J Gastrointest Surg DOI 10.1007/s11605-015-2812-5

ORIGINAL ARTICLE

Role of Laparoscopic Partial Splenectomy for Tumorous Lesions of the Spleen Soo Ho Lee 1 & Jun Suh Lee 1 & Young Chul Yoon 2 & Tae Ho Hong 1

Received: 15 January 2015 / Accepted: 25 March 2015 # 2015 The Society for Surgery of the Alimentary Tract

Abstract Background Laparoscopic partial splenectomy (LPS) is a surgical option for splenic masses, with the goal of reducing postoperative complications while preserving splenic function. Methods Thirty-seven patients who underwent laparoscopic splenectomy for tumorous lesions of the spleen at two affiliated hospitals were enrolled. Among them, 22 patients underwent laparoscopic total splenectomy (LTS) and 15 patients underwent LPS. Results The tumorous lesions of the spleen in both groups, in order of decreasing frequency, consisted of epithelial cysts, hemangiomas, lymphangiomas, abscesses, metastatic tumors, and hamartomas. All procedures were completed by laparoscopy, and the pathologic lesions in the spleen were completely removed in both groups. There were no significant differences between the groups in terms of the operative time (LTS 151.5±98.5 min, LPS 168.6±46.8 min, p=0.483), intraoperative blood loss (LTS 337.3±188.4 ml, LPS 422.6±187.4 ml, p=0.185), and transfusion rate (LTS 3/22 [13.6 %], LPS 3/15 [20.0 %], p=0.606). However, there were significant differences in postoperative complications such as pleural effusion (LTS 9/22 [40.9 %], LPS 0/15 [0 %], p=0.005), splenic vein thrombosis (LTS 10/22 [45.5 %], LPS 0/15 [0 %], p=0.002), and postoperative hospital stay (LTS 5.4±1.8 days, LPS 4.2±0.8 days, p=0.027). Conclusions LPS is a feasible, safe surgical procedure in patients with tumorous lesions of the spleen, and it represents an effective approach to reduce postoperative hospital stay and complications. Keywords Spleen . Laparoscopic splenectomy . Partial splenectomy

Abbreviations OPSS Overwhelming postsplenectomy sepsis LPS Laparoscopic partial splenectomy LTS Laparoscopic total splenectomy

* Tae Ho Hong [email protected] 1

Department of Hepato-biliary and Pancreas Surgery, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of Korea, Banpo-daero 222, Seocho-gu, Seoul 137-701, South Korea

2

Department of Hepato-biliary and Pancreas Surgery, College of Medicine, Incheon St. Mary’s Hospital, The Catholic University of Korea, Bupyeong, South Korea

BMI ASA class VAS PSVT

Body mass index American Society of Anesthesiologist class Visual analog scale Portal or splenic vein thrombosis

Introduction Laparoscopic splenectomy has become the method of choice for the surgical treatment of various splenic diseases, and it has the advantages of a minimally invasive procedure with smaller incisions and reduced incisional pain.1,2 However, total splenectomy, even via laparoscopy, could still lead to several severe complications such as pulmonary complications, overwhelming postsplenectomy sepsis (OPSS), and vascular derangements including thromboembolism and subsequent pulmonary hypertension.3 One study reported that clinically evident thrombosis occurred in up to 10 % of patients following total splenectomy, which may increase even further with

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the use of laparoscopy.4 The most serious complication inherent to total splenectomy is OPSS, which can occur in up to 4.4 % of the splenectomized patients and carries a mortality risk of approximately 50 to 80 %.5 For these reasons, investigators have sought to preserve the immunologic function of the spleen via complete removal of the pathologic lesion, coupled with attempts to solve the thromboembolic complications after splenectomy. The partial splenectomy was developed as part of these attempts.4,6,7 The first successful partial splenectomy via the open approach was reported in 1980 by Morgenstern and Shapiro,8 and the same procedure was performed via laparoscopy in 1995 by Uranus et al.9 Surgeons were initially reluctant to perform laparoscopic partial splenectomy (LPS) because of the technical difficulties and the bleeding risk. However, with a better understanding of the vascular anatomy of the spleen and the development of fine laparoscopic skills,10,11 several surgeons began performing LPS in patients with hematologic diseases and reported its safety and feasibility.4–7,12 To date, several case reports have described the use of LPS for tumorous lesions in the spleen. However, there are not sufficient data to compare the surgical results of LPS and laparoscopic total splenectomy (LTS). In this study, we compared the surgical results and complications of LPS and LTS for tumorous lesions in the spleen.

