1932

Abstract

Digital pathology, powered by whole-slide imaging technology, has the potential to transform the landscape of cancer research and diagnosis. By converting traditional histopathological specimens into high-resolution digital images, it paves the way for computer-aided analysis, uncovering a new horizon for the integration of artificial intelligence (AI) and machine learning (ML). The accuracy of AI- and ML-driven tools in distinguishing benign from malignant tumors and predicting patient outcomes has ushered in an era of unprecedented opportunities in cancer care. However, this promising field also presents substantial challenges, such as data security, ethical considerations, and the need for standardization. In this review, we delve into the needs that digital pathology addresses in cancer research, the opportunities it presents, its inherent potential, and the challenges it faces. The goal of this review is to stimulate a comprehensive discourse on harnessing digital pathology and AI in health care, with an emphasis on cancer diagnosis and research.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cancerbio-062822-010523
2024-06-12
2024-06-18
Loading full text...

Full text loading...

/deliver/fulltext/cancerbio/8/1/annurev-cancerbio-062822-010523.html?itemId=/content/journals/10.1146/annurev-cancerbio-062822-010523&mimeType=html&fmt=ahah

Literature Cited

  1. Aatresh AA, Alabhya K, Lal S, Kini J, Saxena PP. 2021.. LiverNet: efficient and robust deep learning model for automatic diagnosis of sub-types of liver hepatocellular carcinoma cancer from H&E stained liver histopathology images. . Int. J. Comput.-Assist. Radiol. Surg. 16:(9):154963
    [Crossref] [Google Scholar]
  2. Aeffner F, Zarella MD, Buchbinder N, Bui MM, Goodman MR, et al. 2019.. Introduction to digital image analysis in whole-slide imaging: a white paper from the Digital Pathology Association. . J. Pathol. Inform. 10:(1):9
    [Crossref] [Google Scholar]
  3. Ahmed S, Shaikh A, Alshahrani H, Alghamdi A, Alrizq M, et al. 2021.. Transfer learning approach for classification of histopathology whole slide images. . Sensors 21:(16):5361
    [Crossref] [Google Scholar]
  4. Allen TC. 2019.. Regulating artificial intelligence for a successful pathology future. . Arch. Pathol. Lab. Med. 143:(10):117579
    [Crossref] [Google Scholar]
  5. Atupelage C, Nagahashi H, Kimura F, Yamaguchi M, Tokiya A, et al. 2014.. Computational hepatocellular carcinoma tumor grading based on cell nuclei classification. . J. Med. Imaging 1::034501
    [Crossref] [Google Scholar]
  6. Bach S, Binder A, Montavon G, Klauschen F, Müller K-R, Samek W. 2015.. On pixel-wise explanations for non-linear classifier decisions by layer-wise relevance propagation. . PLOS ONE 10:(7):e0130140
    [Crossref] [Google Scholar]
  7. Balthazar P, Harri P, Prater A, Safdar NM. 2018.. Protecting your patients’ interests in the era of big data, artificial intelligence, and predictive analytics. . J. Am. Coll. Radiol. 15:(3, Part B):58086
    [Crossref] [Google Scholar]
  8. Barker J, Hoogi A, Depeursinge A, Rubin DL. 2016.. Automated classification of brain tumor type in whole-slide digital pathology images using local representative tiles. . Med. Image Anal. 30::6071
    [Crossref] [Google Scholar]
  9. Basu S, Kolouri S, Rohde GK. 2014.. Detecting and visualizing cell phenotype differences from microscopy images using transport-based morphometry. . PNAS 111:(9):344853
    [Crossref] [Google Scholar]
  10. Bera K, Schalper KA, Rimm DL, Velcheti V, Madabhushi A. 2019.. Artificial intelligence in digital pathology—new tools for diagnosis and precision oncology. . Nat. Rev. Clin. Oncol. 16:(11):70315
    [Crossref] [Google Scholar]
  11. Bian Z, Guo C, Jiang S, Zhu J, Wang R, et al. 2020.. Autofocusing technologies for whole slide imaging and automated microscopy. . J. Biophotonics 13:(12):e202000227
    [Crossref] [Google Scholar]
  12. Bianconi F, Álvarez-Larrán A, Fernández A. 2015.. Discrimination between tumour epithelium and stroma via perception-based features. . Neurocomputing 154::11926
