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World Journal of Surgical Oncology logoLink to World Journal of Surgical Oncology
. 2016 Dec 8;14:304. doi: 10.1186/s12957-016-1062-7

Minimally invasive oesophagectomy versus open esophagectomy for resectable esophageal cancer: a meta-analysis

Waresijiang Yibulayin 1, Sikandaer Abulizi 1, Hongbo Lv 1, Wei Sun 1,✉
PMCID: PMC5143462  PMID: 27927246

Abstract

Background

Open esophagectomy (OE) is associated with significant morbidity and mortality. Minimally invasive oesophagectomy (MIO) reduces complications in resectable esophageal cancer. The aim of this study is to explore the superiority of MIO in reducing complications and in-hospital mortality than OE.

Methods

MEDLINE, Embase, Science Citation Index, Wanfang, and Wiley Online Library were thoroughly searched. Odds ratio (OR)/weighted mean difference (WMD) with a 95% confidence interval (CI) was used to assess the strength of association.

Results

Fifty-seven studies containing 15,790 cases of resectable esophageal cancer were included. MIO had less intraoperative blood loss, short hospital stay, and high operative time (P < 0.05) than OE. MIO also had reduced incidence of total complications; (OR = 0.700, 95% CI = 0.626 ~ 0.781, P V < 0.05), pulmonary complications (OR = 0.527, 95% CI = 0431 ~ 0.645, P V < 0.05), cardiovascular complications (OR = 0.770, 95% CI = 0.681 ~ 0.872, P V < 0.05), and surgical technology related (STR) complications (OR = 0.639, 95% CI = 0.522 ~ 0.781, P V < 0.05), as well as lower in-hospital mortality (OR = 0.668, 95% CI = 0.539 ~ 0.827, P V < 0.05). However, the number of harvested lymph nodes, intensive care unit (ICU) stay, gastrointestinal complications, anastomotic leak (AL), and recurrent laryngeal nerve palsy (RLNP) had no significant difference.

Conclusions

MIO is superior to OE in terms of perioperative complications and in-hospital mortality.

Keywords: Minimally invasive esophagectomy, Open esophagectomy, Complications, Mortality

Background

A global incidence of esophageal cancer has increased by 50% in the past two decades. Each year, around 482,300 people are diagnosed with esophageal cancer, and 84.3% die of the disease worldwide [1, 2]. At present, the primary method of treating patients with esophageal cancer has been surgery. However, the traditional open esophagectomy (OE) procedure has high complication rates resulting in significant morbidity and mortality [3, 4]. Various studies showed in-hospital mortality between 1.2 and 8.8% [4–7], even as high as 29% [8].

Minimally invasive oesophagectomy (MIO), which was first described in the 1990s [9, 10], was attributed to be superior in reducing postoperative outcomes, without compromising oncological outcomes and avoiding thoracotomy and laparotomy. The basis of minimally invasive techniques in esophageal surgery is to maintain the therapy effectiveness and quality of traditional operations, while reducing perioperative injury. Nevertheless, the real benefits of minimally invasive approach for esophagectomy are still controversial [11–13]. A number of meta-analyses and even randomized controlled trials demonstrated MIO to be superior in reducing risk of postoperative outcomes, but their results are not very consistent, especially on the issue of in-hospital mortality [14–30]. Furthermore, these studies ignored preoperative clinical data and other Chinese relevant literatures. We, therefore, performed a meta-analysis combining the relevant publications and comprehensively assess the superiority of MIO.

Materials and methods

Search strategy

MEDLINE, Embase, Science Citation Index, Wanfang, and Wiley Online Library were thoroughly searched with terms “Minimally Invasive Esophagectomy” or “Open Esophagectomy,” “Esophagectomy,””MIE,” “laparasc,” “thoracosc,” “VATS,” “transhiatal” (date until May 2016). Relevant literatures containing full text were back tracked thoroughly, while abstracts and unpublished reports were excluded.

Selections of studies

Inclusion criteria

The inclusion criteria are as follows: (1) randomized or non-randomized controlled studies with parallel controls, (2) comparison on OE versus MIO, (3) sufficient data of estimated odds ratios (ORs)/weighted mean difference (WMD) and 95% confidence intervals (CIs).

Exclusion criteria

The exclusion criteria are as follows: (1) studies that were not compared or case report, (2) incomplete literature, and (3) overlapped studies.

Data extraction

Two investigators read all the included literatures carefully and extracted all the data, such as first author, published year, numbers of case and controls, outcomes of interest, etc. If two investigators have divergent ideas on any data, the third investigator would be asked to check and reach consensus on the data.

Outcomes of interest

  1. Definition of MIO was thoracoscopic/laparotomy-assisted esophagectomy, hybrid minimally invasive esophagectomy, total thoracoscopic/hand-assisted thoracotomy, hand-assisted laparotomy, or minilaparotomy/laparoscopic esophagectomy.

