Int J Clin Exp Med 2015;8(8):13657-13669 www.ijcem.com /ISSN:1940-5901/IJCEM0007685
Original Article Surgical interventions for gastric cancer: a review of systematic reviews Weiling He1*, Jian Tu2*, Zijun Huo3, Yuhuang Li4, Jintao Peng5, Zhenwen Qiu6, Dandong Luo6, Zunfu Ke7, Xinlin Chen8 Department of Gastrointestinal and Pancreatic Surgery, Centre of Gastric Cancer, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, Guangdong Province, P. R. China; 2Musculoskeletal Center, Department of Orthopaedic Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou City 510080, Guangdong Province, China; 3Department of Endocrinology, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou City 510080, Guangdong Province, China; 4Department of Molecular & Medical Genetics, Oregon Health & Science University, 3181 S.W. Sam Jackson Park Rd. Portland, Oregon 97239, USA; 5The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou City 510080, Guangdong Province, China; 6The First Affiliated Hospital, Guangzhou university of Chinese Medicine, Guangzhou 510405, Guangdong Province, P. R. China; 7 Department of Pathology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, Guangdong Province, China; 8School of Basic Medical Sciences, Guangzhou university of Chinese Medicine, Guangzhou Higher Education Mega Center, Guangzhou 510006, Guangdong Province, P. R. China. *Equal contributors. 1
Received March 7, 2015; Accepted May 28, 2015; Epub August 15, 2015; Published August 30, 2015 Abstract: Aim: To evaluate methodological quality and the extent of concordance among meta-analysis and/or systematic reviews on surgical interventions for gastric cancer (GC). Methods: A comprehensive search of PubMed, Medline, EMBASE, the Cochrane library and the DARE database was conducted to identify the reviews comparing different surgical interventions for GC prior to April 2014. After applying included criteria, available data were summarized and appraised by the Oxman and Guyatt scale. Results: Fifty six reviews were included. Forty five reviews (80.4%) were well conducted, with scores of adapted Oxman and Guyatt scale ≥ 14. The reviews differed in criteria for avoiding bias and assessing the validity of the primary studies. Many primary studies displayed major methodological flaws, such as randomization, allocation concealment, and dropouts and withdrawals. According to the concordance assessment, laparoscopy-assisted gastrectomy (LAG) was superior to open gastrectomy, and laparoscopy-assisted distal gastrectomy was superior to open distal gastrectomy in short-term outcomes. However, the concordance regarding other surgical interventions, such as D1 vs. D2 lymphadenectomy, and robotic gastrectomy vs. LAG were absent. Conclusion: Systematic reviews on surgical interventions for GC displayed relatively high methodological quality. The improvement of methodological quality and reporting was necessary for primary studies. The superiority of laparoscopic over open surgery was demonstrated. But concordance on other surgical interventions was rare, which needed more well-designed RCTs and systematic reviews. Keywords: Gastric cancer, surgical intervention, systematic review, meta-analysis, methodological quality
Introduction Gastric cancer (GC) is the fourth most common cancer and the second leading cause of cancer-related death worldwide. Although perioperative and adjuvant chemotherapy can improve outcome of GC patients, surgery remains the only curative therapy [1, 2]. Currently, complete resection of cancer (R0) is regarded as standard and basic intervention for GC patients, especially for early or/and resectable ones [3, 4]. Since laparoscopyassisted gastrectomy (LAG) was firstly applied
in 1991, it has gained wide popularity and challenge among surgeons due to its minimal invasion. Later, robotic gastrectomy (RG) was performed in order to overcome technological disadvantages of LAG to some degree. However, LAG, RG and open surgery are still debated as to which is best for GC patients [5, 6]. In addition, controversy over extent of lymphadenectomy during GC surgery never ends. In Asia area, a D2 lymphadenectomy is recommended as standard treatment, while western surgeons would like to perform a D1 resection [7-9]. More and more systematic reviews and meta-analy-
Surgical interventions for gastric cancer sis have assessed the effectiveness among different kinds of surgery performances, along with increasing randomized clinical trials (RCTs) were conducted. Nevertheless, these reviews tend to have certain flaws and problems. Firstly, discordance among these systematic reviews is common, and methodological quality of reviews was reported as a source of discordance. Secondarily, methodological quality of primary studies within these systematic reviews varied widely, which impaired the quality of these reviews. However, a review of systematic review was introduced to solve these problems 6 years ago [10]. The review of systematic review is a systematic process that can help reviewers reach reasoned decisions about the incorporation of existing systematic reviews on a topic-by-topic basis. Thus, well-designed review of systematic reviews on various surgery strategies for GC patients is needed. The aim of this study is to evaluate the methodological quality of systematic reviews and primary studies in the field of GC surgery, as well as the concordance among these systematic reviews. Methods Article identification A comprehensive search of databases, including PubMed, Medline, EMBASE, the Cochrane library and the DARE database, was conducted using the searching terms of gastric cancer, surgery and systematic review/meta-analysis. The related article function was also used to broaden the search. Additional studies were manually searched in the reference of all retrieved articles. The last searching date was April 29, 2014. Two authors (He WL and Tu J) independently screened the title and abstract to determine potential eligibility for this review. When discrepancies occurred, consensus was achieved after further discussion. Article selection The inclusion criteria were defined as follows: (1) the article must be systematic review and/ or meta-analysis; (2) reviews focused on surgical interventions for GC patients; (3) reviews reporting the efficacy; (4) reviews published in English. Narrative reviews and systematic reviews concentrating on chemotherapy for GC patients were excluded. When the same review group reported duplicate papers on the same topic, the most informative and well-designed one will be chose. 13658
Data extraction Two authors (Ke ZF and Hou ZJ) independently extracted and summarized the data for the following parameters: authors, publication year, publish journal, types of GC patients, and types of intervention (number of treatment group and control group), number and design of primary studies, outcomes. When differences among outcomes existed, the systematic review will be classified according to the primary outcome. Each intervention-specific conclusion reported in a systematic review was classified as “benefit”, “inconclusive”, “no benefit”. When the primary outcomes (including overall complications, operation time, estimated bold loss survival, or survival time) were positive between different surgical interventions, this conclusion was regarded as “benefit”. While the primary outcomes were negative between different surgical interventions, this conclusion was regarded as “no benefit”. Additionally, when the authors of the systematic review cannot draw the conclusions, the tag of “inconclusive” was given to this review. Once more than 75% agreement was reached, concordance between reviews with similar interventions can be set [11]. We contacted the author for detailed information if relevant information was unclear or missing. Quality assessment An adapted scoring approach based on the Oxman and Guyatt scale was used to evaluate the quality of systematic reviews [12, 13]. The scale consisted of 9 items: search methods used to find evidence (Item 1), scope of search (Item 2), criteria for inclusion and exclusion (Item 3), criteria for avoiding bias (Item 4), reporting of criteria for assessing the validity of primary studies (Item 5), assessing the validity of primary studies using appropriate criteria (Item 6), methods of combining the data (Item 7 and Item 8), and conclusions supported by the data or analysis reported in the review (Item 9). The score of each item ranged from 0 to 2 points, resulting in a maximum score of 18 points. High quality was defined when the scores ≥ 14. Moderate quality was defined between scores 11 to 13; while low quality was defined with scores ≤ 10. The items, including randomization, allocation concealment, baseline comparability, blinding (patients, health care providers, data collectors and outcome assessors), dropouts and withdrawals, adverse events, and contamination and cointervention Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer
Figure 1. Selection of studies for inclusion in the review of systematic reviews.
