New insights into carnitine-acylcarnitine translocase deficiency from 23 cases: Management challenges and potential therapeutic approaches.


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:
07 2021
Historique:
revised: 19 02 2021
received: 01 10 2020
accepted: 23 02 2021
pubmed: 27 2 2021
medline: 18 1 2022
entrez: 26 2 2021
Statut: ppublish

Résumé

Carnitine acyl-carnitine translocase deficiency (CACTD) is a rare autosomal recessive disorder of mitochondrial long-chain fatty-acid transport. Most patients present in the first 2 days of life, with hypoketotic hypoglycaemia, hyperammonaemia, cardiomyopathy or arrhythmia, hepatomegaly and elevated liver enzymes. Multi-centre international retrospective chart review of clinical presentation, biochemistry, treatment modalities including diet, subsequent complications, and mode of death of all patients. Twenty-three patients from nine tertiary metabolic units were identified. Seven attenuated patients of Pakistani heritage, six of these homozygous c.82G>T, had later onset manifestations and long-term survival without chronic hyperammonemia. Of the 16 classical cases, 15 had cardiac involvement at presentation comprising cardiac arrhythmias (9/15), cardiac arrest (7/15), and cardiac hypertrophy (9/15). Where recorded, ammonia levels were elevated in all but one severe case (13/14 measured) and 14/16 had hypoglycaemia. Nine classical patients survived longer-term-most with feeding difficulties and cognitive delay. Hyperammonaemia appears refractory to ammonia scavenger treatment and carglumic acid, but responds well to high glucose delivery during acute metabolic crises. High-energy intake seems necessary to prevent decompensation. Anaplerosis utilising therapeutic d,l-3-hydroxybutyrate, Triheptanoin and increased protein intake, appeared to improve chronic hyperammonemia and metabolic stability where trialled in individual cases. CACTD is a rare disorder of fatty acid oxidation with a preponderance to severe cardiac dysfunction. Long-term survival is possible in classical early-onset cases with long-chain fat restriction, judicious use of glucose infusions, and medium chain triglyceride supplementation. Adjunctive therapies supporting anaplerosis may improve longer-term outcomes.

Identifiants

pubmed: 33634872
doi: 10.1002/jimd.12371
doi:

Substances chimiques

Carnitine Acyltransferases EC 2.3.1.-
Carnitine S7UI8SM58A

Types de publication

Journal Article Multicenter Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

903-915

Informations de copyright

© 2021 SSIEM.

