Computer-Aided Imaging Analysis of Probe-Based Confocal Laser Endomicroscopy With Molecular Labeling and Gene Expression Identifies Markers of Response to Biological Therapy in IBD Patients: The Endo-Omics Study

Journal article

Iacucci, M., Jeffery, L., Acharjee, A., Grisan, E., Buda, A., Nardone, O.M., Smith, S.C.L., Labarile, N., Zardo, D., Ungar, B., Hunter, S., Mao, R., Cannatelli,R., Shivaji, U.N., Parigi, T.L., Reynolds, G.M., Gkoutos, G.V. and Ghosh, S. (2022). Computer-Aided Imaging Analysis of Probe-Based Confocal Laser Endomicroscopy With Molecular Labeling and Gene Expression Identifies Markers of Response to Biological Therapy in IBD Patients: The Endo-Omics Study. Inflammatory Bowel Diseases. 2022 (izac233), pp. 1-12. https://doi.org/0.1093/ibd/izac233
AuthorsIacucci, M., Jeffery, L., Acharjee, A., Grisan, E., Buda, A., Nardone, O.M., Smith, S.C.L., Labarile, N., Zardo, D., Ungar, B., Hunter, S., Mao, R., Cannatelli,R., Shivaji, U.N., Parigi, T.L., Reynolds, G.M., Gkoutos, G.V. and Ghosh, S.
Abstract

Abstract
Background
We aimed to predict response to biologics in inflammatory bowel disease (IBD) using computerized image analysis of probe confocal laser endomicroscopy (pCLE) in vivo and assess the binding of fluorescent-labeled biologics ex vivo. Additionally, we investigated genes predictive of anti-tumor necrosis factor (TNF) response.

Methods
Twenty-nine patients (15 with Crohn’s disease [CD], 14 with ulcerative colitis [UC]) underwent colonoscopy with pCLE before and 12 to 14 weeks after starting anti-TNF or anti-integrin α4β7 therapy. Biopsies were taken for fluorescein isothiocyanate–labeled infliximab and vedolizumab staining and gene expression analysis. Computer-aided quantitative image analysis of pCLE was performed. Differentially expressed genes predictive of response were determined and validated in a public cohort.

Results
In vivo, vessel tortuosity, crypt morphology, and fluorescein leakage predicted response in UC (area under the receiver-operating characteristic curve [AUROC], 0.93; accuracy 85%, positive predictive value [PPV] 89%; negative predictive value [NPV] 75%) and CD (AUROC, 0.79; accuracy 80%; PPV 75%; NPV 83%) patients. Ex vivo, increased binding of labeled biologic at baseline predicted response in UC (UC) (AUROC, 83%; accuracy 77%; PPV 89%; NPV 50%) but not in Crohn’s disease (AUROC 58%). A total of 325 differentially expressed genes distinguished responders from nonresponders, 86 of which fell within the most enriched pathways. A panel including ACTN1, CXCL6, LAMA4, EMILIN1, CRIP2, CXCL13, and MAPKAPK2 showed good prediction of anti-TNF response (AUROC >0.7).

Conclusions
Higher mucosal binding of the drug target is associated with response to therapy in UC. In vivo, mucosal and microvascular changes detected by pCLE are associated with response to biologics in inflammatory bowel disease. Anti-TNF–responsive UC patients have a less inflamed and fibrotic state pretreatment. Chemotactic pathways involving CXCL6 or CXCL13 may be novel targets for therapy in nonresponders.