Materials and Methods This study was approved by the Institutional Review Board at Seoul St. Mary’s Hospital and Incheon St. Mary’s Hospital. Data were collected retrospectively on 107 patients who underwent splenectomy for splenic tumorous lesions from March 2008 to September 2014 at these two affiliated hospitals. Of these, 46 patients who concomitantly underwent other major operations were excluded. Twenty-one patients with hematologic diseases, such as lymphoma or leukemia, and three patients who underwent laparotomy splenectomy for tumorous lesions of the spleen were also excluded. Therefore, the final analysis was performed on 37 patents, including 22 patients who underwent LTS and 15 patients who underwent LPS. All operations were performed by three skilled surgeons; one of these surgeons (TH Hong) began performing LPS for solitary tumorous lesions of the spleen in April 2009. Clinical data were collected for age, sex, body mass index (BMI), American Society of Anesthesiologists (ASA) classification, operative time, intraoperative blood loss, transfusion rate, postoperative hospital stay, pre- and postoperative results of complete blood count, chest X-ray, and computed tomography (CT). Preoperative enhanced CT scans were performed to assess the tumor location and evaluate the splenic vascular structure. Prophylactic antibiotics were administered half an

hour before the operation and were continued for 24 h for all the patients. In cases with definite infection, such as splenic abscess, antibiotics were continued accordingly. The immunization history of the patient was reviewed, and vaccines against pneumococcal, meningococcal, and Haemophilus influenzae-type B bacteria were administered before the operation according to the institutional guidelines. Operative Technique The LTS surgical procedure was performed with an anterior approach using four trocars in a true lateral position. The dissection began by opening the gastrocolic and gastrosplenic ligaments to access the lesser sac. The splenophrenic and splenorenal ligaments were also divided to fall to the spleen medially. The tail of the pancreas was identified near the splenic hilum. In most cases, the tail of the pancreas and the splenic hilum were accessible, so an endovascular stapler was used when ligating the splenic vessels. However, additional clipping or intracorporeal suture was sometimes required if bleeding occurred after stapling. The splenic vessels were isolated individually and ligated with metal clips or endoloops in some cases in which the tail of the pancreas extended into the splenic hilum and there was no enough space to apply the endovascular stapler. After the complete detachment of the spleen, the specimen was placed into an endosurgical bag that was inserted through the 12-mm port. The endosurgical bag was retrieved through the extended 12-mm port site without specimen damage. The patient’s positioning and trocar insertions for cases of LPS were similar to those for cases of LTS. The perisplenic ligaments such as the gastrocolic, the splenocolic, and the splenorenal ligament were dissected, except around the presumed remnant spleen, such that partial mobilization of the spleen was performed. The stomach was grabbed and retracted medially for better exposure of the splenic pedicle. The main splenic vessels and lobar splenic vessels were identified by meticulous dissection. The splenic lobar vessels that supplied the pathologic lesion of the spleen were selectively ligated with metal clips (Fig. 1a), which created a clear line of demarcation on the surface of the spleen (Fig. 1b). Splenic parenchymal dissection was performed by following a line 1 cm from the line demarcated by the clips. Splenic parenchymal transection was accomplished using an ultrasonic device without uncontrolled bleeding or oozing (Fig. 2). The resected spleen was placed in a sturdy endosurgical bag, and the bag was brought out through the 12-mm port site. Mild venous oozing or small bleeding areas on the cut surface then were controlled by electrocauterization or gauze compression. Postoperative chest X-ray was performed routinely on the first postoperative day (POD) and at the time of discharge from the hospital. All the patients underwent postoperative CT scan on POD 3, and in some patients, an additional