were used to assess the methodological quality of primary studies within the included systematic reviews. Data analysis The SPSS (Version 17; SPSS Inc) software was performed to analyze data and outcomes. The quality scores ware described by mean, while the characteristics were presented as frequency and percentage. Result Data identification and characteristics of included systematic reviews A total of 2104 articles were identified by comprehensive search, of which 2039 were exclud13659
ed based on titles and abstracts screening. 63 Articles were eligible for full text appraising, after which, 6 systematic reviews were excluded because of incomplete data provided in the studies [14-19]. At least, 56 systematic reviews were included [20-75] (Figure 1). Table 1 showed the characteristics of the eligible reviews. The majority of these systematic reviews were focused on 4 types of interventions: LAG vs. open gastrectomy (OG) (15 reviews); laparoscopy-assisted distal gastrectomy (LADG) vs. open distal gastrectomy (ODG) (13 reviews); D1 lymphadenectomy vs. D2 lymphadenectomy (8 reviews); RG vs. LAG (3 reviews). In terms of patients, 12 of 56 included reviews only involved the specific surgical treatment for early gastric cancer (EGC), and 8 of 56 included reviews only involved the specifInt J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Table 1. The characteristic of the eligible reviews Study
Types of No. of primary patients studies (RCTs)
Intervention (treatment vs. control)
No. of patients Outcomes (treatment vs. control)
Wang WZ 2014
GC
18 (0)
LAG vs. OG
955 vs. 1358
OT, EBL, LND, PTM, PM, TLD, TFF
Ye LY 2013
AGC
7 (1)
LAG vs. OG
365 vs. 450
LND, PMM, CRR
Chen K 2013
GC
15 (2)
LAG vs. OG
1327vs. 1192
Shen H 2013
GC
8 (8)
LAG vs. OG
409 vs. 752
PMM, OC, LND
Xiong JJ 2013a
GC
15 (0)
LAG vs. OG
811 vs. 1211
OT, EBL, OC, PMM, TFF, TLD, HS
Wang W 2013
GC
8 (0)
LAG vs. OG
599 vs. 939
OT, EBL, LND, HS
Zhang CD 2013
EGC
16 (5)
LAG vs. OG
919 vs. 746
OT, WL, EBL, LND, TFF, TLD, CRR, HS, OC
Choi YY 2013
AGC
10 (1)
LAG vs. OG
859 vs. 960
DFS, SR
Jiang L 2013a
EGC
8 (8)
LAG vs. OG
402 vs. 382
OT, EBL, PMM, OC, LND, HS, ALS, OS
Haverkamp L 2013
GC
8 (0)
LAG vs. ODG
314 vs. 384
OT, EBL, HS, OC
Sun JF 2012
GC
8 (8)
LAG vs. OG
402 vs. 380
EBL, TFF, TLD, OC, HS, LND, WL
Martínez-Ramos D 2011
AGC
7 (2)
LAG vs. OG
174 vs. 278
OT, EBL, HS, SR, LND
Liang YC 2011
EGC
6 (6)
LAG vs. OG
343 vs. 325
OT, EBL, WL, OC, TFF, TLD, HS, LND
Wei HB 2011
GC
10 (1)
LAG vs. OG + D2
495 vs. 544
OT, EBL, LND, HS, TFF, OC, SR
Wang Y 2013
EGC
8 (8)
LADG vs. ODG
323 vs. 306
OT, EBL, LND, OC, HS, TLD
Qiu JG 2013
AGC
7 (0)
LADG vs. ODG
626 vs. 645
OT, EBL, LND, TLD, TFF, OC, SC, PTM
Zeng YK 2012
EGC
22 (5)
LADG vs. ODG
1596 vs. 1815
Viñuela EF 2012
GC
6 (6)
LADG vs. ODG
343 vs. 323
PMM, OC, LND, OT, EBL, HS
Ohtani H 2011
GC
5 (5)
LADG vs. ODG
164 vs. 162
OT, EBL, LND, TLD, HS, OC,PMM, CRR
Peng JS 2010
EGC
6 (6)
LADG vs. ODG
107 vs. 111
OT, EBL, OC, TFF, HS
Ohtani H 2010
EGC
4 (4)
LADG vs. ODG
323 vs. 306
OT, EBL, LND, TLD, HS, OC, CRR, PMM
Yakoub D 2009
EGC
12 (3)
LADG vs. ODG
516 vs. 435
5-year SR, PMM, LND, HS, RR, OC
Chen XZ 2009
EGC
6 (6)
LADG vs. ODG
323 vs. 306
LND, OT, EBL, PMM, OC
Memon MA 2008
GC
4 (4)
LADG vs. ODG
80 vs. 82
Hosono S 2006
GC
16 (4)
LADG vs. ODG
837 vs. 774
PMM, CRR, 5-year SR
Ding J 2012
GC
8 (0)
LADG vs. ODG + D2
510 vs. 550
OT, EBL, LND, TFF, HS, OC, PMM, CRR
Jiang L 2014
GC
8 (8)
D1 vs. D2
1042 vs. 1002
PMM, 5-year SR, ALS, RR, WI, hemorrhage rate
Jiang L 2013b
GC
12 (8)
D1 vs. D2
1606 vs. 1558
SR, RFS
Memon MA 2011
GC
6 (6)
D1 vs. D2
946 vs. 930
HS, OC, ALS, RR, PMM
Yang SH 2009a
GC
8 (8)
D1 vs. D2
907 vs. 875
PMM, OT, EBL, LND, HS, TLD
Yang SH 2009b
GC
5 (5)
D2 vs. D3
599 vs. 588
OT, PMM, 5-year SR
Lustosa SAS 2008
GC
5 (5)
D1 vs. D2 or D3
791 vs. 758
TLD, TFF, ALS, OC, HS, PMM
McCulloch P 2004
GC
19 (6)
D1 vs. D2
580 vs. 531
PMM, OC, 5-year SR
Seevaratnam R 2012
GC
5 (5)
D1 lymph node dissection vs. D2 lymph node dissection
845 vs. 797
5-year SR, PMM, RR
Liao GX 2013a
GC
4 (0)
RG vs. OG
520 vs. 5260
OT, EBL, HS, OC, LND, PMM, WI, ALS
Liao GX 2013b
GC
7 (0)
RG vs. LAG
762 vs. 1473
OT, EBL, HS, OC, PTM,
Xiong J 2013
GC
9 (0)
RG vs. LAG
736 vs. 1759
EBL, TLD, LND, PTM, PMM, ASL, TFF, HS
Xiong BH 2012
GC
3 (0)
RG vs. LAG
268 vs. 650
OT, OC, EBL, LND, HS, PMM
13660
OT, OT, EBL, LND, PTM, TFF, TLD, HS, OC, PMM
LND, OT, HS, OC, CRR, SR
OT, PMM, 5-year SR
Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Sun J 2013
AGC
14 (0)
Palliative gastrectomy vs. non-gastrectomy
1461 vs. 1542
Xiong JJ 2013 b
GC
3 (3)
R-Y gastrojejunostomy vs. B-I anastomosis after distal gastrectomy
238 vs. 240
OS OT, EBL, HS, ALS, BR, RG, DS, RE
Kim DG 2013
GC
3 (0)
ICBI with LADG vs. ECBI with LADG
341 vs. 457
OT, TFF, HS
Ding J 2013
GC
8 (8)
Gastrointestinal decompression vs. no gastrointestinal decompression
482 vs. 477
HS, TFF, OC, PMM
Lian JJ 2012
EGC
9 (0)
EMR vs. ESD
2053 vs. 1495
ERR, HCRR, OC, OT, CRR
Park YM 2011
EGC
12 (0)
EMR vs. ESD
2072 vs. 1734
ERR, EBL, OT, PMM, complete resection, perforation
Roberts P 2012
GC
8 (0)
Gastrectomy + PD vs. Gastrectomy
132 vs. 260
OC, PMM, ALS
Wen L 2012
GC
8 (1)
TG vs. PG
728 vs. 349
SR, PMM, CRR
Wang Z 2011
GC
4 (4)
Drainage vs. No drainage
220 vs. 218
PMM, OC, RR, WI, ALS, OT, HS
Liu HP 2011
AGC
5 (5)
Drainage vs. No drainage
218 vs. 220
WI, PMM, SR, SC, IA
Zong L 2011
GC
12 (12)
Roux-en-Y with a pouch vs. without a pouch
506 vs. 512
DS, BR, RE, QOL
Zheng B 2011
GC
3 (3)
D2 lymphadenectomy vs. D4 lymphadenectomy
528 vs. 539
5-year SR, PMM, RR, OT, LND
Zorcolo L 2011
EGC
6 (6)
MIDG vs. ODG
343 vs. 323
OT, EBL, LND, HS, TFF, TLD, OC
Bracale U 2011
GC
9 (1)
TLG vs. OG
828 vs. 664
OT, EBL, TFF, LND, PMM, HS
Chen XZ 2010
AGC
3 (3)
D2 + PAND vs. D2
528 vs. 539
5-year SR, PMM
Wang Z 2010
AGC
8 (4)
D2 + PAND vs. D2
1169 vs. 852
5-year SR, PMM, OT, EBL
Yang K 2009
GC
3 (3)
Gastrectomy plus splenectomy vs. gastrectomy alone
231 vs. 235
5-year SR, PMM, LND, HS, RR
Yang Z 2008
GC
5 (5)
Nasogastric or nasojejunal decompression vs. no decompression
361 vs. 356
OT, EBL, HS, LND, OC, CRR, TLD, PMM
GC: gastric cancer; AGC: advanced gastric cancer; EGC: early gastric cancer. D1: D1 lymphadenectomy; D2: D2 lymphadenectomy; D3: D3 lymphadenectomy; D4: D4 lymphadenectomy; ECBI: extracorporeal Billroth I; ESD: endoscopic submucosal dissection; EMR: endoscopic mucosal resection; ICBI: intracorporeal Billroth I; LADG: laparoscopy-assisted distal gastrectomy; LAG: laparoscopy-assisted gastrectomy; MIDG: minimally invasive distal gastrectomy; MVR: multivisceral resection; ODG: open distal gastrectomy; OG: open gastrectomy; PAND: para-aortic nodal dissection; PG: proximal gastrectomy; RG: robotic gastrectomy; TG: total gastrectomy; TLG: totally laparoscopic gastrectomy; ALS: anastomotic leakage and stricture; BR: bile reflux; CRR: cancer recurrence rate; DS: dumping symptoms; EBL: estimated bold loss; ERR: en bloc resection rate; HCRR: histologic curative resection rate; HR: survival rate; HS: hospital stay; IA: intra-abdominal abscess; LND: lymph node dissection; OC: overall complications; OT: operation time; PMM: postoperative mortality and morbidity; PTM: proximal tumor margin; QOL: quality of life; RFS: recurrence free survival; RR: re-operation rate; RG: remnant gastritis; RE: reflex esophagitis; SR: survival rate; TLD: time to liquid diet; TFF: Time to first flatus; WL: wound lengths; WI: wound infection.
