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The performance of digital microscopy for primary diagnosis in human pathology: a systematic review

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Abstract

Validation studies of whole slide imaging (WSI) systems produce evidence regarding digital microscopy (DM). This systematic review aimed to provide information about the performance of WSI devices by evaluating intraobserver agreement reported in previously published studies as the best evidence to elucidate whether DM is reliable for primary diagnostic purposes. In addition, this review delineates the reasons for the occurrence of discordant diagnoses. Scopus, MEDLINE/PubMed, and Embase were searched electronically. A total of 13 articles were included. The total sample of 2145 had a majority of 695 (32.4%) cases from dermatopathology, followed by 200 (9.3%) cases from gastrointestinal pathology. Intraobserver agreements showed an excellent concordance, with values ranging from 87% to 98.3% (κ coefficient range 0.8–0.98). Ten studies (77%) reported a total of 128 disagreements. The remaining three studies (23%) did not report the exact number and nature of disagreements. Borderline/challenging cases were the most frequently reported reason for disagreements (53.8%). Six authors reported limitations of the equipment and/or limited image resolution as reasons for the discordant diagnoses. Within these articles, the reported pitfalls were as follows: difficulties in the identification of eosinophilic granular bodies in brain biopsies; eosinophils and nucleated red blood cells; and mitotic figures, nuclear details, and chromatin patterns in neuropathology specimens. The lack of image clarity was reported to be associated with difficulties in the identification of microorganisms (e.g., Candida albicans, Helicobacter pylori, and Giardia lamblia). However, authors stated that the intraobserver variances do not derive from technical limitations of WSI. A lack of clinical information was reported by four authors as a source for disagreements. Two studies (15.4%) reported poor quality of the biopsies, specifically small size of the biopsy material or inadequate routine laboratory processes as reasons for disagreements. One author (7.7%) indicated the lack of immunohistochemistry and special stains as a source for discordance. Furthermore, nine studies (69.2%) did not consider the performance of the digital method—limitations of the equipment, insufficient magnification/limited image resolution—as reasons for disagreements. To summarize the pitfalls of digital pathology practice and better address the root cause of the diagnostic discordance, we suggest a Categorization for Digital Pathology Discrepancies to be used in further validations studies. Among 99 discordances, only 37 (37.3%) had preferred diagnosis rendered by means of WSI. The risk of bias and applicability concerns were judged with the QUADAS-2. Two studies (15.4%) presented an unclear risk of bias in the sample selection domain and 2 (15.4%) presented a high risk of bias in the index test domain. Regarding applicability, all studies included were classified as a low concern in all domains. The included studies were optimally designed to validate WSI for general clinical use, providing evidence with confidence. In general, this systematic review showed a high concordance between diagnoses achieved by using WSI and conventional light microscope (CLM), summarizes difficulties related to specific findings of certain areas of pathology—including dermatopathology, pediatric pathology, neuropathology, and gastrointestinal pathology—and demonstrated that WSI can be used to render primary diagnoses in several subspecialties of human pathology.

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References

  1. Pantanowitz L, Sinard JH, Henricks WH, Fatheree LA, Carter AB, Contis L, Beckwith BA, Evans AJ, Lal A, Parwani AV, College of American Pathologists Pathology and Laboratory Quality Center (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  Google Scholar 

  2. Pantanowitz L, Evans A, Pfeifer J, Collins LC, Valenstein PN, Kaplan KJ, Wilbur DC, Colgan TJ (2011) Review of the current state of whole slide imaging in pathology. J Pathol Inform 2:36. https://doi.org/10.4103/2153-3539.83746

    Article  PubMed  PubMed Central  Google Scholar 

  3. Koch LH, Lampros JN, Delong LK, Chen SC, Woosley JT, Hood AF (2009) Randomized comparison of virtual microscopy and traditional glass microscopy in diagnostic accuracy among dermatology and pathology residents. Hum Pathol 40:662–667. https://doi.org/10.1016/j.humpath.2008.10.009

    Article  PubMed  Google Scholar 

  4. Whiting P, Harbord R, Kleijnen J (2005) No role for quality scores in systematic reviews of diagnostic accuracy studies. BMC Med Res Methodol 5:19. https://doi.org/10.1186/1471-2288-5-19

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cornish TC, Swapp RE, Kaplan KJ (2012) Whole-slide imaging: routine pathologic diagnosis. Adv Anat Pathol 19:152–159. https://doi.org/10.1097/PAP.0b013e318253459e

    Article  PubMed  Google Scholar 

  6. Food and Drug Administration (2017) FDA allows marketing of first whole slide imaging system for digital pathology. https://www.fda.gov/newsevents/newsroom/pressannouncements/ucm552742.htm. Accessed 16 Mar 2017

  7. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097. https://doi.org/10.1371/journal.pmed.1000097

    Article  PubMed  PubMed Central  Google Scholar 

  8. Williams BJ, Hanby A, Millican-Slater R, Nijhawan A, Verghese E, Treanor D (2018) Digital pathology for the primary diagnosis of breast histopathological specimens: an innovative validation and concordance study on digital pathology validation and training. Histopathology 72:662–671. https://doi.org/10.1111/his.13403

    Article  PubMed  Google Scholar 

  9. Goacher E, Randell R, Williams B, Treanor D (2017) The diagnostic concordance of whole slide imaging and light microscopy: a systematic review. Arch Pathol Lab Med 141:151–161. https://doi.org/10.5858/arpa.2016-0025-RA

    Article  PubMed  Google Scholar 

  10. Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A (2016) Rayyan—a web and mobile app for systematic reviews. Syst Rev 5:210. https://doi.org/10.1186/s13643-016-0384-4

    Article  PubMed  PubMed Central  Google Scholar 

  11. Cochrane Effective Practice and Organisation of Care (EPOC) (2017). EPOC Resources for review authors. https://epoc.cochrane.org/resources/epoc-resources-review-authors

  12. Nielsen PS, Lindebjerg J, Rasmussen J, Starklint H, Waldstrøm M, Nielsen B (2010) Virtual microscopy: an evaluation of its validity and diagnostic performance in routine histologic diagnosis of skin tumors. Hum Pathol 41:1770–1776. https://doi.org/10.1016/j.humpath.2010.05.015

    Article  PubMed  Google Scholar 

  13. Al-Janabi S, Huisman A, Vink A et al (2012) Whole slide images for primary diagnostics in dermatopathology: a feasibility study. J Clin Pathol 65:152–158. https://doi.org/10.1136/jclinpath-2011-200277

    Article  PubMed  Google Scholar 

  14. Al-Janabi S, Huisman A, Vink A et al (2012) Whole slide images for primary diagnostics of gastrointestinal tract pathology: a feasibility study. Hum Pathol 43:702–707. https://doi.org/10.1016/j.humpath.2011.06.017

    Article  PubMed  Google Scholar 

  15. Al-Janabi S, Huisman A, Willems SM, Van Diest PJ (2012) Digital slide images for primary diagnostics in breast pathology: a feasibility study. Hum Pathol 43:2318–2325. https://doi.org/10.1016/j.humpath.2012.03.027

    Article  PubMed  CAS  Google Scholar 

  16. Al-Janabi S, Huisman A, Nikkels PGJ et al (2013) Whole slide images for primary diagnostics of paediatric pathology specimens: a feasibility study. J Clin Pathol 66:218–223. https://doi.org/10.1136/jclinpath-2012-201104

    Article  PubMed  Google Scholar 

  17. Al-Janabi S, Huisman A, Jonges GN et al (2014) Whole slide images for primary diagnostics of urinary system pathology: a feasibility study. J Ren Inj Prev 3:91–96. https://doi.org/10.12861/jrip.2014.26

    Article  PubMed  Google Scholar 

  18. Arnold MA, Chenever E, Baker PB, Boué DR, Fung B, Hammond S, Hendrickson BW, Kahwash SB, Pierson CR, Prasad V, Nicol KK, Barr T (2015) The College of American Pathologists Guidelines for whole slide imaging validation are feasible for pediatric pathology: a pediatric pathology practice experience. Pediatr Dev Pathol 18:109–116. https://doi.org/10.2350/14-07-1523-OA.1

    Article  PubMed  Google Scholar 

  19. Kent MN, Olsen TG, Feeser TA, Tesno KC, Moad JC, Conroy MP, Kendrick MJ, Stephenson SR, Murchland MR, Khan AU, Peacock EA, Brumfiel A, Bottomley MA (2017) Diagnostic accuracy of virtual pathology vs traditional microscopy in a large dermatopathology study. JAMA Dermatol 153:1285–1291. https://doi.org/10.1001/jamadermatol.2017.3284

    Article  PubMed  PubMed Central  Google Scholar 

  20. Loughrey MB, Kelly PJ, Houghton OP, Coleman HG, Houghton JP, Carson A, Salto-Tellez M, Hamilton PW (2015) Digital slide viewing for primary reporting in gastrointestinal pathology: a validation study. Virchows Arch 467:137–144. https://doi.org/10.1007/s00428-015-1780-1

    Article  PubMed  Google Scholar 

  21. Pekmezci M, Uysal SP, Orhan Y et al (2016) Pitfalls in the use of whole slide imaging for the diagnosis of central nervous system tumors: a pilot study in surgical neuropathology. J Pathol Inform 7:25. https://doi.org/10.4103/2153-3539.181769

    Article  PubMed  PubMed Central  Google Scholar 

  22. Saco A, Diaz A, Hernandez M, Martinez D, Montironi C, Castillo P, Rakislova N, del Pino M, Martinez A, Ordi J (2017) Validation of whole-slide imaging in the primary diagnosis of liver biopsies in a university hospital. Dig Liver Dis 49:1240–1246. https://doi.org/10.1016/j.dld.2017.07.002

    Article  PubMed  Google Scholar 

  23. Tabata K, Mori I, Sasaki T, Itoh T, Shiraishi T, Yoshimi N, Maeda I, Harada O, Taniyama K, Taniyama D, Watanabe M, Mikami Y, Sato S, Kashima Y, Fujimura S, Fukuoka J (2017) Whole-slide imaging at primary pathological diagnosis: validation of whole-slide imaging-based primary pathological diagnosis at twelve Japanese academic institutes. Pathol Int 67:547–554. https://doi.org/10.1111/pin.12590

    Article  PubMed  Google Scholar 

  24. Thrall MJ, Wimmer JL, Schwartz MR (2015) Validation of multiple whole slide imaging scanners based on the guideline from the College of American Pathologists pathology and laboratory quality center. Arch Pathol Lab Med 139:656–664. https://doi.org/10.5858/arpa.2014-0073-OA

    Article  PubMed  CAS  Google Scholar 

  25. Camparo P, Ramirez A, Claude V et al (2009) Whole slide imaging in daily routine examination in a pathologic department: Experience of a military hospital network in Paris. Rev Fr Lab 38:49–55 RFL-01-2008-38-408-1773-035x-101019-200812623

    Google Scholar 

  26. Wang M, Liu S, Xie C et al (2015) Making primary diagnosis on liver allograft biopsies with whole slide images - a validation study. Am J Clin Pathol 144:A168. https://doi.org/10.1093/ajcp/144.suppl2.168

    Article  Google Scholar 

  27. Gage JC, Joste N, Ronnett BM, Stoler M, Hunt WC, Schiffman M, Wheeler CM (2013) A comparison of cervical histopathology variability using whole slide digitized images versus glass slides: experience with a statewide registry. Hum Pathol 44:2542–2548. https://doi.org/10.1016/j.humpath.2013.06.015

    Article  PubMed  Google Scholar 

  28. Zeitouni J, Jorda M, Reyes C, Nadji M (2012) Validation of whole slide imaging for the first line diagnosis of prostate biopsies. Lab Invest 92:519A–520A. https://doi.org/10.1038/labinvest.2012.24

  29. Gerhard R, Honorio A, Gentili A et al (2014) Primary histopathological diagnosis using whole slide imaging (WSI): a validation study. Lab Invest 94:399A. https://doi.org/10.1038/labinvest.2014.28

  30. Goodman S, Kandil D, Khan (2014) A Diagnosis of breast needle core biopsies using whole slide imaging. Lab Invest 94:399A. https://doi.org/10.1038/labinvest.2014.28