J Gastrointest Surg Fig. 1 The splenic lobar vessels that supply the pathologic lesion of the spleen were selectively ligated with metal clips (a), which created a clear line of demarcation on the surface of the spleen (b)

follow-up CT scan was performed at an outpatient clinic. A visual analog scale (VAS) was measured to evaluate the degree of postoperative pain 24 h after the operation. Complete blood counts for all the patients were evaluated each day until POD 3. We removed the drain if the output was less than 100 ml/24 h and the patient was hemodynamically stable. Information on complications, including wound complications; bleeding; venous thrombosis; and pulmonary complications, such as atelectasis, pleural effusion, or pneumonia, was collected for all the patients. The diagnosis of atelectasis was based on the official reading of the chest X-ray. Pleural effusion was diagnosed by postoperative chest X-ray, and the grade was classified as follows: grade 1 (costophrenic angle blunting), grade 2 (mild effusion that caused whitish areas at the lung base but did not require intervention), and grade 3 (moderate to severe effusion that required intervention). Portal or splenic vein thrombosis (PSVT) was diagnosed by a radiologist and a surgeon based on the detection of an unenhanced region in the dilated splenoportal system by postoperative CT scan. The grade of the PSVT was classified as follows: 1 (thrombus within the splenic vein that did not cross the middle point of the splenic vein), 2 (thrombosis within the splenic vein and across the middle point of the splenic vein, but not extending to the portal vein), and 3 (thrombosis extending to the portal vein) (Fig. 3). In the case of grade 1 patients, follow-up CT scan was performed 1 week later at an outpatient clinic to evaluate the progression of the PSVT. In grade 2 patients, close follow-up was needed to evaluate the progression of the PSVT, so the CT scan was carried out 3 or 4 days later without anticoagulation therapy. Anticoagulation Fig. 2 Transection of the splenic parenchyma was carried out using an ultrasonic scalpel (a). The cut surface of the spleen is shown in b

therapy was applied to grade 3 patients, and a CT scan was performed once a month for 6 months. Statistical Analysis Statistical analysis was performed using SPSS software version 20.0 for Mac (Statistical Product and Service Solutions, version 20.0; SPSS Inc., Chicago, IL). The t test was used for continuous data, and descriptive statistics were reported as means±standard deviation. The chi-square test was used for categorical data, which were described using frequency distributions. The 95 % confidence interval for differences in proportions was calculated, and the tests for statistical significance were two-sided with a level of significance of 0.05.

Results Demographics The demographics and pathologic diagnoses of the included patients are shown in Table 1. Both groups were comparable in terms of age, gender, and ASA class (Table 1); however, the mean BMI was significantly higher in the LPS group (24.5± 2.9) compared to the LTS group (22.6±2.4) (p=0.032). In both groups, splenic epithelial cyst was the most common disease type (10 patients, six in the LTS group and four in the LPS group). The second most common disease types were hemangioma (eight patients, five in the LTS group and three in the LPS group) and lymphangioma (eight patients, four in the LTS group and four in the LPS group). The next common

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Fig. 3 PSVT was graded as follows: grade 1 PSVT, thrombosis (arrow head) within the splenic vein that does not cross the middle point of the splenic vein (a); grade 2 PSVT, thrombosis (arrow head) within the

splenic vein and across the middle point of the splenic vein, but not extending to the portal vein (b); and grade 3 PSVT, thrombosis (arrow head) extending to the portal vein (c)

diseases included splenic abscess (five patients, four in the LTS group and one in the LPS group), metastatic splenic tumor (four patients, three in the LTS group and one in the LPS group), and hamartoma (two patients, zero in the LTS group and two in the LPS group). There was no difference in disease characteristics between the two groups (p=0.475). LPS was performed in the case of solitary tumors of the spleen, although the LTS group included two cases with multiple tumors in the spleen. There was no significant difference in tumor size between groups, which was measured as the largest diameter of the tumor in the spleen (LTS 5.9±3.1 cm, LPS 7.2±3.2 cm, p=0.234). For the LPS group, the mean volume of the remnant splenic tissue was 46.1 % (±12.3) as measured by postoperative CT scan and there were 3 cases of upper pole resections and 12 cases of lower pole resections.

