PICaSSO Histologic Remission Index (PHRI) in Ulcerative Colitis – Development of a Novel Simplified Histological Score for Monitoring Mucosal Healing and Predicting Clinical Outcomes and its Applicability in an Artificial Intelligence System

Journal article

Gui, X., Bazarova, A., del Amor, R., Vieth, M., de Hertogh, G., Villanacci, V., Zardo, D., Parigi, T. L., Røyset, E., Shivaji, U., Monica, M. A.T., Mandelli, G., Bhandari, P., Danese, S., Ferraz, J., Hayee, B., Lazarev, M., Parra-Blanco, A., Pastorelli, L., Panaccione, R., Rath, T., Tontini, G.E., Ralf, H., Bisschops, R., Grisan, E., Naranjo, V., Ghosh, S. and Iacucci, M. (2022). PICaSSO Histologic Remission Index (PHRI) in Ulcerative Colitis – Development of a Novel Simplified Histological Score for Monitoring Mucosal Healing and Predicting Clinical Outcomes and its Applicability in an Artificial Intelligence System. Gut. https://doi.org/10.1136/gutjnl-2021-326376
AuthorsGui, X., Bazarova, A., del Amor, R., Vieth, M., de Hertogh, G., Villanacci, V., Zardo, D., Parigi, T. L., Røyset, E., Shivaji, U., Monica, M. A.T., Mandelli, G., Bhandari, P., Danese, S., Ferraz, J., Hayee, B., Lazarev, M., Parra-Blanco, A., Pastorelli, L., Panaccione, R., Rath, T., Tontini, G.E., Ralf, H., Bisschops, R., Grisan, E., Naranjo, V., Ghosh, S. and Iacucci, M.
Abstract

Histological assessment is critical for the management of ulcerative colitis (UC). We aimed to develop a simple histologic index, aligned to endoscopy, correlated with clinical outcomes, and easy to apply to a computer aided diagnosis (CAD) system to evaluate inflammatory activity.
Methods
We analysed 614 biopsies from 307 UC patients enrolled into our prospective multicentre study, exploring the correlations between histological and endoscopic scores as well as adverse clinical outcomes. We then developed the PICaSSO histologic remission index (PHRI) and validated its reproducibility in comparison to multiple histologic indices. Finally, to implement PHRI into a CAD system, we trained and tested a novel deep learning strategy based on a convolutional neural network architecture to detect neutrophils, calculate PHRI and identify active from quiescent UC using a subset of 84 biopsies.
Results
PHRI showed the strongest correlation with endoscopic scores (MES, UCEIS, and PICaSSO) and with clinical outcomes. Our inter-reader agreement was almost perfect (ICC 0.84). A PHRI score of 1 could accurately stratify patients’ risk of adverse outcomes within 12 months. Our preliminary artificial intelligence algorithm identified active from quiescent UC with 80% sensitivity and 100% specificity.
Conclusions
PHRI is the simplest histological index in UC and it exhibits the highest correlation with endoscopic activity and clinical outcomes. A PHRI-based CAD was accurate in predicting histologic remission.

KeywordsInflammatory bowel disease (IBD); ulcerative colitis (UC); endoscopic remission (ER); mucosal healing (MH); histologic remission (HR); histologic healing (HH); histological index; artificial intelligence (AI); machine learning; computer aided diagnosis
Year2022
JournalGut
PublisherBMJ
Digital Object Identifier (DOI)https://doi.org/10.1136/gutjnl-2021-326376
Web address (URL)http://dx.doi.org/10.1136/gutjnl-2021-326376
Publication dates
Online16 Feb 2022
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Accepted22 Jan 2022
Deposited28 Jan 2022
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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