  2. Preoperative clinical data included age, neoadjuvant therapy, comorbidity, TNM staging, and gender.

  3. Postoperative data contained operative duration, blood loss, intensive care unit (ICU) stay, hospital stay, and harvested lymph nodes.

  4. The complications are as follows. (1) Mortality included in-hospital mortality and 30-day mortality. (2) Pulmonary complications included pneumonia, respiratory failure, adult respiratory distress syndrome (ARDS), etc. (3) Cardiovascular complications included arrhythmia, heart failure, acute myocardial infarction, deep vein thrombosis, pulmonary embolism, etc. (4) Gastrointestinal complications included gastric tip necrosis, anastomotic stricture, delayed gastric emptying, gastric volvulus, etc. (5) Surgical technology related (STR) complications included splenic laceration, tracheal laceration, pneumothorax, chylothorax, hemorrhage, etc.

Statistical analysis

Data was analyzed using STATA 11 (Stata Corp LP, College Station, Texas, 2011). Fixed or random effects models [31] were used. Odds ratio (OR) was used for categorical variables, while weighted mean difference (WMD) was used for continuous variables, such as operative time, harvested lymph nodes, and blood loss [32]. Q test was used to check the heterogeneity among each study. If the heterogeneity was high (I 2 > 50%), Random Effects Model was used to calculate the pooled OR/WMD. Otherwise, the fixed effects model was used [33]. If the heterogeneity test was statistically significant, sensitivity analysis, subgroup analysis, and Galbraith Plot Analysis were performed to find out potential origin of heterogeneity. Egger’s Test and Begg’s Funnel Plot were used for diagnosis of potential publication bias [34]. A P value <0.05 was considered as statistical significance. Duval and Tweedie nonparametric “trim and fill” procedure was used to assess the possible effect of publication bias [35].

The Newcastle Ottawa Quality Assessment Scale was used to assess the validity and quality of studies [36], as recommended in the Cochrane Handbook [37]. This scale assigns a star rating based on pre-specified criteria. A total number of quality star ranged from one (low quality) to nine (high quality). A maximum of one star can be attained for each category, except comparability, which has maximum of two stars. The more the stars, the higher is the quality of study.

Results

Study characteristics

A flow chart of the literature search process is shown in Fig. 1. A total of 1021 unique records were identified by search strategy; 917 records were excluded; 16 studies were meta-analyses or systematic overviews [14–19]; ten were review; and four were letter; nine studies did not compare the outcomes of interest [3, 5–12], and six studies were duplicate to previous study. Therefore, 57 studies containing 15,790 cases (both MIO and OE) were included in this meta-analysis [30, 38–93].

Fig. 1.

Fig. 1

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Study flow chart explaining the selection of 57 studies included in the meta-analysis

Preoperative clinical data as well as quality star ranging from 6 to 8 are shown in Table 1. Of 15,790 cases, 5235 (33.2%) were MIO and 10,555 (66.8%) were OE. Thirty one studies were done in European countries and 26 in Asian countries, where 13 were from China [45–57]. Moreover, 39 studies involved total MIE, 12 studies thoracoscopic-assisted MIE (TA), and seven studies were hybrid (TA + MIE). TNM staging were reported in 40 studies (6265 cases), where 1973 patients (64.4%) in the MIO group and 1042 patients (32.5%) in the OE group were of early stage (stages I and II), mainly male (78.4% (MIO) vs 68.3% (OE)).

Table 1.

