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Introduction
In the Summer 2024 edition of ACP news Dr Bracey discussed “what makes an expert in Histopathology”. During my F1 placement in Pathology we discussed his and local colleagues preference for gaining expert second opinions digitally, given the potential advantages this method offers1. Given that Dr Bracey and his colleagues had recently started sending some external second opinions digitally we decided to audit the external expert opinions sent from the department of histopathology in Royal Cornwall Hospital and compare the conventional glass versus the newer digital method for turnaround times, acceptability to local and remote users as well as quality and complexity considerations.
Methods
The laboratory information system (Clinisys Winpath) was searched for cases sent away in a single calendar year (June 2023 – June 2024) and the departmental list of consultation experts. A spreadsheet was produced with columns corresponding to specimen number, tissue type, sample date, provisional report authorisation date, remote hospital destination, and final report date together with final diagnosis. A list of digitally referred cases were collated with the same column labels from Dr Bracey’s email records for the same dates.
The method used for sending glass slide second opinions was to write a letter to the remote expert, and include with this the provisional report, glass slides and a representative paraffin block in a parcel via a tracked recorded delivery. In contrast, for the digital referrals the relevant glass slides were scanned using a Grundium Ocus 40 or 3DHistech p250II whole slide image scanner, with creation of a web link, produced using the cloud-based Pathomation software (see figure 1). This web link could then be sent to the expert via secure nhs.net email with a provisional report and relevant clinical details. In some cases the digital slides were shown “live” to the remote expert via Microsoft Teams, enabling a two-way conversation and sharing of macroscopic and radiology images. Due to the relative infancy of the digital method, unless it was explicitly stated by the remote expert that we use their name, the remote digital opinion was treated as a form of education and guidance, and not formally documented in the final report, with the local pathologist retaining all responsibility for the final diagnosis.
Results
175 cases were identified during the study period. More than half (95) of these cases were excluded from the analysis due to being cases sent away for different reasons other than an expert opinion, for example SLA (service level agreement) for external reporting of medical liver and kidney biopsies, external registration of suspected trophoblastic and registration of straightforward malignant diagnoses for specialist regional surgical MDTs. After excluding these cases, 81 cases remained, 57 had been sent away as glass slides (plus or minus paraffin blocks) and 24 cases as digital slides.
| Subspeciality / tissue type | Cases (glass) | Cases (digital) | Locations (Glass) | Locations (Digital) |
| Soft tissue & osteoarticular | 19 | 4 | Plymouth, Bristol, London, Oxford | London, Sheffield, Bristol |
| Skin | 16 | 1 | London | Sheffield |
| Gynaecological | 7 | 3 | Birmingham, Exeter | Birmingham, Exeter |
| Gastrointestinal inc HPB | 5 | 7 | Southampton,London, Plymouth | Southampton, Bristol, Cheltenham |
| Head and neck | 4 | 7 | London, Sheffield | London, Sheffield |
| Lymphoreticular | 3 | 1 | London | Oxford |
| Endocrine | 3 | 1 | Portsmouth | North Tees |
| Average TAT days (range min to max) | 24 (5-71) | 3 (1-12) | Table 1: List of cases including tissue type, turnaround times and expert locations | |
Glass slide and digital referrals contained a similar mix of cases from multiple sub-specialities (see table 1 above) including some very unusual and difficult cases in both groups. Some examples of challenging diagnoses for glass second opinion included Castleman disease, angiosarcoma, benign colorectal vascular intrusion, and laryngeal carcinosarcoma. Challenging digital second opinions included salivary acinic cell carcinoma with high grade transformation, laryngeal chondrosarcoma, gastric pyloric gland adenoma, abdominal synovial sarcoma and atypical Spitz tumour. In addition many of the same experts were approached for both glass slide and digital expert opinions therefore the improved digital turnaround times cannot be attributed solely to the enthusiasm of carefully chosen experts. Despite the similarities in sub-speciality tissue types, case difficulty, locations and experts used, there was a dramatic difference in the time taken to receive a second opinion, with an average turnaround time for receipt of the second opinion being 24 days (ranging from 5 to 71 days) for glass, and 3 days (1 to 12 days) for digital. In fact, half (12 out of 24) digital cases received the second opinion less than 24 hours of being contacted. Dr Bracey’s colleagues are increasingly passionate about using digital pathology for external second opinions, and several of the remote experts have made it clear they also prefer this method, stating reasons like “avoiding desk clutter”, discussing the case in context with the local team while the “details are more fresh in our minds” , and “not having to wait for glass slides” to arrive. Another expert colleague said “when glass slides arrive for second opinions, I just cannot bring myself to open the damn boxes, arrange them on my desk in order, match the IHC, etc. There’s too much payload in the prep before seeing the case. With digital, the case can be opened with just a click of the link, there’s no desk clutter and hence there’s no brain clutter. It’s all so straightforward”.
| Advantages of Digital Second Opinion | Disadvantages c/w Glass Slide Method |
| -Rapid turnaround time critical particularly for malignant diagnoses. -Referrer and expert can view slides simultaneously in different locations allowing an interactive learning experience. -Additional experts can see the same slides at different locations allowing multiple expert consensus. -Physical slides do not leave the referrer’s department so there is no risk of loss or damage so no delay to local MDT review. -Remote mentoring to enable development of local expertise. -Remote expert can rapidly respond to communicate unavailability or unwillingness to give a digital opinion if necessary. | -Additional time investment for the referring pathologist. -May be less acceptable to some remote experts who do not know the referrer. -Referrer may be unfamiliar with digital pathology and may prefer a more “formally documented opinion” despite the increased delay. -Remote experts may be less familiar and not confident with digital slide technology. -Remote experts may not have a mechanism for recording and justifying the DCC time dedicated to digital opinions. -Additional costs of high quality equipment and digital slide storage. -Technical hurdles include ring-fenced NHS IT infrastructure and tendency of NHS to choose “on prem” solutions. Perception of lower security. -Current lack of a national NHS full interconnected digital pathology system. |
| Table 2: Perceived advantages and disadvantages of digital vs glass expert opinions | |
Discussion
This local pilot study has compared an informal method of digital slide sharing with conventional glass slide expert second opinion. Our results suggest it is acceptable to a group of referring local pathologists, and to selected experts in multiple NHS locations. Despite the relatively small sample size and short period of time studied, results of this pilot study suggest that the digital method saves valuable time for clinical teams to implement a management plan with an average 3 day turnaround time for digital opinions versus 24 days for the conventional postal method. With reduced administration staff in Histopathology departments there can be several days of delay booking out material from one department and booking in and labelling into another especially factoring in weekends delays. It is not uncommon for slides to take at least a week for a case to actually arrive on the desk of a pathologist, even at at a neighbouring NHS trust. If the case is complex and doesn’t contain necessary clinical and radiological detail many additional investigations can be needed and even national experts frequently have to show cases around other colleagues, sometimes involving packaging material up again to send off to another trust with necessary expertise and or access to specialised testing. Clinical teams managing malignant disease cannot feasibly delay treatment in many cases and it is the authors experience that management plans often proceed based on balance of probabilities when external second opinions are significantly delayed. In this small pilot study the turnaround times of remote expert opinions took an average of 3 days compared with the 24 day average of conventional glass slide referrals for a comparable range of tissue types and experts at similar geographical locations. These were actionable diagnoses but even when further testing is necessary for example predictive molecular testing, it is useful for expert guidance regarding which testing is likely to be most fruitful. Given the dramatically reduced turnaround times using this digital method, despite the disadvantages (see table 2) it seems unethical not to use digital pathology for future second opinions whenever possible.
