Laparoscopic Splenectomy and Esophagogastric Devascularization Versus Endoscopic Varices Ligation Plus Laparoscopic Splenectomy in the Treatment of Portal Hypertension

Abstract

Background/Aims:

To compare laparoscopic splenectomy and esophagogastric devascularization (LSED) with endoscopic variceal ligation (EVL) plus laparoscopic splenectomy (LS) in treating esophagogastric variceal bleeding (EGVB) caused by portal hypertension (PH).

Methods:

Between January 2015 and May 2022, 87 patients with PH caused by hepatitis B cirrhosis were included in the retrospective study (34 in LSED versus 53 in EVL + LS).

Results:

The clinical features of both groups were well-matched (P > .05). The EVL+LS group was associated with shorter operation time, lower operative blood loss, faster gastrointestinal (GI) recovery, lower C-reactive protein levels, and shorter hospital stays after operation (P < .05). Operative morbidity was more significant in the LSED group (19 55.9% versus 18 33.9%) (P < .05). On postoperative days 1 and 3, albumin levels were remarkably lower (P < .05) in the LSED group. The mean follow-up was 24.3 months for LSED and 26.5 for EVL+LS. Hematological parameters, hepatic functional status, hepatic hemodynamics, and endoscopy indicated a substantial improvement in both groups (P < .05), but no significant difference was identified (P > .05). There was no discernible difference in the incidence of GI bleeding between the two groups (P > .05).

Conclusion:

EVL+LS is a safer, simpler, and more minimally invasive treatment of EGVB secondary to PH.

Introduction

Due to the high prevalence of chronic hepatitis B infection worldwide, many individuals experience portal hypertension (PH).¹ PH can cause esophagogastric variceal bleeding (EGVB) and hypersplenism, which are severe complications. The most frequent of these causes of death in PH patients is EGVB.²

Currently, the main treatment methods for EGVB include transjugular intrahepatic portosystemic shunt (TIPS), endoscopic treatment, splenectomy, and esophagogastric devascularization.³ The first-line therapy for EGVB is endoscopic, such as endoscopic variceal ligation (EVL). However, EVL cannot alleviate PH or hypersplenism.⁴ TIPS has two apparent disadvantages, causing liver failure and hepatic encephalopathy, which leads to TIPS in most cases only as a rescue treatment rather than as a preferred method for preventing recurrent variceal bleeding.⁵

Splenectomy reduces portal venous pressure and resolves hypersplenism. In addition, it prevents hepatic fibrosis,⁶ enhances liver function, and promotes liver regeneration.⁷ Therefore, splenectomy is considered a valuable option for treating hypersplenism in cirrhosis. With the advancement of laparoscopic equipment and the maturity of the surgeon's technique, laparoscopic splenectomy (LS) is widely used. To treat hypersplenism and gastroesophageal varices, LS in conjunction with esophagogastric devascularization is the best option.⁸

However, splenectomy plus esophagogastric devascularization does not eliminate varices. Instead, the reversed blood flow in the esophageal submucosa and muscle layer may raise the risk of variceal bleeding by raising the venous pressure near the distal end of the stomach. Therefore, someone proposed a new treatment for esophageal varices, splenectomy plus EVL, and satisfactory results were obtained.^9,10 This study compared the efficacy of EVL+LS and laparoscopic splenectomy and esophagogastric devascularization (LSED) in treating EGVB due to PH.

Materials and Methods

Patients

This study included 87 patients with PH caused by hepatitis B cirrhosis who were hospitalized at the Second Department of Hepatobiliary Surgery, Sichuan Provincial People's Hospital, between January 2015 and May 2022. Thirty-four of the 87 cases underwent LSED, and the other 53 underwent EVL+LS. Two criteria were used to define the indications for both groups: (1) PH from hepatitis B cirrhosis with upper gastrointestinal (GI) bleeding; and (2) PH due to hepatitis B-induced cirrhosis with severe esophageal varices and severe hypersplenism (white blood cell [WBC] counts <3 × 10³/dL or/and platelet [PLT] counts <50 × 10³/dL).¹¹ Exclusion criteria include but are not limited to (1) acute bleeding within 72 hours; (2) chronic portal vein obstruction; (3) hepatocellular carcinoma or other malignancies; and (4) severe gastric varices.

