Skip to main content
Top
Published in: General Thoracic and Cardiovascular Surgery 8/2021

01-08-2021 | Computed Tomography | Original Article

Clinical impact and utility of positron emission tomography on occult lymph node metastasis and survival: radical surgery for stage I lung cancer

Authors: Haruaki Hino, Takahiro Utsumi, Natsumi Maru, Hiroshi Matsui, Yohei Taniguchi, Tomohito Saito, Tomohiro Murakawa

Published in: General Thoracic and Cardiovascular Surgery | Issue 8/2021

Login to get access

Abstract

Objective

The surgical result of early-staged lung cancer is not satisfactory due to unexpected postoperative lymph node metastasis and recurrence. This study aimed to investigate which preoperative factors—including the standard uptake value max (SUVmax) of positron emission tomography—could predict occult lymph node metastasis and survival.

Methods

We retrospectively analyzed data from 598 patients with clinical stage I lung cancer who underwent surgery, and examined their preoperative clinical characteristics.

Results

A total of 1586 patients had surgery for primary lung cancer between 2006 and 2019; 598 patients with clinical stage I lung cancer were the study inclusion; occult lymph node metastasis was detected in 102 (17.1%). Univariable and multivariable analyses showed that SUVmax ≥ 3 (P < 0.001), clinical invasive tumor size ≥ 2 cm (P = 0.009), and carcinoembryonic antigen > 5 (P = 0.03) were associated with significant risk factors rated (%) for occult lymph node metastasis, as follows: high-risk group (three factors), moderate-risk group (two factors) and low-risk group (one factor or none) corresponding to 32.2 (28/87), 22.8 (41/180) and 7.3 (19/262), respectively (P < 0.001). The 5-year overall survival rates (%) of patients without lymph node metastasis holding SUVmax 6 or over were as poor as those of patients with lymph node metastasis (72.0% vs 64.1%; P = 0.56).

