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1. A Solve-RD ClinVar-based reanalysis of 1522 index cases from ERN-ITHACA reveals common pitfalls and misinterpretations in exome sequencing

Author

Denomme-Pichon A. -S., Bruel A. -L., Duffourd Y., Safraou H., Thauvin-Robinet C., Tran Mau-Them F., Philippe C., Vitobello A., Jean-Marcais N., Moutton S., Thevenon J., Faivre L., Matalonga L., de Boer E., Gilissen C., Hoischen A., Kleefstra T., Pfundt R., de Vries B. B. A., Willemsen M. H., Vissers L. E. L. M., Jackson A., Banka S., Clayton-Smith J., Benetti E., Fallerini C., Renieri A., Ciolfi A., Dallapiccola B., Pizzi S., Radio F. C., Tartaglia M., Ellwanger K., Graessner H., Haack T. B., Zurek B., Havlovicova M., Macek M., Ryba L., Schwarz M., Votypka P., Lopez-Martin E., Posada M., Mencarelli M. A., Rooryck C., Trimouille A., Verloes A., Abbott K. M., Kerstjens M., Martin E. L., Maystadt I., Morleo M., Nigro V., Pinelli M., Riess O., Agathe J. -M. D. S., Santen G. W. E., Thauvin C., Torella A., Vissers L., Zguro K., Boer E. D., Cohen E., Danis D., Gao F., Horvath R., Johari M., Johanson L., Li S., Morsy H., Nelson I., Paramonov I., te Paske I. B. A. W., Robinson P., Savarese M., Steyaert W., Topf A., van der Velde J. K., Vandrovcova J., Ossowski S., Demidov G., Sturm M., Schulze-Hentrich J. M., Schule R., Xu J., Kessler C., Wayand M., Synofzik M., Wilke C., Traschutz A., Schols L., Hengel H., Lerche H., Kegele J., Heutink P., Brunner H., Scheffer H., Hoogerbrugge N., 't Hoen P. A. C., Sablauskas K., de Voer R. M., Kamsteeg E. -J., van de Warrenburg B., van Os N., Paske I. T., Janssen E., Steehouwer M., Yaldiz B., Brookes A. J., Veal C., Gibson S., Maddi V., Mehtarizadeh M., Riaz U., Warren G., Dizjikan F. Y., Shorter T., Straub V., Bettolo C. M., Manera J. D., Hambleton S., Engelhardt K., Alexander E., Peyron C., Pelissier A., Beltran S., Gut I. G., Laurie S., Piscia D., Papakonstantinou A., Bullich G., Corvo A., Fernandez-Callejo M., Hernandez C., Pico D., Lochmuller H., Gumus G., Bros-Facer V., Rath A., Hanauer M., Lagorce D., Hongnat O., Chahdil M., Lebreton E., Stevanin G., Durr A., Davoine C. -S., Guillot-Noel L., Heinzmann A., Coarelli G., Bonne G., Evangelista T., Allamand V., Ben Yaou R., Metay C., Eymard B., Atalaia A., Stojkovic T., Turnovec M., Thomasova D., Kremlikova R. P., Frankova V., Liskova P., Dolezalova P., Parkinson H., Keane T., Freeberg M., Thomas C., Spalding D., Robert G., Costa A., Patch C., Hanna M., Houlden H., Reilly M., Efthymiou S., Cali E., Magrinelli F., Sisodiya S. M., Rohrer J., Muntoni F., Zaharieva I., Sarkozy A., Timmerman V., Baets J., de Vries G., De Winter J., Beijer D., de Jonghe P., Van de Vondel L., De Ridder W., Weckhuysen S., Mutarelli M., Varavallo A., Banfi S., Musacchia F., Piluso G., Ferlini A., Selvatici R., Gualandi F., Bigoni S., Rossi R., Neri M., Aretz S., Spier I., Sommer A. K., Peters S., Oliveira C., Pelaez J. G., Matos A. R., Jose C. S., Ferreira M., Gullo I., Fernandes S., Garrido L., Ferreira P., Carneiro F., Swertz M. A., Johansson L., van der Vries G., Neerincx P. B., Ruvolo D., Kerstjens Frederikse W. S., Zonneveld-Huijssoon E., Roelofs-Prins D., van Gijn M., Kohler S., Metcalfe A., Drunat S., Heron D., Mignot C., Keren B., Lacombe D., Capella G., Valle L., Holinski-Feder E., Laner A., Steinke-Lange V., Cilio M. -R., Carpancea E., Depondt C., Lederer D., Sznajer Y., Duerinckx S., Mary S., Macaya A., Cazurro-Gutierrez A., Perez-Duenas B., Munell F., Jarava C. F., Maso L. B., Marce-Grau A., Colobran R., Hackman P., Udd B., Hemelsoet D., Dermaut B., Schuermans N., Poppe B., Verdin H., Osorio A. N., Depienne C., Roos A., Cordts I., Deschauer M., Striano P., Zara F., Riva A., Iacomino M., Uva P., Scala M., Scudieri P., Basak A. N., Claeys K., Boztug K., Haimel M., W. E G., Ruivenkamp C. A. L., Natera de Benito D., Thompson R., Polavarapu K., Grimbacher B., Zaganas I., Kokosali E., Lambros M., Evangeliou A., Spilioti M., Kapaki E., Bourbouli M., Balicza P., Molnar M. J., De la Paz M. P., Sanchez E. B., Delgado B. M., Alonso Garcia de la Rosa F. J., Schrock E., Rump A., Mei D., Vetro A., Balestrini S., Guerrini R., Chinnery P. F., Ratnaike T., Schon K., Maver A., Peterlin B., Munchau A., Lohmann K., Herzog R., Pauly M., May P., Beeson D., Cossins J., Furini S., Afenjar A., Goldenberg A., Masurel A., Phan A., Dieux-Coeslier A., Fargeot A., Guerrot A. -M., Toutain A., Molin A., Sorlin A., Putoux A., Jouret B., Laudier B., Demeer B., Doray B., Bonniaud B., Isidor B., Gilbert-Dussardier B., Leheup B., Reversade B., Paul C., Vincent-Delorme C., Neiva C., Poirsier C., Quelin C., Chiaverini C., Coubes C., Francannet C., Colson C., Desplantes C., Wells C., Goizet C., Sanlaville D., Amram D., Lehalle D., Genevieve D., Gaillard D., Zivi E., Sarrazin E., Steichen E., Schaefer E., Lacaze E., Jacquemin E., Bongers E., Kilic E., Colin E., Giuliano F., Prieur F., Laffargue F., Morice-Picard F., Petit F., Cartault F., Feillet F., Baujat G., Morin G., Diene G., Journel H., Perthus I., Lespinasse J., Alessandri J. -L., Amiel J., Martinovic J., Delanne J., Albuisson J., Lambert L., Perrin L., Ousager L. B., Van Maldergem L., Pinson L., Ruaud L., Samimi M., Bournez M., Bonnet-Dupeyron M. N., Vincent M., Jacquemont M. -L., Cordier-Alex M. -P., Gerard-Blanluet M., Willems M., Spodenkiewicz M., Doco-Fenzy M., Rossi M., Renaud M., Fradin M., Mathieu M., Holder-Espinasse M. H., Houcinat N., Hanna N., Leperrier N., Chassaing N., Philip N., Boute O., Van Kien P. K., Parent P., Bitoun P., Sarda P., Vabres P., Jouk P. -S., Touraine R., El Chehadeh S., Whalen S., Marlin S., Passemard S., Grotto S., Bellanger S. A., Blesson S., Nambot S., Naudion S., Lyonnet S., Odent S., Attie-Bitach T., Busa T., Drouin-Garraud V., Layet V., Bizaoui V., Cusin V., Capri Y., Alembik Y., Unión Europea. Comisión Europea. H2020, Unión Europea. Comisión Europea. 7 Programa Marco, Instituto de Salud Carlos III, Instituto Nacional de Bioinformatica (España), Ministry of Health (República Checa), Ministry of Education, Youth and Sports (República Checa), Denomme-Pichon, A. -S., Bruel, A. -L., Duffourd, Y., Safraou, H., Thauvin-Robinet, C., Tran Mau-Them, F., Philippe, C., Vitobello, A., Jean-Marcais, N., Moutton, S., Thevenon, J., Faivre, L., Matalonga, L., de Boer, E., Gilissen, C., Hoischen, A., Kleefstra, T., Pfundt, R., de Vries, B. B. A., Willemsen, M. H., Vissers, L. E. L. M., Jackson, A., Banka, S., Clayton-Smith, J., Benetti, E., Fallerini, C., Renieri, A., Ciolfi, A., Dallapiccola, B., Pizzi, S., Radio, F. C., Tartaglia, M., Ellwanger, K., Graessner, H., Haack, T. B., Zurek, B., Havlovicova, M., Macek, M., Ryba, L., Schwarz, M., Votypka, P., Lopez-Martin, E., Posada, M., Mencarelli, M. A., Rooryck, C., Trimouille, A., Verloes, A., Abbott, K. M., Kerstjens, M., Martin, E. L., Maystadt, I., Morleo, M., Nigro, V., Pinelli, M., Riess, O., Agathe, J. -M. D. S., Santen, G. W. E., Thauvin, C., Torella, A., Vissers, L., Zguro, K., Boer, E. D., Cohen, E., Danis, D., Gao, F., Horvath, R., Johari, M., Johanson, L., Li, S., Morsy, H., Nelson, I., Paramonov, I., te Paske, I. B. A. W., Robinson, P., Savarese, M., Steyaert, W., Topf, A., van der Velde, J. K., Vandrovcova, J., Ossowski, S., Demidov, G., Sturm, M., Schulze-Hentrich, J. M., Schule, R., Xu, J., Kessler, C., Wayand, M., Synofzik, M., Wilke, C., Traschutz, A., Schols, L., Hengel, H., Lerche, H., Kegele, J., Heutink, P., Brunner, H., Scheffer, H., Hoogerbrugge, N., 't Hoen, P. A. C., Sablauskas, K., de Voer, R. M., Kamsteeg, E. -J., van de Warrenburg, B., van Os, N., Paske, I. T., Janssen, E., Steehouwer, M., Yaldiz, B., Brookes, A. J., Veal, C., Gibson, S., Maddi, V., Mehtarizadeh, M., Riaz, U., Warren, G., Dizjikan, F. Y., Shorter, T., Straub, V., Bettolo, C. M., Manera, J. D., Hambleton, S., Engelhardt, K., Alexander, E., Peyron, C., Pelissier, A., Beltran, S., Gut, I. G., Laurie, S., Piscia, D., Papakonstantinou, A., Bullich, G., Corvo, A., Fernandez-Callejo, M., Hernandez, C., Pico, D., Lochmuller, H., Gumus, G., Bros-Facer, V., Rath, A., Hanauer, M., Lagorce, D., Hongnat, O., Chahdil, M., Lebreton, E., Stevanin, G., Durr, A., Davoine, C. -S., Guillot-Noel, L., Heinzmann, A., Coarelli, G., Bonne, G., Evangelista, T., Allamand, V., Ben Yaou, R., Metay, C., Eymard, B., Atalaia, A., Stojkovic, T., Turnovec, M., Thomasova, D., Kremlikova, R. P., Frankova, V., Liskova, P., Dolezalova, P., Parkinson, H., Keane, T., Freeberg, M., Thomas, C., Spalding, D., Robert, G., Costa, A., Patch, C., Hanna, M., Houlden, H., Reilly, M., Efthymiou, S., Cali, E., Magrinelli, F., Sisodiya, S. M., Rohrer, J., Muntoni, F., Zaharieva, I., Sarkozy, A., Timmerman, V., Baets, J., de Vries, G., De Winter, J., Beijer, D., de Jonghe, P., Van de Vondel, L., De Ridder, W., Weckhuysen, S., Mutarelli, M., Varavallo, A., Banfi, S., Musacchia, F., Piluso, G., Ferlini, A., Selvatici, R., Gualandi, F., Bigoni, S., Rossi, R., Neri, M., Aretz, S., Spier, I., Sommer, A. K., Peters, S., Oliveira, C., Pelaez, J. G., Matos, A. R., Jose, C. S., Ferreira, M., Gullo, I., Fernandes, S., Garrido, L., Ferreira, P., Carneiro, F., Swertz, M. A., Johansson, L., van der Vries, G., Neerincx, P. B., Ruvolo, D., Kerstjens Frederikse, W. S., Zonneveld-Huijssoon, E., Roelofs-Prins, D., van Gijn, M., Kohler, S., Metcalfe, A., Drunat, S., Heron, D., Mignot, C., Keren, B., Lacombe, D., Capella, G., Valle, L., Holinski-Feder, E., Laner, A., Steinke-Lange, V., Cilio, M. -R., Carpancea, E., Depondt, C., Lederer, D., Sznajer, Y., Duerinckx, S., Mary, S., Macaya, A., Cazurro-Gutierrez, A., Perez-Duenas, B., Munell, F., Jarava, C. F., Maso, L. B., Marce-Grau, A., Colobran, R., Hackman, P., Udd, B., Hemelsoet, D., Dermaut, B., Schuermans, N., Poppe, B., Verdin, H., Osorio, A. N., Depienne, C., Roos, A., Cordts, I., Deschauer, M., Striano, P., Zara, F., Riva, A., Iacomino, M., Uva, P., Scala, M., Scudieri, P., Basak, A. N., Claeys, K., Boztug, K., Haimel, M., W. E, G., Ruivenkamp, C. A. L., Natera de Benito, D., Thompson, R., Polavarapu, K., Grimbacher, B., Zaganas, I., Kokosali, E., Lambros, M., Evangeliou, A., Spilioti, M., Kapaki, E., Bourbouli, M., Balicza, P., Molnar, M. J., De la Paz, M. P., Sanchez, E. B., Delgado, B. M., Alonso Garcia de la Rosa, F. J., Schrock, E., Rump, A., Mei, D., Vetro, A., Balestrini, S., Guerrini, R., Chinnery, P. F., Ratnaike, T., Schon, K., Maver, A., Peterlin, B., Munchau, A., Lohmann, K., Herzog, R., Pauly, M., May, P., Beeson, D., Cossins, J., Furini, S., Afenjar, A., Goldenberg, A., Masurel, A., Phan, A., Dieux-Coeslier, A., Fargeot, A., Guerrot, A. -M., Toutain, A., Molin, A., Sorlin, A., Putoux, A., Jouret, B., Laudier, B., Demeer, B., Doray, B., Bonniaud, B., Isidor, B., Gilbert-Dussardier, B., Leheup, B., Reversade, B., Paul, C., Vincent-Delorme, C., Neiva, C., Poirsier, C., Quelin, C., Chiaverini, C., Coubes, C., Francannet, C., Colson, C., Desplantes, C., Wells, C., Goizet, C., Sanlaville, D., Amram, D., Lehalle, D., Genevieve, D., Gaillard, D., Zivi, E., Sarrazin, E., Steichen, E., Schaefer, E., Lacaze, E., Jacquemin, E., Bongers, E., Kilic, E., Colin, E., Giuliano, F., Prieur, F., Laffargue, F., Morice-Picard, F., Petit, F., Cartault, F., Feillet, F., Baujat, G., Morin, G., Diene, G., Journel, H., Perthus, I., Lespinasse, J., Alessandri, J. -L., Amiel, J., Martinovic, J., Delanne, J., Albuisson, J., Lambert, L., Perrin, L., Ousager, L. B., Van Maldergem, L., Pinson, L., Ruaud, L., Samimi, M., Bournez, M., Bonnet-Dupeyron, M. N., Vincent, M., Jacquemont, M. -L., Cordier-Alex, M. -P., Gerard-Blanluet, M., Willems, M., Spodenkiewicz, M., Doco-Fenzy, M., Rossi, M., Renaud, M., Fradin, M., Mathieu, M., Holder-Espinasse, M. H., Houcinat, N., Hanna, N., Leperrier, N., Chassaing, N., Philip, N., Boute, O., Van Kien, P. K., Parent, P., Bitoun, P., Sarda, P., Vabres, P., Jouk, P. -S., Touraine, R., El Chehadeh, S., Whalen, S., Marlin, S., Passemard, S., Grotto, S., Bellanger, S. A., Blesson, S., Nambot, S., Naudion, S., Lyonnet, S., Odent, S., Attie-Bitach, T., Busa, T., Drouin-Garraud, V., Layet, V., Bizaoui, V., Cusin, V., Capri, Y., Alembik, Y., and Luxembourg Centre for Systems Biomedicine (LCSB): Bioinformatics Core (R. Schneider Group) [research center]

