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Laparoscopic Versus Open Splenectomy for Portal Hypertension: A Systematic Review of Comparative Studies Yunqiang Cai, Zhihong Liu and Xubao Liu SURG INNOV published online 3 February 2014 DOI: 10.1177/1553350613520513 The online version of this article can be found at: http://sri.sagepub.com/content/early/2014/02/03/1553350613520513
Published by: http://www.sagepublications.com
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Institute for Research into Cancer of the Digestive System
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SRIXXX10.1177/1553350613520513Surgical InnovationCai et al
Article
Laparoscopic Versus Open Splenectomy for Portal Hypertension: A Systematic Review of Comparative Studies
Surgical Innovation 1–6 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1553350613520513 sri.sagepub.com
Yunqiang Cai, MD1, Zhihong Liu, MD1, and Xubao Liu, MD, PhD1
Abstract Background. Laparoscopic splenectomy has become the gold-standard procedure for normal to moderately enlarged spleens. However, the safety of laparoscopic splenectomy for patients with portal hypertension remains controversial. We carried out this systematic review to identify the feasibility and safety of laparoscopic splenectomy in treating portal hypertension. Data sources. A systematic search for comparative studies that compared laparoscopic splenectomy with open splenectomy for portal hypertension was carried out. Studies were independently reviewed for quality, inclusion and exclusion criteria, demographic characteristics, and perioperative outcomes. Conclusion. Although laparoscopic splenectomy is associated with longer operating time, it offers advantages over the open procedure in terms of less blood loss, lower operative complications, earlier resumption of oral intake, and shorter posthospital stay. Therefore, laparoscopic splenectomy is a safe and feasible intervention for portal hypertension. Keywords laparoscopy, splenectomy, portal hypertension, open, comparative
Laparoscopic splenectomy was first reported by Delaitre and Maignien1 and has been adopted as the standard technique for most indications of splenectomy throughout the world.2,3 Laparoscopic splenectomy for portal hypertension is technically challenging because of the frequent coexistence of multiple collateral varices, splenomegaly, poor liver function, and thrombocytopenia.4,5 Portal hypertension caused by liver cirrhosis is considered as a contraindication to laparoscopic splenectomy in the clinical practice guidelines of the European Association for Endoscopic Surgery.6 Along with the development of operative instruments and the accumulation of operating experience, the indication for laparoscopic splenectomy has rapidly increased. Several experienced surgeons have attempted to perform laparoscopic splenectomy for patients with portal hypertension. Owing to its rarity, randomized controlled study for this topic is difficult to perform. Only a few retrospective studies reporting the outcomes of laparoscopic splenectomy for patients with portal hypertension are available, revealing the safety and feasibility of this procedure. This systematic review of published comparative studies in laparoscopic versus open splenectomy for portal hypertension was designed to appraise the claims of such benefits. To the best of our knowledge, this study is the first systematic review available for this subject.
Materials and Methods Review Strategy A literature search via PubMed, Embase, and MEDLINE from 1991 to 2012 was carried out. The subject headings “splenectomy,” “laparosc*,” “portal hypertension,” “hypersplenism,” and “liver cirrhosis” were used in combination with the Boolean operators “AND” and “OR.” Two authors independently performed this procedure. The reference lists of the original articles were also screened for further relevant studies.
Study Selection Potentially eligible studies were independently reviewed by 2 authors for inclusion and exclusion criteria. Studies were included in this review only when they fulfilled the following criteria: English articles published in peerreviewed journals and comparative studies concerning the 1
Sichuan University, Chengdu, China
Corresponding Author: Xubao Liu, Department of Hepatopancreatobiliary Surgery, West China Hospital, Sichuan University, No 37, Guo Xue Xiang, Chengdu, Sichuan, 610041, China. Email: [email protected]
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Surgical Innovation sample size. Differences between variables were compared using the nonparametric Mann-Whitney U test, the χ2 test, and Fisher’s exact test. P < .05 was considered statistically significant.
Results
Figure 1. Flow chart outlining the search history used to identify studies.
perioperative outcomes of laparoscopic splenectomy versus open splenectomy for portal hypertension. The following articles were excluded: abstracts, letters, editorials, expert opinions, reviews, case reports, and animal studies. When studies were reported by the same institution, the more recent publication was included. A summary of the study selection process is provided in Figure 1.
Study Quality No randomized controlled studies were available. All studies included in this review were retrospectively designed. Several authors matched the laparoscopic and open group for demographic characteristics, such as age, sex, and Child–Pugh class, to overcome the shortcoming of the retrospective study. The qualities of studies included in this review were appraised using the Oxford Centre of Evidence-Based Medicine Level of Evidence Scale.7 The evidence level of each study is demonstrated in Table 1.
Data Extraction The data of each study were extracted using a standardized data extraction form. We collected data on age, gender, Child-Pugh class, operating time, estimated blood loss, conversion rate, complications, postoperative hospital stays, additional surgery, and resumption of oral intake. This procedure was independently carried out by 2 reviewers.
Statistical Analysis The data extracted from each article were analyzed as performed by Jusoh and Ammori8 in their review. Numerical data were expressed as mean ± standard deviation, and the results were averaged by weighting the
The initial search yielded 246 potentially eligible articles. The abstracts of these articles were reviewed, and 228 articles were excluded because they were classified as nonEnglish articles, reviews, abstracts, opinions, or animal studies. The full texts of the remaining 18 articles were closely reviewed, and 12 noncomparative studies were excluded, leaving 6 studies that fulfilled the inclusion criteria for analysis.9-14 An article reported by Zheng et al10 contained in a later study14 was excluded from this review. The design of each study and the demographic characteristics of the patients are presented in Table 1. Overall, no significant difference was found between the 2 groups in terms of age, gender, and Child-Pugh class. The intraoperative outcomes and postoperative details are presented in Tables 2 and 3.