Conclusions

We might consider wedge resection or segmentectomy, omitting lymphadenectomy, for the low-risk group; adjuvant therapy is indicated for patients without lymph node metastasis having SUVmax 6 or over.
Appendix
Available only for authorised users
Literature
1.
go back to reference Minn H, Zasadny KR, Quint LE, Wahl RL. Lung cancer: reproducibility of quantitative measurements for evaluating 2-[F-18]-fluoro-2-deoxy-d-glucose uptake at PET. Radiology. 1995;196:167–73.CrossRef Minn H, Zasadny KR, Quint LE, Wahl RL. Lung cancer: reproducibility of quantitative measurements for evaluating 2-[F-18]-fluoro-2-deoxy-d-glucose uptake at PET. Radiology. 1995;196:167–73.CrossRef
2.
go back to reference Bollineni VR, Ytre-Hauge S, Bollineni-Balabay O, Salvesen HB, Haldorsen IS. High diagnostic value of 18F-FDG PET/CT in endometrial cancer: systematic review and meta-analysis of the literature. J Nucl Med. 2016;57:879–85.CrossRef Bollineni VR, Ytre-Hauge S, Bollineni-Balabay O, Salvesen HB, Haldorsen IS. High diagnostic value of 18F-FDG PET/CT in endometrial cancer: systematic review and meta-analysis of the literature. J Nucl Med. 2016;57:879–85.CrossRef
3.
go back to reference Goel R, Moore W, Sumer B, Khan S, Sher D, Subramaniam RM. clinical practice in PET/CT for the management of head and neck squamous cell cancer. AJR Am J Roentgenol. 2017;209:289–303.CrossRef Goel R, Moore W, Sumer B, Khan S, Sher D, Subramaniam RM. clinical practice in PET/CT for the management of head and neck squamous cell cancer. AJR Am J Roentgenol. 2017;209:289–303.CrossRef
4.
go back to reference Fischer B, Lassen U, Mortensen J, Larsen S, Loft A, Bertelsen A, et al. Preoperative staging of lung cancer with combined PET-CT. N Engl J Med. 2009;361:32–9.CrossRef Fischer B, Lassen U, Mortensen J, Larsen S, Loft A, Bertelsen A, et al. Preoperative staging of lung cancer with combined PET-CT. N Engl J Med. 2009;361:32–9.CrossRef
5.
go back to reference Zhao L, He ZY, Zhong XN, Cui ML. (18)FDG-PET/CT for detection of mediastinal nodal metastasis in non-small cell lung cancer: a meta-analysis. Surg Oncol. 2012;21:230–6.CrossRef Zhao L, He ZY, Zhong XN, Cui ML. (18)FDG-PET/CT for detection of mediastinal nodal metastasis in non-small cell lung cancer: a meta-analysis. Surg Oncol. 2012;21:230–6.CrossRef
6.
go back to reference Takahashi Y, Suzuki S, Matsutani N, Kawamura M. 18F-fluorodeoxyglucose positron emission tomography/computed tomography in the evaluation of clinically node-negative non-small cell lung cancer. Thorac Cancer. 2019;10:413–20.CrossRef Takahashi Y, Suzuki S, Matsutani N, Kawamura M. 18F-fluorodeoxyglucose positron emission tomography/computed tomography in the evaluation of clinically node-negative non-small cell lung cancer. Thorac Cancer. 2019;10:413–20.CrossRef
7.
go back to reference Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40:373–83.CrossRef Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40:373–83.CrossRef
8.
go back to reference Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.CrossRef Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.CrossRef
9.
go back to reference Rami-Porta R, Bolejack V, Giroux DJ, Chansky K, Crowley J, Asamura H, et al. The IASLC lung cancer staging project: the new database to inform the eighth edition of the TNM classification of lung cancer. J Thorac Oncol. 2014;9:1618–24.CrossRef Rami-Porta R, Bolejack V, Giroux DJ, Chansky K, Crowley J, Asamura H, et al. The IASLC lung cancer staging project: the new database to inform the eighth edition of the TNM classification of lung cancer. J Thorac Oncol. 2014;9:1618–24.CrossRef
10.
go back to reference Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC. Pathology and genetics of tumours of the lung, pleura, thymus and heart. In: Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC, editors. World Health Organization classification of tumours. Lyon: IARC Press; 2004. p. 9–124. Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC. Pathology and genetics of tumours of the lung, pleura, thymus and heart. In: Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC, editors. World Health Organization classification of tumours. Lyon: IARC Press; 2004. p. 9–124.
11.
go back to reference Cerfolio RJ, Bryant AS, Ohja B, Bartolucci AA. The maximum standardized uptake values on positron emission tomography of a non-small cell lung cancer predict stage, recurrence, and survival. J Thorac Cardiovasc Surg. 2005;130:151–9.CrossRef Cerfolio RJ, Bryant AS, Ohja B, Bartolucci AA. The maximum standardized uptake values on positron emission tomography of a non-small cell lung cancer predict stage, recurrence, and survival. J Thorac Cardiovasc Surg. 2005;130:151–9.CrossRef
12.
go back to reference Okada M, Nakayama H, Okumura S, Daisaki H, Adachi S, Yoshimura M, et al. Multicenter analysis of high-resolution computed tomography and positron emission tomography/computed tomography findings to choose therapeutic strategies for clinical stage IA lung adenocarcinoma. J Thorac Cardiovasc Surg. 2011;141:1384–91.CrossRef Okada M, Nakayama H, Okumura S, Daisaki H, Adachi S, Yoshimura M, et al. Multicenter analysis of high-resolution computed tomography and positron emission tomography/computed tomography findings to choose therapeutic strategies for clinical stage IA lung adenocarcinoma. J Thorac Cardiovasc Surg. 2011;141:1384–91.CrossRef
13.
go back to reference Tsutani Y, Miyata Y, Nakayama H, Okumura S, Adachi S, Yoshimura M, et al. Solid tumor size on high-resolution computed tomography and maximum standardized uptake on positron emission tomography for new clinical T descriptors with T1 lung adenocarcinoma. Ann Oncol. 2013;24:2376–81.CrossRef Tsutani Y, Miyata Y, Nakayama H, Okumura S, Adachi S, Yoshimura M, et al. Solid tumor size on high-resolution computed tomography and maximum standardized uptake on positron emission tomography for new clinical T descriptors with T1 lung adenocarcinoma. Ann Oncol. 2013;24:2376–81.CrossRef
14.
go back to reference Hung JJ, Yeh YC, Jeng WJ, Wu YC, Chou TY, Hsu WH. Factors predicting occult lymph node metastasis in completely resected lung adenocarcinoma of 3 cm or smaller. Eur J Cardiothorac Surg. 2016;50:329–36.CrossRef Hung JJ, Yeh YC, Jeng WJ, Wu YC, Chou TY, Hsu WH. Factors predicting occult lymph node metastasis in completely resected lung adenocarcinoma of 3 cm or smaller. Eur J Cardiothorac Surg. 2016;50:329–36.CrossRef
15.
go back to reference Moon Y, Kim KS, Lee KY, Sung SW, Kim YK, Park JK. Clinicopathologic factors associated with occult lymph node metastasis in patients with clinically diagnosed N0 lung adenocarcinoma. Ann Thorac Surg. 2016;101:1928–35.CrossRef Moon Y, Kim KS, Lee KY, Sung SW, Kim YK, Park JK. Clinicopathologic factors associated with occult lymph node metastasis in patients with clinically diagnosed N0 lung adenocarcinoma. Ann Thorac Surg. 2016;101:1928–35.CrossRef
16.
go back to reference Seto K, Kuroda H, Yoshida T, Sakata S, Mizuno T, Sakakura N, et al. Higher frequency of occult lymph node metastasis in clinical N0 pulmonary adenocarcinoma with ALK rearrangement. Cancer Manag Res. 2018;10:2117–24.CrossRef Seto K, Kuroda H, Yoshida T, Sakata S, Mizuno T, Sakakura N, et al. Higher frequency of occult lymph node metastasis in clinical N0 pulmonary adenocarcinoma with ALK rearrangement. Cancer Manag Res. 2018;10:2117–24.CrossRef
17.
go back to reference Decaluwé H, Moons J, Fieuws S, De Wever W, Deroose C, Stanzi A, et al. Is central lung tumour location really predictive for occult mediastinal nodal disease in (suspected) non-small-cell lung cancer staged cN0 on 18F-fluorodeoxyglucose positron emission tomography-computed tomography? Eur J Cardiothorac Surg. 2018;54:134–40.CrossRef Decaluwé H, Moons J, Fieuws S, De Wever W, Deroose C, Stanzi A, et al. Is central lung tumour location really predictive for occult mediastinal nodal disease in (suspected) non-small-cell lung cancer staged cN0 on 18F-fluorodeoxyglucose positron emission tomography-computed tomography? Eur J Cardiothorac Surg. 2018;54:134–40.CrossRef
18.
go back to reference Zhang C, Pang G, Ma C, Wu J, Wang P, Wang K. Preoperative risk assessment of lymph node metastasis in cT1 lung cancer: a retrospective study from Eastern China. J Immunol Res. 2019;2019:6263249.PubMedPubMedCentral Zhang C, Pang G, Ma C, Wu J, Wang P, Wang K. Preoperative risk assessment of lymph node metastasis in cT1 lung cancer: a retrospective study from Eastern China. J Immunol Res. 2019;2019:6263249.PubMedPubMedCentral
19.
go back to reference Moon Y, Choi SY, Park JK, Lee KY. Risk Factors for occult lymph node metastasis in peripheral non-small cell lung cancer with invasive component size 3 cm or less. World J Surg. 2020;44:1658–65.CrossRef Moon Y, Choi SY, Park JK, Lee KY. Risk Factors for occult lymph node metastasis in peripheral non-small cell lung cancer with invasive component size 3 cm or less. World J Surg. 2020;44:1658–65.CrossRef
20.
go back to reference Vaghjiani RG, Takahashi Y, Eguchi T, Lu S, Kameda K, Tano Z, et al. Tumor spread through air spaces is a predictor of occult lymph node metastasis in clinical stage IA lung adenocarcinoma. J Thorac Oncol. 2020;15:792–802.CrossRef Vaghjiani RG, Takahashi Y, Eguchi T, Lu S, Kameda K, Tano Z, et al. Tumor spread through air spaces is a predictor of occult lymph node metastasis in clinical stage IA lung adenocarcinoma. J Thorac Oncol. 2020;15:792–802.CrossRef
21.
go back to reference Yasufuku K, Pierre A, Darling G, de Perrot M, Waddell T, Johnston M, et al. A prospective controlled trial of endobronchial ultrasound-guided transbronchial needle aspiration compared with mediastinoscopy for mediastinal lymph node staging of lung cancer. J Thorac Cardiovasc Surg. 2011;142:1393-400.e1.CrossRef Yasufuku K, Pierre A, Darling G, de Perrot M, Waddell T, Johnston M, et al. A prospective controlled trial of endobronchial ultrasound-guided transbronchial needle aspiration compared with mediastinoscopy for mediastinal lymph node staging of lung cancer. J Thorac Cardiovasc Surg. 2011;142:1393-400.e1.CrossRef
22.
go back to reference De Leyn P, Dooms C, Kuzdzal J, Lardinois D, Passlick B, Rami-Porta R, et al. Revised ESTS guidelines for preoperative mediastinal lymph node staging for non-small-cell lung cancer. Eur J Cardiothorac Surg. 2014;45:787–98.CrossRef De Leyn P, Dooms C, Kuzdzal J, Lardinois D, Passlick B, Rami-Porta R, et al. Revised ESTS guidelines for preoperative mediastinal lymph node staging for non-small-cell lung cancer. Eur J Cardiothorac Surg. 2014;45:787–98.CrossRef
23.
go back to reference Silvestri GA, Gonzalez AV, Jantz MA, Margolis ML, Gould MK, Tanoue LT, et al. Methods for staging non-small cell lung cancer: diagnosis and management of lung cancer, 3rd Ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2013;143(5 Suppl):e211S-e250S.CrossRef Silvestri GA, Gonzalez AV, Jantz MA, Margolis ML, Gould MK, Tanoue LT, et al. Methods for staging non-small cell lung cancer: diagnosis and management of lung cancer, 3rd Ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2013;143(5 Suppl):e211S-e250S.CrossRef
24.
go back to reference Grutters JP, Kessels AG, Pijls-Johannesma M, De Ruysscher D, Joore MA, Lambin P. Comparison of the effectiveness of radiotherapy with photons, protons and carbon-ions for non-small cell lung cancer: a meta-analysis. Radiother Oncol. 2010;95:32–40.CrossRef Grutters JP, Kessels AG, Pijls-Johannesma M, De Ruysscher D, Joore MA, Lambin P. Comparison of the effectiveness of radiotherapy with photons, protons and carbon-ions for non-small cell lung cancer: a meta-analysis. Radiother Oncol. 2010;95:32–40.CrossRef
25.
go back to reference Bedetti B, Bertolaccini L, Rocco R, Schmidt J, Solli P, Scarci M. Segmentectomy versus lobectomy for stage I non-small cell lung cancer: a systematic review and meta-analysis. J Thorac Dis. 2017;9:1615–23.CrossRef Bedetti B, Bertolaccini L, Rocco R, Schmidt J, Solli P, Scarci M. Segmentectomy versus lobectomy for stage I non-small cell lung cancer: a systematic review and meta-analysis. J Thorac Dis. 2017;9:1615–23.CrossRef
26.
go back to reference Wang D, Zhang M, Gao X, Yu L. Prognostic value of baseline 18F-FDG PET/CT functional parameters in patients with advanced lung adenocarcinoma stratified by EGFR mutation status. PLoS ONE. 2016;11:e0158307.CrossRef Wang D, Zhang M, Gao X, Yu L. Prognostic value of baseline 18F-FDG PET/CT functional parameters in patients with advanced lung adenocarcinoma stratified by EGFR mutation status. PLoS ONE. 2016;11:e0158307.CrossRef
Metadata
Title
Clinical impact and utility of positron emission tomography on occult lymph node metastasis and survival: radical surgery for stage I lung cancer
Authors
Haruaki Hino
Takahiro Utsumi
Natsumi Maru
Hiroshi Matsui
Yohei Taniguchi
Tomohito Saito
Tomohiro Murakawa
Publication date
01-08-2021
Publisher
Springer Singapore
Published in
General Thoracic and Cardiovascular Surgery / Issue 8/2021
Print ISSN: 1863-6705
Electronic ISSN: 1863-6713
DOI
https://doi.org/10.1007/s11748-021-01606-4

Other articles of this Issue 8/2021

General Thoracic and Cardiovascular Surgery 8/2021 Go to the issue