Hand-Assisted Laparoscopic Splenectomy Is a Better Choice for Patients with Supramassive Splenomegaly Due to Liver Cirrhosis

Abstract

Background:

The current laparoscopic splenectomy (LS) procedure used for cirrhotic patients still has limitations. The aim of our study was to determine a standard according to the splenic size for hand-assisted LS (HALS) in patients with splenomegaly and hypersplenism due to cirrhosis.

Patients and Methods:

We conducted a retrospectively review of cirrhotic patients who underwent splenectomy between 2008 and 2011. All patients were divided into two groups: Group A (19 patients), in which patients' operations were conducted by HALS, and Group B (20 patients), in which patients were treated with LS. Then the patients in Group A were classified on the basis of the spleen size: massive splenomegaly (Group A1) and supramassive splenomegaly (Group A2). Likewise, so were patients in Group B: massive splenomegaly (Group B1) and supramassive splenomegaly (Group B2). Perioperative outcomes of these patients were compared.

Results:

The comparison of HALS and LS based on spleen size demonstrated that in the massive splenomegaly groups, Group A1 and Group B1 had similar estimated blood loss and morbidity, and no transfusion was required in these patients. In the supramassive splenomegaly groups, compared with Group A2, Group B2 had longer operative time, more estimated blood loss, more patients requiring transfusion, and more complications that needed surgical intervention. However, no significant differences were observed in the requirement of analgesia, time of returning to oral intake, and length of hospitalization in these paired groups.

Conclusions:

In cirrhotic patients with supramassive splenomegaly, HALS should be considered because of its safety, feasibility, and effectiveness.

Introduction

Since the first report of laparoscopic splenectomy (LS) was published in 1991,¹ LS has become a standard technique for removal of normal-sized spleens throughout the world. With the progress of surgical instruments and surgeon experience, LS is feasible and safe for patients with splenomegaly. Compared with open splenectomy, LS has less estimated blood loss, fewer complications, and faster recovery.²

Up to now, the adoption of LS in patients with splenomegaly and hypersplenism secondary to cirrhosis is still controversial.^3,4 Ohta et al.⁵ showed that the frequent coexistence of varices, perisplenic collateral vessels, splenomegaly, and thrombocytopenia all lead to an increased risk of intraoperative hemorrhage and conversion to open surgery. Therefore careful attention should be paid in this procedure. One study⁶ suggested mild or moderate cirrhosis of the liver is not a contraindication for laparoscopic procedures, including LS. According to our experience, total laparoscopic techniques are not suitable in all situations. So we introduce the technique of hand-assisted LS (HALS), which allows the surgeon to insert one hand into the peritoneal cavity while maintaining pneumoperitoneum. It can make extremely difficult cases feasible and safe.⁷ However, few studies have been done on HALS in patients with liver cirrhosis, so the aim of our study was to standardize the application of HALS according to the size of spleen enlargement in cirrhotic patients. In our study, splenomegaly was classified into two types: massive splenomegaly (maximum diameter greater than 17 cm) and supramassive splenomegaly (maximum diameter greater than 22 cm).⁸

Patients and Methods

Patients

In the period from May 2008 to January 2011, 44 patients with splenomegaly and hypersplenism secondary to liver cirrhosis underwent either HALS or LS in the Department of Hepatopancreatobiliary Surgery, West China Hospital of Sichuan University, Chengdu, China. The indications for splenectomy included bleeding tendency due to thrombocytopenia (platelet count lower than 30×10⁹/L) (n=17), difficulties in receiving treatment for hepatocarcinoma or hepatitis due to thrombocytopenia (n=30), and high risk of esophageal variceal hemorrhage due to server portal hypertension (n=15). We excluded 5 patients who concomitantly underwent other major surgeries (radiofrequency ablation for hepatocarcinoma, cholecystectomy for cholecyslithiasis, or herniorraphy for hernia). We conducted a retrospective chart review of these patients: 19 patients were treated by the hand-assisted laparoscopic technique (Group A), and 20 patients were treated with the total laparoscopic approach (Group B). Patients in Group A were then classified according to spleen size obtained in preoperative computed tomography imaging: massive splenomegaly (Group A1, n=8) and supramassive splenomegaly (Group A2, n=11). In the same manner, Group B was divided into massive splenomegaly (Group B1, n=10) and supramassive splenomegaly (Group B2, n=10).