Intraoperative Outcomes Conversions. Three studies11-13 in this review reported their conversion series. The overall conversion rate was 5%. All these conversions were a result of uncontrolled intraoperative bleeding. Operating Time. All the studies in this review reported the operating time. Overall, compared with the open group, the laparoscopic splenectomy group was associated with longer operating times (194.1 vs 171.2 minutes, P < .05). Estimated Blood Loss. All the studies included in this review reported the estimated blood loss in milliliters, demonstrating that the patients in the laparoscopic splenectomy group suffered less blood loss. The overall estimated blood loss was significantly lower in the laparoscopic group (214.8 vs 568.3 mL, P < .01). Transfusion. Two studies12,13 reported the number of patients who needed blood transfusions during the operation. Zhu et al11 reported the average number of units of red blood cells transfused for their patients. These studies revealed that the patients in the laparoscopic splenectomy group needed less blood transfusion, which was in agreement with the result that patients in the laparoscopic splenectomy group suffered less blood loss.
Postoperative Outcomes Spleen Weight. Three studies9,11,13 reported the weight of the spleens of the patients, but the method used to measure
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Cai et al Table 1. Details of Patients From Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Number of Patients
Age (years)
Laparoscopic Open (n = 180) (n = 243) Study Design Laparoscopic
Study Watanabe et al9 (2007) Jiang et al12 (2009)
25
28
26
26
Zhu et al11 (2009)
81
135
13
Cai et al (2011)
24
24
Zheng et al (2013)
24
30
Retrospective 63 (42-72) cohort Retrospective 41.5 ± 21.8 cohort Retrospective 49 cohort Retrospective 50.5 ± 10.9 cohort Retrospective 43 (20–56) cohort
Sex: M, F
Open
Child-Pugh Class: A, B, C
P Value Laparoscopic Open P Value Laparoscopic
P Value Evidencea
Open
NA
NA
19, 6
NA
NA
20, 5, 0
NA
NA
3b
44.6 ± 19.6
NS
19, 7
21, 5
NS
17, 8, 1
20, 5, 1
NS
3b
51
NA
38, 43
56, 79
NA
46, 35, 0
57, 53, 15
NA
3b
44.6 ± 13.7
NS
10, 14
13, 11
NS
11, 12, 1
10, 14, 0
NS
3b
47 (18–68)
NS
7, 17
13, 17
NS
15, 9, 0
16, 14, 0
NS
3b
Abbreviations: M, male; F, female; NA, not available; NS, not significant. Oxford Centre of Evidence-Based Medicine Level of Evidence Scale.
a
Table 2. Operative Outcomes of Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Operating time (minutes)a Conversions, n (%) Laparoscopic
Study 9
Watanabe et al (2007) Jiang et al12 (2009) Zhu et al11 (2009) Cai et al13 (2011) Zheng et al (2013)
0 2 (7.69%) 5 (6.17%) 2 (8.3%) 0
Open
173 ± 53 205 ± 60 235 ± 36 178 ± 47 174 ± 42 156 ± 36 224 ± 44 186 ± 83 210 (140-360) 190 (150-270)
Estimated blood loss (mL)a
P Value
Laparoscopic
Open
NS P < .05 NS NS NS
359 ± 280 750 ± 600 200 ± 30 420 ± 50 150.6 ± 135.4 633.8 ± 340.3 162 ± 126 421 ± 347 90 (30-300) 350 (150-800)
Transfusion, n (%) P Value Laparoscopic P < .05 P < .01 P < .01 P < .05 P < .01
0 6 (23.1%) 1.0 ± 1.3a 2 (8.3%) NA
Open
P Value
2 (7.14%) 10 (38.5%) 4.4 ± 2.1a 9 (37.5%) NA
P < .01 P < .05 P < .01 P < .05 NA
Abbreviations: NA, not available; NS, not significant. a Data shown represent mean (±SD) or median (range).
Table 3. Postoperative Outcomes of Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Hospital Stay (days)a
Complications, n (%) Study 9
Watanabe et al (2007) Jiang et al12 (2009) Zhu et al11 (2009) Cai et al13 (2011) Zheng et al (2013)
Spleen Weight (g)a
Laparoscopic
Open
P Value
Laparoscopic
Open
P Value
Laparoscopic
Open
P Value
7 (28%) 5 (19.2%) 22 (27.2%) 3 (12.5%) 4 (16.7%)
10 (35.7%) 11 (42.3%) 34 (25.2%) 10 (41.7%) 10 (33.3%)
NS P < .05 NA P < .05 NS
NA 6.5 ± 2.3 8.2 ± 2.0 7.5 ± 1.7 NA
NA 11.7 ± 4.5 11.9 ±3.8 9.9 ± 3.4 NA
NA P < .05 P < .01 P < .05 NA
525 ± 300 NA 585.7 ± 184.6 1405 ± 752 NA
460 ± 200 NA 591.1 ± 153.4 1243 ± 418 NA
NS NA NS NS NA
Abbreviations: NA, not available; NS, not significant. Data shown represent mean (±SD) or median (range).