Références

Stanley CA, Hale DE, Berry GT, Deleeuw S, Boxer J, Bonnefont JP. Brief report: a deficiency of carnitine-acylcarnitine translocase in the inner mitochondrial membrane. N Engl J Med. 1992;327(1):19-23. https://doi.org/10.1056/NEJM199207023270104.
Yan HM, Hu H, Ahmed A, et al. Carnitine-acylcarnitine translocase deficiency with c.199-10 T>G and novel c.1A>G mutation: two case reports and brief literature review. Medicine (Baltimore). 2017;96(45):e8549. https://doi.org/10.1097/MD.0000000000008549.
Longo N, Amat di San Filippo C, Pasquali M. Disorders of carnitine transport and the carnitine cycle. Am J Med Genet C Semin Med Genet. 2006;142C(2):77-85. https://doi.org/10.1002/ajmg.c.30087.
Roschinger W, Muntau AC, Duran M, et al. Carnitine-acylcarnitine translocase deficiency: metabolic consequences of an impaired mitochondrial carnitine cycle. Clin Chim Acta. 2000;298(1-2):55-68. https://doi.org/10.1016/s0009-8981(00)00268-0.
Rubio-Gozalbo ME, Bakker JA, Waterham HR, Wanders RJ. Carnitine-acylcarnitine translocase deficiency, clinical, biochemical and genetic aspects. Mol Asp Med. 2004;25(5-6):521-532.
Saudubray JM, Martin D, de Lonlay P, et al. Recognition and management of fatty acid oxidation defects: a series of 107 patients. J Inherit Metab Dis. 1999;22(4):488-502. https://doi.org/10.1023/a:1005556207210.
Chalmers RA, Stanley CA, English N, Wigglesworth JS. Mitochondrial carnitine-acylcarnitine translocase deficiency presenting as sudden neonatal death. J Pediatr. 1997;131(2):220-225. https://doi.org/10.1016/s0022-3476(97)70157-4.
Parini R, Invernizzi F, Menni F, et al. Medium-chain triglyceride loading test in carnitine-acylcarnitine translocase deficiency: insights on treatment. J Inherit Metab Dis. 1999;22(6):733-739. https://doi.org/10.1023/a:1005548201355.
Arnold GL, Van Hove J, Freedenberg D, et al. A Delphi clinical practice protocol for the management of very long chain acyl-CoA dehydrogenase deficiency. Mol Genet Metab. 2009;96(3):85-90.
Hsu BY, Iacobazzi V, Wang Z, et al. Aberrant mRNA splicing associated with coding region mutations in children with carnitine-acylcarnitine translocase deficiency. Mol Genet Metab. 2001;74(1-2):248-255. https://doi.org/10.1006/mgme.2001.3235.
Vitoria I, Martin-Hernandez E, Pena-Quintana L, et al. Carnitine-acylcarnitine translocase deficiency: experience with four cases in Spain and review of the literature. JIMD Reports. 2015;20:11-20.
Pierre G, Macdonald A, Gray G, Hendriksz C, Preece MA, Chakrapani A. Prospective treatment in carnitine-acylcarnitine translocase deficiency. J Inherit Metab Dis. 2007;30(5):815. https://doi.org/10.1007/s10545-007-0518-x.
Bhattacharya K, Matar W, Tolun A, et al. The use of sodium DL-3-Hydroxybutyrate in severe acute neuro-metabolic compromise in patients with inherited ketone body synthetic disorders. Orphanet J Rare Dis. 2020;15(53). https://dx.doi.org/10.1186/s13023-020-1316-x.
Hammond J, Sim KG, Trenholm A, Stanley EL, Wilcken B. Sudden infant death in infancy - two NZ cases of carnitine acylcarnitine translocase deficiency. J Inherit Metab Dis. 1998;21(Suppl 2):60.
Lopriore E, Gemke RJ, Verhoeven NM, et al. Carnitine-acylcarnitine translocase deficiency: phenotype, residual enzyme activity and outcome. Eur J Pediatr. 2001;160(2):101-104. https://doi.org/10.1007/s004310000644.
Costa C, Costa JM, Nuoffer JM, et al. Identification of the molecular defect in a severe case of carnitine-acylcarnitine carrier deficiency. J Inherit Metab Dis. 1999;22(3):267-270. https://doi.org/10.1023/a:1005590223680.
Costa C, Costa JM, Slama A, et al. Mutational spectrum and DNA-based prenatal diagnosis in carnitine-acylcarnitine translocase deficiency. Mol Genet Metab. 2003;78(1):68-73. https://doi.org/10.1016/s96-7192(02)00205-6.
Stanley CA. Hyperinsulinism/hyperammonemia syndrome: insights into the regulatory role of glutamate dehydrogenase in ammonia metabolism. Mol Genet Metab. 2004;81(Suppl 1):S45-S51. https://doi.org/10.1016/j.ymgme.2003.10.013.
Saheki T, Kobayashi K, Iijima M, et al. Adult-onset type II citrullinemia and idiopathic neonatal hepatitis caused by citrin deficiency: involvement of the aspartate glutamate carrier for urea synthesis and maintenance of the urea cycle. Mol Genet Metab. 2004;81(Suppl 1):S20-S26. https://doi.org/10.1016/j.ymgme.2004.01.006.
Haberle J, Chakrapani A, Ah Mew N, Longo N. Hyperammonaemia in classic organic acidaemias: a review of the literature and two case histories. Orphanet J Rare Dis. 2018;13(1):219. https://doi.org/10.1186/s13023-018-0963-7.
Soria LR, Nitzahn M, De Angelis A, et al. Hepatic glutamine synthetase augmentation enhances ammonia detoxification. J Inherit Metab Dis. 2019;42(6):1128-1135. https://doi.org/10.1002/jimd.12070.
Mahapatra S, Ananth A, Baugh N, Damian M, Enns GM. Triheptanoin: a rescue therapy for cardiogenic shock in carnitine-acylcarnitine translocase deficiency. JIMD Reports. 2018;39:19-23. https://doi.org/10.1007/8904_2017_36.
Vockley J, Charrow H, Ganesh J, et al. Triheptanoin treatment in patients with pediatric cardiomyopathy associated with long chain-fatty acid oxidation disorders. Mol Genet Metab. 2016;119(3):223-231. https://doi.org/10.1016/j.ymgme.2016.08.008.
