Maple syrup urine disease: Clinical outcomes, metabolic control, and genotypes in a screened population after four decades of newborn bloodspot screening in the Republic of Ireland.


Journal

Journal of inherited metabolic disease
ISSN: 1573-2665
Titre abrégé: J Inherit Metab Dis
Pays: United States
ID NLM: 7910918

Informations de publication

Date de publication:
05 2021
Historique:
revised: 05 11 2020
received: 04 08 2020
accepted: 07 12 2020
pubmed: 11 12 2020
medline: 28 12 2021
entrez: 10 12 2020
Statut: ppublish

Résumé

Since 1972, 18 patients (10 females/8 males) have been detected by newborn bloodspot screening (NBS) with neonatal-onset maple syrup urine disease (MSUD) in Ireland. Patients were stratified into three clusters according to clinical outcome at the time of data collection, including developmental, clinical, and IQ data. A fourth cluster comprised of two early childhood deaths; a third patient died as an adult. We present neuroimaging and electroencephalography together with clinical and biochemical data. Incidence of MSUD (1972-2018) was 1 in 147 975. Overall good clinical outcomes were achieved with 15/18 patients alive and with essentially normal functioning (with only the lowest performing cluster lying beyond a single SD on their full scale intelligence quotient). Molecular genetic analysis revealed genotypes hitherto not reported, including a possible digenic inheritance state for the BCKDHA and DBT genes in one family. Treatment has been based on early implementation of emergency treatment, diet, close monitoring, and even dialysis in the setting of acute metabolic decompensation. A plasma leucine ≥400 μmol/L (outside therapeutic range) was more frequently observed in infancy or during adolescence, possibly due to infections, hormonal changes, or noncompliance. Children require careful management during metabolic decompensations in early childhood, and this represented a key risk period in our cohort. A high level of metabolic control can be achieved through diet with early implementation of a "sick day" regime and, in some cases, dialysis as a rescue therapy. The Irish cohort, despite largely classical phenotypes, achieved good outcomes in the NBS era, underlining the importance of early diagnosis and skilled multidisciplinary team management.

Identifiants

pubmed: 33300147
doi: 10.1002/jimd.12337
doi:

Substances chimiques

Leucine GMW67QNF9C

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

639-655

Informations de copyright

© 2020 SSIEM.