    [Crossref] [Google Scholar]
  13. Bilal M, Raza SEA, Azam A, Graham S, Ilyas M, et al. 2021.. Development and validation of a weakly supervised deep learning framework to predict the status of molecular pathways and key mutations in colorectal cancer from routine histology images: a retrospective study. . Lancet Digit. Health 3:(12):e763
    [Crossref] [Google Scholar]
  14. Bisson T, Franz M, Dogon OI, Romberg D, Jansen C, et al. 2023.. Anonymization of whole slide images in histopathology for research and education. . Digit. Health 9:. https://doi.org/10.1177/20552076231171475
    [Google Scholar]
  15. Boissin C, Laflamme L, Fransén J, Lundin M, Huss F, et al. 2023.. Development and evaluation of deep learning algorithms for assessment of acute burns and the need for surgery. . Sci. Rep. 13::1794
    [Crossref] [Google Scholar]
  16. Border SP, Sarder P. 2022.. From what to why, the growing need for a focus shift toward explainability of AI in digital pathology. . Front. Physiol. 12::821217
    [Crossref] [Google Scholar]
  17. Bulten W, Pinckaers H, van Boven H, Vink R, de Bel T, et al. 2020.. Automated deep-learning system for Gleason grading of prostate cancer using biopsies: a diagnostic study. . Lancet Oncol. 21:(2):23341
    [Crossref] [Google Scholar]
  18. Bychkov D, Linder N, Turkki R, Nordling S, Kovanen PE, et al. 2018.. Deep learning based tissue analysis predicts outcome in colorectal cancer. . Sci. Rep. 8::3395
    [Crossref] [Google Scholar]
  19. Campanella G, Hanna MG, Geneslaw L, Miraflor A, Krauss Silva VW, et al. 2019.. Clinical-grade computational pathology using weakly supervised deep learning on whole slide images. . Nat. Med. 25:(8):13019
    [Crossref] [Google Scholar]
  20. Chen L, Zeng H, Xiang Y, Huang Y, Luo Y, Ma X. 2021.. Histopathological images and multi-omics integration predict molecular characteristics and survival in lung adenocarcinoma. . Front. Cell Dev. Biol. 9::720110
    [Crossref] [Google Scholar]
  21. Cheng W-C, Saleheen F, Badano A. 2019.. Assessing color performance of whole-slide imaging scanners for digital pathology. . Color Res. Appl. 44:(3):32234
    [Crossref] [Google Scholar]
  22. Clark K, Vendt B, Smith K, Freymann J, Kirby J, et al. 2013.. The Cancer Imaging Archive (TCIA): maintaining and operating a public information repository. . J. Digit. Imaging 26:(6):104557
    [Crossref] [Google Scholar]
  23. Coudray N, Ocampo PS, Sakellaropoulos T, Narula N, Snuderl M, et al. 2018.. Classification and mutation prediction from non–small cell lung cancer histopathology images using deep learning. . Nat. Med. 24:(10):155967
    [Crossref] [Google Scholar]
  24. Coulter C, McKay F, Hallowell N, Browning L, Colling R, et al. 2022.. Understanding the ethical and legal considerations of digital pathology. . J. Pathol. Clin. Res. 8:(2):10115
    [Crossref] [Google Scholar]
  25. Couture HD, Williams LA, Geradts J, Nyante SJ, Butler EN, et al. 2018.. Image analysis with deep learning to predict breast cancer grade, ER status, histologic subtype, and intrinsic subtype. . npj Breast Cancer 4::30
    [Crossref] [Google Scholar]
  26. Davnall F, Yip CSP, Ljungqvist G, Selmi M, Ng F, et al. 2012.. Assessment of tumor heterogeneity: an emerging imaging tool for clinical practice?. Insights Imaging 3:(6):57389
    [Crossref] [Google Scholar]
  27. Diao JA, Wang JK, Chui WF, Mountain V, Gullapally SC, et al. 2021.. Human-interpretable image features derived from densely mapped cancer pathology slides predict diverse molecular phenotypes. . Nat. Commun. 12::1613
    [Crossref] [Google Scholar]
  28. Đorđević M, Životić M, Radojević Škodrić S, Nešović Ostojić J, Marković Lipkovski J, et al. 2021.. Effects of automation on sustainability of immunohistochemistry laboratory. . Healthcare 9:(7):866
    [Crossref] [Google Scholar]
  29. Duanmu H, Bhattarai S, Li H, Cheng CC, Wang F, et al. 2021.. Spatial attention–based deep learning system for breast cancer pathological complete response prediction with serial histopathology images in multiple stains. . In Medical Image Computing and Computer Assisted Intervention (MICCAI 2021), 24th International Conference, Strasbourg, France, September 27–October 1, 2021, Proceedings, Part VIII, pp. 55060. Berlin:: Springer
    [Google Scholar]
  30. Ehteshami Bejnordi B, Veta M, van Diest PJ, van Ginneken B, Karssemeijer N, et al. 2017.. Diagnostic assessment of deep learning algorithms for detection of lymph node metastases in women with breast cancer. . JAMA 318:(22):2199210
    [Crossref] [Google Scholar]
  31. Eloy C, Vale J, Curado M, Polónia A, Campelos S, et al. 2021.. Digital pathology workflow implementation at IPATIMUP. . Diagnostics 11:(11):2111
    [Crossref] [Google Scholar]
  32. Faratian D, Kay C, Robson T, Campbell FM, Grant M, et al. 2009.. Automated image analysis for high-throughput quantitative detection of ER and PR expression levels in large-scale clinical studies: the TEAM Trial experience. . Histopathology 55:(5):58793
    [Crossref] [Google Scholar]
  33. Fenstermaker M, Tomlins SA, Singh K, Wiens J, Morgan TM. 2020.. Development and validation of a deep-learning model to assist with renal cell carcinoma histopathologic interpretation. . Urology 144::15257
    [Crossref] [Google Scholar]
  34. Fu H, Mi W, Pan B, Guo Y, Li J, et al. 2021.. Automatic pancreatic ductal adenocarcinoma detection in whole slide images using deep convolutional neural networks. . Front. Oncol. 11::665929
    [Crossref] [Google Scholar]
  35. Gamper J, Koohbanani NA, Benes K, Graham S, Jahanifar M, et al. 2020.. PanNuke dataset extension, insights and baselines. . arXiv:2003.10778 [eess.IV]
  36. Ghaznavi F, Evans A, Madabhushi A, Feldman M. 2013.. Digital imaging in pathology: whole-slide imaging and beyond. . Annu. Rev. Pathol. Mech. Dis. 8::33159
    [Crossref] [Google Scholar]
  37. Gilpin LH, Bau D, Yuan BZ, Bajwa A, Specter M, Kagal L. 2019.. Explaining explanations: an overview of interpretability of machine learning. . In 2018 IEEE 5th International Conference on Data Science and Advanced Analytics (DSAA), pp. 8089. Piscataway, NJ:: IEEE
    [Google Scholar]
  38. Giraldo NA, Nguyen P, Engle EL, Kaunitz GJ, Cottrell TR, et al. 2018.. Multidimensional, quantitative assessment of PD-1/PD-L1 expression in patients with Merkel cell carcinoma and association with response to pembrolizumab. . J. Immunother. Cancer 6:(1):99
    [Crossref] [Google Scholar]
  39. Graham S, Vu QD, Raza SEA, Azam A, Tsang YW, et al. 2019.. Hover-Net: Simultaneous segmentation and classification of nuclei in multi-tissue histology images. . Med. Image Anal. 58::101563
    [Crossref] [Google Scholar]
  40. Guo H, Birsa J, Farahani N, Hartman DJ, Piccoli A, et al. 2016.. Digital pathology and anatomic pathology laboratory information system integration to support digital pathology sign-out. . J. Pathol. Inform. 7::23
    [Crossref] [Google Scholar]
  41. Gupta D, Saul M, Gilbertson J. 2004.. Evaluation of a deidentification (De-Id) software engine to share pathology reports and clinical documents for research. . Am. J. Clin. Pathol. 121:(2):17686
    [Crossref] [Google Scholar]
  42. Gurcan MN, Boucheron L, Can A, Madabhushi A, Rajpoot N, Yener B. 2009.. Histopathological image analysis: a review. . IEEE Rev. Biomed. Eng. 2::14771
    [Crossref] [Google Scholar]
  43. Gutman DA, Cobb J, Somanna D, Park Y, Wang F, et al. 2013.. Cancer Digital Slide Archive: an informatics resource to support integrated in silico analysis of TCGA pathology data. . J. Am. Med. Inform. Assoc. 20:(6):109198
    [Crossref] [Google Scholar]
  44. Haghighi M, Tolley J, Schito AN, Kwan R, Garcia C, et al. 2021.. Whole slide imaging for teleconsultation: the Mount Sinai Hospital, Labcorp Dianon, and Philips collaborative experience. . J. Pathol. Inform. 12::53
    [Crossref] [Google Scholar]
  45. Hanna MG, Reuter VE, Ardon O, Kim D, Sirintrapun SJ, et al. 2020.. Validation of a digital pathology system including remote review during the COVID-19 pandemic. . Mod. Pathol. 33:(11):211527
    [Crossref] [Google Scholar]
  46. Haralick RM, Shanmugam K, Dinstein I. 1973.. Textural features for image classification. . IEEE Trans. Syst. Man Cybern. SMC-3:(6):61021
    [Crossref] [Google Scholar]
  47. Harmon SA, Sanford TH, Brown GT, Yang C, Mehralivand S, et al. 2020.. Multiresolution application of artificial intelligence in digital pathology for prediction of positive lymph nodes from primary tumors in bladder cancer. . JCO Clin. Cancer Inform. 4::36782
    [Crossref] [Google Scholar]
  48. Heindl A, Nawaz S, Yuan Y. 2015.. Mapping spatial heterogeneity in the tumor microenvironment: a new era for digital pathology. . Lab. Investig. 95:(4):37784
    [Crossref] [Google Scholar]
  49. Höhn J, Krieghoff-Henning E, Jutzi TB, von Kalle C, Utikal JS, et al. 2021.. Combining CNN-based histologic whole slide image analysis and patient data to improve skin cancer classification. . Eur. J. Cancer 149::94101
    [Crossref] [Google Scholar]
  50. Holub P, Müller H, Bíl T, Pireddu L, Plass M, et al. 2023.. Privacy risks of whole-slide image sharing in digital pathology. . Nat. Commun. 14::2577
    [Crossref] [Google Scholar]
  51. Homeyer A, Geißler C, Schwen LO, Zakrzewski F, Evans T, et al. 2022.. Recommendations on compiling test datasets for evaluating artificial intelligence solutions in pathology. . Mod. Pathol. 35:(12):175969
    [Crossref] [Google Scholar]
  52. Hoskins KF, Danciu OC, Ko NY, Calip GS. 2021.. Association of race/ethnicity and the 21-gene recurrence score with breast cancer–specific mortality among US women. . JAMA Oncol. 7:(3):37078
    [Crossref] [Google Scholar]
  53. Howard FM, Dolezal J, Kochanny S, Schulte J, Chen H, et al. 2021.. The impact of site-specific digital histology signatures on deep learning model accuracy and bias. . Nat. Commun. 12::4423
    [Crossref] [Google Scholar]
  54. Ilse M, Tomczak JM, Welling M. 2018.. Attention-based deep multiple instance learning. . Proc. Mach. Learn. Res. 80::212736
    [Google Scholar]
  55. Indu M, Rathy R, Binu MP. 2016.. “ Slide less pathology”: fairy tale or reality?. J. Oral Maxillofac. Pathol. 20:(2):28488
    [Crossref] [Google Scholar]
  56. Irshad H, Jalali S, Roux L, Racoceanu D, Hwee LJ, et al. 2013.. Automated mitosis detection using texture, SIFT features and HMAX biologically inspired approach. . J. Pathol. Inform. 4:(Suppl.):S12
    [Crossref] [Google Scholar]
  57. Jaber MI, Song B, Taylor C, Vaske CJ, Benz SC, et al. 2020.. A deep learning image-based intrinsic molecular subtype classifier of breast tumors reveals tumor heterogeneity that may affect survival. . Breast Cancer Res. 22:(1):12
    [Crossref] [Google Scholar]
  58. Janowczyk A, Zuo R, Gilmore H, Feldman M, Madabhushi A. 2019.. HistoQC: an open-source quality control tool for digital pathology slides. . JCO Clin. Cancer Inform. 3::17
    [Crossref] [Google Scholar]
  59. Johnson DB, Bordeaux J, Kim JY, Vaupel C, Rimm DL, et al. 2018.. Quantitative spatial profiling of PD-1/PD-L1 interaction and HLA-DR/IDO-1 predicts improved outcomes of anti-PD-1 therapies in metastatic melanoma. . Clin. Cancer Res. 24:(21):525060
    [Crossref] [Google Scholar]
  60. Katare P, Gorthi SS. 2021.. Recent technical advances in whole slide imaging instrumentation. . J. Microsc. 284:(2):10317
    [Crossref] [Google Scholar]
  61. Kather JN, Pearson AT, Halama N, Jäger D, Krause J, et al. 2019.. Deep learning can predict microsatellite instability directly from histology in gastrointestinal cancer. . Nat. Med. 25:(7):105456
    [Crossref] [Google Scholar]
  62. Kather JN, Weis C-A, Bianconi F, Melchers SM, Schad LR, et al. 2016.. Multi-class texture analysis in colorectal cancer histology. . Sci. Rep. 6::27988
    [Crossref] [Google Scholar]
  63. Kiani A, Uyumazturk B, Rajpurkar P, Wang A, Gao R, et al. 2020.. Impact of a deep learning assistant on the histopathologic classification of liver cancer. . npj Digit. Med. 3::23
    [Crossref] [Google Scholar]
  64. Kim I, Kang K, Song Y, Kim T-J. 2022.. Application of artificial intelligence in pathology: trends and challenges. . Diagnostics 12:(11):2794
    [Crossref] [Google Scholar]
  65. Köteles MM, Vigdorovits A, Kumar D, Mihai I-M, Jurescu A, et al. 2023.. Comparative evaluation of breast ductal carcinoma grading: a deep-learning model and general pathologists’ assessment approach. . Diagnostics 13:(14):2326
    [Crossref] [Google Scholar]
  66. Koyuncu CF, Nag R, Lu C, Corredor G, Viswanathan VS, et al. 2022.. Image analysis reveals differences in tumor multinucleations in Black and White patients with human papillomavirus–associated oropharyngeal squamous cell carcinoma. . Cancer 128:(21):383142
    [Crossref] [Google Scholar]
  67. Kumar N, Verma R, Anand D, Zhou Y, Onder OF, et al. 2020.. A multi-organ nucleus segmentation challenge. . IEEE Trans. Med. Imaging 39:(5):138091
    [Crossref] [Google Scholar]
  68. Lambin P, Leijenaar RTH, Deist TM, Peerlings J, de Jong EEC, et al. 2017.. Radiomics: the bridge between medical imaging and personalized medicine. . Nat. Rev. Clin. Oncol. 14:(12):74962
    [Crossref] [Google Scholar]
  69. Larrazabal AJ, Nieto N, Peterson V, Milone DH, Ferrante E. 2020.. Gender imbalance in medical imaging datasets produces biased classifiers for computer-aided diagnosis. . PNAS 117:(23):1259294
    [Crossref] [Google Scholar]
  70. LeCun Y, Bengio Y, Hinton G. 2015.. Deep learning. . Nature 521:(7553):43644
    [Crossref] [Google Scholar]
  71. Li L, Dangott BJ, Parwani AV. 2010.. Development and use of a genitourinary pathology digital teaching set for trainee education. . J. Pathol. Inform. 1:(1):2
    [Crossref] [Google Scholar]
  72. Linder N, Konsti J, Turkki R, Rahtu E, Lundin M, et al. 2012.. Identification of tumor epithelium and stroma in tissue microarrays using texture analysis. . Diagn. Pathol. 7:(1):22
    [Crossref] [Google Scholar]
  73. Litjens G, Sánchez CI, Timofeeva N, Hermsen M, Nagtegaal I, et al. 2016.. Deep learning as a tool for increased accuracy and efficiency of histopathological diagnosis. . Sci. Rep. 6::26286
    [Crossref] [Google Scholar]
  74. Louis DN, Feldman M, Carter AB, Dighe AS, Pfeifer JD, et al. 2016.. Computational pathology: a path ahead. . Arch. Pathol. Lab. Med. 140:(1):4150
    [Crossref] [Google Scholar]
  75. Louis DN, Gerber GK, Baron JM, Bry L, Dighe AS, et al. 2014.. Computational pathology: an emerging definition. . Arch. Pathol. Lab. Med. 138:(9):113338
    [Crossref] [Google Scholar]
  76. Lu MY, Williamson DFK, Chen TY, Chen RJ, Barbieri M, Mahmood F. 2021.. Data-efficient and weakly supervised computational pathology on whole-slide images. . Nat. Biomed. Eng. 5:(6):55570
    [Crossref] [Google Scholar]
  77. McKay F, Williams BJ, Prestwich G, Bansal D, Hallowell N, Treanor D. 2022.. The ethical challenges of artificial intelligence–driven digital pathology. . J. Pathol. Clin. Res. 8:(3):20916
    [Crossref] [Google Scholar]
  78. Mobadersany P, Yousefi S, Amgad M, Gutman DA, Barnholtz-Sloan JS, et al. 2018.. Predicting cancer outcomes from histology and genomics using convolutional networks. . PNAS 115:(13):E297079
    [Crossref] [Google Scholar]
  79. Mukhopadhyay S, Booth AL, Calkins SM, Doxtader EE, Fine SW, et al. 2020.. Leveraging technology for remote learning in the era of COVID-19 and social distancing. . Arch. Pathol. Lab. Med. 144:(9):102736
    [Crossref] [Google Scholar]
  80. Mukhopadhyay S, Feldman MD, Abels E, Ashfaq R, Beltaifa S, et al. 2018.. Whole slide imaging versus microscopy for primary diagnosis in surgical pathology: a multicenter blinded randomized noninferiority study of 1992 cases (pivotal study). . Am. J. Surg. Pathol. 42:(1):39
    [Crossref] [Google Scholar]
  81. Nakagawa K, Moukheiber L, Celi LA, Patel M, Mahmood F, et al. 2023.. AI in pathology: What could possibly go wrong?. Semin. Diagn. Pathol. 40:(2):1008
    [Crossref] [Google Scholar]
  82. Nateghi R, Danyali H, Helfroush MS. 2017.. Maximized inter-class weighted mean for fast and accurate mitosis cells detection in breast cancer histopathology images. . J. Med. Syst. 41:(9):146