Iacobazzi V, Invernizzi F, Baratta S, et al. Molecular and functional analysis of SLC25A20 mutations causing carnitine-acylcarnitine translocase deficiency. Hum Mutat. 2004;24(4):312-320. https://doi.org/10.1002/humu.20085.
Giudetti A, Stanca E, Siculella L, Gnoni G, Damiano F. Nutritional and hormonal regulation of citrate and carnitine/acylcarnitine transporters: two mitochondrial carriers involved in fatty acid metabolism. Int J Mol Sci. 2016;17(6):817-831. https://doi.org/10.3390/ijms17060817.
Prentki M, Corkey BE, Madiraju SRM. Lipid-associated metabolic signalling networks in pancreatic beta cell function. Diabetologia. 2019;19(10):19-4976.
Tucci S, Flogel U, Hermann S, Sturm M, Schafers M, Spiekerkoetter U. Development and pathomechanisms of cardiomyopathy in very long-chain acyl-CoA dehydrogenase deficient (VLCAD[−/−]) mice. Biochim Biophys Acta. 2014;1842(5):677-685.
Pande SV, Brivet M, Slama A, Demaugre F, Aufrant C, Saudubray JM. Carnitine-acylcarnitine translocase deficiency with severe hypoglycemia and auriculo ventricular block. Translocase assay in permeabilized fibroblasts. J Clin Invest. 1993;91(3):1247-1252. https://doi.org/10.1172/JCI116288.
Gillingham MB, Elizondo G, Behrend A, et al. Higher dietary protein intake preserves lean body mass, lowers liver lipid deposition, and maintains metabolic control in participants with long-chain fatty acid oxidation disorders. J Inherit Metab Dis. 2019;42(5):857-869. https://doi.org/10.1002/jimd.12155.
Tucci S, Herebian D, Sturm M, Seibt A, Spiekerkoetter U. Tissue-specific strategies of the very-long chain acyl-CoA dehydrogenase-deficient (VLCAD−/−) mouse to compensate a defective fatty acid beta-oxidation. PLoS One. 2012;7(9):e45429.
Morris AA, Olpin SE, Brivet M, Turnbull DM, Jones RA, Leonard JV. A patient with carnitine-acylcarnitine translocase deficiency with a mild phenotype. J Pediatr. 1998;132(3 Pt 1):514-516. https://doi.org/10.1016/s0022-3476(98)70030-7.
Iacobazzi V, Pasquali M, Singh R, et al. Response to therapy in carnitine/acylcarnitine translocase (CACT) deficiency due to a novel missense mutation. Am J Med Genet A. 2004;126A(2):150-155. https://doi.org/10.1002/ajmg.a.20573.
Korman SH, Pitt JJ, Boneh A, et al. A novel SLC25A20 splicing mutation in patients of different ethnic origin with neonatally lethal carnitine-acylcarnitine translocase (CACT) deficiency. Mol Genet Metab. 2006;89(4):332-338. https://doi.org/10.1016/j.ymgme.2006.06.009.
Vatanavicharn N, Yamada K, Aoyama Y, et al. Carnitine-acylcarnitine translocase deficiency: two neonatal cases with common splicing mutation and in vitro bezafibrate response. Brain Dev. 2015;37(7):698-703.
Fukushima T, Kaneoka H, Yasuno T, et al. Three novel mutations in the carnitine-acylcarnitine translocase (CACT) gene in patients with CACT deficiency and in healthy individuals. J Hum Genet. 2013;58(12):788-793. https://doi.org/10.1038/jhg.2013.103.
Al Aqeel AI, Rashid MS, Ruiter JP, Ijlst L, Wanders RJ. A novel molecular defect of the carnitine acylcarnitine translocase gene in a Saudi patient. Clin Genet. 2003;64(2):163-165. https://doi.org/10.1034/j.399-0004.2003.00117.x.
Bonnet D, Martin D, Pascale De L, et al. Arrhythmias and conduction defects as presenting symptoms of fatty acid oxidation disorders in children. Circulation. 1999;100(22):2248-2253. https://doi.org/10.1161/01.cir.100.22.2248.
Ogier de Baulny H, Slama A, Touati G, Turnbull DM, Pourfarzam M, Brivet M. Neonatal hyperammonemia caused by a defect of carnitine-acylcarnitine translocase. J Pediatr. 1995;127(5):723-728. https://doi.org/10.1016/s0022-3476(95)70160-5.
Khabbush A, Orford M, Tsai YC, et al. Neuronal decanoic acid oxidation is markedly lower than that of octanoic acid: a mechanistic insight into the medium-chain triglyceride ketogenic diet. Epilepsia. 2017;58(8):1423-1429. https://doi.org/10.1111/epi.13833.
Rogawski MA. A fatty acid in the MCT ketogenic diet for epilepsy treatment blocks AMPA receptors. Brain. 2016;139(Pt 2):306-309. https://doi.org/10.1093/brain/awv369.
Van Hove JL, Grunewald S, Jaeken J, et al. D,L-3-hydroxybutyrate treatment of multiple acyl-CoA dehydrogenase deficiency (MADD). Lancet (Lond, Engl). 2003;361(9367):1433-1435.
Van Rijt WJ, Heiner-Fokkema MR, du Marchie Sarvaas GJ, et al. Favorable outcome after physiologic dose of sodium-D,L-3-hydroxybutyrate in severe MADD. Pediatrics. 2014;134(4):e1224-e1228.
Gautschi M, Weisstanner C, Slotboom J, Nava E, Zürcher T, Nuoffer JM. Highly efficient ketone body treatment in multiple acyl-CoA dehydrogenase deficiency-related leukodystrophy. Pediatr Res. 2015;77(1-1):91-98. https://doi.org/10.1038/pr.2014.154.
Wang GL, Wang J, Douglas G, et al. Expanded molecular features of carnitine acyl-carnitine translocase (CACT) deficiency by comprehensive molecular analysis. Mol Genet Metab. 2011;103(4):349-357. https://doi.org/10.1016/j.ymgme.2011.05.001.
Lee RS, Lam CW, Lai CK, et al. Carnitine-acylcarnitine translocase deficiency in three neonates presenting with rapid deterioration and cardiac arrest. Hong Kong Med J. 2007;13(1):66-68.