a
the spleen weight was not mentioned. The laparoscopic splenectomy group was associated with larger spleens, but the difference was not statistically significant (Table 4). Postoperative Hospital Stays. Two studies9,14 did not report postoperative hospital stays. When the results from 3 studies were pooled, the postoperative hospital stays were significantly lower in the laparoscopic group (Table 4). Resumption of Oral Intake. Three studies12-14 reported the resumption of oral intake of their patients, detecting a significantly shorter time to resumption of oral intake in the
laparoscopic series compared with the open series. The difference was statistically significant (Table 4). Complications. All the studies reported the details of complications associated with the operation. All the reports detected significantly fewer complications in the laparoscopic splenectomy group compared with the open group, especially in terms of wound infection, pleural effusion, and pulmonary infection. Zhu et al11 reported 2 cases of diaphragm rupture and 1 case of colon rupture, which were sutured during the operations. The overall complication associated with the laparoscopic splenectomy group was 22.7%, whereas the complication rate in the
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Table 4. Summary of Results of Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Laparoscopic Series Number of Patients Available
Total number of patients Conversions, n (%) Spleen weight (g)a Operating time (minutes)a Estimated blood loss (mL)a Transfusion, n (%) Postoperative hospital stays (days)a Resumption of oral intake (days)a Complications, n (%) Additional operations Esophagogastric devascularization, n (%)
Result
Open Series Number of Patients Available
180
Result
P Value NS P < .05 P < .01 P < .05 P < .01 P < .01 P = .06 NS
243
180 130 180 180 50 131 74 180
9 (5%) 989.3 194.1 214.8 8 (16%) 7.7 2 41 (22.7%)
187 243 243 50 165 80 243
655.1 171.2 568.3 19 (38%) 13.02 4 75 (30.9%)
180
55 (30.6%)
243
64 (26.3%)
Abbreviation: NS, not significant. a Data averaged by weighting the sample size.
open group was 30.9%. There was no mortality in both groups. The patients in the laparoscopic splenectomy group suffered fewer complications, but the differences were not statistically significant (P = .065).
Discussion Portal hypertension is the increase in portosystemic pressure gradient in any portion of the portal venous system. Although portal hypertension can result from prehepatic abnormalities, intrahepatic noncirrhotic causes, or posthepatic abnormalities, liver cirrhosis is by far the most common cause of portal hypertension.15 The development of collateral circulation, such as esophageal collateral vessels, is a compensatory response to decompress portal hypertension.16 Hypersplenism is a common complication of portal hypertension. Splenectomy is performed for thrombocytopenia secondary to hypersplenism or as a part of devascularization of the upper stomach and esophageal transaction.17 Furthermore, splenectomy can alleviate thrombocytopenia in cirrhotic patients, thereby enabling them to undergo treatment of hepatocellular carcinoma,18 or is used prior to pegylated-interferon plus ribavirin therapy for hepatitis infection.19 Open splenectomy has been performed for hypersplenism since the 1950s, and several studies have documented the efficacy of this approach. Splenectomy is indicated when the platelet count drops below 30 × 109/L.9 Esophagogastric variceal bleeding is another common complication of portal hypertension, which is the most common cause of death.16,20 Esophagogastric devascularization is widely used in Asia in the surgical treatment of esophagogastric variceal bleeding caused
by portal hypertension.21,22 This procedure is an effective intervention for such bleeding.14 Massive intraoperative hemorrhage is the main cause for the conversion of laparoscopic splenectomy,23,24 which is in agreement with the findings of this review. All conversions included in this review were a result of hemorrhage. Patients suffering from portal hypertension may also be afflicted with thrombocytopenia, poor liver function, massive splenomegaly, impaired coagulation factors, and development of multiple collateral vessels.5,25 Ohta et al24 performed a study to analyze the risk factors for massive intraoperative bleeding during laparoscopic splenectomy, demonstrating that liver cirrhosis, portal hypertension, splenomegaly, Child class, and preoperative platelet count are risk factors. Consequently, although some data show that laparoscopic splenectomy can be performed safely and successfully for patients with portal hypertension, many surgeons still consider portal hypertension as a contraindication to the laparoscopic approach.26,27 Mortality-associated open abdominal operations ranged from 10% in patients with Child-Pugh classification A to 82% in patients with Child-Pugh classification C.28 As a minimally invasive procedure, laparoscopic splenectomy is superior to open splenectomy with regard to postoperative pain, length of hospital stay, and perioperative complications.29-31 Because of the high morbidity associated with open splenectomy and the advantages associated with laparoscopic splenectomy, several experienced surgeons have begun to perform laparoscopic splenectomy for patients with portal hypertension. In the setting of portal hypertension, bleeding tendency and splenomegaly are the main reasons that contraindicate laparoscopic splenectomy. The development of
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Cai et al operative instruments and the accumulation of operative experience have begun to overcome these shortcomings. During the past decades, several techniques have been developed to decrease blood loss during laparoscopic splenectomy. Ultrasonic coagulating shears, endovascular stapler, and LigaSure are recommended to facilitate vascular control, decrease blood loss, and shorten the operating time. Newcomb et al32 performed an animal study that compared the homeostasis effect of currently available 5-mm laparoscopic ultrasonic and electrosurgical devices, showing that LigaSure has better homeostasis, especially for the medium and large vessels. This result has been confirmed in several human studies.9,19,24,25,33 Thus, we recommend the use of LigaSure for the division of gastrosplenic ligaments, including short gastric vessels, vascularized retroperitoneal ligaments, and esophagogastric variceal vessels in patients with portal hypertension. The splenic artery and vein can be transected en bloc with the application of a linear laparoscopic