Subjects
Exome reanalysis, Neurodevelopmental disorders Donders Center for Medical Neuroscience [Radboudumc 7], Multidisciplinaire, généralités & autres [D99] [Sciences de la santé humaine], Developmental disorder, lnfectious Diseases and Global Health Radboud Institute for Molecular Life Sciences [Radboudumc 4], Biology and Life Sciences, Metabolic Disorders Radboud Institute for Molecular Life Sciences [Radboudumc 6], ClinVar, Rare diseases, All institutes and research themes of the Radboud University Medical Center, Medicine and Health Sciences, Genetics & genetic processes [F10] [Life sciences], Génétique & processus génétiques [F10] [Sciences du vivant], Multidisciplinary, general & others [D99] [Human health sciences], Exome reanalysi, Genetics (clinical)
Abstract

Purpose: Within the Solve-RD project (https://solve-rd.eu/), the European Reference Network for Intellectual disability, TeleHealth, Autism and Congenital Anomalies aimed to investigate whether a reanalysis of exomes from unsolved cases based on ClinVar annotations could establish additional diagnoses. We present the results of the "ClinVar low-hanging fruit" reanalysis, reasons for the failure of previous analyses, and lessons learned. Methods: Data from the first 3576 exomes (1522 probands and 2054 relatives) collected from European Reference Network for Intellectual disability, TeleHealth, Autism and Congenital Anomalies was reanalyzed by the Solve-RD consortium by evaluating for the presence of single-nucleotide variant, and small insertions and deletions already reported as (likely) pathogenic in ClinVar. Variants were filtered according to frequency, genotype, and mode of inheritance and reinterpreted. Results: We identified causal variants in 59 cases (3.9%), 50 of them also raised by other approaches and 9 leading to new diagnoses, highlighting interpretation challenges: variants in genes not known to be involved in human disease at the time of the first analysis, misleading genotypes, or variants undetected by local pipelines (variants in off-target regions, low quality filters, low allelic balance, or high frequency). Conclusion: The "ClinVar low-hanging fruit" analysis represents an effective, fast, and easy approach to recover causal variants from exome sequencing data, herewith contributing to the reduction of the diagnostic deadlock. The Solve-RD project has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement number 779257. Data were analyzed using the RD-Connect Genome-Phenome Analysis Platform, which received funding from the EU projects RD-Connect, Solve-RD, and European Joint Programme on Rare Diseases (grant numbers FP7 305444, H2020 779257, H2020 825575), Instituto de Salud Carlos III (grant numbers PT13/0001/0044, PT17/0009/0019; Instituto Nacional de Bioinformática), and ELIXIR Implementation Studies. The collaborations in this study were facilitated by the European Reference Network for Intellectual disability, TeleHealth, Autism and Congenital Anomalies, one of the 24 European Reference Networks approved by the European Reference Network Board of Member States, cofunded by the European Commission. This project was supported by the Czech Ministry of Health (number 00064203) and by the Czech Ministry of Education, Youth and Sports (number - LM2018132) to M.M. Sí

