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Intraoperative assessment of axillary sentinel lymph nodes by telepathology

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Abstract

Purpose

Although axillary dissection is no longer indicated for many breast cancer patients with 1–2 positive axillary sentinel lymph nodes (ASLN), intraoperative ASLN assessment is still performed in many institutions for patients undergoing mastectomy or neoadjuvant therapy. With recent advancements in digital pathology, pathologists increasingly evaluate ASLN via remote telepathology. We aimed to compare the performance characteristics of remote telepathology and conventional on-site intraoperative ASLN assessment.

Methods

Data from ASLN evaluation for breast cancer patients performed at two sites between April 2021 and October 2022 was collated. Remote telepathology consultation was conducted via the Aperio eSlideManager system.

Results

A total of 385 patients were identified during the study period (83 telepathology, 302 on-site evaluations). Although not statistically significant (P = 0.20), the overall discrepancy rate between intraoperative and final diagnoses was slightly higher at 9.6% (8/83) for telepathology compared with 5.3% (16/302) for on-site assessment. Further comparison of performance characteristics of ASLN assessment between telepathology and conventional on-site evaluation revealed no statistically significant differences between deferral rates, discrepancy rates, interpretive or sampling errors, major or minor disagreements, false negative or false positive results as well as clinical impact and turn-around time (P ≥ 0.12).

Conclusion

ASLN assessment via telepathology is not significantly different from conventional on-site evaluation, although it shows a slightly higher overall discrepancy rate between intraoperative and final diagnoses (9.6% vs. 5.3%). Further studies are warranted to ensure accuracy of ASLN assessment via telepathology.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Laws A, Kantor O, King TA (2023) Surgical management of the axilla for breast cancer. Hematol Oncol Clin North Am 37:51–77. https://doi.org/10.1016/j.hoc.2022.08.005

    Article  PubMed  Google Scholar 

  2. Black DM, Mittendorf EA (2013) Landmark trials affecting the surgical management of invasive breast cancer. Surg Clin North Am 93:501–518. https://doi.org/10.1016/j.suc.2012.12.007

    Article  PubMed  PubMed Central  Google Scholar 

  3. Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE, Cataliotti L, Westenberg AH, Klinkenbijl JH, Orzalesi L, Bouma WH, van der Mijle HC, Nieuwenhuijzen GA, Veltkamp SC, Slaets L, Duez NJ, de Graaf PW, van Dalen T, Marinelli A, Rijna H, Snoj M, Bundred NJ, Merkus JW, Belkacemi Y, Petignat P, Schinagl DA, Coens C, Messina CG, Bogaerts J, Rutgers EJ (2014) Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981–22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol 15:1303–1310. https://doi.org/10.1016/S1470-2045(14)70460-7

    Article  PubMed  PubMed Central  Google Scholar 

  4. Savolt A, Peley G, Polgar C, Udvarhelyi N, Rubovszky G, Kovacs E, Gyorffy B, Kasler M, Matrai Z (2017) Eight-year follow up result of the OTOASOR trial: the optimal treatment of the axilla - surgery or radiotherapy after positive sentinel lymph node biopsy in early-stage breast cancer: a randomized, single centre, phase III, non-inferiority trial. Eur J Surg Oncol 43:672–679. https://doi.org/10.1016/j.ejso.2016.12.011

    Article  CAS  PubMed  Google Scholar 

  5. Kantor O, Means J, Grossmith S, Dey T, Bellon JR, Mittendorf EA, King TA (2022) Optimizing axillary management in clinical T1-2N0 mastectomy patients with positive sentinel lymph nodes. Ann Surg Oncol 29:972–980. https://doi.org/10.1245/s10434-021-10726-3

    Article  PubMed  Google Scholar 

  6. Williams AD, Khan AJ, Sevilimedu V, Barrio AV, Morrow M, Mamtani A (2022) Omission of intraoperative frozen section may reduce axillary overtreatment among clinically node-negative patients having upfront mastectomy. Ann Surg Oncol 29:8037–8043. https://doi.org/10.1245/s10434-022-12238-0

    Article  PubMed  Google Scholar 

  7. Hanna MG, Reuter VE, Hameed MR, Tan LK, Chiang S, Sigel C, Hollmann T, Giri D, Samboy J, Moradel C, Rosado A, Otilano JR 3rd, England C, Corsale L, Stamelos E, Yagi Y, Schuffler PJ, Fuchs T, Klimstra DS, Sirintrapun SJ (2019) Whole slide imaging equivalency and efficiency study: experience at a large academic center. Mod Pathol 32:916–928. https://doi.org/10.1038/s41379-019-0205-0

    Article  PubMed  Google Scholar 

  8. Hanna MG, Reuter VE, Ardon O, Kim D, Sirintrapun SJ, Schuffler PJ, Busam KJ, Sauter JL, Brogi E, Tan LK, Xu B, Bale T, Agaram NP, Tang LH, Ellenson LH, Philip J, Corsale L, Stamelos E, Friedlander MA, Ntiamoah P, Labasin M, England C, Klimstra DS, Hameed M (2020) Validation of a digital pathology system including remote review during the COVID-19 pandemic. Mod Pathol 33:2115–2127. https://doi.org/10.1038/s41379-020-0601-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Pantanowitz L, Sinard JH, Henricks WH, Fatheree LA, Carter AB, Contis L, Beckwith BA, Evans AJ, Lal A, Parwani AV, College of American Pathologists P, Laboratory Quality C (2013) Validating whole slide imaging for diagnostic purposes in pathology: guideline from the College of American Pathologists Pathology and Laboratory Quality Center. Arch Pathol Lab Med 137:1710–1722. https://doi.org/10.5858/arpa.2013-0093-CP

    Article  PubMed  PubMed Central  Google Scholar 

  10. Abels E, Pantanowitz L (2017) Current state of the regulatory trajectory for whole slide imaging devices in the USA. J Pathol Inform 8:23. https://doi.org/10.4103/jpi.jpi_11_17

    Article  PubMed  PubMed Central  Google Scholar 

  11. Taylor CR (2014) Issues in using whole slide imaging for diagnostic pathology: routine stains, immunohistochemistry and predictive markers. Biotech Histochem 89:419–423. https://doi.org/10.3109/10520295.2013.861512

    Article  CAS  PubMed  Google Scholar 

  12. Griffin J, Treanor D (2017) Digital pathology in clinical use: where are we now and what is holding us back? Histopathology 70:134–145. https://doi.org/10.1111/his.12993

    Article  PubMed  Google Scholar 

  13. Evans AJ, Chetty R, Clarke BA, Croul S, Ghazarian DM, Kiehl TR, Perez Ordonez B, Ilaalagan S, Asa SL (2009) Primary frozen section diagnosis by robotic microscopy and virtual slide telepathology: the University Health Network experience. Hum Pathol 40:1070–1081. https://doi.org/10.1016/j.humpath.2009.04.012

    Article  PubMed  Google Scholar 

  14. Bauer TW, Slaw RJ (2014) Validating whole-slide imaging for consultation diagnoses in surgical pathology. Arch Pathol Lab Med 138:1459–1465. https://doi.org/10.5858/arpa.2013-0541-OA

    Article  PubMed  Google Scholar 

  15. Kaplan KJ, Burgess JR, Sandberg GD, Myers CP, Bigott TR, Greenspan RB (2002) Use of robotic telepathology for frozen-section diagnosis: a retrospective trial of a telepathology system for intraoperative consultation. Mod Pathol 15:1197–1204. https://doi.org/10.1097/01.MP.0000033928.11585.42

    Article  PubMed  Google Scholar 

  16. Mukhopadhyay S, Feldman MD, Abels E, Ashfaq R, Beltaifa S, Cacciabeve NG, Cathro HP, Cheng L, Cooper K, Dickey GE, Gill RM, Heaton RP Jr, Kerstens R, Lindberg GM, Malhotra RK, Mandell JW, Manlucu ED, Mills AM, Mills SE, Moskaluk CA, Nelis M, Patil DT, Przybycin CG, Reynolds JP, Rubin BP, Saboorian MH, Salicru M, Samols MA, Sturgis CD, Turner KO, Wick MR, Yoon JY, Zhao P, Taylor CR (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 42:39–52. https://doi.org/10.1097/PAS.0000000000000948

    Article  PubMed  Google Scholar 

  17. Vitkovski T, Bhuiya T, Esposito M (2015) Utility of telepathology as a consultation tool between an off-site surgical pathology suite and affiliated hospitals in the frozen section diagnosis of lung neoplasms. J Pathol Inform 6:55. https://doi.org/10.4103/2153-3539.168515

    Article  PubMed  PubMed Central  Google Scholar 

  18. Fallon MA, Wilbur DC, Prasad M (2010) Ovarian frozen section diagnosis: use of whole-slide imaging shows excellent correlation between virtual slide and original interpretations in a large series of cases. Arch Pathol Lab Med 134:1020–1023. https://doi.org/10.5858/2009-0320-OA.1

    Article  PubMed  Google Scholar 

  19. Frierson HF, Galgano MT (2007) Frozen-section diagnosis by wireless telepathology and ultra portable computer: use in pathology resident/faculty consultation. Hum Pathol 38:1330–1334. https://doi.org/10.1016/j.humpath.2007.02.006

    Article  PubMed  Google Scholar 

  20. Weinstein RS (1986) Prospects for telepathology. Hum Pathol 17:433–434. https://doi.org/10.1016/s0046-8177(86)80028-4

    Article  CAS  PubMed  Google Scholar 

  21. Weinstein RS, Graham AR, Richter LC, Barker GP, Krupinski EA, Lopez AM, Erps KA, Bhattacharyya AK, Yagi Y, Gilbertson JR (2009) Overview of telepathology, virtual microscopy, and whole slide imaging: prospects for the future. Hum Pathol 40:1057–1069. https://doi.org/10.1016/j.humpath.2009.04.006

    Article  PubMed  Google Scholar 

  22. Wellnitz U, Binder B, Fritz P, Friedel G, Schwarzmann P (2000) Reliability of telepathology for frozen section service. Anal Cell Pathol 21:213–222. https://doi.org/10.1155/2000/904578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dietz RL, Hartman DJ, Pantanowitz L (2020) Systematic review of the use of telepathology during intraoperative consultation. Am J Clin Pathol 153:198–209. https://doi.org/10.1093/ajcp/aqz155

    Article  PubMed  Google Scholar 

  24. Liu LC, Lang JE, Lu Y, Roe D, Hwang SE, Ewing CA, Esserman LJ, Morita E, Treseler P, Leong SP (2011) Intraoperative frozen section analysis of sentinel lymph nodes in breast cancer patients: a meta-analysis and single-institution experience. Cancer 117:250–258. https://doi.org/10.1002/cncr.25606

    Article  PubMed  Google Scholar 

  25. Holck S, Galatius H, Engel U, Wagner F, Hoffmann J (2004) False-negative frozen section of sentinel lymph node biopsy for breast cancer. Breast 13:42–48. https://doi.org/10.1016/S0960-9776(03)00124-3

    Article  CAS  PubMed  Google Scholar 

  26. Wang L, Leng B, Rampisela D (2021) Five-year review of intraoperative pathology consultation in a single institution. Proc (Bayl Univ Med Cent) 34:649–653. https://doi.org/10.1080/08998280.2021.1941700

    Article  PubMed  Google Scholar 

  27. Kantasiripitak C, Laohawetwanit T, Apornvirat S, Niemnapa K (2022) Validation of whole slide imaging for frozen section diagnosis of lymph node metastasis: a retrospective study from a tertiary care hospital in Thailand. Ann Diagn Pathol 60:151987. https://doi.org/10.1016/j.anndiagpath.2022.151987

    Article  PubMed  Google Scholar 

  28. Gifford AJ, Colebatch AJ, Litkouhi S, Hersch F, Warzecha W, Snook K, Sywak M, Gill AJ (2012) Remote frozen section examination of breast sentinel lymph nodes by telepathology. ANZ J Surg 82:803–808. https://doi.org/10.1111/j.1445-2197.2012.06191.x

    Article  PubMed  Google Scholar 

  29. Winokur TS, McClellan S, Siegal GP, Redden D, Gore P, Lazenby A, Reddy V, Listinsky CM, Conner DA, Goldman J, Grimes G, Vaughn G, McDonald JM (2000) A prospective trial of telepathology for intraoperative consultation (frozen sections). Hum Pathol 31:781–785. https://doi.org/10.1053/hupa.2000.8452

    Article  CAS  PubMed  Google Scholar 

  30. Demichelis F, Barbareschi M, Boi S, Clemente C, Dalla Palma P, Eccher C, Forti S (2001) Robotic telepathology for intraoperative remote diagnosis using a still-imaging-based system. Am J Clin Pathol 116:744–752. https://doi.org/10.1309/D71Y-7RLE-JGJP-A427

    Article  CAS  PubMed  Google Scholar 

  31. Baak JP, van Diest PJ, Meijer GA (2000) Experience with a dynamic inexpensive video-conferencing system for frozen section telepathology. Anal Cell Pathol 21:169–175. https://doi.org/10.1155/2000/908426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Hutarew G, Dandachi N, Strasser F, Prokop E, Dietze O (2003) Two-year evaluation of telepathology. J Telemed Telecare 9:194–199. https://doi.org/10.1258/135763303322225508

    Article  PubMed  Google Scholar 

  33. Hatami H, Mohsenifar Z, Alavi SN (2015) The diagnostic accuracy of frozen section compared to permanent section: a single center study in Iran. Iran J Pathol 10:295–299