vascular stapler, without tedious individual dissection of splenic hilum vessels, thereby decreasing the risk of bleeding.11 Preoperative splenic artery embolization can effectively decrease splenic volume, facilitate the operation, and decrease the risk of massive bleeding from the splenic hilum.34,35 This procedure can also alleviate thrombocytopenia secondary to hypersplenism.36 Currently, no defined criteria exist for the use of preoperative splenic artery embolization before laparoscopic splenectomy. Poulin et al36 recommended its use for spleens that are 20 to 30 cm long. Zhu et al11 ligated the splenic artery during the operation, thus decreasing splenic volume and blood loss. In our practice, we found that this procedure may be tedious, even dangerous in patients with collateral vessels around the splenic artery. Therefore, we recommend preoperative splenic artery embolization in the setting of portal hypertension. In the laparoscopic splenectomy procedure, the division and complete elevation of the upper pole of the spleen is critical. Kawanaka et al25 reported 7 cases of uncontrollable bleeding during the division of the splenic hilar pedicles with an endoscopic linear vascular stapler because the first stapler cannot cross all the splenic hilar pedicles. We also reported a conversion as a result of hemorrhage from the splenic hilum, caused by the insufficient elevation of the upper pole of the spleen.13 In cases of patients with massive splenomegaly or/and multiple collateral vessels, the elevation of the upper pole of the spleen may be difficult. Thus, we recommend handassisted splenectomy for such cases. The development of hand-assisted laparoscopic splenectomy overcomes several disadvantages associated with conventional laparoscopic splenectomy, such as lack of tactile sensation feedback, lack of quick access in the event of unexpected hemorrhage, and difficulties with
intracorporal suturing.37 Furthermore, the surgeon can insert his or her hand into the patient’s abdomen under pneumoperitoneum, allowing the gentle traction and countertraction on tissues and digital blunt dissection.38 The use of a hand port can reduce operating time, increase safety, and shorten the learning curve.39
Conclusion As a minimally invasive surgery, laparoscopic splenectomy has advantages over the open procedure in terms of less blood loss, shorter postoperative hospital stay, fewer complications associated with operation, and earlier resumption of oral intake. Although the learning curve is not defined, we believe that laparoscopic splenectomy for portal hypertension is a safe and feasible intervention. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by the West China Hospital, Sichuan University.
References 1. Delaitre B, Maignien B. Splenectomy by the laparoscopic approach: report of a case. Presse Med. 1991;20:2263. 2. Bell RL, Reinhardt KE, Cho E, Flowers JL. A ten-year, single institution experience with laparoscopic splenectomy. JSLS. 2005;9:163-168. 3. Silecchia G, Boru CE, Fantini A, et al. Laparoscopic splenectomy in the management of benign and malignant hematologic diseases. JSLS. 2006;10:199-205. 4. Wang Y, Zhan X, Zhu Y, et al. Laparoscopic splenectomy in portal hypertension: a single-surgeon 13-year experience. Surg Endosc. 2010;24:1164-1169. 5. Klingler PJ, Tsiotos GG, Glaser KS, Hinder RA. Laparoscopic splenectomy: evolution and current status. Surg Laparosc Endosc. 1999; 9: 1-8. 6. Habermalz B, Sauerland S, Decker G, et al. Laparoscopic splenectomy: the clinical practice guidelines of the European Association for Endoscopic Surgery (EAES). Surg Endosc. 2008;22:821-848. 7. Phillips B, Ball C, Sackett D, et al. Oxford Centre for Evidence-Based Medicine Level of Evidence. http://www. cebm.net/index.aspx?o=1025. Accessed May 3, 2009. 8. Jusoh AC, Ammori BJ. Laparoscopic versus open distal pancreatectomy: a systematic review of comparative studies. Surg Endosc. 2012;26:904-913. 9. Watanabe Y, Horiuchi A, Yoshida M, et al. Significance of laparoscopic splenectomy in patients with hypersplenism. World J Surg. 2007;31:549-555.
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10. Xin Z, Qingguang L, Yingmin Y. Total laparoscopic versus open splenectomy and esophagogastric devascularization in the management of portal hypertension: a comparative study. Dig Surg. 2009;26: 499-505. 11. Zhu JH, Wang YD, Ye ZY, et al. Laparoscopic ver sus open splenectomy for hypersplenism secondary to liver cirrhosis. Surg Laparosc Endosc Percutan Tech. 2009;19:258-262. 12. Jiang XZ, Zhao SY, Luo H, et al. Laparoscopic and open splenectomy and azygoportal disconnection for portal hypertension. World J Gastroenterol. 2009;15:3421-3425. 13. Cai YQ, Zhou J, Chen XD, et al. Laparoscopic splenectomy is an effective and safe intervention for hypersplenism secondary to liver cirrhosis. Surg Endosc. 2011;25:3791-3797. 14. Zheng X, Liu Q, Yao Y. Laparoscopic splenectomy and esophagogastric devascularization is a safe, effective, minimally invasive alternative for the reatment of portal hypertension with refractory variceal bleeding. Surg Innov. 2013;20:32-39. 15. Bari K, Garcia-Tsao G. Treatment of portal hypertension. World J Gastroenterol. 2012;18:1166-1175. 16. Kim MY, Baik SK, Lee SS. Hemodynamic alterations in cirrhosis and portal hypertension. Korean J Hepatol. 2010;16:347-352. 17. Tomikawa M, Hashizume M, Saku M, et al. Effectiveness of gastric devascularization and splenectomy for patients with gastric varices. J Am Coll Surg. 2000;191:498-503. 18. Sugawara Y, Yamamoto J, Shimada K, et al. Splenectomy in patients with hepatocellular carcinoma and hypersplenism. J Am Coll Surg. 2000;190:446-450. 19. Kercher KW, Carbonell AM, Heniford BT, et al. Laparoscopic splenectomy reverses thrombocytopenia in patients with hepatitis C cirrhosis and portal hypertension. J Gastrointest Surg. 2004;8:120-126. 20. Sass DA, Chopra KB. Portal hypertension and variceal hemorrhage. Med Clin North Am. 2009;93:837-853. 21. Carvalho DL, Capua A Jr, Leme PL. Portal flow and hepatic function after splenectomy and esophagogastric devascularization. Int Surg. 2008;93:314-320. 22. Tomikawa M, Akahoshi T, Sugimachi K, et al. An assessment of surgery for portal hypertensive patients performed at a single community hospital. Surg Today. 2010;40:620-625. 23. Grahn SW, Alvarez J III, Kirkwood K. Trends in laparoscopic splenectomy for massive splenomegaly. Arch Surg. 2006;141:755-761; discussion 761-752. 24. Ohta M, Nishizaki T, Matsumoto T, et al. Analysis of risk factors for massive intraoperative bleeding during laparoscopic splenectomy. J Hepatobiliary Pancreat Surg. 2005;12:433-437.
