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Original article|Articles in Press

Development and validation of a convolutional neural network model for diagnosing Helicobacter pylori infections with endoscopic images: a multicenter study

  • Author Footnotes
    ∗ Dr Seo and Hotak Hong contributed equally to this article.
    Ji Yeon Seo
    Footnotes
    ∗ Dr Seo and Hotak Hong contributed equally to this article.
    Affiliations
    Department of Internal Medicine, Healthcare Research Institute, Healthcare System Gangnam Center, Seoul National University Hospital, Seoul, Republic of Korea
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  • Author Footnotes
    ∗ Dr Seo and Hotak Hong contributed equally to this article.
    Hotak Hong
    Footnotes
    ∗ Dr Seo and Hotak Hong contributed equally to this article.
    Affiliations
    Artificial Intelligence Research Center, JLK Inc, Seoul, Republic of Korea
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  • Wi-Sun Ryu
    Affiliations
    Artificial Intelligence Research Center, JLK Inc, Seoul, Republic of Korea
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  • Dongmin Kim
    Affiliations
    Artificial Intelligence Research Center, JLK Inc, Seoul, Republic of Korea
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  • Jaeyoung Chun
    Affiliations
    Department of Internal Medicine, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea
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  • Min-Sun Kwak
    Correspondence
    Reprint requests: Min-Sun Kwak, MD, PhD, Department of Internal Medicine, Healthcare Research Institute, Healthcare System Gangnam Center, Seoul National University Hospital, 39FL, Gangnam Finance Center 737, Yeoksam-Dong, Gangnam-Gu, Seoul 06236, Korea.
    Affiliations
    Department of Internal Medicine, Healthcare Research Institute, Healthcare System Gangnam Center, Seoul National University Hospital, Seoul, Republic of Korea
    Search for articles by this author
  • Author Footnotes
    ∗ Dr Seo and Hotak Hong contributed equally to this article.
Published:January 11, 2023DOI:https://doi.org/10.1016/j.gie.2023.01.007

      Background and Aims

      Insufficient validation limits the generalizability of deep learning in diagnosing Helicobacter pylori infection with endoscopic images. The aim of this study was to develop a deep learning model for the diagnosis of H pylori infection using endoscopic images and validate the model with internal and external datasets.

      Methods

      A convolutional neural network (CNN) model was developed based on a training dataset comprising 13,403 endoscopic images from 952 patients who underwent endoscopy at Seoul National University Hospital Gangnam Center. Internal validation was performed using a separate dataset comprised of images of 411 individuals of Korean descent and 131 of non-Korean descent. External validation was performed with the images of 160 patients in Gangnam Severance Hospital. Gradient-weighted class activation mapping was performed to visually explain the model.

      Results

      In predicting H pylori ever-infected status, the sensitivity, specificity, and accuracy of internal validation for people of Korean descent were .96 (95% confidence interval [CI], .93-.98), .90 (95% CI, .85-.95), and .94 (95% CI, .91-.96), respectively. In the internal validation for people of non-Korean descent, the sensitivity, specificity, and accuracy in predicting H pylori ever-infected status were .92 (95% CI, .86-.98), .79 (95% CI, .67-.91), and .88 (95% CI, .82-.93), respectively. In the external validation cohort, sensitivity, specificity, and accuracy were .86 (95% CI, .80-.93), .88 (95% CI, .79-.96), and .87 (95% CI, .82-.92), respectively, when performing 2-group categorization. Gradient-weighted class activation mapping showed that the CNN model captured the characteristic findings of each group.

      Conclusions

      This CNN model for diagnosing H pylori infection showed good overall performance in internal and external validation datasets, particularly in categorizing patients into the never- versus ever-infected groups.