although there was one patient who was initially planned to receive LPS but was converted to LTS. There was no significant difference in operative time, intraoperative blood loss, or transfusion rate between the two groups. The operative times for the LTS group and LPS group were 151.5 min (±98.5) and 168.6 min (±46.8), respectively (p=0.483). The intraoperative blood loss in the LTS group and the LPS group was 337.3 ml (±188.4) and 422.6 ml (±187.4), respectively (p=0.185). The transfusion rate in the LTS group and the LPS group was three of 22 patients (13.6 %) and three of 15 patients (20 %), respectively (p=0.606). There was no significant difference in the VAS pain score between the LTS group and the LPS group (4.1±1.2 vs. 4.0±0.9, respectively, p=0.947) or in the postoperative maintenance of the drain (3.0±1.1 vs. 2.6±1.1 days, respectively, p=0.398). Postoperative thrombocytosis (platelet count>45,000×106/L) occurred in 10 of 22 (45.5 %) patients; however, only one thrombocytosis case (6.7 %) was identified in the LPS group (p=0.011). As shown in Table 2, three types of complications were observed in the two groups: postoperative atelectasis, pleural effusion, and PSVT. There were two cases (13.3 %) of atelectasis in the LPS group, although five of the 22 patients (22.7 %) in the LTS group suffered from atelectasis (p=0.474). There were no symptoms in three of the five patients with atelectasis. However, two of the patients developed fever and coughing and they were treated with conservative management without antibiotics and discharged after improvement of the chest X-ray findings. There was no evidence of pleural effusion in the LPS group, although nine of the 22 (40.9 %) patients in the LTS group developed pleural effusion (p=0.005). Seven patients had grade 1 effusion, one patient had grade 2 effusion, and another patient had grade 3 effusion that required drainage tube insertion. The drainage tube was removed after improvement of the symptoms and the chest X-ray findings. PSVT was not observed in the LPS group, although 10 of the 22 (45.5 %) patients in the LTS group developed PSVT (p=0.002). Four patients with PSVT were classified as grade 1, and three patients were classified as grade 2. Three patients with grade 3 PSVT received prompt therapeutic doses of lowmolecular-weight heparin followed by an oral anticoagulant

Surgical Results All pathologic lesions in the spleen were completely removed in both groups. No cases were converted to an open procedure, Table 1

Patient characteristics of the LTS and LPS groups LTS (N=22)

LPS (N=15)

p value 0.798 0.823 0.032 0.365 0.475

Age (years) Male/female BMI (kg/m2) ASA score I/II/III Pathology Epithelial cyst

48.1±18.0 7:15 22.6±2.4 10/11/1

46.5±19.2 6:9 24.5±2.9 10/4/1

6

4

Hemangioma Lymphangioma Abscess Metastatic tumor Hamartoma Tumor size (cm) Remnant spleen (%)

5 4 4 3 0 5.9±3.1 0

3 4 1 1 2 7.2±3.2 46.1±12.3

0.234

Values are presented as the mean±standard deviation or as a number LTS laparoscopic total splenectomy, LPS laparoscopic partial splenectomy, BMI body mass index, ASA American Society of Anesthesiologists

J Gastrointest Surg Table 2 Comparisons of surgical results between the LTS and LPS groups

LTS (N=22)

LPS (N=15)

p value

Operative time (min) Intraoperative blood loss (ml) Cases of transfusion (%) VAS for pain Maintenance of drain (days)

151.5±98.5 337.3±188.4 3 (13.6) 4.1±1.2 3.0±1.1

168.6±46.8 422.6±187.4 3 (20) 4.0±0.9 2.6±1.1

0.483 0.185 0.606 0.947 0.398

Postoperative platelet count (×109/L) Cases of thrombocytosis (%) Hospital stay (days) Complications Atelectasis (%) Pleural effusion (%) PSVT (%)

