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Current Medical Imaging

Editor-in-Chief

ISSN (Print): 1573-4056
ISSN (Online): 1875-6603

Systematic Review Article

Radiomics and Artificial Intelligence in Predicting Axillary Lymph Node Metastasis in Breast Cancer: A Systematic Review

Author(s): Abdullah S. Eldaly, Francisco R. Avila, Ricardo A. Torres-Guzman, Karla Maita, John P. Garcia, Luiza Palmieri Serrano and Antonio J. Forte*

Volume 19, Issue 6, 2023

Published on: 16 September, 2022

Article ID: e220822207829 Pages: 15

DOI: 10.2174/1573405618666220822093226

Price: $65

Abstract

Background: Breast cancer is the most common malignancy and the second most common cause of death in women worldwide. Axillary lymph node metastasis (ALNM) is the most significant prognostic factor in breast cancer. Under the current guidelines, sentinel lymph node biopsy (SLNB) is the standard of axillary staging in patients with clinically-node negative breast cancer. Despite the minimally invasive nature of SLNB, it can cause short and long-term morbidities, including pain, sensory impairment, and upper limb motor dysfunction. However, lymphedema remains the most feared adverse event, and it affects 7% of patients within 36 months of follow-up.

Recently, we have witnessed the implication of radiomics and artificial intelligence domains in the diagnosis and follow-up of many malignancies with promising results. Therefore, we have conducted a systematic search to investigate the potential of radiomics and artificial intelligence in predicting ALNM.

Methods: Four electronic databases were searched: PubMed, Scopus, CINAHL, and Web of Science. We used the Preferred Reporting Items for Systematic Reviews and Meta-Analysis as our basis of organization.

Results: For radiomics, the area under the curve (AUC) for the included studies ranged from 0.715 to 0.93. Accuracy ranged from 67.7% to 98%. Sensitivity and specificity ranged from 70.3% to 97.8% and 58.4% to 98.2%, respectively. For other artificial intelligence methods, AUC ranged from 0.68 to 0.98, while accuracy ranged from 55% to 89%.

Conclusion: The results of radiomics and artificial intelligence in predicting ALNM are promising. However, validation as a substitute for SLNB requires more substantial evidence from large randomized trials.

Keywords: Radiomics, Artificial Intelligence, Breast Cancer, Axillary Lymph Node Biopsy, Lymphedema, Systematic Review