      Abbreviations:

      AI (artificial intelligence), CNN (convolutional neural network), CI (confidence interval), SNUH-GC (Seoul National University Hospital Gangnam Center)
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      References

        • Bray F.
        • Ferlay J.
        • Soerjomataram I.
        • et al.
        Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
        CA Cancer J Clin. 2018; 68: 394-424
        • Correa P.
        • Houghton J.
        Carcinogenesis of Helicobacter pylori.
        Gastroenterology. 2007; 133: 659-672
        • Thijs J.C.
        • van Zwet A.A.
        • Thijs W.J.
        • et al.
        Diagnostic tests for Helicobacter pylori: a prospective evaluation of their accuracy, without selecting a single test as the gold standard.
        Am J Gastroenterol. 1996; 91: 2125-2129
        • IARC Helicobacter pylori Working Group
        Helicobacter pylori eradication as a strategy for gastric cancer prevention. Lyon, France: International Agency for Research on Cancer (IARC Working Group Reports, No. 8).
        (Available at:)
        • Choi I.J.
        • Kim C.G.
        • Lee J.Y.
        • et al.
        Family history of gastric cancer and Helicobacter pylori treatment.
        N Engl J Med. 2020; 382: 427-436
        • Choi I.J.
        • Kook M.C.
        • Kim Y.I.
        • et al.
        Helicobacter pylori therapy for the prevention of metachronous gastric cancer.
        N Engl J Med. 2018; 378: 1085-1095
        • Ford A.C.
        • Forman D.
        • Hunt R.H.
        • et al.
        Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta-analysis of randomised controlled trials.
        BMJ. 2014; 348: g3174
        • Best L.M.
        • Takwoingi Y.
        • Siddique S.
        • et al.
        Non-invasive diagnostic tests for Helicobacter pylori infection.
        Cochrane Database Syst Rev. 2018; 3: CD012080
        • Ferwana M.
        • Abdulmajeed I.
        • Alhajiahmed A.
        • et al.
        Accuracy of urea breath test in Helicobacter pylori infection: meta-analysis.
        World J Gastroenterol. 2015; 21: 1305-1314
        • Lin C.W.
        • Wang H.H.
        • Chang Y.F.
        • et al.
        Evaluation of CLO test and polymerase chain reaction for biopsy-dependent diagnosis of Helicobacter pylori infection.
        Zhonghua Min Guo Wei Sheng Wu Ji Mian Yi Xue Za Zhi. 1997; 30: 219-227
        • Gisbert J.P.
        • Esteban C.
        • Jimenez I.
        • et al.
        13C-urea breath test during hospitalization for the diagnosis of Helicobacter pylori infection in peptic ulcer bleeding.
        Helicobacter. 2007; 12: 231-237
        • Glover B.
        • Teare J.
        • Ashrafian H.
        • et al.
        The endoscopic predictors of Helicobacter pylori status: a meta-analysis of diagnostic performance.
        Ther Adv Gastrointest Endosc. 2020;
        • Sugano K.
        Screening of gastric cancer in Asia.
        Best Pract Res Clin Gastroenterol. 2015; 29: 895-905
        • Watanabe K.
        • Nagata N.
        • Shimbo T.
        • et al.
        Accuracy of endoscopic diagnosis of Helicobacter pylori infection according to level of endoscopic experience and the effect of training.
        BMC Gastroenterol. 2013; 13: 128
        • Bang C.S.
        • Lee J.J.
        • Baik G.H.
        Artificial intelligence for the prediction of Helicobacter pylori infection in endoscopic images: systematic review and meta-analysis of diagnostic test accuracy.
        J Med Internet Res. 2020; 22e21983
        • Dilaghi E.
        • Lahner E.
        • Annibale B.
        • et al.
        Systematic review and meta-analysis: artificial intelligence for the diagnosis of gastric precancerous lesions and Helicobacter pylori infection.
        Dig Liver Dis. 2022;
        • Shichijo S.
        • Endo Y.
        • Aoyama K.
        • et al.
        Application of convolutional neural networks for evaluating Helicobacter pylori infection status on the basis of endoscopic images.
        Scand J Gastroenterol. 2019; 54: 158-163
        • Yasuda T.
        • Hiroyasu T.
        • Hiwa S.
        • et al.
        Potential of automatic diagnosis system with linked color imaging for diagnosis of Helicobacter pylori infection.
        Dig Endosc. 2020; 32: 373-381
        • Nakashima H.
        • Kawahira H.
        • Kawachi H.
        • et al.
        Endoscopic three-categorical diagnosis of Helicobacter pylori infection using linked color imaging and deep learning: a single-center prospective study (with video).
        Gastric Cancer. 2020; 23: 1033-1040
        • Johnson J.M.
        • Khoshgoftaar T.M.
        Survey on deep learning with class imbalance.
        J Big Data. 2019; 6: 27
        • Poolsawad N.
        • Kambhampati C.
        • Cleland J.G.F.
        Balancing class for performance of classification with a clinical dataset.
        Lecture Notes Engineer Comput Sci. 2014; 1: 237-242
      1. Szegedy C, Vanhoucke V, Ioffe S, et al. Rethinking the inception architecture for computer vision. 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR). 2016. p. 2818-26.