Références

Holmes Morton D, Strauss KA, Robinson DL, et al. Diagnosis and treatment of maple syrup disease: a study of 36 patients. Pediatrics. 2002;109:999-1008. https://doi.org/10.1542/peds.109.6.999.
Snyderman SE. The therapy of maple syrup urine disease. Am J Dis Child. 1967;113:68-73. https://doi.org/10.1017/CBO9781107415324.004.
Chuang DT, Chuang JL, Wynn RM. Lessons from genetic disorders of branched-chain amino acid metabolism. J Nutr. 2006;136:243-249. https://doi.org/10.1093/jn/136.1.243s.
Strauss KA, Carson VJ, Soltys K, et al. Branched-chain α-ketoacid dehydrogenase deficiency (maple syrup urine disease): treatment, biomarkers, and outcomes. Mol Genet Metab. 2020;129:1-14. https://doi.org/10.1016/j.ymgme.2020.01.006.
Oyarzabal A, Martínez-Pardo M, Merinero B, et al. A novel regulatory defect in the branched-chain α-keto acid dehydrogenase complex due to a mutation in the PPM1K gene causes a mild variant phenotype of maple syrup urine disease. Hum Mutat. 2013;34:355-362. https://doi.org/10.1002/humu.22242.
Knerr I, Weinhold N, Vockley J, Gibson KM. Advances and challenges in the treatment of branched chain amino/keto acid metabolic defects. J Inherit Metab Dis. 2012;35:29-40. https://doi.org/10.1007/s10545-010-9269-1.Advances.
Nyhan WL, Rice-kelts M, Klein J, et al. Treatment of the acute crisis in maple syrup urine disease. JAMA Pediatr. 1998;152:593-598.
Simon E, Fingerhut R, Baumkotter J, et al. Maple syrup urine disease: Favourable effect of early diagnosis by newborn screening on the neonatal course of the disease. J Inherit Metab Dis. 2006;29:532-537. https://doi.org/10.1007/s10545-006-0315-y.
Kelleher K, Mayne PD. A Practical Guide to Newborn Bloodspot Screening in Ireland; 2018. https://www.hse.ie/eng/health/child/newbornscreening/newbornbloodspotscreening/information-for-professionals/newbornbloodspot6th.pdf.
Zinnanti WJ, Lazovic J. Interrupting the mechanisms of brain injury in a model of maple syrup urine disease encephalopathy. J Inherit Metab Dis. 2012;35:71-79. https://doi.org/10.1007/s10545-011-9333-5.
Wajner M, Coelho DM, Barschak AG, et al. Reduction of large neutral amino acid concentrations in plasma and CSF of patients with maple syrup urine disease during crises. J Inherit Metab Dis. 2000;23:505-512. https://doi.org/10.1023/A:1005668431926.
Murin R, Schaer A, Kowtharapu BS, et al. Expression of 3-hydroxyisobutyrate dehydrogenase in cultured neural cells. J Neuochemistry. 2008;105:1176-1186. https://doi.org/10.1111/j.1471-4159.2008.05298.x.
Treacy E, Clow CL, Reade TR, Chitayat D, Mamer OA, Scriver CR. Maple syrup urine disease: interrelations between branched-chain amino-, oxo- and hydroxyacids; implications for treatment; associations with CNS dysmyelination. J Inherit Metab Dis. 1992;15:121-135. https://doi.org/10.1007/BF01800354.
Lee JY, Chiong MA, Estrada SC, Cutiongco-de la Paz EM, Silao CLT, Padilla CD. Maple syrup urine disease (MSUD)-clinical profile of 47 Filipino patients. J Inherit Metab Dis. 2008;31:281-285. https://doi.org/10.1007/s10545-008-0859-0.
Silao CLT, Padilla CD, Matsuo M. A novel deletion creating a new terminal exon of the dihydrolipoyl transacylase gene is a founder mutation of Filipino maple syrup urine disease. Mol Genet Metab. 2004;81:100-104. https://doi.org/10.1016/j.ymgme.2003.10.006.
de Castro-Hamoy LG, Chiong MAD, Estrada SC, Cordero CP. Challenges in the management of patients with maple syrup urine disease diagnosed by newborn screening in a developing country. J Community Genet. 2017;8:9-15. https://doi.org/10.1007/s12687-016-0281-5.
Murphy AM, Lambert D, Treacy EP, O'Meara A, Lynch SA. Incidence and prevalence of mucopolysaccharidosis type 1 in the Irish Republic. Arch Dis Child. 2009;94:52-54. https://doi.org/10.1136/adc.2007.135772.
Vandenbroucke JP, Von Elm E, Altman DG, et al. Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. PLoS Med. 2007;4:1628-1654. https://doi.org/10.1371/journal.pmed.0040297.
Couce ML, Ramos F, Bueno MA, et al. Evolution of maple syrup urine disease in patients diagnosed by newborn screening versus late diagnosis. Eur J Paediatr Neurol. 2015;19:652-659. https://doi.org/10.1016/j.ejpn.2015.07.009.
Herber S, Schwartz IVD, Nalin T, et al. Maple syrup urine disease in Brazil: a panorama of the last two decades. J Pediatr (Rio J). 2015;91:292-298. https://doi.org/10.1016/j.jped.2014.08.010.
Khalifa OA, Imtiaz F, Ramzan K, et al. Genotype-phenotype correlation of 33 patients with maple syrup urine disease. Am J Med Genet Part A. 2020;182:1-15. https://doi.org/10.1002/ajmg.a.61806.
Lynch SA, Crushell E, Lambert DM, et al. Catalogue of inherited disorders found among the Irish traveller population. J Med Genet. 2018;55:233-239. https://doi.org/10.1136/jmedgenet-2017-104974.
Frazier DM, Allgeier C, Homer C, et al. Nutrition management guideline for maple syrup urine disease: an evidence- and consensus-based approach. Mol Genet Metab. 2014;112:210-217. https://doi.org/10.1016/j.ymgme.2014.05.006.
