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Image-based biomarkers for solid tumor quantification

  • Oncology
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Abstract

The last few decades have witnessed tremendous technological developments in image-based biomarkers for tumor quantification and characterization. Initially limited to manual one- and two-dimensional size measurements, image biomarkers have evolved to harness developments not only in image acquisition technology but also in image processing and analysis algorithms. At the same time, clinical validation remains a major challenge for the vast majority of these novel techniques, and there is still a major gap between the latest technological developments and image biomarkers used in everyday clinical practice. Currently, the imaging biomarker field is attracting increasing attention not only because of the tremendous interest in cutting-edge therapeutic developments and personalized medicine but also because of the recent progress in the application of artificial intelligence (AI) algorithms to large-scale datasets. Thus, the goal of the present article is to review the current state of the art for image biomarkers and their use for characterization and predictive quantification of solid tumors. Beginning with an overview of validated imaging biomarkers in current clinical practice, we proceed to a review of AI-based methods for tumor characterization, such as radiomics-based approaches and deep learning.

Key Points

Recent years have seen tremendous technological developments in image-based biomarkers for tumor quantification and characterization.

Image-based biomarkers can be used on an ongoing basis, in a non-invasive (or mildly invasive) way, to monitor the development and progression of the disease or its response to therapy.

We review the current state of the art for image biomarkers, as well as the recent developments in artificial intelligence (AI) algorithms for image processing and analysis.

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Abbreviations

18F-FDG PET:

18F-fluorodeoxyglucose positron emission tomography

AI:

Artificial intelligence

CNN:

Convolutional neural network

EASL:

European Association for the Study of the Liver

mRECIST:

Modified Response Evaluation Criteria in Solid Tumors

PERCIST:

Positron Emission Tomography Response Criteria in Solid Tumors

RECIST:

Response Evaluation Criteria in Solid Tumors

WHO:

World Health Organization

References

  1. Food and Drug Administration & National Institutes of Health. BEST (biomarkers, endpoints, and other tools) resource. NCBI http://www.ncbi.nlm.nih.gov/books/NBK326791. Accessed on 10 Jan 2019.

  2. Aerts HJ (2016) The potential of radiomic-based phenotyping in precision medicine. A review. JAMA Oncol 2(12):1636–1642

    Article  PubMed  Google Scholar 

  3. Amin S, Bathe OF (2016) Response biomarkers: re-envisioning the approach to tailoring drug therapy for cancer. BMC Cancer 16:850

    Article  PubMed  PubMed Central  Google Scholar 

  4. Harry VN, Semple SI, Parkin DE, Gilbert FJ (2010) Use of new imaging techniques to predict tumour response to therapy. Lancet Oncol 11:92–102

    Article  PubMed  Google Scholar 

  5. O’Connor JP, Aboagye EO, Adams JE et al (2017) Imaging biomarker roadmap for cancer studies. Nat Rev Clin Oncol 14(3):169–186

  6. Savadjiev P, Chong J, Dohan A, et al (2019) Demystification of AI-driven medical image interpretation: past, present and future. Eur Radiol 29(3):1616–1624

  7. World Health Organization. ( 1979) . WHO handbook for reporting results of cancer treatment. World Health Organization. Geneva, Switzerland https://www.who.int/iris/handle/10665/37200

  8. Miller AB, Hoogstraten B, Staquet M, Winkler A (1981) Reporting results of cancer treatment. Cancer 47(1):207–214

    Article  CAS  PubMed  Google Scholar 

  9. Therasse P, Arbuck SG, Eisenhauer EA et al (2000) New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 92(3):205–216

  10. Shah GD, Kesari S, Xu R, et al (2006) Comparison of linear and volumetric criteria in assessing tumor response in adult high-grade gliomas. Neuro Oncol 8(1):38–46

  11. Dempsey MF, Condon BR, Hadley DM (2005) Measurement of tumor “size” in recurrent malignant glioma: 1D, 2D, or 3D? AJNR Am J Neuroradiol 26(4):770–776

    PubMed  PubMed Central  Google Scholar 

  12. Aghighi M, Boe J, Rosenberg J et al (2016) Three-dimensional radiologic assessment of chemotherapy response in Ewing sarcoma can be used to predict clinical outcome. Radiology 280(3):905–915

    Article  PubMed  Google Scholar 

  13. Lubner MG, Stabo N, Lubner SJ, Del Rio AM, Song C, Pickhardt PJ (2017) Volumetric versus unidimensional measures of metastatic colorectal cancer in assessing disease response. Clin Colorectal Cancer 16(4):324–333

