Importance of the vessel distribution at splenic hilum for laparoscopic Warshaw procedure

INTRODUCTION

Laparoscopic spleen-preserving distal pancreatectomy (LSPDP) is widely used for the treatment of benign and/or low-grade malignant tumors in the pancreatic body and tail. A major advantage with preservation of the spleen is maintaining immunity against bacteria and neoplasms. Shoup et al reported that the incidence of infectious complications in DP with splenectomy was 28%, whereas the incidence of complications in splenic preservation was only 9%.¹ However, weak points of spleen preservation include the insufficiency of lymph node dissection and the difficulty of the surgical techniques.

There are two surgical methods that enable preservation of the spleen. One involves preserving the splenic artery and vein, which was reported by Kimura et al.² The other involves cutting the splenic artery and splenic vein and is known as the Warshaw procedure.³ Laparoscopic DP is associated with a reduction in the morbidity rate and hospital stay compared to conventional surgery.⁴ Because of the simplicity of the procedure, LWP has an advantage in reducing the operation time and blood loss compared to LSPDP with splenic vessels preserving.⁵ However, LWP has risks of splenic infarction and gastric varices formation due to left-sided portal hypertension.^6-9 Therefore, it is important to preserve the splenic hilum vascular arcade as well as the left gastroepiploic vessels and short gastric vessels. However, the relationship between the splenic hilum vessel distribution and splenic infarction or varices formation in LWP has not been described.

In the present study, we describe the influence of splenic vessels distribution on splenic infarction, according to the classification by Michels, the distribution of splenic vessels as distributed type (vessels spread to splenic hilum like fan shape) and magistral type (vessels spread to splenic hilum narrowly) at the splenic hilum.¹⁰

CASE SERIES

From February 2007 to February 2017, a total of 19 patients underwent LWT for benign or low-grade malignant lesions in the pancreatic body and tail at our institution. This study was reviewed and approved by the Ethics Committee of the Nagasaki University Hospital. The characteristics of the patients are described in Table 1. The average tumor size was 5 cm, and 78% (14/18) of pathological diagnoses were pancreatic cystic disease.

We retrospectively analyzed the operative and long-term outcomes. We also examined the relationship between the type of splenic hilum vessel distribution and the splenic vessel number and presence of splenic infarction. The distribution of the splenic hilum vessels was evaluated using contrast enhancement computed tomography (CE-CT) with the SYNAPSE VINCENT software program (Fujifilm, Tokyo) and classified into distributed type (vessels spread to the splenic hilum in a fan shape) and magistral type (vessels spread to the splenic hilum narrowly) at the splenic hilum (Figure 1). The number of splenic vessels was counted on CE-CT (Figure 2). Patients were followed up for their laboratory data and CE-CT findings within 3 months, 6 months and 1 year after the operation, and every year thereafter.

The operative and long-term outcomes were described as median values. Clinical outcomes were statically analyzed using Fisher's exact test and Mann-Whitney U tests with the IBM Statistical package of social sciences (SPSS) Statistics 21 software program (SPSS Inc., Chicago, IL).

Surgical procedure

In the LWP procedure, after induction of general anesthesia, patients were placed in the supine position. After obtaining pneumoperitoneum, the lessor sac was opened using the laparoscopic LigasureTM Vessel Sealing System (Covidien, Mansfield, MA, USA). During dissection of lessor sac, the left gastroepiploic vessels and short gastric vessels were needed to preserve for maintaining the blood flow to the spleen. The important part of LWP is obtaining a favorable laparoscopic view, so we used two threads to lift the stomach. After achieving the appropriate view, the tumor location was confirmed by laparoscopic ultrasonography, and the resection line of the pancreas was determined. The splenic artery was divided from the pancreas, and the pancreas was tunneled into using the Endo RetractTM Maxi (Covidien). A 4-Fr nylon tube was useful for encircling and hanging the pancreas. During vessels transection, a 4-Fr nylon tube was effective for securing the stapler insertion and ensuring an appropriate field of view. After mobilizing the pancreas from the retroperitoneum, we confirmed the end of the pancreatic tail and made sure to preserve the furcation point of the splenic artery and splenic hilum vascular arcade as well as the left gastroepiploic vessels and short gastric vessels (Figure 3). Finally, we checked the color of the spleen and confirmed the blood flow using laparoscopic ultrasonography.

