Spinal muscular atrophy is also a disorder of spermatogenesis

Abstract Background Spinal muscular atrophy (SMA) patients benefit from pre-mRNA splicing modifiers targeting the SMN2 gene, which aims to increase functional SMN production. The animal toxicity affecting spermatogenesis associated with one such treatment raised questions about male SMA patients’ sp...

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Main Authors: Armelle Magot, Arnaud Reignier, Olivier Binois, Anne Laure Bedat-Millet, Jean-Baptiste Davion, Louise Debergé, Karima Ghorab, Lucie Guyant, Émilie Laheranne, Pascal Laforet, Claire Lefeuvre, Martial Mallaret, Maud Michaud, Chahla Omar, Aleksandra Nadaj-Pakleza, Guillaume Nicolas, Jean Baptiste Noury, Antoine Pegat, Morgane Péré, Emmanuelle Salort-Campana, Guilhem Sole, Marco Spinazzi, Céline Tard, Carole Vuillerot, Yann Péréon
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Orphanet Journal of Rare Diseases
Online Access:https://doi.org/10.1186/s13023-024-03494-2
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author Armelle Magot
Arnaud Reignier
Olivier Binois
Anne Laure Bedat-Millet
Jean-Baptiste Davion
Louise Debergé
Karima Ghorab
Lucie Guyant
Émilie Laheranne
Pascal Laforet
Claire Lefeuvre
Martial Mallaret
Maud Michaud
Chahla Omar
Aleksandra Nadaj-Pakleza
Guillaume Nicolas
Jean Baptiste Noury
Antoine Pegat
Morgane Péré
Emmanuelle Salort-Campana
Guilhem Sole
Marco Spinazzi
Céline Tard
Carole Vuillerot
Yann Péréon
author_facet Armelle Magot
Arnaud Reignier
Olivier Binois
Anne Laure Bedat-Millet
Jean-Baptiste Davion
Louise Debergé
Karima Ghorab
Lucie Guyant
Émilie Laheranne
Pascal Laforet
Claire Lefeuvre
Martial Mallaret
Maud Michaud
Chahla Omar
Aleksandra Nadaj-Pakleza
Guillaume Nicolas
Jean Baptiste Noury
Antoine Pegat
Morgane Péré
Emmanuelle Salort-Campana
Guilhem Sole
Marco Spinazzi
Céline Tard
Carole Vuillerot
Yann Péréon
author_sort Armelle Magot
collection DOAJ
description Abstract Background Spinal muscular atrophy (SMA) patients benefit from pre-mRNA splicing modifiers targeting the SMN2 gene, which aims to increase functional SMN production. The animal toxicity affecting spermatogenesis associated with one such treatment raised questions about male SMA patients’ spermatogenesis. Methods This descriptive, cross-sectional study was conducted from June 2022 to July 2023. The study involved adult male patients with genetically confirmed SMA type 2 (SMA2) or SMA3 from 13 French neuromuscular centers. The patients’ general data, motor severity, urological history, exposure to certain factors, parenthood, and spermogram results were obtained. All patients were enrolled prior to exposure to risdiplam. Findings Sixty-eight patients were enrolled ( 36 SMA2 and 32 SMA3 patients). Forty-one patients had fertility data (parenthood history and spermogram analyses) and underwent 33 spermograms. Fertility disorders were identified in 27 of the 41 patients (65·9%, 95%CI 51·3–80·4%) in particular SMA2 patients: 19 cases (90.5%, CI 77·9–100%) (SMA3: 8 cases (40%, CI 18·5–61·5%). Among the patients with available spermograms, 81% (27/33) had abnormal sperm concentration; 30% presented azoospermia. These abnormalities were significantly associated with SMA type (more prevalent in SMA2 patients, p < 0·001), disease motor severity, which included age at the loss of walking ability and wheelchair use duration (p < 0·001). The Motor Function Measure (MFM) determined that the sperm counts were also correlated with disease severity (p < 0·01). Interpretation The fertility disorders were correlated with SMA severity and were particularly evident in SMA2 patients. In the latter, sperm concentration positively correlated with MFM. This study is the first one to link fertility disorders with spermogram abnormalities in SMA males. Understanding spermatogenesis in SMA is crucial, especially with new therapies such as risdiplam. Consequently, conducting systematic spermogram studies prior to SMA treatment is recommended.
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spelling doaj-art-d9aab0adccd2475f92a72c0717eae0b22025-08-20T02:31:52ZengBMCOrphanet Journal of Rare Diseases1750-11722024-12-011911910.1186/s13023-024-03494-2Spinal muscular atrophy is also a disorder of spermatogenesisArmelle Magot0Arnaud Reignier1Olivier Binois2Anne Laure Bedat-Millet3Jean-Baptiste Davion4Louise Debergé5Karima Ghorab6Lucie Guyant7Émilie Laheranne8Pascal Laforet9Claire Lefeuvre10Martial Mallaret11Maud Michaud12Chahla Omar13Aleksandra Nadaj-Pakleza14Guillaume Nicolas15Jean Baptiste Noury16Antoine Pegat17Morgane Péré18Emmanuelle Salort-Campana19Guilhem Sole20Marco Spinazzi21Céline Tard22Carole Vuillerot23Yann Péréon24Centre de Référence Des Maladies Neuromusculaires AOC, CHU de Nantes, Filnemus, Euro-NMD, Hôtel DieuService de Médecine Et Biologie de La Reproduction, Gynécologie Médicale, CHU de NantesService de Biologie de La Reproduction–CECOS, Hôpital Antoine Béclère, AP-HP, Université Paris SaclayCentre de Référence Des Maladies Neuromusculaires Nord/Est/Ile de France, Services de Neurologie Et Neurophysiologie, CHU Charles NicolleCentre de Référence Des Maladies Neuromusculaires Nord/Est/Ile de France, CHU LilleCentre de Référence Des Maladies Neuromusculaires AOC, Service de Neurologie Et Des Maladies Neuromusculaires, CHU de Bordeaux, FILNEMUS, Euro-NMDCentre de Référence Des Maladies Neuromusculaires AOC, CHU de LimogesService de Neurophysiologie Et Service de Génétique Clinique, CHU de RouenCentre de Référence Des Maladies Neuromusculaires AOC, Service de Neurologie Et Des Maladies Neuromusculaires, CHU de Bordeaux, FILNEMUS, Euro-NMDService de Neurologie, CHU Raymond Poincaré, APHPService de Neurologie, CHU Raymond Poincaré, APHPCentre de Référence Des Maladies Neuromusculaires, Service de Neurologie, CHU Grenoble Alpes, Université Grenoble Alpes, Inserm, U1216, Grenoble Institut NeurosciencesService de Neurologie, Centre de Référence Maladies Neuromusculaires Nord-Est-Ile de France, CHRU CentralService de Neurologie, CHU Raymond Poincaré, APHPCentre de Référence Des Maladies Neuromusculaires Nord/Est/Ile de France, Service de Neurologie, Hôpitaux Universitaires de Strasbourg, EURO-NMDService de Neurologie, CHU Raymond Poincaré, APHPCentre de Référence Des Maladies Neuromusculaires AOC, Inserm, LBAI, UMR1227, CHRU de BrestService ENMG Et de Pathologies Neuromusculaires, Centre de Référence Des Maladies Neuromusculaires PACA-Réunion-Rhône Alpes, Hôpital Neurologique P. Wertheimer, Hospices Civils de LyonPlateforme de Méthodologie Et de Biostatistique, Centre Hospitalier Universitaire de NantesCentre de Référence PACA Réunion Rhône Alpes, AP-HM, Hôpital La Timone, FILNEMUSCentre de Référence Des Maladies Neuromusculaires AOC, Service de Neurologie Et Des Maladies Neuromusculaires, CHU de Bordeaux, FILNEMUS, Euro-NMDCentre de Référence Des Maladies Neuromusculaires AOC, Service de Neurologie, CHU d’AngersCentre de Référence Des Maladies Neuromusculaires Nord/Est/Ile de France, CHU LilleCentre de Référence Des Maladies Neuromusculaires Nord/Est/Ile-de-France, Service de Neurologie, U1172, CHU de LilleCentre de Référence Des Maladies Neuromusculaires AOC, CHU de