Standard follow-up after curative surgery for advanced gastric cancer: secondary analysis of a multicentre randomized clinical trial (KLASS-02) (original) (raw)

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Centre for Gastric Cancer, National Cancer Centre

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Goyang

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Korea

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Department of Surgery, Yonsei University College of Medicine

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Seoul

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Korea

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Department of Surgery, Seoul National University Hospital

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Seoul

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Korea

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Department of Surgery, Chonnam National University Hwasun Hospital

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Gwangju

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Korea

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Department of Surgery, Seoul National University Hospital

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Seoul

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Korea

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Department of Surgery, Samsung Medical Centre, Sungkyunkwan University School of Medicine

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Seoul

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Korea

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Department of Surgery, Yeouido St Mary’s Hospital, Catholic University of Korea

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Seoul

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Korea

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Department of Surgery, Yonsei University College of Medicine

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Seoul

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Korea

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Department of Surgery, Seoul National University Bundang Hospital

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Seongnam

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Korea

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Department of Surgery, Keimyung University Dongsan Medical Centre

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Daegu

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Korea

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Received:

06 October 2022

Revision received:

12 November 2022

Accepted:

04 January 2023

Published:

01 February 2023

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Sin Hye Park, Woo Jin Hyung, Han-Kwang Yang, Young-Kyu Park, Hyuk-Joon Lee, Ji Yeong An, Wook Kim, Hyoung-Il Kim, Hyung-Ho Kim, Seung Wan Ryu, Hoon Hur, Min-Chan Kim, Seong-Ho Kong, Gyu Seok Cho, Jin-Jo Kim, Do Joong Park, Young-Woo Kim, Jong Won Kim, Joo-Ho Lee, Sang-Uk Han, Keun Won Ryu, Standard follow-up after curative surgery for advanced gastric cancer: secondary analysis of a multicentre randomized clinical trial (KLASS-02), British Journal of Surgery, Volume 110, Issue 4, April 2023, Pages 449–455, https://doi.org/10.1093/bjs/znad002
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Abstract

Background

The benefit of regular follow-up after curative resection for gastric cancer is controversial as there is no evidence that it will improve survival. This study assessed whether regular follow-up leads to improved survival in patients after surgery for gastric cancer.

Methods

A secondary analysis was undertaken of patients who participated in an RCT of laparoscopic versus open distal gastrectomy for advanced gastric cancer between November 2011 and April 2015. Depending on whether patients were compliant with the initial trial follow-up protocol or not, they were analysed as having had either regular or irregular follow-up. Clinicopathological characteristics, recurrence patterns, detection, treatments, and survival were compared between the groups.

Results

The regular and irregular follow-up groups comprised 712 and 263 patients respectively. Disease recurrence within 36 months was more common in the regular group than in the irregular group (17.0 versus 11.4 per cent; P = 0.041). Recurrence patterns did not differ between the groups. The 3-year recurrence-free survival rate was worse in the regular than in the irregular group (81.2 versus 86.5 per cent; P = 0.031). However, the 5-year overall survival rate was comparable (84.5 versus 87.5 per cent respectively; P = 0.160). Multivariable analysis revealed that type of follow-up was not an independent factor affecting 5-year overall survival.

Conclusion

Regular follow-up after radical gastrectomy was not associated with improved overall survival.

Introduction

Gastric cancer is the fifth most common cancer in terms of incidence, and ranks fourth in terms of cancer mortality rates worldwide1. As of 2018, gastric cancer has accounted for the largest proportion of cases among those of all types of cancer in South Korea2,3. Curative resection with perioperative treatment is the main treatment modality for localized resectable gastric cancer4,5. After curative gastrectomy, follow-up is often undertaken to detect and treat recurrence at an early stage6,7. Another potential benefit of routine follow-up is the ability to address patients’ anxiety, postoperative symptoms, and nutritional deficits that may occur after gastrectomy and adjuvant chemotherapy. In contrast, intensive follow-up strategies involving frequent examinations including CT and oesophagogastroduodenoscopy may be inconvenient for many patients, and lead to an increase in healthcare costs.

An RCT8 compared high- and low-frequency follow-up in patients with stage II or III colorectal cancer, and reported no significant reduction in 5-year overall survival (OS). Several retrospective studies9–12 of patients with gastric cancer obtained similar results. Hence, evidence supporting a survival benefit of regular surveillance in gastric cancer is lacking. There is no consensus on the need for, and frequency of, follow-up after curative gastrectomy5,13–16 and different follow-up strategies after curative surgery for gastric cancer are in use6,7,17.

Therefore, this study aimed to assess whether regular follow-up after curative gastrectomy for gastric cancer is associated with improved survival by analysing data from a prospective multicentre RCT18,19.

