The Use of Digital Pathology and Artificial Intelligence in Histopathological Diagnostic Assessment of Prostate Cancer: A Survey of Prostate Cancer UK Supporters
Abstract
:1. Introduction
2. Materials and Methods
2.1. Survey Design
2.2. Survey Composition
2.3. Statistical Analysis
3. Results
3.1. Response
3.2. Understanding of the Role of Histopathology
3.3. Views on Digitisation of Pathology
3.3.1. Increased Efficiency and Technical Aspects
3.3.2. Formation of a Permanent Record
3.3.3. Sharing of Digital Images
3.3.4. Deployment of AI Techniques
3.3.5. Reservations towards DP
3.4. On the Introduction of AI in the Reporting of Histopathology
3.4.1. Technical Performance
3.4.2. Preference for Human Review
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Fischer, G.; Anderson, L.; Ranson, M.; Sellen, D.; McArthur, E. Public perceptions on pathology: A fundamental change is required. J. Clin. Pathol. 2021, 74, 812–815. [Google Scholar] [CrossRef] [PubMed]
- Titford, M. A short history of histopathology technique. J. Histotechnol. 2006, 29, 99–110. [Google Scholar] [CrossRef]
- Browning, L.; Fryer, E.; Roskell, D.; White, K.; Colling, R.; Rittscher, J.; Verrill, C. Role of digital pathology in diagnostic histopathology in the response to COVID-19: Results from a survey of experience in a UK tertiary referral hospital. J. Clin. Pathol. 2021, 74, 129–132. [Google Scholar] [CrossRef] [PubMed]
- Salto-Tellez, M.; Maxwell, P.; Hamilton, P. Artificial intelligence-the third revolution in pathology. Histopathology 2019, 74, 372–376. [Google Scholar] [CrossRef] [Green Version]
- Williams, B.J.; Lee, J.; Oien, K.A.; Treanor, D. Digital pathology access and usage in the UK: Results from a national survey on behalf of the National Cancer Research Institute’s CM-Path initiative. J. Clin. Pathol. 2018, 71, 463–466. [Google Scholar] [CrossRef]
- Williams, B.J.; Bottoms, D.; Treanor, D. Future-proofing pathology: The case for clinical adoption of digital pathology. J. Clin. Pathol. 2017, 70, 1010–1018. [Google Scholar] [CrossRef] [Green Version]
- Pell, R.; Oien, K.; Robinson, M.; Pitman, H.; Rajpoot, N.; Rittscher, J.; Snead, D.; Verrill, C.; Driskell, O.J.; Hall, A.; et al. The use of digital pathology and image analysis in clinical trials. J. Pathol. Clin. Res. 2019, 5, 81–90. [Google Scholar] [CrossRef] [Green Version]
- Hamilton, P.W.; Wang, Y.; McCullough, S.J. Virtual microscopy and digital pathology in training and education. APMIS 2012, 120, 305–315. [Google Scholar] [CrossRef]
- Browning, L.; Colling, R.; Rittscher, J.; Winter, L.; McEntyre, N.; Verrill, C. Implementation of digital pathology into diagnostic practice: Perceptions and opinions of histopathology trainees and implications for training. J. Clin. Pathol. 2020, 73, 223–227. [Google Scholar] [CrossRef]
- Colling, R.; Protheroe, A.; Sullivan, M.; Macpherson, R.; Tuthill, M.; Redgwell, J.; Traill, Z.; Molyneux, A.; Johnson, E.; Abdullah, N.; et al. Digital Pathology Transformation in a Supraregional Germ Cell Tumour Network. Diagnostics 2021, 11, 2191. [Google Scholar] [CrossRef]
- Bankhead, P.; Fernández, J.A.; McArt, D.G.; Boyle, D.P.; Li, G.; Loughrey, M.B.; Irwin, G.W.; Harkin, D.P.; James, J.A.; McQuaid, S.; et al. Integrated tumor identification and automated scoring minimizes pathologist involvement and provides new insights to key biomarkers in breast cancer. Lab. Investig. 2018, 98, 15–26. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saha, M.; Chakraborty, C.; Arun, I.; Ahmed, R.; Chatterjee, S. An Advanced Deep Learning Approach for Ki-67 Stained Hotspot Detection and Proliferation Rate Scoring for Prognostic Evaluation of Breast Cancer. Sci. Rep. 2017, 7, 3213. [Google Scholar] [CrossRef] [PubMed]
- Coudray, N.; Ocampo, P.S.; Sakellaropoulos, T.; Narula, N.; Snuderl, M.; Fenyö, D.; Moreira, A.L.; Razavian, N.; Tsirigos, A. Classification and mutation prediction from non-small cell lung cancer histopathology images using deep learning. Nat. Med. 2018, 24, 1559–1567. [Google Scholar] [CrossRef] [PubMed]
- Kather, J.N.; Pearson, A.T.; Halama, N.; Jäger, D.; Krause, J.; Loosen, S.H.; Marx, A.; Boor, P.; Tacke, F.; Neumann, U.P.; et al. Deep learning can predict microsatellite instability directly from histology in gastrointestinal cancer. Nat. Med. 2019, 25, 1054–1056. [Google Scholar] [CrossRef]
- Raciti, P.; Sue, J.; Ceballos, R.; Godrich, R.; Kunz, J.D.; Kapur, S.; Reuter, V.; Grady, L.; Kanan, C.; Klimstra, D.S.; et al. Novel artificial intelligence system increases the detection of prostate cancer in whole slide images of core needle biopsies. Mod. Pathol. 2020, 33, 2058–2066. [Google Scholar] [CrossRef]
- Chatrian, A.; Colling, R.T.; Browning, L.; Alham, N.K.; Sirinukunwattana, K.; Malacrino, S.; Haghighat, M.; Aberdeen, A.; Monks, A.; Moxley-Wyles, B.; et al. Artificial intelligence for advance requesting of immunohistochemistry in diagnostically uncertain prostate biopsies. Mod. Pathol. 2021, 34, 1780–1794. [Google Scholar] [CrossRef]
- Food and Drug Administration. FDA Authorizes Software That Can Help Identify Prostate Cancer. Available online: https://www.fda.gov/news-events/press-announcements/fda-authorizes-software-can-help-identify-prostate-cancer (accessed on 25 April 2022).
- National Prostate Cancer Audit. Annual Report 2021. Available online: https://www.npca.org.uk/content/uploads/2022/01/NPCA-Annual-Report-2021_Final_13.01.22-1.pdf (accessed on 14 November 2021).
- Betsi Cadwaladr University Health Board. ‘We Are Pioneers’ Says Betsi Consultant Using Artificial Intelligence to Improve Prostate Cancer Diagnosis. Available online: https://bcuhb.nhs.wales/news/health-board-news/we-are-pioneers-says-betsi-consultant-using-artificial-intelligence-to-improve-prostate-cancer-diagnosis (accessed on 15 December 2021).
- Neudert, L.M.; Knuutila, A.; Howard, P. Global Attitudes Towards AI, Machine Learning and Automated Decision Making—Implications for Involving Artificial Intelligence in Public Service and Good Governance. Available online: https://oxcaigg.oii.ox.ac.uk/publications/global-attitudes-towards-ai-machine-learning-automated-decision-making-2/ (accessed on 14 November 2021).
- Gao, S.; He, L.; Chen, Y.; Li, D.; Lai, K. Public Perception of Artificial Intelligence in Medical Care: Content Analysis of Social Media. J. Med. Internet Res. 2020, 22, e16649. [Google Scholar] [CrossRef]
- de Vries, C.F.; Morrissey, B.E.; Duggan, D.; Staff, R.T.; Lip, G. Screening participants’ attitudes to the introduction of artificial intelligence in breast screening. J. Med. Screen. 2021, 28, 221–222. [Google Scholar] [CrossRef]
- Royal College of Pathologists. Meeting Pathology Demand: Histopathology Workplace Census (2017/18). Available online: https://www.rcpath.org/uploads/assets/952a934d-2ec3-48c9-a8e6e00fcdca700f/Meeting-Pathology-Demand-Histopathology-Workforce-Census-2018.pdf (accessed on 15 December 2021).
- Nickel, B.; Moynihan, R.; Barratt, A.; Brito, J.P.; McCaffery, K. Renaming low risk conditions labelled as cancer. BMJ 2018, 362, k3322. [Google Scholar] [CrossRef] [Green Version]
- Badani, K.K.; Kaul, S.; Menon, M. Evolution of robotic radical prostatectomy: Assessment after 2766 procedures. Cancer 2007, 110, 1951–1958. [Google Scholar] [CrossRef]
- Berryhill, R., Jr.; Jhaveri, J.; Yadav, R.; Leung, R.; Rao, S.; El-Hakim, A.; Tewari, A. Robotic prostatectomy: A review of outcomes compared with laparoscopic and open approaches. Urology 2008, 72, 15–23. [Google Scholar] [CrossRef] [PubMed]
- Reynolds, B.R.; Bulsara, C.; Zeps, N.; Codde, J.; Lawrentschuk, N.; Bolton, D.; Vivian, J. Exploring pathways towards improving patient experience of robot-assisted radical prostatectomy (RARP): Assessing patient satisfaction and attitudes. BJU Int. 2018, 121 (Suppl. S3), 33–39. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McDermott, H.; Choudhury, N.; Lewin-Runacres, M.; Aemn, I.; Moss, E. Gender differences in understanding and acceptance of robot-assisted surgery. J. Robot. Surg. 2020, 14, 227–232. [Google Scholar] [CrossRef] [Green Version]
- Ongena, Y.P.; Haan, M.; Yakar, D.; Kwee, T.C. Patients’ views on the implementation of artificial intelligence in radiology: Development and validation of a standardized questionnaire. Eur. Radiol. 2020, 30, 1033–1040. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Coulter, C.; McKay, F.; Hallowell, N.; Browning, L.; Colling, R.; Macklin, P.; Sorell, T.; Aslam, M.; Bryson, G.; Treanor, D.; et al. Understanding the ethical and legal considerations of Digital Pathology. J. Pathol. Clin. Res. 2022, 8, 101–115. [Google Scholar] [CrossRef] [PubMed]
- Sorell, T.; Rajpoot, N.; Verrill, C. Ethical issues in computational pathology. J. Med. Ethics 2022, 48, 278–284. [Google Scholar] [CrossRef]
- Canadian Association of Pathologists. Code of Ethics for Storage and Transmission of Electronic Laboratory Data. Available online: https://cap-acp.org/code_ethics_storage_electronic_lab_data.php (accessed on 22 October 2021).
- Organisation for Economic Cooperation and Development (OECD). Guidelines Governing the Protection of Privacy and Transborder Flows of Personal Data. Available online: https://www.oecd.org/sti/ieconomy/oecd_privacy_framework.pdf (accessed on 22 October 2021).