Preoperative evaluation included a defined protocol of blood tests, chest radiography, spirometry, abdominal ultrasound, computed tomography scan, and upper GI endoscopy. Blood tests had WBC, PLT, hemoglobin, alanine aminotransferase (ALT), aspartate transaminase (AST), albumin serum (Alb), total bilirubin (TBIL), international normalized ratio (INR), prothrombin time (PT), HBsAg, HCV antibody, alpha-fetoprotein, and C-reactive protein (CRP). Liver function was assessed using the Child–Pugh grade and model for end-stage liver disease (MELD) score.

All patients had esophageal varices, 8 mild, 25 moderate, 54 severe, and 16 coupled with the red-color sign, all verified by endoscopy. Sixty-three individuals had experienced upper GI bleeding at least once before. The remaining 24 patients, who had no history of bleeding, suffered from severe esophageal varices and hypersplenism. Preoperative clinical parameters, operative details, complications after surgery, and follow-up outcomes were prospectively gathered and retrospectively assessed. Patient characteristics are listed in Table 1. All surgeries were done by the same medical team, with the patient's permission.

Table 1.

Clinical Characteristics of Patients

	LSED (n = 42)	EVL+LS (n = 65)	P
Sex
Male (n)	26	42	.8218
Female (n)	16	23	.8218
Age (year; mean ± SD)	45.3 ± 11.4	41.8 ± 13.6	.2164
WBC count (10⁹/L)	2.2 ± 1.3	2.4 ± 1.1	.4433
PLT count (10⁹/L)	35.7 ± 14.7	31.3 ± 16.5	.2092
HGB (g/L)	96.3 ± 28.7	87.8 ± 26.6	.1622
AST (U/L)	36.5 ± 16.4	38.3 ± 18.8	.6485
ALT (U/L)	42.9 ± 17.2	44.7 ± 19.7	.6636
Alb (g/L)	34.6 ± 4.2	36.3 ± 5.2	.1134
PT (second)	12.3 ± 1.7	12.0 ± 1.8	.4405
MELD score (mean ± SD)	7.88 ± 2.33	7.81 ± 2.41	.8938
Child–Pugh classification
Grade A (n)	31	48	.9954
Grade B (n)	9	12	.8435
Grade C (n)	2	5	.8930
CRP (mg/L)	8.9 ± 6.7	7.7 ± 7.1	.4340
Esophageal varices
Mild (n)	3	7	.6338
Moderate (n)	11	20	.7085
Severe (n)	28	38	.3904
Bleeding history (n)	25	38	.8521
HARI	0.78 ± 0.06	0.76 ± 0.08	.2152
PVF (mL/s)	47.6 ± 15.3	48.7 ± 17.5	.7648
Mean follow-up time (mean)	24.3 ± 14.7	26.5 ± 16.6	.5303

Alb, albumin serum; ALT, alanine aminotransferase; AST, aspartate transaminase; CRP, C-reactive protein; EVL, endoscopic variceal ligation; HARI, hepatic artery resistant index; HGB, hemoglobin; LS, laparoscopic splenectomy; LSED, laparoscopic splenectomy and esophagogastric devascularization; MELD, model for end-stage liver disease; PLT, platelet; PT, prothrombin time; PVF, portal venous flow; SD, standard deviation; WBC, white blood cell.

Examination of hepatic hemodynamics

The measurement of portal venous flow and hepatic artery resistant index was realized according to our report before.¹² Color Doppler ultrasound detection was performed preoperatively, on postoperative day (POD) 7, and at each follow-up visit.