Nantes, Filnemus, Euro-NMD, Hôtel DieuAbstract Background Spinal muscular atrophy (SMA) patients benefit from pre-mRNA splicing modifiers targeting the SMN2 gene, which aims to increase functional SMN production. The animal toxicity affecting spermatogenesis associated with one such treatment raised questions about male SMA patients’ spermatogenesis. Methods This descriptive, cross-sectional study was conducted from June 2022 to July 2023. The study involved adult male patients with genetically confirmed SMA type 2 (SMA2) or SMA3 from 13 French neuromuscular centers. The patients’ general data, motor severity, urological history, exposure to certain factors, parenthood, and spermogram results were obtained. All patients were enrolled prior to exposure to risdiplam. Findings Sixty-eight patients were enrolled ( 36 SMA2 and 32 SMA3 patients). Forty-one patients had fertility data (parenthood history and spermogram analyses) and underwent 33 spermograms. Fertility disorders were identified in 27 of the 41 patients (65·9%, 95%CI 51·3–80·4%) in particular SMA2 patients: 19 cases (90.5%, CI 77·9–100%) (SMA3: 8 cases (40%, CI 18·5–61·5%). Among the patients with available spermograms, 81% (27/33) had abnormal sperm concentration; 30% presented azoospermia. These abnormalities were significantly associated with SMA type (more prevalent in SMA2 patients, p < 0·001), disease motor severity, which included age at the loss of walking ability and wheelchair use duration (p < 0·001). The Motor Function Measure (MFM) determined that the sperm counts were also correlated with disease severity (p < 0·01). Interpretation The fertility disorders were correlated with SMA severity and were particularly evident in SMA2 patients. In the latter, sperm concentration positively correlated with MFM. This study is the first one to link fertility disorders with spermogram abnormalities in SMA males. Understanding spermatogenesis in SMA is crucial, especially with new therapies such as risdiplam. Consequently, conducting systematic spermogram studies prior to SMA treatment is recommended.https://doi.org/10.1186/s13023-024-03494-2
spellingShingle Armelle Magot
Arnaud Reignier
Olivier Binois
Anne Laure Bedat-Millet
Jean-Baptiste Davion
Louise Debergé
Karima Ghorab
Lucie Guyant
Émilie Laheranne
Pascal Laforet
Claire Lefeuvre
Martial Mallaret
Maud Michaud
Chahla Omar
Aleksandra Nadaj-Pakleza
Guillaume Nicolas
Jean Baptiste Noury
Antoine Pegat
Morgane Péré
Emmanuelle Salort-Campana
Guilhem Sole
Marco Spinazzi
Céline Tard
Carole Vuillerot
Yann Péréon
Spinal muscular atrophy is also a disorder of spermatogenesis
Orphanet Journal of Rare Diseases
title Spinal muscular atrophy is also a disorder of spermatogenesis
title_full Spinal muscular atrophy is also a disorder of spermatogenesis
title_fullStr Spinal muscular atrophy is also a disorder of spermatogenesis
title_full_unstemmed Spinal muscular atrophy is also a disorder of spermatogenesis
title_short Spinal muscular atrophy is also a disorder of spermatogenesis
title_sort spinal muscular atrophy is also a disorder of spermatogenesis
url https://doi.org/10.1186/s13023-024-03494-2
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