RESULTS

The operative and long-term outcomes are described in Table 2, and the median follow-up duration was 71 (range 16-132) months.

The median operative time, blood loss and hospital stay were 295 min (201-512), 200 gr (5-3250) and 16 (8-29) days. There were no grade B or C pancreatic fistulae. All patients’ platelet counts turned to normal within one month. Six patients (32%) with splenic partial infarction and 3 (16%) with gastric varices were detected, but they have not needed any treatments. Regarding the classification of splenic hilum vessels distribution, 16 out of 19 cases were distributed type, and 6 were magistral type.

Three of 16 distributed type patients (23%) developed splenic infarction. In contrast, all of the magistral type patients (100%) showed splenic infarction. The incidence of splenic infarction was significantly higher among the magistral type patients than in the distributed type patients (p<0.01). The rate of splenic infarction area was 10%, 25% and 40% in the distributed type patients and 25%, 40% and 60% in the magistral type patients (Table 3). The number of vessels in the splenic hilum was significantly lower in the patients who developed splenic infarction. However, the condition of all six of the patients with splenic infarction improved spontaneously without any treatment. The type of splenic hilum vessel distribution in the three perigastric varices cases was distributed type. Perigastric varices formation was not related to the type of splenic hilum vessel distribution. In the three perigastric varices cases, there were no gastric submucosal changes on endoscopic findings. None of these cases have needed any treatments.

DISCUSSION

LSPDP is widely used in the pancreatic surgery field. The advantages of preserving the spleen are well known; preservation reduces the risk of infection, including overwhelming post-splenectomy infection and the incidence of cancer.^2,11-13 Furthermore, distal pancreatectomy with splenectomy was associated with an increased risk of grade B or C pancreatic fistula.^14,15 Furthermore, the enlarged visual effect of laparoscopic surgery is a feasible way of confirming the small vessels from front and back, thereby helping to prevent small-vessel injury.

For the above reasons, LSPDP is the first choice for treating benign and low-grade malignant tumor in our institution. The LWP has been considered useful for reducing blood loss and operation times compared to LSPDP with SVP because of the simplicity of the procedure.¹⁶ However, due to advances in laparoscopic techniques, recent reports have failed to note any marked difference in the outcomes between the LWP and LSPDP with SVP.^17-19 LSPDP is safe and efficient from the viewpoint of preserving the spleen in both LWT and LSPDP with SVP. For these reasons, for tumors close to splenic vessels and/or in cases of difficult dissection from splenic vessels, we select the LWP.

A recent meta-analysis noted no significant difference between the LWP and LSPDP with SVP in the overall rate of postoperative complications, including perigastric collateral vessels.^20,21 However, Miura et al and Tien et al showed a high risk of perigastric varices formation detected on CT (70% and 29.7%, respectively) after an open Warshaw technique. In our series, only 3 patients (16%) developed perigastric varices.^6,7 In two of these three cases, the distance between the tumor and splenic hilum was within 5 mm. Because the distance between the tumor and the splenic hilum was relatively small, the cutting line was close to the splenic hilum, resulting in perfusion injury and perigastric varices formation. There was an increase of one patient from our past report in 2014, and this patient has subsequently been routinely followed up, with CT and endoscopic examinations performed; however, there have been no gastric submucosal changes on endoscopic findings, and the patient hasn’t needed any treatments.²² The differences in the varices formation rates between the present and previous reports are considered to be due to differences between laparoscopic and laparotomy, with the enlarged visual effect of laparoscopic surgery making it possible to preserve the vascular arcade of the splenic hilum more reliably.

In addition to perigastric varices formation, splenic infarction frequently occurred after the Warshaw technique. Kim et al and we 22 have reported that asymptomatic splenic infarction occurred in 54.2% (66/122) and 24% (4/17) of patients who underwent LWP, respectively, but recovered within 3 and 6 months after operation, provided the splenic hilum vessels were sufficiently preserved.¹⁷ In contrast, Ferrone et al reported that 3 of 156 patients (1.9%) needed splenectomy after an open Warshaw technique due to abdominal pain and a fever.⁸ Stefano et al reported the results of a meta-analysis of splenic infarction between the LWP and LSPDP with SVP. Those authors found that the LWP was associated with a significantly higher incidence of splenectomy than LSPDP with SVP.²¹ In the present study, the rate of splenic infarction was 32% (6/19) and we evaluated the correlation between splenic vessel distribution in the splenic hilum and splenic infarction. The distributed type was the major type of splenic vessel anatomy, as splenic vessels spread to the splenic hilum in a fan shape and formed an arcade at the splenic hilum. In magistral type, the splenic trunk is long, and branches cluster more closely in the splenic hilum with a poor arcade. However, in the present study, we showed a technique for preserving the furcation point of the splenic artery and splenic hilum vascular arcade, thereby preventing splenic infarction; the infarction rate was 100% in the magistral type. These results indicated that completely maintaining the splenic perfusion was difficult in magistral type due to poor formation of the vascular arcade. However, preserving the furcation point limited the extent of splenic infarction and did not result in intervention-requiring complications.

The patency of vessels after LSPDP with SVP has been reported by several authors. Yoon et al described the obliteration rate of the splenic vein as 50.1% at 6 months after LSPDP with SVP.²³ Collateral vessel formation was confirmed in 41% (9/22) of patients. According to their findings, the risk factors for poor patency of splenic vessels were postoperative pancreatic fistula and intra-abdominal collection. Hwang et al also reported the obliteration rate of the splenic vein after LSPDP with SVP to be 17.2% (5/30) and the perigastric varices formation rate to be 13.8% (4/30), but no splenic infarction. Comparing these results with our own, LSPDP with SVP seems able to prevent the occurrence of splenic infarction, but there is no marked difference in the rate of perigastric varices formation. Even when splenic infarction occurred, it disappeared in all cases, and no adverse events were observed.

This study had several limitations owing to its retrospective nature and the number of cases is small. Despite several limitations were existed, this is the first study to describe the influence of splenic vessels distribution on splenic infarction, according to the classification by Michels, the distribution of splenic vessels as distributed type (vessels spread to splenic hilum like fan shape) and magistral type (vessels spread to splenic hilum narrowly) at the splenic hilum.

CONCLUSIONS

In conclusion, although LWP is a safe procedure, there is a high risk of splenic infarction if the splenic vessel distribution is a magistral type. Understanding the type before surgery leads to the identification of an appropriate vascular dissection position and reduces postoperative complications. A larger study is needed to confirm the safety and efficacy of the LWP and its short- and long-term outcomes.

Funding: No funding sources

Conflict of interest: None declared

Ethical approval: Not required

REFERENCES

1. 1. Shoup M, Brennan MF, McWhite K, Leung DH, Klimstra D, Conlon KC. The value of splenic preservation with distal pancreatectomy. Arch Surg. 2002;137:164-8.
2. 2. Kimura W, Inoue T, Futakawa N, Shinkai H, Han I, Muto T. Spleen-preserving distal pancreatectomy with conservation of the splenic artery and vein. Surgery. 1996;120:885-90.
3. 3. Warshaw AL. Conservation of the spleen with distal pancreatectomy. Arch Surg. 1988;123:550-3.
4. 4. Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg. 2012;255:1048-59.
5. 5. Kim H, Song KB, Hwang DW, Lee JH, Shin SH, Jun ES, et al. A single-center experience with the laparoscopic Warshaw technique in 122 concecutive patients. Surg Endosc. 2016;30:4057-64.
6. 6. Miura F, Takada T, Asano T, Kenmochi T, Ochiai T, Amano H, et al. Hemodynamic changes of splenogastric circulation after spleen preserving pancreatectomy with excision of splenic artery and vein. Surgery. 2005;138:518-22.
7. 7. Tien YW, Liu KL, Hu RH, Wang HP, Chang KJ, Lee PH. Risk of varices bleeding after spleen-preserving distal pancreatectomy with excision of splenic artery and vein. Ann Surg Oncol. 2010;17:2193-8.
8. 8. Ferrone CR, Konstantinidis IT, Sahani DV, Wargo JA, Fernandez-del Castillo C, Warshaw AL. Twenty-three years of the Warshaw operation for distal pancreatectomy with preservation of the spleen. Ann Surg. 2011;253:1136-9.
9. 9. Louis D, Alassiri A, Kirzin S, Blaye-Felice S, Chalret du Rieu M, Julio CH, Bloom E, et al. Gastric bleeding risk following spleen preserving distal pancreatectomy with excision of the splenic vessels: a long-term follow-up. HPB (Oxford). 2017;19:345-51.
10. 10. Michels NA. The variational anatomy of the spleen and splenic artery. Am J Anat. 1942;70:20.
11. 11. Lynch AM, Kapila R. Overwhelming postsplenectomy infection. Infect Dis Clin North Am. 2012;10:693-707.
12. 12. Moffett SL. Overwhelming postsplenectomy infection: managing patients at risk. JAAPA. 2009;22:36-9.
13. 13. Linet MS, Nyrén O, Gridley G, Mellemkjaer L, McLaughlin JK, Olsen JH, et al. Risk of cancer following splenectomy. Int J Cancer. 1996;66:611-6.
14. 14. Goh BK, Tan YM, Chung YF, Cheow PC, Ong HS, Chan WH, et al. Critical appraisal of 232 consecutive distal pancreatectomies with emphasis on risk factors, outcome, and management of the postoperative pancreatic fistula: a 21-year experience at a single institution. Arch Surg. 2008;143:956-65.
15. 15. Kleeff J, Diener MK, Z'graggen K, Hinz U, Wagner M, Bachmann J, et al. Distal pancreatectomy: risk factors for surgical failure in 302 consecutive cases. Ann Surg. 2007;245:573-82.
16. 16. Jain G, Chakravartty S, Patel AG. Spleen-preserving distal pancreatectomy with and without splenic vessel ligation: a systematic review. HPB (Oxford). 2013;15:403-10.
17. 17. Kim H, Song KB, Hwang DW, Lee JH, Shin SH, Jun ES, et al. A single-center experience with the laparoscopic Warshaw technique in 122 consecutive patients. Surg Endosc. 2016;30:4057-64.
18. 18. Boselli C, Barberini F, Listorti C, Castellani E, Renzi C, Corsi A, et al. Distal pancreatectomy with splenic preservation: A short-term outcome analysis of the Warshaw technique. Int J Surg. 2015;21:S40-3.
19. 19. Song KB, Kim SC, Park JB, Kim YH, Jung YS, Kim MH, et al. Single-center experience of laparoscopic left pancreatic resection in 359 consecutive patients: changing the surgical paradigm of left pancreatic resection. Surg Endosc. 2011;25:3364-72.
20. 20. Elabbasy F, Gadde R, Hanna MM, Sleeman D, Livingstone A, Yakoub D. Minimally invasive spleen-preserving distal pancreatectomy: Does splenic vessel preservation have better postoperative outcomes? A systematic review and meta-analysis. Hepatobiliary Pancreat Dis Int. 2015;14:346-53.
21. 21. Partelli S, Cirocchi R, Randolph J, Parisi A, Coratti A, Falconi M. A systematic review and meta-analysis of spleen-preserving distal pancreatectomy with preservation or ligation of the splenic artery and vein. Surgeon. 2016;14:109-18.
22. 22. Matsushima H, Kuroki T, Adachi T, Kitasato A, Hirabaru M, Hidaka M, et al. Laparoscopic spleen-preserving distal pancreatectomy with and without splenic vessel preservation: the role of the Warshaw procedure. Pancreatology. 2014;14:530-5.
23. 23. Yoon YS, Lee KH, Han HS, Cho JY, Ahn KS. Patency of splenic vessels after laparoscopic spleen and splenic vessel-preserving distal pancreatectomy. Br J Surg. 2009;96:633-40.
24. 24. Hwang HK, Chung YE, Kim KA, Kang CM, Lee WJ. Revisiting vascular patency after spleen-preserving laparoscopic distal pancreatectomy with conservation of splenic vessels. Surg Endosc. 2012;26:1765-71.