Auteurs

Bryony Ryder (B)

Division of Clinical and Metabolic Genetics, The Hospital for Sick Children, Toronto, Ontario, Canada.
National Metabolic Service, Starship Children's Hospital, Auckland, New Zealand.

Michal Inbar-Feigenberg (M)

Division of Clinical and Metabolic Genetics, The Hospital for Sick Children, Toronto, Ontario, Canada.

Emma Glamuzina (E)

National Metabolic Service, Starship Children's Hospital, Auckland, New Zealand.

Rebecca Halligan (R)

Department of Inherited Metabolic Disorders, Birmingham Women's and Children's Hospital Foundation Trust, Birmingham, UK.
Department of Metabolic Medicine, Evelina Children's Hospital, London, UK.

Roshni Vara (R)

Department of Metabolic Medicine, Evelina Children's Hospital, London, UK.

Aoife Elliot (A)

Queensland Lifespan Metabolic Medicine Service, Queensland Children's Hospital, Brisbane, QLD, Australia.

David Coman (D)

Queensland Lifespan Metabolic Medicine Service, Queensland Children's Hospital, Brisbane, QLD, Australia.
School of Medicine University of Queensland and Griffith University, Brisbane, Queensland, Australia.

Tahlee Minto (T)

Queensland Lifespan Metabolic Medicine Service, Queensland Children's Hospital, Brisbane, QLD, Australia.

Katherine Lewis (K)

Queensland Lifespan Metabolic Medicine Service, Queensland Children's Hospital, Brisbane, QLD, Australia.

Manuel Schiff (M)

Reference Centre for Inherited Metabolic Diseases, AP-HP, Necker University Hospital, University of Paris, Paris, France.
INSERM U1163, Institut Imagine, Paris, France.

Suresh Vijay (S)

Department of Inherited Metabolic Disorders, Birmingham Women's and Children's Hospital Foundation Trust, Birmingham, UK.

Rhonda Akroyd (R)

National Metabolic Service, Starship Children's Hospital, Auckland, New Zealand.

Sue Thompson (S)

Department of Metabolic Genetics, Sydney Children's Hospitals' Network NSW, Sydney, New South Wales, Australia.
Faculty of Health and Medical Science, University of Sydney, Sydney, New South Wales, Australia.

Anita MacDonald (A)

Department of Inherited Metabolic Disorders, Birmingham Women's and Children's Hospital Foundation Trust, Birmingham, UK.

Abigail J M Woodward (AJM)

Department of Nutrition & Dietetics, Evelina London Children's Hospital, London, UK.

Joanne E L Gribben (JEL)

Department of Nutrition & Dietetics, Evelina London Children's Hospital, London, UK.

Stephanie Grunewald (S)

Metabolic Medicine Department, Great Ormond Street Hospital, Institute of Child Health University College London, NIHR Biomedical Research Centre, London, UK.

Kiran Belaramani (K)

Department of Metabolic Medicine, Hong Kong Children's Hospital, Ngau Tau Kok, Hong Kong.

Madeleine Hall (M)

Departments of Metabolic Medicine & Nutrition, Women's and Children's Hospital, North Adelaide, South Australia, Australia.

Natalie van der Haak (N)

Departments of Metabolic Medicine & Nutrition, Women's and Children's Hospital, North Adelaide, South Australia, Australia.

Beena Devanapalli (B)

Department of Metabolic Genetics, Sydney Children's Hospitals' Network NSW, Sydney, New South Wales, Australia.

Adviye Ayper Tolun (AA)

Department of Metabolic Genetics, Sydney Children's Hospitals' Network NSW, Sydney, New South Wales, Australia.

Callum Wilson (C)

National Metabolic Service, Starship Children's Hospital, Auckland, New Zealand.

Kaustuv Bhattacharya (K)

Department of Metabolic Genetics, Sydney Children's Hospitals' Network NSW, Sydney, New South Wales, Australia.
Faculty of Health and Medical Science, University of Sydney, Sydney, New South Wales, Australia.

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