- Colling, R.; Pitman, H.; Oien, K.; Rajpoot, N.; Macklin, P.; CM-Path AI in Histopathology Working Group; Snead, D.; Sackville, T.; Verrill, C. Artificial intelligence in digital pathology: A roadmap to routine use in clinical practice. J. Pathol. 2019, 249, 143–150. [Google Scholar] [CrossRef]
Theme | Example Quotations |
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(a) Efficiency and technical aspects | Having had prostate cancer anything that speeds up and increases the accuracy of diagnosis has to be good. I am no expert but anything that makes viewing samples easier should make the doctors work easier and perhaps more accurate. I have done microscope work before, and it can be tiring and challenging especially if you are trying to count occurrences over an area. Digital leaves less room for human error. It sounds positive but without lots more information I could not say very positive, how secure will this data be, how reliable is the digital screening, is it at least as reliable… as a human? |
(b) Record permanence | As a digital record, it can be transferred between departments enabling specialists to discuss it. More importantly, it can’t be lost easily. A permanent record would provide a baseline assessment in case of need for further biopsies. A digital record could be kept for MDT meetings. I approve of the positive digital record, but the sample(s) should not be discarded before a conclusive diagnosis (higher magnification may be needed than the digital images). Any use of more modern technology cannot be a negative as long as the control over data is maintained properly/adequately. I suppose I wouldn’t like my digital records getting into the wrong hands!! |
(c) Sharing of images | A digital record is easily stored and can be easily shared with appropriate people. If requested, it could be shared with the patient to aid understanding of the result. Ability to share between experts, and ability to share/show the patient. There is a digital record of the sample(s) which can easily be recalled as a basis for comparison if there is/are ever repeat tests. Also, the record will be an element in a database of all biopsies which might be valuable for statistical or other test purposes. Having an electronic library enables medical staff and researchers to have better access. I had three biopsies in all… I trusted the histopathologists to produce the necessary reports, which were then used to decide the way ahead. The first biopsy was abroad, and I actually brought the original slides back to UK with the report; that would, of course, have been easier had they been digital. As a patient I have no particular view on digital vs. analogue slides, except that digital probably eases record-keeping and referral. I would have been very interested to have seen the samples and had their significance explained to me. Makes the data/information available for study/research/analysis to many more specialists instantly. My consultant explained in detail what the outcome was from the histology, but I did not see a digital scan of the biopsies. I think that would be helpful. Opportunity for referring back to the images. Allows teams to see the images and comment. Other centres able to easily review the histopathology ensuring uniformity in research, etc. This should enable retrospective scanning back over images if something useful is discovered in the future, where historic biopsy data, perhaps combined with progression/survival data, would be useful. However, it’s important the biological samples are retained too, so they can be used for things like genomic sequencing. |
(d) AI | AI is infallible if programmed correctly As long as a person who checks the results is experienced in reading them and the digital image is not a just compared to a digital library. Digital images can be stored to compare at a later date, it should be a positive move. Assuming the quality of image is as good, and the data is properly managed, the added availability should help diagnosis. It may also assist machine learning for analysis and more accurate diagnosis. It seems to make sense to digitize records. It should speed their transfer from one party to another and will make it easier for more than one professional to examine them. It might also facilitate the use of ai to review them. Provided the “library” of samples was large quantities and good enough quality, using automated digital imaging can cover more areas of the “slide” and present the targeted cells for review by qualified human to maximise efficiency and throughput. AI technology can help and be taught to find needles in haystacks… Can machines interpret as well as humans in this situation, I don’t know the answer to this question? |
(e) Reservations towards DP | The important factor for me as a potential cancer sufferer was to know that every process was being done to the best level possible. I did not want or need to know the details of the process itself but trusted that I was getting the best. As techniques advance, I think I would have the same attitude. Trust that the people know what they are doing and using the best technology. Either cancer is present or its not, how you record it is immaterial. I am only interested in the results. As a patient I am just interested in the results regardless of how they have been arrived at. I would think that an expert examining the sample would always be more reliable than a computer, but maybe there is a role for both approaches if there is time and money available Is it necessary to keep digital records? Once you know the result, a record is kept. So what? How is this going to help me? |
