | Management | |
|---|---|---|
| Grade I | 11 | |
| Focal splenic infarction (< 10%) | 4 | Observation |
| Pancreatic fistula* | 5 | Observation |
| Intra-abdominal fluid collection | 2 | Observation |
| Grade IIIa | 4 | |
| Pancreatic fistula* | 2 | Drain reposition |
| Intra-abdominal fluid collection | 1 | Drain reposition |
| Pleural effusion | 1 | Sonographically guided aspiration |
Grade I complication: any deviation from the normal postoperative course without the need for pharmacological treatment or surgical, endoscopic and radiological interventions; grade IIIa: surgical, endoscopic or radiological intervention required, not performed under general anaesthesia19.
Defined according to the International Study Group on Pancreatic Fistula20. Two complications occurred simultaneously in four patients: focal splenic infarction and intra-abdominal fluid collection (two patients), splenic infarction and pancreatic fistula (one), and pancreatic fistula and pleural effusion (one).
Postoperative complications
| No. of complications | Management | |
|---|---|---|
| Grade I | 11 | |
| Focal splenic infarction (< 10%) | 4 | Observation |
| Pancreatic fistula* | 5 | Observation |
| Intra-abdominal fluid collection | 2 | Observation |
| Grade IIIa | 4 | |
| Pancreatic fistula* | 2 | Drain reposition |
| Intra-abdominal fluid collection | 1 | Drain reposition |
| Pleural effusion | 1 | Sonographically guided aspiration |
| No. of complications | Management | |
|---|---|---|
| Grade I | 11 | |
| Focal splenic infarction (< 10%) | 4 | Observation |
| Pancreatic fistula* | 5 | Observation |
| Intra-abdominal fluid collection | 2 | Observation |
| Grade IIIa | 4 | |
| Pancreatic fistula* | 2 | Drain reposition |
| Intra-abdominal fluid collection | 1 | Drain reposition |
| Pleural effusion | 1 | Sonographically guided aspiration |
Grade I complication: any deviation from the normal postoperative course without the need for pharmacological treatment or surgical, endoscopic and radiological interventions; grade IIIa: surgical, endoscopic or radiological intervention required, not performed under general anaesthesia19.
Defined according to the International Study Group on Pancreatic Fistula20. Two complications occurred simultaneously in four patients: focal splenic infarction and intra-abdominal fluid collection (two patients), splenic infarction and pancreatic fistula (one), and pancreatic fistula and pleural effusion (one).
Patency of the splenic artery
The patency of the splenic artery, as assessed by preoperative CT, was classified as grade 0 in 20 patients and grade 1 in two. In the early postoperative phase patency was classified as grade 0 in 16 patients and grade 1 in six (Figs 1 and 2). Two patients with grade 1 patency before surgery improved to grade 0 in the early postoperative period. After a median follow-up of 15·0 (4·4–35·2) months from the initial postoperative scan, patency improved from grade 1 to grade 0 in three of six patients, and patency was preserved in all patients with grade 0 patency at the first scan (Fig. 2). Therefore, 19 of 22 patients showed normal patency of the splenic artery in the late postoperative period. No patient had grade 2 patency of the splenic artery after surgery.
Splenic artery patency. a Coronal volume rendering image showing an intact (grade 0) splenic artery (arrows). b Oblique axial maximum 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
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 and grade 2 in one (Fig. 3). In two patients with grade 1 patency before surgery, the splenic vein recovered to grade 0 patency, one within a month and the other by late follow-up after 6 months. One patient with grade 2 patency did not improve but developed extensive collaterals. The patency of the splenic vein in the early postoperative period was grade 0 in five of 22 patients, grade 1 in ten and grade 2 in seven (Fig. 4). Among ten patients with grade 1 patency in the early postoperative period, patency improved to grade 0 in four patients and deteriorated to grade 2 in three (Fig. 4). There was no change in patency from grade 0 or 2 early after operation. Nine of the 22 patients had normal patency of the splenic vein 6 months or more after surgery.
Splenic vein patency. a Oblique axial reformation image showing intact (grade 0) splenic vein (arrows). b Transverse computed tomography image showing stenotic (grade 1) splenic vein (arrows). Arrowheads indicate the perivascular cuffing, which probably corresponds 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, postoperative inflammation; S, focal infarction of the spleen
Changes in splenic vein patency over time
Risk factors for poor patency of the splenic vessels
In the early postoperative period, postoperative intra-abdominal complications, including pancreatic fistulas and intra-abdominal fluid collections, were identified as significant risk factors for poor patency of the splenic vein. None of the patients with grade 0 patency experienced any intra-abdominal complications, whereas ten of 17 with grade 1 or 2 patency had intra-abdominal complications (P = 0·040). Although patients with poor patency of the splenic vein in the early and late periods had greater intraoperative blood loss, this difference did not reach statistical significance (P = 0·101 and P = 0·082 respectively).