Preoperative management

Preoperative computed tomography was performed in all cases to assess splenic size, ascites, and perisplenic collateral vessels. We routinely conducted screening esophagogastroduodenoscopy for all patients before surgery, and endoscopic variceal ligation was performed in patients with medium or large varices in order to prevent lethal hemorrhaging.

Surgical technique

All the surgeries were done by the same surgeon. In the hand-assisted technique, patients were placed in a right semidecubitus position with the left flank elevated at 45°, and the operating table was slightly tilted in a reverse Trendelenburg position. The first 10-mm trocar, used for the 30° camera, was placed in the lower umbilicus. One 12-mm bladeless trocar was placed at the left midclavicular line below the inferior margin of the spleen, and another 5-mm bladeless trocar was placed at the left axillary line below the inferior pole of the spleen. The hand port was inserted through a subxiphoid midline incision approximately 6 cm in length. Then the nondominant hand of the surgeon can be inserted through this hand port to help complete the surgery. Splenic attachments and ligaments were divided using an ultrasound dissector or LigaSure™ vessel sealing system (Covidien) in the order of splenogastric ligament, splenocolic ligament, splenorenal ligament, and splenophrenic ligament. After the spleen was mobilized from the attachments and ligaments, the splenic hilar pedicles were transected with an endoscopic linear vascular stapler. The resected spleen was placed into a retrieval bag and extracted from the midline incision. A suction drain was placed in the splenic fossa. We routinely cut a small piece from the liver for biopsy at the end of surgery. LS was performed in a four-trocar manner as described in our previous report.⁹

Statistical analysis

Data were collected retrospectively in these patients and included both demographic and perioperative clinical data. Variables were analyzed using SPSS version 17.0 for Windows (SPSS, Inc.). All variables were expressed as mean±standard deviation values or counts (percentage). Paired groups were compared using Student's t test, chi-squared test, Fisher's exact test, and Mann–Whitney U test. A value of P<.05 was considered to be statistically significant.

Results

Demographic characteristic and preoperative details

Demographic characteristic and preoperative variables are shown in Table 1. For the two different surgical procedures, overall, more Child–Pugh B patients underwent HALS (P=.048). Both Group A and Group B were comparable for main clinical features; however, hemoglobin (97±25 versus 114±20 g/L, P=.02) and platelet count (30±12 versus 42±16×10⁹/L, P=.014) were lower in Group A. There were no differences in terms of age, sex, white blood cell count, prothrombin time, alanine aminotransferase, aspartate aminotransferase, total bilirubin, serum albumin, Child–Pugh score, and splenic size between the two groups. In the setting of massive splenomegaly, compared with Group B1, Group A1 had a lower hemoglobin level (92±27 versus 121±18 g/L, P=.012), whereas other preoperative details showed no statistically significant differences. In the two supramassive splenomegaly groups, both Group A2 and Group B2 had comparable preoperative details. The diagnosis of each case is shown in Table 1.

Table 1.

