Laparoscopic or open abdominal surgery with thoracotomy: future directions from the ROMIO trial in esophageal cancer

The ROMIO randomized clinical trial (1) was an eight-center, United Kingdom-based randomized controlled trial (RCT) designed to evaluate whether minimally invasive gastric mobilization with thoracotomy, a hybrid esophagectomy procedure, resulted in faster recovery than conventional open thoracotomy with laparotomy. The primary outcome measured was the recovery of physical function, assessed using the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC QLQ-C30) at 3 and 6 weeks postoperatively and 3 months after randomization. This study also examined the postoperative complication rates and cost-effectiveness of the procedures. The results indicated no significant difference in physical function between the hybrid and open surgery groups (mean score at 3 months: hybrid surgery, 69 vs. open surgery, 68), with comparable complication rates and cost-effectiveness.

Similar to the ROMIO trial, the MIRO trial compared hybrid surgery (open thoracotomy and laparoscopic surgery) with open thoracotomy and laparotomy (2,3). The MIRO trial reported that hybrid surgery was less invasive, resulted in faster postoperative recovery, and was associated with a lower risk of postoperative complications, particularly pulmonary complications (4). However, in the ROMIO trial, the incidence of pulmonary complications following hybrid surgery was 33%, which was higher than the 18% reported in the MIRO trial and not significantly different from the rate reported after open surgery.

Differences in patient backgrounds and definitions of comorbidities need to be considered when interpreting the results of the two trials. For example, patients in the ROMIO trial had higher mean age, body mass index (BMI), and adenocarcinoma proportion, while the MIRO trial had a higher proportion of patients with a World Health Organization (WHO) performance status of 1 or higher. Also, the ROMIO trial used the Esophagectomy Complications Consensus Group (ECCG) definition (5), while the MIRO trial used the Clavien-Dindo classification for postoperative complications. Regarding preoperative treatment, the overall rate in the ROMIO study was 83% and 73% in the MIRO study. Of these, preoperative chemoradiation (CRT) was administered in 18% of the hybrid group and 17% of the open surgery group in the ROMIO trial, and in 35% of the hybrid group and 29% of the open surgery group in the MIRO trial. In the NeoRes trial (6) comparing preoperative chemotherapy (cisplatin and fluorouracil) with preoperative chemoradiotherapy (same regimen plus 40 Gy of radiation), the incidence of Clavien-Dindo grade IIIb or higher was higher in the CRT group (30% vs. 17%, P=0.05). However, in the Neo-AEGIS study (7), which compared preoperative CRT [CROSS protocol; paclitaxel and carboplatin, radiotherapy (41.4 Gy)] with perioperative chemotherapy (FLOT protocol; fluorouracil, leucovorin, oxaliplatin, and docetaxel), there was no difference in postoperative pulmonary complication rates between treatment groups (16% in CROSS and 20% in FLOT); therefore, it is unclear whether preoperative treatment affects the incidence of postoperative pulmonary complications.

The ROMIO study did not report the operative times for either group, making it difficult to assess the impact on postoperative complications. In contrast, the MIRO study found no significant difference in operative times between the hybrid and open surgery groups. In the ROMIO study, laparoscopic surgery was especially beneficial for patients with a low BMI who were classified as “not overweight or obese. This benefit was thought to be due to the lower amount of adipose tissue in these patients, which improved intra-abdominal visibility and facilitated manipulation of the instruments. In addition, patients with low BMI have a lower risk of obesity-related complications, thus increasing the safety of laparoscopic surgery.

The TIME trial (8) compared right thoracoscopic and laparoscopic surgery [minimally invasive surgery (MIE)] with right thoracoscopy and laparotomy in patients with resectable intrathoracic esophageal carcinomas, including gastroesophageal junction tumors (Siewert Type I). The MIE group had a reduced risk of postoperative complications, especially pulmonary complications (12% in the hybrid group and 36% in the open surgery group), and a higher quality of life, indicating faster recovery. Furthermore, the MIE group exhibited a higher 3-year survival rate (50.5% vs. 40.4%, P=0.207) (9). The mean age of patients in the TIME trial was lower than that in the ROMIO trial, as was the proportion of patients with adenocarcinoma; however, the rates of preoperative treatment were similar. Based on the findings of the TIME trial, it can be inferred that minimally invasive thoracic procedures significantly impact pulmonary complications. This may account for the observed lack of difference between fully open thoraco-laparotomy and the hybrid of open thoracotomy with laparoscopic procedures.

The treatment of esophageal cancer in Japan differs from that in Western countries in several key aspects: preoperative chemotherapy is standard, squamous cell carcinoma is more prevalent, and there is a greater emphasis on superior mediastinal lymph node dissection (10). Some reports have indicated that laparoscopic surgery is associated with fewer complications than open surgery (11,12). However, a study using nationwide Japanese databases found no significant difference in the incidence of pulmonary complications between open and laparoscopic procedures (13).

The ROMIO Trial also included an economic analysis. Hybrid surgery incurred higher costs for equipment and supplies (£626 vs. £514) and slightly higher labor costs (£3,067 vs. £2,972) due to longer operative times. However, lower intensive care unit (ICU) costs (£12,545 vs. £15,342) narrowed the overall cost difference, with minimal difference in cost-effectiveness [quality-adjusted life-years (QALYs): hybrid 0.150 vs. open 0.157]. Lee et al. compared the 1-year postoperative costs and cost-effectiveness between MIE and open esophagectomy (OE) (14). They found that MIE had a lower complication rate, shorter ICU stay, and shorter hospital stay, making it $1,641 less expensive than OE, with an increase of 0.022 QALYs. Liu et al. (15) compared the costs of the MIE and OE groups and found that the total cost of MIE was higher than that of OE (MIE $9,923 vs. OE $6,267, P<0.001) because the surgical costs of MIE were higher than those of OE (MIE $14,890 vs. OE: $12,643, P=0.027); however, the postoperative costs for ICU and ward care were significantly lower in the MIE group than in the OE group (MIE $3,891 vs. OE $5,807, P=0.001). It is also challenging to compare economic outcomes across different regions due to varying socioeconomic statuses, affordability, and costs associated with each treatment option. However, the overall conclusion remained that there was no conclusive difference across the studies mentioned.

The ROMIO trial compared postoperative pain over the six days following surgery. It found that a greater proportion of participants allocated to open surgery received pain relief from epidural infusion at three days post-surgery compared to the hybrid surgery group. Booka et al. (16) reported that laparoscopic abdominal manipulation for esophagectomy resulted in less postoperative pain, accelerated recovery, and a reduced incidence of postoperative pneumonia. They also investigated the relationship between the level of epidural catheter insertion after esophagectomy for esophageal cancer and postoperative pain control and reported that insertion at T7/T8 significantly reduced pain, whereas epidural catheter insertion at T8/T9 significantly increased postoperative pain (17). Thus, even with laparoscopic abdominal surgery, the pain-reducing benefits of the procedure may be compromised if a small incision is made in the epigastrium during the creation of the gastric tube.

In conclusion, the choice between laparoscopic and open surgery for esophagectomy is at the discretion of the surgeon and the institution. However, minimizing postoperative complications is crucial regardless of the procedure selected. Additionally, multidisciplinary studies are required to assess patient pain, long-term quality of life, and cost-effectiveness.

Acknowledgments

We would like to thank Editage (www.editage.jp) for English language editing.

Footnote

Provenance and Peer Review: This article was commissioned by the editorial office, Journal of Thoracic Disease. The article has undergone external peer review.

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Funding: None.

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1927/coif). The authors have no conflicts of interest to declare.

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