Collateral circulation
At late follow-up CT, collateral vessels of splenic venous flow were identified in nine of the ten patents who had total occlusion (grade 2) of the splenic vein. One of these patients had minor collateral vessels (short gastric vessels) associated with total occlusion of the splenic vein before surgery, which developed into gastric varices after operation. Collaterals were located in the short gastric vein (three), gastroepiploic vein (five), coronary vein (three), left adrenal vein (one) and retroperitoneal vein (two); four patients had at least two collaterals (Fig. 5). No patient had bleeding from the gastric varices and there was no splenomegaly or thrombocytopenia. No collateral vessels were observed in patients with grade 0 or 1 patency.
Collateral veins. a Coronal volume rendering image showing an engorged gastroepiploic vein (arrows). b Coronal reformation image showing varices (V) at the gastric wall (G). S, spleen; K, left kidney
Perfusion of the spleen
Grade 0 splenic perfusion was observed in 18 of 22 patients within a month of surgery and in 21 after 6 months. Four patients had focal splenic infarction affecting less than 10 per cent of splenic volume within a month of operation, which was asymptomatic and had disappeared in three patients by the late follow-up.
Discussion
This study has shown that the patency of the splenic vessels cannot always be preserved even after splenic vessel-preserving laparoscopic SPDP. In particular, the patency of the splenic vein was more often compromised than that of the splenic artery. Only nine of 22 patients showed normal patency of the splenic vein at least 6 months after surgery, whereas 19 patients had a fully patent splenic artery. Most previous studies on splenic vessel-preserving laparoscopic SPDP have focused on the feasibility and safety of the procedure, with results based on early postoperative outcome. Splenic blood supply has been investigated previously after splenic vessel-sacrificing laparoscopic SPDP21,22, but not in detail after the splenic vessel-preserving procedure.
Although the direct cause of vascular occlusion could not be determined in this study, there are several plausible explanations for the higher occlusion rate of the splenic vein compared with the splenic artery. First, dissection of the splenic vein from the pancreas is more demanding technically; the procedure requires more manipulation because the splenic vein is densely adherent to the pancreas, and small branches are encountered more frequently than with the splenic artery. Although not statistically significant, the greater intraoperative blood loss in patients with poor patency of the splenic vein after operation seems to support this concept. Second, the vein has fewer muscle and elastic fibres, and it transports blood under lower pressure and at a lower speed than the artery. These structural and functional properties may make the splenic vein more susceptible to thrombosis and inflammation23–26. In the present study, patients with poor vascular patency of the splenic vein experienced more postoperative intra-abdominal complications than patients with normal vascular patency in the month after operation. However, the effects of intra-abdominal complications on vessel patency were reversed in some patients in the late postoperative period.
Despite compromised patency of the preserved splenic vessels, splenic perfusion was well maintained in most patients. More than three-quarters of the patients had normal splenic perfusion and the remainder had asymptomatic splenic infarction affecting less than 10 per cent of the total volume. Sato and colleagues22 reported that the splenic blood supply decreased to half of its previous level after splenic vessel-sacrificing SPDP, although it had recovered to the preoperative level by 10 days after operation. Therefore, after splenic vessel-sacrificing SPDP, there is a risk of spleen-related complications such as splenic infarction and abscess until splenic perfusion normalizes.
The potential advantage of maintaining perfusion to the spleen in splenic vessel-preserving SPDP should be balanced against the possibility of splenic vein occlusion and the potential risk of left-sided portal hypertension27,28. In the present study, nine of ten patients with complete splenic vein occlusion developed a collateral circulation. However, none experienced gastrointestinal bleeding. In one patient, minor collateral vessels associated with total occlusion of the splenic vein before operation developed into gastric varices. Therefore, the preoperative patency of the splenic vessels should be evaluated carefully when selecting patients for splenic vessel-preserving laparoscopic SPDP. If total occlusion of the splenic vessels is evident, a splenic vessel-preserving procedure may not be indicated because total vascular occlusion may not recover even after resection and left-sided portal hypertension may ensue. Interestingly, disturbance of the splenogastric circulation has also been reported after splenic vessel-sacrificing SPDP, but reasons for the increased gastric venous flow that resulted in gastric varices were not clear29. To confirm the clinical significance of the venous collaterals and varices that develop after laparoscopic SPDP with or without preservation of the splenic vessels, further long-term follow-up and a comparative study between the two operative procedures are needed.
A possible limitation of the present study is the wide variation in follow-up, from 4·4 to 35·2 months. This was a consequence of the retrospective nature of this investigation. The results for vascular patency and formation of collaterals may vary depending on the duration of follow-up. However, although partial vascular occlusion may change over time, total vascular occlusion is less likely to improve, irrespective of the follow-up time. In this study, none of the ten patients with total vascular occlusion experienced improvement in splenic venous patency, and nine of them developed collaterals.
Splenic vessel-preserving laparoscopic SPDP has the short-term benefit of good perfusion to the spleen, but there is a risk of postoperative occlusion of the splenic vein and left-sided portal hypertension in the long term. Patency of the splenic vessels should be checked within a month of operation, and long-term follow-up is needed especially for those with poor splenic vein patency. A larger study is needed to confirm the clinical significance of the short- and long-term outcomes after this operation.
Acknowledgements
This study was supported by a grant from the Korea Healthcare Technology Research and Development Project, Ministry of Health and Welfare, Korea (A060299). The authors declare no conflict of interest.