Graphical Abstract

[1]
Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71(3): 209-49.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[2]
Donepudi MS, Kondapalli K, Amos SJ, Venkanteshan P. Breast cancer statistics and markers. J Cancer Res Ther 2014; 10(3): 506-11.
[PMID: 25313729]
[3]
Beenken SW, Urist MM, Zhang Y, et al. Axillary lymph node status, but not tumor size, predicts locoregional recurrence and overall survival after mastectomy for breast cancer. Ann Surg 2003; 237(5): 732-8.
[http://dx.doi.org/10.1097/01.SLA.0000065289.06765.71] [PMID: 12724640]
[4]
Chang JM, Leung JWT, Moy L, Ha SM, Moon WK. Axillary nodal evaluation in breast cancer: State of the art. Radiology 2020; 295(3): 500-15.
[http://dx.doi.org/10.1148/radiol.2020192534] [PMID: 32315268]
[5]
Caudle AS, Cupp JA, Kuerer HM. Management of axillary disease. Surg Oncol Clin N Am 2014; 23(3): 473-86.
[http://dx.doi.org/10.1016/j.soc.2014.03.007] [PMID: 24882346]
[6]
Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: A randomized clinical trial. JAMA 2011; 305(6): 569-75.
[http://dx.doi.org/10.1001/jama.2011.90] [PMID: 21304082]
[7]
Giuliano AE, Ballman KV, McCall L, et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: The ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA 2017; 318(10): 918-26.
[http://dx.doi.org/10.1001/jama.2017.11470] [PMID: 28898379]
[8]
Sclafani LM, Baron RH. Sentinel lymph node biopsy and axillary dissection: Added morbidity of the arm, shoulder and chest wall after mastectomy and reconstruction. Cancer J 2008; 14(4): 216-22.
[http://dx.doi.org/10.1097/PPO.0b013e31817fbe5e] [PMID: 18677128]
[9]
McLaughlin SA, Wright MJ, Morris KT, et al. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements. J Clin Oncol 2008; 26(32): 5213-9.
[http://dx.doi.org/10.1200/JCO.2008.16.3725] [PMID: 18838709]
[10]
Tew K, Irwig L, Matthews A, Crowe P, Macaskill P. Meta-analysis of sentinel node imprint cytology in breast cancer. Br J Surg 2005; 92(9): 1068-80.
[http://dx.doi.org/10.1002/bjs.5139] [PMID: 16106479]
[11]
Lambin P, Leijenaar RTH, Deist TM, et al. Radiomics: The bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 2017; 14(12): 749-62.
[http://dx.doi.org/10.1038/nrclinonc.2017.141] [PMID: 28975929]
[12]
Drukker K, Giger M, Meinel LA, Starkey A, Janardanan J, Abe H. Quantitative ultrasound image analysis of axillary lymph node status in breast cancer patients. Int J CARS 2013; 8(6): 895-903.
[http://dx.doi.org/10.1007/s11548-013-0829-3] [PMID: 23526445]
[13]
Gao Y, Luo Y, Zhao C, et al. Nomogram based on radiomics analysis of primary breast cancer ultrasound images: Prediction of axillary lymph node tumor burden in patients. Eur Radiol 2021; 31(2): 928-37.
[http://dx.doi.org/10.1007/s00330-020-07181-1] [PMID: 32845388]
[14]
Lee YW, Huang CS, Shih CC, Chang RF. Axillary lymph node metastasis status prediction of early-stage breast cancer using convolutional neural networks. Comput Biol Med 2021; 130104206
[http://dx.doi.org/10.1016/j.compbiomed.2020.104206] [PMID: 33421823]
[15]
Yu Y, He Z, Ouyang J, et al. Magnetic resonance imaging radiomics predicts preoperative axillary lymph node metastasis to support surgical decisions and is associated with tumor microenvironment in invasive breast cancer: A machine learning, multicenter study. EBioMedicine 2021; 69103460
[http://dx.doi.org/10.1016/j.ebiom.2021.103460] [PMID: 34233259]
[16]
Yu Y, Tan Y, Xie C, et al. Development and validation of a preoperative magnetic resonance imaging radiomics-based signature to predict axillary lymph node metastasis and disease-free survival in patients with early-stage breast cancer. JAMA Netw Open 2020; 3(12)e2028086
[http://dx.doi.org/10.1001/jamanetworkopen.2020.28086] [PMID: 33289845]
[17]
Dong Y, Feng Q, Yang W, et al. Preoperative prediction of sentinel lymph node metastasis in breast cancer based on radiomics of T2-weighted fat-suppression and diffusion-weighted MRI. Eur Radiol 2018; 28(2): 582-91.
