Carsten Gerhart Bönnemann, M.D.

Acting Neurogenetics Branch (NGB) Chief and Senior Investigator, Neuromuscular & Neurogenetic Diseases of Childhood Section, NGB
Carsten Bönnemann, M.D.
Division
Division of Intramural Research
Areas of Interest

Neuroscience, Clinical Research, Genetics and Genomics, and Neurological Disorders

Contact
carsten.bonnemann@nih.gov
301-594-5496

Dr. Bönnemann received his M.D. from Freiburg University, Germany. He completed pediatric training and venia legendi (Habilitation) in Germany. Residency in pediatric neurology at MGH/Harvard was followed by postdoctoral work with Dr. Louis Kunkel at Children's Hospital Boston working on the molecular genetics of muscular dystrophy.

In 2002, he joined the Children's Hospital of Philadelphia/University of Pennsylvania as Assistant Professor, Co-Director of the Neuromuscular Program, and Director of the Neurogenetics Clinic. He joined NINDS in 2010 as Senior Investigator and Chief of the Neuromuscular and Neurogenetic Disorders of Childhood Section and currently serves as the Acting Chief of the Neurogenetics Branch. Dr. Bönnemann was a Pew Fellow in the Biomedical Sciences. He received the 2009 Derek Denny Brown Neurological Scholar Award.

Research in Dr. Bönnemann's laboratory revolves around molecular mechanisms underlying early onset muscle disease (congenital muscular dystrophies, congenital myopathies, and reducing body myopathy). The laboratory's goal is to identify the genetic and cellular mechanisms in these conditions in order to develop strategies for molecular-based treatments.

Research Interests:

The overall clinical and laboratory interests of the Neuromuscular & Neurogenetic Diseases of Childhood Section (NNDCS) focus on early onset neuromuscular disorders of childhood, on their genetic and molecular pathogenesis, the pathways involved, and on developing preclinical translational models to lead to actual clinical trials. In the clinical part of the NNDCS we are leveraging next generation genomic technology towards the diagnosis and gene discovery in children with complex neuromuscular and neurogenetic conditions, identifying new genetics entities as well as establishing phenotypic spectra and defining the natural history of selected genetic entities. NNDCS has contributed significantly to the knowledge about the genetic bases, natural history and outcome measures in the congenital muscular dystrophies and has initiated a first clinical trial in this patient group (using omigapil).

Research in the NNDCS lab further focuses on the molecular pathogenesis of early onset muscle disorders using cellular and newly generated animal models, with the goal of defining opportunities for therapeutic interventions. A particular effort is devoted to gene editing approaches as well as RNA directed therapeutics directed at allele specific knockdown of dominantly acting mutations. We are also determining natural history and outcome measures in giant axonal neuropathy and in this condition have initiated the first intrathecal AAV9 mediated gene transfer trial in humans.

Focused Research Areas:

PaVe-GT: Platform Vector Gene Therapy

The Platform Vector Gene Therapy (PaVe-GT) team is studying the use of self-complementary AAV and various vector/expression constructs to target the neuromuscular junction (NMJ) that will then be used to treat established animal models in order to determine if gene therapy is successful at restoring NMJ structure and muscle function. With assistance from NCATS and NHGRI, we plan to demonstrate this platform-based gene therapy approach from conception, preclinical optimization, production, toxicology studies, regulatory filings and interactions, all the way to a clinical trial and make all learnings from this fully available. To find more information and contacts, please visit PaVe-GT.

GAN

Giant axonal neuropathy (GAN) is an ultrarare childhood onset autosomal recessive neurodegenerative disease that leads to both central and peripheral nervous system involvement. Its classic form is fatal and leads to early respiratory insufficiency. Our natural history study in GAN has focused on the identification of functional outcome measures, as well as neuroimaging, electrophysiologic, and biologic markers linked to phenotype and disease severity. In parallel, our group has developed and led a first in human intrathecal gene transfer clinical trial to assess the safety and efficacy of scAAV9-JeT-GAN which is ongoing. Additional clinical assessments and work has led to a deeper understanding of the broader phenotypic spectrum in GAN.

Contact: Diana Bharucha, MD

RNA- and DNA-based Therapies for the Collagen VI Dystrophies

The Bönnemann lab fosters a team of researchers dedicated to developing RNA- and DNA-based therapies for the collagen VI dystrophies. Collagen VI dystrophies are a group of congenital neuromuscular disorders characterized by generalized muscle weakness, progressive contractures and respiratory dysfunction, for which there is no effective treatment.