Demographic Characteristics and Preoperative Details

	Laparoscopic technique			Massive splenomegaly			Supramassive splenomegaly
Variable	Group A	Group B	P value	Group A1	Group B1	P value	Group A2	Group B2	P value
Number of cases	19	20		8	10		11	10
Age (years)	48±11	48±12	NS	51±10	47±11	NS	45±12	48±12	NS
Sex (M:F)	7:12	9:11	NS	4:4	2:8	NS	4:7	7:3	NS
Hemoglobin (g/L)	97±25	114±20	.02	92±27	121±18	.012	100±24	106±21	NS
WBC (×10⁹/L)	2.48±1.03	2.64±1.21	NS	2.31±0.99	3.36±1.21	NS	2.60±1.10	1.92±0.69	NS
PLT (×10⁹/L)	30±12	42±16	.014	34±9	45±18	NS	27±13	40±14	NS
PT (seconds)	14.1±1.4	13.5±1.0	NS	13.8±1.7	13.3±0.9	NS	14.4±1.1	13.7±1.2	NS
Total bilirubin (μmol/L)	27.7±14.6	22.3±8.0	NS	24.8±11.5	25.1±5.4	NS	29.8±16.8	19.4±9.5	NS
ALT (IU/L)	32±14	44±38	NS	25±6	46±33	NS	37±16	42±44	NS
AST (IU/L)	42±17	54±48	NS	35±9	58±32	NS	47±20	55±62	NS
Serum albumin (g/L)	38.3±5.1	37.9±4.6	NS	38.1±4.5	40±4.8	NS	38.5±5.8	35.7±3.4	NS
Child–Pugh score	6.5±1.2	5.9±0.8	NS	6.3±1.3	5.5±0.5	NS	6.6±1.1	6.2±1.0	NS
Child–Pugh Class			.048			NS			NS
A	9 (47%)	16 (80%)		5 (63%)	10 (100%)		4 (36%)	6 (60%)
B	10 (53%)	4 (20%)		3 (37%)	0		7 (64%)	4 (40%)
C	0	0		0	0		0	0
Diagnosis
Posthepatitis B cirrhosis	15 (78%)	18 (90%)		3 (37.5%)	9 (90%)		11 (100%)	9 (90%)
Posthepatitis C cirrhosis	1 (5.5%)	1 (5%)		2 (25%)	1 (10%)		0	0
Schistosomiasis cirrhosis	2 (11%)	1 (5%)		2 (25%)	0		0	1 (10%)
Alcoholic cirrhosis	1 (5.5%)	0		1 (12.5%)	0		0	0
Spleen size (cm)	28±7	24±5	NS	21±1	20±1	NS	32±6	28±3	NS

Data are mean±standard deviation values or numbers with percentage in parentheses unless otherwise indicated.

ALT, alanine aminotransferase; AST, aspartate aminotransferase; F, female; M, male; NS, not significant; PLT, platelet; PT, prothrombin time; WBC, white blood cell.

Intraoperative data

As shown in Table 2, there were no conversions to open surgery in any of our cases. Overall, the hand-assisted technique (Group A) was superior to the total laparoscopic approach (Group B) in terms of operative time (124±42 versus 195±43 minutes, P=0) and estimated blood loss (92±65 versus 169±136 mL, P=.031). In the paired groups with massive splenomegaly, patients in both Group A1 and Group B1 had similar estimated blood loss (63±26 versus 66±20 mL, difference not significant), although Group A1 had a shorter operative time (94±19 versus 162±24 minutes, P=0). No patients in either Group A1 or B1 required blood transfusion. In patients with supramassive splenomegaly, Group B2 had longer operative time (229±29 versus 146±40 minutes, P=0) and more estimated blood loss (272±122 versus 113±78 mL, P=.002) than Group A2. More patients in Group B2 (n=4, 40%) required blood transfusion compared with Group A2 (n=1, 9%) although there was no statistically significant difference.

Table 2.

Intraoperative Data

	Laparoscopic technique			Massive splenogmegaly			Supramassive splenomegaly
Variable	Group A	Group B	P value	Group A1	Group B1	P value	Group A2	Group B2	P value
Number of cases	19	20		8	10		11	10
OT (minutes)	124±42	195±43	0	94±19	162±24	0	146±40	229±29	0
EBL (mL)	92±65	169±136	.031	63±26	66±20	NS	113±78	272±122	.002
Transfusion	1 (5%)	4 (20%)	NS	0	0	NS	1 (9%)	4 (40%)	NS
Conversion	0	0		0	0		0	0

Data are mean±standard deviation values or numbers with percentage in parentheses unless otherwise indicated.