    PubMed  PubMed Central  Google Scholar 

  34. Ferreiro JA, Myers JL, Bostwick DG (1995) Accuracy of frozen section diagnosis in surgical pathology: review of a 1-year experience with 24,880 cases at Mayo Clinic Rochester. Mayo Clin Proc 70:1137–1141. https://doi.org/10.4065/70.12.1137

    Article  CAS  PubMed  Google Scholar 

  35. Preeti A, Sameer G, Kulranjan S, Arun Abhinav S, Preeti R, Sunita Y, Madhu Mati G (2016) Intra-operative frozen sections: experience at a Tertiary Care Centre. Asian Pac J Cancer Prev 17:5057–5061. https://doi.org/10.22034/APJCP.2016.17.12.5057

    Article  PubMed  PubMed Central  Google Scholar 

  36. Hufnagl P, Bayer G, Oberbamscheidt P, Wehrstedt K, Guski H, Hauptmann S, Dietel M (2000) Comparison of different telepathology solutions for primary frozen section diagnostic. Anal Cell Pathol 21:161–167. https://doi.org/10.1155/2000/123057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Onguru O, Celasun B (2000) Intra-hospital use of a telepathology system. Pathol Oncol Res 6:197–201. https://doi.org/10.1007/BF03032373

    Article  CAS  PubMed  Google Scholar 

  38. Winokur TS, McClellan S, Siegal GP, Reddy V, Listinsky CM, Conner D, Goldman J, Grimes G, Vaughn G, McDonald JM (1998) An initial trial of a prototype telepathology system featuring static imaging with discrete control of the remote microscope. Am J Clin Pathol 110:43–49. https://doi.org/10.1093/ajcp/110.1.43

    Article  CAS  PubMed  Google Scholar 

  39. Hitchcock CL, Hitchcock LE (2005) Three years of experience with routine use of telepathology in assessment of excisional and aspirate biopsies of breast lesions. Croat Med J 46:449–457

    PubMed  Google Scholar 

  40. Tetu B, Perron E, Louahlia S, Pare G, Trudel MC, Meyer J (2014) The Eastern Quebec Telepathology Network: a three-year experience of clinical diagnostic services. Diagn Pathol 9(Suppl 1):S1. https://doi.org/10.1186/1746-1596-9-S1-S1

    Article  PubMed  PubMed Central  Google Scholar 

  41. Huang Y, Lei Y, Wang Q, Li D, Ma L, Guo L, Tang M, Liu G, Yan Q, Shen L, Tong G, Jing Z, Zhang Y, Deng Y (2018) Telepathology consultation for frozen section diagnosis in China. Diagn Pathol 13:29. https://doi.org/10.1186/s13000-018-0705-0

    Article  PubMed  PubMed Central  Google Scholar 

  42. Kaushal RK, Rajaganesan S, Rao V, Sali A, More B, Desai SB (2021) Validation of a portable whole-slide imaging system for frozen section diagnosis. J Pathol Inform 12:33. https://doi.org/10.4103/jpi.jpi_95_20

    Article  PubMed  PubMed Central  Google Scholar 

  43. French JMR, Betney DT, Abah U, Bhatt N, Internullo E, Casali G, Batchelor TJP, West DG (2019) Digital pathology is a practical alternative to on-site intraoperative frozen section diagnosis in thoracic surgery. Histopathology 74:902–907. https://doi.org/10.1111/his.13804

    Article  PubMed  Google Scholar 

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The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

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Authors and Affiliations

  1. Department of Pathology and Laboratory Medicine, Emory University Hospital, 1364 Clifton Road NE, Atlanta, GA, 30322, USA

    Gulisa Turashvili, Sandra Gjorgova Gjeorgjievski, Qun Wang, Abdulwahab Ewaz, Di Ai, Xiaoxian Li & Sunil S. Badve

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  1. Gulisa Turashvili
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  4. Abdulwahab Ewaz
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Contributions

B and T conceived of and designed the study. All authors participated in morphologic evaluation of surgical specimens. T drafted the article and performed statistical analyses. All authors reviewed, edited, and approved of the final article.

Corresponding author

Correspondence to Gulisa Turashvili.

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Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

Informed consent was not sought as this was a quality assurance activity for retrospectively identified cases in which axillary sentinel nodes were assessed as part of routine clinical care. Analysis of deidentified data was performed in accordance with the ethical standards set in the 1964 Declaration of Helsinki.

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Turashvili, G., Gjeorgjievski, S.G., Wang, Q. et al. Intraoperative assessment of axillary sentinel lymph nodes by telepathology. Breast Cancer Res Treat 202, 423–434 (2023). https://doi.org/10.1007/s10549-023-07101-z

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