25. Kawanaka H, Akahoshi T, Kinjo N, et al. Technical standardization of laparoscopic splenectomy harmonized with hand-assisted laparoscopic surgery for patients with liver cirrhosis and hypersplenism. J Hepatobiliary Pancreat Surg. 2009;16:749-757. 26. Heniford BT, Matthews BD, Answini GA, Walsh RM. Laparoscopic splenectomy for malignant diseases. Semin Laparosc Surg. 2000;7:93-100. 27. Khoursheed M, Al-Sayegh F, Al-Bader I, et al. Laparoscopic splenectomy for hematological disorders. Med Princ Pract. 2004;13:122-125. 28. Mansour A, Watson W, Shayani V, Pickleman J. Abdominal operations in patients with cirrhosis: still a major surgical challenge. Surgery. 1997;122:730-735; discussion 735-736. 29. Cobb WS, Heniford BT, Burns JM, et al. Cirrhosis is not a contraindication to laparoscopic surgery. Surg Endosc. 2005;19:418-423. 30. Winslow ER, Brunt LM. Perioperative outcomes of laparoscopic versus open splenectomy: a meta-analysis with an emphasis on complications. Surgery. 2003;134:647-653; discussion 654-645. 31. Donini A, Baccarani U, Terrosu G, et al. Laparoscopic vs open splenectomy in the management of hematologic diseases. Surg Endosc. 1999;13:1220-1225. 32. Newcomb WL, Hope WW, Schmelzer TM, et al. Comparison of blood vessel sealing among new electrosurgical and ultrasonic devices. Surg Endosc. 2009;23:90-96. 33. Canda AE, Ozsoy Y, Yuksel S. Laparoscopic splenec tomy using LigaSure in benign hematologic diseases. Surg Laparosc Endosc Percutan Tech. 2009;19:69-71. 34. Reso A, Brar MS, Church N, et al. Outcome of laparoscopic splenectomy with preoperative splenic artery embolization for massive splenomegaly. Surg Endosc. 2010;24:2008-2012. 35. Iwase K, Higaki J, Yoon HE, et al. Splenic artery embolization using contour emboli before laparoscopic or laparoscopically assisted splenectomy. Surg Laparosc Endosc Percutan Tech. 2002;12:331-336. 36. Poulin EC, Mamazza J, Schlachta CM. Splenic artery embolization before laparoscopic splenectomy: an update. Surg Endosc. 1998;12:870-875. 37. Barbaros U, Dinccag A, Sumer A, et al. Prospective randomized comparison of clinical results between handassisted laparoscopic and open splenectomies. Surg Endosc. 2010;24:25-32. 38. Litwin DE, Darzi A, Jakimowicz J, et al. Hand-assisted laparoscopic surgery (HAlaparoscopic splenectomy) with the HandPort system: initial experience with 68 patients. Ann Surg. 2000;231:715-723. 39. Kaban GK, Czerniach DR, Litwin DE. Hand-assisted laparoscopic surgery. Surg Technol Int. 2003;11:63-70.
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Laparoscopic Versus Open Splenectomy for Portal Hypertension: A Systematic Review of Comparative Studies Yunqiang Cai, Zhihong Liu and Xubao Liu SURG INNOV published online 3 February 2014 DOI: 10.1177/1553350613520513 The online version of this article can be found at: http://sri.sagepub.com/content/early/2014/02/03/1553350613520513
Published by: http://www.sagepublications.com
On behalf of:
Institute for Research into Cancer of the Digestive System
Additional services and information for Surgical Innovation can be found at: Email Alerts: http://sri.sagepub.com/cgi/alerts Subscriptions: http://sri.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - Feb 3, 2014 What is This?
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520513
research-article2014
SRIXXX10.1177/1553350613520513Surgical InnovationCai et al
Article
Laparoscopic Versus Open Splenectomy for Portal Hypertension: A Systematic Review of Comparative Studies
Surgical Innovation 1–6 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1553350613520513 sri.sagepub.com
Yunqiang Cai, MD1, Zhihong Liu, MD1, and Xubao Liu, MD, PhD1
Abstract Background. Laparoscopic splenectomy has become the gold-standard procedure for normal to moderately enlarged spleens. However, the safety of laparoscopic splenectomy for patients with portal hypertension remains controversial. We carried out this systematic review to identify the feasibility and safety of laparoscopic splenectomy in treating portal hypertension. Data sources. A systematic search for comparative studies that compared laparoscopic splenectomy with open splenectomy for portal hypertension was carried out. Studies were independently reviewed for quality, inclusion and exclusion criteria, demographic characteristics, and perioperative outcomes. Conclusion. Although laparoscopic splenectomy is associated with longer operating time, it offers advantages over the open procedure in terms of less blood loss, lower operative complications, earlier resumption of oral intake, and shorter posthospital stay. Therefore, laparoscopic splenectomy is a safe and feasible intervention for portal hypertension. Keywords laparoscopy, splenectomy, portal hypertension, open, comparative
Laparoscopic splenectomy was first reported by Delaitre and Maignien1 and has been adopted as the standard technique for most indications of splenectomy throughout the world.2,3 Laparoscopic splenectomy for portal hypertension is technically challenging because of the frequent coexistence of multiple collateral varices, splenomegaly, poor liver function, and thrombocytopenia.4,5 Portal hypertension caused by liver cirrhosis is considered as a contraindication to laparoscopic splenectomy in the clinical practice guidelines of the European Association for Endoscopic Surgery.6 Along with the development of operative instruments and the accumulation of operating experience, the indication for laparoscopic splenectomy has rapidly increased. Several experienced surgeons have attempted to perform laparoscopic splenectomy for patients with portal hypertension. Owing to its rarity, randomized controlled study for this topic is difficult to perform. Only a few retrospective studies reporting the outcomes of laparoscopic splenectomy for patients with portal hypertension are available, revealing the safety and feasibility of this procedure. This systematic review of published comparative studies in laparoscopic versus open splenectomy for portal hypertension was designed to appraise the claims of such benefits. To the best of our knowledge, this study is the first systematic review available for this subject.