EBL, estimated blood loss; Ns, not significant; OT, operative time.

Postoperative data

As shown in Table 3, length of hospital stay, requirement of analgesia, and time of returning to first oral intake were comparable between the hand-assisted laparoscopic technique and the total laparoscopic approach regardless of the spleen size. Overall incidence of complications was higher in Group B (n=9, 45%) than in Group A (n=4, 27%) with no statistical significance for the difference. One patient (17%) with massive splenomegaly in Group A1 suffered spontaneous peritonitis, and 2 patients (20%) in Group B1 suffered fever (n=1) or ascites (n=1). In the supramassive splenomegaly groups, 3 patients (27%) in Group A2 suffered ascites (n=2) or fever (n=1). In Group B2, 7 patients (70%) suffered postoperative bleeding (n=1), pancreatic leakage (n=1), splenic fossa abscess (n=1), fever (n=2), portal vein thrombosis (n=1), or ascites (n=1), as shown in Table 3. All complications were resolved by pharmacological treatment except for 3 patients in Group B2 who required surgical intervention: 1 patient in Group B2 required reoperation after LS due to postoperative bleeding from the artery of the pancreatic tail, and the other 2 patients in Group B2 required punctured drainage because of pancreatic leakage and splenic fossa abscess. There was no 30-day mortality in our study. As shown in Table 4, compared with preoperative data, platelet count increased rapidly in Group A (30±11 versus 268±190×10⁹/L, P=0) and Group B (42±16 versus 199±122×10⁹/L, P=0). White blood cell count also increased in Group A (2.48±1.03 versus 9.49±2.50×10⁹/L, P=0) and Group B (2.64±1.21 versus 8.4±1.58×10⁹/L, P=0). Total bilirubin decreased in Group A (27.7±14.7 versus 18.6±7.8 μmol/L, P=0) with a statistically significant difference, but that in Group B showed no significant change. Alanine aminotransferase and aspartate aminotransferase in both groups showed no significant change during our short-term observation.

Table 3.

Postoperative Data

	Laparoscopic technique			Massive splenomegaly			Supramassive splenomegaly
Variable	Group A	Group B	P value	Group A1	Group B1	P value	Group A2	Group B2	P value
Number of cases	19	20		8	10		11	10
LOS (days)	7.2±2.8	8.5±2.3	NS	7.9±3.8	7.7±1.7	NS	7.5±1.8	9.3±2.5	NS
Oral intake (hours)	23.6±3.3	26.1±6.2	NS	22.3±3.2	23.2±5.1	NS	25.2±2.8	28.2±5.9	NS
Complication	4 (21%)	9 (45%)	NS	1 (13%)	2 (20%)	NS	3 (27%)	7 (70%)	NS
Postoperative bleeding	0	1		0	0		0	1
Pancreatic leakage	0	1		0	0		0	1
Splenic fossa abscess	0	1		0	0		0	1
Fever (>38.5°C)^a	1	3		0	1		1	2
Spontaneous peritonitis	1	0		1	0		0	0
Portal vein thrombosis	0	1		0	0		0	1
Ascites	2	2		0	1		2	1
Analgesia	3 (16%)	3 (15%)	NS	1 (13%)	1 (10%)	NS	2 (18%)	2 (20%)	NS

Data are mean±standard deviation values or numbers with percentage in parentheses unless otherwise indicated.

Normal temperature is 37°C.

LOS, length of hospital stay; NS, not significant.

Table 4.