Endoscopic examination

The routine preoperative endoscopic examination was performed 2–5 days before the LS and at each follow-up visit. Esophageal varices were graded using the Dagradi classification.

Endoscopic variceal ligation

At the same time as preoperative endoscopic examination, the EVL was performed once on the patients with severe esophageal varices in the EVL+LS group. An endoscope (GIFO 260; Olympus Optical, Tokyo, Japan) was inserted after applying local lidocaine. For patients with just esophageal varices, 6–18 bands were placed over varices starting in the distal esophagus using a multiband endoscopic ligating device (Tian. Yi. Ltd. Tianjin, China). Ligature was continued until varices were no longer visible.

Laparoscopic splenectomy

Both groups need to undergo LS. After general anesthesia, the patient is placed in the correct lateral position, with the left side elevated by ∼60°. Four ports are typically required for a 10 mm 30° laparoscope, an ultrasonic dissector (Harmonic Scalpel; Ethicon Endo-Surgery), and a linear laparoscopic stapler (Echelon 60 ENDOPATH Stapler; Ethicon Endo-Surgery, LLC, Cincinnati, OH). The table was inclined to the reverse Trendelenburg position. Dissect the perisplenic attachments in order: splenic ligament, splenic flexure attachment, splenic ligament, and splenic ligament. The linear laparoscopic vascular stapler transected the hilum after separating the spleen's upper pole from the diaphragm. The spleen is stripped, retracted, and placed in the spleen retrieval bag. Splenic blood autotransfusion was performed in all 87 cases.

Laparoscopic esophagogastric devascularization

In the LSED group, after the splenectomy, patients were positioned in the supine posture. Starting from the middle of the greater curvature of the stomach, the main branch of the gastric coronary vein, the posterior gastric vein, and the left gastric artery were stripped using an ultrasonic stripper and vascular locks. The gastrohepatic ligament was severed, and the veins on the side of the stomach's lesser curvature received the same treatment. To separate the paraesophageal venous collaterals, the esophagus was pulled downward.

Postoperative management

The same team of surgeons provided the same postoperative care to all patients. If HBV DNA levels were positive, patients were administered anti-HBV treatment. On the first, third, and seventh PODs, serum ALT, AST, PT, TBIL, creatinine, Alb, INR, and CRP levels were evaluated to assess liver function impairment and recovery. The MELD score was calculated based on the following three variables: INR, TBIL, and creatinine on POD 7 and at each follow-up visit. In our study, the MELD scale was the original version developed by the Mayo Clinic.

Patient follow-up

Both groups of patients were followed up for the final review. Mean follow-up for EVL+LS and LSED was 24.3 ± 14.7 months (range 6–57 months) and 26.5 ± 16.6 months (range 6–58 months), respectively (P > .05). Patients were followed for at least 6 months. Patients were followed after discharge at 4 weeks, 3 months, 6 months, and every 6 months after that until the last follow-up visit. Routine surveillance included clinical assessment, HBV DNA levels, upper GI endoscopy, and abdominal ultrasound. The degree of varices, hepatic hemodynamics, and functional liver reserve were assessed at each follow-up visit.

Statistical methods

All analyses were done in SPSS 19.0. Categorical data were examined using the χ² or Fisher exact tests, while quantitative data were evaluated using the paired-sample t-test. Results were presented as mean value ± standard deviation, and P value <.05 was considered statistically significant.

Results

The two groups were similar regarding preoperative clinical features, including gender, age, hematological parameters, liver functional status, endoscopy, history of esophageal bleeding, and hepatic hemodynamics (Table 1).

In the EVL+LS group, all patients underwent successful surgery without conversion from laparoscopic to open surgery. In the LSED group, one conversion procedure was performed. The EVL+LS group was associated with shorter operation time (excluding the time of endoscopic examination or EVL), faster recovery of GI function, postoperative hospitalization (after the LS or LSED), and intraoperative bleeding than the LSED group (Table 2).

Table 2.

Intraoperative, Postoperative Data and Results of Follow-Up

	LSED (n = 42)	EVL+LS (n = 65)	P
Conversion (n)	1	0	.3908
Operation time (minute)	242 ± 47	187 ± 52	.0000
Intraoperative blood loss (mL)	221 ± 112	115 ± 89	.0000
Autotransfusion volume (mL)	269 ± 107	257 ± 91	.5770
Intraoperative allogeneic transfusion (n)	8	6	.1305
GI function recovery time (day)	3.6 ± 0.9	2.1 ± 0.7	.0000
Postoperative hospital stay (day)	10.7 ± 2.1	7.1 ± 2.3	.0000
Complication
Pulmonary infection (n)	2	0	.1500
Ascites (n)	5	3	.2963
Pulmonary effusion (n)	5	2	.1541
Gastric perforation (n)	1	0	.3908
Pancreatic leakage (n)	1	2	1.0000
Postoperative bleeding (n)	1	0	.3908
Portal or splenic vein thrombosis (n)	11	17	.9784
Operative morbidity, n (%)	19^a (55.9)	18^b (33.9)	.0436
POD 7
WBC count (10⁹/L)	7.2 ± 1.6^*	6.6 ± 1.8^*	.1172
PLT count (10⁹/L)	203.7 ± 119.2^*	211.3 ± 128.7^*	.7828
HGB (g/L)	126.6 ± 17.6^*	120.5 ± 16.9^*	.1097
HARI	0.67 ± 0.07^*	0.65 ± 0.09^*	.2748
PVF (mL/s)	18.7 ± 13.5^*	21.6 ± 10.3^*	.2603
MELD score range	5.26 ± 2.81^*	5.31 ± 2.66^*	.9335
Results of follow-up (at last visit)
WBC count (10⁹/L)	5.6 ± 2.2^#	6.4 ± 2.5^#	.1311
PLT count (10⁹/L)	133.7 ± 76.7^#	141.7 ± 85.5^#	.6589
HGB (g/L)	122.2 ± 29.3^#	127.8 ± 36.1^#	.4506
HARI	0.61 ± 0.11^#	0.63 ± 0.14^#	.4830
PVF (mL/s)	24.9 ± 16.7^#	23.5 ± 17.5^#	.7119
MELD score range	5.74 ± 2.67^#	5.63 ± 2.84^#	.8573
Esophageal varices
Mild (n)	17^#	26^#	.9316
Moderate (n)	13	20	.9626
Severe (n)	4^#	7^#	.8942
Rebleeding (n)	2	3	.6682

Twenty-six complications occurred in 19 patients.

Twenty-four complications occurred in 18 patients.

Statistically significant difference between preoperation and POD 7.

Statistically significant difference between preoperation and last visit.

EVL, endoscopic variceal ligation; GI, gastrointestinal; HARI, hepatic artery resistant index; HGB, hemoglobin; LS, laparoscopic splenectomy; LSED, laparoscopic splenectomy and esophagogastric devascularization; MELD, model for end-stage liver disease; PLT, platelet; POD, postoperative day; PVF, portal venous flow; WBC, white blood cell.

In the LSED group, 19 patients developed 26 complications, including 1 stomach perforation, 1 pancreas leak, 1 postoperative bleeding, 2 lung infections, 5 lung effusions, 5 severe ascites, and 11 portal or splenic vein thrombosis. In the EVL+LS group, 18 patients developed 24 postoperative complications, including 2 pancreas leaks, 2 lung infections, 3 severe ascites, and 17 portal or splenic vein thrombosis. Overall surgical morbidity was significantly higher for LSED (19, 55.9%) compared with EVL+LS (18, 33.9%) (P = .0436). Complications were not significantly different. The postoperative outcomes are shown in Table 2.