Contact: Veronique Bolduc PhD, Astrid Brull, PhD 

Generation and Characterization of Collagen VI Preclinical Mouse Models

The availability of animal models that accurately recapitulate the molecular and functional hallmarks of common collagen VI dystrophies pathogenic variants is essential to test our RNA- and DNA-based approaches in vivo. In addition to having acquired mice recapitulating either recessive null variants (Col6a2-/-) or a dominant-negative in-frame exon skip variant (Col6a3∆16/+), we have generated novel models, including a humanized knock-in mouse (Col6a1hum/hum) that will allow us to insert common variants in the context of the human sequence (such as the intron 11 pseudoexon, or glycine substitutions). We use behavioral, histological and molecular readouts (grip strength, inverted screen test, muscle histology, immunofluorescence, RT-PCR, western blotting) to follow muscle disease progression.

Characterization of the Collagen VI-producing Cells of the Muscle

Collagen VI is mainly produced by the fibro-adipogenic progenitor (FAP) cells of the muscle, but their precise location, behavior and function remains unknown. Characterization of this cell population, in the context of disease, is paramount to the development of RNA- and DNA-based therapies, as the therapeutic molecules will only be effective in cells expressing the targeted genes.  We are using in situ hybridization tools (such as RNAscope and BaseScope) on various mouse models to identify and spatially locate the collagen VI-expressing cells of the muscle.

Validation of RNA and DNA Targets and Optimization of Antisense Oligonucleotides 

Dominant-negative variants in any of the COL6A1, COL6A2 and COL6A3 genes are a frequent cause of collagen VI dystrophies. Our working hypothesis is that the suppression of the dominant-negative allele would allow the unaffected allele to effectively rebuild the collagen VI matrix. We are testing various strategies, such as allele-specific silencing (using small interfering RNAs), exon skipping (splice-modulating antisense oligonucleotides), RNA editing (ADAR-recruiting oligonucleotides), as well as DNA editing (CRISPR/Cas9 guide RNAs) to suppress or correct the dominant-negative transcripts or DNA. While our approach is currently variant-specific, the knowledge acquired will be transferable to other variants acting with a similar mechanism. We are validating these approaches using relevant cellular models (patient-derived skin fibroblasts) and molecular readouts (RT-PCR, quantitative and digital PCR, western blotting, immunofluorescence), and aim to achieve efficacy and specificity.

Screening of Antisense Chemistries and Viral Vectors for Effective Delivery to Fibro-adipogenic Progenitors

We work with various academic and industry collaborators to translate the aforementioned therapeutic approaches to preclinical testing in relevant animal models. One of our aims is to identify oligonucleotide chemistries that effectively target the muscle fibro-adipogenic progenitor cells. To that end, we are injecting the molecules into a reporter mouse model, and using fluorescence-activated cell sorting, sequencing, quantitative and digital PCR, and immunohistofluorescence as readouts.

Transcriptomics

The transcriptomics team is focused on using novel genomic and computational tools to understand, diagnose and treat congenital muscle diseases. To accomplish this goal, we use data-driven approaches such as short-read, long-read, single-cell, and spatial RNA-seq to determine the expression, splicing, and spatial location of transcripts in muscles of various conditions. Our interdisciplinary team is composed of clinicians, bioinformaticians, experimental biologists and collaborators such as Children’s National Hospital, Broad Institute, Scripps University, Yale University, and the Pediatric cell atlas consortium.

Contact: Prech "Brian" Uapinyoying

Molecular Diagnostics of Patients with Rare and Unknown Neuromuscular Disorders

Use RNA-seq data to supplement whole exome and whole genome sequencing data to validate and find novel splice variants.

Use computational tools computational tools to detect aberrant events in patient RNAseq data.

Long-read sequencing and next generation mapping tools to find structural variants.

Gene Expression Studies of Congenital Muscle Diseases

Differential expression analysis of muscle from patients who have rare congenital myopathies to define the molecular pathophysiology and for potential therapeutic targets.

Understanding how muscle resident cells coordinate their responses during muscle repair in wild-type and muscular dystrophy mouse models using single-cell/nuclei RNA-seq.

Pediatric Cell Atlas of Skeletal Muscle

The project is aimed to provide a transcriptomic reference map at the single cell/nuclei level for multiple healthy muscle types across different ages (infants to adolescents) and ethnicities.