Keywordsulcerative colitis, Crohn’s disease, biological agents, probe confocal laser endomicroscopy, RNA transcriptomics, endoscopic molecular labeling, artificial intelligence
Year2022
JournalInflammatory Bowel Diseases
Journal citation2022 (izac233), pp. 1-12
PublisherOxford University Press (OUP)
ISSN1536-4844
Digital Object Identifier (DOI)https://doi.org/0.1093/ibd/izac233
Web address (URL)https://academic.oup.com/ibdjournal/advance-article/doi/10.1093/ibd/izac233/6827973#381182784
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Print15 Nov 2022
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Accepted11 Oct 2022
Deposited17 Nov 2022
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Favaron, T., Huang, D.Y., Christensen-Jeffries, K., Eckersley, R., Sidhu, P.S. and Grisan, E. (2019). Building a reduced dictionary of relevant perfusion patterns from CEUS data for the classification of testis lesions. 2019 IEEE 16th International Symposium on Biomedical Imaging. Venice, Italy 08 - 11 Apr 2019 Institute of Electrical and Electronics Engineers (IEEE). https://doi.org/10.1109/ISBI.2019.8759528
Deep Convolutional Neural Network for Survival Estimation of Amyotrophic Lateral Sclerosis patients
Grisan, E., Zandon`a, A. and Di Camillo, B. (2019). Deep Convolutional Neural Network for Survival Estimation of Amyotrophic Lateral Sclerosis patients. European Symposium on Artificial Neural Networks, Computational Intelligence and Machine Learning. Bruges, Belgium 24 - 26 Apr 2019 i6doc.
Prediction of Adverse Glycemic Events from Continuous Glucose Monitoring Signal
Gadaleta, M., Facchinetti, A., Grisan, E. and Rossi, M. (2019). Prediction of Adverse Glycemic Events from Continuous Glucose Monitoring Signal. IEEE Journal of Biomedical and Health Informatics. 23 (2). https://doi.org/10.1109/JBHI.2018.2823763
Sparse Image Reconstruction for Contrast Enhanced Cardiac Ultrasound using Diverging Waves
Stanziola, A., Toulemonde, M., Papadopoulou, V., Corbett, R., Duncan, N., Grisan, E. and Tang, M-X. (2019). Sparse Image Reconstruction for Contrast Enhanced Cardiac Ultrasound using Diverging Waves. IEEE International Ultrasonics Symposium 2019. Glasgow 09 2009 - 06 Oct 2019 Institute of Electrical and Electronics Engineers (IEEE).
Super resolution ultrasound image filtering with machine learning to reduce the localization error
Harput, S., Fong, L.H., Stanziola, A., Zhang, G., Toulemonde, M., Zhou, J., Christensen-Jeffries, K., Brown, J., Eckersley, R., Grisan, E., Dunsby, C. and Tang, M. (2019). Super resolution ultrasound image filtering with machine learning to reduce the localization error. IEEE International Ultrasonics Symposium 2019. Glasgow 09 2009 - 06 Oct 2019 Institute of Electrical and Electronics Engineers (IEEE).
Temporal Convolution Networks for Real-Time Abdominal Fetal Aorta Analysis with Ultrasound
Savioli, N., Visentin, S., Cosmi, E., Grisan, E., Lamata, P. and Montana, G. (2018). Temporal Convolution Networks for Real-Time Abdominal Fetal Aorta Analysis with Ultrasound. Artificial Neural Networks and Machine Learning – ICANN 2018. Rhodes, Greece 04 - 07 Oct 2018 Springer. https://doi.org/10.1007/978-3-030-01421-6_15
Quantitative imaging by pixel-based contrast-enhanced ultrasound reveals a linear relationship between synovial vascular perfusion and the recruitment of pathogenic IL-17A-F+IL-23+ CD161+ CD4+ T helper cells in psoriatic arthritis joints
