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Thoracoscopic three-port single versus multiple intercostal for radical resection of esophageal cancer: a retrospective analysis

BMC Cancer volume 24, Article number: 1104 (2024) Cite this article

Abstract

Background

The purpose of this retrospective study was to compare the safety and feasibility of single-intercostal totally minimally invasive Ivor Lewis esophagectomy (MIIE) with those of multiple-intercostal MIIE.

Methods

Between January 2016 and December 2022, clinical data were collected for 528 patients who successfully underwent totally minimally invasive esophagectomy. Among these patients, 294 underwent MIIE, with 200 undergoing the single-intercostal approach and 94 undergoing the multiple-intercostal approach. Propensity score matching (PSM) was applied to the cohort of 294 patients. Subsequently, perioperative outcomes and other pertinent clinical data were analyzed retrospectively.

Results

A total of 294 patients were subjected to PSM, and 89 groups of patient data (178 persons in total) were well balanced and included in the follow-up statistics. Compared to the multiple intercostal group, the single intercostal group had a shorter operative time (280 min vs. 310 min; p < 0.05). Moreover, there was no significant difference in the incidence of major perioperative complications (p > 0.05). The total number of lymph nodes sampled (25.30 vs. 27.55, p > 0.05) and recurrent laryngeal nerve lymph nodes sampled on the both sides (p > 0.05) did not significantly differ. The single intercostal group had lower postoperative long-term usage of morphine (0,0–60 vs. 20,20–130; p < 0.01), total temporary addition (10,0–30 vs. 20,20–40; p < 0.01) and temporary usage in the first 3 days after surgery (0,0–15 vs. 10,10–20; p < 0.01) than did the multicostal group.There were no significant differences in age, sex, tumor location or extent of lymphadenectomy or in the clinical factors between the single-intercostal group (p > 0.05).

Conclusions

Both techniques can be used for the treatment of esophageal cancer. Compared to multiple intercostal MIIE, the feasibility of which has been proven internationally, the single intercostal technique can also be applied to patients of different age groups and sexes and with different tumor locations. It can provide surgeons with an additional surgical option.

Trial registration

This study was retrospectively registered by the Ethics Committee of the Second Affiliated Hospital of Zhejiang University School of Medicine, and written informed consent was exempted from ethical review. The registration number was 20,230,326. The date of registration was 2023.03.26.

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Background

Esophageal cancer ranks seventh in terms of incidence worldwide, and its mortality rate is the sixth highest among all types of cancers for reasons like the timeliness of diagnosis and aggressiveness of the disease itself [1]. According to the data published, the number of new cases and deaths from esophageal cancer in China are still increasing [2]. Frequently, surgery is the cornerstone of curative-intent treatment for esophageal cancer [3]. Since the right thoracoscopic approach was utilized in 1992, the treatment of esophageal cancer has gradually evolved from open surgery to minimally invasive surgery [4]. Several analyses have proven that the incidence of complications in patients who have undergone minimally invasive esophagectomy has decreased, and the quality of life after surgery has improved [5,6,7,8].

Beginning as early as 2003, Luketich's team described their procedure in detail and reported that, compared with traditional open surgical approaches, minimally invasive esophagectomy significantly reduced mortality and operative time [9]. The results of several subsequent studies have confirmed the significant reductions in mortality, recurrence, anastomotic leakage and pneumonia in patients who underwent minimally invasive surgery compared to patients who underwent open surgery [10,11,12]. In addition, the considerable advantages of minimally invasive Ivor Lewis esophagectomy, such as the relatively complete resection of lymph nodes and long-term survival rate, have been confirmed [13, 14]. And the length of hospitalization and overall complication rates have also decreased significantly compared to those of open and hybrid procedures [15, 16].