[http://dx.doi.org/10.1007/s00330-017-5005-7] [PMID: 28828635]
[18]
Ha R, Chang P, Karcich J, et al. Axillary lymph node evaluation utilizing convolutional neural networks using MRI dataset. J Digit Imaging 2018; 31(6): 851-6.
[http://dx.doi.org/10.1007/s10278-018-0086-7] [PMID: 29696472]
[19]
Luo J, Ning Z, Zhang S, Feng Q, Zhang Y. Bag of deep features for preoperative prediction of sentinel lymph node metastasis in breast cancer. Phys Med Biol 2018; 63(24)245014
[http://dx.doi.org/10.1088/1361-6560/aaf241] [PMID: 30523819]
[20]
Han L, Zhu Y, Liu Z, et al. Radiomic nomogram for prediction of axillary lymph node metastasis in breast cancer. Eur Radiol 2019; 29(7): 3820-9.
[http://dx.doi.org/10.1007/s00330-018-5981-2] [PMID: 30701328]
[21]
Cui X, Wang N, Zhao Y, et al. Preoperative prediction of axillary lymph node metastasis in breast cancer using radiomics features of DCE-MRI. Sci Rep 2019; 9(1): 2240.
[http://dx.doi.org/10.1038/s41598-019-38502-0] [PMID: 30783148]
[22]
Liu C, Ding J, Spuhler K, et al. Preoperative prediction of sentinel lymph node metastasis in breast cancer by radiomic signatures from dynamic contrast-enhanced MRI. J Magn Reson Imaging 2019; 49(1): 131-40.
[http://dx.doi.org/10.1002/jmri.26224] [PMID: 30171822]
[23]
Shan YN, Xu W, Wang R, Wang W, Pang PP, Shen QJ. A nomogram combined radiomics and kinetic curve pattern as imaging biomarker for detecting metastatic axillary lymph node in invasive breast cancer. Front Oncol 2020; 10: 1463.
[http://dx.doi.org/10.3389/fonc.2020.01463] [PMID: 32983979]
[24]
Tan H, Gan F, Wu Y, et al. Preoperative prediction of axillary lymph node metastasis in breast carcinoma using radiomics features based on the fat-suppressed T2 sequence. Acad Radiol 2020; 27(9): 1217-25.
[http://dx.doi.org/10.1016/j.acra.2019.11.004] [PMID: 31879160]
[25]
Arefan D, Chai R, Sun M, Zuley ML, Wu S. Machine learning prediction of axillary lymph node metastasis in breast cancer: 2D versus 3D radiomic features. Med Phys 2020; 47(12): 6334-42.
[http://dx.doi.org/10.1002/mp.14538] [PMID: 33058224]
[26]
Mao N, Dai Y, Lin F, et al. Radiomics nomogram of DCE-MRI for the prediction of axillary lymph node metastasis in breast cancer. Front Oncol 2020; 10541849
[http://dx.doi.org/10.3389/fonc.2020.541849] [PMID: 33381444]
[27]
Ren T, Cattell R, Duanmu H, et al. Convolutional neural network detection of axillary lymph node metastasis using standard clinical breast MRI. Clin Breast Cancer 2020; 20(3): e301-8.
[http://dx.doi.org/10.1016/j.clbc.2019.11.009] [PMID: 32139272]
[28]
Zha HL, Zong M, Liu XP, et al. Preoperative ultrasound-based radiomics score can improve the accuracy of the Memorial Sloan Kettering Cancer Center nomogram for predicting sentinel lymph node metastasis in breast cancer. Eur J Radiol 2021; 135109512
[http://dx.doi.org/10.1016/j.ejrad.2020.109512] [PMID: 33429302]
[29]
Zheng X, Yao Z, Huang Y, et al. Deep learning radiomics can predict axillary lymph node status in early-stage breast cancer. Nat Commun 2020; 11(1): 1236.
[http://dx.doi.org/10.1038/s41467-020-15027-z] [PMID: 32144248]
[30]
Qiu X, Jiang Y, Zhao Q, Yan C, Huang M, Jiang T. Could ultrasound-based radiomics noninvasively predict axillary lymph node metastasis in breast cancer? J Ultrasound Med 2020; 39(10): 1897-905.
[http://dx.doi.org/10.1002/jum.15294] [PMID: 32329142]
[31]
Guo X, Liu Z, Sun C, et al. Deep learning radiomics of ultrasonography: Identifying the risk of axillary non-sentinel lymph node involvement in primary breast cancer. EBioMedicine 2020; 60103018
[http://dx.doi.org/10.1016/j.ebiom.2020.103018] [PMID: 32980697]
[32]
Yu FH, Wang JX, Ye XH, Deng J, Hang J, Yang B. Ultrasound-based radiomics nomogram: A potential biomarker to predict axillary lymph node metastasis in early-stage invasive breast cancer. Eur J Radiol 2019; 119108658
[http://dx.doi.org/10.1016/j.ejrad.2019.108658] [PMID: 31521878]
[33]