Methods

Study design and patients

The present study involved a secondary analysis of data from KLASS-02, an RCT that compared laparoscopic with open distal gastrectomy with D2 lymphadenectomy for advanced gastric cancer5,18,19. Patients with clinical T2–T4a and clinical N0 or N1 (limited perigastric nodal metastasis) cancer were included from November 2011 to April 2015. Of the 1050 patients randomized, 39 were excluded because of withdrawal of informed consent or non-curative surgery owing to distant metastases. Thirty-six patients were excluded from the analyses as they underwent non-curative resection (R1 or R2), died after operation, or were lost to follow-up after surgery.

The eighth edition of the UICC/AJCC staging system20 was used for gastric cancer staging. Postoperative adjuvant chemotherapy was recommended for patients with pathological stage II or more advanced disease. Adjuvant chemotherapy based on TS (tegafur/gimeracil/octeracil)-1 or 5-fluorouracil was administered within 4–6 weeks after curative resection.

According to the study protocol, all patients were assessed every 3 months during the first 2 years and every 6 months for the next 3 years after surgery21. A patient visiting the hospital 30 days before or after the scheduled date was not considered a violation of the protocol. Patients with symptoms could consult a physician irrespective of the follow-up schedule. During the 36-month follow-up, patients who visited the hospital according to the protocol were included in the regular follow-up group, whereas those who did not were included in the irregular follow-up group. When a patient was seen on a regular basis according to the protocol, but this changed to irregular intervals after diagnosis of recurrence, the patient remained in the regular follow-up group. After the 36-month follow-up, survival or date and cause of death were confirmed by telephone or hospital visit every 6 months.

Physical examination and laboratory tests (tumour markers, complete blood cell count, and blood chemistry) were carried out at each visit to check for recurrence (Table S1). Chest radiographs were captured every 6 months. Abdominopelvic CT was performed every 6 months for the first 3 years, and every 6 months or annually thereafter, and endoscopy was undertaken 1 year from the date of surgery. If recurrence was suspected based on the results of the abovementioned examinations, it was confirmed by PET, liver MRI, biopsy, or laparoscopic exploration.

Locoregional recurrence was defined as any proven tumour relapse within the remnant stomach or anastomosis, and regional lymph node metastasis at the surgical site. Peritoneal recurrence was defined by positive cytology in ascitic fluid, peritoneal nodules or thickening on imaging, or tumour invasion of the ovary. Distant metastasis was defined as any tumour relapse at the organ site or in lymph nodes, such as the para-aortic or retroperitoneal lymph nodes. The recurrence patterns were divided into locoregional, peritoneal, and distant recurrences.

After the diagnosis of recurrence, patients received palliative chemotherapy, additional surgery, radiation therapy, or supportive care. Additional operations included R0 or palliative resection for symptoms.

Patients were monitored for postoperative complications during follow-up. Early complications were defined as surgery-related adverse outcomes occurring within 21 days after surgery. Late complications were defined as complications occurring after 21 days. Postoperative morbidity was graded using the Clavien–Dindo classification system22.

Clinicopathological characteristics and survival were compared between the regular and irregular follow-up groups. OS was defined as the interval from the date of surgery to the date of the last follow-up or death from any cause. Recurrence-free survival (RFS) was defined as the interval from surgery until recurrence or death from any cause.

All study procedures were performed in accordance with the principles of the 1964 Declaration of Helsinki. The need for patient consent was waived owing to the retrospective nature of the study. This study was approved by the Institutional Review Board of the National Cancer Centre (approval number NCC 2021-0182).

Statistical analysis

Significant differences in categorical and continuous variables were examined using the χ2 test or Fisher’s exact test and Student’s t test or Mann–Whitney U test respectively. Kaplan–Meier curves were used to calculate OS and RFS, and survival was compared by means of log rank tests. Cox proportional hazards analysis was applied to analyse the association between follow-up interval and survival. The results obtained from the Cox regression model were presented as HRs with 95 per cent confidence intervals. Variables that were significant (P < 0.200) in the univariable analysis were included in the multivariable analysis. P < 0.050 was considered statistically significant. All data analyses were conducted using R version 3.6.3 (Systat Software, San Jose, CA, USA).

Results

Patients

Of a total of 975 patients, 712 were included in the regular and 263 in the irregular follow-up group. Characteristics of the groups are summarized in Table 1. The proportion of patients classified as ASA II and III was larger in the irregular follow-up group, as was the proportion with pathological T2-4. A larger proportion of patients in the regular follow-up group received adjuvant chemotherapy.

Table 1

Patient, disease, and treatment characteristics

Values are n (%) unless otherwise indicated. *Includes only stage II or III disease. †χ2 or Fisher’s exact test, except ‡Mann–Whitney U test.

