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Published in: BMC Cancer 1/2024

Open Access 01-12-2024 | NSCLC | Research

Ultrasound-based radiomics machine learning models for diagnosing cervical lymph node metastasis in patients with non-small cell lung cancer: a multicentre study

Authors: Zhiqiang Deng, Xiaoling Liu, Renmei Wu, Haoji Yan, Lingyun Gou, Wenlong Hu, Jiaxin Wan, Chenwanqiu Song, Jing Chen, Daiyuan Ma, Haining Zhou, Dong Tian

Published in: BMC Cancer | Issue 1/2024

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Abstract

Background

Cervical lymph node metastasis (LNM) is an important prognostic factor for patients with non-small cell lung cancer (NSCLC). We aimed to develop and validate machine learning models that use ultrasound radiomic and descriptive semantic features to diagnose cervical LNM in patients with NSCLC.

Methods

This study included NSCLC patients who underwent neck ultrasound examination followed by cervical lymph node (LN) biopsy between January 2019 and January 2022 from three institutes. Radiomic features were extracted from the ultrasound images at the maximum cross-sectional areas of cervical LNs. Logistic regression (LR) and random forest (RF) models were developed. Model performance was assessed by the area under the curve (AUC) and accuracy, validated internally and externally by fivefold cross-validation and hold-out method, respectively.

Results

In total, 313 patients with a median age of 64 years were included, and 276 (88.18%) had cervical LNM. Three descriptive semantic features, including long diameter, shape, and corticomedullary boundary, were selected by multivariate analysis. Out of the 474 identified radiomic features, 9 were determined to fit the LR model, while 15 fit the RF model. The average AUCs of the semantic and radiomics models were 0.876 (range: 0.781–0.961) and 0.883 (range: 0.798–0.966), respectively. However, the average AUC was higher for the semantic-radiomics combined LR model (0.901; range: 0.862–0.927). When the RF algorithm was applied, the average AUCs of the radiomics and semantic-radiomics combined models were improved to 0.908 (range: 0.837–0.966) and 0.922 (range: 0.872–0.982), respectively. The models tested by the hold-out method had similar results, with the semantic-radiomics combined RF model achieving the highest AUC value of 0.901 (95% CI, 0.886–0.968).

Conclusions

The ultrasound radiomic models showed potential for accurately diagnosing cervical LNM in patients with NSCLC when integrated with descriptive semantic features. The RF model outperformed the conventional LR model in diagnosing cervical LNM in NSCLC patients.
Appendix
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Literature
1.
go back to reference Ferlay J, Colombet M, Soerjomataram I, Parkin DM, Piñeros M, Znaor A, et al. Cancer statistics for the year 2020: An overview. Int J Cancer. 2021. Ferlay J, Colombet M, Soerjomataram I, Parkin DM, Piñeros M, Znaor A, et al. Cancer statistics for the year 2020: An overview. Int J Cancer. 2021.
3.
go back to reference Duma N, Santana-Davila R, Molina JR. Non-small cell lung cancer: epidemiology, screening, diagnosis, and treatment. Mayo Clin Proc. 2019;94(8):1623–40.CrossRefPubMed Duma N, Santana-Davila R, Molina JR. Non-small cell lung cancer: epidemiology, screening, diagnosis, and treatment. Mayo Clin Proc. 2019;94(8):1623–40.CrossRefPubMed
4.
go back to reference Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, Fagerstrom RM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395–409.CrossRefPubMed Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, Fagerstrom RM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395–409.CrossRefPubMed
5.
go back to reference de Koning HJ, van der Aalst CM, de Jong PA, Scholten ET, Nackaerts K, Heuvelmans MA, et al. Reduced lung-cancer mortality with volume ct screening in a randomized trial. N Engl J Med. 2020;382(6):503–13.CrossRefPubMed de Koning HJ, van der Aalst CM, de Jong PA, Scholten ET, Nackaerts K, Heuvelmans MA, et al. Reduced lung-cancer mortality with volume ct screening in a randomized trial. N Engl J Med. 2020;382(6):503–13.CrossRefPubMed
6.
go back to reference Bade BC, Dela Cruz CS. Lung Cancer 2020: Epidemiology, Etiology, and Prevention. Clin Chest Med. 2020;41(1):1–24.CrossRefPubMed Bade BC, Dela Cruz CS. Lung Cancer 2020: Epidemiology, Etiology, and Prevention. Clin Chest Med. 2020;41(1):1–24.CrossRefPubMed
7.
go back to reference Hoosein MM, Barnes D, Khan AN, Peake MD, Bennett J, Purnell D, et al. The importance of ultrasound in staging and gaining a pathological diagnosis in patients with lung cancer–a two year single centre experience. Thorax. 2011;66(5):414–7.CrossRefPubMed Hoosein MM, Barnes D, Khan AN, Peake MD, Bennett J, Purnell D, et al. The importance of ultrasound in staging and gaining a pathological diagnosis in patients with lung cancer–a two year single centre experience. Thorax. 2011;66(5):414–7.CrossRefPubMed
8.
go back to reference Detterbeck FC, Boffa DJ, Kim AW, Tanoue LT. The eighth edition lung cancer stage classification. Chest. 2017;151(1):193–203.CrossRefPubMed Detterbeck FC, Boffa DJ, Kim AW, Tanoue LT. The eighth edition lung cancer stage classification. Chest. 2017;151(1):193–203.CrossRefPubMed
9.
go back to reference Khan TM, Verbus EA, Gandhi S, Heymach JV, Hernandez JM, Elamin YY. Osimertinib, Surgery, and radiation therapy in treating patients with stage IIIB or IV non-small cell lung cancer with EGFR mutations (NORTHSTAR). Ann Surg Oncol. 2022;29(8):4688–9.CrossRefPubMed Khan TM, Verbus EA, Gandhi S, Heymach JV, Hernandez JM, Elamin YY. Osimertinib, Surgery, and radiation therapy in treating patients with stage IIIB or IV non-small cell lung cancer with EGFR mutations (NORTHSTAR). Ann Surg Oncol. 2022;29(8):4688–9.CrossRefPubMed
10.
go back to reference King J, Patel K, Woolf D, Hatton MQ. The Use of Palliative radiotherapy in the treatment of lung cancer. Clin Oncol (R Coll Radiol). 2022;34(11):761–70.CrossRefPubMed King J, Patel K, Woolf D, Hatton MQ. The Use of Palliative radiotherapy in the treatment of lung cancer. Clin Oncol (R Coll Radiol). 2022;34(11):761–70.CrossRefPubMed
11.
go back to reference Han F, Xu M, Xie T, Wang JW, Lin QG, Guo ZX, et al. Efficacy of ultrasound-guided core needle biopsy in cervical lymphadenopathy: A retrospective study of 6,695 cases. Eur Radiol. 2018;28(5):1809–17.CrossRefPubMed Han F, Xu M, Xie T, Wang JW, Lin QG, Guo ZX, et al. Efficacy of ultrasound-guided core needle biopsy in cervical lymphadenopathy: A retrospective study of 6,695 cases. Eur Radiol. 2018;28(5):1809–17.CrossRefPubMed
12.
go back to reference Leng XF, Zhu Y, Wang GP, Jin J, Xian L, Zhang YH. Accuracy of ultrasound for the diagnosis of cervical lymph node metastasis in esophageal cancer: a systematic review and meta-analysis. J Thorac Dis. 2016;8(8):2146–57.CrossRefPubMedPubMedCentral Leng XF, Zhu Y, Wang GP, Jin J, Xian L, Zhang YH. Accuracy of ultrasound for the diagnosis of cervical lymph node metastasis in esophageal cancer: a systematic review and meta-analysis. J Thorac Dis. 2016;8(8):2146–57.CrossRefPubMedPubMedCentral
13.
go back to reference Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG, Granton P, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48(4):441–6.CrossRefPubMedPubMedCentral Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG, Granton P, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48(4):441–6.CrossRefPubMedPubMedCentral
14.
go back to reference Handelman GS, Kok HK, Chandra RV, Razavi AH, Lee MJ, Asadi H. eDoctor: machine learning and the future of medicine. J Intern Med. 2018;284(6):603–19.CrossRefPubMed Handelman GS, Kok HK, Chandra RV, Razavi AH, Lee MJ, Asadi H. eDoctor: machine learning and the future of medicine. J Intern Med. 2018;284(6):603–19.CrossRefPubMed
15.
go back to reference van den Brekel MW, Stel HV, Castelijns JA, Nauta JJ, van der Waal I, Valk J, et al. Cervical lymph node metastasis: assessment of radiologic criteria. Radiology. 1990;177(2):379–84.CrossRefPubMed van den Brekel MW, Stel HV, Castelijns JA, Nauta JJ, van der Waal I, Valk J, et al. Cervical lymph node metastasis: assessment of radiologic criteria. Radiology. 1990;177(2):379–84.CrossRefPubMed
16.
go back to reference Robbins KT, Clayman G, Levine PA, Medina J, Sessions R, Shaha A, et al. Neck dissection classification update: revisions proposed by the American head and neck society and the american academy of otolaryngology-head and neck surgery. Arch Otolaryngol Head Neck Surg. 2002;128(7):751–8.CrossRefPubMed Robbins KT, Clayman G, Levine PA, Medina J, Sessions R, Shaha A, et al. Neck dissection classification update: revisions proposed by the American head and neck society and the american academy of otolaryngology-head and neck surgery. Arch Otolaryngol Head Neck Surg. 2002;128(7):751–8.CrossRefPubMed
17.
go back to reference van Griethuysen JJM, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77(21):e104–7.CrossRefPubMedPubMedCentral van Griethuysen JJM, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77(21):e104–7.CrossRefPubMedPubMedCentral
18.
go back to reference Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16(4):385–95.CrossRefPubMed Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16(4):385–95.CrossRefPubMed
19.
go back to reference Hong H, Xiaoling G, Hua Y, editors. Variable selection using mean decrease accuracy and mean decrease gini based on random forest. 2016 7th IEEE International Conference on Software Engineering and Service Science (ICSESS); 2016 26–28 Aug. 2016. Hong H, Xiaoling G, Hua Y, editors. Variable selection using mean decrease accuracy and mean decrease gini based on random forest. 2016 7th IEEE International Conference on Software Engineering and Service Science (ICSESS); 2016 26–28 Aug. 2016.
20.
go back to reference Bryson TC, Shah GV, Srinivasan A, Mukherji SK. Cervical lymph node evaluation and diagnosis. Otolaryngol Clin North Am. 2012;45(6):1363–83.CrossRefPubMed Bryson TC, Shah GV, Srinivasan A, Mukherji SK. Cervical lymph node evaluation and diagnosis. Otolaryngol Clin North Am. 2012;45(6):1363–83.CrossRefPubMed
21.
go back to reference Gupta A, Rahman K, Shahid M, Kumar A, Qaseem SMD, Hassan SA, et al. Sonographic assessment of cervical lymphadenopathy: role of high-resolution and color Doppler imaging. Head Neck. 2011;33(3):297–302.CrossRefPubMed Gupta A, Rahman K, Shahid M, Kumar A, Qaseem SMD, Hassan SA, et al. Sonographic assessment of cervical lymphadenopathy: role of high-resolution and color Doppler imaging. Head Neck. 2011;33(3):297–302.CrossRefPubMed
22.
go back to reference Lin M, Tang X, Cao L, Liao Y, Zhang Y, Zhou J. Using ultrasound radiomics analysis to diagnose cervical lymph node metastasis in patients with nasopharyngeal carcinoma. European Radiology. 2023;33(2):774–83. Lin M, Tang X, Cao L, Liao Y, Zhang Y, Zhou J. Using ultrasound radiomics analysis to diagnose cervical lymph node metastasis in patients with nasopharyngeal carcinoma. European Radiology. 2023;33(2):774–83.
23.
go back to reference Prativadi R, Dahiya N, Kamaya A, Bhatt S. Chapter 5 Ultrasound characteristics of benign vs malignant cervical Lymph nodes. Semin Ultrasound CT MR. 2017;38(5):506–15.CrossRefPubMed Prativadi R, Dahiya N, Kamaya A, Bhatt S. Chapter 5 Ultrasound characteristics of benign vs malignant cervical Lymph nodes. Semin Ultrasound CT MR. 2017;38(5):506–15.CrossRefPubMed
24.
go back to reference Lambin P, Leijenaar RTH, Deist TM, Peerlings J, de Jong EEC, van Timmeren J, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017;14(12):749–62.CrossRefPubMed Lambin P, Leijenaar RTH, Deist TM, Peerlings J, de Jong EEC, van Timmeren J, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017;14(12):749–62.CrossRefPubMed
25.
go back to reference Tian D, Yan HJ, Shiiya H, Sato M, Shinozaki-Ushiku A, Nakajima J. Machine learning-based radiomic computed tomography phenotyping of thymic epithelial tumors: Predicting pathological and survival outcomes. J Thorac Cardiovasc Surg. 2022. Tian D, Yan HJ, Shiiya H, Sato M, Shinozaki-Ushiku A, Nakajima J. Machine learning-based radiomic computed tomography phenotyping of thymic epithelial tumors: Predicting pathological and survival outcomes. J Thorac Cardiovasc Surg. 2022.
26.
go back to reference Wen Q, Wang Z, Traverso A, Liu Y, Xu R, Feng Y, et al. A radiomics nomogram for the ultrasound-based evaluation of central cervical lymph node metastasis in papillary thyroid carcinoma. Front Endocrinol. 2022;13:1064434.CrossRef Wen Q, Wang Z, Traverso A, Liu Y, Xu R, Feng Y, et al. A radiomics nomogram for the ultrasound-based evaluation of central cervical lymph node metastasis in papillary thyroid carcinoma. Front Endocrinol. 2022;13:1064434.CrossRef
27.
go back to reference Zheng X, Yao Z, Huang Y, Yu Y, Wang Y, Liu Y, et al. Deep learning radiomics can predict axillary lymph node status in early-stage breast cancer. Nat Commun. 2020;11(1):1236.CrossRefPubMedPubMedCentral Zheng X, Yao Z, Huang Y, Yu Y, Wang Y, Liu Y, et al. Deep learning radiomics can predict axillary lymph node status in early-stage breast cancer. Nat Commun. 2020;11(1):1236.CrossRefPubMedPubMedCentral
28.
go back to reference Tian D, Shiiya H, Takahashi M, Terasaki Y, Urushiyama H, Shinozaki-Ushiku A, et al. Noninvasive monitoring of allograft rejection in a rat lung transplant model: Application of machine learning-based (18)F-fluorodeoxyglucose positron emission tomography radiomics. J Heart Lung Transplant. 2022;41(6):722–31.CrossRefPubMed Tian D, Shiiya H, Takahashi M, Terasaki Y, Urushiyama H, Shinozaki-Ushiku A, et al. Noninvasive monitoring of allograft rejection in a rat lung transplant model: Application of machine learning-based (18)F-fluorodeoxyglucose positron emission tomography radiomics. J Heart Lung Transplant. 2022;41(6):722–31.CrossRefPubMed
29.
go back to reference Tian D, Yan H-J, Huang H, Zuo Y-J, Liu M-Z, Zhao J, et al. Machine learning-based prognostic model for patients after lung transplantation. JAMA Netw Open. 2023;6(5):e2312022.CrossRefPubMedPubMedCentral Tian D, Yan H-J, Huang H, Zuo Y-J, Liu M-Z, Zhao J, et al. Machine learning-based prognostic model for patients after lung transplantation. JAMA Netw Open. 2023;6(5):e2312022.CrossRefPubMedPubMedCentral
31.
go back to reference Xu L, Yang P, Liang W, Liu W, Wang W, Luo C, et al. A radiomics approach based on support vector machine using MR images for preoperative lymph node status evaluation in intrahepatic cholangiocarcinoma. Theranostics. 2019;9(18):5374–85.CrossRefPubMedPubMedCentral Xu L, Yang P, Liang W, Liu W, Wang W, Luo C, et al. A radiomics approach based on support vector machine using MR images for preoperative lymph node status evaluation in intrahepatic cholangiocarcinoma. Theranostics. 2019;9(18):5374–85.CrossRefPubMedPubMedCentral
32.
go back to reference Liang W, Yang P, Huang R, Xu L, Wang J, Liu W, et al. A combined nomogram model to preoperatively predict histologic grade in pancreatic neuroendocrine tumors. Clin Cancer Res. 2019;25(2):584–94.CrossRefPubMed Liang W, Yang P, Huang R, Xu L, Wang J, Liu W, et al. A combined nomogram model to preoperatively predict histologic grade in pancreatic neuroendocrine tumors. Clin Cancer Res. 2019;25(2):584–94.CrossRefPubMed
Metadata
Title
Ultrasound-based radiomics machine learning models for diagnosing cervical lymph node metastasis in patients with non-small cell lung cancer: a multicentre study
Authors
Zhiqiang Deng
Xiaoling Liu
Renmei Wu
Haoji Yan
Lingyun Gou
Wenlong Hu
Jiaxin Wan
Chenwanqiu Song
Jing Chen
Daiyuan Ma
Haining Zhou
Dong Tian
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2024
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-024-12306-6

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