Table 3. The number of primary studies achieving the quality criteria Randomization Primary studies % Reviews
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118/284 41.5 36
Allocation Baseline Patients concealment comparability blinded 46/149 30.9 33
176/219 80.4 37
11/379 2.9 33
Health care providers blinded 0/284 0.0 33
Data collectors blinded 0/284 0.0 33
Outcome Dropouts and assessors withdrawals blinded 4/284 1/159 1.4 0.6 33 20
Reporting adverse events 209/299 69.9 27
Contamination or cointervention 25/38 65.8 6
Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Table 2. The numbers of the reviews based on the adapted Oxman and Guyatt scale (n = 56) Items Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9
2 55 50 53 34 48 46 55 54 56
Score 1 1 6 3 20 2 2 0 1 0
0 0 0 0 2 6 7 1 1 0
Mean score 1.9 1.8 1.9 1.3 1.6 1.5 1.9 1.9 2.0
ic surgical treatment for advanced gastric cancer (AGC), while others involved different types of gastric cancer. The median number of patients involved in the reviews was 1459.8, ranged from 162 to 5787. The median of that in treatment group were 652.4, while the median of that in control group were 748.7. The median number of primary studies included in the reviews was 8.25, varied from 3 to 22, 43.5% of which was RCTs. Methodological quality of systematic reviews Tables 2 and 5 outlined the results of the methodological quality assessment for 56 systematic reviews using the adapted the Oxman and Guyatt scale. The average score of all reviews was 15.9, ranged from 7 to 18. 45 of the included reviews (80.4%) were with high quality (mean score ≥ 14), 8 of the reviews (14.3%) were with moderate quality (mean score between 11 and 13), while other 3 reviews (5.4%) were with low quality (mean score ≤ 10). The most common flaws were criteria for avoiding bias (Item 4), reporting of criteria for assessing the validity of primary studies (Item 5), assessing the validity of primary studies using appropriate criteria (Item 6). The overall agreement between the two reviewers regarding quality evaluation was 89.3%, indicating good initial agreement. 100% agreement was attained after a senior investigator was consulted. Methodological quality of primary studies Table 3 elucidated the results of methodological quality assessment of primary studies, which contained the total number and percent13662
age of primary studies that used quality criteria to assess the risk of bias. Randomization and the bias of baseline comparability were relatively most frequently evaluated (36 and 37 reviews respectively), and were achieved in 41.5% and 80.4% of primary studies. Only 33 systematic reviews reported allocation concealment, patients blinded, health care provider blinded, data collectors blinded, outcome assessors blinded, and a paucity of primary studies (< 5%) within them achieved these 5 criteria, except the allocation concealment (30.9%). Only 20 systematic reviews assessed the bias of dropouts and withdrawals, with 0.6% primary studies attained it. Additionally, 27 of 56 systematic reviews evaluated the bias of reporting adverse events, and 69.9% primary studies obtained it. However, only 6 reviews evaluated the contamination or cointervention, and 65.8% of primary studies achieved it. Concordance among reviews The concordance among reviews was summarized in Table 4, which is organized according to types of interventions. The difference between LAG and OG was analyzed in 15 systematic reviews, all of which beneficial conclusions were reported. Therefore, there is concordance among reviews regarding the effectiveness between LAG and OG. The similar results were also demonstrated on LADG vs. ODG. In addition, concordance was also concluded on endoscopic submucosal dissection (ESD) vs. endoscopic mucosal resection (EMR), D2 lymphadenectomy + Para-aortic nodal dissection (PALN) vs. D2 lymphadenectomy, and decompression vs. no decompression after gastrectomy. Nevertheless, there was no concordance in conclusion about the effectiveness between D1 vs. D2 lymphadenectomy, and RG vs. LAG. As for EGC, 9 reviews focused on the efficacy of laparoscopic surgery and conventional open surgery, and concordance existed. In terms of AGC, 4 reviews discussed the oncologic safety of LAG over OG. All of them have gained the conclusion that LAG was not inferior to OG for AGC, suggesting that concordance was illustrated. Discussion A review of reviews is regarded as a method to evaluate trend in methodological quality in a clinical area [76-78]. In this review of systematic reviews on surgical interventions for GC, we Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Table 4. The concordance about efficacy among the reviews Specific Intervention
No. of Reviews
Conclusion Review Article Benefit
Inconclusive
No benefit
consensus
LAG vs. OG
15
15
0
0
yes
LADG vs. ODG
13
12
1
0
Yes
D1 vs. D2
8
4
4
0
No
RG vs. LAG
3
2
1
0
No
ESD vs. EMR
2
2
0
0
Yes
D2 + PAND vs. D2
2
0
0
2
Yes
Decompression vs. no decompression
2
0
0
2
Yes
Drainage vs. no drainage
2
1
1
0
No
R-Y gastrojejunostomy vs. B-I anastomosis after distal gastrectomy
2
1
1
0
No
ICBI vs. ECBI
2
1
1
0
#
MVR vs. No MVR
1
1
0
0
#
RG vs. OG
1
0
1
0
#
TG vs. PG
1
1
0
0
#
D4 vs. D2
1
1
0
0
#
D2 vs. D3
1
1
0
0
#
#: means unable to assess concordance; D1: D1 lymphadenectomy; D2: D2 lymphadenectomy; D3: D3 lymphadenectomy; D4: D4 lymphadenectomy; ECBI: extracorporeal Billroth I; ESD: endoscopic submucosal dissection; EMR: endoscopic mucosal resection; ICBI: intracorporeal Billroth I; LADG: laparoscopy-assisted distal gastrectomy; LAG: laparoscopy-assisted gastrectomy; MIDG: minimally invasive distal gastrectomy; MVR: multivisceral resection; ODG: open distal gastrectomy; OG: open gastrectomy; PAND: para-aortic nodal dissection; PG: proximal gastrectomy; RG: robotic gastrectomy; TG: total gastrectomy; TLG: totally laparoscopic gastrectomy.
