Advertisement
REVIEW ARTICLE (META-ANALYSIS)| Volume 103, ISSUE 12, P2444-2453, December 2022

Prevalence of Neuropsychiatric Disorders in Duchenne and Becker Muscular Dystrophies: A Systematic Review and Meta-analysis

      Abstract

      Objective

      To estimate the prevalence of neuropsychiatric disorders, including autism spectrum disorders (ASDs), attention-deficit hyperactivity disorder (ADHD), depression, anxiety disorders, and obsessive-compulsive disorder (OCD), in populations with Duchenne muscular dystrophy (DMD) and Becker muscular dystrophy (BMD).

      Data Sources

      MEDLINE (via PubMed), Scopus, Web of Science, and Cochrane Library from inception to November 2021.

      Study Selection

      Observational studies of individuals with DMD or BMD that estimated the prevalence of ASDs, ADHD, depression, anxiety disorders, and OCD in each population.

      Data Extraction

      A random-effects meta-analysis was performed on each outcome and each population (ie, DMD, BMD).

      Data Synthesis

      Twenty-three studies were included in the meta-analysis. In DMD, there was a prevalence of 7.0% of ASDs, 18.0% of ADHD, 11.0% of depression, 24.0% of anxiety disorders, and 12.0% of OCD. Furthermore, in BMD, there was a prevalence of 6.0% of ASDs, 28.0% of ADHD, 7.0% of depression, 25.0% of anxiety disorders, and 7.0% of OCD.

      Conclusions

      The prevalence of these neuropsychiatric disorders is higher among patients with DMD or BMD than among the general population, and the presence of these disorders may negatively influence optimal medical management.

      List of abbreviations:

      ADHD (attention-deficit hyperactivity disorder), ASD (autism spectrum disorder), BMD (Becker muscular dystrophy), CNS (central nervous system), DMD (Duchenne muscular dystrophy), OCD (obsessive-compulsive disorder)

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Holland A
        • Carberry S
        • Ohlendieck K.
        Proteomics of the dystrophin-glycoprotein complex and dystrophinopathy.
        Curr Protein Pept Sci. 2014; 14: 680-697
        • Waldrop MA
        • Flanigan KM.
        Update in Duchenne and Becker muscular dystrophy.
        Curr. Opin Neurol. 2019; 32: 722-727
        • Mah JK
        • Korngut L
        • Dykeman J
        • Day L
        • Pringsheim T
        • Jette N.
        A systematic review and meta-analysis on the epidemiology of Duchenne and Becker muscular dystrophy.
        Neuromuscul. Disord. 2014; 24: 482-491
        • Bushby KM
        • Thambyayah M
        • Gardner-Medwin D.
        Prevalence and incidence of Becker muscular dystrophy.
        Lancet. 1991; 337: 1022-1024
        • Birnkrant DJ
        • Bushby K
        • Bann CM
        • et al.
        Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and neuromuscular, rehabilitation, endocrine, and gastrointestinal and nutritional management.
        Lancet Neurol. 2018; 17: 251-267
        • Birnkrant DJ
        • Bushby K
        • Bann CM
        • et al.
        Diagnosis and management of Duchenne muscular dystrophy, part 2: respiratory, cardiac, bone health, and orthopaedic management.
        Lancet Neurol. 2018; 17: 347-361
        • Pascual-Morena C
        • Cavero-Redondo I
        • Saz-Lara A
        • Sequí-Domínguez I
        • Lucerón-Lucas-Torres M
        • Martínez-Vizcaíno V
        Genetic modifiers and phenotype of duchenne muscular dystrophy: a systematic review and meta-analysis.
        Pharmaceuticals (Basel). 2021; 14: 798
        • Goemans N.
        How glucocorticoids change life in Duchenne muscular dystrophy.
        Lancet. 2018; 391: 406-407
        • Pascual-Morena C
        • Cavero-Redondo I
        • Álvarez-Bueno C
        • Mesas AE
        • Pozuelo-Carrascosa D
        • Martínez-Vizcaíno V.
        Restorative treatments of dystrophin expression in Duchenne muscular dystrophy: a systematic review.
        Ann Clin Transl Neurol. 2020; 7 (acn3.51149)
        • Ricotti V
        • Roberts RG
        • Muntoni F.
        Dystrophin and the brain.
        Dev Med Child Neurol. 2011; 53: 12
        • Birnkrant DJ
        • Bushby K
        • Bann CM
        • et al.
        Diagnosis and management of Duchenne muscular dystrophy, part 3: primary care, emergency management, psychosocial care, and transitions of care across the lifespan.
        Lancet Neurol. 2018; 17: 445-455
        • Doorenweerd N.
        Combining genetics, neuropsychology and neuroimaging to improve understanding of brain involvement in Duchenne muscular dystrophy - a narrative review.
        Neuromuscul Disord. 2020; 30: 437-442
        • Daoud F
        • Candelario-Martínez A
        • Billard JM
        • et al.
        Role of mental retardation-associated dystrophin-gene product Dp71 in excitatory synapse organization, synaptic plasticity and behavioral functions.
        PLoS One. 2008; 4: e6574
        • Doorenweerd N
        • Mahfouz A
        • van Putten M
        • et al.
        Timing and localization of human dystrophin isoform expression provide insights into the cognitive phenotype of Duchenne muscular dystrophy.
        Sci Rep. 2017; 7: 12575
        • Higgins JP
        • Green S.
        Cochrane handbook for systematic reviews of interventions: Cochrane book series.
        John Wiley and Sons, Hoboken2008
        • Stroup DF
        • Berlin JA
        • Morton SC
        • et al.
        Meta-analysis of observational studies in epidemiology: a proposal for reporting.
        J Am Med Assoc. 2000; 283: 2008-2012
      1. National Heart, Lung, and Blood Institute. Study quality assessment tools. Available at: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools. Accessed April 17, 2021.

        • Tufanaru C
        • Munn Z
        • Stephenson M
        • Aromataris E.
        Fixed or random effects meta-analysis? Common methodological issues in systematic reviews of effectiveness.
        Int J Evid Based Healthc. 2015; 13: 196-207
        • DerSimonian R
        • Laird N.
        Meta-analysis in clinical trials.
        Control Clin Trials. 1986; 7: 177-188
        • Higgins JPT
        • Thompson SG.
        Quantifying heterogeneity in a meta-analysis.
        Stat Med. 2002; 21: 1539-1558
        • Egger M
        • Smith GD
        • Schneider M
        • Minder C.
        Bias in meta-analysis detected by a simple, graphical test measures of funnel plot asymmetry.
        BMJ. 1997; 315: 629-634
        • Lambert JT
        • Darmahkasih AJ
        • Horn PS
        • et al.
        Neurodevelopmental, behavioral, and emotional symptoms in Becker muscular dystrophy.
        Muscle Nerve. 2020; 61: 156-162
        • Latimer R
        • Street N
        • Conway KC
        • et al.
        Secondary conditions among males with Duchenne or Becker muscular dystrophy.
        J Child Neurol. 2017; 32: 663-670
        • Mori-Yoshimura M
        • Mizuno Y
        • Yoshida S
        • et al.
        Social involvement issues in patients with Becker muscular dystrophy: a questionnaire survey of subjects from a patient registry.
        Brain Dev. 2018; 40: 268-277
        • Mori-Yoshimura M
        • Mizuno Y
        • Yoshida S
        • et al.
        Psychiatric and neurodevelopmental aspects of Becker muscular dystrophy.
        Neuromuscul Disord. 2019; 29: 930-939
        • Young HK
        • Barton BA
        • Waisbren S
        • et al.
        Cognitive and psychological profile of males with Becker muscular dystrophy.
        J Child Neurol. 2008; 23: 155-162
        • Banihani R
        • Smile S
        • Yoon G
        • et al.
        Cognitive and neurobehavioral profile in boys with Duchenne muscular dystrophy.
        J Child Neurol. 2015; 30: 1472-1482
        • Colombo P
        • Nobile M
        • Tesei A
        • et al.
        Assessing mental health in boys with Duchenne muscular dystrophy: emotional, behavioural and neurodevelopmental profile in an Italian clinical sample.
        Eur J Paediatr Neurol. 2017; 21: 639-647
        • Crescimanno G
        • Greco F
        • D'Alia R
        • Messina L
        • Marrone O
        Quality of life in long term ventilated adult patients with Duchenne muscular dystrophy.
        Neuromuscul Disord. 2019; 29: 569-575
        • Darke J
        • Bushby K
        • Couteur AL
        • McConachie H.
        Survey of behaviour problems in children with neuromuscular diseases.
        Eur J Paediatr Neurol. 2006; 10: 129-134
        • Darmahkasih AJ
        • Rybalsky I
        • Tian C
        • et al.
        Neurodevelopmental, behavioral, and emotional symptoms common in Duchenne muscular dystrophy.
        Muscle Nerve. 2020; 61: 466-474
        • Elsenbruch S
        • Schmid J
        • Lutz S
        • Geers B
        • Schara U.
        Self-reported quality of life and depressive symptoms in children, adolescents, and adults with Duchenne muscular dystrophy: a cross-sectional survey study.
        Neuropediatrics. 2013; 44: 257-264
        • Fitzpatrick C
        • Barry C
        • Garvey C.
        Psychiatric disorder among boys with Duchenne muscular dystrophy.
        Dev Med Child Neurol. 1986; 28: 589-595
        • Hendriksen JGM
        • Vles JSH.
        Neuropsychiatric disorders in males with Duchenne muscular dystrophy: frequency rate of attention-deficit hyperactivity disorder (ADHD), autism spectrum disorder, and obsessive-compulsive disorder.
        J Child Neurol. 2008; 23: 477-481
        • Hendriksen RGF
        • Vles JSH
        • Aalbers MW
        • Chin RFM
        • Hendriksen JGM.
        Brain-related comorbidities in boys and men with Duchenne muscular dystrophy: a descriptive study.
        Eur J Paediatr Neurol. 2018; 22: 488-497
        • Ozer U
        • Tufan AE.
        Psychiatric comorbidities in cases with Duchenne muscular dystrophy: a case series.
        Dusunen Adam. 2019; 32: 359-364
        • Pane M
        • Lombardo ME