Changes of Blood Count and Liver Function Before and After the Surgery

	HALS (n=19)			LS (n=20)
Variable	Preoperative	Postoperative	P value	Preoperative	Postoperative	P value
Hemoglobin (g/L)	97±25	96±18	NS	114±20	110±14	NS
WBC (×10⁹/L)	2.48±1.03	9.49±2.50	0	2.64±1.21	8.40±1.58	0
PLT (×10⁹/L)	30±11	268±190	0	42±16	199±122	0
Total bilirubin (μmol/L)	27.7±14.7	18.6±7.8	.002	22.4±8.2	21.0±10.4	NS
ALT (IU/L)	32±14	40±16	NS	44±38	40±45	NS
AST (IU/L)	42±17	45±25	NS	54±48	45±35	NS

Data are mean±standard deviation values or numbers with percentage in parentheses unless otherwise indicated.

ALT, alanine aminotransferase; AST, aspartate aminotransferase; HALS, hand-assisted laparoscopic splenectomy; LS. laparoscopic splenectomy; NS, not significant; PLT, platelet; WBC, white blood cell.

Discussion

Liver cirrhosis is defined as the histological development of regenerative nodules surrounded by fibrous bands in response to chronic liver injury.¹⁰ Liver biopsy is the gold standard for the establishment of diagnosis and staging of the disease¹¹ and gives valuable information regarding management and prognosis.¹² Therefore we cut a 1-×1-cm tissue sample from liver for biopsy at the end of each surgery.

Gastroesophageal varices due to portal hypertension are present in approximately 50% of patients with liver cirrhosis. This is an important finding, as rupture of these portosystemic collaterals results in variceal hemorrhage, which is the most common lethal complication of cirrhosis.^10,13 There are many methods treating varices due to portal hypertension such as transjugular intrahepatic portosystemic shunt, shunt, or devascularization surgery.^13,14 According to the American Association for the Study of Liver Disease practice guideline,¹³ we routinely conducted screening esophagogastroduodenoscopy for all patients and performed endoscopic varices ligation in patients with medium or large varices, which have a high risk of hemorrhage. Long-term follow-up regarding recurrent varices, variceal hemorrhaging, and quality of life is ongoing.

Thrombocytopenia or pancytopenia, due to hypersplenism in cirrhotic patients, may hinder the application of aggressive but effective therapies, such as interferon or chemotherapy for hepatocellular carcinoma.¹⁵ Severe thrombocytopenia increases the risk of spontaneous bleeding.¹⁶ Ikegama et al.¹⁷ and Imura et al.¹⁸ showed that splenectomy plays an important role in the treatment of cirrhotic patients with hypersplenism and may improve liver function to some degree. As in many other studies, the white blood cell count and platelet count rapidly reached normal levels in both Group A and Group B. However, we cannot draw a conclusion about the liver function improvement because of insufficient observation time in our study.

LS has been proved a safe and feasible procedure for splenomegaly.^19,20 With the development of surgical instruments such as the ultrasonic dissector, vessel sealing system (LigaSure Atlas™), and linear cutter stapler (Endo GIA™; Covidien), LS has been applied to the treatment of cirrhotic patients with splenomegaly and hypersplenism in a few institutions. Hama et al.²¹ and Watanabe et al.²² described the safety and feasibility of LS in cirrhotic patients. Although their data show that LS can be performed safely and successfully for patients with liver cirrhosis, the clinical practice guidelines of the European Association for Endoscopic Surgery still consider portal hypertension due to cirrhosis a contraindication to the laparoscopic approach.³ Supramassive splenomegaly in cirrhotic patients makes the procedure for LS technically challenging.²³ The frequent coexistence of perisplenic collateral vessels and thrombocytopenia in patients with a cirrhotic liver dramatically increases the risk of massive intraoperative bleeding and increases the conversion rate.²⁴ These challenges inevitably limit the popularization of LS to all but the most experienced surgeons and institutions. The hand-assisted approach was used in order to overcome these hurdles.²⁵ However, its application still requires standardization. Rosen et al.²⁶ suggested that the hand-assisted technique should be initiated at the onset of the procedure for those spleens measuring larger than 22 cm in maximum diameter or weighing more than 1500 g. We chose to use the maximum diameter of the spleen, which can be obtained by preoperative imaging, as our reference parameter because the weight of morcellated spleen, described by many authors when presenting their results, far underestimated the weight of intact spleen.²⁷ The maximum spleen diameter attained through preoperative imaging can be used as a decision-making parameter for the choice of procedure. In order to compare complications between paired groups, we applied the standard of classification of surgical complication that divides complications into five grades according to severity.²⁸

