Abstract
Background:
The study aimed to clarify the characteristics of lymph node metastasis (LNM) and to compare the oncologic outcomes of minimally invasive esophagectomy (MIE) with open esophagectomy (OE) in terms of lymph node dissection (LND) in thoracic esophageal cancer patients.
Methods:
The data from esophageal cancer patients who underwent MIE or OE from January 2016 to January 2019 were retrospectively reviewed. The characteristics of LNM in thoracic esophageal cancer were discussed, and the differences in numbers of LND, LND rate, and LNM rate/degree of upper mediastinum between MIE and OE were compared.
Results:
For overall characteristics of LNM in 249 included patients, the highest rate of LNM was found in upper mediastinum, while LNM rate in middle and lower mediastinum, and abdomen increased with the tumor site moving down. The patients were divided into MIE (n = 204) and OE groups (n = 45). In terms of number of LND, there were significant differences in upper mediastinum between MIE and OE groups (8 [5, 11] vs. 5 [3, 8], P < 0.001). The comparative analysis of regional lymph node showed there was no significant difference except the subgroup of upper mediastinal 2L and 4L group (3 [1, 5] vs. 0 [0, 2], P < 0.001 and 0 [0, 2] vs. 0, P = 0.012, respectively). Meanwhile, there was no significant difference in terms of LND rate except 2L (89.7% [183/204] vs. 71.1% [32/45], P = 0.001) and 4L (41.2% [84/204] vs. 22.2% [10/45], P = 0.018) groups. For LNM rate of T3 stage, there was no significant difference between MIE and OE groups, and the comparative analysis of regional lymph node showed that there was no significant difference except 2L group (11.1% [5/45] vs. 38.1% [8/21], P = 0.025). The LNM degree of OE group was significantly higher than that of MIE group (27.2% [47/173] vs. 7.6% [32/419], P < 0.001), and the comparative analysis of regional LNM degree showed that there was no significant difference except 2L (34.7% [17/49] vs. 7.7% [13/169], P < 0.001) and 4L (23.8% [5/21] vs. 3.9% [2/51], P = 0.031) subgroups.
Conclusion:
MIE may have an advantage in LND of upper mediastinum 2L and 4L groups, while it was similar to OE in other stations of LND.
Keywords: Esophageal neoplasms, Lymph node, Minimally invasive esophagectomy, Open esophagectomy
Introduction
Cancer is the leading cause of deaths in China, seriously threatening human health and life expectancy.[1,2] Esophageal cancer is a common malignancy of the digestive tract with family clustering.[3] A high incidence of esophageal cancer has been reported in China, especially in Henan province among the highest mortality in the world.[4] Esophageal cancer can be divided into cervical and thoracic esophageal cancers according to tumor sites.[5,6] Cancer cases coded as thoracic esophagus include upper, middle, and lower esophageal carcinoma, and the carcinomas were predominantly located in the middle thoracic esophagus (51.6%).[7,8] Minimal invasive esophagectomy (MIE) and open esophagectomy (OE) are the main treatment methods for esophageal cancer.[9,10] Clinically, the surgical approaches include left thoracotomy (Sweet), right thoracotomy (McKeown or Ivor–Lewis), and transmediastinal and esophageal hiatus approaches.[11] The surgical treatment for esophageal cancer is relatively complicated, due to the special anatomical position of esophagus.[12] The potential advantage of MIE is the avoidance of thoracotomy, thus causing less surgical access-related trauma.
Existing literature has shown that right/left thoracotomy approach has significant advantages in improving prognosis and long-term survival rate of esophageal cancer patients.[13–15] However, the 5-year overall survival rate of patients with esophageal cancer worldwide is still less than 20%,[16] which gradually decreases with the increasing of number and metastasis range of lymph nodes.[17,18] Therefore, reasonable lymph node dissection (LND) is very critical for long-term prognosis of esophageal cancer patients. Recently, despite many studies having made comparison between MIE and OE,[19] there are few reports on the characteristics of lymph node metastasis (LNM) and regional LND.
According to the standard of esophageal lymph node grouping formulated by American Joint Committee on Cancer (AJCC) and Union for International Cancer Control (UICC),[20] this study aimed to clarify the characteristics of LNM and to compare the outcomes of MIE with OE (McKeown or Ivor–Lewis) in terms of LND in thoracic esophageal cancer patients. This comparative study is expected to provide better guidance and a clearer set of objectives for LND in surgical treatment of esophageal cancer, so as to achieve a better survival prognosis.