Published
2023
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2. Overview of the Canadian Clinician Investigator Trainees’ research presented at the 2019 CSCI-CITAC Joint Meeting

Author

Julieta Lazarte, Joel Neves Briard, Tina Binesh Marvasti, Tianwei E Zhou, Jillian A. Macklin, Sophie Hu, Cory Lefebvre, Mylvaganam Sivakami, Elina K. Cook, Christopher S. Balestrini, Mark Trinder, Heather T Whittaker, Adam Pietrobon, Valera Castanov, and Matthaeus A. Ware

Subjects
Canada, Biomedical Research, Universities, Clinician scientist, media_common.quotation_subject, Library science, Career planning, General Medicine, Research Personnel, Child health, Alberta, Presentation, Clinical investigation, Humans, Early career, Child, Psychology, Societies, Medical, Panel discussion, media_common
Abstract

The 2019 Annual General Meeting and Young Investigators’ Forum of the Canadian Society for Clinical Investigation / Société Canadienne de Recherche Clinique (CSCI/SCRC) and Clinician Investigator Trainee Association of Canada / Association des Cliniciens-Chercheurs en Formation du Canada (CITAC/ACCFC) was held in Banff, Alberta on November 8–10th, 2019. The theme was “Positioning Early Career Investigators for Success: Strategy and Resilience”. Lectures and workshops provided knowledge and tools to facilitate the attendees’ development as clinician investigators. Dr. Jason Berman (President of CSCI/SCRC), Elina Cook (President of CITAC/ACCFC) and Drs. Doreen Rabi and Zelma Kiss (University of Calgary Organizing Co-Chairs) gave opening presentations. The keynote speakers were Dr. William Foulkes (McGill University) (Distinguished Scientist Award winner) and Dr. Andrés Finzi (Université de Montréal) (Joe Doupe Young Investigator Award winner). Dr. Robert Bortolussi (Dalhousie University) received the Distinguished Service Award for his work as the Editor-in-Chief of Clinical and Investigative Medicine and for being instrumental in the development of the Canadian Child Health Clinician Scientist Program. This meeting was the first to host a panel discussion with Drs. Stephen Robbins and Marcello Tonelli from the Canadian Institutes of Health Research. Workshops on communication, career planning and work-life balance were hosted by André Picard and Drs. Todd Anderson, Karen Tang, William Ghali, May Lynn Quan, Alicia Polachek and Shannon Ruzycki. The AGM showcased 90 presentations from clinician investigator trainees from across Canada. Most of the abstracts are summarized in this review. Eight outstanding abstracts were selected for oral presentation at the President’s Forum.

Published
2020
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3. Does vascular stiffness predict white matter hyperintensity burden in ischemic heart disease with preserved ejection fraction?

Author

Baraa K. Al-Khazraji, J. Kevin Shoemaker, Christopher S. Balestrini, and Neville Suskin

Subjects
Adult, Male, Middle Cerebral Artery, medicine.medical_specialty, animal structures, Carotid Artery, Common, Physiology, Myocardial Ischemia, Blood Pressure, Disease, 030204 cardiovascular system & hematology, 03 medical and health sciences, Vascular Stiffness, 0302 clinical medicine, Vascular stiffness, Physiology (medical), Internal medicine, medicine.artery, Humans, Medicine, Aged, Ultrasonography, Ejection fraction, business.industry, Stroke Volume, Middle Aged, medicine.disease, Magnetic Resonance Imaging, White Matter, White matter hyperintensity, Middle cerebral artery, Arterial stiffness, Cardiology, Female, Normal blood, Cardiology and Cardiovascular Medicine, business, Ischemic heart, Blood Flow Velocity, 030217 neurology & neurosurgery
Abstract

The survival rate of patients with ischemic heart disease (IHD) is increasing. However, survivors experience increased risk for neurological complications. The mechanisms for this increased risk are unknown. We tested the hypothesis that patients with IHD have greater carotid and cerebrovascular stiffness, and these indexes predict white matter small vessel disease. Fifty participants (age, 40-78 yr), 30 with IHD with preserved ejection fraction and 20 healthy age-matched controls, were studied using ultrasound imaging of the common carotid artery (CCA) and middle cerebral artery (MCA), as well as magnetic resonance imaging (T1, T2-FLAIR), to measure white matter lesion volume (WMLv). Carotid β-stiffness provided the primary measure of peripheral vascular stiffness. Carotid-cerebral pulse wave transit time (ccPWTT) provided a marker of cerebrovascular stiffness. Pulsatility index (PI) and resistive index (RI) of the MCA were calculated as measures of downstream cerebrovascular resistance. When compared with controls, patients with IHD exhibited greater β-stiffness [8.5 ± 3.3 vs. 6.8 ± 2.2 arbitrary units (AU)

Published
2020
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4. Utilidad de otras técnicas de imagen en la valoración de la enfermedad coronaria: Ultrasonido intravascular (IVUS)

Author

Carlos S Balestrini, José Federico Saaibi Solano, Tamara Gorgadze, and Libardo Augusto Medina López

Subjects
03 medical and health sciences, 0302 clinical medicine, RC666-701, Diseases of the circulatory (Cardiovascular) system, 030212 general & internal medicine, 030204 cardiovascular system & hematology, Cardiology and Cardiovascular Medicine
Abstract

Resumen: El ultrasonido intravascular en una herramienta de imagen complementaria a la angiografía coronaria para la evaluación de la enfermedad coronaria, que permite una visualización global de la placa aterosclerótica y tiene una aplicación clínica de suma importancia, pues ayuda a definir qué lesiones ameritan o no intervención cuando la angiografía coronaria por sí sola no es clara. De igual manera, permite optimizar las intervenciones coronarias, incluidas intervenciones en tronco, bifurcaciones y oclusiones crónicas, con el fin de disminuir la subexpansión o la malaposición de los stent y de esta manera minimizar eventos clínicos futuros como la trombosis y la restenosis de los stents. De forma adicional, permite realizar un análisis de la composición histológica de la placa aterosclerótica pudiendo identificar características de riesgo para eventos coronarios relacionados con esta. Abstract: Intravascular ultrasound (IVUS) is a complementary imaging tool to coronary angiography for the evaluation of coronary disease. It provides an overview of the atherosclerotic plaque and has a clinical application of considerable importance, as it helps to define whether or not lesions merit an intervention when coronary angiography on its own is not clear. Similarly, it helps to optimise coronary interventions, including those in the trunk, bifurcations, and chronic occlusions, with aim of decreasing the sub-expansion or poor positioning of the stent, and thus minimises future clinical events like thrombosis and the restenosis of the stents. Additionally, it helps to perform an analysis of the histological composition of the atherosclerotic plaque, on being able to identify risk characteristics for coronary events associated with the plaque. Palabras clave: Angiografía, Enfermedad coronaria, Imagen, Ecografía intravascular, Angioplastia coronaria, Keywords: Angiography, Coronary disease, Image, Intravascular ultrasound, Coronary angioplasty

Published
2019
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5. Autonomic Dysregulation in Adolescent Concussion Is Sex- and Posture-Dependent

Author

Kolten C. Abbott, Christopher S. Balestrini, Lisa Fischer, Stephen A. Klassen, Douglas D. Fraser, Marcy Erin Moir, and Joel Kevin Shoemaker

Subjects
sex differences, Male, medicine.medical_specialty, Mean arterial pressure, adolescent concussion, Supine position, Adolescent, Adolescent concussion, Posture, Poison control, Physical Therapy, Sports Therapy and Rehabilitation, Sitting, 03 medical and health sciences, 0302 clinical medicine, Sex Factors, Heart Rate, Internal medicine, Heart rate, Concussion, Sex differences, medicine, Sport-related concussion, Heart rate variability, Humans, Autonomic nervous system, Orthopedics and Sports Medicine, 030212 general & internal medicine, Child, Brain Concussion, Original Research, business.industry, sport-related concussion, autonomic nervous system, heart rate variability, blood pressure, 030229 sport sciences, medicine.disease, Blood pressure, Case-Control Studies, Cardiology, Female, business
Abstract

Objective: To study autonomic responses to postural changes in concussed adolescents. The influence of sex was also studied. Design: Longitudinal cohort observational study. Participants: Concussed adolescents (CONC; n = 65; 26 male adolescents; age 15 ± 1 years, range = 12-18 years) and a control (CTRL) group of nonconcussed adolescents of similar age and sport (CTRL; n = 54; 29 male adolescents; age 14 ± 1 years, range = 12-18 years). Interventions: Concussed participants were monitored through 6 weekly visits throughout usual physician care. Control participants underwent 2 visits separated by at least 1 week to account for intrapersonal variation in testing measures. Main Outcome Measures: Heart rate variability as the root mean square of successive differences in R–R intervals (RMSSD), heart rate (HR), and blood pressure [mean arterial pressure (MAP) and diastolic blood pressure (DBP)] were measured in supine, sitting, and standing postures. Results: A mixed analysis of variance revealed a group × sex × posture interaction (P = 0.04) where seated values of RMSSD were less in concussed female participants versus control female participants (42 ± 4 vs 61 ± 7 ms; P = 0.01; Mann–Whitney rank test). Compared with CTRL, CONC exhibited increased pretesting seated DBP (69 ± 1 vs 74 ± 1 mm Hg; P < 0.01), MAP (83 ± 1 vs 86 ± 1 mm Hg; P = 0.02), and baseline seated HR (72 ± 1 vs 77 ± 2 bpm; P = 0.03). Values of DBP (P = 0.03) and MAP (P < 0.01) improved at clinical discharge, whereas the RMSSD in female participants did not (P > 0.5). Data are mean ± SEM. Conclusions: A modest reduction in female cardiac autonomic regulation was observed during seated postures. Alterations in seated concussed DBP and MAP, but not RMSSD, resolved at clinical discharge (median = 37 days). The results indicate that, in adolescents, concussion may impair cardiovagal function in a sex- and posture-dependent manner. The findings also suggest that BP metrics, but not RMSSD, are associated with clinical concussion recovery.