Clinical Team

  • A. Reghan Foley, MD, Senior Research Physician
  • Sandra Donkervoort, MS, CGC, Lead Genetic Counselor
  • Rotem Orbach, MD, Staff Clinician
  • Diana Bharucha-Goebel, MD, Clinical Research Collaborator
  • Meghan McAnally, MD, MPH, Clinical Fellow
  • Ruchee Patel, MD, Clinical Fellow
  • Gilberto Mike Averion, BSN, RN, Clinical Research Nurse
  • Dana Macdonald, BSN, RN, Clinical Research Nurse
  • Alexa Yarish, BA, Research Coordinator
  • Joshua J. Todd, PhD, MBA, Staff Scientist (Clinical)
  • Kia Brooks, MS, Regulatory Affairs Specialist/Protocol Navigator
  • Christopher Mendoza, Patient Care Coordinator
  • Abigail Potticary, BS, IRTA
  • Jin Haugland, BS, IRTA

 

Lab Team

  • Yaqun Zou, MD, Staff Scientist
  • Véronique Bolduc, PhD, Staff Scientist
  • Ying Hu, MS, Biologist
  • Jachinta Rooney, PhD, Biologist
  • Pankaj Pathak, PhD, Research Fellow
  • Astrid Brull, PhD, Postdoctoral Visiting Fellow
  • P. Brian Uapinyoying, PhD, Post-doctoral IRTA
  • Sarah Silverstein, BS, Pre-doctoral IRTA
  • Fady Guirguis, BS, Pre-doctoral IRTA
  • Matthew Lefkowitz, BS, Pre-doctoral IRTA
  • Joseph Alisch, BS, MRSP
  • Sahil Malhotra, BS, IRTA
  • Berit Lubben, BS, IRTA
  • Jenny Xu, BS, IRTA
  • Jack Howell, BS, IRTA
  • Sofia Eisenberg, Academic Intern

 

Selected Publications

Gene and Mutation Discovery

  1. Bönnemann CG, Modi R, Noguchi S, Mizuno Y, Yoshida M, Gussoni E, McNally EM, Duggan DJ, Angelini C, Hoffman EP (1995)
    Beta-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex.
    Nat Genet, 11:266-73. PubMed ID: 7581449
     
  2. Schessl J, Zou Y, McGrath MJ, Cowling BS, Maiti B, Chin SS, Sewry C, Battini R, Hu Y, Cottle DL, Rosenblatt M, Spruce L, Ganguly A, Kirschner J, Judkins AR, Golden JA, Goebel HH, Muntoni F, Flanigan KM, Mitchell CA, Bönnemann CG (2008)
    Proteomic identification of FHL1 as the protein mutated in human reducing body myopathy.
    J Clin Invest, 118:904-12. PubMed ID: 18274675
     
  3. Zou Y, Zwolanek D, Izu Y, Gandhy S, Schreiber G, Brockmann K, Devoto M, Tian Z, Hu Y, Veit G, Meier M, Stetefeld J, Hicks D, Straub V, Voermans NC, Birk DE, Barton ER, Koch M, Bönnemann CG (2014)
    Recessive and dominant mutations in COL12A1 cause a novel EDS/myopathy overlap syndrome in humans and mice.
    Hum Mol Genet, 23:2339-52. PubMed ID: 24334604
     
  4. Chesler AT, Szczot M, Bharucha-Goebel D, Čeko M, Donkervoort S, Laubacher C, Hayes LH, Alter K, Zampieri C, Stanley C, Innes AM, Mah JK, Grosmann CM, Bradley N, Nguyen D, Foley AR, Le Pichon CE, Bönnemann CG (2016)
    The Role of PIEZO2 in Human Mechanosensation.
    N Engl J Med, 375:1355-1364. PubMed ID: 27653382
     
  5. Zou Y, Donkervoort S, Salo AM, Foley AR, Barnes AM, Hu Y, Makareeva E, Leach ME, Mohassel P, Dastgir J, Deardorff MA, Cohn RD, DiNonno WO, Malfait F, Lek M, Leikin S, Marini JC, Myllyharju J, Bönnemann CG (2017)
    P4HA1 mutations cause a unique congenital disorder of connective tissue involving tendon, bone, muscle and the eye.
    Hum Mol Genet, 26:2207-2217. PubMed ID: 28419360
     