Knerr I, Vockley J, Gibson KM. Disorders of leucine, isoleucine, and valine metabolism. In: Blau N, Duran M, Gibson KM, Dionisi Vici C, eds. Physician's Guide to the Diagnosis, Treatment, and Follow-Up of Inherited Metabolic Diseases. Heidelberg, Berlin, Germany: Springer Berlin Heidelberg; 2014:103-141.
Acosta PB, Yannicelli S, Division ALRP. Nutrition Support Protocols: the Ross Metabolic Formula System. Ross Products Division, Abbot Laboratories; 2001. https://www.hse.ie/eng/health/child/newbornscreening/newbornbloodspotscreening/information-for-professionals/newbornbloodspot6th.pdf.
Berry GT, Heidenreich R, Kaplan P, et al. Branched chain amino acid free parenteral nutrition in the treatment of acute metabolic decompensation inpatients with maple syrup urine disease. N Engl J Med. 1991;324:175-179.
Kindt E, Halvorsen S. The need of essential amino acids in children an evaluation based on the intake of phenylalanine, and valine in children with phenylketonuria, tyrosine amino transferase defect, and maple syrup urine disease. Am J Clin Nutr. 1980;33:279-286.
Medford E, Hare DJ, Wittkowski A. Demographic and psychosocial influences on treatment adherence for children and adolescents with PKU: a systematic review. JIMD Rep. 2017;39:107-116. https://doi.org/10.1007/8904.
Yap S, Naughten E. Homocystinuria due to cystathionine β-synthase deficiency in Ireland: 25 years' experience of a newborn screened and treated population with reference to clinical outcome and biochemical control. J Inherit Metab Dis. 1998;21:738-747. https://doi.org/10.1023/A:1005445132327.
Gortner L, Leupold D, Pohlandt F, Bartmann P. Peritoneal dialysis in the treatment of metabolic crises caused by inherited disorders of organic and amino acid metabolism. Acta Paediatr Int J Paediatr. 1989;78:706-711.
Jan W, Zimmerman RA, Wang ZJ, et al. MR diffusion imaging and MR spectroscopy of maple syrup urine disease during acute metabolic decompensation. Neuroradiology. 2003;45:393-399. https://doi.org/10.1007/s00234-003-0955-7.
Ha JS, Kim TK, Eun BL, et al. Maple syrup urine disease encephalopathy: a follow-up study in the acute stage using diffusion-weighted MRI. Pediatr Radiol. 2004;34:163-166. https://doi.org/10.1007/s00247-003-1058-7.
Sakai M, Inoue Y, Oba H, et al. Age dependence of diffusion-weighted magnetic resonance imaging findings in maple syrup urine disease encephalopathy. J Comput Assist Tomogr. 2005;29:524-527. https://doi.org/10.1097/01.rct.0000164667.65648.72.
Tharp BR. Unique EEG pattern (comb-like rhythm) in neonatal maple syrup urine disease. Pediatr Neurol. 1992;8:65-68. https://doi.org/10.1016/0887-8994(92)90056-5.
Agadi S, Sutton VR, Quach MM, Riviello JJ. The electroencephalogram in neonatal maple syrup urine disease: a case report. Clin EEG Neurosci. 2012;43:64-67. https://doi.org/10.1177/1550059411429521.
Grigg-Damberger MM, Coker SB, Halsey CL, Anderson CL. Neonatal burst suppression: its developmental significance. Pediatr Neurol. 1989;5:84-92. https://doi.org/10.1016/0887-8994(89)90032-5.
Thenayan EAL, Savard M, Sharpe MD, Norton L, Young B. Electroencephalogram for prognosis after cardiac arrest. J Crit Care. 2010;25:300-304. https://doi.org/10.1016/j.jcrc.2009.06.049.
Abi-Warde M-T, Roda C, Arnoux J, et al. Long-term metabolic follow-up and clinical outcome of 35 patients with maple syrup urine disease. J Inherit Metab Dis. 2017;40:783-792. https://doi.org/10.1007/s10545-017-0083-x.
Hoffmann B, Helbling C, Schadewaldt P, Wendel U. Impact of longitudinal plasma leucine levels on the intellectual outcome in patients with classic MSUD. Pediatr Res. 2006;59:17-20. https://doi.org/10.1203/01.pdr.0000190571.60385.34.
Neisser U, Boodoo G, Bouchard TJ, et al. Intelligence: knowns and unknowns. Am Psychol. 1996;51:77-101. https://doi.org/10.1037/0003-066X.51.2.77.
Trahan LH, Stuebing KK, Fletcher JM, Hiscock M. The Flynn effect: a meta-analysis. Psychol Bull. 2014;140:1332-1360. https://doi.org/10.1037/a0037173.
Bouchereau J, Leduc-Leballeur J, Pichard S, et al. Neurocognitive profiles in MSUD school-age patients. J Inherit Metab Dis. 2017;40:377-383. https://doi.org/10.1007/s10545-017-0033-7.
Molema F, Martinelli D, Hörster F, et al. Liver and/or kidney transplantation in amino and organic acid-related inborn errors of metabolism: An overview on European data. J Inherit Metab Dis. 2020. https://doi.org/10.1002/jimd.12318. [Online ahead of print].
Doull I, Evans H, Clarke J, et al. Full, shared and hybrid paediatric care for cystic fibrosis in south and mid Wales. Arch Dis Child. 2012;97:17-20. https://doi.org/10.1136/adc.2010.199380.
Sinha MD, Webb NJA. Shared care of children with renal disease. Curr Paediatr. 2006;16:254-258. https://doi.org/10.1016/j.cupe.2006.05.007.
Vockley J, Rinaldo P, Bennett MJ, Matern D, Vladutiu GD. Synergistic heterozygosity: disease resulting from multiple partial defects in one or more metabolic pathways. Mol Genet Metab. 2000;71:10-18. https://doi.org/10.1006/mgme.2000.3066.