Coronado-Gutiérrez D. Santamaría G, Ganau S, et al. Quantitative ultrasound image analysis of axillary lymph nodes to diagnose metastatic involvement in breast cancer. Ultrasound Med Biol 2019; 45(11): 2932-41.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2019.07.413] [PMID: 31444031]
[34]
Chen F, Liu J, Zhang X, Liao H. Probability analysis of axillary lymph node metastasis in breast cancer patients using particle space-time distribution model. Healthc Technol Lett 2019; 6(6): 266-70.
[http://dx.doi.org/10.1049/htl.2019.0072] [PMID: 32038869]
[35]
Zhang Q, Suo J, Chang W, Shi J, Chen M. Dual-modal computer-assisted evaluation of axillary lymph node metastasis in breast cancer patients on both real-time elastography and B-mode ultrasound. Eur J Radiol 2017; 95: 66-74.
[http://dx.doi.org/10.1016/j.ejrad.2017.07.027] [PMID: 28987700]
[36]
Chmielewski A, Dufort P, Scaranelo AM. A computerized system to assess axillary lymph node malignancy from sonographic images. Ultrasound Med Biol 2015; 41(10): 2690-9.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2015.05.022] [PMID: 26206257]
[37]
Zeng R, Zhang X, Zheng C, et al. Decoupling convolution network for characterizing the metastatic lymph nodes of breast cancer patients. Med Phys 2021; 48(7): 3679-90.
[http://dx.doi.org/10.1002/mp.14876] [PMID: 33825207]
[38]
Yang X, Wu L, Ye W, et al. Deep learning signature based on staging CT for preoperative prediction of sentinel lymph node metastasis in breast cancer. Acad Radiol 2020; 27(9): 1226-33.
[http://dx.doi.org/10.1016/j.acra.2019.11.007] [PMID: 31818648]
[39]
Shaish H, Mutasa S, Makkar J, Chang P, Schwartz L, Ahmed F. Prediction of lymph node maximum standardized uptake value in patients with cancer using a 3D convolutional neural network: A proof-of-concept study. AJR Am J Roentgenol 2019; 212(2): 238-44.
[http://dx.doi.org/10.2214/AJR.18.20094] [PMID: 30540209]
[40]
Ashiba H, Nakayama R. Computerized evaluation scheme to detect metastasis in sentinel lymph nodes using contrast-enhanced computed tomography before breast cancer surgery. Radiological Phys Technol 2019; 12(1): 55-60.
[http://dx.doi.org/10.1007/s12194-018-00491-6] [PMID: 30499048]
[41]
Yang J, Wang T, Yang L, et al. Preoperative prediction of axillary lymph node metastasis in breast cancer using mammography-based radiomics method. Sci Rep 2019; 9(1): 4429.
[http://dx.doi.org/10.1038/s41598-019-40831-z] [PMID: 30872652]
[42]
Mao N, Yin P, Li Q, et al. Radiomics nomogram of contrast-enhanced spectral mammography for prediction of axillary lymph node metastasis in breast cancer: A multicenter study. Eur Radiol 2020; 30(12): 6732-9.
[http://dx.doi.org/10.1007/s00330-020-07016-z] [PMID: 32607630]
[43]
Zarella MD, Breen DE, Reza A, Milutinovic A, Garcia FU. Lymph node metastasis status in breast carcinoma can be predicted via image analysis of tumor histology. Anal Quant Cytol Histol 2015; 37(5): 273-85.
[PMID: 26856112]
[44]
Naguib RNG, Adams AE, Horne CHW, Angus B, Sherbet GV, Lennard TWJ. The detection of nodal metastasis in breast cancer using neural network techniques. Physiol Meas 1996; 17(4): 297-303.
[http://dx.doi.org/10.1088/0967-3334/17/4/007] [PMID: 8953628]
[45]
Duan M, Zhang L, Wang Y, et al. Computational pan-cancer characterization of model-based quantitative transcription regulations dysregulated in regional lymph node metastasis. Comput Biol Med 2021; 135104571
[http://dx.doi.org/10.1016/j.compbiomed.2021.104571] [PMID: 34166881]
[46]
Fanizzi A, Pomarico D, Paradiso A, et al. Predicting of sentinel lymph node status in breast cancer patients with clinically negative nodes: A validation study. Cancers (Basel) 2021; 13(2): 352-2.
[http://dx.doi.org/10.3390/cancers13020352] [PMID: 33477893]
[47]
Marchevsky AM, Shah S, Patel S. Reasoning with uncertainty in pathology: Artificial neural networks and logistic regression as tools for prediction of lymph node status in breast cancer patients. Mod Pathol 1999; 12(5): 505-13.
[48]
