Spleen-preserving distal pancreatectomy for intraductal papillary mucinous neoplasm

The number of patients diagnosed with intraductal papillary mucinous neoplasms (IPMNs) is increasing due to advances in imaging modalities (1). Several guidelines have suggested the criteria of candidate for surgical resection of IPMNs (2-4). However, there is no consensus regarding an appropriate surgical procedure because the preoperative definitive diagnosis of pathological grading of IPMN is still difficult at present. For IPMNs with low-grade to high-grade dysplasia (carcinoma in situ), which show an extremely low rate of lymph node metastases (LNMs) (5), lymph node dissection is not required, as only radical tumor resection is sufficient for cure. However, IPMNs suspected to be invasive carcinomas reportedly require pancreatectomy with appropriate lymph node dissection (5). Thus, when the preoperative diagnosis shows no evidence of invasive carcinoma, surgeons often perform organ-preserving pancreatectomy with informed consent. Recent advances in imaging modalities have improved the accuracy of the preoperative diagnosis of IPMN before it progresses to an invasive carcinoma, and the use of organ-preserving pancreatectomy is increasing. Spleen-preserving distal pancreatectomy (SPDP) is a good surgical option, especially for IPMNs without the suspicion of invasive components in the body or tail of the pancreas. In a PubMed search, the number of results on using “spleen-preserving distal pancreatectomy” as key words has increased considerably. However, large-scale studies demonstrating the feasibility of SPDP for IPMN have rarely been reported. Gorris et al. stated that as there is a low rate of LNM (4.3%) detected in patients without suspected malignant IPMN, SPDP can be considered to have oncological safety and favorable short- and long-term outcomes (1).

Meta-analyses have shown that distal pancreatectomy with splenectomy (DPS) is associated with more frequent early postoperative infectious complications, including pancreatic fistula, compared to SPDP (6). In addition, SPDP showed a significantly shorter surgical duration and less intraoperative blood loss than DPS (6). Regarding long-term outcomes, although a study comparing overwhelming postsplenectomy infections has not been published (7), several reports have concluded that patients who underwent SPDP had fewer episodes of the common cold or flu than those who underwent DPS (8,9). Preserving organs and immune function is of great advantage in both young and elderly patients. Therefore, if patients with IPMN are diagnosed as having no malignancy (no invasive carcinoma) preoperatively, we can suggest SPDP for surgical resection to avoid overtreatment. However, it is exceedingly challenging to predict pathology preoperatively. We sometimes encounter patients with IPMN who were diagnosed preoperatively as having no malignancy, but invasive carcinoma is diagnosed postoperatively. Gorris et al. defined solid masses, malignant cytology, and preoperative lymphadenopathy as preoperative findings that raise the suspicion of malignancy (1). Gorris et al. reported 4.3% of LNM and 11.3% of invasive carcinoma (1). Since the actual LNM rates were unclear because fewer lymph nodes were harvested in the SPDP group than in the DPS group, some cases might be fatal owing to lymph node recurrences. Detailed data, including the recurrence rate or treatment for recurrence, are important to demonstrate the feasibility of SPDP. Although Gorris et al. showed no inferiority of SPDP compared with DPS for IPMN with no suspicious malignancy in terms of long-term outcomes (1), the cause of death in patients who underwent SPDP was not described in their study (1). The establishment of a more accurate diagnosis using high-quality endoscopic ultrasonography or (18)F-fluorodeoxyglucose positron emission tomography (10) might be useful for selecting appropriate candidates for SPDP in patients with IPMN, but further research is needed. In patients with IPMN and suspected malignancy (invasive carcinoma), although the positive prognostic impact of lymph node dissection in invasive pancreatic carcinoma has not been sufficiently demonstrated in large-scale studies, conventional DPS and lymph node dissection is applied at present. Furthermore, we should take into consideration the reoperation for splenectomy with lymph nodes dissection in patient found to have underlying malignancy after SPDP.

SPDP includes two types of procedures: the Warshaw (splenic vessels removal) (11) and Kimura (splenic vessels preservation) (12). The SPDP procedures which Gorris et al. performed were approximately half Kimura procedure and half Warshaw procedure (1). Conventionally, the Kimura procedure reportedly requires a longer surgical duration than the Warshaw procedure (13), but recent studies have shown similar outcomes between both procedures (14,15). Furthermore, in a recent study comparing minimally invasive SPDP, both the Kimura and Warshaw procedures revealed equivalent short-term outcomes (16). However, the rate of unplanned splenectomy is reportedly higher in the Warshaw procedure (14,15). In addition, postoperative splenic infarction and gastric varices were more frequent in the Warshaw procedure than in the Kimura procedure in meta-analyses (6,15). Therefore, the Kimura procedure is preferred for SPDP. One of the major issues associated with the Kimura procedure is the location of pancreatic transection, which is determined by the tumor location (17,18). If the pancreas is transected above the portal vein, it should be detached from the splenic vessels over a long distance during the Kimura procedure. When a tumor is located in the pancreatic tail, the distance to be detached from the splenic vessels is short. Thus, the tumor location is important in clinical practice in terms of surgical difficulty.

Gorris et al. did not report long-term postoperative outcomes of gastric varices (1). A recent study that included 335 patients with SPDP showed that perigastric variceal formation detected using postoperative imaging was more frequent in the Warshaw (n=44) group than in the Kimura group (n=291) (14). Furthermore, the postoperative platelet count was significantly lower in the Warshaw group than Kimura group (14). However, the clinical events until 5 years after surgery were similar in both groups. The occlusion rate of preserved splenic veins was approximately 20% in the Kimura group (14). The cause of splenic vein occlusion was unclear, but one possible reason might be inflammation caused by pancreatic fistulas. However, no reports have suggested an association between pancreatic fistula and splenic vessel occlusion. In addition, the relationship between the tumor and splenic vessels might be one of the factors associated with postoperative occlusion of splenic vessels. Further research may clarify the mechanism of splenic vein occlusion after the Kimura procedure. When the factors associated with postoperative occlusion of the splenic vessels are revealed, it would be useful to determine whether the Kimura or Warshaw procedure should be indicated for SPDP.

Korrel et al. reported that 217 patients of 1,095 patients who underwent the intended minimally invasive SPDP showed unsuccessful spleen preservation (16). A stepwise strategy is important for the SPDP. Since the Kimura procedure is now preferred for SPDP (15), we first intend to preserve the splenic vessels if there were no oncological issues. However, when severe splenic vessel injury occurs, the surgical option should be changed to a Warshaw procedure. Finally, if we could not preserve the spleen due to uncontrollable bleeding or spleen infarction, we change the strategy to a combined resection of the spleen. Therefore, we should preserve the gastrosplenic ligament until the final stage of operation in the Kimura procedure because we may change the SPDP procedure intraoperatively. Furthermore, in the Warshaw procedure, the left gastroepiploic vessels are important for preventing splenic ischemia (19). Nevertheless, if both the splenic artery and vein cannot be preserved, preserving just the splenic vein may be an option (20).

Minimally invasive distal pancreatectomy is a good option for patients with IPMN located in the pancreatic body or tail. Furthermore, robotic approach may have advantages for spleen preserving procedure (21-23). The robotic approach can facilitate meticulous access to the splenic vessels (Figure 1). In addition, robotic approaches for benign pancreatic tumors may have greater potential for minimally invasive pancreatic parenchymal-preserving procedures such as central pancreatectomy (24).

Figure 1 Intraoperative findings of robotic Kimura procedure. (A) Robotic approach enables meticulous approach to splenic vessels. The branches of splenic vessels are easily divided. (B) Splenic vessels are preserved over the entire length. *, splenic artery; ^†, splenic vein; ^¶, pancreas.

Finally, the spleen should be preserved if the patient can be deemed oncologically and technically safe considering the immune consequences of splenectomy (25). However, no study has reported that SPDP contributes to the prevention of late-onset overwhelming post-splenectomy infections (7). Furthermore, the long-term outcomes of SPDP, including immune function and issues associated with epigastric varices, have not been sufficiently demonstrated by large-scale studies. Further studies, such as randomized controlled trials that evaluate the long-term outcomes of SPDP, are required to demonstrate the feasibility of function-preserving pancreatectomy for patients with less malignant or benign pancreatic tumors.

Acknowledgments

Funding: None.

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Ethical Statement: The author is accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for the publication of this Editorial Commentary and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

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