  31. Parimi V, Borys A, Zhou Y et al (2016) Validation of whole frozen section slide image diagnosis in surgical pathology. Lab Invest 96:399A–400A. https://doi.org/10.1038/labinvest.2016.15

  32. Bradshaw S, Driman D, Dupre M et al (2013) Inter- and intra-observer agreement in diagnosing dysplasia in Barrett’s esophagus: comparison of routine glass slide vs. digital image examination. Lab Investig 93:471–489. https://doi.org/10.1038/labinvest.2013.36

    Article  Google Scholar 

  33. Sturm B, Fleskens S, Bot F et al (2013) Larynx virtual microscopy validation study. Virchows Arch 463:109–352. https://doi.org/10.1007/s00428-013-1444-y

    Article  Google Scholar 

  34. Sturm B, Mooi W, Creytens D et al (2017) Validation of diagnosing melanocytic lesions on whole slide images- does z-stack scanning improve diagnostic accuracy? Virchows Arch 471:S15. https://doi.org/10.1007/s00428-013-1444-y

    Article  Google Scholar 

  35. Maleeff BE (2014) Validation of a digital pathology whole slide imaging system. Microsc Microanal 20:1410–1411. https://doi.org/10.1017/S1431927614008782

    Article  Google Scholar 

  36. Eccher A, Calio A, Colombari R et al (2015) Validation of digital whole slide imaging according to the College of American Pathologists Guidelines in the evaluation of pre-implant kidney biopsies. Lab Investig 95:499A. https://doi.org/10.1038/labinvest.2015.25

    Article  Google Scholar 

  37. Hoffmann J, McGinnis L, Mafnas CT et al (2016) Validation of digital whole slide imaging system for intraoperative breast sentinel lymph node touch prep analysis: a single institution experience. Lab Investig 96:391–402. https://doi.org/10.1177/20101058110200S101

    Article  Google Scholar 

  38. Wilson I, Treanor D, Williams B (2017) Belfast Pathology 2017. 10th joint meeting of the British division of the international academy of pathology and the pathological Society of Great Britain & Ireland, 20-23 June 2017. J Pathol 243:S1–S41. https://doi.org/10.1002/path.4984

    Article  Google Scholar 

  39. Randell R, Ruddle RA, Mello-Thoms C, Thomas RG, Quirke P, Treanor D (2013) Virtual reality microscope versus conventional microscope regarding time to diagnosis: An experimental study. Histopathology 62:351–358. https://doi.org/10.1111/j.1365-2559.2012.04323.x

    Article  PubMed  Google Scholar 

  40. Lee JJ, Jedrych J, Pantanowitz L (2017) Validation of digital pathology for primary histopathological diagnosis of routine, inflammatory dermatopathology cases 0:1–7. https://doi.org/10.1097/DAD.0000000000000888

  41. Rodriguez-Urrego PA, Cronin AM, Al-Ahmadie HA et al (2011) Interobserver and intraobserver reproducibility in digital and routine microscopic assessment of prostate needle biopsies. Hum Pathol 42:68–74. https://doi.org/10.1016/j.humpath.2010.07.001

    Article  PubMed  Google Scholar 

  42. Jara-Lazaro AR, Tan PH (2012) Comparing digital and optical microscopy diagnoses of breast and prostate core biopsies. Pathology 44:46–48. https://doi.org/10.1097/PAT.0b013e32834e4254

    Article  PubMed  Google Scholar 

  43. Krishnamurthy S, Mathews K, McClure S, Murray M, Gilcrease M, Albarracin C, Spinosa J, Chang B, Ho J, Holt J, Cohen A, Giri D, Garg K, Bassett RL Jr, Liang K (2013) Multi-institutional comparison of whole slide digital imaging and optical microscopy for interpretation of hematoxylin-eosin-stained breast tissue sections. Arch Pathol Lab Med 137:1733–1739. https://doi.org/10.5858/arpa.2012-0437-OA