Materials and Methods Review Strategy A literature search via PubMed, Embase, and MEDLINE from 1991 to 2012 was carried out. The subject headings “splenectomy,” “laparosc*,” “portal hypertension,” “hypersplenism,” and “liver cirrhosis” were used in combination with the Boolean operators “AND” and “OR.” Two authors independently performed this procedure. The reference lists of the original articles were also screened for further relevant studies.
Study Selection Potentially eligible studies were independently reviewed by 2 authors for inclusion and exclusion criteria. Studies were included in this review only when they fulfilled the following criteria: English articles published in peerreviewed journals and comparative studies concerning the 1
Sichuan University, Chengdu, China
Corresponding Author: Xubao Liu, Department of Hepatopancreatobiliary Surgery, West China Hospital, Sichuan University, No 37, Guo Xue Xiang, Chengdu, Sichuan, 610041, China. Email: [email protected]
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Surgical Innovation sample size. Differences between variables were compared using the nonparametric Mann-Whitney U test, the χ2 test, and Fisher’s exact test. P < .05 was considered statistically significant.
Results
Figure 1. Flow chart outlining the search history used to identify studies.
perioperative outcomes of laparoscopic splenectomy versus open splenectomy for portal hypertension. The following articles were excluded: abstracts, letters, editorials, expert opinions, reviews, case reports, and animal studies. When studies were reported by the same institution, the more recent publication was included. A summary of the study selection process is provided in Figure 1.
Study Quality No randomized controlled studies were available. All studies included in this review were retrospectively designed. Several authors matched the laparoscopic and open group for demographic characteristics, such as age, sex, and Child–Pugh class, to overcome the shortcoming of the retrospective study. The qualities of studies included in this review were appraised using the Oxford Centre of Evidence-Based Medicine Level of Evidence Scale.7 The evidence level of each study is demonstrated in Table 1.
Data Extraction The data of each study were extracted using a standardized data extraction form. We collected data on age, gender, Child-Pugh class, operating time, estimated blood loss, conversion rate, complications, postoperative hospital stays, additional surgery, and resumption of oral intake. This procedure was independently carried out by 2 reviewers.
Statistical Analysis The data extracted from each article were analyzed as performed by Jusoh and Ammori8 in their review. Numerical data were expressed as mean ± standard deviation, and the results were averaged by weighting the
The initial search yielded 246 potentially eligible articles. The abstracts of these articles were reviewed, and 228 articles were excluded because they were classified as nonEnglish articles, reviews, abstracts, opinions, or animal studies. The full texts of the remaining 18 articles were closely reviewed, and 12 noncomparative studies were excluded, leaving 6 studies that fulfilled the inclusion criteria for analysis.9-14 An article reported by Zheng et al10 contained in a later study14 was excluded from this review. The design of each study and the demographic characteristics of the patients are presented in Table 1. Overall, no significant difference was found between the 2 groups in terms of age, gender, and Child-Pugh class. The intraoperative outcomes and postoperative details are presented in Tables 2 and 3.
Intraoperative Outcomes Conversions. Three studies11-13 in this review reported their conversion series. The overall conversion rate was 5%. All these conversions were a result of uncontrolled intraoperative bleeding. Operating Time. All the studies in this review reported the operating time. Overall, compared with the open group, the laparoscopic splenectomy group was associated with longer operating times (194.1 vs 171.2 minutes, P < .05). Estimated Blood Loss. All the studies included in this review reported the estimated blood loss in milliliters, demonstrating that the patients in the laparoscopic splenectomy group suffered less blood loss. The overall estimated blood loss was significantly lower in the laparoscopic group (214.8 vs 568.3 mL, P < .01). Transfusion. Two studies12,13 reported the number of patients who needed blood transfusions during the operation. Zhu et al11 reported the average number of units of red blood cells transfused for their patients. These studies revealed that the patients in the laparoscopic splenectomy group needed less blood transfusion, which was in agreement with the result that patients in the laparoscopic splenectomy group suffered less blood loss.
Postoperative Outcomes Spleen Weight. Three studies9,11,13 reported the weight of the spleens of the patients, but the method used to measure
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Cai et al Table 1. Details of Patients From Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Number of Patients
Age (years)
Laparoscopic Open (n = 180) (n = 243) Study Design Laparoscopic
Study Watanabe et al9 (2007) Jiang et al12 (2009)
25
28
26
26
Zhu et al11 (2009)
81
135
13
Cai et al (2011)
24
24
Zheng et al (2013)
24
30
Retrospective 63 (42-72) cohort Retrospective 41.5 ± 21.8 cohort Retrospective 49 cohort Retrospective 50.5 ± 10.9 cohort Retrospective 43 (20–56) cohort
Sex: M, F
Open
Child-Pugh Class: A, B, C
P Value Laparoscopic Open P Value Laparoscopic
P Value Evidencea
Open
NA
NA
19, 6
NA
NA
20, 5, 0
NA
NA
3b
44.6 ± 19.6
NS
19, 7
21, 5
NS
17, 8, 1
20, 5, 1
NS
3b
51
NA
38, 43
56, 79
NA
46, 35, 0
57, 53, 15
NA
3b
44.6 ± 13.7
NS
10, 14
13, 11
NS
11, 12, 1
10, 14, 0
NS
3b
47 (18–68)
NS
7, 17
13, 17
NS
15, 9, 0
16, 14, 0
NS
3b
Abbreviations: M, male; F, female; NA, not available; NS, not significant. Oxford Centre of Evidence-Based Medicine Level of Evidence Scale.
a
Table 2. Operative Outcomes of Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Operating time (minutes)a Conversions, n (%) Laparoscopic
Study 9
Watanabe et al (2007) Jiang et al12 (2009) Zhu et al11 (2009) Cai et al13 (2011) Zheng et al (2013)
0 2 (7.69%) 5 (6.17%) 2 (8.3%) 0
Open
173 ± 53 205 ± 60 235 ± 36 178 ± 47 174 ± 42 156 ± 36 224 ± 44 186 ± 83 210 (140-360) 190 (150-270)
Estimated blood loss (mL)a
P Value
Laparoscopic
Open
NS P < .05 NS NS NS
359 ± 280 750 ± 600 200 ± 30 420 ± 50 150.6 ± 135.4 633.8 ± 340.3 162 ± 126 421 ± 347 90 (30-300) 350 (150-800)
Transfusion, n (%) P Value Laparoscopic P < .05 P < .01 P < .01 P < .05 P < .01
0 6 (23.1%) 1.0 ± 1.3a 2 (8.3%) NA
Open
P Value
2 (7.14%) 10 (38.5%) 4.4 ± 2.1a 9 (37.5%) NA
P < .01 P < .05 P < .01 P < .05 NA
Abbreviations: NA, not available; NS, not significant. a Data shown represent mean (±SD) or median (range).
Table 3. Postoperative Outcomes of Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Hospital Stay (days)a
Complications, n (%) Study 9
Watanabe et al (2007) Jiang et al12 (2009) Zhu et al11 (2009) Cai et al13 (2011) Zheng et al (2013)
Spleen Weight (g)a
Laparoscopic
Open
P Value
Laparoscopic
Open
P Value
Laparoscopic
Open
P Value
7 (28%) 5 (19.2%) 22 (27.2%) 3 (12.5%) 4 (16.7%)
10 (35.7%) 11 (42.3%) 34 (25.2%) 10 (41.7%) 10 (33.3%)
NS P < .05 NA P < .05 NS
NA 6.5 ± 2.3 8.2 ± 2.0 7.5 ± 1.7 NA
NA 11.7 ± 4.5 11.9 ±3.8 9.9 ± 3.4 NA
NA P < .05 P < .01 P < .05 NA
525 ± 300 NA 585.7 ± 184.6 1405 ± 752 NA
460 ± 200 NA 591.1 ± 153.4 1243 ± 418 NA
NS NA NS NS NA
Abbreviations: NA, not available; NS, not significant. Data shown represent mean (±SD) or median (range).
a
the spleen weight was not mentioned. The laparoscopic splenectomy group was associated with larger spleens, but the difference was not statistically significant (Table 4). Postoperative Hospital Stays. Two studies9,14 did not report postoperative hospital stays. When the results from 3 studies were pooled, the postoperative hospital stays were significantly lower in the laparoscopic group (Table 4). Resumption of Oral Intake. Three studies12-14 reported the resumption of oral intake of their patients, detecting a significantly shorter time to resumption of oral intake in the
laparoscopic series compared with the open series. The difference was statistically significant (Table 4). Complications. All the studies reported the details of complications associated with the operation. All the reports detected significantly fewer complications in the laparoscopic splenectomy group compared with the open group, especially in terms of wound infection, pleural effusion, and pulmonary infection. Zhu et al11 reported 2 cases of diaphragm rupture and 1 case of colon rupture, which were sutured during the operations. The overall complication associated with the laparoscopic splenectomy group was 22.7%, whereas the complication rate in the
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Surgical Innovation
Table 4. Summary of Results of Comparative Studies of Laparoscopic Versus Open Splenectomy for Massive Splenomegaly. Laparoscopic Series Number of Patients Available
Total number of patients Conversions, n (%) Spleen weight (g)a Operating time (minutes)a Estimated blood loss (mL)a Transfusion, n (%) Postoperative hospital stays (days)a Resumption of oral intake (days)a Complications, n (%) Additional operations Esophagogastric devascularization, n (%)
Result
Open Series Number of Patients Available
180
Result
P Value NS P < .05 P < .01 P < .05 P < .01 P < .01 P = .06 NS
243
180 130 180 180 50 131 74 180
9 (5%) 989.3 194.1 214.8 8 (16%) 7.7 2 41 (22.7%)
187 243 243 50 165 80 243
655.1 171.2 568.3 19 (38%) 13.02 4 75 (30.9%)
180
55 (30.6%)
243
64 (26.3%)
Abbreviation: NS, not significant. a Data averaged by weighting the sample size.
open group was 30.9%. There was no mortality in both groups. The patients in the laparoscopic splenectomy group suffered fewer complications, but the differences were not statistically significant (P = .065).
Discussion Portal hypertension is the increase in portosystemic pressure gradient in any portion of the portal venous system. Although portal hypertension can result from prehepatic abnormalities, intrahepatic noncirrhotic causes, or posthepatic abnormalities, liver cirrhosis is by far the most common cause of portal hypertension.15 The development of collateral circulation, such as esophageal collateral vessels, is a compensatory response to decompress portal hypertension.16 Hypersplenism is a common complication of portal hypertension. Splenectomy is performed for thrombocytopenia secondary to hypersplenism or as a part of devascularization of the upper stomach and esophageal transaction.17 Furthermore, splenectomy can alleviate thrombocytopenia in cirrhotic patients, thereby enabling them to undergo treatment of hepatocellular carcinoma,18 or is used prior to pegylated-interferon plus ribavirin therapy for hepatitis infection.19 Open splenectomy has been performed for hypersplenism since the 1950s, and several studies have documented the efficacy of this approach. Splenectomy is indicated when the platelet count drops below 30 × 109/L.9 Esophagogastric variceal bleeding is another common complication of portal hypertension, which is the most common cause of death.16,20 Esophagogastric devascularization is widely used in Asia in the surgical treatment of esophagogastric variceal bleeding caused
by portal hypertension.21,22 This procedure is an effective intervention for such bleeding.14 Massive intraoperative hemorrhage is the main cause for the conversion of laparoscopic splenectomy,23,24 which is in agreement with the findings of this review. All conversions included in this review were a result of hemorrhage. Patients suffering from portal hypertension may also be afflicted with thrombocytopenia, poor liver function, massive splenomegaly, impaired coagulation factors, and development of multiple collateral vessels.5,25 Ohta et al24 performed a study to analyze the risk factors for massive intraoperative bleeding during laparoscopic splenectomy, demonstrating that liver cirrhosis, portal hypertension, splenomegaly, Child class, and preoperative platelet count are risk factors. Consequently, although some data show that laparoscopic splenectomy can be performed safely and successfully for patients with portal hypertension, many surgeons still consider portal hypertension as a contraindication to the laparoscopic approach.26,27 Mortality-associated open abdominal operations ranged from 10% in patients with Child-Pugh classification A to 82% in patients with Child-Pugh classification C.28 As a minimally invasive procedure, laparoscopic splenectomy is superior to open splenectomy with regard to postoperative pain, length of hospital stay, and perioperative complications.29-31 Because of the high morbidity associated with open splenectomy and the advantages associated with laparoscopic splenectomy, several experienced surgeons have begun to perform laparoscopic splenectomy for patients with portal hypertension. In the setting of portal hypertension, bleeding tendency and splenomegaly are the main reasons that contraindicate laparoscopic splenectomy. The development of
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Cai et al operative instruments and the accumulation of operative experience have begun to overcome these shortcomings. During the past decades, several techniques have been developed to decrease blood loss during laparoscopic splenectomy. Ultrasonic coagulating shears, endovascular stapler, and LigaSure are recommended to facilitate vascular control, decrease blood loss, and shorten the operating time. Newcomb et al32 performed an animal study that compared the homeostasis effect of currently available 5-mm laparoscopic ultrasonic and electrosurgical devices, showing that LigaSure has better homeostasis, especially for the medium and large vessels. This result has been confirmed in several human studies.9,19,24,25,33 Thus, we recommend the use of LigaSure for the division of gastrosplenic ligaments, including short gastric vessels, vascularized retroperitoneal ligaments, and esophagogastric variceal vessels in patients with portal hypertension. The splenic artery and vein can be transected en bloc with the application of a linear laparoscopic vascular stapler, without tedious individual dissection of splenic hilum vessels, thereby decreasing the risk of bleeding.11 Preoperative splenic artery embolization can effectively decrease splenic volume, facilitate the operation, and decrease the risk of massive bleeding from the splenic hilum.34,35 This procedure can also alleviate thrombocytopenia secondary to hypersplenism.36 Currently, no defined criteria exist for the use of preoperative splenic artery embolization before laparoscopic splenectomy. Poulin et al36 recommended its use for spleens that are 20 to 30 cm long. Zhu et al11 ligated the splenic artery during the operation, thus decreasing splenic volume and blood loss. In our practice, we found that this procedure may be tedious, even dangerous in patients with collateral vessels around the splenic artery. Therefore, we recommend preoperative splenic artery embolization in the setting of portal hypertension. In the laparoscopic splenectomy procedure, the division and complete elevation of the upper pole of the spleen is critical. Kawanaka et al25 reported 7 cases of uncontrollable bleeding during the division of the splenic hilar pedicles with an endoscopic linear vascular stapler because the first stapler cannot cross all the splenic hilar pedicles. We also reported a conversion as a result of hemorrhage from the splenic hilum, caused by the insufficient elevation of the upper pole of the spleen.13 In cases of patients with massive splenomegaly or/and multiple collateral vessels, the elevation of the upper pole of the spleen may be difficult. Thus, we recommend handassisted splenectomy for such cases. The development of hand-assisted laparoscopic splenectomy overcomes several disadvantages associated with conventional laparoscopic splenectomy, such as lack of tactile sensation feedback, lack of quick access in the event of unexpected hemorrhage, and difficulties with
intracorporal suturing.37 Furthermore, the surgeon can insert his or her hand into the patient’s abdomen under pneumoperitoneum, allowing the gentle traction and countertraction on tissues and digital blunt dissection.38 The use of a hand port can reduce operating time, increase safety, and shorten the learning curve.39
Conclusion As a minimally invasive surgery, laparoscopic splenectomy has advantages over the open procedure in terms of less blood loss, shorter postoperative hospital stay, fewer complications associated with operation, and earlier resumption of oral intake. Although the learning curve is not defined, we believe that laparoscopic splenectomy for portal hypertension is a safe and feasible intervention. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by the West China Hospital, Sichuan University.
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