445±319 10 (45.5) 5.4±1.8

228±85 1 (6.7) 4.2±0.8

0.015 0.011 0.027

5 (22.7) 9 (40.9) 10 (45.5)

2 (13.3) 0 (0) 0 (0)

0.474 0.005 0.002

Values are presented as the mean±standard deviation or as a number LTS laparoscopic total splenectomy, LPS laparoscopic partial splenectomy, VAS visual analog scale, PSVT portal or splenic vein thrombosis

therapy for 6 months. All grade 3 PSVT cases resolved after 6 months of anticoagulant therapy. The average postoperative hospital stay in the LPS group was significantly shorter (4.2±0.8 days) than that in the LTS group (5.4±1.8 days) (p=0.027). No patient in either group developed significant postoperative bleeding or intra-abdominal abscess or required re-operation.

Discussion Primary or metastatic tumors of the spleen are relatively uncommon entities, and most cases are asymptomatic. However, without accurate diagnosis and proper treatment, these tumors can lead to serious problems such as spontaneous rupture or profound hemorrhage. Therefore, appropriate management is needed to effectively remove pathologic lesions of the spleen and simultaneously minimize the postoperative complications related to management. To date, many surgeons have performed total splenectomy for the treatment of splenic tumorous lesions without consideration of any other options. However, concerns related to the sequelae of total splenectomy have increased because serious complications, such as PSVT and OPSS, have been associated with this procedure.6,13 For these reasons, there has been increasing interest in the application of partial splenectomy. With recent improvements in the development of laparoscopic instruments, the techniques of laparoscopic surgery, and the understanding of the vascular structure of the spleen, some surgeons have reported LPS to be a safe and feasible approach in patients with hematologic splenic diseases such as hereditary spherocytosis.2,4–7 The results of the present study support the safety and feasibility of LPS in patients with splenic tumorous lesions.

There were no significant differences in operative time, intraoperative blood loss, transfusion rate, and VAS pain scores between the LTS group and the LPS group. Although the average amount of intraoperative blood loss was slightly higher in the LPS group than the LTS group, this difference was not statistically significant. Indeed, intraoperative blood loss is measured using the suction bottle, which is not accurate considering the posture of the patient during the operation. There were also no statistically significant differences in the transfusion rates between the two groups. In the case of LPS, the first three patients required blood transfusion. Monopolar electrocauterization was used for the resection of splenic parenchyma in the early experience with LPS, and a considerable amount of bleeding occurred at the resection surface of the spleen. After accumulation of experience, splenic parenchymal transection was accomplished using an ultrasonic device, upon which uncontrolled bleeding or oozing did not occur. Subsequently, the bleeding was decreased, and blood transfusion was no longer required. Some authors have reported a high incidence of venous thrombosis after splenectomy. In a prospective study, Ikeda et al.14 showed that the incidence of PSVT was as high as 55 %, which was greater than that previously reported by other authors. Krauth et al.13 also suggested that the incidence of PSVT is higher than what would be expected, and PSVT also carries some serious potential risks that could cause intestinal ischemia. We performed an analysis (unpublished) to evaluate the incidence of PSVT in 92 patients who received total splenectomy for various reasons in our centers between March 2008 and September 2014. PSVT was observed in 28 of the 92 patients (30.4 %), and the classifications were as follows: grade 1 PSVT in 14 patients (15.2 %), grade 2 PSVT in 8 patients (8.7 %), and grade 3 PSVT in 6 patients (6.5 %). The result of this brief analysis was in close agreement with