Characteristics of included studies in this meta-analysis

Study Year Country Cases Gender (M) Age, years NT NOS Hybrid Preoperative comorbidity (MIO/OE) TNM stage (MIO/OE)
(MIO/OE) (MIO/OE) (MIO/OE) (MIO/OE) Cardiovascular Pulmonary Diabetes 0 + I + II III + IV
Nguyen 2000 USA 18/36 7/29 64 ± 12/67 ± 8 9/9 6 MIE NR NR NR NR NR
Osugi 2003 Japan 77/72 64/57 63.7 ± 9 · 6/64 · ±9 · 3 NR 7 TA NR NR NR NR NR
Kunisaki 2004 Japan 15/30 12/21 62.3 ± 8.1/63 ± 6 NR 6 MIE NR NR NR NR NR
Bernabe 2004 USA 17/14 16/11 63.9 ± 13.5/64.1 ± 10.7 NR 6 TA NR NR NR NR NR
Van den Broek 2004 Netherlands 25/20 19/14 63 ± 8/64 ± 8 17/4 7 TA NR NR NR 8/10 17/10
Braghetto 2006 Chile 47/119 NR NR 0/0 8 MIE NR NR NR 41/80 6/39
Bresadola 2006 Italy 14/14 8/13 61.9 ± 7.7/59.3 ± 10.9 NR 6 MIE NR NR NR 11/6 3/8
Shiraishi 2006 Japan 116/37 94/31 61.5 ± 8.1/66.5 ± 9.3 26/10 7 Hybrid NR NR NR NR NR
Smithers 2007 Australia 332/114 267/104 64 (27–85)/62.5 (29–81) 136/29 8 Hybrid 76/22 NR 27/4 192/36 118/75
Benzoni 2007 Italy 9/13 6/11 63.6 ± 2.6/60.2 ± 2.4 6/6 8 TA NR 2/4 NR 9/7 0/6
Fabian 2008 USA 22/43 16/31 63 (46–86)/61 (35–82) 9/16 7 MIE NR NR NR 14/25 7/19
Parameswaran 2009 UK 50/30 45/21 67 (47–81)/68 (47–81) 32/12 8 MIE NR NR NR 27/17 23/13
Saha 2009 UK 16/28 13/24 65 (50–80)/64 (35–78) NR 8 MIE NR NR NR NR NR
Zingg 2009 Australia 56/98 45/71 66.3 ± 1.3/67.8 ± 1.1 40/48 8 MIE 4/7 13/35 6/12 35/47 21/42
Pham 2010 USA 44/46 41/33 63 ± 8.6/61 ± 10.7 29/23 6 MIE NR NR NR 20/20 20/19
Perry 2010 USA 21/21 18/17 69 ± 8/61 ± 9 NR 7 MIE NR NR NR NR NR
Hamouda 2010 UK 51/24 44/23 62/60 44/20 7 MIE NR NR NR NR NR
Safranek 2010 UK 75/46 53/38 60 (44–77)/64(41–74) 71/34 7 Hybrid NR NR NR 31/29 44/17
Schoppmann 2010 Australia 31/31 25/21 61.5 (36–75)/58.6 (34–77) 15/7 8 MIE 6/8 10/8 1/1 18/19 13/12
Schröder 2010 Germany 238/181 198/151 61.1 (60–62)/57.8 (56–59) 144/66 6 TA NR NR NR NR NR
Mehran 2011 USA 44/44 43/40 61.0 (42–79)/62.5 (38–83) 31/30 7 MIE NR NR NR 23/21 16/20
Berger 2011 USA 65/53 51/38 61 (41–78)/62 (40–86) 28/43 6 MIE NR NR NR 52/41 13/12
Lee 2011 Japan 74/64 73/61 59.7 ± 10.3/56.6 ± 11.6 47/52 8 Hybrid NR NR NR 54/49 20/15
Nafteux 2011 Belgium 65/101 52/81 63 (41–82)/64 (29–82) NR 8 MIE 11/24 6/13 6/12 NR NR
Yamasaki 2011 Japan 109/107 87/95 64.6 ± 8.5/64.7 ± 8.0 85/68 8 TA 20/20 11/13 10/6 NR NR
Biere 2012 Netherlands 59/56 43/46 62 (34–75)/62 (42–75) 59/56 8 MIE NR NR NR 31/26 15/19
Maas 2012 Netherlands 50/50 41/33 62.5 (57–69)/65 (57–69) 23/13 8 MIE NR NR NR 19/19 31/31
Briez 2012 France 140/140 110/117 NR 67/69 8 TA NR NR NR 92/89 48/51
Kinjo 2012 Japan 106/79 87/70 62.7 ± 7.4/63.3 ± 8.6 54/11 7 MIE NR NR NR 65/45 41/34
Mamidanna 2012 UK 1155/6347 892/4870 NR NR 7 MIE 400/2234 141/782 90/598 NR NR
Sihag 2012 USA 38/76 29/61 61.4 ± 8.1/63.3 ± 9.3 25/46 7 MIE 6/16 8/13 NR 29/53 9/23
Sundaram 2012 USA 47/57 38/52 67.3 (42–79)/61.7 (34–84) 35/40 8 MIE 33/42 NR 11/14 NR NR
Tsujimoto 2012 Japan 22/27 21/21 70 ± 5.4/67 ± 10.1 8/16 6 TA NR NR NR 12/14 10/13
Javidfar 2012 USA 92/165 71/122 65 (56–74)/68 (60–74) 51/96 7 MIE 9/23 9/23 22/35 65/96 27/69
Bailey 2013 UK 39/31 32/27 65 (37–78)/62 (38–78) 33/31 7 TA NR NR NR NR NR
Ichikawa 2013 Japan 152/163 129/145 63.8 ± 8.5/64.6 ± 8.6 54/64 8 TA 23/35 21/24 26/37 101/81 51/79
Kitagawa 2013 Japan 45/47 35/40 63 (47–77)/64 (39–83) 8/11 7 MIE NR NR 8/8 NR NR
Noble 2013 UK 53/53 43/45 66 (45–85)/64 (36–81) 13/11 8 MIE NR NR NR NR NR
Parameswaran 2013 UK 67/19 47/15 64 (45–84)/64 (51–77) 50/17 7 Hybrid NR NR NR 43/8 23/11
Takeno 2013 Japan 91/166 77/147 63.7/64.2 NR 8 TA NR NR NR NR NR
Kubo 2014 Japan 135/74 111/60 64.1 ± 8.2/62.2 ± 7.2 22/4 7 Hybrid 12/3 9/7 NR 112/41 23/33
Schneider 2014 UK 19/61 46/15 62.3 (35–74)/66.7 (45–79) 7/45 6 MIE NR NR NR 16/36 2/24
Daiko 2015 Japan 31/33 28/28 66 (49–78)/65 (49–76) NR 7 MIE NR NR NR 23/32 8/1
Kauppi 2015 Finland 74/79 59/68 66 (51–85)/63 (39–82) 61/62 8 MIE 14/17 12/14 17/13 28/25 46/54
Law 1997 China 18/63 13/55 66 (43–80)/63 (36–84) NR 7 MIE NR NR NR 5/15 13/45
Chen 2010 China 67/38 45/25 61 ± 7/66 ± 6 NR 7 MIE 15/4 10/3 9/2 42/15 25/23
Gao 2011 China 96/78 89/70 58.5 ± 7.3/59.1 ± 6.4 NR 6 MIE NR NR NR 54/40 42/38
Shen 2012 China 76/71 52/50 60.9 ± 9/62.6 ± 8.7 NR 6 MIE NR NR NR 41/44 35/27
Liu 2012 China 98/105 67/71 62.3 ± 10.1/65.8 ± 7.6 NR 6 MIE 13/18 40/37 6/8 51/43 47/62
Mao 2012 China 34/38 28/26 62/60 NR 6 TA NR NR NR 27/21 7/17
Wang 2012 China 260/322 194/232 61.6 ± 8.761.2 ± 8.8 37/44 6 MIE NR NR NR 201/234 59/88
MU 2014 China 176/142 116/106 60 (55–66)/59 (54–62) NR 6 MIE NR NR NR 120/109 56/33
Meng 2014 China 94/89 65/63 59.7 ± 9.3/61.1 ± 6.7 NR 7 MIE 11/14 27/31 12/10 56/50 38/39
Zhang 2014 China 60/61 48/47 62.4 ± 8/61.8 ± 8.4 NR 6 MIE NR NR NR 41/42 19/19
Chen 2015 China 59/59 42/40 57 (41–72)/56 (48–71) NR 7 MIE 4/2 1/0 2/3 56/55 3/4
Yang 2015 China 62/62 45/45 62 ± 9/62 ± 8 NR 7 MIE NR NR NR 44/43 18/19
Li 2015 China 89/318 66/227 73 (70–83)/73 (70–85) NR 7 MIE NR NR NR 64/188 25/126
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NT neoadjuvant therapy, NOS Newcastle-Ottawa quality assessment scale, MIO minimally invasive oesophagectomy, including MIE,TA, and hybrid MIE, OE open esophagectomy, MIE total minimally invasive esophagectomy, TA thoracoscopic-assisted MIE, Hybrid hybrid minimally invasive oesophagectomy

Preoperative clinical data

Fifty-seven studies reported patient’s age. There was no statistical significance between two groups after pooled analysis (WMD = −0.343, 95%CI = −1.200 ~ 0.514, P V < 0.433). Thirty-three studies (5243 cases) reported that the patients in MIE group received more neoadjuvant therapy (Table 3, pooled OR = 1.364, 95% CI = 1.042 ~ 1.785, P V = 0.024). Sixteen studies reported preoperative comorbidity, where there was no statistical significance between two groups (P V > 0.05).

Table 3.

Differences between MIO and OE surgery patients

Variables No. studies WMD/OR (95%CI) P V P Q I 2 (%) P E
Age, years 57 (n = 15790) −0.343 (−1.200, 0.514) 0.433 <0.05 68.1 0.059
NT 34 (n = 5138) 1.364 (1.042,1.785) 0.024 <0.05 73.0 0.362
Comorbidity
 Cardiovascular 16 (n = 10337) 0.913 (0.815,1.022) 0.112 0.030 44.2 0.930
 Pulmonary 15 (n = 9779) 0.949 (0.819,1.099) 0.485 0.881 0 0.722
 Diabetes 15 (n = 9983) 0.942 (0.798,1.111) 0.476 0.457 0 0.082
Operating time, min 46 (n = 6260) 24.427 (10.912,37.943) <0.05 <0.05 96.1 0.155
Blood loss, ml 40 (n = 5285) −196.060 (−255.195,-136.926) <0.05 <0.05 98.9 0.592
LN harvest 46 (n = 6390) −1.275 (−5.851,3.301) 0.585 <0.05 99.8 0.786
LOS, day 45 (n = 13899) −3.660 (−4.891,-2.428) <0.05 <0.05 86.0 0.175
ICU stay, day 27 (n = 10761) −1.599 (−2.680, −0.518) 0.004 <0.05 98.2 0.078
Complication
Total complication 35 (n = 5991) 0.700 (0.626,0.781) <0.05 0.012 38.5 0.178
Pulmonary 50 (n = 14781) 0.527 (0.431, 0.645) <0.05 <0.05 60.3 <0.05
Circulatory system 36 (n = 12883) 0.770 (0.681,0.872) <0.05 0.427 2.4 0.386
Digestive system 21 (n = 4081) 1.097 (0.835,1.442) 0.507 0.083 31.7 0.664
AL 50 (n = 7528) 1.023 (0.870,1.202) 0.785 0.304 8.5 0.018
RLNP 37 (n = 5429) 1.108 (0.917,1.339) 0.289 0.089 24.8 0.014
STR 39 (n = 5991) 0.639 (0.522,0.781) <0.05 0.918 0 0.206
Mortality 38 (n = 14132) 0.668 (0.539,0.827) <0.05 0.944 0 0.508
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NT neoadjuvant therapy, LN lymph node, LOS length of hospital stay, ICU intensive care unit, AL anastomotic leak, RLNP recurrent laryngeal nerve palsy, STR surgical technology-related, Mortality in-hospital/30-day mortality, P V the P value for pooled, P Q the P value for Q test, P E the P value for Egger’s test

Postoperative data

Forty-six studies (6260 cases) reported that operative time was higher in MIO group (Table 3, pooled WMD = 1.364, 95% CI = 10.912 ~ 37.943, P V < 0.05). Forty studies (5285 cases) reported less blood loss in MIO group (WMD = −196, 95% CI = −255.195 ~ −136.926, P V < 0.05). Duration of hospital stay (13,899 cases), including ICU stay (10,761 cases), were found to be significantly lower in MIO group (WMD = −1.599, 95% CI = (−2.680 ~ −0.518,P V < 0.05 and WMD = −3.66, 95% CI = −4.891 ~ −2.428, P V < 0.05). There was no significant difference between two groups in forty-six studies (6390 cases) reported for harvested lymph nodes (Table 3, WMD = −1.275, 95% CI = −5.851 ~ 3.301, P V = 0.585). There was significant heterogeneity in the outcome among all the indices of postoperative data. Stratified analysis was performed according to ethnicity (Asian/Caucasian); however, heterogeneity still existed in subgroups. We then gradually removed small sample size, with emphasis on not altering the overall qualitative results.

Complications

MIO and total complications

Thirty-five studies including 5991 cases reported total complications, where 41.5% (1206/2907) were allocated to MIE group and 48.2% (1486/3084) were allocated to OE group, with overall morbidity of 44.9% (2692/5991) (see Table 2).

Table 2.

Outcomes of complication in included studies

Study Total Pulmonary Circulatory system Digestive system AL RLNP STR Mortality
MIO/OE MIO/OE MIO/OE MIO/OE MIO/OE MIO/OE MIO/OE MIO/OE MIO/OE
Nguyen NR 2/6 1/1 1/2 3/4 0/4 0/1 0/1
Osugi 25/27 12/14 3/2 NR 2/1 11/9 4/4 NR
Kunisaki NR 0/1 NR NR 2/1 3/3 NR NR
Bernabe NR NR NR 7/8 NR NR NR NR
Van den Broek 14/18 2/2 NR 3/5 2/3 2/3 2/4 NR
Braghetto 18/72 7/22 0/3 4/6 3/17 0/2 1/0 3/13
Bresadola NR 1/2 1/0 NR 1/2 3/1 NR NR
Shiraishi NR 25/12 13/9 NR 12/9 42/10 NR 6/5
Smithers 207/76 106/44 60/24 83/9 17/11 8/0 25/14 7/3
Benzoni NR 0/2 NR 0/1 1/1 1/1 NR 0/1
Fabian 15/31 1/18 5/8 1/0 3/3 1/2 0/3 1/4
Parameswaran 24/15 4/2 0/3 3/1 4/1 6/0 5/4 NR
Saha 3/6 NR NR NR 2/3 NR NR 0/2
Zingg 19/20 17/33 NR NR 11/11 NR 2/2 2/6
Pham 34/27 13/9 18/16 3/1 4/5 6/0 3/10 3/2
Perry 13/17 2/3 5/8 5/4 4/6 1/2 2/5 NR
Hamouda NR 15/5 5/3 3/1 4/2 NR 3/0 NR
Safranek NR 19/13 NR 17/4 11/1 10/1 5/5 3/1
Schoppmann NR 5/17 NR 0/1 1/8 4/13 3/4 NR
Schröder NR NR NR NR 18/17 NR NR 7/11
Mehran NR 14/15 9/9 18/8 11/6 NR NR NR
Berger 31/32 10/22 1/6 NR 9/6 NR NR 5/4
Lee NR 11/20 NR NR 10/18 NR NR 4/8
Nafteux 44/61 17/47 11/13 13/6 5/10 NR 6/9 2/2
Yamasaki 26/38 7/15 3/6 0/2 6/4 17/20 3/5 0/2
Biere NR 14/35 1/1 1/0 7/4 1/8 1/1 3/1
Maas 21/33 9/13 3/6 NR 4/3 3/5 2/5 0/1
Briez 50/83 22/60 NR 6/4 8/6 NR NR 2/10
Kinjo 54/54 22/31 10/5 8/9 11/13 21/10 4/10 NR
Mamidanna NR 276/1419 165/1035 NR NR NR NR 46/274
Sihag NR 1/33 5/19 NR 0/2 NR 3/5 0/2
Sundaram 28/41 5/19 9/19 26/10 4/4 1/1 10/11 2/1
Tsujimoto 13/16 2/10 NR 1/1 7/3 2/2 1/4 1/5
Javidfar NR 9/26 29/56 19/33 5/7 3/0 22/38 3/7
Bailey NR 15/18 4/9 1/0 1/0 NR 6/15 2/2
Ichikawa 94/117 20/33 17/38 4/5 14/27 60/77 2/2 0/8
Kitagawa NR 6/14 NR NR NR NR 13/20 2/1
Noble NR 14/18 10/7 NR 5/2 NR 2/2 1/1
Parameswaran 42/12 7/2 2/1 14/2 NR 2/1 6/3 3/1
Takeno 39/69 NR NR NR NR NR NR 4/15
Kubo 57/35 13/16 NR 2/0 10/7 37/14 18/19 2/2
Schneider 7/13 NR NR NR NR NR NR 0/2
Daiko 10/12 NR NR NR 6/4 3/6 2/6 NR
Kauppi 37/48 13/15 17/27 5/14 5/5 0/4 12/11 NR
Law NR 4/15 3/16 NR 0/2 4/8 NR NR
Chen NR 7/10 NR 2/0 1/0 NR 2/1 NR
Gao 31/36 13/11 NR 7/12 7/6 2/4 1/2 2/3
Shen 32/28 5/6 9/8 1/1 16/14 7/2 2/3 0/1
Liu 22/38 5/21 4/13 3/5 2/4 3/4 3/5 1/3
Mao 14/16 0/2 1/6 0/1 8/1 5/3 NR NR
Wang 90/145 12/23 21/36 11/13 26/32 6/7 8/16 2/11
MU 28/22 6/4 NR NR 12/4 NR NR 1/1
Meng 24/41 9/24 4/11 2/2 6/7 4/4 3/4 1/4
Zhang NR 4/7 3/5 3/2 3/2 2/1 2/7 NR
Chen 14/19 2/4 3/5 NR 2/3 4/5 1/1 NR
Yang 19/31 NR NR NR NR NR NR NR
Li 32/137 8/51 9/34 2/5 19/45 18/49 4/19 3/16
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AL anastomotic leak, RLNP recurrent laryngeal nerve palsy, STR surgical technology-related, Mortality in-hospital/30-day mortality

Low heterogeneity was found among studies (I 2 = 38.5%, P Q = 0.012), so the fixed effects model was used (see Table 3). The pooled OR = 0.70, 95% CI = 0.626 ~ 0.781, P V < 0.05 indicated total complication was significantly lower in MIO group (Fig. 2). Publication bias was assessed by Egger’s Test and Begg’s Funnel Plot; no publication bias could be discovered (P E = 0.178).

Fig. 2.

Fig. 2

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Meta-analysis for MIE and total complications

MIO and pulmonary complications

Fifty studies including 14,781 cases reported pulmonary complications, where 17.1% (813/4761) were in MIO group and 22.6% (2264/10,020) were in OE group, with overall morbidity of 20.8% (3077/14,781).

There was very strong evidence of reduced risk of pulmonary complications in the MIO group (OR = 0.527, 95%CI = 0.431 ~ 0.645, P V < 0.05), with statistical heterogeneity (I 2 of 60.3%, P Q = 0.012) (Fig. 3, Table 3). In order to find out other sources of heterogeneity, Galbraith Plot Analysis was performed to identify which study results in the heterogeneity (Fig. 4). Pham et al. [52] and Mamidanna et al. [66] were outliers from the Galbraith Plot Analysis and I 2 values decreased after removing the study (OR = 0.502 95% CI = 0.425 ~ 0.592, P V < 0.05, I 2 = 26.6%, P Q = 0.05). However, the funnel plot figure (Fig. 5) showed significant statistical difference (P E < 0.05), indicating the possibility of publication bias.

Fig. 3.

Fig. 3

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Meta-analysis for MIE and pulmonary complications

Fig. 4.

Fig. 4

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Galbraith plot of MIE and pulmonary complications

Fig. 5.

Fig. 5

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Begg’s Test of MIE and pulmonary complications

MIO and mortality

Thirty-eight studies addressed the mortality (MIO 4379 vs OE 9753). The mortality risk was 3.8% (124/4379) in MIO group versus 4.5% (437/9753) in OE group. There was very strong evidence of reduced mortality in MIO group (OR = 0.668, 95% CI = 0.539 ~ 0.827, P V < 0.05), with statistical homogeneity (I 2 of 0%, P Q = 0.944) (Fig. 6).

