Autism spectrum disorder in young patients with congenital central hypoventilation syndrome: role of the autonomic nervous system dysfunction.
Humans
Autism Spectrum Disorder
/ physiopathology
Female
Male
Hypoventilation
/ congenital
Retrospective Studies
Sleep Apnea, Central
/ physiopathology
Adolescent
Child
Autonomic Nervous System
/ physiopathology
Young Adult
Autonomic Nervous System Diseases
/ physiopathology
Child, Preschool
Risk Factors
Autism spectrum disorder
Autonomic nervous system
Congenital central hypoventilation syndrome
Heart rate variability
Journal
Orphanet journal of rare diseases
ISSN: 1750-1172
Titre abrégé: Orphanet J Rare Dis
Pays: England
ID NLM: 101266602
Informations de publication
Date de publication:
03 Jul 2024
03 Jul 2024
Historique:
received:
07
11
2023
accepted:
16
06
2024
medline:
4
7
2024
pubmed:
4
7
2024
entrez:
3
7
2024
Statut:
epublish
Résumé
Congenital central hypoventilation syndrome (CCHS) is a rare condition characterized by alveolar hypoventilation and autonomic nervous system (ANS) dysfunction requiring long-term ventilation. CCHS could constitute a risk factor of autism spectrum disorder (ASD) due to birth injury related to respiratory failure, which remains to be determined. ANS dysfunction has also been described in ASD and there are indications for altered contribution of ANS-central nervous system interaction in processing of social information; thus, CCHS could be a risk factor for ASD based on pathophysiological background also. Our study aimed to determine the prevalence of ASD among CCHS patients, identify risk factors, and explore the relationship between the ANS, evaluated by heart rate variability indices, and adaptative functioning. Our retrospective study, based on the analysis of records of a French national center of patients with CCHS under 20 years of age, determined that the prevalence of ASD (diagnosed by a psychiatrist, following the criteria of DSM-4 or DSM-5) was 6/69 patients, 8.7% (95% confidence interval: 3.3-18.0%). In a case (CCHS with ASD, n = 6) - control (CCHS without ASD, n = 12) study with matching on sex, longer neonatal hospitalization stay and glycemic dysfunction were associated with ASD. Adaptative functioning was assessed using Vineland Adaptative behavioral scales (VABS) and heart rate variability indices (including daytime RMSSD as an index of parasympathetic modulation) were obtained from ECG Holter performed the same day. In 19 young subjects with CCHS who had both ECG Holter and VABS, significant positive correlations were observed between RMSSD and three of four sub-domains of the VABS (communication: R = 0.50, p = 0.028; daily living skills: R = 0.60, p = 0.006; socialization: R = 0.52, p = 0.021). Our study suggests a high prevalence of ASD in patients with CCHS. Glycemic dysfunction and longer initial hospitalization stays were associated with ASD development. A defect in parasympathetic modulation was associated with worse adaptative functioning.
Sections du résumé
BACKGROUND
BACKGROUND
Congenital central hypoventilation syndrome (CCHS) is a rare condition characterized by alveolar hypoventilation and autonomic nervous system (ANS) dysfunction requiring long-term ventilation. CCHS could constitute a risk factor of autism spectrum disorder (ASD) due to birth injury related to respiratory failure, which remains to be determined. ANS dysfunction has also been described in ASD and there are indications for altered contribution of ANS-central nervous system interaction in processing of social information; thus, CCHS could be a risk factor for ASD based on pathophysiological background also. Our study aimed to determine the prevalence of ASD among CCHS patients, identify risk factors, and explore the relationship between the ANS, evaluated by heart rate variability indices, and adaptative functioning.