  6. Cummings BB, Marshall JL, Tukiainen T, Lek M, Donkervoort S, Foley AR, Bolduc V, Waddell LB, Sandaradura SA, O'Grady GL, Estrella E, Reddy HM, Zhao F, Weisburd B, Karczewski KJ, O'Donnell-Luria AH, Birnbaum D, Sarkozy A, Hu Y, Gonorazky H, Claeys K, Joshi H, Bournazos A, Oates EC, Ghaoui R, Davis MR, Laing NG, Topf A, , Kang PB, Beggs AH, North KN, Straub V, Dowling JJ, Muntoni F, Clarke NF, Cooper ST, Bönnemann CG, MacArthur DG (2017)
    Improving genetic diagnosis in Mendelian disease with transcriptome sequencing.
    Sci Transl Med, 9 PubMed ID: 28424332
     
  7. Stavusis J, Lace B, Schäfer J, Geist J, Inashkina I, Kidere D, Pajusalu S, Wright NT, Saak A, Weinhold M, Haubenberger D, Jackson S, Kontrogianni-Konstantopoulos A, Bönnemann CG (2019)
    Novel mutations in MYBPC1 are associated with myogenic tremor and mild myopathy.
    Ann Neurol, 86:129-142. PubMed ID: 31025394
     
  8. Lopes Abath Neto O, Medne L, Donkervoort S, Rodríguez-García ME, Bolduc V, Hu Y, Guadagnin E, Foley AR, Brandsema JF, Glanzman AM, Tennekoon GI, Santi M, Berger JH, Megeney LA, Komaki H, Inoue M, Cotrina-Vinagre FJ, Hernández-Lain A, Martin-Hernández E, Williams L, Borell S, Schorling D, Lin K, Kolokotronis K, Lichter-Konecki U, Kirschner J, Nishino I, Banwell B, Martínez-Azorín F, Burgon PG, Bönnemann CG (2021)
    MLIP causes recessive myopathy with rhabdomyolysis, myalgia and baseline elevated  serum creatine kinase.
    Brain, 144:2722-2731. PubMed ID: 34581780
     
  9. Mohassel P, Donkervoort S, Lone MA, Nalls M, Gable K, Gupta SD, Foley AR, Hu Y, Saute JAM, Moreira AL, Kok F, Introna A, Logroscino G, Grunseich C, Nickolls AR, Pourshafie N, Neuhaus SB, Saade D, Gangfuß A, Kölbel H, Piccus Z, Le Pichon CE, Fiorillo C, Ly CV, Töpf A, Brady L, Specht S, Zidell A, Pedro H, Mittelmann E, Thomas FP, Chao KR, Konersman CG, Cho MT, Brandt T, Straub V, Connolly AM, Schara U, Roos A, Tarnopolsky M, Höke A, Brown RH, Lee CH, Hornemann T, Dunn TM, Bönnemann CG (2021)
    Childhood amyotrophic lateral sclerosis caused by excess sphingolipid synthesis.
    Nat Med, 27:1197-1204. PubMed ID: 34059824

  10. Kim HJ, Mohassel P, Donkervoort S, Guo L, O'Donovan K, Coughlin M, Lornage X, Foulds N, Hammans SR, Foley AR, Fare CM, Ford AF, Ogasawara M, Sato A, Iida A, Munot P, Ambegaonkar G, Phadke R, O'Donovan DG, Buchert R, Grimmel M, Töpf A, Zaharieva IT, Brady L, Hu Y, Lloyd TE, Klein A, Steinlin M, Kuster A, Mercier S, Marcorelles P, Péréon Y, Fleurence E, Manzur A, Ennis S, Upstill-Goddard R, Bello L, Bertolin C, Pegoraro E, Salviati L, French CE, Shatillo A, Raymond FL, Haack TB, Quijano-Roy S, Böhm J, Nelson I, Stojkovic T, Evangelista T, Straub V, Romero NB, Laporte J, Muntoni F, Nishino I, Tarnopolsky MA, Shorter J, Bönnemann CG, Taylor JP (2022)
    Heterozygous frameshift variants in HNRNPA2B1 cause early-onset oculopharyngeal muscular dystrophy.
    Nat Commun, 13:2306. PubMed ID: 35484142

Mechanisms and Preclinical Genetic Therapeutic Approaches

  1. Zou Y, Zhang RZ, Sabatelli P, Chu ML, Bönnemann CG (2008)
    Muscle interstitial fibroblasts are the main source of collagen VI synthesis in skeletal muscle: implications for congenital muscular dystrophy types Ullrich and Bethlem.
    J Neuropathol Exp Neurol, 67:144-54. PubMed ID: 18219255
     
