Skip to main content
Top

03-05-2024 | Mucosa Associated Lymphoid Tissue | Oncology

Artificial intelligence-based differential diagnosis of orbital MALT lymphoma and IgG4 related ophthalmic disease using hematoxylin–eosin images

Authors: Mizuki Tagami, Mizuho Nishio, Atsuko Yoshikawa, Norihiko Misawa, Atsushi Sakai, Yusuke Haruna, Mami Tomita, Atsushi Azumi, Shigeru Honda

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology

Login to get access

Abstract

Purpose

To investigate the possibility of distinguishing between IgG4-related ophthalmic disease (IgG4-ROD) and orbital MALT lymphoma using artificial intelligence (AI) and hematoxylin–eosin (HE) images.

Methods

After identifying a total of 127 patients from whom we were able to procure tissue blocks with IgG4-ROD and orbital MALT lymphoma, we performed histological and molecular genetic analyses, such as gene rearrangement. Subsequently, pathological HE images were collected from these patients followed by the cutting out of 10 different image patches from the HE image of each patient. A total of 970 image patches from the 97 patients were used to construct nine different models of deep learning, and the 300 image patches from the remaining 30 patients were used to evaluate the diagnostic performance of the models. Area under the curve (AUC) and accuracy (ACC) were used for the performance evaluation of the deep learning models. In addition, four ophthalmologists performed the binary classification between IgG4-ROD and orbital MALT lymphoma.

Results

EVA, which is a vision-centric foundation model to explore the limits of visual representation, was the best deep learning model among the nine models. The results of EVA were ACC = 73.3% and AUC = 0.807. The ACC of the four ophthalmologists ranged from 40 to 60%.

Conclusions

It was possible to construct an AI software based on deep learning that was able to distinguish between IgG4-ROD and orbital MALT. This AI model may be useful as an initial screening tool to direct further ancillary investigations.
Literature
2.
go back to reference Sogabe Y, Ohshima K-i, Azumi A, Takahira M, Kase S, Tsuji H, Yoshikawa H, Nakamura T (2014) Location and frequency of lesions in patients with IgG4-related ophthalmic diseases. Graefes Arch Clin Exp Ophthalmol 252:531–538CrossRefPubMed Sogabe Y, Ohshima K-i, Azumi A, Takahira M, Kase S, Tsuji H, Yoshikawa H, Nakamura T (2014) Location and frequency of lesions in patients with IgG4-related ophthalmic diseases. Graefes Arch Clin Exp Ophthalmol 252:531–538CrossRefPubMed
3.
go back to reference Deshpande V, Zen Y, Chan JK, Yi EE, Sato Y, Yoshino T, Klöppel G, Heathcote JG, Khosroshahi A, Ferry JA (2012) Consensus statement on the pathology of IgG4-related disease. Mod Pathol 25:1181–1192CrossRefPubMed Deshpande V, Zen Y, Chan JK, Yi EE, Sato Y, Yoshino T, Klöppel G, Heathcote JG, Khosroshahi A, Ferry JA (2012) Consensus statement on the pathology of IgG4-related disease. Mod Pathol 25:1181–1192CrossRefPubMed
4.
go back to reference Andrew NH, Sladden N, Kearney DJ, Selva D (2015) An analysis of IgG4-related disease (IgG4-RD) among idiopathic orbital inflammations and benign lymphoid hyperplasias using two consensus-based diagnostic criteria for IgG4-RD. Br J Ophthalmol 99:376–381CrossRefPubMed Andrew NH, Sladden N, Kearney DJ, Selva D (2015) An analysis of IgG4-related disease (IgG4-RD) among idiopathic orbital inflammations and benign lymphoid hyperplasias using two consensus-based diagnostic criteria for IgG4-RD. Br J Ophthalmol 99:376–381CrossRefPubMed
5.
go back to reference Cleary ML, Chao J, Warnke R, Sklar J (1984) Immunoglobulin gene rearrangement as a diagnostic criterion of B-cell lymphoma. Proc Natl Acad Sci 81:593–597CrossRefPubMedPubMedCentral Cleary ML, Chao J, Warnke R, Sklar J (1984) Immunoglobulin gene rearrangement as a diagnostic criterion of B-cell lymphoma. Proc Natl Acad Sci 81:593–597CrossRefPubMedPubMedCentral
7.
go back to reference Tagami M, Nishio M, Katsuyama-Yoshikawa A, Misawa N, Sakai A, Haruna Y, Azumi A, Honda S (2023) Machine learning model with texture analysis for automatic classification of histopathological images of ocular adnexal mucosa-associated lymphoid tissue lymphoma of two different origins. Curr Eye Res 1–8. https://doi.org/10.1080/02713683.2023.2246696 Tagami M, Nishio M, Katsuyama-Yoshikawa A, Misawa N, Sakai A, Haruna Y, Azumi A, Honda S (2023) Machine learning model with texture analysis for automatic classification of histopathological images of ocular adnexal mucosa-associated lymphoid tissue lymphoma of two different origins. Curr Eye Res 1–8. https://​doi.​org/​10.​1080/​02713683.​2023.​2246696
9.
go back to reference Fang Y, Wang W, Xie B, Sun Q, Wu L, Wang X, Huang T, Wang X, Cao Y (2023) Eva: exploring the limits of masked visual representation learning at scale. Proceedings of the IEEE/CVF Conference on Computer Vision and Pattern Recognition, pp 19358–19369. https://arxiv.org/abs/2211.07636 Fang Y, Wang W, Xie B, Sun Q, Wu L, Wang X, Huang T, Wang X, Cao Y (2023) Eva: exploring the limits of masked visual representation learning at scale. Proceedings of the IEEE/CVF Conference on Computer Vision and Pattern Recognition, pp 19358–19369.  https://​arxiv.​org/​abs/​2211.​07636
10.
go back to reference Dosovitskiy A, Beyer L, Kolesnikov A, Weissenborn D, Zhai X, Unterthiner T, Dehghani M, Minderer M, Heigold G, Gelly S (2020) An image is worth 16x16 words: transformers for image recognition at scale. https://arxiv.org/abs/2010.11929 Dosovitskiy A, Beyer L, Kolesnikov A, Weissenborn D, Zhai X, Unterthiner T, Dehghani M, Minderer M, Heigold G, Gelly S (2020) An image is worth 16x16 words: transformers for image recognition at scale. https://​arxiv.​org/​abs/​2010.​11929
11.
go back to reference Tan M, Le Q (2019) EfficientNet: rethinking model scaling for convolutional neural networks. In: Kamalika C, Ruslan S (eds) Proceedings of the 36th International Conference on Machine Learning. PMLR, Proceedings of Machine Learning Research, pp. 6105–6114. https://arxiv.org/abs/1905.11946 Tan M, Le Q (2019) EfficientNet: rethinking model scaling for convolutional neural networks. In: Kamalika C, Ruslan S (eds) Proceedings of the 36th International Conference on Machine Learning. PMLR, Proceedings of Machine Learning Research, pp. 6105–6114. https://​arxiv.​org/​abs/​1905.​11946
13.
go back to reference Miyoshi H, Sato K, Kabeya Y, Yonezawa S, Nakano H, Takeuchi Y, Ozawa I, Higo S, Yanagida E, Yamada K (2020) Deep learning shows the capability of high-level computer-aided diagnosis in malignant lymphoma. Lab Invest 100:1300–1310CrossRefPubMed Miyoshi H, Sato K, Kabeya Y, Yonezawa S, Nakano H, Takeuchi Y, Ozawa I, Higo S, Yanagida E, Yamada K (2020) Deep learning shows the capability of high-level computer-aided diagnosis in malignant lymphoma. Lab Invest 100:1300–1310CrossRefPubMed
14.
go back to reference Cheuk W, Yuen HK, Chan JK (2007) Chronic sclerosing dacryoadenitis: part of the spectrum of IgG4-related Sclerosing disease? Am J Surg Pathol 31:643–645CrossRefPubMed Cheuk W, Yuen HK, Chan JK (2007) Chronic sclerosing dacryoadenitis: part of the spectrum of IgG4-related Sclerosing disease? Am J Surg Pathol 31:643–645CrossRefPubMed
15.
go back to reference Umehara H, Okazaki K, Masaki Y, Kawano M, Yamamoto M, Saeki T, Matsui S, Yoshino T, Nakamura S, Kawa S, Hamano H, Kamisawa T, Shimosegawa T, Shimatsu A, Nakamura S, Ito T, Notohara K, Sumida T, Tanaka Y, Mimori T, Chiba T, Mishima M, Hibi T, Tsubouchi H, Inui K, Ohara H (2012) Comprehensive diagnostic criteria for IgG4-related disease (IgG4-RD), 2011. Mod Rheumatol 22:21–30. https://doi.org/10.1007/s10165-011-0571-zCrossRefPubMed Umehara H, Okazaki K, Masaki Y, Kawano M, Yamamoto M, Saeki T, Matsui S, Yoshino T, Nakamura S, Kawa S, Hamano H, Kamisawa T, Shimosegawa T, Shimatsu A, Nakamura S, Ito T, Notohara K, Sumida T, Tanaka Y, Mimori T, Chiba T, Mishima M, Hibi T, Tsubouchi H, Inui K, Ohara H (2012) Comprehensive diagnostic criteria for IgG4-related disease (IgG4-RD), 2011. Mod Rheumatol 22:21–30. https://​doi.​org/​10.​1007/​s10165-011-0571-zCrossRefPubMed
19.
go back to reference Swiderska-Chadaj Z, Hebeda KM, van den Brand M, Litjens G (2021) Artificial intelligence to detect MYC translocation in slides of diffuse large B-cell lymphoma. Virchows Arch 479:617–621CrossRefPubMed Swiderska-Chadaj Z, Hebeda KM, van den Brand M, Litjens G (2021) Artificial intelligence to detect MYC translocation in slides of diffuse large B-cell lymphoma. Virchows Arch 479:617–621CrossRefPubMed
20.
go back to reference El Hussein S, Chen P, Medeiros LJ, Wistuba II, Jaffray D, Wu J, Khoury JD (2022) Artificial intelligence strategy integrating morphologic and architectural biomarkers provides robust diagnostic accuracy for disease progression in chronic lymphocytic leukemia. J Pathol 256:4–14CrossRefPubMed El Hussein S, Chen P, Medeiros LJ, Wistuba II, Jaffray D, Wu J, Khoury JD (2022) Artificial intelligence strategy integrating morphologic and architectural biomarkers provides robust diagnostic accuracy for disease progression in chronic lymphocytic leukemia. J Pathol 256:4–14CrossRefPubMed
21.
go back to reference El Achi H, Khoury JD (2020) Artificial intelligence and digital microscopy applications in diagnostic hematopathology. Cancers (Basel) 12:797CrossRefPubMed El Achi H, Khoury JD (2020) Artificial intelligence and digital microscopy applications in diagnostic hematopathology. Cancers (Basel) 12:797CrossRefPubMed
22.
go back to reference Li D, Bledsoe JR, Zeng Y, Liu W, Hu Y, Bi K, Liang A, Li S (2020) A deep learning diagnostic platform for diffuse large B-cell lymphoma with high accuracy across multiple hospitals. Nat Commun 11:1–9CrossRef Li D, Bledsoe JR, Zeng Y, Liu W, Hu Y, Bi K, Liang A, Li S (2020) A deep learning diagnostic platform for diffuse large B-cell lymphoma with high accuracy across multiple hospitals. Nat Commun 11:1–9CrossRef
23.
go back to reference Sato Y, Notohara K, Kojima M, Takata K, Masaki Y, Yoshino T (2010) IgG4-related disease: historical overview and pathology of hematological disorders. Pathol Int 60:247–258CrossRefPubMed Sato Y, Notohara K, Kojima M, Takata K, Masaki Y, Yoshino T (2010) IgG4-related disease: historical overview and pathology of hematological disorders. Pathol Int 60:247–258CrossRefPubMed
24.
go back to reference Bledsoe JR, Wallace ZS, Deshpande V, Richter JR, Klapman J, Cowan A, Stone JH, Ferry JA (2017) Atypical IgG4+ plasmacytic proliferations and lymphomas: characterization of 11 cases. Am J Clin Pathol 148:215–235CrossRefPubMed Bledsoe JR, Wallace ZS, Deshpande V, Richter JR, Klapman J, Cowan A, Stone JH, Ferry JA (2017) Atypical IgG4+ plasmacytic proliferations and lymphomas: characterization of 11 cases. Am J Clin Pathol 148:215–235CrossRefPubMed
25.
go back to reference Bledsoe JR, Wallace ZS, Stone JH, Deshpande V, Ferry JA (2018) Lymphomas in IgG4-related disease: clinicopathologic features in a Western population. Virchows Arch 472:839–852CrossRefPubMed Bledsoe JR, Wallace ZS, Stone JH, Deshpande V, Ferry JA (2018) Lymphomas in IgG4-related disease: clinicopathologic features in a Western population. Virchows Arch 472:839–852CrossRefPubMed
Metadata
Title
Artificial intelligence-based differential diagnosis of orbital MALT lymphoma and IgG4 related ophthalmic disease using hematoxylin–eosin images
Authors
Mizuki Tagami
Mizuho Nishio
Atsuko Yoshikawa
Norihiko Misawa
Atsushi Sakai
Yusuke Haruna
Mami Tomita
Atsushi Azumi
Shigeru Honda
Publication date
03-05-2024
Publisher
Springer Berlin Heidelberg
Published in
Graefe's Archive for Clinical and Experimental Ophthalmology
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI
https://doi.org/10.1007/s00417-024-06501-1