    Article  PubMed  Google Scholar 

  14. Galanis E, Buckner JC, Maurer MJ et al (2006) Validation of neuroradiologic response assessment in gliomas: measurement by RECIST, two-dimensional, computerassisted tumor area, and computer-assisted tumor volume methods. Neuro Oncol 8(2):156–165

  15. Jaffe CC (2006) Measures of response: RECIST, WHO, and new alternatives. J Clin Oncol 24(20):3245–3251

    Article  PubMed  Google Scholar 

  16. Atri M (2006) New technologies and directed agents for applications of cancer imaging. J Clin Oncol 24(20):3299–3308

    Article  PubMed  Google Scholar 

  17. Bruix J, Sherman M, Llovet JM et al (2001) Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 35(3):421–430

    Article  CAS  PubMed  Google Scholar 

  18. Lencioni R, Llovet JM (2010) Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis 30:52–60

    Article  CAS  PubMed  Google Scholar 

  19. Choi H, Charnsangavej C, Faria SC et al (2007) Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria. J Clin Oncol 25:1753–1759

    Article  PubMed  Google Scholar 

  20. Maier-Hein L, Eisenmann M, Reinke A et al (2018) Why rankings of biomedical image analysis competitions should be interpreted with care. Nat Commun 9(1):5217

  21. Kelloff GJ, Hoffman JM, Johnson B et al (2005) Progress and promise of FDG-PET imaging for cancer patient management and oncologic drug development. Clin Cancer Res 11(8):2785–2808

    Article  CAS  PubMed  Google Scholar 

  22. Wahl RL, Jacene H, Kasamon Y, Lodge MA (2009) From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med 50(Suppl 1):122S–150S

    Article  CAS  PubMed  Google Scholar 

  23. Segal E, Sirlin CB, Ooi C et al (2007) Decoding global gene expression programs in liver cancer by noninvasive imaging. Nat Biotechnol 25:675–680

    Article  CAS  PubMed  Google Scholar 

  24. Chun YS, Vauthey JN, Boonsirikamchai P et al (2009) Association of computed tomography morphologic criteria with pathologic response and survival in patients treated with bevacizumab for colorectal liver metastases. JAMA 302(21):2338–2344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Jansen RW, van Amstel P, Martens RM, Kooi IE, Wesseling P, de Langen AJ (2018) Non-invasive tumor genotyping using radiogenomic biomarkers, a systematic review and oncology-wide pathway analysis. Oncotarget 9(28):20134–20155

    Article  PubMed  PubMed Central  Google Scholar 

  26. Aerts HJ, Velazquez ER, Leijenaar RT et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006

    Article  CAS  PubMed  Google Scholar 

  27. Larue RT, Defraene G, De Ruysscher D, Lambin P, van Elmpt W (2017) Quantitative radiomics studies for tissue characterization: a review of technology and methodological procedures. Br J Radiol 90(1070):20160665

    Article  PubMed  PubMed Central  Google Scholar 

  28. O’Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A (2015) Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res 21(2):249–257

    Article  CAS  PubMed  Google Scholar 

  29. Vallières M, Freeman CR, Skamene SR, El Naq I (2015) A radiomics model from joint FDG-PET and MRI texture features for the prediction of lung metastases in soft-tissue sarcomas of the extremities. Phys Med Biol 60:5471–5496

    Article  PubMed  Google Scholar 

  30. van Griethuysen JJM, Fedorov A, Parmar C et al (2017) Computational radiomics system to decode the radiographic phenotype. Cancer Res 77(21):e104–e107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Chamming’s F, Ueno Y, Ferré R et al (2017) Features from computerized texture analysis of breast cancers at pretreatment MR imaging are associated with response to neoadjuvant chemotherapy. Radiology. https://doi.org/10.1148/radiol.2017170143

  32. Ueno Y, Forghani B, Forghani R et al (2017) Endometrial carcinoma: MR imaging-based texture model for preoperative risk stratification—a preliminary analysis. Radiology 284(3):748–757

    Article  PubMed  Google Scholar 

  33. Parmar C, Leijenaar RTH, Grossmann P et al (2015) Radiomic feature clusters and prognostic signatures specific for lung and head & neck cancer. Sci Rep 5:11044

    Article  PubMed  PubMed Central  Google Scholar 

  34. Schad L (2004) Problems in texture analysis with magnetic resonance imaging. Dialogues Clin Neurosci 6(2):235–242

    PubMed  PubMed Central  Google Scholar 

  35. Schad L, Lundervold A (2006) Influence of resolution and signal to noise ratio on MR image texture. In: Hajek M, Dezortova M, Materka A, Lerski R (eds) Texture analysis for magnetic resonance imaging. HRaNa, Prague, pp 129–149

    Google Scholar 

  36. Guyon I, Elisseeff A (2003) An introduction to variable and feature selection. J Mach Learn Res 3:1157–1182

    Google Scholar 

  37. Hastie T, Tibshirani R, Friedman JH (2009) The elements of statistical learning: data mining, inference, and prediction, 2nd edn. Springer, New York

    Book  Google Scholar 

  38. Kraus WL (2015) Editorial: would you like a hypothesis with those data? Omics and the age of discovery science. Mol Endocrinol 29(11):1531–1534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. LeCun Y, Bengio Y, Hinton G (2015) Deep learning. Nature 521:436–444

    Article  CAS  PubMed  Google Scholar 

  40. Chartrand G, Cheng PM, Vorontsov E et al (2017) Deep learning: a primer for radiologists. Radiographics 37(7):2113–2131

    Article  PubMed  Google Scholar 

  41. Litjens G, Kooi T, Bejnordi BE et al (2017) A survey on deep learning in medical image analysis. Med Image Anal 42:60–88

    Article  PubMed  Google Scholar 

  42. Hosny A, Parmar C, Quackenbush J, Schwartz LH, Aerts HJWL (2018) Artificial intelligence in radiology. Nat Rev Cancer 18(8):500–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ypsilantis PP, Siddique M, Sohn HM et al (2015) Predicting response to neoadjuvant chemotherapy with PET imaging using convolutional neural networks. PLoS One 10(9):e0137036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Li Z, Wang Y, Yu J, Guo Y, Cao W (2017) Deep learning based radiomics (DLR) and its usage in noninvasive IDH1 prediction for low grade glioma. Sci Rep 7(1):5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. US Department of Health and Human Services. Guidance regarding methods for de-identification of protected health information in accordance with the Health Insurance Portability and Accountability Act (HIPAA) privacy rule. http://www.hhs.gov/hipaa/for-professionals/privacy/special-topics/de-identification/index.html. Accessed on 10 Jan 2019

  46. Perez L, Wang J (2017) The effectiveness of data augmentation in image classification using deep learning. Retrieved from http://arxiv.org/abs/1712.04621

    Google Scholar 

  47. Tajbakhsh N, Shin JY, Gurudu SR et al (2016) Convolutional neural networks for medical image analysis: full training or fine tuning? IEEE Trans Med Imaging 35(5):1299–1312

    Article  PubMed  Google Scholar 

  48. Shin HC, Roth HR, Gao M et al (2016) Deep convolutional neural networks for computer-aided detection: CNN architectures, dataset characteristics and transfer learning. IEEE Trans Med Imaging 35(5):1285–1298

    Article  PubMed  Google Scholar 

  49. Hinton G (2018) Deep learning—a technology with the potential to transform health care. JAMA 320(11):1101–1102

    Article  PubMed  Google Scholar 

  50. Anthimopoulos M, Christodoulidis S, Ebner L, Christe A, Mougiakakou S (2016) Lung pattern classification for interstitial lung diseases using a deep convolutional neural network. IEEE Trans Med Imaging 35:1207–1216

    Article  PubMed  Google Scholar 

  51. Lakhani P, Sundaram B (2017) Deep learning at chest radiography: automated classification of pulmonary tuberculosis by using convolutional neural networks. Radiology 284(2):574–582

    Article  PubMed  Google Scholar 

  52. Chang P, Grinband J, Weinberg BD et al (2018) Deep-learning convolutional neural networks accurately classify genetic mutations in gliomas. AJNR Am J Neuroradiol 39(7):1201–1207

  53. Ronneberger O, Fischer P, Brox T (2015) U-net: convolutional networks for biomedical image segmentation. In: Proceedings of the medical image computing and computer-assisted intervention. In: Lecture notes in computer science, vol 9351, pp 234–241

    Google Scholar 

  54. Setio AAA, Ciompi F, Litjens G et al (2016) Pulmonary nodule detection in CT images: false positive reduction using multi-view convolutional networks. IEEE Trans Med Imaging 35:1160–1169

    Article  PubMed  Google Scholar 

  55. Ciompi F, Chung K, van Riel SJ et al (2017) Towards automatic pulmonary nodule management in lung cancer screening with deep learning. Sci Rep 7:46479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lai M (2015) Deep learning for medical image segmentation. Retrieved from https://arxiv.org/abs/1505.02000

    Google Scholar 

  57. Bodalal Z, Trebeschi S, Beets-Tan R (2018) Radiomics: a critical step towards integrated healthcare. Insights Imaging 9(6):911–914

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Benoit Gallix.

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Savadjiev, P., Chong, J., Dohan, A. et al. Image-based biomarkers for solid tumor quantification. Eur Radiol 29, 5431–5440 (2019). https://doi.org/10.1007/s00330-019-06169-w

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