Table 1

Patient, disease, and treatment characteristics

Values are n (%) unless otherwise indicated. *Includes only stage II or III disease. †χ2 or Fisher’s exact test, except ‡Mann–Whitney U test.

Disease recurrence

Recurrence developed in 151 patients during the 36-month follow-up (Table 2). The median time to recurrence after radical gastrectomy was 21 (i.q.r. 16–27) months in the group with irregular follow-up and 14 (8–23) months in that with regular follow-up (P < 0.001). The incidence of recurrence during the 36 months was higher in the regular follow-up group (17.0 per cent, 121 of 712 patients) than in the irregular follow-up group (11.4 per cent, 30 of 263) (P = 0.041).

Table 2

Disease recurrence and treatment according to follow-up

Values are n (%) unless otherwise indicated. *Includes only patients who developed recurrence (regular group 121, irregular group 30). †Among 120 patients with recurrence in regular follow-up group; 1 patient with no evaluation of symptoms or treatment for recurrence excluded. ‡Laparoscopic biopsy or exploratory laparotomy, ascitic fluid cytology, CT or ultrasound-guided biopsy. §Endoscopic retrograde bile drainage, double-J stent insertion, and unspecified treatment. ¶χ2 or Fisher’s exact test, except #Mann–Whitney U test.

Table 2

Disease recurrence and treatment according to follow-up

Values are n (%) unless otherwise indicated. *Includes only patients who developed recurrence (regular group 121, irregular group 30). †Among 120 patients with recurrence in regular follow-up group; 1 patient with no evaluation of symptoms or treatment for recurrence excluded. ‡Laparoscopic biopsy or exploratory laparotomy, ascitic fluid cytology, CT or ultrasound-guided biopsy. §Endoscopic retrograde bile drainage, double-J stent insertion, and unspecified treatment. ¶χ2 or Fisher’s exact test, except #Mann–Whitney U test.

Some 117 of 151 patients (77.5 per cent) were asymptomatic at the time of detection of recurrence. Abdominal pain was the most common symptom, present in 15 of 151 patients (9.9 per cent). There was no significant difference in recurrence patterns between the two groups. Abdominopelvic CT detected recurrences in 88.7 per cent of patients. Two of the 134 patients (1.5 per cent) had normal CT findings, but raised levels of tumour markers, and were diagnosed with regional and distant lymph node metastases on PET–CT. There was no significant difference in the treatment of recurrence between the two groups; patients with recurrence were most often treated with palliative chemotherapy.

Overall and recurrence-free survival

The 3-year RFS rates in the regular and irregular follow-up groups were 81.2 (95 per cent c.i. 78.1 to 83.9) and 86.5 (81.7 to 90.2) per cent respectively (P = 0.031) (Fig. 1a). The 5-year OS rate was 84.5 per cent in the regular follow-up group and 87.5 per cent in the irregular follow-up group; this difference was not statistically significant (P = 0.160) (Fig. 1b).

Fig. 1

Kaplan–Meier survival plots for patients in the regular and irregular follow-up groups

a 3-year recurrence-free survival and b 5-year overall survival. aP = 0.031, bP = 0.160 (log rank test).

Multivariable analysis revealed that undifferentiated histology, advanced N category, short interval from gastrectomy to recurrence, presence of cancer-related symptoms, and palliative chemotherapy were independent prognostic factors for 5-year OS (Table 3). Type of follow-up was not a significant factor affecting 5-year OS.

Table 3

Univariable and multivariable analysis of 5-year overall survival

Abbreviations: BMI, body mass index; ASA, American Society of Anesthesiologists.

Table 3

Univariable and multivariable analysis of 5-year overall survival

Abbreviations: BMI, body mass index; ASA, American Society of Anesthesiologists.

Discussion

In the present study, the incidence of recurrence and survival after curative gastrectomy was assessed among patients who underwent regular and irregular follow-up within the KLASS-02 RCT. The incidence of recurrence during the 36-month interval was higher and the 3-year RFS rate was significantly lower in the regular compared with the irregular follow-up group. The 5-year OS was comparable between the groups. Type of follow-up was not an independent factor affecting OS.

In contrast to previous retrospective studies9–12 of the role of follow-up after surgery for gastric cancer, data on disease recurrence and death were obtained from a large RCT in the present study.

It has been reported that intensive follow-up leads to longer postrecurrence survival with similar OS. This can be attributed to the early detection of recurrence during follow-up11,23. Other studies7,24 have reported no differences in OS between patients with asymptomatic recurrence detected earlier through regular follow-up and those with symptomatic recurrence detected later owing to the lack of regular follow-up. The reason for the difference in 3-year RFS in the present study was that recurrence was detected earlier in the regular follow-up group. Frequent evaluations in the regular follow-up group might have increased the rate of detection of asymptomatic recurrence. These results are interpreted as having been affected by lead-time bias, and the need for regular follow-up is controversial23.