Widespread implementation of digital pathology in the NHS is currently limited by multiple factors including financial constraints and organisational barriers. While there have been some notable digital pathology successes especially since the COVID19 pandemic 2-5, implementations are usually at single hospitals or single NHS trusts, and even when at multiple sites often do not allow viewing of digital slides by employees of different NHS organisations unless VPN access or honorary contracts are arranged. Microsoft Teams can be useful to project slides from digital slides or a microscope with an attached camera3, but this requires pathologists to find time to meet at a mutually agreeable time, and it is sometimes easier to find time in ones own schedule to look at digital (or glass) slides. Another disadvantage of informal second opinions especially for an expert working at another NHS trust is the difficulty registering the time taken in their job plans. When physical material arrives in a department there is always a record of the slides booked in, with letters and review report recorded on the expert’s hospital LIS which enables quantification of time spent reviewing and reporting the case. With digital opinions there is no such physical record, however it would be reasonable in such cases to book in a paper report from the external trust with a record of the number of digital slides reviewed and the review report. In this way a formal review report can be generated based on this, with the appropriate patient demographics and the expert has a local record of the work done. There are also private companies specialising in second opinion work which can digitise the slides and allocate the case to the most appropriate expert available nationally or internationally who then do the work in their spare time and are paid according to the perceived complexity of the case. Once the case is digitised on their system there are no longer organisational or geographical barriers to the case being shown around additional experts if required.
An increasing number of web based digital pathology systems are file format agnostic and allow sharing of anonymised slide links which can be viewed in any computer browser such as Pathomation, the system we used in this pilot study. Ideally however all NHS organisations should be linked by a single digital pathology system and single electronic patient record to benefit patients through real time collaboration between clinical staff at any hospital. While this may currently seem impossible with the dispersed geographical nature of the NHS and current levels of funding, there are already moves towards a single national digital pathology system in the North of England in the form of the National Pathology Imaging Cooperative (NPIC6). This collaborative venture aims to harness economies of scale to expand and protect our crucial histopathology specialist services as well as developing and implementing artificial intelligence algorithms with the ultimate aim of improving quality and patient safety in Histopathology reporting. Expert opinions are likely to continue being a vital part of diagnosis, particularly for rare diseases for decades to come. It seems obvious to the authors that the most efficient and shortest path towards the most appropriate expert pathologist for any given case should always be chosen when considering the patient waiting for their result and potential life saving treatment.
References
1. Bracey TS. Digital Pathology . Royal College of Surgeons Bulletin. 2017;99(3):93–6.
2. Bracey TS. The Nomadic Digital Pathologist. Validation of a simple, dual slide scanner with remote reporting for a regional upper gastrointestinal specialist multidisciplinary meeting. J Pathol Inform. 2023;14:100161.
3. Bracey, TS., Arif, S., Ralte, A. M., Shaaban, A. M., & Ganesan, R. (2021). Histopathology during the COVID-19 pandemic: resilience through adaptation and innovation. Diagnostic Histopathology (Oxford, England), 27(3), 108–115.
4. Browning L, Fryer E, Roskell D, White K, Colling R, Rittscher J, et al. 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 Feb;74(2):129–32.
5. Williams BJ, Fraggetta F, Hanna MG, Huang R, Lennerz J, Salgado R, et al. The Future of Pathology: What can we Learn from the COVID-19 Pandemic? J Pathol Inform. 2020;11:15.
6. Humphries, M. P., Kaye, D., Stankeviciute, G., Halliwell, J., Wright, A. I., Bansal, D., Brettle, D., & Treanor, D. (2024). Development of a multi-scanner facility for data acquisition for digital pathology artificial intelligence. The Journal of Pathology, 264(1), 80–89.
Acknowledgments
Dr Bracey would like to thank his local colleagues for their support and enthusiasm, and remote experts for their frequent interactions, guidance and help, in particular Professors and Drs Adrian Bateman, Ali Khurram, Eddy Odell, Gillian Hall, Khin Thway, Cyril Fisher, Shonali Natu, and Raji Ganesan.