Overall, the surgeon chose the technique based on patient, and open, hybrid or totally minimally invasive procedures were effective and feasible. For the past few years, by mastering and promoting the traditional minimally invasive Ivor Lewis technique, a modified technique, the single intercostal surgical approach, has been adopted by our department at the same time, which has reduced the number of intercostal spaces. It was suitable for finding and recognizing anatomical locations during surgery, and it also supported successful completion of surgery. However, the occurrence of complications during the postoperative period of this technique has not been verified; therefore, in the present study, we performed a retrospective analysis to provide surgeons with additional treatment options.

Methods

Patients

This retrospective study was approved by the Ethics Committee of the Second Affiliated Hospital of Zhejiang University School of Medicine,written informed consent was exempted from ethical review, and the ethical review acceptance number was 20,230,326. From January 2016 to December 2022, the relevant clinical data of 294 patients were collected, including 200 patients who underwent single intercostal MIIE and 94 patients who underwent multiple intercostal MIIE. All of the operations were performed by multiple experienced surgeons. All patients were evaluated by gastroscopy and other supplementary examinations, including pulmonary function tests, cardiac function assessments, computed tomography of the chest, and magnetic resonance imaging of the brain before surgery. We ultimately performed propensity score matching analysis on all patients by matching the collected basic demographic data. The associated perioperative outcomes were subsequently compared.

Surgical technique

The surgery was divided into two major steps: laparoscopic and thoracoscopic. The same method was used for both laparoscopic procedures. The patient was placed in a supine position, and five incisions were required (Fig. 1). Then, we completed gastric dissociation and produced a tubular stomach under pneumoperitoneum. The difference was mainly in the thoracoscopic region, and the details of single-intercostal MIIE were described in our previous article [17]. Patients were placed in left lateral position with single lung ventilation and three small incisions were made. Then we dissociated the esophagus and retrived the paraesophageal lymph nodes, inferior tracheal protuberance lymph nodes and recurrent laryngeal nerve lymph nodes. During the anastomosis stage, a 25-mm anvil was positioned into the proximal esophagus utilizing the "Reversal Penetrating or Single-strand Purse-string Suture Technique". Following the excision of esophageal specimens, a circular stapler was inserted into the thoracic cavity via the primary operation port and subsequently docked with the anvil. A nasointestinal feeding tube or jejunostomy tube was routinely placed. Multiple intercostal MIIE was performed via a traditional approach which was similar to our single intercostal MIIE [13]. The surgical highlights and differences are emphasized as follows.

Fig. 1
figure 1

Gastric dissociation and the production of the tubular stomach during laparoscopic stage

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In the single-intercostal group, the sixth or seventh intercostal space was selected. A 1 cm incision was made in both the posterior axillary line and the midaxillary line, which were used as the observation port and the secondary operation port, respectively. A 2.5 cm incision was made in the anterior axillary line as the main operation port. Esophageal dissociation and lymphadenectomy were completed via a thoracoscope. The tubular stomach and esophagus were then mechanically anastomosed. (Fig. 2).

Fig. 2
figure 2

Single intercostal totally minimally invasive Ivor Lewis esophagectomy thoracoscopic stage

Full size image

In the multiple intercostal group, a 1 cm incision was made in the midaxillary line of the eighth intercostal space as the observation port, a 1 cm incision was made in the sixth or seventh intercostal space as the secondary operation port, and a 3 cm incision was made in the anterior axillary line of the fifth intercostal space as the main operation port. Esophageal dissociation and lymphadenectomy were also completed via a thoracoscope. The tubular stomach and esophagus were also mechanically anastomosed. (Fig. 3).

Fig. 3
figure 3

Multiple intercostal totally minimally invasive Ivor Lewis esophagectomy thoracoscopic stage

Full size image

Postoperative Management:

All patients used almost the same postoperative management strategies, which included the following:

  1. (1)

    A nasointestinal feeding tube or jejunostomy tube was routinely placed in both groups;

  2. (2)

    Patients received standard postoperative analgesia and were given basic supportive therapy;

  3. (3)

    During the first postoperative day, we paid attention to basic laboratory indicators such as C-reactive protein, albumin, hemoglobin and white blood cells;

  4. (4)

    The criteria for discharge were as follows: enteral nutrition started on the second postoperative day; esophagography was performed on the seventh day to exclude anastomotic leakage; gradually started to eat fluids and semifluids without adverse reactions; all drains were removed; oral analgesics could control pain; no serious complications needed to be addressed; and discharge was granted after evaluation by the attending physician.