        • Alfieri P
        • et al.
        Attention deficit hyperactivity disorder and cognitive function in Duchenne muscular dystrophy: phenotype-genotype correlation.
        J Pediatr. 2012; 161: 705-709
        • Pangalila RF
        • van den Bos GA
        • Bartels B
        • Bergen M
        • Stam HJ
        • Roebroeck ME.
        Prevalence of fatigue, pain, and affective disorders in adults with Duchenne muscular dystrophy and their associations with quality of life.
        Arch Phys Med Rehabil. 2015; 96: 1242-1247
        • Ricotti V
        • Mandy WPL
        • Scoto M
        • et al.
        Neurodevelopmental, emotional, and behavioural problems in Duchenne muscular dystrophy in relation to underlying dystrophin gene mutations.
        Dev Med Child Neurol. 2016; 58: 77-84
        • Steele M
        • Taylor E
        • Young C
        • McGrath P
        • Lyttle BDB
        • Davidson B.
        Mental health of children and adolescents with Duchenne muscular dystrophy.
        Dev Med Child Neurol. 2008; 50: 638-639
        • Tesei A
        • Nobile M
        • Colombo P
        • et al.
        Mental health and coping strategies in families of children and young adults with muscular dystrophies.
        J Neurol. 2020; 267: 2054-2069
        • Thangarajh M
        • Spurney CF
        • Gordish-Dressman H
        • et al.
        Neurodevelopmental needs in young boys with Duchenne muscular dystrophy (DMD): observations from the Cooperative International Neuromuscular Research Group (CINRG) DMD Natural History Study (DNHS).
        PLoS Curr. 2018; 10 (ecurrents.md.4cdeb6970e54034db2bc3dfa54b4d987)
        • Thangarajh M
        • Hendriksen J
        • McDermott MP
        • Martens W
        • Hart KA
        • Griggs RC.
        Relationships between DMD mutations and neurodevelopment in dystrophinopathy.
        Neurology. 2019; 93: E1597-E1604
        • Wei Y
        • Speechley KN
        • Zou G
        • Campbell C.
        Factors associated with health-related quality of life in children with Duchenne muscular dystrophy.
        J Child Neurol. 2016; 31: 879-886
        • Wu JY
        • Kuban KCK
        • Allred E
        • Shapiro F
        • Darras BT.
        Association of Duchenne muscular dystrophy with autism spectrum disorder.
        J Child Neurol. 2005; 20: 790-795
        • Baxter AJ
        • Brugha TS
        • Erskine HE
        • Scheurer RW
        • Vos T
        • Scott JG.
        The epidemiology and global burden of autism spectrum disorders.
        Psychol Med. 2015; 45: 601-613
        • Graus-Porta D
        • Blaess S
        • Senften M
        • et al.
        Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex.
        Neuron. 2001; 31: 367-379
        • Ash A
        • Machado L
        • Raleigh SM
        • Anthony K.
        Neuropathophysiology of Duchenne muscular dystrophy: involvement of the dystrophin isoform Dp71 in cell migration and proliferation.
        Neuromuscul Disord. 2018; 28: S13-S14
        • Reiner O
        • Karzbrun E
        • Kshirsagar A
        • Kaibuchi K.
        Regulation of neuronal migration, an emerging topic in autism spectrum disorders.
        J Neurochem. 2016; 136: 440-456
        • Jagadha V
        • Becker LE.
        Brain morphology in Duchenne muscular dystrophy: a Golgi study.
        Pediatr Neurol. 1988; 4: 87-92
        • Polanczyk GV
        • Salum GA
        • Sugaya LS
        • Caye A
        • Rohde LA.
        Annual research review: a meta-analysis of the worldwide prevalence of mental disorders in children and adolescents.
        J Child Psychol Psychiatry. 2015; 56: 345-365
        • Tripp G
        • Wickens JR.
        Neurobiology of ADHD.
        Neuropharmacology. 2009; 57: 579-589
        • Grillner P
        • Mercuri NB.
        Intrinsic membrane properties and synaptic inputs regulating the firing activity of the dopamine neurons.
        Behav Brain Res. 2002; 130: 149-169
      2. Power H, Fawcett JM, Fawcett E. A meta-analysis of the worldwide prevalence of obsessive compulsive disorder: are women at greater risk? Paper presented at: Canadian Psychological Association Convention. May 31- June 2, 2019; Nova Scotia, Canada.