Auteurs

Daniel O'Reilly (D)

National Centre for Inherited Metabolic Disorders, Children's Health Ireland at Temple Street, Dublin, Ireland.

Ellen Crushell (E)

National Centre for Inherited Metabolic Disorders, Children's Health Ireland at Temple Street, Dublin, Ireland.

Joanne Hughes (J)

National Centre for Inherited Metabolic Disorders, Children's Health Ireland at Temple Street, Dublin, Ireland.

Stephanie Ryan (S)

Department of Paediatric Radiology, Children's Health Ireland at Temple Street, Dublin, Ireland.

Yvonne Rogers (Y)

National Centre for Inherited Metabolic Disorders, Children's Health Ireland at Temple Street, Dublin, Ireland.

Ingrid Borovickova (I)

Metabolic Laboratory, Children's Health Ireland at Temple Street, Dublin, Ireland.
National Newborn Screening Laboratory, Children's Health Ireland at Temple Street, Dublin, Ireland.

Philip Mayne (P)

Metabolic Laboratory, Children's Health Ireland at Temple Street, Dublin, Ireland.
National Newborn Screening Laboratory, Children's Health Ireland at Temple Street, Dublin, Ireland.

Michael Riordan (M)

Department of Nephrology, Children's Health Ireland at Temple Street, Dublin, Ireland.

Atif Awan (A)

Department of Nephrology, Children's Health Ireland at Temple Street, Dublin, Ireland.

Kevin Carson (K)

Paediatric Intensive Care Unit, Children's Health Ireland at Temple Street, Dublin, Ireland.

Kim Hunter (K)

Paediatric Intensive Care Unit, Children's Health Ireland at Temple Street, Dublin, Ireland.

Bryan Lynch (B)

Department of Neurology, Children's Health Ireland at Temple Street, Dublin, Ireland.

Amre Shahwan (A)

Department of Neurology, Children's Health Ireland at Temple Street, Dublin, Ireland.

Véronique Rüfenacht (V)

Division of Metabolism and Children's Research Centre, University Children's Hospital, Zurich, Switzerland.

Johannes Häberle (J)

Division of Metabolism and Children's Research Centre, University Children's Hospital, Zurich, Switzerland.

Eileen P Treacy (EP)

Adult Metabolic Services/National Centre for Inherited Metabolic Disorders, Mater Misericordiae University Hospital, Dublin, Ireland.

Ahmad A Monavari (AA)

National Centre for Inherited Metabolic Disorders, Children's Health Ireland at Temple Street, Dublin, Ireland.

Ina Knerr (I)

National Centre for Inherited Metabolic Disorders, Children's Health Ireland at Temple Street, Dublin, Ireland.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH