Improved sensitivity and specificity for citrin deficiency using selected amino acids and acylcarnitines in the newborn screening.

NICCD arginine citrin deficiency citrulline free carnitine newborn screening tyrosine

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:
08 Sep 2023
Historique:
revised: 27 07 2023
received: 22 05 2023
accepted: 18 08 2023
pubmed: 8 9 2023
medline: 8 9 2023
entrez: 8 9 2023
Statut: aheadofprint

Résumé

Citrin deficiency is an autosomal recessive disorder caused by a defect of citrin resulting from mutations in the SLC25A13 gene. Intrahepatic cholestasis and various metabolic abnormalities, including hypoglycemia, galactosemia, citrullinemia, and hyperammonemia may be present in neonates or infants in the "neonatal intrahepatic cholestasis caused by citrin deficiency" (NICCD) form of the disease. Because at present, newborn screening (NBS) for citrin deficiency using citrulline levels in dried blood spots (DBS) can only detect some of the patients, we tried to develop a new evaluation system to more reliably detect newborns with citrin deficiency utilizing parameters already in place in present NBS methods. To achieve this goal, we re-analyzed NBS profiles of amino acids and acylcarnitines in 96 NICCD patients, who were diagnosed through selective screening or positive family history. Hereby, we identified the combined evaluation of arginine (Arg), citrulline (Cit), isoleucine+leucine (Ile + Leu), tyrosine (Tyr), free carnitine (C0) / glutarylcarnitine (C5-DC) ratio in DBS as potentially sensitive to diagnose citrin deficiency in pre-symptomatic newborns. In particular, a scoring system using threshold levels for Arg (≥9 μmol/L), Cit (≥ 39 μmol/L), Ile + Leu (≥ 99 μmol/L), Tyr (≥ 96 μmol/L) and C0/C5-DC ratio (≥327) was significantly effective to detect newborns who later developed NICCD, and could thus be implemented in existing NBS programs at no extra analytical costs whenever citrin deficiency is considered to become a novel target disease.

Identifiants

pubmed: 37681292
doi: 10.1002/jimd.12673
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Swiss National Science Foundation
ID : 320030_207965
Pays : Switzerland

Informations de copyright

© 2023 SSIEM.

