TY - JOUR
T1 - The emerging spectrum of fetal acetylcholine receptor antibody-related disorders (FARAD)
AU - Allen, Nicholas M.
AU - O'Rahelly, Mark
AU - Eymard, Bruno
AU - Chouchane, Mondher
AU - Hahn, Andreas
AU - Kearns, Gerry
AU - Kim, Dae-Seong
AU - Byun, Shin Yun
AU - Nguyen, Cam-Tu Emilie
AU - Schara-Schmidt, Ulrike
AU - Kölbel, Heike
AU - Marina, Adela Della
AU - Schneider-Gold, Christiane
AU - Roefke, Kathryn
AU - Thieme, Andrea
AU - Van Den Bergh, Peter
AU - Avalos, Gloria
AU - Álvarez-Velasco, Rodrigo
AU - Natera-De Benito, Daniel
AU - Cheng, Man Hin Mark
AU - Chan, Wing Ki
AU - Wan, Hoi Shan
AU - Thomas, Mary Ann
AU - Borch, Lauren
AU - Lauzon, Julie
AU - Kornblum, Cornelia
AU - Reimann, Jens
AU - Mueller, Andreas
AU - Kuntzer, Thierry
AU - Norwood, Fiona
AU - Ramdas, Sithara
AU - Jacobson, Leslie W.
AU - Jie, Xiaobo
AU - Fernandez-Garcia, Miguel A.
AU - Wraige, Elizabeth
AU - Lim, Ming
AU - Lin, Jean Pierre
AU - Claeys, Kristl G.
AU - Aktas, Selma
AU - Oskoui, Maryam
AU - Hacohen, Yael
AU - Masud, Ameneh
AU - Leite, M Isabel
AU - Palace, Jacqueline
AU - De Vivo, Darryl
AU - Vincent, Angela
AU - Jungbluth, Heinz
N1 - Publisher Copyright:
© 2023 The Author(s).
PY - 2023/10/1
Y1 - 2023/10/1
N2 - In utero exposure to maternal antibodies targeting the fetal acetylcholine receptor isoform (fAChR) can impair fetal movement, leading to arthrogryposis multiplex congenita (AMC). Fetal AChR antibodies have also been implicated in apparently rare, milder myopathic presentations termed fetal acetylcholine receptor inactivation syndrome (FARIS). The full spectrum associated with fAChR antibodies is still poorly understood. Moreover, since some mothers have no myasthenic symptoms, the condition is likely underreported, resulting in failure to implement effective preventive strategies. Here we report clinical and immunological data from a multicentre cohort (n = 46 cases) associated with maternal fAChR antibodies, including 29 novel and 17 previously reported with novel follow-up data. Remarkably, in 50% of mothers there was no previously established myasthenia gravis (MG) diagnosis. All mothers (n = 30) had AChR antibodies and, when tested, binding to fAChR was often much greater than that to the adult AChR isoform. Offspring death occurred in 11/46 (23.9%) cases, mainly antenatally due to termination of pregnancy prompted by severe AMC (7/46, 15.2%), or during early infancy, mainly from respiratory failure (4/46, 8.7%). Weakness, contractures, bulbar and respiratory involvement were prominent early in life, but improved gradually over time. Facial (25/34; 73.5%) and variable peripheral weakness (14/32; 43.8%), velopharyngeal insufficiency (18/24; 75%) and feeding difficulties (16/36; 44.4%) were the most common sequelae in long-term survivors. Other unexpected features included hearing loss (12/32; 37.5%), diaphragmatic paresis (5/35; 14.3%), CNS involvement (7/40; 17.5%) and pyloric stenosis (3/37; 8.1%). Oral salbutamol used empirically in 16/37 (43.2%) offspring resulted in symptom improvement in 13/16 (81.3%). Combining our series with all previously published cases, we identified 21/85 mothers treated with variable combinations of immunotherapies (corticosteroids/intravenous immunoglobulin/plasmapheresis) during pregnancy either for maternal MG symptom control (12/21 cases) or for fetal protection (9/21 cases). Compared to untreated pregnancies (64/85), maternal treatment resulted in a significant reduction in offspring deaths (P < 0.05) and other complications, with treatment approaches involving intravenous immunoglobulin/ plasmapheresis administered early in pregnancy most effective. We conclude that presentations due to in utero exposure to maternal (fetal) AChR antibodies are more common than currently recognized and may mimic a wide range of neuromuscular disorders. Considering the wide clinical spectrum and likely diversity of underlying mechanisms, we propose 'fetal acetylcholine receptor antibody-related disorders' (FARAD) as the most accurate term for these presentations. FARAD is vitally important to recognize, to institute appropriate management strategies for affected offspring and to improve outcomes in future pregnancies. Oral salbutamol is a symptomatic treatment option in survivors.
AB - In utero exposure to maternal antibodies targeting the fetal acetylcholine receptor isoform (fAChR) can impair fetal movement, leading to arthrogryposis multiplex congenita (AMC). Fetal AChR antibodies have also been implicated in apparently rare, milder myopathic presentations termed fetal acetylcholine receptor inactivation syndrome (FARIS). The full spectrum associated with fAChR antibodies is still poorly understood. Moreover, since some mothers have no myasthenic symptoms, the condition is likely underreported, resulting in failure to implement effective preventive strategies. Here we report clinical and immunological data from a multicentre cohort (n = 46 cases) associated with maternal fAChR antibodies, including 29 novel and 17 previously reported with novel follow-up data. Remarkably, in 50% of mothers there was no previously established myasthenia gravis (MG) diagnosis. All mothers (n = 30) had AChR antibodies and, when tested, binding to fAChR was often much greater than that to the adult AChR isoform. Offspring death occurred in 11/46 (23.9%) cases, mainly antenatally due to termination of pregnancy prompted by severe AMC (7/46, 15.2%), or during early infancy, mainly from respiratory failure (4/46, 8.7%). Weakness, contractures, bulbar and respiratory involvement were prominent early in life, but improved gradually over time. Facial (25/34; 73.5%) and variable peripheral weakness (14/32; 43.8%), velopharyngeal insufficiency (18/24; 75%) and feeding difficulties (16/36; 44.4%) were the most common sequelae in long-term survivors. Other unexpected features included hearing loss (12/32; 37.5%), diaphragmatic paresis (5/35; 14.3%), CNS involvement (7/40; 17.5%) and pyloric stenosis (3/37; 8.1%). Oral salbutamol used empirically in 16/37 (43.2%) offspring resulted in symptom improvement in 13/16 (81.3%). Combining our series with all previously published cases, we identified 21/85 mothers treated with variable combinations of immunotherapies (corticosteroids/intravenous immunoglobulin/plasmapheresis) during pregnancy either for maternal MG symptom control (12/21 cases) or for fetal protection (9/21 cases). Compared to untreated pregnancies (64/85), maternal treatment resulted in a significant reduction in offspring deaths (P < 0.05) and other complications, with treatment approaches involving intravenous immunoglobulin/ plasmapheresis administered early in pregnancy most effective. We conclude that presentations due to in utero exposure to maternal (fetal) AChR antibodies are more common than currently recognized and may mimic a wide range of neuromuscular disorders. Considering the wide clinical spectrum and likely diversity of underlying mechanisms, we propose 'fetal acetylcholine receptor antibody-related disorders' (FARAD) as the most accurate term for these presentations. FARAD is vitally important to recognize, to institute appropriate management strategies for affected offspring and to improve outcomes in future pregnancies. Oral salbutamol is a symptomatic treatment option in survivors.
KW - arthrogryposis multiplex congenita
KW - congenital myopathy
KW - fetal acetylcholine receptor inactivation syndrome
KW - myasthenia gravis
KW - salbutamol
KW - transient neonatal myasthenia gravis
UR - http://hdl.handle.net/10379/18015
UR - https://www.scopus.com/pages/publications/85164075559
U2 - 10.13025/22443
DO - 10.13025/22443
M3 - Article
C2 - 37186601
SN - 0006-8950
VL - 146
SP - 4233
EP - 4246
JO - Brain
JF - Brain
IS - 10
ER -