    [Crossref] [Google Scholar]
  83. Niazi MKK, Parwani AV, Gurcan MN. 2019.. Digital pathology and artificial intelligence. . Lancet Oncol. 20:(5):e25361
    [Crossref] [Google Scholar]
  84. Ning Z, Pan W, Chen Y, Xiao Q, Zhang X, et al. 2020.. Integrative analysis of cross-modal features for the prognosis prediction of clear cell renal cell carcinoma. . Bioinformatics 36:(9):288895
    [Crossref] [Google Scholar]
  85. Nir G, Hor S, Karimi D, Fazli L, Skinnider BF, et al. 2018.. Automatic grading of prostate cancer in digitized histopathology images: learning from multiple experts. . Med. Image Anal. 50::16780
    [Crossref] [Google Scholar]
  86. Obermeyer Z, Powers B, Vogeli C, Mullainathan S. 2019.. Dissecting racial bias in an algorithm used to manage the health of populations. . Science 366:(6464):44753
    [Crossref] [Google Scholar]
  87. Omar M, Xu Z, Rand SB, Mohammad M, Salles DC, et al. 2022.. Using attention-based deep learning to predict ERG:TMPRSS2 fusion status in prostate cancer from whole slide images. . bioRxiv 2022.11.18.517111. https://doi.org/10.1101/2022.11.18.517111
  88. Ordi J, Castillo P, Saco A, del Pino M, Ordi O, et al. 2015a.. Validation of whole slide imaging in the primary diagnosis of gynaecological pathology in a university hospital. . J. Clin. Pathol. 68:(1):3339
    [Crossref] [Google Scholar]
  89. Ordi O, Bombí JA, Martínez A, Ramírez J, Alòs L, et al. 2015b.. Virtual microscopy in the undergraduate teaching of pathology. . J. Pathol. Inform. 6::1
    [Crossref] [Google Scholar]
  90. Paik S, Shak S, Tang G, Kim C, Baker J, et al. 2004.. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. . N. Engl. J. Med. 351:(27):281726
    [Crossref] [Google Scholar]
  91. Pan SJ, Yang Q. 2010.. A survey on transfer learning. . IEEE Trans. Knowl. Data Eng. 22:(10):134559
    [Crossref] [Google Scholar]
  92. Panch T, Mattie H, Atun R. 2019.. Artificial intelligence and algorithmic bias: implications for health systems. . J. Glob. Health 9:(2):010318
    [Crossref] [Google Scholar]
  93. Patel A, Balis UGJ, Cheng J, Li Z, Lujan G, et al. 2021.. Contemporary whole slide imaging devices and their applications within the modern pathology department: a selected hardware review. . J. Pathol. Inform. 12::50
    [Crossref] [Google Scholar]
  94. Prall F, Hühns M. 2019.. Quantitative evaluation of TP53 immunohistochemistry to predict gene mutations: lessons learnt from a series of colorectal carcinomas. . Hum. Pathol. 84::24653
    [Crossref] [Google Scholar]
  95. Price WN, Cohen IG. 2019.. Privacy in the age of medical big data. . Nat. Med. 25:(1):3743
    [Crossref] [Google Scholar]
  96. Prichard JW. 2014.. Overview of automated immunohistochemistry. . Arch. Pathol. Lab. Med. 138:(12):157882
    [Crossref] [Google Scholar]
  97. Rawat RR, Ruderman D, Macklin P, Rimm DL, Agus DB. 2018.. Correlating nuclear morphometric patterns with estrogen receptor status in breast cancer pathologic specimens. . npj Breast Cancer 4::32
    [Crossref] [Google Scholar]
  98. Reid MD, Bagci P, Ohike N, Saka B, Erbarut Seven I, et al. 2015.. Calculation of the Ki67 index in pancreatic neuroendocrine tumors: a comparative analysis of four counting methodologies. . Mod. Pathol. 28:(5):68694
    [Crossref] [Google Scholar]
  99. Retamero JA, Aneiros-Fernandez J, del Moral RG. 2019.. Complete digital pathology for routine histopathology diagnosis in a multicenter hospital network. . Arch. Pathol. Lab. Med. 144:(2):22128
    [Crossref] [Google Scholar]
  100. Rosenthal J, Carelli R, Omar M, Brundage D, Halbert E, et al. 2022.. Building tools for machine learning and artificial intelligence in cancer research: best practices and a case study with the PathML toolkit for computational pathology. . Mol. Cancer Res. 20:(2):2026
    [Crossref] [Google Scholar]
  101. Sarode VR, Xiang QD, Christie A, Collins R, Rao R, et al. 2015.. Evaluation of HER2/neu status by immunohistochemistry using computer-based image analysis and correlation with gene amplification by fluorescence in situ hybridization assay: a 10-year experience and impact of test standardization on concordance rate. . Arch. Pathol. Lab. Med. 139:(7):92228