RESULTS
RESULTS
Our retrospective study, based on the analysis of records of a French national center of patients with CCHS under 20 years of age, determined that the prevalence of ASD (diagnosed by a psychiatrist, following the criteria of DSM-4 or DSM-5) was 6/69 patients, 8.7% (95% confidence interval: 3.3-18.0%). In a case (CCHS with ASD, n = 6) - control (CCHS without ASD, n = 12) study with matching on sex, longer neonatal hospitalization stay and glycemic dysfunction were associated with ASD. Adaptative functioning was assessed using Vineland Adaptative behavioral scales (VABS) and heart rate variability indices (including daytime RMSSD as an index of parasympathetic modulation) were obtained from ECG Holter performed the same day. In 19 young subjects with CCHS who had both ECG Holter and VABS, significant positive correlations were observed between RMSSD and three of four sub-domains of the VABS (communication: R = 0.50, p = 0.028; daily living skills: R = 0.60, p = 0.006; socialization: R = 0.52, p = 0.021).
CONCLUSION
CONCLUSIONS
Our study suggests a high prevalence of ASD in patients with CCHS. Glycemic dysfunction and longer initial hospitalization stays were associated with ASD development. A defect in parasympathetic modulation was associated with worse adaptative functioning.
Identifiants
pubmed: 38961480
doi: 10.1186/s13023-024-03257-z
pii: 10.1186/s13023-024-03257-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
249Informations de copyright
© 2024. The Author(s).
Références
Trang H, Samuels M, Ceccherini I, Frerick M, Garcia-Teresa MA, Peters J, et al. Guidelines for diagnosis and management of congenital central hypoventilation syndrome. Orphanet J Rare Dis. 2020;15:252.
doi: 10.1186/s13023-020-01460-2
pubmed: 32958024
pmcid: 7503443
Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature. 1999;399:366–70.
doi: 10.1038/20700
pubmed: 10360575
Vanderlaan M, Holbrook CR, Wang M, Tuell A, Gozal D. Epidemiologic survey of 196 patients with congenital central hypoventilation syndrome. Pediatr Pulmonol. 2004;37:217–29.
doi: 10.1002/ppul.10438
pubmed: 14966815
Trang H, Bourgeois P, Cheliout-Heraut F. Neurocognition in congenital Central Hypoventilation Syndrome: influence of genotype and ventilation method. Orphanet J Rare Dis. 2020;15:322.
doi: 10.1186/s13023-020-01601-7
pubmed: 33203435
pmcid: 7670788
Charnay AJ, Antisdel-Lomaglio JE, Zelko FA, Rand CM, Le M, Gordon SC, et al. Congenital Central Hypoventilation Syndrome: Neurocognition already reduced in preschool-aged children. Chest. 2016;149:809–15.
doi: 10.1378/chest.15-0402
pubmed: 26378991
Macdonald KT, Mosquera RA, Yadav A, Caldas-Vasquez MC, Emanuel H, Rennie K. Neurocognitive functioning in individuals with congenital central hypoventilation syndrome. BMC Pediatr. 2020;20:194.
doi: 10.1186/s12887-020-2006-5
pubmed: 32375736
pmcid: 7203975
Seijas-Gomez R, Esteso-Orduna B, Melero-Llorente J, Fournier-Del Castillo MC. [Clinical and neuropsychological characteristics in congenital central hypoventilation syndrome]. Rev Neurol. 2018;66:303–7.
pubmed: 29696617
Lai M-C, Lombardo MV, Baron-Cohen S. Autism Lancet Lond Engl. 2014;383:896–910.
doi: 10.1016/S0140-6736(13)61539-1
Gardener H, Spiegelman D, Buka SL. Perinatal and neonatal risk factors for autism: a Comprehensive Meta-analysis. Pediatrics. 2011;128:344.
doi: 10.1542/peds.2010-1036
pubmed: 21746727
pmcid: 3387855
van Hoorn A, Carpenter T, Oak K, Laugharne R, Ring H, Shankar R. Neuromodulation of autism spectrum disorders using vagal nerve stimulation. J Clin Neurosci off J Neurosurg Soc Australas. 2019;63:8–12.
Karjalainen S, Aro T, Parviainen T. Coactivation of autonomic and central nervous systems during Processing of socially relevant Information in Autism Spectrum disorder: a systematic review. Neuropsychol Rev. 2023.
McCormick CEB, Sheinkopf SJ, Levine TP, LaGasse LL, Tronick E, Lester BL. Diminished respiratory sinus arrhythmia response in infants later diagnosed with autism spectrum disorder. Autism Res off J Int Soc Autism Res. 2018;11:726–31.
doi: 10.1002/aur.1929
Ornoy A, Gorobets D, Weinstein-Fudim L, Becker M. Sex-related changes in the clinical, genetic, electrophysiological, Connectivity, and Molecular presentations of ASD: a comparison between human and animal models of ASD with reference to Our Data. Int J Mol Sci. 2023;24:3287.
doi: 10.3390/ijms24043287
pubmed: 36834699
pmcid: 9965966
Sparrow SS, Cicchetti DV, The Vineland Adaptive Behavior Scales. Major Psychol Assess Instrum Vol 2. Needham, Heights. MA, US: Allyn & Bacon; 1989. pp. 199–231.
Hayden-Evans M, Milbourn B, D’Arcy E, Chamberlain A, Afsharnejad B, Evans K, et al. An evaluation of the overall utility of measures of functioning suitable for school-aged children on the Autism Spectrum: a scoping review. Int J Environ Res Public Health. 2022;19:14114.
doi: 10.3390/ijerph192114114
pubmed: 36360993
pmcid: 9659140
Pichot V, Roche F, Celle S, Barthélémy J-C, Chouchou F. HRVanalysis: a Free Software for analyzing Cardiac autonomic activity. Front Physiol. 2016;7:557.
doi: 10.3389/fphys.2016.00557
pubmed: 27920726
pmcid: 5118625
Dudoignon B, Denjoy I, Patout M, Matrot B, Gallego J, Bokov P, et al. Heart rate variability in congenital central hypoventilation syndrome: relationships with hypertension and sinus pauses. Pediatr Res. 2023;93:1003–9.
doi: 10.1038/s41390-022-02215-4
pubmed: 35882978
Bougeard C, Picarel-Blanchot F, Schmid R, Campbell R, Buitelaar J. Prevalence of Autism Spectrum disorder and co-morbidities in children and adolescents: a systematic literature review. Focus Am Psychiatr Publ. 2024;22:212–28.
pubmed: 38680973
Daniels AM, Mandell DS. Explaining differences in age at autism spectrum disorder diagnosis: a critical review. Autism Int J Res Pract. 2014;18:583–97.
doi: 10.1177/1362361313480277
Guthrie W, Swineford LB, Nottke C, Wetherby AM. Early diagnosis of autism spectrum disorder: stability and change in clinical diagnosis and symptom presentation. J Child Psychol Psychiatry. 2013;54:582–90.
doi: 10.1111/jcpp.12008
pubmed: 23078094
pmcid: 3556369
Beopoulos A, Géa M, Fasano A, Iris F. Autism spectrum disorders pathogenesis: toward a comprehensive model based on neuroanatomic and neurodevelopment considerations. Front Neurosci. 2022;16:988735.
doi: 10.3389/fnins.2022.988735
pubmed: 36408388
pmcid: 9671112
Montirosso R, Morandi F, D’Aloisio C, Berna A, Provenzi L, Borgatti R. International Classification of Functioning, disability and health in children with congenital central hypoventilation syndrome. Disabil Rehabil. 2009;31(Suppl 1):S144–152.
doi: 10.3109/09638280903317807
pubmed: 19968527
Kumar R, Woo MS, Macey PM, Woo MA, Harper RM. Progressive gray matter changes in patients with congenital central hypoventilation syndrome. Pediatr Res. 2012;71:701–6.
doi: 10.1038/pr.2012.25
pubmed: 22343924
pmcid: 3638962
Zelko FA, Nelson MN, Leurgans SE, Berry-Kravis EM, Weese-Mayer DE. Congenital central hypoventilation syndrome: neurocognitive functioning in school age children. Pediatr Pulmonol. 2010;45:92–8.
doi: 10.1002/ppul.21170
pubmed: 19960523