In our study, patients in Groups A1 and B1 with massive splenomegaly had comparable estimated blood loss (63±26 versus 66±20 mL, difference not significant) and morbidity (13% [n=1] versus 20% [n=2], difference not significant). No patients required blood transfusion in these two groups, and complications in these two groups were grade I or grade II, which could be resolved by medication. However, patients in Group B2 had significantly more estimated blood loss (272±122 versus 113±78 mL, P=.002) compared with patients in Group A2. Although no statistically significant difference was observed, there were more transfusion cases in Group B2 compared with Group A2 (20% [n=4] versus 6.7% [n=1]) for intraoperative bleeding. Three complications in Group B2 were grade III and required surgical intervention, whereas all complications in Group A2 were grade I or grade II. We conclude that when the spleen is larger than 22 cm (supramassive splenomegaly), total LS does not provide enough work space for dissection and countertraction or effective tamponade of the bleeding site, thus leading to longer operative times, more intraoperative blood loss, and higher rates of morbidities. We also observed that although preoperative data were comparable with the exception of spleen size, patients in Group A2 had longer operative times (146±40 versus 94±19 minutes, P=.004) and more intraoperative blood loss (113±78 versus 63±26 mL, P=.099) than patients in Group A1. These results indicated that HALS, to some extent, was also affected by the spleen size. However, the upper limit of spleen size that can be safely treated by the hand-assisted approach remains unclear. In our study, no patients who underwent HALS converted to open surgery even when the spleen had a maximum diameter of 45 cm. Targarona et al.²⁹ conducted a comparison between HALS and standard LS for splenomegaly and concluded that HALS was associated with shorter operative times, less morbidities, and shorter hospital stays. Wang et al.³⁰ also attested to the superiority of HALS over LS in patients with splenomegaly (spleen size range, 16–40 cm). As in our study, they attained a mean operative time of 141 minutes, an estimated blood loss of 86 mL, and no conversions to open splenectomy when using HALS. They concluded that by means of the hand-port system, the surgeon can easily manipulate the enlarged spleen by hand; the fingers of the surgeon can be used as a multifunctional “instrument” with intact feedback. These advantages of the hand-assisted technique helped lower intraoperative blood loss and morbidity rates.

The removal of enlarged spleens can be a potentially difficult task. With the LS approach, the ability to guide the spleen into a retrieval bag and to extract it from the abdominal cavity is severely hampered by its size. In our study, the time used to extract the enlarged spleen was the main contributing factor to significantly longer operative time. In other studies,^30,31 morcellation and removal of supramassive spleens often required creating an accessory incision at the end of the surgery. However, this incision could be used strategically at the start of the surgery by using a hand-port, with the potential to simplify the procedure and shorten operative time.

In our study, no statistically significant differences were seen between paired groups in terms of length of hospital stay, time of returning to oral intake, and application of analgesia. The results of our study are in keeping with those of recent publications.^30,32 These indicated that the advantages of minimally invasive surgery are not lost with the incorporation of the hand-port for HALS.

In conclusion, although this study was nonrandomized and retrospective, the upper size limit for safe HALS remains unclear; our data suggest that HALS should be considered in a cirrhotic patient with a spleen larger than 22 cm (supramassive splemomegaly) for its safety, feasibility, and effectiveness. Future randomized controlled prospective studies are required to confirm these findings.

Footnotes

Acknowledgments

The study was supported by a grant from the West China Hospital, Sichuan University.

Disclosure Statement

No competing financial interests exist.

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