Published
2021

7. Concussion Symptoms Predictive of Adolescent Sport-Related Concussion Injury

Author

Lisa Fischer, David Humphreys, Mark Daley, Christopher S. Balestrini, Marci Erin Moir, Emilie Woehrle, Kolten C. Abbott, Alexandra Harriss, Douglas D. Fraser, and Joel Kevin Shoemaker

Subjects
Male, medicine.medical_specialty, Adolescent, media_common.quotation_subject, Post-concussion symptom scale, Poison control, Physical Therapy, Sports Therapy and Rehabilitation, Anxiety, Irritability, 03 medical and health sciences, 0302 clinical medicine, Predictive Value of Tests, Sleep Initiation and Maintenance Disorders, Outcome Assessment, Health Care, Sadness, Concussion, Injury prevention, medicine, Medicine and Health Sciences, Psychology, Humans, Orthopedics and Sports Medicine, Affective Symptoms, 030212 general & internal medicine, Child, Retrospective Studies, media_common, Post-Concussion Syndrome, business.industry, Decision Trees, Youth Sports, Neurosciences, Retrospective cohort study, 030229 sport sciences, Rivermead post-concussion symptoms questionnaire, medicine.disease, Concussion symptoms, Irritable Mood, Predictive value of tests, Athletic Injuries, Physical therapy, Female, Self Report, Symptom Assessment, medicine.symptom, business
Abstract

Objective To assess the predictive capability of the postconcussion symptom scale (PCSS) of the sport concussion assessment tool (SCAT) III to differentiate concussed and nonconcussed adolescents. Design Retrospective. Setting Tertiary. Participants Sixty-nine concussed (15.2 ± 1.6 years old) and 55 control (14.4 ± 1.7 years old) adolescents. Independent variables Postconcussion symptom scale. Main outcome measure Two-proportion z-test determined differences in symptom endorsement between groups. To assess the predictive power of the PCSS, we trained an ensemble classifier composed of a forest of 1000 decision trees to classify subjects as concussed, or not concussed, based on PCSS responses. The initial classifier was trained on all 22-concussion symptoms addressed in the PCSS, whereas the second classifier removed concussion symptoms that were not statistically significant between groups. Results Concussion symptoms common between groups were trouble falling asleep, more emotional, irritability, sadness, and anxious. After removal, analysis of the second classifier indicated that the 5 leading feature rankings of symptoms were headache, head pressure, light sensitivity, noise sensitivity, and "don't feel right," which accounted for 52% of the variance between groups. Conclusions Collectively, self-reported symptoms through the PCSS can differentiate concussed and nonconcussed adolescents. However, predictability for adolescent patients may be improved by removing emotional and sleep domain symptoms.

Published
2020

8. Physician-Scientist trainees: A 'call to action' to confront future career challenges

Author

Christopher S. Balestrini

Subjects
Canada, Biomedical Research, 020208 electrical & electronic engineering, Perspective (graphical), Translational research, 02 engineering and technology, General Medicine, Future career, Medical research, 01 natural sciences, Call to action, 010309 optics, Physicians, 0103 physical sciences, 0202 electrical engineering, electronic engineering, information engineering, Humans, Engineering ethics, Sociology, Students, PATH (variable)
Abstract

Throughout their careers, physician-scientists must adapt to the dynamic landscape of the medical research environment. As such, current physicianscientist trainees must overcome unique obstacles on the path to productive research careers. In the paper by Levit et al. in this month’s Clinical and Investigative Medicine issue, Canadian research leaders describe the challenges and opportunities for the next generation of physician-scientists [1]. They paint a cautiously optimistic picture. The current article is an outlook and concurrent “call to action” for how ongoing physician-scientist concerns can be conquered from the perspective of a current Canadian MD-PhD student.

Published
2020

9. Commentaries on Viewpoint: Physiology and fast marathons

Author

Andrew N. Bosch, José Manuel González-Yáñez, Wouter Hoogkamer, Daniel Boullosa, João Paulo Vilas-Boas, Ricardo J. Fernandes, Mikaela C. Gabler, Beat Knechtle, Robert F. Chapman, Daniel H. Craighead, Richard C. Blagrove, Jonathon W. Senefeld, Grégoire P. Millet, Anton Ušaj, Shane A. Bielko, Stephen J. Ives, Dieter Böning, Rodrigo Ramirez-Campillo, Daniel Muniz-Pumares, Billy Sperlich, Margaret A. Leist, Rasmus Kopp Hansen, Rodrigo Del Rio, Borja Muniz-Pardos, Fergus M. Guppy, Laura Hottenrott, Pedro L. Valenzuela, Peter G. Weyand, Kuno Hottenrott, Arthur H. Dewolf, Juan Del Coso, Paul J. Stapley, Jeferson Macedo Vianna, David C. Andrade, Stefanos Volianitis, Flávio de Oliveira Pires, Thiago Ribeiro Lopes, Hunter L. Paris, Alicia S. Oumsang, Konstantinos Angeloudis, Jordan Santos-Concejero, Ana Lilia Rayas-Gómez, Felix Proessl, Julien Louis, Hans-Christer Holmberg, Cayque Brietzke, Pantelis Theo Nikolaidis, Shalaya Kipp, Erin C. Sinai, Stéphane Perrey, Yuri de Almeida Costa Campos, Tadej Debevec, Brandon A. Yates, William Malysa, Philip R. Hayes, Tony Meireles dos Santos, Alain Riveros-Rivera, Curtis S. Goss, Shaun Sutehall, Christoph Zinner, José Manuel González-Rayas, Paulo Henrique Silva Marques de Azevedo, Ben Hunter, Bastien Bontemps, Fernando González-Mohíno, Thomas Gronwald, Christopher S. Balestrini, Albaro Escalera, Paulo Estevão Franco-Alvarenga, Rodger Kram, Sandro Fernandes da Silva, Mast T. Lige, Gwenael Layec, José María González-Ravé, Miller P. Guimarães, Bruno M. Silva, Niels H. Secher, Lindsay Bottoms, Romuald Lepers, Davide Malatesta, and Yannis P. Pitsiladis

Subjects
Cognitive science, FISIOLOGIA DO EXERCÍCIO, Physiology, Physiology (medical), Psychology, Running
Published
2020
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10. An Investigation of Dynamic Cerebral Autoregulation in Adolescent Concussion

Author

J. Kevin Shoemaker, Douglas D. Fraser, Lisa Fischer, Christopher S. Balestrini, Kolten C. Abbott, Stephen A. Klassen, and M. Erin Moir

Subjects
Male, Middle Cerebral Artery, medicine.medical_specialty, Adolescent, Brachial Artery, medicine.medical_treatment, Blood Pressure, Physical Therapy, Sports Therapy and Rehabilitation, Anxiety, 030204 cardiovascular system & hematology, Pediatrics, Cerebral autoregulation, Electrocardiography, 03 medical and health sciences, 0302 clinical medicine, Respiratory Rate, Initial visit, Internal medicine, Concussion, Homeostasis, Humans, Medicine, Orthopedics and Sports Medicine, Cardiac Output, Brain Concussion, Rehabilitation, Vasomotor, business.industry, Hemodynamics, Stroke Volume, Ultrasonography, Doppler, medicine.disease, Blood pressure, Cerebral blood flow, Cerebrovascular Circulation, Athletic Injuries, Cardiology, Brachial artery Blood pressure, Female, business, Blood Flow Velocity, 030217 neurology & neurosurgery
Abstract

Purpose Although cerebrovascular impairments are believed to contribute to concussion symptoms, little information exists regarding brain vasomotor control in adolescent concussion, particularly autoregulatory control that forms a fundamental response mechanism during changes in blood pressure. This research tested the hypothesis that adolescent concussion is marked by impaired dynamic cerebral autoregulation. Methods Nineteen concussed adolescents (15 ± 2 yr, 13 females) and 18 healthy controls (15 ± 2 yr, 9 females) completed two sit-to-stand trials. Brachial artery blood pressure and cerebral blood flow velocity in the right middle cerebral artery were measured continuously. Dynamic rate of regulation was calculated as the rate of change in cerebrovascular resistance relative to the change in arterial blood pressure. The concussed adolescents were followed through their rehabilitation for up to 12 wk. Results At the first visit, the concussed adolescents demonstrated reduced rate of regulation compared with the healthy controls (0.12 ± 0.04 vs 0.19 ± 0.06 s, P ≤ 0.001). At the concussed adolescents final visit, after symptom resolution, the rate of regulation improved to levels that were not different from the healthy controls (n = 9; 0.15 ± 0.08 vs 0.19 ± 0.06 s, P= 0.06). Two distinct groups were observed at the final visit with some individuals experiencing recovery of dynamic cerebral autoregulation and others showing no marked change from the initial visit. Conclusion Adolescents demonstrate an impairment in dynamic cerebral autoregulation after concussion that improves along with clinical symptoms in some individuals and remains impaired in others despite symptom resolution.