  2. Lampe AK, Zou Y, Sudano D, O'Brien KK, Hicks D, Laval SH, Charlton R, Jimenez-Mallebrera C, Zhang RZ, Finkel RS, Tennekoon G, Schreiber G, van der Knaap MS, Marks H, Straub V, Flanigan KM, Chu ML, Muntoni F, Bushby KM, Bönnemann CG (2008)
    Exon skipping mutations in collagen VI are common and are predictive for severity and inheritance.
    Hum Mutat, 29:809-22. PubMed ID: 18366090
     
  3. Foley AR, Hu Y, Zou Y, Columbus A, Shoffner J, Dunn DM, Weiss RB, Bönnemann CG (2009)
    Autosomal recessive inheritance of classic Bethlem myopathy.
    Neuromuscul Disord, 19:813-7. PubMed ID: 19884007
     
  4. Foley AR, Hu Y, Zou Y, Yang M, Medne L, Leach M, Conlin LK, Spinner N, Shaikh TH, Falk M, Neumeyer AM, Bliss L, Tseng BS, Winder TL, Bönnemann CG (2011)
    Large genomic deletions: a novel cause of Ullrich congenital muscular dystrophy.
    Ann Neurol, 69:206-11. PubMed ID: 21280092
     
  5. Butterfield RJ, Foley AR, Dastgir J, Asman S, Dunn DM, Zou Y, Hu Y, Donkervoort S, Flanigan KM, Swoboda KJ, Winder TL, Weiss RB, Bönnemann CG (2013)
    Position of glycine substitutions in the triple helix of COL6A1, COL6A2, and COL6A3 is correlated with severity and mode of inheritance in collagen VI myopathies.
    Hum Mutat, 34:1558-67. PubMed ID: 24038877
     
  6. Bolduc V, Zou Y, Ko D, Bönnemann CG (2014)
    siRNA-mediated Allele-specific Silencing of a COL6A3 Mutation in a Cellular Model of Dominant Ullrich Muscular Dystrophy.
    Mol Ther Nucleic Acids, 3:e147. PubMed ID: 24518369
     
  7. Donkervoort S, Hu Y, Stojkovic T, Voermans NC, Foley AR, Leach ME, Dastgir J, Bolduc V, Cullup T, de Becdelièvre A, Yang L, Su H, Meilleur K, Schindler AB, Kamsteeg EJ, Richard P, Butterfield RJ, Winder TL, Crawford TO, Weiss RB, Muntoni F, Allamand V, Bönnemann CG (2015)
    Mosaicism for dominant collagen 6 mutations as a cause for intrafamilial phenotypic variability.
    Hum Mutat, 36:48-56. PubMed ID: 25204870
     
  8. Bolduc V, Foley AR, Solomon-Degefa H, Sarathy A, Donkervoort S, Hu Y, Chen GS, Sizov K, Nalls M, Zhou H, Aguti S, Cummings BB, Lek M, Tukiainen T, Marshall JL, Regev O, Marek-Yagel D, Sarkozy A, Butterfield RJ, Jou C, Jimenez-Mallebrera C, Li Y, Gartioux C, Mamchaoui K, Allamand V, Gualandi F, Ferlini A, Hanssen E, , Wilton SD, Lamandé SR, MacArthur DG, Wagener R, Muntoni F, Bönnemann CG (2019)
    A recurrent COL6A1 pseudoexon insertion causes muscular dystrophy and is effectively targeted by splice-correction therapies.
    JCI Insight, 4 PubMed ID: 30895940

  9. Nickolls AR, Lee MM, Espinoza DF, Szczot M, Lam RM, Wang Q, Beers J, Zou J, Nguyen MQ, Solinski HJ, AlJanahi AA, Johnson KR, Ward ME, Chesler AT, Bönnemann CG (2020)
    Transcriptional Programming of Human Mechanosensory Neuron Subtypes from Pluripotent Stem Cells.
    Cell Rep, 30:932-946.e7. PubMed ID: 31968264

Outcome Measures, Gene Therapy, and Clinical Trials

  1. Foley AR, Quijano-Roy S, Collins J, Straub V, McCallum M, Deconinck N, Mercuri E, Pane M, D'Amico A, Bertini E, North K, Ryan MM, Richard P, Allamand V, Hicks D, Lamandé S, Hu Y, Gualandi F, Auh S, Muntoni F, Bönnemann CG (2013)
    Natural history of pulmonary function in collagen VI-related myopathies.
    Brain, 136:3625-33. PubMed ID: 24271325
     