    Article  PubMed  Google Scholar 

  44. Campbell W, Lele S, West W et al (2012) Diagnoses rendered by whole slide imaging (WSI) alone are accurate for use in a general surgical pathology practice. Lab Investig 92:494–509. https://doi.org/10.1038/labinvest.2012.23

    Article  Google Scholar 

  45. Campbell WS, Lele SM, West WW, Lazenby AJ, Smith LM, Hinrichs SH (2012) Concordance between whole-slide imaging and light microscopy for routine surgical pathology. Hum Pathol 43:1739–1744. https://doi.org/10.1016/j.humpath.2011.12.023

    Article  PubMed  Google Scholar 

  46. Campbell WS, Hinrichs SH, Lele SM, Baker JJ, Lazenby AJ, Talmon GA, Smith LM, West WW (2014) Whole slide imaging diagnostic concordance with light microscopy for breast needle biopsies. Hum Pathol 45:1713–1721. https://doi.org/10.1016/j.humpath.2014.04.007

    Article  PubMed  Google Scholar 

  47. Brunelli M, Beccari S, Colombari R et al (2014) iPathology cockpit diagnostic station: validation according to College of American Pathologists Pathology and Laboratory Quality Center recommendation at the hospital trust and University of Verona. Diagn Pathol 9(Suppl 1):S12. https://doi.org/10.1186/1746-1596-9-S1-S12

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ordi J, Castillo P, Saco A, del Pino M, Ordi O, Rodríguez-Carunchio L, Ramírez J (2015) Validation of whole slide imaging in the primary diagnosis of gynaecological pathology in a university hospital. J Clin Pathol 68:33–39. https://doi.org/10.1136/jclinpath-2014-202524

    Article  PubMed  Google Scholar 

  49. Snead DRJ, Tsang YW, Meskiri A, Kimani PK, Crossman R, Rajpoot NM, Blessing E, Chen K, Gopalakrishnan K, Matthews P, Momtahan N, Read-Jones S, Sah S, Simmons E, Sinha B, Suortamo S, Yeo Y, el Daly H, Cree IA (2016) Validation of digital pathology imaging for primary histopathological diagnosis. Histopathology 68:1063–1072. https://doi.org/10.1111/his.12879

    Article  PubMed  Google Scholar 

  50. Fónyad L, Krenács T, Nagy P, Zalatnai A, Csomor J, Sápi Z, Pápay J, Schönléber J, Diczházi C, Molnár B (2012) Validation of diagnostic accuracy using digital slides in routine histopathology. Diagn Pathol 7:35. https://doi.org/10.1186/1746-1596-7-35

    Article  PubMed  PubMed Central  Google Scholar 

  51. Shah KK, Lehman JS, Gibson LE, Lohse CM, Comfere NI, Wieland CN (2016) Validation of diagnostic accuracy with whole-slide imaging compared with glass slide review in dermatopathology. J Am Acad Dermatol 75:1229–1237. https://doi.org/10.1016/j.jaad.2016.08.024

    Article  PubMed  Google Scholar 

  52. Elmore J, Longton G, Pepe M et al (2017) A randomized study comparing digital imaging to traditional glass slide microscopy for breast biopsy and cancer diagnosis. J Pathol Inform 8:12. https://doi.org/10.4103/2153-3539.201920

    Article  PubMed  PubMed Central  Google Scholar 

  53. Mills AM, Gradecki SE, Horton BJ et al (2018) Diagnostic Efficiency in Digital Pathology: A Comparison of Optical Versus Digital Assessment in 510 Surgical Pathology Cases. Am J Surg Pathol. 42(1):53–59. https://doi.org/10.1097/PAS.0000000000000930

  54. Foad AFA (2017) Comparing the use of virtual and conventional light microscopy in practical sessions: virtual reality in Tabuk University. J Taibah Univ Med Sci 12:183–186. https://doi.org/10.1016/j.jtumed.2016.10.015

    Article  PubMed  Google Scholar 

  55. Bauer TW, Schoenfield L, Slaw RJ, Yerian L, Sun Z, Henricks WH (2013) Validation of whole slide imaging for primary diagnosis in surgical pathology. Arch Pathol Lab Med 137:518–524. https://doi.org/10.5858/arpa.2011-0678-OA