Published
2018
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11. Evaluation of a 3D-Printed-Head Simulation Technique for Teaching Flexible Nasopharyngoscopy to Radiation Oncology Residents

Author

Santiago Cobos, Madeleine E. Norris, Paige Eansor, David A. Palma, Anthony C. Nichols, Leah A. D'Souza, Donna H. Murrell, Katherine E. Willmore, Manas Sharma, Justin D. Pautler, Christopher D. Goodman, Andrew Warner, Christopher S. Balestrini, and Jasbir Jaswal

Subjects
Models, Anatomic, medicine.medical_specialty, Cancer Research, Wilcoxon signed-rank test, media_common.quotation_subject, Teaching method, Fidelity, Nasopharyngoscopy, Nose, Article, 030218 nuclear medicine & medical imaging, 03 medical and health sciences, 0302 clinical medicine, Radiation oncology, Medicine and Health Sciences, Medicine, Humans, Medical physics, Radiology, Nuclear Medicine and imaging, Head and neck, Simulation Training, media_common, Radiation, business.industry, Internship and Residency, Rubric, Endoscopy, Test (assessment), Oncology, 030220 oncology & carcinogenesis, Printing, Three-Dimensional, Radiation Oncology, Pharynx, business, Head
Abstract

© 2020 Elsevier Inc. Purpose: Simulation-based medical education is an effective tool for medical teaching, but simulation-based medical education deployment in radiation oncology (RO) is limited. Flexible nasopharyngoscopy (FNP), an essential skill for RO residents, requires practice that typically occurs on volunteer patients, introducing the potential for stress and discomfort. We sought to develop a high-fidelity simulator and intervention that provides RO residents the opportunity to develop FNP skills in a low-pressure environment. Methods and Materials: Computed tomography images were used to create an anatomically accurate 3-dimensional–printed model of the head and neck region. An intervention incorporating didactic instruction, multimedia content, and FNP practice on the model was designed and administered to RO residents attending the Anatomy and Radiology Contouring Bootcamp. Participants completed pre- and postintervention evaluations of the training session and model fidelity, and self-assessments of FNP skill and confidence performing FNP. Participants were video recorded performing FNP pre- and postintervention. Videos were scored by a blinded observer on a predefined rubric. Changes in scores were evaluated using the Wilcoxon signed-rank test. Results: Twenty-four participants from 17 institutions and 4 countries completed the intervention, 50% were women, and most were senior residents. Postintervention, FNP confidence and FNP performance improved significantly (mean ± standard deviation on a 10-point scale: 1.8 ± 1.8, P < .001; 2.2 ± 2.0, P < .001, respectively). Participants felt the model was helpful (mean ± standard deviation on a 5-point scale: 4.2 ± 0.6), anatomically correct (4.1 ± 0.9), and aided in spatial comprehension (4.3 ± 0.8). Overall satisfaction for the intervention was high (4.3 ± 0.8). Participants strongly agreed the intervention should be integrated into RO training programs (4.3 ± 0.8). Conclusions: A 3-dimensional–printed model and associated intervention were effective at improving FNP performance and the teaching method was rated highly by participants. RO residents may benefit from broader dissemination of this technique to improve trainee performance.

Published
2020
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12. 43: Evaluation of a 3d-Printed-Head Simulation Technique for Teaching Flexible Nasopharyngoscopy to Radiation Oncology Residents

Author

Katherine E. Willmore, David A. Palma, Santiago Cobos, Andrew Warner, Justin D. Pautler, Jasbir Jaswal, Madeleine E. Norris, Christopher Goodman, Leah D’Souza, Paige Eansor, Anthony C. Nichols, Christopher S. Balestrini, Donna H. Murrell, and Manas Sharma

Subjects
3d printed, medicine.medical_specialty, Oncology, business.industry, Radiation oncology, Head (vessel), Medicine, Radiology, Nuclear Medicine and imaging, Medical physics, Hematology, Nasopharyngoscopy, business
Published
2020
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13. Concussion in Adolescents Impairs Heart Rate Response to Brief Handgrip Exercise

Author

Emilie Woehrle, J. K. Shoemaker, Douglas D. Fraser, Marcy Erin Moir, Kolten Abbott, Christopher S. Balestrini, Alexandra Harriss, and Lisa Fischer

Subjects
Male, medicine.medical_specialty, Time Factors, Adolescent, Hemodynamics, Physical Therapy, Sports Therapy and Rehabilitation, Isometric exercise, 030204 cardiovascular system & hematology, Autonomic Nervous System, 03 medical and health sciences, 0302 clinical medicine, Heart Rate, Isometric Contraction, Internal medicine, Heart rate, Concussion, Medicine and Health Sciences, medicine, Humans, Handgrip exercise, Orthopedics and Sports Medicine, Brain Concussion, Heart rate response, Analysis of Variance, Hand Strength, business.industry, medicine.disease, Case-Control Studies, Cardiology, Female, Observational study, Analysis of variance, business, 030217 neurology & neurosurgery, Preliminary Data
Abstract

OBJECTIVE: Test the hypotheses that (1) concussion in adolescents impairs autonomic neural control of heart rate (HR), and (2) HR reactivity improves with symptom resolution. DESIGN: Observational, case-control. PARTICIPANTS: Nineteen concussed adolescents (8 female adolescents; age 15 ± 2 years) and 16 healthy controls (6 female adolescents, age 15 ± 2 years). INTERVENTION: All participants performed an isometric handgrip (IHG) at 30% maximum voluntary contraction lasting 30 seconds. Heart rate (electrocardiogram) and hemodynamic responses (photoplethysmographic Finometer) were recorded from 30 seconds of baseline and the last 10 seconds of handgrip. MAIN OUTCOME MEASURES: The HR response (ΔHR) at the onset of moderate-intensity IHG using a mixed 1-way analysis of variance. RESULTS: A group × time interaction (P < 0.005) indicated that handgrip evoked a greater ΔHR among control participants (13 ± 10 beats/min) compared with concussed (6.4 ± 6.3 beats/min; group P = 0.63; time P < 0.001; d = 0.77). CONCLUSION: These preliminary results suggest that a concussion impairs the ability to elevate HR at the exercise onset and, given the nature of the task, this could be interpreted to reflect reduced ability to withdraw cardiovagal control. Therefore, the data support the hypothesis of neural cardiac dysregulation in adolescents diagnosed with concussion. CLINICAL RELEVANCE: The IHG test could aid concussion diagnosis and support return-to-play decisions.

Published
2018
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14. Cerebrovascular compliance within the rigid confines of the skull

Author

Mair Zamir, M. Erin Moir, Stephen A. Klassen, Christopher S. Balestrini, and J. Kevin Shoemaker

Subjects
medicine.medical_specialty, Cerebrovascular compliance, Physiology, Intracranial pressure, cerebral blood flow, Intracranial compliance, intracranial pressure, Pulsatile flow, cerebrovascular compliance, lcsh:Physiology, 03 medical and health sciences, Cerebral circulation, pulsatile blood flow, 0302 clinical medicine, 030202 anesthesiology, Physiology (medical), Internal medicine, medicine, Medicine and Health Sciences, Pulsatile blood flow, Original Research, lcsh:QP1-981, business.industry, intracranial compliance, Cerebral blood flow, Compliance (physiology), Skull, medicine.anatomical_structure, Cardiology, business, 030217 neurology & neurosurgery
Abstract

© 2018 Zamir, Moir, Klassen, Balestrini and Shoemaker. Pulsatile blood flow is generally mediated by the compliance of blood vessels whereby they distend locally and momentarily to accommodate the passage of the pressure wave. This freedom of the blood vessels to exercise their compliance may be suppressed within the confines of the rigid skull. The effect of this on the mechanics of pulsatile blood flow within the cerebral circulation is not known, and the situation is compounded by experimental access difficulties. We present an approach which we have developed to overcome these difficulties in a study of the mechanics of pulsatile cerebral blood flow. The main finding is that while the innate compliance of cerebral vessels is indeed suppressed within the confines of the skull, this is compensated somewhat by compliance provided by other "extravascular" elements within the skull. The net result is what we have termed "intracranial compliance," which we argue is more pertinent to the mechanics of pulsatile cerebral blood flow than is intracranial pressure.