Fig. 6.

Fig. 6

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Meta-analysis for MIE and Mortality

MIO and cardiovascular complications

Thirty-six studies reported cardiovascular complications (MIO 3745 vs OE 9138). There was very strong evidence of reduced cardiovascular complications in MIO group (OR = 0.770, 95% CI = 0.681 ~ 0.872, P V < 0.05), with statistical homogeneity (I 2 of 2.4%, P Q = 0.427) (Fig. 7).

Fig. 7.

Fig. 7

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Meta-analysis of MIE and cardiovascular complications

MIO and surgical technology related (STR) complications

Thirty-nine studies reported STR complications (MIO2933 vs OE 3058). There was very strong evidence of reduced STR complications in MIO group (OR = 0.770, 95% CI = 0.681 ~ 0.872, P V < 0.05), with statistical homogeneity (I 2 of 2.4%, P Q = 0.918) (Fig. 8 and Table 3).

Fig. 8.

Fig. 8

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Meta-analysis of MIE and STR complications

MIO and gastrointestinal complications

Twenty-one studies reported gastrointestinal complications (MIO 1872 vs OE 2209). There was no evidence of reduced gastrointestinal complications in MIO group (OR = 1.097, 95% CI = 0.835 ~ 1.442, P V = 0.507), with statistical homogeneity (I 2 of 31.7%, P Q = 0.083) (Table 3).

MIO and anastomotic leak (AL)

Fifty studies reported anastomotic leak (MIO 3680 vs OE 3848). There was no evidence of reduced anastomotic leak in MIO group (OR = 1.023, 95% CI = 0.870 ~ 1.202, P V = 0.785), with statistical homogeneity (I 2 of 8.5%, P Q = 0.304) (Table 3).

MIO and recurrent laryngeal nerve palsy (RLNP)

Thirty-seven studies reported recurrent laryngeal nerve palsy (MIO 2624 vs OE 2805). There was no evidence of reduced RLNP in MIO group (OR = 1.108, 95% CI = 0.917 ~ 1.339, P V = 0.289), with statistical homogeneity (I 2 of 24.8%, P Q = 0.089) (Table 3).

Publication bias analysis

Publication bias was assessed by Egger’s Test and Begg’s Funnel Plot. Begg’s Funnel Plot is shown in Fig. 5, with significant statistical difference (P E < 0.05) (Table 3). This indicated the possibility of publication bias, so sensitivity analysis using “trim and fill” method was carried out, with the aim to impute hypothetically negative unpublished studies, to mirror the positive studies that cause funnel plot asymmetry [35], and to show consistent and stable results between MIO and pulmonary complications (Fig. 9), anastomotic leak, and recurrent laryngeal nerve palsy.

Fig. 9.

Fig. 9

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The “trim and fill” method for MIE and pulmonary complications

Sensitivity analysis

As sample size for cases and controls in all studies is not same (ranging from 9 to 6347), we gradually removed small sample size without altering the qualitative overall results. According to the sensitivity analysis shown in Fig. 10, we removed the Mamidanna et al. [66], without alteration, where I 2 values decreased, indicating that the results were stable.

Fig. 10.

Fig. 10

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The sensitivity analysis of MIE and pulmonary complications

Discussion

MIO has been investigated for decades and is considered to be advantageous compared to OE. However, in the previous studies, the analyzed groups of patients who underwent MIO were small and the reports were mostly retrospective comparative studies, and there was no consensus as to which operative method is superior [94]. Therefore, an updated meta-analysis is performed, which includes the largest and the most complete collections of published data.

We found higher operative duration in the MIO group, consistent with Kunisaki’s [40], Shiraishi’s [45], and randomized controlled trials [30] reported, perhaps due to surgeons’ familiarization with a new and complex techniques. Blood loss in the MIO group was found to be lower compared with OE, in accordance with the results of several case reported and recently published meta-analyses [14, 20].

A shorter hospital stay in the MIO group indicated a faster postoperative recovery than OE group, consistent with other published meta-analyses [14, 20, 21, 30].

We did not find a significant number of harvested lymph nodes in the MIO group [23]. However, significant heterogeneity was seen among all indices of postoperative data, explained by the fact that postoperative data are dependent on operator and tumor characteristics.

Total complication rates varied between 20.5 and 63.5% (Table 2). The MIO group showed lower total complication rates, pulmonary complications occupying the major part. However, a number of studies have reported significantly lower pulmonary complications for those who underwent MIO 17.1% (813/4761) versus OE 22.6% (2264/10,020), with overall morbidity of 20.8% (3077/14,781), consistent with the result of 3.1–37.0% from other studies [15–20, 45, 58–76, 95].

Kinugasa et al. and Ferguson et al. [95, 96] noted that development of pneumonia post procedure was associated with worse prognosis for overall survival (P < 0.01). In addition, Dumont et al. [97] also showed that two thirds of all fatal complications were respiratory in nature. Sauvanet et al. [98] reported that pulmonary morbidity was associated with age >60, with no significant differences in two groups.