        • Domschke K
        • Lawford B
        • Young R
        • et al.
        Dysbindin (DTNBP1) - a role in psychotic depression?.
        J Psychiatr Res. 2011; 45: 588-595
        • Vaillend C
        • Chaussenot R.
        Relationships linking emotional, motor, cognitive and GABAergic dysfunctions in dystrophin-deficient mdx mice.
        Hum Mol Genet. 2017; 26: 1041-1055
        • Goldberg D
        • Fawcett J.
        The importance of anxiety in both major depression and bipolar disorder.
        Depress Anxiety. 2012; 29: 471-478
        • Nelson JM
        • Liebel SW.
        Anxiety and depression among college students with attention-deficit/hyperactivity disorder (ADHD): cross-informant, sex, and subtype differences.
        J Am Coll Health. 2018; 66: 123-132
        • Poysky J
        • Kinnett K.
        Facilitating family adjustment to a diagnosis of Duchenne muscular dystrophy: April 24-25, 2008, Miami, Florida.
        Neuromuscul Disord. 2009; 19: 733-738
        • Erby LH
        • Rushton C
        • Geller G.
        “My son is still walking”: stages of receptivity to discussions of advance care planning among parents of sons with Duchenne muscular dystrophy.
        Semin Pediatr Neurol. 2006; 13: 132-140
        • Apkon SD
        • Alman B
        • Birnkrant DJ
        • et al.
        Orthopedic and surgical management of the patient with Duchenne muscular dystrophy.
        Pediatrics. 2018; 142: S82-S89
        • Vaillend C
        • Perronnet C
        • Ros C
        • et al.
        Rescue of a dystrophin-like protein by exon skipping in vivo restores GABAA-receptor clustering in the hippocampus of the mdx mouse.
        Mol Ther. 2010; 18: 1683-1688
        • Vaillend C
        • Zarrouki F
        • Vacca O.
        Gene therapy for central nervous system in Duchenne Muscular Dystrophy.
        Muscle Gene Ther. 2019; : 417-438
        • Wurster CD
        • Ludolph AC.
        Antisense oligonucleotides in neurological disorders.
        Ther Adv Neurol Disord. 2018; 111756286418776932
        • Devinsky O
        • King L
        • Bluvstein J
        • Friedman D.
        Ataluren for drug-resistant epilepsy in nonsense variant-mediated Dravet syndrome and CDKL5 deficiency disorder.
        Ann Clin Transl Neurol. 2021; 8: 639-644
        • Goyenvalle A
        • Griffith G
        • Babbs A
        • et al.
        Functional correction in mouse models of muscular dystrophy using exon-skipping tricyclo-DNA oligomers.
        Nat Med. 2015; 21: 270-275