Published
2018

15. Carotid Arterial Stiffness Predicts White Matter Lesion Volume in Older Adults

Author

Neville Suskin, J. Kevin Shoemaker, Baraa K. Al-Khazraji, Navena R. Lingum, Christopher S. Balestrini, and Jennifer L. Vording

Subjects
medicine.medical_specialty, business.industry, White matter lesion, medicine.disease, Biochemistry, Volume (thermodynamics), Internal medicine, Genetics, Cardiology, medicine, Arterial stiffness, business, Molecular Biology, Biotechnology
Published
2018
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16. Cerebrovascular Compliance is Affected by Posture

Author

Mair Zamir, J. Kevin Shoemaker, Christopher S. Balestrini, Stephen A. Klassen, and M. Erin Moir

Subjects
Compliance (physiology), medicine.medical_specialty, Physical medicine and rehabilitation, business.industry, Genetics, Medicine, business, Molecular Biology, Biochemistry, Biotechnology
Published
2018
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17. Impaired Dynamic Cerebral Autoregulation to Postural Stress Following Concussive Injuries in Adolescents

Author

Moir, M. Erin, Abbott, Kolten C., Balestrini, Christopher S., Fischer, Lisa K., Fraser, Douglas D., and Shoemaker, J. Kevin

Subjects
Pediatrics
Abstract

Concussions disproportionately affect adolescents and ongoing maturation places this population at increased risk for prolonged recovery and long-term impairments in neurologic functioning. Although cerebrovascular impairments are believed to contribute to concussion symptoms and recovery, little information exists regarding brain vasomotor control in adolescent concussion, particularly during rapid changes in blood pressure that demand a dynamic cerebral autoregulatory response. The current investigation tested the hypothesis that adolescent concussion is marked by impaired dynamic cerebral autoregulation (CA). Twenty-two adolescents diagnosed with a concussion (CONC; 13 females; 15 ± 1 years; 26 ± 20 days post-injury, SCAT3 symptom score = 12 ± 6) and twenty-seven healthy controls (CTRL; 15 females; 14 ± 2 years; SCAT3 symptom score = 6 ± 4) completed two repeated sit-to-stand trials. CONC were followed through their rehabilitation for up to 12-weeks. Arterial blood pressure (ABP), cerebral blood flow velocity (CBFV), end-tidal carbon dioxide partial pressure (PetCO2), and heart rate (HR) were measured continuously with finger photoplethysmography (Finapres Medical Systems BV), transcranial Doppler ultrasound (Multigon Industries), a gas analyzer (AD Instruments), and a standard 3-lead electrocardiogram (ECG), respectively. Furthermore, cardiac output (CO) was provided via the Model flow algorithm and cerebrovascular resistance (CVR) was calculated. The rate of the drop in CVR relative to the change in ABP provided the rate of regulation (RoR). The drop in ABP with standing was similar between CONC and CTRL (25 ± 8 vs. 24 ± 7 mmHg; p = 0.62) although the time to ABP nadir was longer in CONC compared with CTRL (7.2 ± 1.1 vs. 6.1 ± 1.3 sec; p = 0.002). Similarly, time to CBFV nadir was longer in CONC compared with CTRL (5.9 ± 1.4 vs. 4.4 ± 2.0 sec; p = 0.003). Compared to CTRL, RoR was reduced in CONC at study entry (0.21 ± 0.06 vs. 0.16 ± 0.04 sec−1; p = 0.005). However, at the time of CONC final visit (SCAT3 symptom score = 4 ± 5), RoR improved to levels similar to CTRL (0.20 ± 0.08 vs. 0.21 ± 0.06 sec−1; p = 0.55). During sitting and standing, CONC and CTRL had similar PetCO2. The change in heart rate with standing was similar between CONC and CTRL (30 ± 6 vs. 26 ± 9 bpm; p = 0.09) although the time to peak HR was longer in CONC compared with CTRL (10.8 ± 2.5 vs. 9.4 ± 2.0 sec; p = 0.004). Furthermore, a similar increase in CO was witnessed with standing in CONC and CTRL (1.4 ± 1.6 vs. 1.7 ± 0.7 L/min; p = 0.28). Impairments in dynamic CA are evident in adolescents following a concussive injury which recover in accordance with clinical symptoms. Therefore, RoR may aid decisions regarding diagnosis, rehabilitation, and recovery of adolescent concussion.

Published
2017

18. Autonomic Dysregulation in Adolescent Concussion: Characterization and Temporal Resolution of Neurological Outcomes

Author

Balestrini, Christopher S., Moir, M. Erin, Abbott, Kolten C., Johnson, Marjorie, Fischer, Lisa K., Fraser, Douglas D., and Shoemaker, J. Kevin

Subjects
Pediatrics
Abstract

Although incidence is at epidemic levels, objective indicators of neurologic damage in adolescent concussion remain poorly described. Autonomic markers such as heart rate variability (HRV) have provided equivocal results; however, these predominantly are made under conditions of minimal physiologic stress. The current investigation employs postural stressors to examine underlying neurological outcomes associated with acute concussion and clinical recovery to test the hypothesis that concussion impairs dynamic autonomic adjustments in adolescents. We examined concussed adolescents (CONC; n = 35; 14 males; age 15 ± 1 yrs, range = 12–18 yrs) for up to 6 weekly visits from diagnosis. A group of age and activity level-matched non-concussed adolescents (CTRL; n = 35; 19 males; age 14 ± 2 yrs, range = 12–18 yrs) formed the reference control. HRV (root mean square of successive differences in R-R intervals (RMSSD)) and heart rate were assessed during a sit-to-stand protocol (two trials of seated posture (three minutes), followed by two minutes of standing). Measurements were taken during the last minute of sitting and standing, the ten second period following the postural stress of standing, as well as the ten second period from maximum HR. While seated, RMSSD was lower in CONC (41 ± 24 msec) compared with CTRL (60 ± 40 msec; p < 0.05). 31 patients provided weekly data until clinical discharge. Compared with the first visit (43 ± 25 msec), seated RMSSD in CONC increased (51 ± 36 msec; p = 0.05) at the time of clinical discharge. Upon standing (10 seconds following postural change to standing), RMSSD was lower in CONC versus CTRL (13 ± 7 vs. 18 ± 12 msec; p < 0.05). Compared with the first visit, RMSSD following the induced postural stress did not improve in CONC over the six week recovery period. Following maximal HR, CTRL had increased RMSSD versus CONC (46 ± 30 vs. 34 ± 19 msec; p < 0.05). Compared with CTRL, seated HR was higher in CONC. This tachycardia effect persisted throughout the sit-to-stand protocol (78 ± 12 vs. 72 ± 12 bpm; p < 0.05) and was maintained until the time of clinical discharge (79 ± 13 vs. 72 ± 12 bpm; p < 0.05). In adolescent concussion, autonomic cardiac impairment is demonstrated by reduced RMSSD in the seated position and throughout the adjustment period in response to postural stress. Further, seated HR is increased following acute concussion and remains elevated by the time of clinical discharge. Seated HRV, but not HR, recovered to levels seen in the control population within three to six weeks. Thus, cardiac adjustments to modest postural stress may represent a measurable neurological impairment in adolescent acute concussion which can be objectively monitored throughout clinical recovery.

Published
2017

19. Retinal nerve fibre layer thinning is associated with drug resistance in epilepsy

Author

Balestrini, S., Clayton, L. M. S., Bartmann, A. P., Chinthapalli, K., Novy, J., Coppola, A., Wandschneider, B., Stern, W. M., Acheson, J., Bell, G. S., Sander, J. W., Sisodiya, S. M., Balestrini, S., Clayton, L. M. S., Bartmann, A. P., Chinthapalli, K., Novy, J., Coppola, A., Wandschneider, B., Stern, W. M., Acheson, J., Bell, G. S., Sander, J. W., and Sisodiya, S. M.

Published
2016

20. Aorto-right atrial fistula secondary to rupture of an occluded old saphenous venous graft to right coronary artery

Author

José F Saaibi, Carlos S Balestrini, and Santiago Navas Ortiz

Subjects
medicine.medical_specialty, business.industry, Fistula, medicine.medical_treatment, General Medicine, medicine.disease, Right atrial, Surgery, Shunt (medical), Coronary artery bypass surgery, Parasternal line, Internal medicine, Heart failure, Right coronary artery, medicine.artery, cardiovascular system, medicine, Cardiology, Radiology, Nuclear Medicine and imaging, Cardiology and Cardiovascular Medicine, business, Cardiac catheterization
Abstract

We report a case of an acquired aorta–right atrial fistula, secondary to a ruptured proximal anastomosis of an old saphenous vein graft 12 years after a coronary artery bypass surgery, in a 57 year old patient with multiple cardiovascular risk factors. On admission, he presented with congestive heart failure and on examination a continuous murmur was detected on the right parasternal border. Catheterization showed a fistula from the proximal anastomosis of an occluded right coronary artery saphenous vein graft draining to the right atrium with a large left to right shunt. The fistula was successfully occluded by a percutaneous approach with a Life Tech duct occluder with complete resolution of heart failure. The patient was discharged one week afterwards. After a two-year follow-up, the fistula remained occluded. © 2013 Wiley Periodicals, Inc.

Published
2014
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21. Audit of use of stiripentol in adults with Dravet syndrome

Author

S, Balestrini and S M, Sisodiya

Subjects
Adult, Male, Adolescent, Dioxolanes, Epilepsies, Myoclonic, Original Articles, stiripentol, NAV1.1 Voltage-Gated Sodium Channel, Child, Preschool, Mutation, Humans, epilepsy, Anticonvulsants, Female, Original Article, antiepileptic drugs, Child, seizures
Abstract

Objectives There are very few data available in the literature on the use of stiripentol in adults with Dravet syndrome (DS). DS cases are increasingly recognized in adulthood, and more children with DS now survive to adulthood. The aim of the study was to document the effectiveness and tolerability of stiripentol in adults with DS. Material and methods We conducted an observational clinical audit in the epilepsy service of the National Hospital for Neurology and Neurosurgery, London (UK). Results We included 13 adult subjects with DS (eight females, five males). The responder (defined as more than 50% reduction in all seizure types) rate was 3/13 (23%) at 36 months. The following other outcomes were reported: seizure exacerbation (3/13, 23%), no change (3/13, 23%), less than 50% reduction in seizures (2/13, 15%), more than 50% reduction in generalized tonic‐clonic seizures but no other seizure types (1/13, 8%), undefined response (1/13, 8%). The retention rate was 62% after 1 year and 31% after 5 years. Adverse effects were reported in 7/13 (54%): the most frequent were anorexia, weight loss, unsteadiness and tiredness. Withdrawal due to adverse effects occurred in 3/13 (23%). Conclusions Compared with previous studies on children with DS, our results show a lower responder rate and a similar tolerability profile. Stiripentol can be effective with a good tolerability profile. Our audit is small, but supports the use of stiripentol in adults with DS when first‐line treatments are ineffective or not tolerated, in keeping with published guidelines.

Published
2016

22. Independent yields of Rb and Cs isotopes from thermal-neutron induced fission ofU235

Author

E. Koglin, G. Jung, K. D. Wünsch, G. Siegert, S. J. Balestrini, Hermann Wollnik, and R. Decker

Subjects
Nuclear reaction, Physics, Nuclear and High Energy Physics, Fission products, Ion beam, Fission, Analytical chemistry, Fission product yield, Neutron radiation, Neutron temperature, Nuclear physics, Physics::Atomic and Molecular Clusters, Neutron, Nuclear Experiment
Abstract

The relative yields of Rb and Cs isotopes from thermal-neutron fission of /sup 235/U have been redetermined using the mass separator OSTIS, on-line at a neutron guide of the High-Flux Beam Reactor at the Institut Laue-Langevin, Grenoble, France. The separator ion source was a hot oven containing /sup 235/U in a graphite matrix. The neutron beam was pulsed. Alkali fission products diffused out of the graphite and were ionized, thus producing a stepwise increase in the analyzed ion beam proportional to the independent fission yield. The ion beam and the fissions in the source were monitored simultaneously. The diffusion of Rb and Cs from the source was exponential in time with half-lives ranging from 2.8 to 18 sec, depending upon the element and source temperature. The independent fission yields of Rb and Cs are normalized by equating their element yields to each other and to a value computed from the charge distributions observed with the recoil separator LOHENGRIN and well established mass yields. Fractional independent yields are deduced from the independent fission yields, and these compare very well with the EOZ model described by Wahl.

Published
1979
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27. Cardiac Phenotype In ATP1A3 Related-Syndromes: A Multicentre Study

Author

Balestrini, S., Mikati, M., Garcia-Roves, R. Alvarez, Carboni, M., Hunanyan, A., Kherallah, B., Mclean, M., Prange, L., Grandis, E., Gagliardi, A., Pisciotta, L., Stagnaro, M., Veneselli, E., Campistol, J., Fons, C., Brashear, A., Miller, C., Samoes, R., Brankovic, V., Padiath, Q., Potic, A., Pilch, J., Vezyroglou, K., Hollingsworth, G., Scheffer, I., Granata, T., Nardo NARDOCCI, Ragona, F., Arzimanoglou, A., Panagiotakaki, E., Carrilho, I., Zucca, C., Novy, J., Dziezyc, K., Parowicz, M., Mazurkiewicz-Beldzinska, M., Weckhuysen, S., Pons, R., Groppa, S., Sinden, D. S., Pitt, G., Tinker, A., Ashworth, M., Michalak, Z., Thom, M., Cross, J. H., Vavassori, R., Kaski, J. P., and Sisodiya, S. M.

28. Increased common carotid artery wall thickness is associated with rapid progression of asymptomatic carotid stenosis

Author

MARINA DIOMEDI, Scacciatelli D, Misaggi G, Balestrini S, Balucani C, Sallustio F, Di Legge S, Stanzione P, and Silvestrini M

Subjects
Male, Echo-Doppler, Carotid Artery, Common, carotid intima-media thickness, Reproducibility of Results, Sensitivity and Specificity, Carotid stenosis progression, Italy, Risk factors, Disease Progression, Prevalence, Humans, Carotid Stenosis, Female, Settore MED/26 - Neurologia, Aged
Abstract

This study aimed to identify clinical and ultrasound imaging predictors of progression of carotid luminal narrowing in subjects with asymptomatic moderate internal carotid artery (ICA) stenosis.A total of 571 subjects with asymptomatic moderate (50-69%) ICA stenoses were enrolled. They underwent ultrasound examination at baseline and after 12 months. Demographics, vascular risk factors, medications, plaque characteristics (surface and echogenicity) and common carotid intima-media thickness (IMT) were collected. At the follow-up examination, any change of ICA stenosis was graded in three categories (i) ≥70% to near occlusion, (ii) near occlusion, and (iii) occlusion. Progression of stenosis was defined as an increase in the stenosis degree by at least one category from baseline to follow-up.At 12 months, progression occurred in 142 subjects (prevalence rate 25%). At the multivariable logistic model, pathological IMT values (considered as binary variable: normal: ≤1 mm vs. pathologic:1 mm) significantly predicted the risk for plaque progression after adjusting the model for possible confounders (OR 2.28, 95% CI 1.18-4.43, P = .014, multivariable logistic model).Our results confirm the role of carotid wall thickening as a marker of atherosclerosis. Carotid IMT measurement should be considered to implement risk stratification in patients with asymptomatic carotid disease.

29. Postictal Psychosis in Epilepsy: A Clinicogenetic Study

Author

Simona Balestrini, Yvonne G. Weber, Antonio Gambardella, Michael G Doyle, Genevieve Rayner, Vera Braatz, Sanjay M. Sisodiya, Norman Delanty, Stella Calafato, Helena Martins Custodio, J Foong, Francesca Bisulli, Samuel F. Berkovic, Luigi Agrò, Christian Hengsbach, Elvira Bramon, Baihan Wang, Gianpiero L. Cavalleri, Costin Leu, Ingrid E. Scheffer, Braatz V., Martins Custodio H., Leu C., Agro L., Wang B., Calafato S., Rayner G., Doyle M.G., Hengsbach C., Bisulli F., Weber Y.G., Gambardella A., Delanty N., Cavalleri G., Foong J., Scheffer I.E., Berkovic S.F., Bramon E., Balestrini S., and Sisodiya S.M.

Subjects
Adult, Male, medicine.medical_specialty, Psychosis, Psychotic Disorder, Polymorphism, Single Nucleotide, Cohort Studies, Epilepsy, Psychiatric history, Internal medicine, medicine, Humans, Family history, Retrospective Studies, Psychiatric assessment, Electroencephalography, Odds ratio, Middle Aged, medicine.disease, Psychotic Disorders, Neurology, Schizophrenia, Case-Control Studies, Female, Neurology (clinical), Cohort Studie, Case-Control Studie, Human, Cohort study
Abstract

Annals of neurology 90(3), 464-476 (2021). doi:10.1002/ana.26174, Published by Wiley-Blackwell, Hoboken, NJ

Published
2021
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30. Real-life survey of pitfalls and successes of precision medicine in genetic epilepsies

Author

Susanne Schubert-Bast, Yvonne G. Weber, Simona Balestrini, Sanjay M. Sisodiya, Cheryl Hemingway, Ingo Borggraefe, Antonietta Coppola, Anna Rosati, Martino Montomoli, Philipp S. Reif, Pasquale Striano, Rikke S. Møller, Felix Rosenow, Katri Silvennoinen, Davide Mei, Serena Troisi, Clinda Puvirajasinghe, Renzo Guerrini, Carla Marini, Antonella Riva, Karl Martin Klein, Holger Lerche, Maria Gogou, Daniela Chiarello, Wendy D Jones, Federico Zara, J. Helen Cross, Balestrini, S, Chiarello, D, Gogou, M, Silvennoinen, K, Puvirajasinghe, C, Jones, Wd, Reif, P, Klein, Km, Rosenow, F, Weber, Yg, Lerche, H, Schubert-Bast, S, Borggraefe, I, Coppola, A, Troisi, S, Møller, R, Riva, A, Striano, P, Zara, F, Hemingway, C, Marini, C, Rosati, A, Mei, D, Montomoli, M, Guerrini, R, Cross, Jh, and Sisodiya, Sm.

Subjects
Adult, Male, medicine.medical_specialty, Adolescent, High variability, MEDLINE, Disease, 03 medical and health sciences, Epilepsy, Young Adult, 0302 clinical medicine, medicine, Humans, ddc:610, Precision Medicine, Intensive care medicine, Child, 030304 developmental biology, Genetic testing, Aged, Retrospective Studies, 0303 health sciences, medicine.diagnostic_test, business.industry, Infant, Middle Aged, medicine.disease, Precision medicine, 3. Good health, Psychiatry and Mental health, Molecular Diagnostic Techniques, Child, Preschool, Cohort, Surgery, Observational study, Female, Neurology (clinical), business, 030217 neurology & neurosurgery
Abstract

Journal of neurology, neurosurgery, and psychiatry 92(10), 1044-1052 (2021). doi:10.1136/jnnp-2020-325932, Published by BMJ Publishing Group, London

Published
2020
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31. Ring Chromosome 17 Not Involving the Miller-Dieker Region: A Case with Drug-Resistant Epilepsy

Author

Fiona Farrell, Antonietta Coppola, Jonathan J. Waters, S. Krithika, Laura Hernandez-Hernandez, Deborah Morrogh, Josemir W. Sander, Sanjay M. Sisodiya, Simona Balestrini, Coppola, A., Morrogh, D., Farrell, F., Balestrini, S., Hernandez-Hernandez, L., Krithika, S., Sander, J. W., Waters, J. J., and Sisodiya, S. M.