Methods
Ethical approval
This study was approved by the Ethics Committee of the Fourth Hospital of Hebei Medical University hospital (No. 2020K-1183). Written informed consent was obtained from all patients.
Patients
A total of 427 primary thoracic esophageal cancer patients who underwent radical surgery from January 2016 to January 2019 in our hospital were retrospectively reviewed. Inclusion criteria were: (1) patients with complete clinical data; (2) tumors located in thoracic segment, no other malignancies history; (3) patients not received neoadjuvant therapies (including neoadjuvant chemotherapy, radiotherapy and other anti-tumor therapy) before surgery; (4) patients underwent OE (McKeown or Ivor–Lewis) or MIE; (5) patients underwent at least two regional (thoraco-abdominal) LND; (6) no distant metastasis detected by preoperative CT and other examinations; and (7) postoperative pathology confirmed R0 resection. Patients with multiple esophageal cancers, or postoperative pathology predicting positive resection margins were excluded. Then they were divided into two groups according to surgical methods: MIE and OE groups.
Surgical protocols
Preoperative preparation was the same for both groups. 150 mL olive oil was orally administered 4 to 8 h before surgery. The stomach was empty, and antibiotics were given 30 min before surgery to prevent infection. Intravenous-inhalation combined anesthesia was performed. The tri-incisional approach (McKeown) was adopted as the surgical approach for MIE with thoracoscope and laparoscope. The McKeown or Ivor–Lewis approach was used for OE, and the thoraco-abdominal two-field LND was required for both approaches.[21] All operations were performed by the same thoracic surgery team, avoiding the selection deviation caused by different surgeons’ technology and experience. They are well-known experts in the industry, and have completed the surgical demonstration of esophageal cancer in provincial and domestic large conferences for many times, and their surgical technology has been unanimously recognized by the industry's peer experts.
Clinical evaluation
The invasion depth of postoperative pathological T stages and lymph node grouping criteria were according to the 8th edition of Tumor, Node, and Metastasis (TNM) staging standard of UICC and AJCC:[20] (1) LND rate = the number of cases of LND in each lymph node group/the total number of cases × 100%, to evaluate the degree and effect of LND; (2) LNM degree = the number of positive lymph nodes in each lymph node group/the total number of LND in this group × 100%, to evaluate the degree of LNM; and (3) LNM rate = the number of cases with LNM in each lymph node group/the total number of cases × 100%, to evaluate the probability of LNM in each lymph node group. Standards for grouping and subregion of lymph nodes are shown in Table 1.
Table 1.
Lymph nodes grouping and sub-regional standards in esophageal cancer.
| Region | Group | Description |
| Upper mediastinum | 2R | Lymph nodes near upper-right trachea |
| 2L | Lymph nodes near upper-left trachea | |
| 8U | Lymph nodes near upper thoracic esophagus | |
| 4R | Lymph nodes near bottom-right trachea | |
| 4L | Lymph nodes near bottom-left trachea | |
| 5 | Lymph nodes under aortic arch | |
| 6 | Lymph nodes near anterior mediastinum | |
| Middle mediastinum | 7 | Lymph nodes under the carina |
| 8M | Lymph nodes near middle thoracic esophagus | |
| 10R | Lymph nodes near right tracheal bronchus | |
| 10L | Lymph nodes near left tracheal bronchus | |
| Lower mediastinum | 8L0 | Lymph nodes near lower thoracic esophagus |
| 9L/R | Lymph nodes near lower pulmonary ligament | |
| 15 | Lymph nodes near diaphragm | |
| Abdominal region | 16 | Lymph nodes near cardia |
| 17 | Lymph nodes near left side of stomach | |
| 18 | Common hepatic artery lymph nodes | |
| 19 | Splenic lymph nodes | |
| 20 | Celiac lymph nodes |
Statistical analysis
All statistical analyses were performed with SPSS version 22 (IBM Corp., Armonk, NY, USA). Continuous variables were expressed as median (interquartile range). Mann–Whitney U test was used for continuous variables that did not meet a normal distribution. Comparison among groups was conducted by Student's t-test, and comparisons of categorical variables and sample composition ratio were conducted by chi-squared test or Fisher's exact test. P < 0.05 was considered statistically significant.