Table 5. The scores of Systematic Reviews Based on the adapted Oxman and Guyatt Scale Study Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9 Total Scores Wang WZ 2014 2 2 2 2 2 2 2 2 2 18 Ye LY 2013 2 2 2 2 2 2 2 2 2 18 Chen K 2013 2 2 2 1 2 2 2 2 2 17 Shen H 2013 2 2 2 2 2 2 2 2 2 18 Xiong JJ 2013a 2 2 2 2 2 2 2 2 2 18 Wang W 2013 2 2 2 2 2 2 2 2 2 18 Zhang CD 2013 2 2 2 2 2 2 2 2 2 18 Choi YY 2013 2 2 2 2 2 2 2 2 2 18 Jiang L 2013a 2 2 2 2 2 2 2 2 2 18 Haverkamp L 2013 2 2 2 1 2 2 2 2 2 17 Sun JF 2012 2 1 1 0 0 0 2 2 2 10 Martínez-Ramos D 2011 1 2 1 1 1 0 2 2 2 12 Liang YC 2011 2 2 2 1 2 2 2 2 2 17 Wei HB 2011 2 2 2 1 0 0 2 2 2 13 Wang Y 2013 2 2 2 2 2 2 2 2 2 18 Qiu JG 2013 2 2 2 1 2 2 2 2 2 17 Zeng YK 2012 2 2 2 0 2 1 2 2 2 15 Viñuela EF 2012 2 2 2 1 2 2 2 2 2 17 Ohtani H 2011 2 1 1 1 0 0 2 2 2 11 Peng JS 2010 2 2 2 0 2 0 2 2 2 14 Ohtani H 2010 2 1 1 1 0 0 2 2 2 11 Yakoub D 2009 2 2 2 1 2 2 2 2 2 17 Chen XZ 2009 2 2 2 1 2 2 2 2 2 17 Memon MA 2008 2 1 1 1 2 2 2 2 2 15 Hosono S 2006 2 1 2 1 0 0 2 2 2 12
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Surgical interventions for gastric cancer Ding J 2012 Jiang L 2014 Jiang L 2013b Memon MA 2011 Yang SH 2009a Yang SH 2009b Lustosa SAS 2008 McCulloch P 2004 Seevaratnam R 2012 Liao GX 2013a Liao GX 2013b Xiong J 2013 Xiong BH 2012 Sun J 2013 Xiong JJ 2013b Kim DG 2013 Ding J 2013 Lian JJ 2012 Roberts P 2012 Wen L 2012 Wang Z 2011 Liu HP 2011 Zong L 2011 Zheng B 2011 Zorcolo L 2011 Park YM 2011 Bracale U 2011 Chen XZ 2010 Wang Z 2010 Yang K 2009 Yang Z 2008 Mean Score
2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 1.9
2 2 2 2 2 2 2 2 2 1 2 2 2 2 2 1 1 2 2 1 2 2 2 2 1 2 2 1 2 2 1 1.8
2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 1.9
not only assessed the methodological quality of included reviews and primary studies, but also appraised the concordance among included reviews. The systematic reviews identified in the current study showed a wide variety of surgical treatments on GC. Regarding the number of included systematic reviews, there is a growing trend of published systematic review about surgical intervention for GC. This may be related with more RCTs conducted and reported in recent year, and more widely accepted consensus on the standard assessment and reporting during the manufacture of a systematic reviews. The overall quality of included systematic reviews was relatively high. However, there were still
13664
1 2 2 0 1 1 1 2 1 2 2 2 1 2 1 1 1 1 1 1 2 1 1 1 1 2 2 1 2 2 1 1.3
2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 0 2 2 0 2 2 1 0 2 0 2 2 2 2 2 2 1.6
2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 0 2 2 0 1 2 2 0 2 0 2 2 1 2 2 2 1.5
2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 2 1.9
2 2 2 0 2 2 2 2 2 1 2 2 2 2 2 2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 2 1.9
2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2.0
17 18 18 7 17 17 16 18 17 16 18 18 17 18 17 12 16 17 9 15 18 16 13 17 12 18 18 15 18 18 16 15.9
some obvious flaws and problems. Firstly, the use of criteria for avoiding bias and assessing the validity of primary studies should be emphasized. Comprehensive evaluation of validity for primary studies would make readers easier to extrapolate the conclusions. Secondarily, there was a paucity of long term outcomes, such as overall survival (OS), disease free survival (DFS), in the majority of included systematic reviews. OS and DFS were widely accepted as the standard endpoint to evaluate the effectiveness of the special intervention for cancer patients. The methodological quality of the primary studies still needed improvement, which could fundamentally affect the quality and conclusion of
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Surgical interventions for gastric cancer systematic reviews. The blindness of patients, health care providers, data collectors, and outcome assessors were achieved rarely in primary studies, which could be determined factors of information bias. However, it is hard to deal with the blindness of patients, data collectors, and surgeons as for surgical interventions. The blindness was nor regarded as an important part for surgical interventions. Therefore, randomization, allocation concealment and dropouts and withdrawals should be improved in further RCTs. On one hand, more well-designed RCTs and long-term follow-up data are required to assess the recurrence and survival of GC patients. On the other hand, more comprehensive and reasonable analyses methods for retrospective data should be developed. Additionally, more rigorous quality assessment criteria and reporting principle should be considered in the primary studies in future, such as Physiotherapy Evidence-Based Database Quality Assessment Scale and Consolidated Standards for Reporting Trials (CONSORT) [79]. From the systematic review compared LAG with OG for GC, concordance was drawn. It was generally accepted that LAG could be performed safely with less complications and a shorter hospital stay, despite longer operation duration. Also, similar results were demonstrated on estimated bold loss (EBL), survival rate between LAG and OG. Nevertheless, this concordance was established on the systematic reviews, the majority of which focused on the short term outcomes of LAG or OG. The long term survival data were rarely pooled in the included systematic reviews. The similar results were also achieved on the comparison between LADG with ODG. Whether the laparoscopic surgery could satisfy oncologic safety and surgical adequacy, regarding radical resection and management of complicated vascular structure, needed to be validated by well-designed and long-term RCTs. As it was known robotic assisted system may be a better alternated tool for surgeon compared laparoscope. It could provide solid figure, clear anatomy margin, and less blood loss. However, non-concordance was gained according to our assessment [80]. It may result from a lack of RCTs and heterogeneity among retrospective studies involved in the systematic reviews.
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Furthermore, there was no concordance between D1 and D2 lymphadenectomy. The conclusions formulated by different authors varied, predominately due to heterogeneity among primary studies. Interestingly, most of primary evidences on lymphadenectomy were from Asia, most of which revealed that D2 lymphadenectomy could benefit patients. While RCTs from western countries usually demonstrated D2 lymphadenectomy was inferior to D1 lymphadenectomy. A bias of Asian patients cannot be ignored here [81]. Maybe it was because higher incidence of GC made Asian surgeons more experienced on lymphadenectomy. Some recent reports illustrated that western surgeons could perform D2 lymphadenectomy with better outcomes and survival benefits after appropriate training [82, 83]. According to some subgroup analyses, D2 lymphadenectomy with spleen and pancreas preservation would benefit long time survival for GC patients. It may be due to that spleen was an immune organ, which helped to keep balance of our immune system and kill cancer cells; or, splenectomy or pancreatectomy was so complicated that may increase more complications [84]. It should be confirmed by further international RCTs. The limitations of this review of systematic reviews were as follows: 1), non-English reviews were not enrolled because of language restriction; 2), two reviewers who screened paper and extracted data were not blinded to study types and outcomes. Conclusion Systematic reviews on surgical interventions for GC displayed a relatively high methodological quality. This review of systematic review identified some significant methodological flaws in the primary studies. The primary studies had problem with blindness, randomization, allocation concealment and dropouts and withdrawals. The concordances on LAG vs. OG, LADG vs. ODG were attained, but the conclusions compared other surgical interventions varied among the reviews. More comprehensive RCTs and reasonable systematic technique were necessary to provide solid evidences. Acknowledgements Supported by National Natural Science Foundation of China (No. 81403296, 31271444 and
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Surgical interventions for gastric cancer 81201726); Science and Technology Development Program of Guangdong (No. 2012B031800115); and Science Novel Program of Guangdong Education Department (No. A2003165) and the Torch Plan of Guangzhou University of Chinese Medicine (No: XH20140105).
[8]
Disclosure of conflict of interest
[10]
[9]
None. Address correspondence to: Zun-Fu Ke, Department of Pathology, The First Affiliated Hospital, Sun Yatsen University, Guangzhou 510080, Guangdong Province, China. Tel: +86 (0)20 87755766; Fax: +86 (0)20 87331059; E-mail: [email protected]; Xinlin Chen, College of Fundamental Medical Science, Guangzhou University of Chinese Medicine, Guangzhou Higher Education Mega Center, Guangzhou 510006, Guangdong Province, P. R. China. Tel: +8620-39358036; Fax: +86-20-39358020; E-mail: [email protected]
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Original Article Surgical interventions for gastric cancer: a review of systematic reviews Weiling He1*, Jian Tu2*, Zijun Huo3, Yuhuang Li4, Jintao Peng5, Zhenwen Qiu6, Dandong Luo6, Zunfu Ke7, Xinlin Chen8 Department of Gastrointestinal and Pancreatic Surgery, Centre of Gastric Cancer, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, Guangdong Province, P. R. China; 2Musculoskeletal Center, Department of Orthopaedic Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou City 510080, Guangdong Province, China; 3Department of Endocrinology, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou City 510080, Guangdong Province, China; 4Department of Molecular & Medical Genetics, Oregon Health & Science University, 3181 S.W. Sam Jackson Park Rd. Portland, Oregon 97239, USA; 5The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou City 510080, Guangdong Province, China; 6The First Affiliated Hospital, Guangzhou university of Chinese Medicine, Guangzhou 510405, Guangdong Province, P. R. China; 7 Department of Pathology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, Guangdong Province, China; 8School of Basic Medical Sciences, Guangzhou university of Chinese Medicine, Guangzhou Higher Education Mega Center, Guangzhou 510006, Guangdong Province, P. R. China. *Equal contributors. 1
Received March 7, 2015; Accepted May 28, 2015; Epub August 15, 2015; Published August 30, 2015 Abstract: Aim: To evaluate methodological quality and the extent of concordance among meta-analysis and/or systematic reviews on surgical interventions for gastric cancer (GC). Methods: A comprehensive search of PubMed, Medline, EMBASE, the Cochrane library and the DARE database was conducted to identify the reviews comparing different surgical interventions for GC prior to April 2014. After applying included criteria, available data were summarized and appraised by the Oxman and Guyatt scale. Results: Fifty six reviews were included. Forty five reviews (80.4%) were well conducted, with scores of adapted Oxman and Guyatt scale ≥ 14. The reviews differed in criteria for avoiding bias and assessing the validity of the primary studies. Many primary studies displayed major methodological flaws, such as randomization, allocation concealment, and dropouts and withdrawals. According to the concordance assessment, laparoscopy-assisted gastrectomy (LAG) was superior to open gastrectomy, and laparoscopy-assisted distal gastrectomy was superior to open distal gastrectomy in short-term outcomes. However, the concordance regarding other surgical interventions, such as D1 vs. D2 lymphadenectomy, and robotic gastrectomy vs. LAG were absent. Conclusion: Systematic reviews on surgical interventions for GC displayed relatively high methodological quality. The improvement of methodological quality and reporting was necessary for primary studies. The superiority of laparoscopic over open surgery was demonstrated. But concordance on other surgical interventions was rare, which needed more well-designed RCTs and systematic reviews. Keywords: Gastric cancer, surgical intervention, systematic review, meta-analysis, methodological quality
Introduction Gastric cancer (GC) is the fourth most common cancer and the second leading cause of cancer-related death worldwide. Although perioperative and adjuvant chemotherapy can improve outcome of GC patients, surgery remains the only curative therapy [1, 2]. Currently, complete resection of cancer (R0) is regarded as standard and basic intervention for GC patients, especially for early or/and resectable ones [3, 4]. Since laparoscopyassisted gastrectomy (LAG) was firstly applied
in 1991, it has gained wide popularity and challenge among surgeons due to its minimal invasion. Later, robotic gastrectomy (RG) was performed in order to overcome technological disadvantages of LAG to some degree. However, LAG, RG and open surgery are still debated as to which is best for GC patients [5, 6]. In addition, controversy over extent of lymphadenectomy during GC surgery never ends. In Asia area, a D2 lymphadenectomy is recommended as standard treatment, while western surgeons would like to perform a D1 resection [7-9]. More and more systematic reviews and meta-analy-
Surgical interventions for gastric cancer sis have assessed the effectiveness among different kinds of surgery performances, along with increasing randomized clinical trials (RCTs) were conducted. Nevertheless, these reviews tend to have certain flaws and problems. Firstly, discordance among these systematic reviews is common, and methodological quality of reviews was reported as a source of discordance. Secondarily, methodological quality of primary studies within these systematic reviews varied widely, which impaired the quality of these reviews. However, a review of systematic review was introduced to solve these problems 6 years ago [10]. The review of systematic review is a systematic process that can help reviewers reach reasoned decisions about the incorporation of existing systematic reviews on a topic-by-topic basis. Thus, well-designed review of systematic reviews on various surgery strategies for GC patients is needed. The aim of this study is to evaluate the methodological quality of systematic reviews and primary studies in the field of GC surgery, as well as the concordance among these systematic reviews. Methods Article identification A comprehensive search of databases, including PubMed, Medline, EMBASE, the Cochrane library and the DARE database, was conducted using the searching terms of gastric cancer, surgery and systematic review/meta-analysis. The related article function was also used to broaden the search. Additional studies were manually searched in the reference of all retrieved articles. The last searching date was April 29, 2014. Two authors (He WL and Tu J) independently screened the title and abstract to determine potential eligibility for this review. When discrepancies occurred, consensus was achieved after further discussion. Article selection The inclusion criteria were defined as follows: (1) the article must be systematic review and/ or meta-analysis; (2) reviews focused on surgical interventions for GC patients; (3) reviews reporting the efficacy; (4) reviews published in English. Narrative reviews and systematic reviews concentrating on chemotherapy for GC patients were excluded. When the same review group reported duplicate papers on the same topic, the most informative and well-designed one will be chose. 13658
Data extraction Two authors (Ke ZF and Hou ZJ) independently extracted and summarized the data for the following parameters: authors, publication year, publish journal, types of GC patients, and types of intervention (number of treatment group and control group), number and design of primary studies, outcomes. When differences among outcomes existed, the systematic review will be classified according to the primary outcome. Each intervention-specific conclusion reported in a systematic review was classified as “benefit”, “inconclusive”, “no benefit”. When the primary outcomes (including overall complications, operation time, estimated bold loss survival, or survival time) were positive between different surgical interventions, this conclusion was regarded as “benefit”. While the primary outcomes were negative between different surgical interventions, this conclusion was regarded as “no benefit”. Additionally, when the authors of the systematic review cannot draw the conclusions, the tag of “inconclusive” was given to this review. Once more than 75% agreement was reached, concordance between reviews with similar interventions can be set [11]. We contacted the author for detailed information if relevant information was unclear or missing. Quality assessment An adapted scoring approach based on the Oxman and Guyatt scale was used to evaluate the quality of systematic reviews [12, 13]. The scale consisted of 9 items: search methods used to find evidence (Item 1), scope of search (Item 2), criteria for inclusion and exclusion (Item 3), criteria for avoiding bias (Item 4), reporting of criteria for assessing the validity of primary studies (Item 5), assessing the validity of primary studies using appropriate criteria (Item 6), methods of combining the data (Item 7 and Item 8), and conclusions supported by the data or analysis reported in the review (Item 9). The score of each item ranged from 0 to 2 points, resulting in a maximum score of 18 points. High quality was defined when the scores ≥ 14. Moderate quality was defined between scores 11 to 13; while low quality was defined with scores ≤ 10. The items, including randomization, allocation concealment, baseline comparability, blinding (patients, health care providers, data collectors and outcome assessors), dropouts and withdrawals, adverse events, and contamination and cointervention Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer
Figure 1. Selection of studies for inclusion in the review of systematic reviews.
were used to assess the methodological quality of primary studies within the included systematic reviews. Data analysis The SPSS (Version 17; SPSS Inc) software was performed to analyze data and outcomes. The quality scores ware described by mean, while the characteristics were presented as frequency and percentage. Result Data identification and characteristics of included systematic reviews A total of 2104 articles were identified by comprehensive search, of which 2039 were exclud13659
ed based on titles and abstracts screening. 63 Articles were eligible for full text appraising, after which, 6 systematic reviews were excluded because of incomplete data provided in the studies [14-19]. At least, 56 systematic reviews were included [20-75] (Figure 1). Table 1 showed the characteristics of the eligible reviews. The majority of these systematic reviews were focused on 4 types of interventions: LAG vs. open gastrectomy (OG) (15 reviews); laparoscopy-assisted distal gastrectomy (LADG) vs. open distal gastrectomy (ODG) (13 reviews); D1 lymphadenectomy vs. D2 lymphadenectomy (8 reviews); RG vs. LAG (3 reviews). In terms of patients, 12 of 56 included reviews only involved the specific surgical treatment for early gastric cancer (EGC), and 8 of 56 included reviews only involved the specifInt J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Table 1. The characteristic of the eligible reviews Study
Types of No. of primary patients studies (RCTs)
Intervention (treatment vs. control)
No. of patients Outcomes (treatment vs. control)
Wang WZ 2014
GC
18 (0)
LAG vs. OG
955 vs. 1358
OT, EBL, LND, PTM, PM, TLD, TFF
Ye LY 2013
AGC
7 (1)
LAG vs. OG
365 vs. 450
LND, PMM, CRR
Chen K 2013
GC
15 (2)
LAG vs. OG
1327vs. 1192
Shen H 2013
GC
8 (8)
LAG vs. OG
409 vs. 752
PMM, OC, LND
Xiong JJ 2013a
GC
15 (0)
LAG vs. OG
811 vs. 1211
OT, EBL, OC, PMM, TFF, TLD, HS
Wang W 2013
GC
8 (0)
LAG vs. OG
599 vs. 939
OT, EBL, LND, HS
Zhang CD 2013
EGC
16 (5)
LAG vs. OG
919 vs. 746
OT, WL, EBL, LND, TFF, TLD, CRR, HS, OC
Choi YY 2013
AGC
10 (1)
LAG vs. OG
859 vs. 960
DFS, SR
Jiang L 2013a
EGC
8 (8)
LAG vs. OG
402 vs. 382
OT, EBL, PMM, OC, LND, HS, ALS, OS
Haverkamp L 2013
GC
8 (0)
LAG vs. ODG
314 vs. 384
OT, EBL, HS, OC
Sun JF 2012
GC
8 (8)
LAG vs. OG
402 vs. 380
EBL, TFF, TLD, OC, HS, LND, WL
Martínez-Ramos D 2011
AGC
7 (2)
LAG vs. OG
174 vs. 278
OT, EBL, HS, SR, LND
Liang YC 2011
EGC
6 (6)
LAG vs. OG
343 vs. 325
OT, EBL, WL, OC, TFF, TLD, HS, LND
Wei HB 2011
GC
10 (1)
LAG vs. OG + D2
495 vs. 544
OT, EBL, LND, HS, TFF, OC, SR
Wang Y 2013
EGC
8 (8)
LADG vs. ODG
323 vs. 306
OT, EBL, LND, OC, HS, TLD
Qiu JG 2013
AGC
7 (0)
LADG vs. ODG
626 vs. 645
OT, EBL, LND, TLD, TFF, OC, SC, PTM
Zeng YK 2012
EGC
22 (5)
LADG vs. ODG
1596 vs. 1815
Viñuela EF 2012
GC
6 (6)
LADG vs. ODG
343 vs. 323
PMM, OC, LND, OT, EBL, HS
Ohtani H 2011
GC
5 (5)
LADG vs. ODG
164 vs. 162
OT, EBL, LND, TLD, HS, OC,PMM, CRR
Peng JS 2010
EGC
6 (6)
LADG vs. ODG
107 vs. 111
OT, EBL, OC, TFF, HS
Ohtani H 2010
EGC
4 (4)
LADG vs. ODG
323 vs. 306
OT, EBL, LND, TLD, HS, OC, CRR, PMM
Yakoub D 2009
EGC
12 (3)
LADG vs. ODG
516 vs. 435
5-year SR, PMM, LND, HS, RR, OC
Chen XZ 2009
EGC
6 (6)
LADG vs. ODG
323 vs. 306
LND, OT, EBL, PMM, OC
Memon MA 2008
GC
4 (4)
LADG vs. ODG
80 vs. 82
Hosono S 2006
GC
16 (4)
LADG vs. ODG
837 vs. 774
PMM, CRR, 5-year SR
Ding J 2012
GC
8 (0)
LADG vs. ODG + D2
510 vs. 550
OT, EBL, LND, TFF, HS, OC, PMM, CRR
Jiang L 2014
GC
8 (8)
D1 vs. D2
1042 vs. 1002
PMM, 5-year SR, ALS, RR, WI, hemorrhage rate
Jiang L 2013b
GC
12 (8)
D1 vs. D2
1606 vs. 1558
SR, RFS
Memon MA 2011
GC
6 (6)
D1 vs. D2
946 vs. 930
HS, OC, ALS, RR, PMM
Yang SH 2009a
GC
8 (8)
D1 vs. D2
907 vs. 875
PMM, OT, EBL, LND, HS, TLD
Yang SH 2009b
GC
5 (5)
D2 vs. D3
599 vs. 588
OT, PMM, 5-year SR
Lustosa SAS 2008
GC
5 (5)
D1 vs. D2 or D3
791 vs. 758
TLD, TFF, ALS, OC, HS, PMM
McCulloch P 2004
GC
19 (6)
D1 vs. D2
580 vs. 531
PMM, OC, 5-year SR
Seevaratnam R 2012
GC
5 (5)
D1 lymph node dissection vs. D2 lymph node dissection
845 vs. 797
5-year SR, PMM, RR
Liao GX 2013a
GC
4 (0)
RG vs. OG
520 vs. 5260
OT, EBL, HS, OC, LND, PMM, WI, ALS
Liao GX 2013b
GC
7 (0)
RG vs. LAG
762 vs. 1473
OT, EBL, HS, OC, PTM,
Xiong J 2013
GC
9 (0)
RG vs. LAG
736 vs. 1759
EBL, TLD, LND, PTM, PMM, ASL, TFF, HS
Xiong BH 2012
GC
3 (0)
RG vs. LAG
268 vs. 650
OT, OC, EBL, LND, HS, PMM
13660
OT, OT, EBL, LND, PTM, TFF, TLD, HS, OC, PMM
LND, OT, HS, OC, CRR, SR
OT, PMM, 5-year SR
Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Sun J 2013
AGC
14 (0)
Palliative gastrectomy vs. non-gastrectomy
1461 vs. 1542
Xiong JJ 2013 b
GC
3 (3)
R-Y gastrojejunostomy vs. B-I anastomosis after distal gastrectomy
238 vs. 240
OS OT, EBL, HS, ALS, BR, RG, DS, RE
Kim DG 2013
GC
3 (0)
ICBI with LADG vs. ECBI with LADG
341 vs. 457
OT, TFF, HS
Ding J 2013
GC
8 (8)
Gastrointestinal decompression vs. no gastrointestinal decompression
482 vs. 477
HS, TFF, OC, PMM
Lian JJ 2012
EGC
9 (0)
EMR vs. ESD
2053 vs. 1495
ERR, HCRR, OC, OT, CRR
Park YM 2011
EGC
12 (0)
EMR vs. ESD
2072 vs. 1734
ERR, EBL, OT, PMM, complete resection, perforation
Roberts P 2012
GC
8 (0)
Gastrectomy + PD vs. Gastrectomy
132 vs. 260
OC, PMM, ALS
Wen L 2012
GC
8 (1)
TG vs. PG
728 vs. 349
SR, PMM, CRR
Wang Z 2011
GC
4 (4)
Drainage vs. No drainage
220 vs. 218
PMM, OC, RR, WI, ALS, OT, HS
Liu HP 2011
AGC
5 (5)
Drainage vs. No drainage
218 vs. 220
WI, PMM, SR, SC, IA
Zong L 2011
GC
12 (12)
Roux-en-Y with a pouch vs. without a pouch
506 vs. 512
DS, BR, RE, QOL
Zheng B 2011
GC
3 (3)
D2 lymphadenectomy vs. D4 lymphadenectomy
528 vs. 539
5-year SR, PMM, RR, OT, LND
Zorcolo L 2011
EGC
6 (6)
MIDG vs. ODG
343 vs. 323
OT, EBL, LND, HS, TFF, TLD, OC
Bracale U 2011
GC
9 (1)
TLG vs. OG
828 vs. 664
OT, EBL, TFF, LND, PMM, HS
Chen XZ 2010
AGC
3 (3)
D2 + PAND vs. D2
528 vs. 539
5-year SR, PMM
Wang Z 2010
AGC
8 (4)
D2 + PAND vs. D2
1169 vs. 852
5-year SR, PMM, OT, EBL
Yang K 2009
GC
3 (3)
Gastrectomy plus splenectomy vs. gastrectomy alone
231 vs. 235
5-year SR, PMM, LND, HS, RR
Yang Z 2008
GC
5 (5)
Nasogastric or nasojejunal decompression vs. no decompression
361 vs. 356
OT, EBL, HS, LND, OC, CRR, TLD, PMM
GC: gastric cancer; AGC: advanced gastric cancer; EGC: early gastric cancer. D1: D1 lymphadenectomy; D2: D2 lymphadenectomy; D3: D3 lymphadenectomy; D4: D4 lymphadenectomy; ECBI: extracorporeal Billroth I; ESD: endoscopic submucosal dissection; EMR: endoscopic mucosal resection; ICBI: intracorporeal Billroth I; LADG: laparoscopy-assisted distal gastrectomy; LAG: laparoscopy-assisted gastrectomy; MIDG: minimally invasive distal gastrectomy; MVR: multivisceral resection; ODG: open distal gastrectomy; OG: open gastrectomy; PAND: para-aortic nodal dissection; PG: proximal gastrectomy; RG: robotic gastrectomy; TG: total gastrectomy; TLG: totally laparoscopic gastrectomy; ALS: anastomotic leakage and stricture; BR: bile reflux; CRR: cancer recurrence rate; DS: dumping symptoms; EBL: estimated bold loss; ERR: en bloc resection rate; HCRR: histologic curative resection rate; HR: survival rate; HS: hospital stay; IA: intra-abdominal abscess; LND: lymph node dissection; OC: overall complications; OT: operation time; PMM: postoperative mortality and morbidity; PTM: proximal tumor margin; QOL: quality of life; RFS: recurrence free survival; RR: re-operation rate; RG: remnant gastritis; RE: reflex esophagitis; SR: survival rate; TLD: time to liquid diet; TFF: Time to first flatus; WL: wound lengths; WI: wound infection.
Table 3. The number of primary studies achieving the quality criteria Randomization Primary studies % Reviews
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118/284 41.5 36
Allocation Baseline Patients concealment comparability blinded 46/149 30.9 33
176/219 80.4 37
11/379 2.9 33
Health care providers blinded 0/284 0.0 33
Data collectors blinded 0/284 0.0 33
Outcome Dropouts and assessors withdrawals blinded 4/284 1/159 1.4 0.6 33 20
Reporting adverse events 209/299 69.9 27
Contamination or cointervention 25/38 65.8 6
Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Table 2. The numbers of the reviews based on the adapted Oxman and Guyatt scale (n = 56) Items Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9
2 55 50 53 34 48 46 55 54 56
Score 1 1 6 3 20 2 2 0 1 0
0 0 0 0 2 6 7 1 1 0
Mean score 1.9 1.8 1.9 1.3 1.6 1.5 1.9 1.9 2.0
ic surgical treatment for advanced gastric cancer (AGC), while others involved different types of gastric cancer. The median number of patients involved in the reviews was 1459.8, ranged from 162 to 5787. The median of that in treatment group were 652.4, while the median of that in control group were 748.7. The median number of primary studies included in the reviews was 8.25, varied from 3 to 22, 43.5% of which was RCTs. Methodological quality of systematic reviews Tables 2 and 5 outlined the results of the methodological quality assessment for 56 systematic reviews using the adapted the Oxman and Guyatt scale. The average score of all reviews was 15.9, ranged from 7 to 18. 45 of the included reviews (80.4%) were with high quality (mean score ≥ 14), 8 of the reviews (14.3%) were with moderate quality (mean score between 11 and 13), while other 3 reviews (5.4%) were with low quality (mean score ≤ 10). The most common flaws were criteria for avoiding bias (Item 4), reporting of criteria for assessing the validity of primary studies (Item 5), assessing the validity of primary studies using appropriate criteria (Item 6). The overall agreement between the two reviewers regarding quality evaluation was 89.3%, indicating good initial agreement. 100% agreement was attained after a senior investigator was consulted. Methodological quality of primary studies Table 3 elucidated the results of methodological quality assessment of primary studies, which contained the total number and percent13662
age of primary studies that used quality criteria to assess the risk of bias. Randomization and the bias of baseline comparability were relatively most frequently evaluated (36 and 37 reviews respectively), and were achieved in 41.5% and 80.4% of primary studies. Only 33 systematic reviews reported allocation concealment, patients blinded, health care provider blinded, data collectors blinded, outcome assessors blinded, and a paucity of primary studies (< 5%) within them achieved these 5 criteria, except the allocation concealment (30.9%). Only 20 systematic reviews assessed the bias of dropouts and withdrawals, with 0.6% primary studies attained it. Additionally, 27 of 56 systematic reviews evaluated the bias of reporting adverse events, and 69.9% primary studies obtained it. However, only 6 reviews evaluated the contamination or cointervention, and 65.8% of primary studies achieved it. Concordance among reviews The concordance among reviews was summarized in Table 4, which is organized according to types of interventions. The difference between LAG and OG was analyzed in 15 systematic reviews, all of which beneficial conclusions were reported. Therefore, there is concordance among reviews regarding the effectiveness between LAG and OG. The similar results were also demonstrated on LADG vs. ODG. In addition, concordance was also concluded on endoscopic submucosal dissection (ESD) vs. endoscopic mucosal resection (EMR), D2 lymphadenectomy + Para-aortic nodal dissection (PALN) vs. D2 lymphadenectomy, and decompression vs. no decompression after gastrectomy. Nevertheless, there was no concordance in conclusion about the effectiveness between D1 vs. D2 lymphadenectomy, and RG vs. LAG. As for EGC, 9 reviews focused on the efficacy of laparoscopic surgery and conventional open surgery, and concordance existed. In terms of AGC, 4 reviews discussed the oncologic safety of LAG over OG. All of them have gained the conclusion that LAG was not inferior to OG for AGC, suggesting that concordance was illustrated. Discussion A review of reviews is regarded as a method to evaluate trend in methodological quality in a clinical area [76-78]. In this review of systematic reviews on surgical interventions for GC, we Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Table 4. The concordance about efficacy among the reviews Specific Intervention
No. of Reviews
Conclusion Review Article Benefit
Inconclusive
No benefit
consensus
LAG vs. OG
15
15
0
0
yes
LADG vs. ODG
13
12
1
0
Yes
D1 vs. D2
8
4
4
0
No
RG vs. LAG
3
2
1
0
No
ESD vs. EMR
2
2
0
0
Yes
D2 + PAND vs. D2
2
0
0
2
Yes
Decompression vs. no decompression
2
0
0
2
Yes
Drainage vs. no drainage
2
1
1
0
No
R-Y gastrojejunostomy vs. B-I anastomosis after distal gastrectomy
2
1
1
0
No
ICBI vs. ECBI
2
1
1
0
#
MVR vs. No MVR
1
1
0
0
#
RG vs. OG
1
0
1
0
#
TG vs. PG
1
1
0
0
#
D4 vs. D2
1
1
0
0
#
D2 vs. D3
1
1
0
0
#
#: means unable to assess concordance; D1: D1 lymphadenectomy; D2: D2 lymphadenectomy; D3: D3 lymphadenectomy; D4: D4 lymphadenectomy; ECBI: extracorporeal Billroth I; ESD: endoscopic submucosal dissection; EMR: endoscopic mucosal resection; ICBI: intracorporeal Billroth I; LADG: laparoscopy-assisted distal gastrectomy; LAG: laparoscopy-assisted gastrectomy; MIDG: minimally invasive distal gastrectomy; MVR: multivisceral resection; ODG: open distal gastrectomy; OG: open gastrectomy; PAND: para-aortic nodal dissection; PG: proximal gastrectomy; RG: robotic gastrectomy; TG: total gastrectomy; TLG: totally laparoscopic gastrectomy.