Subjects
0301 basic medicine, Genetics, Ring chromosome, Status epilepticus, Biology, medicine.disease, Drug Resistant Epilepsy, Subtelomere, 03 medical and health sciences, Epilepsy, 030104 developmental biology, 0302 clinical medicine, Novel Insights from Clinical Practice, Intellectual disability, medicine, Autism, Copy-number variation, medicine.symptom, 030217 neurology & neurosurgery, Genetics (clinical)
Abstract

Chromosomal abnormalities are often identified in people with neurodevelopmental disorders including intellectual disability, autism, and epilepsy. Ring chromosomes, which usually involve gene copy number loss, are formed by fusion of subtelomeric or telomeric chromosomal regions. Some ring chromosomes, including ring 14, 17, and 20, are strongly associated with seizure disorders. We report an individual with a ring chromosome 17, r(17)(p13.3q25.3), with a terminal 17q25.3 deletion and no short arm copy number loss, and with a phenotype characterized by intellectual disability and drug-resistant epilepsy, including a propensity for nonconvulsive status epilepticus.

Published
2017

32. The challenges of treating epilepsy with 25 antiepileptic drugs

Author

Salvatore Striano, Antonietta Coppola, Lia Santulli, Simona Balestrini, Santulli, L., Coppola, A., Balestrini, S., and Striano, S.

Subjects
0301 basic medicine, Drug, medicine.medical_specialty, media_common.quotation_subject, Alternative medicine, Drug resistance, 03 medical and health sciences, Epilepsy, 0302 clinical medicine, Seizures, medicine, Animals, Humans, Intensive care medicine, Psychiatry, media_common, Pharmacology, business.industry, Seizure types, Gold standard, medicine.disease, Clinical trial, 030104 developmental biology, Tolerability, Anticonvulsants, business, 030217 neurology & neurosurgery
Abstract

Nowadays a substantial armamentarium of antiepileptic drugs (AEDs) is available, including drugs with different mechanisms of action, pharmacokinetics, efficacy and tolerability; therefore the choice for the right treatment is often challenging. The specific characteristic of the drug, the epileptic syndrome, seizure types and the patient's features need to be taken into consideration driving the choice through available evidence-based studies, which are often lacking for older AEDs. Besides, study conditions in registered clinical trials (RCTs) are quite different from daily clinical practice, which is more complex and various. When dealing with first diagnosed epilepsy, monotherapy is widely accepted as the gold standard option. Likewise, alternative monotherapy should be considered when the first drug treatment fails. However, the association of different AEDs in polytherapy is a common practice. The choice of AEDs used in association is often based on clinical experience or anecdotal observations or small clinical studies. Polytherapy should be as "rational" as possible and consider the mechanism of action, the pharmacokinetic characteristics and the safety of each drug. When dealing with drug resistant patients, clinicians should never give up and consider the use of AEDs acting on new targets. An attempt to come back to a monotherapy or simpler therapeutic regimen should be pursued even in patients who were previously drug resistant. This review will focus on the strategies to treat epilepsy by choosing among 25 available drugs.

Published
2016

33. Psychiatric comorbidities in patients from seven families with autosomal dominant cortical tremor, myoclonus, and epilepsy

Author

Laura Licchetta, Marcello Esposito, Salvatore Striano, Francesca Bisulli, A Coppola, Simona Balestrini, Federico Zara, Lia Santulli, Leandro Provinciali, Claudia Cagnetti, Carmela Caccavale, Pasquale Striano, Carlo Minetti, Paolo Tinuper, Coppola, Antonietta, Caccavale, Carmela, Santulli, Lia, Balestrini, Simona, Cagnetti, Claudia, Licchetta, Laura, Esposito, Marcello, Bisulli, Francesca, Tinuper, Paolo, Provinciali, Leandro, Minetti, Carlo, Zara, Federico, Striano, Pasquale, Striano, Salvatore, Coppola, A., Caccavale, C., Santulli, L., Balestrini, S., Cagnetti, C., Licchetta, L., Esposito, M., Bisulli, F., Tinuper, P., Provinciali, L., Minetti, C., Zara, F., Striano, P., and Striano, S.

Subjects
0301 basic medicine, Male, Myoclonus, Anxiety, Epilepsy, Behavioral Neuroscience, 0302 clinical medicine, Tremor, Prevalence, Depression, Mental Disorders, Myoclonic Epilepsy, Juvenile, Psychiatric Status Rating Scale, Middle Aged, Neurology, Italy, Mental Disorder, Female, medicine.symptom, Psychology, Human, Adult, congenital, hereditary, and neonatal diseases and abnormalities, medicine.medical_specialty, Mood Disorder, Psychotic Disorder, Personality Disorders, 03 medical and health sciences, Psychasthenia, Young Adult, Minnesota Multiphasic Personality Inventory, mental disorders, medicine, Humans, Psychiatry, Psychiatric Status Rating Scales, Personality disorder, Personality disorders, Quality of life, Neurology (clinical), Mood Disorders, Beck Depression Inventory, medicine.disease, nervous system diseases, 030104 developmental biology, Mood disorders, Psychotic Disorders, Quality of Life, Juvenile myoclonic epilepsy, Myoclonu, 030217 neurology & neurosurgery
Abstract

Objective The objective of this report was to assess the psychiatric comorbidity in a group of patients affected by autosomal dominant cortical tremor, myoclonus, and epilepsy (ADCME). Methods Reliable and validated psychodiagnostic scales including the BDI (Beck Depression Inventory), STAI-Y1 and 2 (State-Trait Anxiety Inventory — Y; 1 and 2), MMPI-2 (Minnesota Multiphasic Personality Inventory — 2), and QoLIE-31 (Quality of Life in Epilepsy Inventory — 31) were administered to 20 patients with ADCME, 20 patients with juvenile myoclonic epilepsy (JME), and 20 healthy controls. Results There was a higher prevalence of mood disorders in patients with ADCME compared to patients with JME and healthy controls, particularly depression (p = 0.035 and p = 0.017, respectively) and state anxiety (p = 0.024 and p = 0.019, respectively). Trait anxiety was not different from JME (p = 0.102) but higher than healthy controls (p = 0.017). The myoclonus score positively correlated with both state (rho: 0.58, p = 0.042) and trait anxiety (rho: 0.65, p = 0.011). These psychiatric features were also often associated with pathological traits of personality: paranoid (OR: 25.7, p = 0.003), psychasthenia (OR: 7.0, p = 0.023), schizophrenia (OR: 8.5, p = 0.011), and hypomania (OR: 5.5, p = 0.022). Finally, in patients with ADCME, decreased quality of life correlated with these psychiatric symptoms. Significance Patients with ADCME show a significant psychiatric burden that impairs their quality of life. A comprehensive psychiatric evaluation should be offered at the time of diagnosis to detect these comorbidities and to treat them.

Published
2015

34. From cannabis to cannabidiol to treat epilepsy, where are we?

Author

Giovambattista De Sarro, Antonietta Coppola, Antonio Leo, Emilio Russo, Simona Balestrini, Maurizio Elia, Pellegrino Lippiello, Rita Citraro, Lippiello, P., Balestrini, S., Leo, A., Coppola, A., Citraro, R., Elia, M., Russo, E., and de Sarro, G.

Subjects
0301 basic medicine, medicine.medical_specialty, medicine.medical_treatment, Epileptogenesis, 03 medical and health sciences, Epilepsy, 0302 clinical medicine, Drug Discovery, medicine, Animals, Cannabidiol, Humans, Intensive care medicine, Psychiatry, Beneficial effects, Cannabis, Pharmacology, Pediatric epilepsy, biology, business.industry, biology.organism_classification, medicine.disease, 030104 developmental biology, Anticonvulsant, Tolerability, Anticonvulsants, business, 030217 neurology & neurosurgery, medicine.drug
Abstract

Background: Several antiepileptic drugs (AEDs), about 25, are currently clinically available for the treatment of patients with epilepsy. Despite this armamentarium and the many recently introduced AEDs, no major advances have been achieved considering the number of drug resistant patients, while many benefits have been indeed obtained for other clinical outcomes (e.g. better tolerability, less interactions). Cannabinoids have long been studied for their potential therapeutical use and more recently phytocannabinoids have been considered a valuable tool for the treatment of several neurological disorders including epilepsy. Among this wide class, the most studied is cannabidiol (CBD) considering its lack of psychotropic effects and its anticonvulsant properties. Objective: Analyse the currently available literature on CBD also in light of other data on phytocannabinoids, reviewing data spanning from the mechanism of action, pharmacokinetic to clinical evidences. Results: Several preclinical studies have tried to understand the mechanism of action of CBD, which still remains largely not understood. CBD has shown significant anticonvulsant effects mainly in acute animal models of seizures; beneficial effects were reported also in animal models of epileptogenesis and chronic models of epilepsy, although not substantial. In contrast, data coming from some studies raise questions on the effects of other cannabinoids and above all marijuana. Conclusion: There is indeed sufficient supporting data for clinical development and important antiepileptic effects and the currently ongoing clinical studies will permit the real usefulness of CBD and possibly other cannabinoids. Undoubtedly, several issues also need to be addressed in the next future (e.g. better pharmacokinetic profiling). Finally, shading light on the mechanism of action and the study of other cannabinoids might represent an advantage for future developments.

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