The pooled OR of 0.527 showed MIO to be more advantageous than OE in reducing pulmonary morbidity. Although statistical heterogeneity and publication bias were found, we demonstrated the superiority of MIO through statistical methods. However, several factors have been associated with pulmonary complications post procedure, including preoperative status, intraoperative details, and postoperative details [99].

Gex et al. reported that overall 30-day mortality rate was 4.3% between 2004 and 2009, compared with 7.6% in 2002 and 2003, and 11.7% in 1997 and 1999 [100]. Our study found the overall 30-day mortality rate of 5.8% and the pooled OR of 0.668, showing that MIO to be advantageous than OE in reducing mortality. The main advantages of MIO over conventional OE are minimal trauma, small incision, less blood loss, etc. [6]. Other factors independently associated with 30-day mortality included TNM staging, preoperative neoadjuvant therapy, comorbidity, diabetes, increased age, and intraoperative blood loss. However, there was no difference between two groups in terms of age and comorbidity. We found increased number of patients having neoadjuvant therapy in MIO group and patients selected for MIO were always in the early stages. The bias in the selection of patients may have influenced the accuracy of the conclusion, which should be taken into consideration.

Arrhythmia, heart failure, pulmonary embolism, and other cardiovascular complications are recognized as common problems that caused significant morbidity and mortality. Zhou et al. [24] reported significant decrease in the morbidity of arrhythmia and pulmonary embolism in MIO group. Corresponding to this, (see Table 3), we found MIO to be superior to OE in reducing morbidity of system complications, according to the pooled OR = 0.777. Weidenhagent et al. [101] also indicated that the perforation from minimally invasive surgery as such could decrease the risks leading to arrhythmia.

Rizk et al. [102] indicated that “surgical technology related complications,” defined as complications caused directly by operative techniques, had no relationship with overall survival post procedure. However, in our meta-analysis, we found strong evidence of reduced risk of STR complications in the MIO group.

Anastomotic leakage (AL) is a serious complication of esophageal resection and is associated with significant morbidity and mortality [4]. In accordance with Zhou et al’s conclusion [17], we also did not find the evidence of reduced risk of anastomotic leak in the MIO group. Similarly, we also did not find any significant differences in two groups in terms of RLNP and gastrointestinal complications.

Although we conducted comprehensive meta-analysis, our study still has its limitations. (1) Out of 57 studies, only one study is randomized controlled trial (RCT), while others were case-control or cross-sectional designs. Seven studies were of small sample size, which might have influenced the final results of our study. (2) Patients selected for MIO are unlikely to have been representative of the general population of esophageal cancer. We found more patients having neoadjuvant therapy in MIO group, and the patients selected for MIO were always in the early stages, creating selection bias. (3) In order to highlight the advantages of MIO, surgeons would prefer to publish positive results, and unsatisfactory results may have been less inclined in their papers; all these can lead to publication bias. (4) In our study, we compared MIO with OE. MIO consists of different procedures. Although we performed a subgroup analysis according to different procedures, the results were also not qualitatively altered. However, lots of differences exist among these procedures, which will affect the quality of this meta-analysis, and the learning curve of MIO is quite steep, which may influence the outcome of MIE. These limitations may result in an overestimation or underestimation of the effect of MIO.

In addition, 19 studies did the follow-up visit, and all those studies indicated that the 3-year survival, 5-year survival, and overall recurrence rate did not differ between the two groups. Due to the difficulty in data extraction, no pooled analysis was performed, which may have influential role in this study.

Conclusions

In summary, this meta-analysis indicates that MIO is a feasible and a reliable surgical procedure and is superior to OE, with less perioperative complications and in-hospital mortality. However, due to certain limitations of this study, as aforementioned above, further large sample and RCT studies are needed to estimate the effect of MIO and establish the guidelines for future.

Acknowledgements

None.

Funding

The authors declare no funding disclosures or sponsors to this study.

Availability of data and materials

The database supporting the conclusion of this article is included within the article and its additional files (fig file and table file).

Authors’ contributions

YW collected and analyzed the data and drafted the manuscript. WS contributed to the designing, writing, and editing of the manuscript, searching for and adding references, and correspondence with the co-authors. AS and HL offered the technical or material support. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Abbreviations

MIE

Minimally invasive esophagectomy

MIO

Minimally invasive oesophagectomy

OE

Open esophagectomy

RLNP

Recurrent laryngeal nerve palsy

STR

Surgical technology related

TA

Thoracoscopic assisted

Contributor Information

Waresijiang Yibulayin, Email: wzs881117@163.com.

Sikandaer Abulizi, Email: dongm311400@sina.com.

Hongbo Lv, Email: lih471003@sina.com.

Wei Sun, Email: yuan2559052@163.com.

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Data Availability Statement

The database supporting the conclusion of this article is included within the article and its additional files (fig file and table file).

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