        • Hirasawa T.
        • Ikenoyama Y.
        • Ishioka M.
        • et al.
        Current status and future perspective of artificial intelligence applications in endoscopic diagnosis and management of gastric cancer.
        Dig Endosc. 2021; 33: 263-272
        • Virtanen P.
        • Gommers R.
        • Oliphant T.E.
        • et al.
        SciPy 1.0: fundamental algorithms for scientific computing in Python.
        Nat Methods. 2020; 17: 261-272
        • Shichijo S.
        • Nomura S.
        • Aoyama K.
        • et al.
        Application of convolutional neural networks in the diagnosis of Helicobacter pylori infection based on endoscopic images.
        EBioMed. 2017; 25: 106-111
        • Mohan B.P.
        • Khan S.R.
        • Kassab L.L.
        • et al.
        Convolutional neural networks in the computer-aided diagnosis of Helicobacter pylori infection and non-causal comparison to physician endoscopists: a systematic review with meta-analysis.
        Ann Gastroenterol. 2021; 34: 20-25
        • Yoshii S.
        • Mabe K.
        • Watano K.
        • et al.
        Validity of endoscopic features for the diagnosis of Helicobacter pylori infection status based on the Kyoto classification of gastritis.
        Dig Endosc. 2020; 32: 74-83
        • Weng C.Y.
        • Xu J.L.
        • Sun S.P.
        • et al.
        Helicobacter pylori eradication: Exploring its impacts on the gastric mucosa.
        World J Gastroenterol. 2021; 27: 5152-5170
        • Quach D.T.
        • Aoki R.
        • Iga A.
        • et al.
        Diagnostic accuracy of H. pylori status by conventional endoscopy: time-trend change after eradication and impact of endoscopic image quality.
        Front Med. 2021; 8830730
        • Ryu K.H.
        • Yi S.Y.
        • Na Y.J.
        • et al.
        Reinfection rate and endoscopic changes after successful eradication of Helicobacter pylori.
        World J Gastroenterol. 2010; 16: 251-255
        • Ghassemi M.
        • Oakden-Rayner L.
        • Beam A.L.
        The false hope of current approaches to explainable artificial intelligence in health care.
        Lancet Digit Health. 2021; 3: e745-e750
        • Hooi J.K.Y.
        • Lai W.Y.
        • Ng W.K.
        • et al.
        Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis.
        Gastroenterology. 2017; 153: 420-429
        • Mahamid M.
        • Mari A.
        • Khoury T.
        • et al.
        Endoscopic and histological findings among Israeli populations infected with Helicobacter pylori: Does ethnicity matter?.
        Isr Med Assoc J. 2019; 21: 339-344
        • Abe T.
        • Kodama M.
        • Murakami K.
        • et al.
        Impact of Helicobacter pylori CagA diversity on gastric mucosal damage: an immunohistochemical study of East-Asian-type CagA.
        J Gastroenterol Hepatol. 2011; 26: 688-693
        • Sakaki N.
        • Kozawa H.
        • Egawa N.
        • et al.
        Ten-year prospective follow-up study on the relationship between Helicobacter pylori infection and progression of atrophic gastritis, particularly assessed by endoscopic findings.
        Aliment Pharmacol Ther. 2002; 16: 198-203