Fiocco, U, Stramare, R, Martini, V, Coran, A, Caso, F, Costa, L, Felicetti, M, Rizzo, G, Tonietto, M, Scanu, A, Oliviero, F, Raffeiner, B, Vezzù, M, Lunardi, F, Scarpa, R, Sacerdoti, D, Rubaltelli, L, Punzi, L, Doria, A and Grisan, E (2017). Quantitative imaging by pixel-based contrast-enhanced ultrasound reveals a linear relationship between synovial vascular perfusion and the recruitment of pathogenic IL-17A-F+IL-23+ CD161+ CD4+ T helper cells in psoriatic arthritis joints. Clinical Rheumatology. 36 (2), pp. 391-399. https://doi.org/10.1007/s10067-016-3500-x
Boosting the Battery Life of Wearables for Health Monitoring Through the Compression of Biosignals
Hooshmand, M, Zordan, D, Del Testa, D, Grisan, E and Rossi, M (2017). Boosting the Battery Life of Wearables for Health Monitoring Through the Compression of Biosignals. IEEE Internet of Things Journal. 4, pp. 1647-1662. https://doi.org/10.1109/JIOT.2017.2689164
Detection of a slow-flow component in contrast-enhanced ultrasound of the synovia for the differential diagnosis of arthritis
Rizzo, G, Tonietto, M, Castellaro, M, Raffeiner, B, Coran, A, Fiocco, U, Stramare, R and Grisan, E (2017). Detection of a slow-flow component in contrast-enhanced ultrasound of the synovia for the differential diagnosis of arthritis. SPIE Medical Imaging. Orlando, FL, USA 11 - 16 Feb 2017 SPIE. https://doi.org/10.1117/12.2250818
Improving the quantification of contrast enhanced ultrasound using a Bayesian approach
Rizzo, G, Tonietto, M, Castellaro, M, Raffeiner, B, Coran, A, Fiocco, U, Stramare, R and Grisan, E (2017). Improving the quantification of contrast enhanced ultrasound using a Bayesian approach. SPIE Medical Imaging. Orlando, FL , USA 16 2016 - 11 Feb 2017 SPIE. https://doi.org/10.1117/12.2250195
Superpixel-based classification of gastric chromoendoscopy images
Boschetto, D and Grisan, E (2017). Superpixel-based classification of gastric chromoendoscopy images. SPIE Medical Imaging. Orlando, FL, USA 11 - 16 Feb 2017 SPIE. https://doi.org/10.1117/12.2254187
Boosted learned kernels for data-driven vesselness measure
Grisan, E (2017). Boosted learned kernels for data-driven vesselness measure. Proceedings Volume 10137, Medical Imaging 2017: Biomedical Applications in Molecular, Structural, and Functional Imaging; 101370Z (2017). Orlando, FL, USA 11 - 16 Feb 2017 SPIE. https://doi.org/10.1117/12.2250370
Cortical Thickness variability in Multiple Sclerosis: The role of lesion segmentation and filling
Palombit, A, Castellaro, M, Calabrese, M, Romualdi, C, Pizzini, FB, Montemezzi, S, Grisan, E and Bertoldo, A (2017). Cortical Thickness variability in Multiple Sclerosis: The role of lesion segmentation and filling. 2017 IEEE 14th International Symposium on Biomedical Imaging (ISBI 2017). Melbourne, VIC, Australia 18 - 21 Apr 2017 pp. 792-795 https://doi.org/10.1109/ISBI.2017.7950637
From macro to nano: Linking quantitative CEUS perfusion parameters to CD4+ T cells subtypes in spondyloarthtitis
Grisan, E, Rizzo, G, Tonietto, M, Coran, A, Raffeiner, B, Scanu, A, Martini, V, Stramare, R and Fiocco, U (2017). From macro to nano: Linking quantitative CEUS perfusion parameters to CD4+ T cells subtypes in spondyloarthtitis. 2017 IEEE 14th International Symposium on Biomedical Imaging (ISBI 2017). Melbourne, VIC, Australia 17 - 21 Apr 2017 Institute of Electrical and Electronics Engineers (IEEE). pp. 899-902 https://doi.org/10.1109/ISBI.2017.7950661
Grade and location of power doppler are predictive of damage progression in rheumatoid arthritis patients in clinical remission by anti-tumour necrosis factor α
Raffeiner, B, Grisan, E, Botsios, C, Stramare, R, Rizzo, G, Bernardi, L, Punzi, L, Ometto, F and Doria, A (2017). Grade and location of power doppler are predictive of damage progression in rheumatoid arthritis patients in clinical remission by anti-tumour necrosis factor α. Rheumatology (United Kingdom). 56, pp. 1320-1325. https://doi.org/10.1093/rheumatology/kex084
Bayesian Quantification of Contrast-Enhanced Ultrasound Images with Adaptive Inclusion of an Irreversible Component
Rizzo, G, Tonietto, M, Castellaro, M, Raffeiner, B, Coran, A, Fiocco, U, Stramare, R and Grisan, E (2017). Bayesian Quantification of Contrast-Enhanced Ultrasound Images with Adaptive Inclusion of an Irreversible Component. IEEE Transactions on Medical Imaging. 36, pp. 1027-1036. https://doi.org/10.1109/TMI.2016.2637698
Tcf7l2 plays pleiotropic roles in the control of glucose homeostasis, pancreas morphology, vascularization and regeneration
Facchinello, N, Tarifeño-Saldivia, E, Grisan, E, Schiavone, M, Peron, M, Mongera, A, Ek, O, Schmitner, N, Meyer, D, Peers, B, Tiso, N and Argenton, F (2017). Tcf7l2 plays pleiotropic roles in the control of glucose homeostasis, pancreas morphology, vascularization and regeneration. Scientific Reports. 7. https://doi.org/10.1038/s41598-017-09867-x
Growth abnormalities of fetuses and infants
Cosmi, E, Grisan, E, Fanos, V, Rizzo, G, Sivanandam, S and Visentin, S (2017). Growth abnormalities of fetuses and infants. BioMed Research International. 2017. https://doi.org/https://www.doi.org/10.1155/2017/3191308
A possible new approach in the prediction of late gestational hypertension: The role of the fetal aortic intima-media thickness
Visentin, S, Londero, AP, Camerin, M, Grisan, E and Cosmi, E (2017). A possible new approach in the prediction of late gestational hypertension: The role of the fetal aortic intima-media thickness. Medicine (United States). 96. https://doi.org/https://www.doi.org/10.1097/MD.0000000000005515
Automatic classification of small bowel mucosa alterations in celiac disease for confocal laser endomicroscopy
Boschetto, D, Di Claudio, G, Mirzaei, H, Leong, R and Grisan, E (2016). Automatic classification of small bowel mucosa alterations in celiac disease for confocal laser endomicroscopy. Medical Imaging 2016: Biomedical Applications in Molecular, Structural, and Functional Imaging. San Diego, United States 27 Feb - 03 Mar 2016 SPIE. https://doi.org/10.1117/12.2217183
Automatic classification of endoscopic images for premalignant conditions of the esophagus
Boschetto, D, Gambaretto, G and Grisan, E (2016). Automatic classification of endoscopic images for premalignant conditions of the esophagus. Medical Imaging 2016: Biomedical Applications in Molecular, Structural, and Functional Imaging. San Diego, United States 27 Feb - 03 Mar 2016 https://doi.org/10.1117/12.2216826
Superpixel-based automatic segmentation of villi in confocal endomicroscopy
Boschetto, D, Mirzaei, H, Leong, RWL and Grisan, E (2016). Superpixel-based automatic segmentation of villi in confocal endomicroscopy. 2016 IEEE-EMBS International Conference on Biomedical and Health Informatics (BHI). Las Vegas, NV, USA 24 - 27 Feb 2016 pp. 168-171 https://doi.org/10.1109/BHI.2016.7455861
Quantification of kidneys from 3D ultrasound in pediatric hydronephrosis
Cerrolaza, J.J., Grisan, E., Safdar, N., Myers, E., Jago, J., Peters, C.A. and Linguraru, M.G. (2015). Quantification of kidneys from 3D ultrasound in pediatric hydronephrosis. Institute of Electrical and Electronics Engineers (IEEE). https://doi.org/10.1109/embc.2015.7318324