Table 5. The scores of Systematic Reviews Based on the adapted Oxman and Guyatt Scale Study Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9 Total Scores Wang WZ 2014 2 2 2 2 2 2 2 2 2 18 Ye LY 2013 2 2 2 2 2 2 2 2 2 18 Chen K 2013 2 2 2 1 2 2 2 2 2 17 Shen H 2013 2 2 2 2 2 2 2 2 2 18 Xiong JJ 2013a 2 2 2 2 2 2 2 2 2 18 Wang W 2013 2 2 2 2 2 2 2 2 2 18 Zhang CD 2013 2 2 2 2 2 2 2 2 2 18 Choi YY 2013 2 2 2 2 2 2 2 2 2 18 Jiang L 2013a 2 2 2 2 2 2 2 2 2 18 Haverkamp L 2013 2 2 2 1 2 2 2 2 2 17 Sun JF 2012 2 1 1 0 0 0 2 2 2 10 Martínez-Ramos D 2011 1 2 1 1 1 0 2 2 2 12 Liang YC 2011 2 2 2 1 2 2 2 2 2 17 Wei HB 2011 2 2 2 1 0 0 2 2 2 13 Wang Y 2013 2 2 2 2 2 2 2 2 2 18 Qiu JG 2013 2 2 2 1 2 2 2 2 2 17 Zeng YK 2012 2 2 2 0 2 1 2 2 2 15 Viñuela EF 2012 2 2 2 1 2 2 2 2 2 17 Ohtani H 2011 2 1 1 1 0 0 2 2 2 11 Peng JS 2010 2 2 2 0 2 0 2 2 2 14 Ohtani H 2010 2 1 1 1 0 0 2 2 2 11 Yakoub D 2009 2 2 2 1 2 2 2 2 2 17 Chen XZ 2009 2 2 2 1 2 2 2 2 2 17 Memon MA 2008 2 1 1 1 2 2 2 2 2 15 Hosono S 2006 2 1 2 1 0 0 2 2 2 12
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Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer Ding J 2012 Jiang L 2014 Jiang L 2013b Memon MA 2011 Yang SH 2009a Yang SH 2009b Lustosa SAS 2008 McCulloch P 2004 Seevaratnam R 2012 Liao GX 2013a Liao GX 2013b Xiong J 2013 Xiong BH 2012 Sun J 2013 Xiong JJ 2013b Kim DG 2013 Ding J 2013 Lian JJ 2012 Roberts P 2012 Wen L 2012 Wang Z 2011 Liu HP 2011 Zong L 2011 Zheng B 2011 Zorcolo L 2011 Park YM 2011 Bracale U 2011 Chen XZ 2010 Wang Z 2010 Yang K 2009 Yang Z 2008 Mean Score
2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 1.9
2 2 2 2 2 2 2 2 2 1 2 2 2 2 2 1 1 2 2 1 2 2 2 2 1 2 2 1 2 2 1 1.8
2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 1.9
not only assessed the methodological quality of included reviews and primary studies, but also appraised the concordance among included reviews. The systematic reviews identified in the current study showed a wide variety of surgical treatments on GC. Regarding the number of included systematic reviews, there is a growing trend of published systematic review about surgical intervention for GC. This may be related with more RCTs conducted and reported in recent year, and more widely accepted consensus on the standard assessment and reporting during the manufacture of a systematic reviews. The overall quality of included systematic reviews was relatively high. However, there were still
13664
1 2 2 0 1 1 1 2 1 2 2 2 1 2 1 1 1 1 1 1 2 1 1 1 1 2 2 1 2 2 1 1.3
2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 0 2 2 0 2 2 1 0 2 0 2 2 2 2 2 2 1.6
2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 0 2 2 0 1 2 2 0 2 0 2 2 1 2 2 2 1.5
2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 2 1.9
2 2 2 0 2 2 2 2 2 1 2 2 2 2 2 2 2 2 0 2 2 2 2 2 2 2 2 2 2 2 2 1.9
2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2.0
17 18 18 7 17 17 16 18 17 16 18 18 17 18 17 12 16 17 9 15 18 16 13 17 12 18 18 15 18 18 16 15.9
some obvious flaws and problems. Firstly, the use of criteria for avoiding bias and assessing the validity of primary studies should be emphasized. Comprehensive evaluation of validity for primary studies would make readers easier to extrapolate the conclusions. Secondarily, there was a paucity of long term outcomes, such as overall survival (OS), disease free survival (DFS), in the majority of included systematic reviews. OS and DFS were widely accepted as the standard endpoint to evaluate the effectiveness of the special intervention for cancer patients. The methodological quality of the primary studies still needed improvement, which could fundamentally affect the quality and conclusion of
Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer systematic reviews. The blindness of patients, health care providers, data collectors, and outcome assessors were achieved rarely in primary studies, which could be determined factors of information bias. However, it is hard to deal with the blindness of patients, data collectors, and surgeons as for surgical interventions. The blindness was nor regarded as an important part for surgical interventions. Therefore, randomization, allocation concealment and dropouts and withdrawals should be improved in further RCTs. On one hand, more well-designed RCTs and long-term follow-up data are required to assess the recurrence and survival of GC patients. On the other hand, more comprehensive and reasonable analyses methods for retrospective data should be developed. Additionally, more rigorous quality assessment criteria and reporting principle should be considered in the primary studies in future, such as Physiotherapy Evidence-Based Database Quality Assessment Scale and Consolidated Standards for Reporting Trials (CONSORT) [79]. From the systematic review compared LAG with OG for GC, concordance was drawn. It was generally accepted that LAG could be performed safely with less complications and a shorter hospital stay, despite longer operation duration. Also, similar results were demonstrated on estimated bold loss (EBL), survival rate between LAG and OG. Nevertheless, this concordance was established on the systematic reviews, the majority of which focused on the short term outcomes of LAG or OG. The long term survival data were rarely pooled in the included systematic reviews. The similar results were also achieved on the comparison between LADG with ODG. Whether the laparoscopic surgery could satisfy oncologic safety and surgical adequacy, regarding radical resection and management of complicated vascular structure, needed to be validated by well-designed and long-term RCTs. As it was known robotic assisted system may be a better alternated tool for surgeon compared laparoscope. It could provide solid figure, clear anatomy margin, and less blood loss. However, non-concordance was gained according to our assessment [80]. It may result from a lack of RCTs and heterogeneity among retrospective studies involved in the systematic reviews.
13665
Furthermore, there was no concordance between D1 and D2 lymphadenectomy. The conclusions formulated by different authors varied, predominately due to heterogeneity among primary studies. Interestingly, most of primary evidences on lymphadenectomy were from Asia, most of which revealed that D2 lymphadenectomy could benefit patients. While RCTs from western countries usually demonstrated D2 lymphadenectomy was inferior to D1 lymphadenectomy. A bias of Asian patients cannot be ignored here [81]. Maybe it was because higher incidence of GC made Asian surgeons more experienced on lymphadenectomy. Some recent reports illustrated that western surgeons could perform D2 lymphadenectomy with better outcomes and survival benefits after appropriate training [82, 83]. According to some subgroup analyses, D2 lymphadenectomy with spleen and pancreas preservation would benefit long time survival for GC patients. It may be due to that spleen was an immune organ, which helped to keep balance of our immune system and kill cancer cells; or, splenectomy or pancreatectomy was so complicated that may increase more complications [84]. It should be confirmed by further international RCTs. The limitations of this review of systematic reviews were as follows: 1), non-English reviews were not enrolled because of language restriction; 2), two reviewers who screened paper and extracted data were not blinded to study types and outcomes. Conclusion Systematic reviews on surgical interventions for GC displayed a relatively high methodological quality. This review of systematic review identified some significant methodological flaws in the primary studies. The primary studies had problem with blindness, randomization, allocation concealment and dropouts and withdrawals. The concordances on LAG vs. OG, LADG vs. ODG were attained, but the conclusions compared other surgical interventions varied among the reviews. More comprehensive RCTs and reasonable systematic technique were necessary to provide solid evidences. Acknowledgements Supported by National Natural Science Foundation of China (No. 81403296, 31271444 and
Int J Clin Exp Med 2015;8(8):13657-13669
Surgical interventions for gastric cancer 81201726); Science and Technology Development Program of Guangdong (No. 2012B031800115); and Science Novel Program of Guangdong Education Department (No. A2003165) and the Torch Plan of Guangzhou University of Chinese Medicine (No: XH20140105).
[8]
Disclosure of conflict of interest
[10]
[9]
None. Address correspondence to: Zun-Fu Ke, Department of Pathology, The First Affiliated Hospital, Sun Yatsen University, Guangzhou 510080, Guangdong Province, China. Tel: +86 (0)20 87755766; Fax: +86 (0)20 87331059; E-mail: [email protected]; Xinlin Chen, College of Fundamental Medical Science, Guangzhou University of Chinese Medicine, Guangzhou Higher Education Mega Center, Guangzhou 510006, Guangdong Province, P. R. China. Tel: +8620-39358036; Fax: +86-20-39358020; E-mail: [email protected]
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