    Article  PubMed  Google Scholar 

  56. Buck T, Dilorio R, Havrilla L, O′Neill D (2014) Validation of a whole slide imaging system for primary diagnosis in surgical pathology: a community hospital experience. J Pathol Inform 5:43. https://doi.org/10.4103/2153-3539.145731

    Article  PubMed  PubMed Central  Google Scholar 

  57. 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 

  58. 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 (2017) Whole slide imaging versus microscopy for primary diagnosis in surgical pathology. Am J Surg Pathol 42:1. https://doi.org/10.1097/PAS.0000000000000948

    Article  Google Scholar 

  59. Williams BJ, DaCosta P, Goacher E, Treanor D (2017) A systematic analysis of discordant diagnoses in digital pathology compared with light microscopy. Arch Pathol Lab Med 141:1712–1718. https://doi.org/10.5858/arpa.2016-0494-OA

    Article  PubMed  Google Scholar 

  60. Cornish TC, Swapp RE, Kaplan KJ (2012) Whole-slide Imaging. Adv Anat Pathol 19:152–159. https://doi.org/10.1097/PAP.0b013e318253459e

    Article  PubMed  Google Scholar 

  61. Saco A, Ramírez J, Rakislova N, Mira A, Ordi J (2016) Validation of whole-slide imaging for Histolopathogical diagnosis: current state. Pathobiology 83:89–98. https://doi.org/10.1159/000442823

    Article  PubMed  Google Scholar 

  62. Araújo ALD, Amaral-Silva GK, Fonseca FP, Palmier NR, Lopes MA, Speight PM, de Almeida OP, Vargas PA, Santos-Silva AR (2018) Validation of digital microscopy in the histopathological diagnoses of oral diseases. Virchows Arch 473:321–327. https://doi.org/10.1007/s00428-018-2382-5

    Article  PubMed  Google Scholar 

  63. Sanders DSA, Grabsch H, Harrison R, Bateman A, Going J, Goldin R, Mapstone N, Novelli M, Walker MM, Jankowski J, on behalf of the AspECT trial management group and trial principal investigators (2012) Comparing virtual with conventional microscopy for the consensus diagnosis of Barrett’s neoplasia in the AspECT Barrett’s chemoprevention trial pathology audit. Histopathology 61:795–800. https://doi.org/10.1111/j.1365-2559.2012.04288.x

    Article  PubMed  CAS  Google Scholar 

  64. Romero Lauro G, Cable W, Lesniak A, Tseytlin E, McHugh J, Parwani A, Pantanowitz L (2013) Digital pathology consultations - a new era in digital imaging, challenges and practical applications. J Digit Imaging 26:668–677. https://doi.org/10.1007/s10278-013-9572-0

    Article  PubMed  PubMed Central  Google Scholar 

  65. Boyce BF (2015) Whole slide imaging: uses and limitations for surgical pathology and teaching. Biotech Histochem 90:321–330. https://doi.org/10.3109/10520295.2015.1033463

    Article  PubMed  CAS  Google Scholar 

  66. Vodovnik A (2016) Diagnostic time in digital pathology: a comparative study on 400 cases. J Pathol Inform 7:4. https://doi.org/10.4103/2153-3539.175377

    Article  PubMed  PubMed Central  Google Scholar 

  67. Fernandes C, Bonan R, Bonan P et al (2018) Dental Students’ Perceptions and Performance in Use of Conventional and Virtual Microscopy in Oral Pathology. J Dent Educ 82:883–890. https://doi.org/10.21815/JDE.018.084

    Article  PubMed  Google Scholar 

  68. 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/10.1043/2009-0320-OA.1

    Article  PubMed  Google Scholar 

  69. Särndal C-E (2003) Stratified sampling. In: Model Assisted Survey Sampling. Springer, pp 100–109

  70. Leeflang MMG, Moons KGM, Reitsma JB, Zwinderman AH (2008) Bias in sensitivity and specificity caused by data-driven selection of optimal cutoff values: mechanisms, magnitude, and solutions. Clin Chem 54:729–737. https://doi.org/10.1373/clinchem.2007.096032

    Article  PubMed  CAS  Google Scholar 

Download references

Funding

Financial support was received from the Coordination for the Improvement of Higher Education Personnel (CAPES/PROEX, Brazil), the National Council for Scientific and Technological Development (CNPq, Brazil) and the grants from São Paulo Research Foundation (FAPESP, Brazil) process number: 2009/53839-2.