    [Crossref] [Google Scholar]
  102. Schmauch B, Romagnoni A, Pronier E, Saillard C, Maillé P, et al. 2020.. A deep learning model to predict RNA-Seq expression of tumours from whole slide images. . Nat Commun. 11::3877
    [Crossref] [Google Scholar]
  103. Schneider L, Laiouar-Pedari S, Kuntz S, Krieghoff-Henning E, Hekler A, et al. 2022.. Integration of deep learning–based image analysis and genomic data in cancer pathology: a systematic review. . Eur. J. Cancer 160::8091
    [Crossref] [Google Scholar]
  104. Schrammen PL, Ghaffari Laleh N, Echle A, Truhn D, Schulz V, et al. 2022.. Weakly supervised annotation-free cancer detection and prediction of genotype in routine histopathology. . J. Pathol. 256:(1):5060
    [Crossref] [Google Scholar]
  105. Schüffler PJ, Geneslaw L, Yarlagadda DVK, Hanna MG, Samboy J, et al. 2021.. Integrated digital pathology at scale: a solution for clinical diagnostics and cancer research at a large academic medical center. . J. Am. Med. Inform. Assoc. 28:(9):187484
    [Crossref] [Google Scholar]
  106. Selvaraju RR, Cogswell M, Das A, Vedantam R, Parikh D, Batra D. 2020.. Grad-CAM: visual explanations from deep networks via gradient-based localization. . Int. J. Comput. Vis. 128:(2):33659
    [Crossref] [Google Scholar]
  107. Shin HC, Roth HR, Gao M, Lu L, Xu Z, et al. 2016.. Deep convolutional neural networks for computer-aided detection: CNN architectures, dataset characteristics and transfer learning. . IEEE Trans. Med. Imaging 35:(5):128598
    [Crossref] [Google Scholar]
  108. Sikaroudi M, Rahnamayan S, Tizhoosh HR. 2022.. Hospital-agnostic image representation learning in digital pathology. . In 44th Annual International Conference of the IEEE Engineering in Medicine & Biology Society, pp. 305558. Piscataway, NJ:: IEEE
    [Google Scholar]
  109. Sirinukunwattana K, Domingo E, Richman SD, Redmond KL, Blake A, et al. 2021.. Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning. . Gut 70:(3):54454
    [Crossref] [Google Scholar]
  110. Stepanova P, Kumar D, Cavonius K, Korpikoski J, Sirjala J, et al. 2023.. Beneficial behavioral effects of chronic cerebral dopamine neurotrophic factor (CDNF) infusion in the N171-82Q transgenic model of Huntington's disease. . Sci. Rep. 13::2953
    [Crossref] [Google Scholar]
  111. Ström P, Kartasalo K, Olsson H, Solorzano L, Delahunt B, et al. 2020.. Artificial intelligence for diagnosis and grading of prostate cancer in biopsies: a population-based, diagnostic study. . Lancet Oncol. 21:(2):22232
    [Crossref] [Google Scholar]
  112. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, et al. 2021.. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. . CA Cancer J. Clin. 71:(3):20949
    [Crossref] [Google Scholar]
  113. Taatjes DJ, Bouffard NA, Barrow T, Devitt KA, Gardner J-A, Braet F. 2019.. Quantitative pixel intensity- and color-based image analysis on minimally compressed files: implications for whole-slide imaging. . Histochem. Cell Biol. 152:(1):1323
    [Crossref] [Google Scholar]
  114. Tabibu S, Vinod PK, Jawahar CV. 2019.. Pan–renal cell carcinoma classification and survival prediction from histopathology images using deep learning. . Sci. Rep. 9::10509
    [Crossref] [Google Scholar]
  115. Tan WCC, Nerurkar SN, Cai HY, Ng HHM, Wu D, et al. 2020.. Overview of multiplex immunohistochemistry/immunofluorescence techniques in the era of cancer immunotherapy. . Cancer Commun. 40:(4):13553
    [Crossref] [Google Scholar]
  116. Tay TKY, Thike AA, Pathmanathan N, Jara-Lazaro AR, Iqbal J, et al. 2018.. Using computer assisted image analysis to determine the optimal Ki67 threshold for predicting outcome of invasive breast cancer. . Oncotarget 9:(14):1161930
    [Crossref] [Google Scholar]
  117. Tellez D, Litjens G, Bándi P, Bulten W, Bokhorst J-M, et al. 2019.. Quantifying the effects of data augmentation and stain color normalization in convolutional neural networks for computational pathology. . Med. Image Anal. 58::101544
    [Crossref] [Google Scholar]
  118. Tizhoosh HR, Pantanowitz L. 2018.. Artificial intelligence and digital pathology: challenges and opportunities. . J. Pathol. Inform. 9::38
    [Crossref] [Google Scholar]
  119. Toki MI, Merritt CR, Wong PF, Smithy JW, Kluger HM, et al. 2019.. High-plex predictive marker discovery for melanoma immunotherapy-treated patients using digital spatial profiling. . Clin. Cancer Res. 25:(18):550312
    [Crossref] [Google Scholar]
  120. Tran KA, Kondrashova O, Bradley A, Williams ED, Pearson JV, Waddell N. 2021.. Deep learning in cancer diagnosis, prognosis and treatment selection. . Genome Med. 13:(1):152
    [Crossref] [Google Scholar]
  121. Turbin DA, Leung S, Cheang MCU, Kennecke HA, Montgomery KD, et al. 2008.. Automated quantitative analysis of estrogen receptor expression in breast carcinoma does not differ from expert pathologist scoring: a tissue microarray study of 3,484 cases. . Breast Cancer Res. Treat. 110:(3):41726
    [Crossref] [Google Scholar]
  122. Turkki R, Linder N, Holopainen T, Wang Y, Grote A, et al. 2015.. Assessment of tumour viability in human lung cancer xenografts with texture-based image analysis. . J. Clin. Pathol. 68:(8):61421
    [Crossref] [Google Scholar]
  123. Vanguri RS, Luo J, Aukerman AT, Egger JV, Fong CJ, et al. 2022.. Multimodal integration of radiology, pathology and genomics for prediction of response to PD-(L)1 blockade in patients with non-small cell lung cancer. . Nat. Cancer 3:(10):115164
    [Crossref] [Google Scholar]
  124. Veta M, Heng YJ, Stathonikos N, Bejnordi BE, Beca F, et al. 2019.. Predicting breast tumor proliferation from whole-slide images: the TUPAC16 challenge. . Med. Image Anal. 54::11121
    [Crossref] [Google Scholar]
  125. Volynskaya Z, Chow H, Evans A, Wolff A, Lagmay-Traya C, Asa SL. 2017.. Integrated pathology informatics enables high-quality personalized and precision medicine: digital pathology and beyond. . Arch. Pathol. Lab. Med. 142:(3):36982
    [Crossref] [Google Scholar]
  126. Wang KS, Yu G, Xu C, Meng XH, Zhou J, et al. 2021.. Accurate diagnosis of colorectal cancer based on histopathology images using artificial intelligence. . BMC Med. 19::76
    [Crossref] [Google Scholar]
  127. Wang X, Chen H, Gan C, Lin H, Dou Q, et al. 2020.. Weakly supervised deep learning for whole slide lung cancer image analysis. . IEEE Trans. Cybern. 50:(9):395062
    [Crossref] [Google Scholar]
  128. Wang Y, Lei B, Elazab A, Tan E-L, Wang W, et al. 2020.. Breast cancer image classification via multi-network features and dual-network orthogonal low-rank learning. . IEEE Access 8::2777992
    [Crossref] [Google Scholar]
  129. Wharton KA, Wood D, Manesse M, Maclean KH, Leiss F, Zuraw A. 2021.. Tissue multiplex analyte detection in anatomic pathology—pathways to clinical implementation. . Front. Mol. Biosci. 8::672531
    [Crossref] [Google Scholar]
  130. Xue Y, Ye J, Zhou Q, Long LR, Antani S, et al. 2021.. Selective synthetic augmentation with HistoGAN for improved histopathology image classification. . Med. Image Anal. 67::101816
    [Crossref] [Google Scholar]
  131. Yang H, Chen L, Cheng Z, Yang M, Wang J, et al. 2021.. Deep learning–based six-type classifier for lung cancer and mimics from histopathological whole slide images: a retrospective study. . BMC Med. 19::80
    [Crossref] [Google Scholar]
  132. Yin P-N, KC K, Wei S, Yu Q, Li R, et al. 2020.. Histopathological distinction of non-invasive and invasive bladder cancers using machine learning approaches. . BMC Med. Inform. Decis. Making 20::162
    [Crossref] [Google Scholar]
  133. Zarella MD, Rivera Alvarez K. 2022.. High-throughput whole-slide scanning to enable large-scale data repository building. . J. Pathol. 257:(4):38390
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-062822-010523
Loading
/content/journals/10.1146/annurev-cancerbio-062822-010523
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error