Mattfeldt T, Kestler HA, Sinn HP. Prediction of the axillary lymph node status in mammary cancer on the basis of clinicopathological data and flow cytometry. Med Biol Eng Comput 2004; 42(6): 733-9.
[http://dx.doi.org/10.1007/BF02345205] [PMID: 15587463]
[49]
Dietzel M, Baltzer PAT, Dietzel A, et al. Application of artificial neural networks for the prediction of lymph node metastases to the ipsilateral axilla - initial experience in 194 patients using magnetic resonance mammography. Acta Radiol 2010; 51(8): 851-8.
[http://dx.doi.org/10.3109/02841851.2010.498444] [PMID: 20707666]
[50]
Takada M, Sugimoto M, Naito Y, et al. Prediction of axillary lymph node metastasis in primary breast cancer patients using a decision tree-based model. BMC Med Inform Decis Mak 2012; 12(1): 54.
[http://dx.doi.org/10.1186/1472-6947-12-54] [PMID: 22695278]
[51]
Karakis R, Tez M, Kilic YA, Kuru Y, Guler I. A genetic algorithm model based on artificial neural network for prediction of the axillary lymph node status in breast cancer. Eng Appl Artif Intell 2013; 26(3): 945-50.
[http://dx.doi.org/10.1016/j.engappai.2012.10.013]
[52]
Wu JL, Tseng HS, Yang LH, et al. Prediction of axillary lymph node metastases in breast cancer patients based on pathologic information of the primary tumor. Med Sci Monit 2014; 20: 577-81.
[http://dx.doi.org/10.12659/MSM.890345] [PMID: 24714517]
[53]
Dihge L, Ohlsson M, Edén P, Bendahl PO, Rydén L. Artificial neural network models to predict nodal status in clinically node-negative breast cancer. BMC Cancer 2019; 19(1): 610.
[http://dx.doi.org/10.1186/s12885-019-5827-6] [PMID: 31226956]
[54]
Dihge L, Vallon-Christersson J, Hegardt C, et al. Prediction of lymph node metastasis in breast cancer by gene expression and clinicopathological models: Development and validation within a population-based cohort. Clin Cancer Res 2019; 25(21): 6368-81.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-0075] [PMID: 31340938]
[55]
Seker H, Odetayo MO, Petrovic D, et al. Assessment of nodal involvement and survival analysis in breast cancer patients using image cytometric data: Statistical, neural network and fuzzy approaches. Anticancer Res 2002; 22(1A): 433-8.
[PMID: 12017328]
[56]
Sacre RA. Clinical evaluation of axillar lymph nodes compared to surgical and pathological findings. Eur J Surg Oncol 1986; 12(2): 169-73.
[57]
Alvarez S, Añorbe E, Alcorta P, López F, Alonso I, Cortés J. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: A systematic review. AJR Am J Roentgenol 2006; 186(5): 1342-8.
[http://dx.doi.org/10.2214/AJR.05.0936] [PMID: 16632729]
[58]
Liang X, Yu J, Wen B, Xie J, Cai Q, Yang Q. MRI and FDG-PET/CT based assessment of axillary lymph node metastasis in early breast cancer: A meta-analysis. Clin Radiol 2017; 72(4): 295-301.
[http://dx.doi.org/10.1016/j.crad.2016.12.001] [PMID: 28139203]
[59]
Mayerhoefer ME, Materka A, Langs G, et al. Introduction to radiomics. J Nucl Med 2020; 61(4): 488-95.
[60]
Lambin P, Rios-Velazquez E, Leijenaar R, et al. Radiomics: Extracting more information from medical images using advanced feature analysis. Eur J Cancer 2012; 48(4): 441-6.
[61]
Cozzi L, Dinapoli N, Fogliata A, et al. Radiomics based analysis to predict local control and survival in hepatocellular carcinoma patients treated with volumetric modulated arc therapy. BMC Cancer 2017; 17(1): 829.
[http://dx.doi.org/10.1186/s12885-017-3847-7] [PMID: 29207975]
[62]
Sun Y, Reynolds HM, Parameswaran B, et al. Multiparametric MRI and radiomics in prostate cancer: A review. Australas Phys Eng Sci Med 2019; 42(1): 3-25.
[http://dx.doi.org/10.1007/s13246-019-00730-z] [PMID: 30762223]
[63]
Horvat N, Veeraraghavan H, Khan M. et al MR imaging of rectal cancer: Radiomics analysis to assess treatment response after neoadjuvant therapy. Radiology 2018; 287(3): 833-43.
[http://dx.doi.org/10.1148/radiol.2018172300] [PMID: 29514017]
[64]
Institute NC. MRI of breast cancer. 1994. Available from: https://visualsonline.cancer.gov/details.cfm?imageid=2703

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