Références

Kobayashi K, Sinasac DS, Iijima M, et al. The gene mutated in adult-onset type II citrullinaemia encodes a putative mitochondrial carrier protein. Nat Genet. 1999;22(2):159-163. doi:10.1038/9667
Ohura T, Kobayashi K, Tazawa Y, et al. Neonatal presentation of adult-onset type II citrullinemia. Hum Genet. 2001;108(2):87-90. doi:10.1007/s004390000448
Tazawa Y, Kobayashi K, Ohura T, et al. Infantile cholestatic jaundice associated with adult-onset type II citrullinemia. J Pediatr. 2001;138(5):735-740. doi:10.1067/mpd.2001.113264
Song Y-Z, Deng M, Chen F-P, et al. Genotypic and phenotypic features of citrin deficiency: five-year experience in a Chinese pediatric center. Int J Mol Med. 2011;28(1):33-40. doi:10.3892/ijmm.2011.653
Ikeda S, Yazaki M, Takei Y, et al. Type II (adult onset) citrullinaemia: clinical pictures and the therapeutic effect of liver transplantation. J Neurol Neurosurg Psychiatry. 2001;71(5):663-670. doi:10.1136/jnnp.71.5.663
Pinto A, Ashmore C, Batzios S, et al. Dietary management, clinical status and outcome of patients with citrin deficiency in the UK. Nutrients. 2020;12(11):3313. doi:10.3390/nu12113313
Kobayashi K, Lu YB, Li MX, et al. Screening of nine SLC25A13 mutations: their frequency in patients with citrin deficiency and high carrier rates in Asian populations. Mol Genet Metab. 2003;80(3):356-359. doi:10.1016/S1096-7192(03)00140-9
Lu YB, Kobayashi K, Ushikai M, et al. Frequency and distribution in East Asia of 12 mutations identified in the SLC25A13 gene of Japanese patients with citrin deficiency. J Hum Genet. 2005;50(7):338-346. doi:10.1007/s10038-005-0262-8
Dimmock D, Maranda B, Dionisi-Vici C, et al. Citrin deficiency, a perplexing global disorder. Mol Genet Metab. 2009;96(1):44-49. doi:10.1016/j.ymgme.2008.10.007
Saritaş Nakip Ö, Yıldız Y, Tokatlı A. Retrospective evaluation of 85 patients with urea cycle disorders: one center experience, three new mutations. J Pediatr Endocrinol Metab. 2020;33(6):721-728. doi:10.1515/jpem-2019-0413
Fernández Tomé L, Stark Aroeira LG, Muñoz Bartolo G, et al. Citrin deficiency: early severe cases in a European country. Clin Res Hepatol Gastroenterol. 2021;45(4):101595. doi:10.1016/j.clinre.2020.101595
Kido J, Häberle J, Sugawara K, et al. Clinical manifestation and long-term outcome of citrin deficiency: report from a nationwide study in Japan. J Inherit Metab Dis. 2022;45(3):431-444. doi:10.1002/jimd.12483
Shigetomi H, Tanaka T, Nagao M, Tsutsumi H. Early detection and diagnosis of neonatal intrahepatic cholestasis caused by citrin deficiency missed by newborn screening using tandem mass spectrometry. Int J Neonatal Screen. 2018;4(1):5. doi:10.3390/ijns4010005
Zhang R, Qiang R, Song C, et al. Spectrum analysis of inborn errors of metabolism for expanded newborn screening in a northwestern Chinese population. Sci Rep. 2021;11(1):2699. doi:10.1038/s41598-021-81897-y
Tabata A, Sheng J-S, Ushikai M, et al. Identification of 13 novel mutations including a retrotransposal insertion in SLC25A13 gene and frequency of 30 mutations found in patients with citrin deficiency. J Hum Genet. 2008;53(6):534-545. doi:10.1007/s10038-008-0282-2
Kido J, Inoue H, Shimotsu H, et al. Effect of L-carnitine on amino acid metabolism in elderly patients undergoing regular hemodialysis. Blood Purif. 2020;49(5):614-621. doi:10.1159/000505609
Shigematsu Y, Hirano S, Hata I, et al. Newborn mass screening and selective screening using electrospray tandem mass spectrometry in Japan. J Chromatogr B Analyt Technol Biomed Life Sci. 2002;776(1):39-48. doi:10.1016/s1570-0232(02)00077-6
Song Y-Z, Li B-X, Chen F-P, et al. Neonatal intrahepatic cholestasis caused by citrin deficiency: clinical and laboratory investigation of 13 subjects in mainland of China. Dig Liver Dis. 2009;41(9):683-689. doi:10.1016/j.dld.2008.11.014
Treepongkaruna S, Jitraruch S, Kodcharin P, et al. Neonatal intrahepatic cholestasis caused by citrin deficiency: prevalence and SLC25A13 mutations among Thai infants. BMC Gastroenterol. 2012;12:141. doi:10.1186/1471-230X-12-141
Oh SH, Lee BH, Kim G-H, Choi J-H, Kim KM, Yoo H-W. Biochemical and molecular characteristics of citrin deficiency in Korean children. J Hum Genet. 2017;62(2):305-307. doi:10.1038/jhg.2016.131
Hayasaka K, Numakura C, Yamakawa M, et al. Medium-chain triglycerides supplement therapy with a low-carbohydrate formula can supply energy and enhance ammonia detoxification in the hepatocytes of patients with adult-onset type II citrullinemia. J Inherit Metab Dis. 2018;41(5):777-784. doi:10.1007/s10545-018-0176-1
Saheki T, Kobayashi K. Mitochondrial aspartate glutamate carrier (citrin) deficiency as the cause of adult-onset type II citrullinemia (CTLN2) and idiopathic neonatal hepatitis (NICCD). J Hum Genet. 2002;47(7):333-341. doi:10.1007/s100380200046
Holecek M, Kandar R, Sispera L, Kovarik M. Acute hyperammonemia activates branched-chain amino acid catabolism and decreases their extracellular concentrations: different sensitivity of red and white muscle. Amino Acids. 2011;40(2):575-584. doi:10.1007/s00726-010-0679-z
Nawabi MD, Block KP, Chakrabarti MC, Buse MG. Administration of endotoxin, tumor necrosis factor, or interleukin 1 to rats activates skeletal muscle branched-chain alpha-keto acid dehydrogenase. J Clin Invest. 1990;85(1):256-263. doi:10.1172/JCI114421
Holecek M, Sprongl L, Tilser I. Metabolism of branched-chain amino acids in starved rats: the role of hepatic tissue. Physiol Res. 2001;50(1):25-33. PMID:11300224.
Holecek M. The BCAA-BCKA cycle: its relation to alanine and glutamine synthesis and protein balance. Nutrition. 2001;17(1):70. doi:10.1016/s0899-9007(00)00483-4
Komatsu M, Kimura T, Yazaki M, et al. Steatogenesis in adult-onset type II citrullinemia is associated with down-regulation of PPARα. Biochim Biophys Acta. 2015;1852(3):473-481. doi:10.1016/j.bbadis.2014.12.011
Wada Y, Arai-Ichinoi N, Kikuchi A, Sakamoto O, Kure S. Hypoketotic hypoglycemia in citrin deficiency: a case report. BMC Pediatr. 2020;20(1):444. doi:10.1186/s12887-020-02349-6
Song YZ, Yazaki M, Saheki T. Citrin deficiency. Human Pathobiochemistry: From Clinical Studies to Molecular Mechanisms. Springer; 2019:3-14.
Wang L-Y, Chen N-I, Chen P-W, et al. Newborn screening for citrin deficiency and carnitine uptake defect using second-tier molecular tests. BMC Med Genet. 2013;14:24. doi:10.1186/1471-2350-14-24
Lin Y, Zheng Q, Zheng T, Zheng Z, Lin W, Fu Q. Expanded newborn screening for inherited metabolic disorders and genetic characteristics in a southern Chinese population. Clin Chim Acta. 2019;494:106-111. doi:10.1016/j.cca.2019.03.1622
Wang T, Ma J, Zhang Q, et al. Expanded newborn screening for inborn errors of metabolism by tandem mass spectrometry in Suzhou, China: disease Spectrum, prevalence, genetic characteristics in a Chinese population. Front Genet. 2019;10:1052. doi:10.3389/fgene.2019.01052
Li X, He J, He L, et al. Spectrum analysis of inherited metabolic disorders for expanded newborn screening in a central Chinese population. Front Genet. 2022;12:763222. doi:10.3389/fgene.2021.763222
Lin Y, Liu Y, Zhu L, et al. Combining newborn metabolic and genetic screening for neonatal intrahepatic cholestasis caused by citrin deficiency. J Inherit Metab Dis. 2020;43(3):467-477. doi:10.1002/jimd.12206
Chen HA, Hsu RH, Chen YH, et al. Improved diagnosis of citrin deficiency by newborn screening using a molecular second-tier test. Mol Genet Metab. 2022;136(4):330-336. doi:10.1016/j.ymgme.2022.06.007
Chen CY, Chang MH, Chen HL, Chien YH, Wu JF. The prognosis of citrin deficiency differs between early-identified newborn and later-onset symptomatic infants. Pediatr Res. 2023;94(3):1151-1157. doi:10.1038/s41390-023-02585-3