Theme | Example Quotations |
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(a) Support for AI | AI might pick up things a tired histopathologist missed, so having them confirm each other’s work would be good. I think evidence shows that the same histopathologist analysing the same slide sometime later does sometimes give a different grade. Getting the grading right is important for picking the right treatment. As long as AI does not become the primary decision maker but takes the strain on some of the more mundane elements of the process, I wouldn’t have a problem. Assuming that AI can meet (maybe exceed) the levels of accuracy of a human this could free up the experts’ time for other uses. Clearly research should be carried out to see whether AI could help. But it should only be pursued if rigorous checking indicates there are benefits over and above what a pathologist can do. I think AI makes sense as long as its role is to assist and not to take over from a trained pathologist. I wouldn’t be comfortable with the latter at this stage, but I see value in perhaps helping to increase the speed of diagnoses, add a degree of consistency in diagnoses which can sometimes be difficult for a pathologist to achieve all the time, and possibly to help detect patterns across a number of patients leading to potential future research and treatment areas. I think it is a good idea; however, a senior pathologist needs to verify the results. Possibly the most important element to modern AI/pattern recognition methodologies is a good reliable data set and to not over train the network. It is essential, therefore, to ensure the quality of the ‘AI’ and also to ensure that if samples are not confirmed by human examination, then the system produces zero false negatives. Also, it is essential to be very cautious of using some ‘AI’ companies as partners as they are nothing short of charlatans. AI has a great potential to speed up diagnosis, a benefit to patients. Quality control would be essential, checking that known true positives are picked up, and regular sampling so a histopathologist can check for false positives and false negatives. My only concern is that it may eventually lead to fewer pathologists being employed and by them becoming “de-skilled”. |
(b) Concerns regarding technical performance | I understand that AI is cost effective and probably can get through a greater workload quicker. My concern, again, is that will something be missed if the programming or the technical quality of the ai is compromised. Good idea but the usual checks and balances need to be good and regularly tested—see post office debacle re their post masters and mistresses. |
(c) Preference for human review | I’m all for the advancement of technology, but for the use of diagnostic purpose I would prefer the opinion of a doctor. You can’t program experience and a “hunch”. As long as AI is used alongside pathologist looking at the data, all will be good but should not replace a pathologist. AI may be something that a younger generation accept without question but for an old dinosaur like me AI Is far from second nature. This does not mean that it couldn’t be useful, it just means that I need convincing. As a lay person, I would have thought it would assist professionals, but I would not want it to be totally replacing an expert. |
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Rakovic, K.; Colling, R.; Browning, L.; Dolton, M.; Horton, M.R.; Protheroe, A.; Lamb, A.D.; Bryant, R.J.; Scheffer, R.; Crofts, J.; et al. The Use of Digital Pathology and Artificial Intelligence in Histopathological Diagnostic Assessment of Prostate Cancer: A Survey of Prostate Cancer UK Supporters. Diagnostics 2022, 12, 1225. https://doi.org/10.3390/diagnostics12051225
Rakovic K, Colling R, Browning L, Dolton M, Horton MR, Protheroe A, Lamb AD, Bryant RJ, Scheffer R, Crofts J, et al. The Use of Digital Pathology and Artificial Intelligence in Histopathological Diagnostic Assessment of Prostate Cancer: A Survey of Prostate Cancer UK Supporters. Diagnostics. 2022; 12(5):1225. https://doi.org/10.3390/diagnostics12051225
Chicago/Turabian StyleRakovic, Kai, Richard Colling, Lisa Browning, Monica Dolton, Margaret R. Horton, Andrew Protheroe, Alastair D. Lamb, Richard J. Bryant, Richard Scheffer, James Crofts, and et al. 2022. "The Use of Digital Pathology and Artificial Intelligence in Histopathological Diagnostic Assessment of Prostate Cancer: A Survey of Prostate Cancer UK Supporters" Diagnostics 12, no. 5: 1225. https://doi.org/10.3390/diagnostics12051225
APA StyleRakovic, K., Colling, R., Browning, L., Dolton, M., Horton, M. R., Protheroe, A., Lamb, A. D., Bryant, R. J., Scheffer, R., Crofts, J., Stanislaus, E., & Verrill, C. (2022). The Use of Digital Pathology and Artificial Intelligence in Histopathological Diagnostic Assessment of Prostate Cancer: A Survey of Prostate Cancer UK Supporters. Diagnostics, 12(5), 1225. https://doi.org/10.3390/diagnostics12051225