Results
Patients
A total of 249 patients were included and divided into MIE group (n = 204) and OE group (n = 45) [Figure 1]. There was no statistically significant difference in age, gender, body mass index (BMI), tumor sites (except middle thoracic), and LNM rates between the two groups [Table 2]. In thoracic upper, middle, and lower esophageal cancer, the differences in LNM rate among upper, middle, lower mediastinum and abdomen were all statistically significant (P < 0.001, P < 0.001, and P = 0.019, respectively; Table 3). LNM rate of upper mediastinum was the highest, while there was no statistically significant difference in tumor site (P = 0.848), indicating that LNM was not related to tumor location. The LNM rates of middle and lower mediastinum and abdomen were all increased with the tumor location moving down, showing significant differences (P = 0.032, P = 0.019, and P < 0.001, respectively) [Table 4].
Figure 1.
Patients selection for the comparisons of minimally invasive esophagectomy and open esophagectomy in lymph node metastasis/dissection for thoracic esophageal cancer.
Table 2.
Characteristics of the MIE and OE groups of esophageal cancer.
| Characteristic | MIE (n = 204) | OE (n = 45) | Statistics | P-value |
| Age (years) | 62.8 ± 7.3 | 62.0 ± 8.1 | 0.59 | 0.557∗ |
| Gender (male/female) | 137/67 | 35/10 | 1.95 | 0.163† |
| BMI (kg/cm2) | 23.34 ± 3.01 | 23.45 ± 3.10 | 0.21 | 0.833∗ |
| T stage | 13.67 | 0.009‡ | ||
| T1a | 5 (2.5) | 0 | ||
| T1b | 53 (26.0) | 7 (15.6) | ||
| T2 | 29 (14.2) | 1 (2.2) | ||
| T3 | 105 (51.5) | 30 (66.7) | ||
| T4 | 12 (5.9) | 7 (15.6) | ||
| Tumor site | 5.21 | 0.074† | ||
| Upper thoracic | 33 (16.2) | 4 (8.9) | ||
| Middle thoracic | 98 (48.0) | 30 (66.7) | ||
| Lower thoracic | 73 (35.8) | 11 (24.4) | ||
| LNM | 1.56 | 0.211† | ||
| Yes | 106 (52.0) | 28 (62.2) | ||
| No | 98 (48.0) | 17 (37.8) | ||
| ASA classification | 5.59 | 0.094‡ | ||
| 1 | 1 | 1 | ||
| 2 | 196 | 40 | ||
| 3 | 6 | 4 | ||
| 4 | 1 | 0 | ||
| NACT (yes/no) | 21/183 | 8/37 | 2.01 | 0.157† |
| Co-existent diseases | 1.66 | 0.678‡ | ||
| Hypertension | 59 | 18 | ||
| Diabetes | 16 | 3 | ||
| Coronary heart disease | 3 | 2 | ||
| Old cerebral infarction | 4 | 1 |
Student's t test.
The chi-squared test.
Fisher's exact test. Data are expressed as n, n (%), mean ± standard deviation. ASA: American Society of Anesthesiologists; BMI: Body mass index; LNM: Lymph node metastatic; MIE: Minimal invasive esophagectomy; NACT: Neo-adjuvant chemotherapy; OE: Open esophagectomy.
Table 3.
Comparison of lymph node metastasis rates in different region of esophageal cancer, n (%).
| Region | Upper mediastinum | Middle mediastinum | Lower mediastinum | Abdomen | χ 2 | P-value |
| Upper thoracic (n = 37) | 41.0 | <0.001 | ||||
| Metastasis | 17 (45.9) | 2 (5.4) | 1 (2.7) | 1 (2.7) | ||
| Not metastasis | 20 (54.1) | 35 (94.6) | 36 (97.3) | 36 (97.3) | ||
| Middle thoracic (n = 128) | 33.63 | <0.001 | ||||
| Metastasis | 53 (41.4) | 27 (21.1) | 14 (10.9) | 30 (23.4) | ||
| Not metastasis | 75 (58.6) | 101 (78.9) | 114 (89.1) | 98 (76.6) | ||
| Lower thoracic (n = 84) | 9.90 | 0.019 | ||||
| Metastasis | 34 (40.5) | 22 (26.2) | 17 (20.2) | 30 (35.7) | ||
| Not metastasis | 50 (59.5) | 62 (73.8) | 67 (79.8) | 54 (64.3) |
Table 4.