Auteurs

Jun Kido (J)

Department of Pediatrics, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan.
Department of Pediatrics, Kumamoto University Hospital, Kumamoto, Japan.
University Children's Hospital Zurich and Children's Research Centre, Zurich, Switzerland.

Johannes Häberle (J)

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

Toju Tanaka (T)

Department of Pediatrics, National Hospital Organization Hokkaido Medical Center, Sapporo, Japan.

Masayoshi Nagao (M)

Department of Pediatrics, National Hospital Organization Hokkaido Medical Center, Sapporo, Japan.

Yoichi Wada (Y)

Department of Pediatrics, Tohoku University School of Medicine, Sendai, Japan.

Chikahiko Numakura (C)

Department of Pediatrics, Yamagata University School of Medicine, Yamagata, Japan.

Ryosuke Bo (R)

Department of Pediatrics, Kobe University Graduate School of Medicine, Kobe, Japan.

Hiromi Nyuzuki (H)

Department of Pediatrics, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

Sumito Dateki (S)

Department of Pediatrics, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan.

Shinsuke Maruyama (S)

Department of Pediatrics, Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima, Japan.

Kei Murayama (K)

Department of Metabolism, Center for Medical Genetics, Chiba Children's Hospital, Chiba, Japan.

Shinichiro Yoshida (S)

Newborn Screening Center, KM Biologics Co., Ltd, Kumamoto, Japan.

Kimitoshi Nakamura (K)

Department of Pediatrics, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan.
Department of Pediatrics, Kumamoto University Hospital, Kumamoto, Japan.

Classifications MeSH