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that of Ikeda and Krauth.13,14 It should be noted that some patients may develop splenic vein thrombosis at a later time. However, considering practicality, multiple follow-up CT scans for the screening of splenic thrombosis are impossible. Thus, the incidence of PSVT could be higher than expected. Therefore, prophylactic anticoagulation should be contemplated for high-risk patients undergoing total splenectomy. In this study, three cases of grade 3 PSVT were observed and these patients were treated promptly with low-molecularweight heparin followed by warfarin. Anticoagulation therapy was maintained for 6 months, until the absence of thrombosis in the porto-mesenteric vein and splenic vein could be confirmed by CT scan. Generally, venous thrombosis occurs in the setting of hypercoagulability, hemodynamic change, and endothelial injury (Virchow’s triad). In LTS, venous stasis can occur due to the severance of all splenic vessels. In addition, the postoperative thrombocytosis that occurred in 45.5 % of patients in the LTS group could have triggered venous thrombosis. PSVT usually presents as a subtle clinical entity in most patients. However, there is also the possibility that high fever, abdominal pain, and portal hypertension can occur.15 Patients with an acute, fully occlusive thrombus in the portal or proximal superior mesenteric vein could develop mesenteric ischemia and signs of peritoneal irritation.15,16 Venous congestion of the intestine may also cause fever and watery diarrhea with or without abdominal pain. Therefore, a high index of suspicion is necessary to make the immediate diagnosis of PSVT. If the clinician does not consider these facts, the diagnosis may be delayed, which can lead to fatal results for the patient. The other important consideration of LTS is the complete loss of the immunologic function of the spleen. Although the incidence of OPSS is very low, mortality rates from sepsis due to encapsulated organisms have been reported to be up to 200 times higher following LTS than in the normal population.17 For these reasons, the volume of the remnant spleen that remains after partial splenectomy is an important concern. If there is no enough splenic tissue left, it would be impossible to maintain the immunologic function of the spleen and prevent OPSS. Studies in rats and humans have suggested that effective immune function is conserved with preservation of approximately 25 % of the normal splenic volume.13,18 In our study, the average remnant spleen volume was 46.0±12.3 %, which was considered to be sufficient to conserve the immune function of the spleen. In one case in the present study, the tumor was situated more closely to the hilum of the spleen than expected based on the preoperative CT images. We initially planned to perform LPS for this case; however, most of the spleen was compromised after ligation of the feeding vessels that supplied the mass, so the procedure was changed to LTS. If the tumor is present in the hilar portion of the spleen, as it was in this case, then partial resection of the spleen can be difficult. Nevertheless, we

believe that in view of the reduction in postsplenectomy complications and preservation of immunologic function, it is worth attempting LPS because the splenic polar arteries supply a considerable amount of remnant spleen, even after ligation of the main splenic vessels. Previously, it was difficult to perform partial splenectomy laparoscopically due to the problem of severe bleeding from the splenic parenchyma. However, laparoscopic instruments have become highly advanced, especially for energy devices such as ultrasonic scissors, which has enabled the reduction of bleeding during transection of the splenic parenchyma. Furthermore, with a better understanding of the splenic vascular structure, i.e., the lack of intraparenchymal anastomoses of the segmental vessels of the spleen, and a clear demarcation line on the splenic surface after ligation of the segmental vessels, it is possible to perform LPS safely by cutting across the spleen within the area where blood flow was blocked. The present study carries the inherent limitations of a retrospective design and a small sample size. These limitations are mainly due to the rarity of splenic tumorous lesions as well as the rarity of the indications for surgical intervention. However, the results of this study suggest that LPS represents a viable alternative to LTS for most patients with tumorous lesions of the spleen.

Conclusion Tumorous lesions in the spleen can be effectively treated via partial splenectomy. Moreover, we believe that the laparoscopic approach is sufficiently safe to complete partial splenectomy, as this approach combines the advantages of partial splenectomy and minimally invasive surgery. This study showed that LPS represents an effective surgical approach to reduce postoperative complications in patients with tumorous lesions of the spleen.

Conflict of Interest None. Funding There was no funding for this study.

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Role of laparoscopic partial splenectomy for tumorous lesions of the spleen.

Laparoscopic partial splenectomy (LPS) is a surgical option for splenic masses, with the goal of reducing postoperative complications while preserving...
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