  2. Vuillerot C, Rippert P, Kinet V, Renders A, Jain M, Waite M, Glanzman AM, Girardot F, Hamroun D, Iwaz J, Ecochard R, Quijano-Roy S, Bérard C, Poirot I, Bönnemann CG, (2014)
    Rasch analysis of the motor function measure in patients with congenital muscle dystrophy and congenital myopathy.
    Arch Phys Med Rehabil, 95:2086-95. PubMed ID: 24973498
     
  3. Meilleur KG, Jain MS, Hynan LS, Shieh CY, Kim E, Waite M, McGuire M, Fiorini C, Glanzman AM, Main M, Rose K, Duong T, Bendixen R, Linton MM, Arveson IC, Nichols C, Yang K, Fischbeck KH, Wagner KR, North K, Mankodi A, Grunseich C, Hartnett EJ, Smith M, Donkervoort S, Schindler A, Kokkinis A, Leach M, Foley AR, Collins J, Muntoni F, Rutkowski A, Bönnemann CG (2015)
    Results of a two-year pilot study of clinical outcome measures in collagen VI- and laminin alpha2-related congenital muscular dystrophies.
    Neuromuscul Disord, 25:43-54. PubMed ID: 25307854
     
  4. Szczot M, Liljencrantz J, Ghitani N, Barik A, Lam R, Thompson JH, Bharucha-Goebel D, Saade D, Necaise A, Donkervoort S, Foley AR, Gordon T, Case L, Bushnell MC, Bönnemann CG, Chesler AT (2018)
    PIEZO2 mediates injury-induced tactile pain in mice and humans.
    Sci Transl Med, 10 PubMed ID: 30305456
     
  5. Jain MS, Meilleur K, Kim E, Norato G, Waite M, Nelson L, McGuire M, Duong T, Keller K, Lott DJ, Glanzman A, Rose K, Main M, Fiorini C, Chrismer I, Linton M, Punjabi M, Elliott J, Tounkara F, Vasavada R, Logaraj R, Winkert J, Donkervoort S, Leach M, Dastgir J, Hynan L, Nichols C, Hartnett E, Averion GM, Collins JC, Kim ES, Kokkinis A, Schindler A, Zukosky K, Fee R, Hinton V, Mohassel P, Bharucha-Goebel D, Vuillerot C, McGraw P, Barton M, Fontana J, Rutkowski A, Foley AR, Bönnemann CG (2019)
    Longitudinal changes in clinical outcome measures in COL6-related dystrophies and LAMA2-related dystrophies.
    Neurology, 93:e1932-e1943. PubMed ID: 31653707
     
  6. Marshall KL, Saade D, Ghitani N, Coombs AM, Szczot M, Keller J, Ogata T, Daou I, Stowers LT, Bönnemann CG, Chesler AT, Patapoutian A (2020)
    PIEZO2 in sensory neurons and urothelial cells coordinates urination.
    Nature, 588:290-295. PubMed ID: 33057202
     
  7. Natera-de Benito D, Foley AR, Domínguez-González C, Ortez C, Jain M, Mebrahtu A, Donkervoort S, Hu Y, Fink M, Yun P, Ogata T, Medina J, Vigo M, Meilleur KG, Leach ME, Dastgir J, Díaz-Manera J, Carrera-García L, Expósito-Escudero J, Alarcon M, Cuadras D, Montiel-Morillo E, Milisenda JC, Dominguez-Rubio R, Olivé M, Colomer J, Jou C, Jimenez-Mallebrera C, Bönnemann CG, Nascimento A (2021)
    Association of Initial Maximal Motor Ability With Long-term Functional Outcome in Patients With COL6-Related Dystrophies.
    Neurology, 96:e1413-e1424. PubMed ID: 33441455
     
  8. Bharucha-Goebel DX, Norato G, Saade D, Paredes E, Biancavilla V, Donkervoort S, Kaur R, Lehky T, Fink M, Armao D, Gray SJ, Waite M, Debs S, Averion G, Hu Y, Zein WM, Foley AR, Jain M, Bönnemann CG (2021)
    Giant axonal neuropathy: cross-sectional analysis of a large natural history cohort.
    Brain, 144:3239-3250. PubMed ID: 34114613
 

Patient Resources

Please find below resources for more information on congenital-onset muscle diseases and links for support groups, international registries and more: