Minimally invasive esophagectomy for esophageal cancer in the People’s Republic of China: an overview

Abstract

Since its introduction in the People’s Republic of China in 1992, minimally invasive esophagectomy (MIE) has shown the classical advantages of minimally invasive surgery over its open counterpart. Like all pioneers of the technique, cardiothoracic surgeons in the People’s Republic of China claim that MIE has a lower risk of pulmonary infection, faster recovery, a shorter hospital stay, and a more rapid return to daily activities than open esophagectomy, while offering the same functional and oncologic results. There has been burgeoning interest in MIE in the People’s Republic of China since 1995. The last decade has witnessed nationwide growth in the application of MIE and yielded a significant amount of scientific data in support of its clinical merits and advantages. However, no prospective randomized controlled trials have actually investigated the benefits of MIE in the People’s Republic of China. Here we review the current data and state of the art MIE treatment for esophageal cancer in the People’s Republic of China.

Keywords:

• esophagectomy
• minimally invasive esophagectomy
• esophageal cancer
• review

Introduction

The global incidence of esophageal cancer has increased by 50% in the past two decades.^1,2 Advances in neoadjuvant and adjuvant chemotherapy and chemoradiotherapy have led to increasingly multimodal treatment for patients with esophageal cancer, which has decreased the rate of local recurrence and improved long-term survival for some patients. However, surgical resection with radical lymphadenectomy is regarded as one of the curative options for resectable esophageal cancer.^3–6 Frequently, due consideration of surgical resection may not be given because of concerns with regard to the morbidity of open esophagectomy.

In an effort to decrease the morbidity associated with open esophagectomy, Chinese surgeons have adopted a minimally invasive approach to esophageal resection. Because of the potential advantages, including avoiding thoracotomy and laparotomy and reducing the rate of pulmonary infections (thus reducing the inpatient stay),^7,8 minimally invasive esophagectomy (MIE) was introduced into clinical practice in Taiwan⁹ in 1992 at the same time as in Western countries,^10–12 was gradually implemented, and is now a commonplace procedure in the People’s Republic of China (Figure 1), including in Beijing,^13–15 Jinan in Shandong Province,¹⁶ Zhengzhou in Henan Province,¹⁷ Nanjing in Jiangsu Province,¹⁸ Shanghai,^19–30 Taizhou in Zhejiang Province,^31–33 Fuzhou in Fujian Province,^34–36 Taipei⁹ and Taichung³⁷ in Taiwan, Hongkong,^38–40 Guangzhou in Guangdong Province,^41,42 Changsha in Hunan Province,⁴³ Chongqing,^44,45 and Chengdu^46–48 and Nanchong⁴⁹ in Sichuan Province. There has been burgeoning interest in MIE since it was first described in Taiwan in 1995⁹ and in the People’s Republic of China in 1999.¹³ The last decade has witnessed nationwide growth in use of MIE, yielding a significant amount of scientific data to support its clinical merits and advantages. Here we review the current data and state of the art for MIE in the treatment of esophageal cancer in the People’s Republic of China.

Figure 1 Fifteen national areas implementing minimally invasive esophagectomy in the People’s Republic of China.

Notes: High-volume centers: First Affiliated Hospital, School of Medicine, Peking University and Chaoyang Hospital, Capital Medical University in Beijing; Shandong Provincial Hospital, Shandong University in Jinan; The Affiliated Tumor Hospital, Zhengzhou University in Zhengzhou; Jiangsu Provincial Cancer Hospital in Nanjing; Zhongshan Hospital, Fudan University, The Cancer Hospital of Fudan University, Changzheng Hospital, Second Military Medical University and Shanghai Chest Hospital, Shanghai Jiaotong University in Shanghai; Taizhou Hospital, Wenzhou Medical College in Taizhou; Affiliated Union Hospital of Fujian Medical University and Fujian Provincial Tumor Hospital of Fujian Medical University in Fuzhou; Chang Gung Memorial Hospital, Chang Gung Medical College in Taipei; Tungs’ Taichung MetroHarbor Hospital in Taichung; University of Hong Kong Medical Centre, Queen Mary Hospital and The Chinese University of Hong Kong, Prince of Wales Hospital in Hongkong; Nanfang Hospital, Southern Medical University and Cancer Center, Sun Yatsen University in Guangzhou; Second Xiangya Hospital of Central South University in Changsha; Daping Hospital, Third Military Medical University in Chongqing; West China Hospital, Sichuan University in Chengdu; The Second Clinical Institute, North Sichuan Medical College in Nanchong.

Literature on MIE in the People’s Republic of China

The current literature was reviewed by searching the PubMed/Medline database from January 1992 to December 2012 using keywords such as “minimally invasive oesophagectomy”, “MIE”, and “China”. Sixty-one full articles were found to be relevant to MIE (Figure 2). A total of 33 publications (54.1%) were in English. However, nearly half of all relevant clinical reports (28, 45.9%) were published in Chinese, despite the fact that it has been necessary to report the current status of MIE as performed in the People’s Republic of China to cardiothoracic surgeons worldwide. A marked increase in the number of papers dedicated to MIE was observed from 2010 to 2012 (Figure 2), which probably reflects increased research interest among the surgical community and wider clinical application of this patient-friendly approach.

Figure 2 Numbers of papers related to minimally invasive esophagectomy performed in the People’s Republic of China identified in the PubMed/Medline database, using keywords such as “minimally invasive oesophagectomy”, “MIE”, and “China”.

Operative data on MIE

Key outcomes of the major studies are summarized in the Tables 1 and 2. Thirty-two relevant papers, consisting of prospective and retrospective studies, were identified. Eight papers directly compared open oesophagectomy and MIE, and^{16,17,21,30,31,39,41,48} five of these involved studies performed prospectively.^{16,31,39,41,48} Common outcome measures included operative data (operative time, blood loss, conversion rate), morbidity (duration of intensive care and total hospital stay), complications (pulmonary complications, anastomotic leaks, chylothorax), mortality data, and follow-up periods. Neoadjuvant treatment numbers were included for each study.

Table 1 Survey over major reports of minimally invasive esophagectomy in the People’s Republic of China: operative data