Statistical analysis

All the data were sourced from a well-maintained database at the Second Affiliated Hospital of Zhejiang University School of Medicine. We used 1:1 propensity score matching to minimize the effect of nonrandomized surgical modality selection on outcomes. Surgical modality was used as the dependent variable. A binary logistic regression model was constructed, and scores were calculated based on the following independent variables: age, sex, history of smoking, history of alcohol consumption, history of hypertension, history of diabetes, history of cardiac disease, body mass index (BMI), forced expiratory volume in the first second (FEV1), FEV1%, tumor location and pathological stage. The matching tolerance was 0.02. Different random number generator seeds were used for multiple matching validation to ensure the accuracy of the results.

Statistics are usually expressed as the mean (SD, 95% confidence interval). Categorical variables are expressed as percentages. Nonnormally distributed variables are summarized as medians (ranges). Normally distributed data were compared by the independent sample Student’s t test, nonnormally distributed variables were compared with the Mann‒Whitney U test, and the Pearson χ2 test was used to analyze categorical variables. All the data were analyzed with SPSS version 26.0 (International Business Machines Corporation, Armonk, NY, USA). Differences were considered significant when the p value was less than 0.05.

Results

From January 2016 to December 2022, 528 patients who underwent total minimally invasive esophagectomy were enrolled in this study; 200 patients underwent single intercostal MIIE, and 94 patients underwent multiple intercostal MIIE (Fig. 4). The basic demographic data were used to perform PSM analysis. Finally, 178 patients were successfully matched, yielding 89 groups of one-to-one analysis subjects. Table 1 shows the basic demographic data and clinical characteristics before and after matching. The data were well balanced, and there was no significant difference between the two groups.

Fig. 4
figure 4

Process diagram for screening and enrollment

Full size image
Table 1 The basic demographic data and clinical characteristics before and after matching
Full size table

Table 2 shows the comparison of perioperative outcomes and surgical details between the two propensity score-matched groups. The operation time in the single intercostal group was 280 min (248–315), which was significantly shorter than the 310 min (252.5–360) in the multiple intercostal group (p < 0.05). In addition, total number of lymph nodes retrieved (25.30, 95% CI: 22.94–27.66 vs. 27.55, 95% CI: 25.01–30.09; p > 0.05), number of left recurrent laryngeal nerve lymph nodes retrived (2.30, 95% CI: 1.77–2.84 vs. 2.02, 95% CI: 1.36–2.69; p > 0.05), number of right recurrent laryngeal nerve lymph nodes retrived (1.36, 95% CI: 0.91–1.81 vs. 1.54, 95% CI: 1.12–1.96; p > 0.05), intraoperative blood loss (111.01, 95% CI: 96.73–125.29 mL vs. 120.56, 95% CI: 100.68–140.45 mL; p = 0.439) and total hospitalization time (11.37, 95% CI: 8.82–13.93 days vs. 11.48, 95% CI: 8.48–14.48 days; p = 0.955) were not significantly different. In the multiple intercostal group, five patients had two or more complications, and the total incidence of all types of complications was 21.3%. Three patients in the single intercostal group had two or more complications. The total incidence of all types of complications was 20.2%. We did not find differences between the two groups (p = 0.853). And all types of major complications, especially recurrent laryngeal nerve injury did not differ significantly (p > 0.05). One patient died in the hospital (1.1%) due to respiratory failure in the single intercostal group. No other in-hospital deaths occurred in this study.

Table 2 Perioperative outcomes in both groups
Full size table

To assess the patients' postoperative pain control, data on the use of relevant analgesics were collected and proportionally translated into morphine dosage.We found that patients in the single intercostal group had significantly lower postoperative long-term usage of morphine (0,0–60 mg vs. 20,20–130 mg; p < 0.01), total temporary addition (10,0–30 mg vs. 20,20–40 mg; p < 0.01) and temporary usage in the first 3 days after surgery (0,0–15 mg vs. 10,10–20 mg; p < 0.01) than did those in the multicostal group (Table 3).

Table 3 Postoperative use of analgesics in both groups
Full size table

In addition to the intercomparison between the two groups, we also focused on the relationship between perioperative outcomes and operative details of the single intercostal group and some preoperative variables, such as age, sex, tumor location (based on endoscopic findings combined with intraoperative findings) and complete clearance of lymph nodes (based on pathology reports). Among these indicators, we did not find significant differences. (Table 4).

Table 4 Relationship between the perioperative outcomes and operative details in the single intercostal group
Full size table

Discussion

The retrospective study we performed suggested that patients who underwent single intercostal surgery may have an advantage in terms of reduced operative time compared to patients who underwent multiple intercostal surgeries. In addition, the single intercostal group also showed a notable advantage in reducing postoperative pain. Some of the other study metrics, such as intraoperative blood loss, length of hospitalization, lymph node clearance, and rate of postoperative complications, did not significantly differ between the two techniques.

A study reported by Biere showed that the in-hospital mortality rate of patients who underwent minimally invasive Ivor Lewis esophagectomy was 3%, with a median hospital stay of 11 days [5]. A meta-analysis performed by Harriott et al. showed that the in-hospital mortality rate of patients after total minimally invasive Ivor Lewis esophagectomy was 2%, with a median hospital stay of 11.9 days [16]. In this study, the in-hospital mortality rate of patients in the single intercostal group was 1.1%. The average total hospitalization times were 11.37 days for single-intercostal patients and 11.48 days for multiple-intercostal patients.And the overall complication rates of patients in the two groups were 20.2% and 21.3%. On the basis of these findings, we can conclude that the single-intercostal surgery is a safe and feasible method for radical resection of esophageal cancer, similar to the widely proven traditional multiple intercostal technique.

In this study, patients underwent radical lymph node dissection, which is routinely performed during radical esophageal cancer surgery. We found that the two procedures were similar in terms of the total number of lymph nodes actually sampled (25.30 vs. 27.55). Recent studies have shown that the extent of lymph node dissection significantly affects overall survival, whether preoperative radiotherapy or neoadjuvant therapy is used or not. According to the existing National Comprehensive Cancer Network guidelines, 15 lymph nodes cleared is set as the standard, but it has been shown that the number of lymph nodes cleared should be 20–25; thus, a significant increase in overall survival and disease-free survival curves was observed [18, 19]. The total number of lymph nodes dissected by both techniques in this study was similar to their results, and a single intercostal resection can also support the routine management of complete lymph node dissection.

We also found that the single intercostal space had potential advantage in reducing the operation time. We hypothesize that this phenomenon may primarily be attributed to two factors. Firstly, the esophagus is anatomically positioned posteriorly. Typically, the posterior axillary line at the seventh intercostal space serves as the observation port. This configuration allows the surgeon to achieve an intuitive, near-parallel view of the esophagus through the camera when the patient is placed in a lateral decubitus position. Consequently, the exposure of the surgical field closely resembles that of open thoracic surgery. Rapid identification of anatomical positions during surgery facilitates successful outcomes and has the potential to expedite the surgical process, thereby reducing operative time. Moreover, there was no increase in the number of instruments required for single intercostal surgery, and the space for instrumentation remained adequate. Secondly, as many reports had explained, the progress of doctors in complex surgical techniques, such as minimally invasive esophagectomy, involved a learning curve process,and the mean length of the learning curve was 119 cases. White, Linda, and other teams conducted a detailed study on the learning curve, and the results showed that before the plateau period, with the continuous accumulation of surgical experience by doctors, the perioperative outcomes of patients were significantly improved, and the incidence of complications was significantly reduced [20, 21].The operations in this study were performed by experienced doctors who had completed over 100 MIIE ever. Strictly speaking, these surgeons developed the single intercostal surgical approach only after achieving proficiency with the multiple intercostal technique. As they honed their skills through the multiple-intercostal method, their overall proficiency was correspondingly enhanced.

We speculated that the single intercostal technique also has the potential advantage of reducing postoperative pain. Studies have shown that acute postoperative pain after thoracoscopic surgery may be due to muscle injury, chest tube placement, or neuropathic pain, mainly due to intercostal nerve irritation [22, 23]. Moreover, acute postoperative pain may progress to chronic pain during the recovery period and negatively affect patient recovery [24]. Therefore, postoperative analgesia is also an important indicator of perioperative outcomes. However, avoiding muscle and intercostal nerve injuries and chest tube placement during surgery are difficult. Our single intercostal technique injured only the intercostal nerves and muscles in a single intercostal space, and the chest tube was placed in the same location, which may be helpful for postoperative pain control.

In conclusion, the single intercostal approach in this study has the following characteristics: (a) the thoracoscopic technique is completed with three small incisions under a single intercostal space; (b) the basic instruments needed during the procedure are the same as those used in traditional surgical approaches, and there is still sufficient room for instruments with a single intercostal space; (c) thoracic surgeons who are proficient in the traditional multiple intercostal approach can master the single intercostal technique quickly;and (d) it has potential advantages in reducing surgical time and controlling postoperative pain.

In addition to the above features, this study has several limitations. First, and most importantly, this study was a retrospective analysis, and although we used propensity score matching analysis to reduce the effect of bias, the surgical modality and surgeons themselves were randomized, and some of the inherent influencing factors still cannot be eliminated. Second, this study included only patients in our hospital, and the conclusions drawn may be limited or biased due to geographic location, hospital infrastructure, and other relevant factors. Therefore, a randomized and multicenter study may be available soon to provide a more authoritative comparison of the two techniques.

Conclusions

Based on our surgical experience and statistics, it can be concluded that both single intercostal and multiple intercostal esophagectomy are safe and feasible. The single intercostal procedure may be useful for providing other surgeons with another surgical option for esophageal cancer.

Availability of data and materials

The datasets used and analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

MIIE:

Totally minimally invasive Ivor Lewis esophagectomy

PSM:

Propensity score matching

BMI:

Body mass index

FEV1:

Forced expiratory volume in the first second

CI:

Confidence interval

HAP:

Hospital acquired pneumonia

AF:

Atrial fibrillation

ARDS:

Acute respiratory distress syndrome

ASA:

American Society of Anesthesiologists

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Acknowledgements

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Funding

The study was supported by funds from Key Research and Development Program of Zhejiang Province (No. 2023C03064) and Natural Science Foundation of Zhejiang Province (LZ20H010001).

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Author notes

  1. Jinghao Huang and Yifan Yu contributed equally to this work.

Authors and Affiliations

  1. Department of Thoracic Surgery, the Second Affiliated Hospital, Zhejiang University School of Medicine, No. 88 Jiefang Road, Hangzhou City, Zhejiang Province, China

    Jinghao Huang, Yifan Yu, Zixiang Wu, Chuanqiang Wu, Jinsheng Li, Zhiling Lou & Ming Wu

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Contributions

JHH, YFY and ZXW contributions to study conception and design, data analysis and interpretation, and preparation of the manuscript. CQW and JSL participated in data collection and analysis.ZLL participated in revising the manuscript critically for important intellectual content. MW supervised the study, helped to draft the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ming Wu.

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This study was reviewed and approved by the Ethics Committee of the Second Affiliated Hospital of Zhejiang University and written informed consent was exempted at the same time. The need for consent to participate was also waived by the ethics committee. The research involved no more than minimal risk to the participants (retrospective data analysis of previously collected medical records).

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The authors declare no competing interests.

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Huang, J., Yu, Y., Wu, Z. et al. Thoracoscopic three-port single versus multiple intercostal for radical resection of esophageal cancer: a retrospective analysis. BMC Cancer 24, 1104 (2024). https://doi.org/10.1186/s12885-024-12754-0

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