Comparison of lymph node metastasis rates in different tumor sites of esophageal cancer, n (%).
| Region | Upper thoracic (n = 37) | Middle thoracic (n = 128) | Lower thoracic (n = 84) | χ 2 | P-value |
| Upper mediastinum | |||||
| Metastasis | 17 (45.9) | 53 (41.4) | 34 (40.5) | 0.33 | 0.848 |
| Not metastasis | 20 (54.1) | 75 (58.6) | 50 (59.5) | ||
| Middle mediastinum | |||||
| Metastasis | 2 (5.4) | 27 (21.1) | 22 (26.2) | 6.87 | 0.032 |
| Not metastasis | 35 (94.6) | 101 (78.9) | 62 (73.8) | ||
| Lower mediastinum | |||||
| Metastasis | 1 (2.7) | 14 (10.9) | 17 (20.2) | 7.91 | 0.019 |
| Not metastasis | 36 (97.3) | 114 (89.1) | 67 (79.8) | ||
| Abdomen | |||||
| Metastasis | 1 (2.7) | 30 (23.4) | 30 (35.7) | 15.29 | <0.001 |
| Not metastasis | 36 (97.3) | 98 (76.6) | 54 (64.3) | ||
LND of the two groups
There was significant difference in the total number of LND between MIE and OE groups (23 [18, 29] vs.19 [16, 25], P = 0.008) [Table 5]. The analysis of regional LND suggested significant differences in the number of upper mediastinal LND between the two groups (8 [5, 11] vs. 5 [3, 8], P < 0.001) [Table 5]. Furthermore, the subgroups of upper mediastinal (2R, 2L, 8U, 4R, and 4L) were stratified according to UICC lymph node grouping, and the results showed there were no significant differences in the number of LND between the two groups, except 2L and 4L subgroup (3 [1, 5] vs. 0 [0, 2], P < 0.001 and 0 [0, 2] vs. 0 [0, 0], P = 0.012, respectively) [Table 5]. In terms of LND rate in upper mediastinum, there were significant differences in 2L and 4L subgroups when comparing MIE and OE groups (89.7% [183/204] vs. 71.1% [32/45], P = 0.001; 41.2% [84/204] vs. 22.2% [10/45], P = 0.018, respectively) [Table 6].
Table 5.
Comparison of the number of lymph nodes dissection in different groups of esophageal cancer.
| Region | MIE (n = 204) | OE (n = 45) | Z-value | P-value |
| Total | 23 (18, 29) | 19 (16, 25) | −2.651 | 0.008 |
| Lymph nodes regions | ||||
| Upper mediastinum | 8 (5, 11) | 5 (3, 8) | −4.220 | <0.001 |
| Middle mediastinum | 5 (3, 7) | 5 (3, 7) | −0.321 | 0.748 |
| Lower mediastinum | 2 (1, 4) | 2 (0, 4) | −1.321 | 0.186 |
| Abdomen | 6 (3, 10) | 6 (3, 9) | −0.026 | 0.979 |
| Upper mediastinum | ||||
| 2R | 3 (2, 5) | 3 (2, 4) | −0.535 | 0.593 |
| 2L | 3 (1, 5) | 0 (0, 2) | −6.092 | <0.001 |
| 8U | 0 (0, 1) | 0 (0, 1) | −0.657 | 0.511 |
| 4R | 0 (0, 0) | 0 (0, 0) | −1.281 | 0.200 |
| 4L | 0 (0, 2) | 0 (0, 0) | −2.524 | 0.012 |
Data were expressed as median (Q1, Q3). Lymph node grouping criteria were made according to the 8th edition TNM staging standard of the Union for International Cancer Control (UICC) and American Joint Committee on Cancer (AJCC). MIE: Minimal invasive esophagectomy; OE: Open esophagectomy; TNM staging: Tumor, Node and Metastasis staging.
Table 6.