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Authors and Affiliations

  1. Oral Diagnosis Department, Semiology and Oral Pathology Areas, Piracicaba Dental School, University of Campinas (UNICAMP), Av. Limeira, 901, Bairro Areião, Piracicaba, São Paulo, 13414-903, Brazil

    Anna Luíza Damaceno Araújo, Lady Paola Aristizábal Arboleda, Natalia Rangel Palmier, Jéssica Montenegro Fonsêca, Mariana de Pauli Paglioni, Wagner Gomes-Silva, Ana Carolina Prado Ribeiro, Felipe Paiva Fonseca, Marcio Ajudarte Lopes, Oslei Paes de Almeida, Pablo Agustin Vargas & Alan Roger Santos-Silva

  2. Dental Oncology Service, Instituto do Câncer do Estado de São Paulo, Faculdade de Medicina da Universidade de São Paulo (FMSUP), São Paulo, Brazil

    Wagner Gomes-Silva, Ana Carolina Prado Ribeiro & Thaís Bianca Brandão

  3. Medical School of Nove de Julho University, São Paulo, Brazil

    Wagner Gomes-Silva

  4. Faculdade de Odontologia, Fernandópolis, Universidade Brasil, São Paulo, Brazil

    Ana Carolina Prado Ribeiro & Luciana Estevam Simonato

  5. Unit of Oral and Maxillofacial Pathology, School of Clinical Dentistry, University of Sheffield, Sheffield, UK

    Paul M. Speight

  6. Clinic, Pathology and Odontological Surgery Department, Minas Gerais Dental School, Federal University of Minas Gerais (UFMG), Belo Horizonte, Minas Gerais, Brazil

    Felipe Paiva Fonseca

  7. Dentistry Program, Health of Science Faculty, Corporación Universitaria Rafael Nuñez (CURN), Cartagena de Índias, Colombia

    Cristhian Camilo Madrid Troconis

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  1. Anna Luíza Damaceno Araújo
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All authors had substantial contributions to the conception, draft and design of this work, (Anna Luíza Damaceno Araújo, Natália Rangel Palmier, Cristhian Camilo Troconis, Paul M. Speight, Oslei Paes de Almeida, Marcio Ajudarte Lopes and Alan Roger Santos-Silva), as well as participation of the acquisition (Lady Paola Aristizábal Arboleda, Natália Rangel Palmier, Jéssica Montenegro Fonsêca, Mariana de Pauli Paglioni, Ana Carolina Prado Ribeiro, Pablo Agustin Vargas, Luciana Estevam Simonato and Wagner Gomes-Silva), analysis (Anna Luíza Damaceno Araújo, Felipe Paiva Fonseca and Lady Paola Aristizábal Arboleda), and interpretation (Anna Luíza Damaceno Araújo, Cristhian Camilo Troconis, Thaís Bianca Brandão and Alan Roger Santos-Silva) of data for the work. The final version of this work was reviewed and approved for publication by all parts included. Authors Anna Luíza Damaceno Araújo and Alan Roger Santos-Silva takes full responsibility for the work as a whole, including the study design, access to data and the decision to submit and publish the manuscript.

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Correspondence to Alan Roger Santos-Silva.

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All authors had substantial contributions to the conception, draft and design of this work, as well as participation of the acquisition, analysis and interpretation of data for the work. The final version of this work was approved for publication by all parts included. If there is a need, all authors agreed to be accountable for any aspects of the work and we ensure that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The authors also state that the material is original, has not been published elsewhere, and is being submitted only to the Virchows Archiv.

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Araújo, A.L.D., Arboleda, L.P.A., Palmier, N.R. et al. The performance of digital microscopy for primary diagnosis in human pathology: a systematic review. Virchows Arch 474, 269–287 (2019). https://doi.org/10.1007/s00428-018-02519-z

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