Reference	PS/RS	Patient (n)	AC	TC	AS	Position	OT (min)	BL (mL)	C, n (%)
Liu et al^Citation9	RS	20	Open	MI	Thoracic	Left Lateral	280	250	NA
Li et al^Citation14	PS	6	MI	MI	Thoracic	Left Lateral	260 ± 42	520 ± 160	0
Li et al^Citation15	RS	6	MI	MI	Thoracic	Left Lateral	380	300	0
Du et al^Citation16	PS	45	Open	HA	Cervical/ thoracic	Left Lateral	29 ± 5 (TC)	93 ± 19 (TC)	NA
		27	Open	MI	Cervical	Left Lateral	425 (240–538)	400 (100–1200)	1 (4)
Liu et al^Citation17	RS	98	MI	MI	Cervical	Left Lateral	134.5 ± 42.3	85.1 ± 32.8	NA
Hou et al^Citation18	RS	41	MI	MI	Cervical	Prone	230 (170–310)	275 (100–320)	NA
		41	MI	MI	Cervical	Left Lateral	280 (190–380)	360 (120–670)	NA
Wu et al^Citation20	PS	32	Open	MI	Cervical	Supine	180	218	0
		8	MI	MI	Cervical	Supine	220	100	0
Zhou et al^Citation22	PS	30	Open	MI	Cervical	Left Lateral	225 (195–290)	250 ± 52.2	1 (3)
Tan et al^Citation23	RS	36	Open	MI	Cervical	Left Lateral	250 (190–330)	165 (100–350)	0
Wang et al^Citation24	PS	27	MI	MI	Cervical	Left Lateral	267 ± 51	327 ± 83	NA
Feng et al^Citation25	PS	27	MI	MI	Cervical	Supine	194.4 ± 26	215 ± 111.6	0
		27	MI	MI	Cervical	Left Lateral	228.1 ± 35.8	142.6 ± 51.3	0
Wang et al^Citation26	RS	48a	MI	MI	Cervical	Left Lateral	279 ± 64	359 ± 156	NA
		49b	MI	MI	Cervical	Left Lateral	266 ± 56	336 ± 130	NA
Feng et al^Citation27	RS	52	MI	MI	Cervical	Left Lateral	82 ± 17 (TC)	139 ± 54 (TC)	0
	RS	36	MI	MI	Cervical	Prone	70 ± 20 (TC)	100 ± 52 (TC)	0
Shen et al^Citation28	RS	76	MI	MI	Cervical	Prone	89 ± 32 (TC)	152 ± 108	0
Feng et al^Citation29	PS	41	MI	MI	Cervical	Decubitus	217 ± 32	142 ± 49	1 (2.4)
	PS	52	MI	MI	Cervical	Prone	202 ± 21	123 ± 56	0
Wang et al^Citation30	RS	260	MI/O	MI	Cervical	Left Lateral	105 ± 30 (TC)	95 ± 48 (TC)	NA
Zhu et al^Citation31	PS	25	Open	MI	Thoracic	Left Lateral	88 ± 15 (TC)	280 ± 132 (TC)	NA
Chen et al^Citation32	PS	67	MI	MI	Cervical	Left Lateral	274 ± 15	225 ± 31	NA
Zhu et al^Citation33	PS	11	MI	MI	Cervical	Left Lateral	242.3 ± 27.0	168.2 ± 95.6	NA
Lin et al^Citation34	RS	80	MI	MI	Cervical	Left Lateral	NA	100–250	6 (8)
Liu et al^Citation35	RS	297	MI	MI	Cervical	Left Lateral	242.3 ± 58.7	NA	1 (3)
Lin et al^Citation36	RS	150	MI	MI	Cervical	Left Lateral	258 ± 45	207 ± 130	6 (4)
Cense et al^Citation38	PS	30	Open	MI	Cervical	Left Lateral	400 (180–570)	700 (164–3000)	2 (7)
Law et al^Citation39	PS	30	Open	MI	Thoracic	Left Lateral (29)/ prone (1)	392 (180–570)	700 (164–3000)	2 (6.7)
Wong et al^Citation40	PS	12	MI	MI	Thoracic	Supine	510 (300–660)	500 (250–2500)	1 (8)
Wang et al^Citation41	PS	33	MI	MI	Cervical	Na	NA	NA	NA
Xie et al^Citation42	RS	100	MI	MI	Cervical	Left Lateral	310	200	4 (4)
Yuan et al^Citation43	PS	32	MI	MI	Cervical	Left Lateral	290.8 ± 36.9	NA	NA
		36	Open	MI	Cervical	Supine	249.0 ± 31.0	NA	NA
Guo et al^Citation44	RS	89	Open	MI	Cervical	Left Lateral	323.7 ± 50.3	307.8 ± 162.7	8 (9.0)
Guo et al^Citation45	RS	135	Open	MI	Cervical	Left Lateral	334 ± 51.1	349.3 ± 164.8	10 (7.4)
Zhang et al^Citation46	RS	160	MI	MI	Cervical	Prone	230–780	20–4000	9 (5.6)
Gao et al^Citation48	PS	96	MI	MI	Cervical	Left Lateral	330.2 ± 36.7	346.7 ± 41.1	0

Notes:

a Retrosternal route of gastric tube reconstruction;

b prevertebral route of gastric tube reconstruction.

Abbreviations: PS, prospective study; RS, retrospective study; AC, abdominal component; TC, thoracic component; AS, anastomosis site; OT, operation time; BL, blood loss; C, conversion rate; MI, minimally invasive; O, open; NA, not available; HA, hand-assisted.

Table 2 Survey of major reports of minimally invasive esophagectomy in the People’s Republic of China: mortality, morbidity, and postoperative complications

Reference	Patient (n)	AL, n (%)	PC, n (%)	Ch, n (%)	ICUS (d)	HS (d)	30-DM	Mortality, n (%)	FP (m)
Liu et al^Citation9	20	0	0	0	NA	19	NA	NA	11.5
Li et al^Citation14	6	0	NA	NA	0	17	NA	NA	2.5
Li et al^Citation15	6	0	0	0	NA	NA	NA	NA	NA
Du et al^Citation16	45	NA	NA	NA	NA	10.0 ± 1.0	NA	NA	NA
Liu et al^Citation17	98	2 (2.0)	10 (10.2)	3 (3.1)	NA	12.7 ± 3.5	1	NA	NA
Hou et al^Citation18	41	1 (2.4)	2 (4.9)	0	NA	NA	NA	NA	15.7
	41	1 (2.4)	1 (2.4)	2 (4.9)	NA	NA	NA	NA	16.3
Wu et al^Citation20	32	3 (9.4)	1 (3.1)	1 (3.1)	2.2	11.6	NA	NA	NA
	8	1 (12.5)	0	0	1.2	10.6	NA	NA	NA
Zhou et al^Citation22	30	2 (6.7)	2 (6.7)	1 (3.3)	NA	11.7 ± 6.3	0	0	NA
Tan et al^Citation23	36	5 (13.9)	1 (2.8)	1 (2.8)	NA	8.7	0	0	NA
Wang et al^Citation24	27	5 (18.5)	1 (3.7)	2 (7.4)	2.3 ± 1.7	NA	NA	NA	NA
Feng et al^Citation25	27	5 (18.5)	7 (25.9)	0	3.1 ± 4.4	11.1 ± 6.6	1	NA	36
	27	4 (14.8)	4 (14.8)	1 (3.7)	1.9 ± 4.2	13.3 ± 10.6	0	NA	36
Wang et al^Citation26	48	10 (20.8)	2 (4.2)	1 (2.1)	2.5 ± 1.7	NA	0	NA	NA
	49	3 (6.1)	6 (12.2)	1 (2.0)	2.8 ± 1.9	NA	0	NA	NA
Feng et al^Citation27	52	8 (15.4)	5 (9.6)	2 (3.8)	1.3 ± 3.5	13.6 ± 9.3	NA	NA	NA
	36	2 (5.6)	1 (2.8)	0	1.1 ± 1.5	10.9 ± 6.0	NA	NA	NA
Shen et al^Citation28	76	16 (21.1)	5 (6.6)	1 (1.3)	NA	19.2 ± 16.3	NA	0	NA
Feng et al^Citation29	41	9 (22.0)	4 (9.8)	NA	3.5 ± 1.3	17.4 ± 12.5	NA	NA	NA
	52	4 (7.7)	5 (9.6)	NA	1.5 ± 1.1	11.4 ± 6.8	NA	NA	NA
Wang et al^Citation30	260	26 (10)	22 (8.5)	3 (1.2)	NA	14.3 ± 7.5	NA	2 (7.7)	NA
Zhu et al^Citation31	25	1 (4)	NA	NA	NA	10.9 ± 2.5	NA	NA	NA
Chen et al^Citation32	67	NA	7 (10.4)	NA	NA	11.5 ± 1.6	NA	NA	14.0 ± 2.2
Zhu et al^Citation33	11	2 (18.2)	3 (27.3)	NA	NA	18.9 ± 10.3	NA	NA	4.5
Lin et al^Citation34	80	1 (1.3)	NA	2 (2.5)	NA	NA	NA	NA	NA
Liu et al^Citation35	297	9 (3.0)	41 (18.8)	NA	NA	17.4 ± 9.8	NA	NA	NA
Lin et al^Citation36	150	9 (6.0)	17 (11.3)	5 (3.3)	NA	NA	2 (1.3)	9 (6)	3–22
Cense et al^Citation38	30	1 (3.3)	12 (40)	NA	NA	NA	NA	NA	NA
	27	1 (3.7)	13 (48.1)	NA	NA	NA	NA	2 (7)	NA
Law et al^Citation39	30	1 (3.3)	12 (40)	0	NA	NA	1	NA	NA
Wong et al^Citation40	12	1 (8.3)	2 (17)	NA	2	41	0	0	NA
Wang et al^Citation41	33	1 (3.0)	0	0	NA	NA	NA	NA	NA
Xie et al^Citation42	100	11 (11)	13 (13)	3 (3)	1 (1)	12 (12)	NA	NA	NA
Yuan et al^Citation43	32	2 (6.3)	NA	NA	1	11.1 ± 1.3	0	NA	NA
	36	5 (13.9)	NA	NA	1	11.6 ± 1.7	0	NA	NA
Guo et al^Citation44	89	6 (6.7)	4 (4.5)	4 (4.5)	NA	15.2 ± 9.8	NA	NA	NA
Guo et al^Citation45	135	9 (6.7)	7 (5.2)	8 (5.9)	NA	NA	NA	NA	NA
Zhang et al^Citation46	160	21 (13.1)	25 (15.6)	4 (2.5)	1	13.1	2 (1.3)	4 (2.5)	NA
Gao et al^Citation48	96	7 (7.3)	13 (13.5)	1 (1.1)	19.2 ± 3.5	12.6 ± 8.8	NA	2 (2.1)	NA