Comparative analysis of lymph node dissection rate in upper mediastinum of esophageal cancer.
| Group | MIE (n = 204) | OE (n = 45) | χ 2 | P-value |
| 2R | 193 (94.6) | 42 (93.3) | 0.01 | 1.000 |
| 2L | 183 (89.7) | 32 (71.1) | 10.81 | 0.001 |
| 8U | 66 (32.4) | 12 (26.7) | 0.55 | 0.457 |
| 4R | 19 (9.3) | 6 (13.3) | 0.29 | 0.591 |
| 4L | 84 (41.2) | 10 (22.2) | 5.64 | 0.018 |
Lymph node grouping criteria were made according to the 8th edition TNM staging standard of the Union for International Cancer Control (UICC) and American Joint Committee on Cancer (AJCC). MIE: Minimal invasive esophagectomy; OE: Open esophagectomy; TNM staging: Tumor, Node and Metastasis staging.
Comparison of LNM rate and degree in the mediastinal region between MIE and OE groups with T3 middle esophageal carcinoma
In terms of LNM rate, there was no significant difference in the overall LNM rate of the upper mediastinum between MIE and OE groups (40.0% [18/45] vs. 61.9% [13/21], P = 0.097) [Table 7]. However, further stratification showed that there were significant differences in LNM rate of respective 2L groups in MIE and OE groups (11.1% [5/45] vs. 38.1% [8/21], P = 0.025). The overall LNM degree in upper mediastinum of OE group was significantly higher than that of MIE group (27.2% [47/173] vs. 7.6% [32/419], P < 0.001). The LNM degree of the respective 2L and 4L subgroups in MIE and OE groups was statistically significantly different (7.7% [13/169] vs. 34.7% [17/49], P < 0.001 and 3.9% [2/51] vs. 23.8% [5/21], P = 0.031, respectively) [Table 7].
Table 7.
Comparative analysis of the metastasis degree and rate of upper mediastinal lymph node of middle esophageal cancer in T3 stage.
| Group | MIE (n = 45) | OE (n = 21) | χ 2 | P-value |
| Metastasis rate, n (%) | ||||
| 2R | 13 (28.9) | 8 (38.1) | 0.56 | 0.455 |
| 2L | 5 (11.1) | 8 (38.1) | 4.97 | 0.025 |
| 8U | 2 (4.4) | 4 (19.0) | 2.14 | 0.144 |
| 4R | 0 | 1 (4.8) | – | 0.318 |
| 4L | 2 (4.4) | 2 (9.5) | 0.06 | 0.801 |
| Total | 18 (40.0) | 13 (61.9) | 2.76 | 0.097 |
| Metastasis degree∗ | ||||
| 2R | 15/174 (8.6) | 20/82 (24.4) | 11.74 | 0.001 |
| 2L | 13/169 (7.7) | 17/49 (34.7) | 23.34 | <0.001 |
| 8U | 2/25 (8.0) | 4/18 (22.2) | 0.78 | 0.378 |
| 4R | 0/22 (0) | 1/3 (33.3) | – | 0.120 |
| 4L | 2/51 (3.9) | 5/21 (23.8) | 4.63 | 0.031 |
| Total | 32/419 (7.6) | 47/173 (27.2) | 40.39 | <0.001 |
Data were expressed as number of lymph node dissection for T3 stage/total lymph node dissection number (%). Lymph node grouping criteria were made according to the 8th edition TNM staging standard of Union for International Cancer Control (UICC) and American Joint Committee on Cancer (AJCC). –: Not applicable. MIE: Minimal invasive esophagectomy; OE: Open esophagectomy; TNM staging: Tumor, Node and Metastasis staging.
Discussion
The incidence and mortality of esophageal cancer are high, with approximately 590,000 new cases and 548,000 deaths worldwide annually.[8,22] Radical surgical resection combined with systematic LND can not only remove tumor, but also prevent or reduce tumor recurrence and prolong survival of patients.[23,24] Traditional open surgeries have been widely recognized and applied in clinical practice.[19,25] Following the progress and development of surgical techniques, the therapeutic protocols for esophageal cancer patients are diversified. Since the end of 20th century, MIE has been recognized by many scholars. Subsequently, thoracoscopy and laparoscopy have been applied in esophageal cancer surgery.[26] Every innovation and progress of esophageal surgery is closely related to LND. Presently, there are still some fundamental issues to be further explored, and one of them is the regularity and characteristics of LNM.