Portal or splenic vein thrombosis was the most frequent complication in both groups. All the pancreatic leakage and portal or splenic vein thrombosis were asymptomatic in both groups. One individual in the LSED group experienced gastric perforation. After 3 weeks of treatment, the patient recovered with drainage and nutritional support therapy. One LSED patient experienced postoperative bleeding on POD 1. After emergency laparoscopic therapy, the patient recovered within 7 days. All the patients with other minor complications recovered after conservative treatment. No severe intraoperative and postoperative complications happened in the EVL+LS group. Deaths due to surgical complications were not reported in any of the groups.

Both groups of patients were discharged from the hospital in good condition. During follow-up, no patient died. Both groups' hematologic metrics, MELD scores, and hepatic hemodynamics improved dramatically without any discernible variations. Both groups saw a considerable improvement in severe esophageal varices, decreasing from 23 to 4 cases in the LSED group (P < .05) and from 31 to 7 points in the EVL+LS group (P < .05). There were no significant differences in endoscopy between both groups. The occurrence of GI rebleeding did not differ substantially (2/34 LSED versus 3/53 EVL+LS, P > .05)—all 5 patients who suffered GI rebleeding recovered by conservative treatment. Long-term effectiveness was similar between the two groups (Table 2).

ALT, AST, and PT levels on PODs 1, 3, 7, and last visit were not significantly different (P > .05). However, albumin levels on PODs 1 and 3 were remarkably (P < .05) lower in the LSED group. Postoperative CRP levels increased in both groups. At POD 1 (38.6 ± 18.5 versus 30.7 ± 17.4 mg/L, P = .0470), POD 3 (97.8 ± 40.7 versus 80.2 ± 36.7 mg/L, P = .0395), and POD 7 (53.8 ± 27.7 versus 42.5 ± 23.8 mg/L, P = .0459), the LSED group's mean CRP levels were substantially more significant than those of the EVL+LS group (Table 3).

Table 3.

Postoperative Data and Results of Follow-Up of Liver Function and C-Reactive Protein

	LSED (n = 34)	EVL+LS (n = 53)	P
POD 1
AST (U/L)	63.8 ± 33.5	58.4 ± 29.7	.4316
ALT (U/L)	54.6 ± 32.2	60.3 ± 35.4	.4501
Alb (g/L)	27.6 ± 3.6	29.4 ± 3.7	.0279
PT (second)	14.3 ± 2.5	13.6 ± 3.1	.2721
CRP (mg/L)	38.6 ± 18.5	30.7 ± 17.4	.0470
POD 3
AST (U/L)	59.6 ± 38.3	55.2 ± 31.3	.5596
ALT (U/L)	57.8 ± 34.7	63.2 ± 36.5	.4944
Alb (g/L)	31.7 ± 4.1	33.6 ± 4.3	.0437
PT (second)	14.0 ± 2.7	14.4 ± 3.3	.5562
CRP (mg/L)	97.8 ± 40.7	80.2 ± 36.7	.0395
POD 7
AST (U/L)	39.8 ± 18.4	44.7 ± 22.8	.2958
ALT (U/L)	47.4 ± 24.3	45.8 ± 19.7	.7369
Alb (g/L)	33.4 ± 3.8	34.2 ± 4.1	.3636
PT (second)	12.8 ± 2.5	13.3 ± 2.8	.3995
CRP (mg/L)	53.8 ± 27.7	42.5 ± 23.8	.0459
Results of follow-up (at last visit)^a
AST (U/L)	33.6 ± 21.2	37.1 ± 23.2	.4798
ALT (U/L)	36.7 ± 19.7	39.4 ± 21.8	.5602
Alb (g/L)	35.7 ± 3.8	36.8 ± 4.5	.2412
PT (second)	11.6 ± 1.6	11.8 ± 1.9	.6123
CRP (mg/L)	8.5 ± 7.1	7.9 ± 7.6	.7134

No significant differences were observed between preoperation and last visit in AST, ALT, Alb, PT, and CRP levels.

Alb, albumin serum; ALT, alanine aminotransferase; AST, aspartate transaminase; CRP, C-reactive protein; EVL, endoscopic variceal ligation; LS, laparoscopic splenectomy; LSED, laparoscopic splenectomy and esophagogastric devascularization; POD, postoperative day; PT, prothrombin time.