In the multivariable analysis, histology, pN category, presence of cancer-related symptoms, interval from gastrectomy to recurrence, and palliative chemotherapy were independent prognostic indicators for OS. Similar to previous studies12,25, undifferentiated histology and advanced stage were factors related to OS in the present study. Moreover, the finding that presence of symptoms at recurrence and shorter interval from gastrectomy to recurrence were significantly associated with OS is in accordance with the results of previous studies9,26. Although unproven, it can be assumed that the presence of symptoms and a shorter recurrence-free interval are related to disease progression from recurrence to cancer-related death.

Type of follow-up did not affect 5-year OS in the present study. This is probably because treatments for recurrent cancer are ineffective and do not improve OS. Despite the survival benefit of palliative chemotherapy for recurrent gastric cancer27,28, there is no evidence suggesting that the earlier detection and treatment of recurrence can prolong survival.

The diagnostic tests for recurrence during follow-up vary between clinicians and institutions. Tumour markers can be tested non-invasively with a diagnostic sensitivity of 44–65.8 per cent29,30. Endoscopy is an effective diagnostic method for the detection of intraluminal recurrence. However, several studies7,31,32 have reported that the recurrence rate is less than 10 per cent. The sensitivity of contrast-enhanced CT in detecting metastases in other solid organs, such as the liver and ovaries, is high, and the detection rates are 60–78.3 per cent11,32. In the present study, CT was the most useful screening modality for detecting recurrence, and was effective. PET–CT can be useful when the imaging findings are equivocal33,34. However, the sensitivity of PET–CT is lower than that of CT in the case of lesions smaller than 1 cm, such as peritoneal seeding or lymph node metastases. Moreover, its accuracy in signet ring cell and mucinous adenocarcinoma is low owing to low fluorodeoxyglucose uptake35,36. Therefore, PET–CT is often used in addition to CT rather than alone.

Until now, no RCT has been conducted to determine whether or not intensive follow-up can improve survival after radical gastrectomy for gastric cancer. Moreover, the effects of intensive follow-up on quality of life and nutritional aspects should be analysed. A prospective multicentre RCT37 is currently being conducted to compare survival, quality of life, and nutrition between groups of patients with locally advanced gastric cancer followed up at 3- and 6-month intervals. This study is expected to aid in determining a follow-up strategy that may be implemented after radical gastrectomy.

Author contributions

Sin Hye Park (data curation, formal analysis, investigation, writing—original draft), Woo jin Hyung (conceptualization, data curation), Han-Kwang Yang (data curation), Young Kyu Park (data curation), Hyuk-Joon Lee (data curation), Ji Yeong An (data curation), Wook Kim (data curation), Hyoung-Il Kim (data curation), Hyung-Ho Kim (data curation), Seung-Wan Ryu (data curation), Hoon Hur (data curation), Min Chan Kim (data curation), Seong Ho Kong (data curation), Gyu Seok Cho (data curation), Jin-Jo Kim (data curation), Do Joong Park (data curation), Young-Woo Kim (data curation, writing—review and editing), Jong Won Kim (data curation), Joo Ho Lee (data curation), Sang-Uk Han (data curation, writing—review and editing), and Keun Won Ryu (conceptualization, data curation, funding acquisition, project administration, supervision, writing—review and editing).

Funding

This research was supported by a grant from the Korea Health Technology R&D Project, through the Korea Health Industry Development Institute (KHIDI) (grant numbers: HI19C0481, HC20C0155), funded by the Ministry of Health and Welfare, Korea.

Disclosure

W.J.H. reports involvement in Hutom (employment and leadership); stock and other ownership interests in Hutom Consulting; an advisory role in Ethicon, Medtronic, and SK Hynix; and surgical research funding from Medtronic and GC Biopharma. H.-K.Y. reports research funding from Stryker. H.H. reports hoonoraria from Johnson & Johnson Medical; and research funding from AstraZeneca and Dong-A ST. D.J.P. reports research funding from Medtronic and Daewoong Pharmaceutical. J.W.K. reports research funding from Novomics and Daewoong Pharmaceutical. S.-U.H. reports research funding from Jeil Pharmaceutical, Ethicon Endo-Surgery, and Johnson & Johnson. The authors declare no other conflict of interest.

Supplementary material

Supplementary material is available at BJS online.

Data availability

Manuscript data is available from the corresponding author on reasonable request.

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© The Author(s) 2023. Published by Oxford University Press on behalf of BJS Society Ltd. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

Topic:

• gastric cancer
• follow-up
• surgical procedures, operative
• surgery, curative
• radical gastrectomy
• secondary data analysis

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