Abbreviations: AL, anastomotic leaks; PC, pulmonary complication; Ch, chylothorax; ICUS (d), intensive care unit stay (days); HS (d), hospital stay (days); 30-DM, 30-day mortality; FP (m), follow-up period (months); NA, not available.

Surgical approaches

Surgical approaches for MIE performed by Chinese cardiothoracic surgeons are multiple and complicated. As listed in Table 1, the majority of centers use mainly total MIE (laparoscopic and thoracoscopic esophagectomy), whereas hybrid MIE (thoracoscopy and laparotomy/laparoscopy and thoracotomy) is used in routine practice in some centers. At our center, we originally used hybrid MIE³¹ but more recently transitioned to a minimally invasive modified McKeown 3-incision total MIE (laparoscopic and thoracoscopic esophagectomy) in 2010.^32,33

Operative time and blood loss

Operative time varied significantly between the studies, reflecting the type of MIE performed as well as accumulated experience and technical skills (Table 1). Blood loss also varied significantly from center to center, comprising around 100–700 mL (Table 1). Major blood loss and need for blood transfusion in particular increased the risk of postoperative morbidity and mortality.

Conversion to open esophagectomy

The conversion rate reported in the literature is in a range of 0%–9.7% (Table 1). However, with surgical experience, the conversion rate reduces and currently does not exceed 5% in expert centers in the People’s Republic of China. The main reason for conversion was bleeding. It is not appropriate to consider conversion from MIE to open esophagectomy as a failure because patient safety and the oncologic integrity of the procedure should be of supreme importance.

Mortality, morbidity, and postoperative complications

Mortality rates following total MIE vary between 0% and 7.7% (Table 2), which compares favorably with an open transthoracic procedure mortality rate of 9.2% and an open transhiatal procedure mortality rate of 7.2%.⁵⁰ However, at least half of the patients who undergo open oesophagectomy, performed through a right thoracotomy and laparotomy, are at risk of developing pulmonary complications requiring a protracted stay in intensive care, with consequences for quality of life during convalescence.⁵⁰ Anastomotic leak is one of the most feared complications of MIE. From the operative data, the MIE leakage rate was in the range of 0%–20.8% (Table 2), which is comparable with the leakage rates reported for open oesophagectomy.⁵¹ Median duration of postoperative stay in intensive care following MIE was one day in the majority of studies (Table 2). MIE is associated with a significant reduction in hospital stay, with a mean postoperative stay of 12 days (Table 2).

Outcomes

There is little survival data for MIE available in the People’s Republic of China. Only one study reported overall survival after MIE.²⁵ Feng et al reported median survival for patients in a thoracoscope-assisted transthoracic esophagectomy group and in a mediastinoscope-assisted transhiatal esophagectomy group of 34.4 months and 36.8 months, respectively.²⁵ There do not appear to be any prospective, randomized, controlled trials comparing the oncologic outcome of MIE with that of open esophagectomy. The present knowledge is based mainly on short-term, nonrandomized comparative studies or historical comparisons with outcomes of open surgery.^31,39,41,48

Conclusion

In conclusion, MIE is becoming more popular in the People’s Republic of China now that Chinese cardiothoracic surgeons are receiving adequate training in major centers. Use of the technique is growing in the People’s Republic of China, as confirmed by the increasing number of recently published papers on MIE. However, no prospective, randomized, controlled trials have investigated the benefits of MIE in this country. Such trials, directly comparing MIE and open approaches, are urgently needed.

Acknowledgments

This work was supported by grants from Zhejiang Provincial Science and Technology Major Projects (2011C13039-2) and Zhejiang Provincial Science and Technology Innovation Team Projects (2011R09040-03).

Disclosure

The authors report no conflicts of interest in this work.