Discussion

PH is a clinical syndrome of portal vein blood flow obstruction or abnormal blood flow, which leads to the continuous increase of portal vein system pressure¹³ and extensive formation of collateral circulation.^14,15 Ideally, the principles of treatment of PH include etiological treatment and reduction of portal pressure, prevention and control of EGVB, and correction of severe hypersplenism.^16,17 Surgical treatment is the most reliable treatment, including shunt and disconnection. In the West, TIPS is usually used in patients whose hemorrhage is challenging to manage by medical and endoscopic means or in patients requiring stabilization before a liver transplant.¹⁸

In Asia, Hassab's operation (splenectomy and azygos vein devascularization) is widely used because of its simplicity, increased hepatic perfusion, and improved hepatic function.¹⁹ It can reduce portal vein pressure and reverse hypersplenism. With the advancement of laparoscopic procedures, laparoscopic splenectomy and portal vein dissection have become commonplace.²⁰ LSED controls hypersplenism and prevents variceal bleeding, making it an alternative treatment for refractory variceal bleeding. However, porto-azygous disconnection blocks the systemic circulation of the portal and azygous veins, resulting in increased portal vein pressure,¹¹ increased risk of portal vein thrombosis,²¹ and gastric mucosal injury. It has been reported that EVL+LS is effective in preventing gastroesophageal variceal rebleeding in patients with cirrhosis.²²

In our study, long-term efficacy was not statistically different between groups. However, the EVL+LS group had significantly faster recovery of GI function and a lower incidence of surgery, probably due to less intraoperative blood loss and less intraoperative GI irritation. In addition, in the LSED group, 2 rare but life-threatening complications occurred, including 1 gastric perforation and 1 postoperative hemorrhage. Gastric perforation may be associated with thermal damage from the ultrasonic stripper and poor healing of gastric wall damage due to poor liver function and reduced blood supply. LSED may be more likely to cause postoperative bleeding as a more complex technique than LS. There was no pulmonary infection in the EVL+LS group. This may be due to faster postoperative recovery, and therefore, earlier postoperative walking.

There was no difference in postoperative ALT, AST, PT, and MELD scores. However, Alb levels were significantly higher on PODs 1 and 3 in the EVL+LS group. CRP is an indicator of tissue damage.²³ Our study showed that the EVL+LS group's CRP level was significantly lower than the LSED group's CRP level, indicating that the EVL+LS group's surgical trauma was less. Compared with LSED, EVL+LS had fewer injuries and less bleeding.

Conclusion

We conclude that EVL+LS are less intraoperative blood loss, low surgery incidence, rapid GI function recovery, and minor surgical trauma. Also, it is effective in controlling hypersplenism and preventing variceal bleeding. It is a safer, simpler, and minimally invasive alternative to LSED for treating EGVB secondary to PH caused by cirrhosis. EVL+LS surgery is less risky and can be widely performed. However, LSED should be undertaken with caution.

Footnotes

Acknowledgments

The authors would like to acknowledge everyone who participated in the study and all the medical personnel who contributed.

Authors' Contributions

X.L., R.C., and J.G. designed the study; R.C., Y.W., and S.L. collected the patient's clinical data; Y.W., and X.L. analyzed the data; X.L., R.C., and J.G. wrote the article. The article has been read and approved, and the authors have recognized it.

Ethical Approval

This study follows the current ethical guidelines of the Helsinki Declaration and was approved by the Human Ethics Committee of the Sichuan Academy of Medical Sciences and Sichuan Provincial People's Hospital.

Consent to Publish

All participants agreed to publish and sign the informed consent form.

Disclosure Statement

The authors declare that there is no conflict of interest. Approval from the hospital board committee is taken for the procedure and case report publication.

Funding Information

This study was funded by the Sichuan Province Science and Technology Support Program (no. 2020YJ0462).

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