Analysis on different areas of LND suggested that the LNM rate of esophageal cancer in the middle and lower mediastinum and abdominal regions showed an increasing trend with the tumor location moving downward. However, the LNM rate of upper mediastinal did not significantly decrease, but was significantly higher than that in other regions. Tachimori et al[27] have reported that among patients with thoracic esophageal cancer, the upper mediastinum had the highest (51.1%) LNM rate, and our study has drawn a similar conclusion. This result is also consistent with the characteristics of esophageal LNM, that is, esophageal lymphatics crisscross in the mucosa and submucosa, and the longitudinal lymphatics are six times larger than the transverse lymphatics. The longitudinal lymphatics can not only directly penetrate the esophageal wall to the nearby regional lymph nodes, but also metastasize to the cervical or abdominal regional lymph nodes along the esophageal longitudinal direction. This metastasizing pattern makes it difficult to predict regional LNM by tumor location and invasion depth. In addition, this study showed that the upper mediastinal LNM rate of esophageal cancer in lower thorax was as high as 40.5% [34/84], which might be related to the regularity of lymphatic reflux. Most intrathoracic lymph nodes reflux into the thoracic duct and finally into the vein angle, which may significantly increase the probability of cancer cells’ metastasis into the upper mediastinum. The above two characteristics of LNM in esophageal cancer suggests that lymph nodes of thoracic and abdominal areas in thoracic esophageal cancer should be dissected systematically and comprehensively, especially in the upper mediastinum to reduce the possibility of local recurrence and metastasis after esophagectomy.
Regarding to the comparison between MIE and traditional OE, previous studies mainly focused on level and ability of tumor resection, so as to ascertain the long-term prognosis of patients.[28,29] Ye et al[30] have reported the differences of LND between MIE and OE groups, while the characteristics of LNM and regional LND were not studied, which were carried out by us. We found a higher trend in total number of LND in the upper mediastinum in MIE group than that in OE group. Further analysis on the results of LND in upper mediastinum showed that the number of LND in 2L and 4L subgroups of MIE group was higher than that of OE group (P < 0.001 and P = 0.012, respectively). LND rates of 2L and 4L subgroups in MIE group were significantly higher than those in OE group (P = 0.001 and P = 0.018, respectively). It is speculated that it is difficult to expose the lymph nodes of upper mediastinum to the operative field, especially for the 2L and 4L subgroups, since they are located at the left side of the recurrent laryngeal nerve chain and adjacent to the tracheal membrane and arterial wall. Due to the magnifying effect of endoscopy and good surgical field of vision, and the use of auxiliary artificial pneumothorax to expand the mediastinal space, MIE surgery makes the anatomical level clearer. Meanwhile, endoscopic instruments are more suitable for fine operation in some narrow spaces, and the protection of surrounding normal tissues is better than open surgery,[31] so as to minimize the injury of recurrent laryngeal nerve in the operation process.
To better determine whether different surgical methods have an impact on LNM degree and LND rate in the upper mediastinal, patients with T3 stage esophageal cancer in the middle thoracic segment were selected for further comparative analysis. The results showed that there was no significant difference in LNM rate of the upper mediastinal between the two groups, but the grouping analysis showed that the LNM rate of the 2L subgroup in OE group was significantly higher than that in MIE group. In addition, the LNM degree of the upper mediastinal lymph nodes in OE group was significantly higher than that of MIE group, and the differences in the 2L and the 4L subgroups were statistically significant. The reason for those results might be due to the different number and rate of LND, and the real metastatic status of esophageal cancer patients can be reflected more accurately and objectively by the degree and rate of LNM in MIE group.
This study has its inherent limitations as a retrospective analysis. First, it was a single-center study, with a small sample size. Second, the follow-up period was shorter, so there was no comparison of survival. Third, the choice of clinical operation cases was influenced by subjective factors. For cases with large tumor and late pathological stage, surgeons tend more to OE, which will also lead to selective bias. Therefore, further studies with larger samples are necessary to confirm those findings.
In conclusion, in esophageal cancer, the LNM rate in the middle, lower mediastinum and abdomen increased with the tumor site moving down. MIE has certain advantages in LND of upper mediastinum of 2L and 4L subgroups, while it is similar to OE in other regions of LND.
Conflicts of interests
None.
Footnotes
How to cite this article: Li Z, Gai C, Zhang Y, Wen S, Lv H, Xu Y, Huang C, Zhao B, Tian Z. Comparisons of minimally invasive esophagectomy and open esophagectomy in lymph node metastasis/dissection for thoracic esophageal cancer. Chin Med J 2022;135:2446–2452. doi: 10.1097/CM9.0000000000002342
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