Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-20T06:27:10.308Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurologic Injury in Isolated Sulfite Oxidase Deficiency

Published online by Cambridge University Press:  23 September 2014

Thomas M. Bosley ,
Ibrahim A. Alorainy ,
Darren T. Oystreck ,
Ali M. Hellani ,
Mohammed Z. Seidahmed ,
Mohamed El Faki Osman ,
Mohamed A. Sabry ,
Mohamed S. Rashed ,
Eiman A. Al-Yamani  and
Khaled K. Abu-Amero
...Show all authors
Thomas M. Bosley
Affiliation:
Department of Ophthalmology, College of Medicine, King Saud University
Ibrahim A. Alorainy
Affiliation:
Radiology, College of Medicine, King Saud University
Darren T. Oystreck
Affiliation:
Department of Ophthalmology, College of Medicine, King Saud University Department of Ophthalmology, College of Medicine, University of Florida, Jacksonville, USA
Ali M. Hellani
Affiliation:
Division of Ophthalmology, Faculty of Health Sciences, University of Stellenbosch, Tygerberg, South Africa
Mohammed Z. Seidahmed
Affiliation:
Department of Genetics, King Faisal Specialist Hospital and Research Centre, Riyadh
Mohamed El Faki Osman
Affiliation:
Pediatrics, College of Medicine, King Saud University
Mohamed A. Sabry
Affiliation:
PGD Laboratory, Saad Medical Center, al Khobar, Saudi Arabia
Mohamed S. Rashed
Affiliation:
PGD Laboratory, Saad Medical Center, al Khobar, Saudi Arabia
Khaled K. Abu-Amero*
Affiliation:
Department of Ophthalmology, College of Medicine, King Saud University
Mustafa A. Salih
Affiliation:
Pediatrics, College of Medicine, King Saud University
*
Department of Ophthalmology, College of Medicine, King Saud University, Riyadh, Saudi Arabia. Email: abuamero@gmail.com.
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Background:

We review clinical, neuroimaging, and genetic information on six individuals with isolated sulfite oxidase deficiency (ISOD).

Methods:

All patients were examined, and clinical records, biochemistry, neuroimaging, and sulfite oxidase gene (SUOX) sequencing were reviewed.

Results:

Data was available on six individuals from four nuclear families affected by ISOD. Each individual began to seize within the first week of life. neurologic development was arrested at brainstem reflexes, and severe microcephaly developed rapidly. neuroimaging within days of birth revealed hypoplasia of the cerebellum and corpus callosum and damage to the supratentorial brain looking like severe hypoxic-ischemic injury that evolved into cystic hemispheric white matter changes. Affected individuals all had elevated urinary S-sulfocysteine and normal urinary xanthine and hypoxanthine levels diagnostic of ISOD. Genetic studies confirmed SUOX mutations in four patients.

Conclusions:

ISOD impairs systemic sulfite metabolism, and yet this genetic disease affects only the brain with damage that is commonly confused with the clinical and radiologic features of severe hypoxic-ischemic encephalopathy.

Résumé

RÉSUMÉ

Lésions neurologiques dans le déficit isolé en sulfite oxydase.

Contexte:

Nous avons revu l'information clinique, de neuroimagerie et génétique de 6 individus atteints d'un déficit isolé en sulfite oxydase (DISD).

Méthode:

Tous les patients ont été examinés et leurs dossiers ont été revus, incluant la biochimie, la neuroimagerie et le séquençage du gène de la sulfite oxydase (SUOX).

Résultats:

Les données de 6 individus, faisant partie de 4 familles nucléaires différentes, atteintes de SUOX, étaient disponibles. Chaque individu a commencé à présenter des crises convulsives au cours de la première semaine de vie. Le développement neurologique était limité à la présence de réflexes du tronc cérébral et une microcéphalie sévère s'installait rapidement. La neuroimagerie effectuée dans les premiers jours après la naissance a montré une hypoplasie du cervelet et du corps calleux et des dommages sus-tentofiels ressemblant à une lésion hypoxique-ischémique sévère qui évoluait vers des changements d'aspect kystique de la substance blanche hémisphérique. Les individus atteints avaient tous un taux urinaire élevé de S-sulfocystéine et un taux urinaire normal de xanthine et d'hypoxanthine, caractéristiques du DISD. Les études génétiques ont confirmé une mutation de SUOX chez 4 patients.

Conclusions:

Le DISD perturbe le métabolisme systémique du sulfite et pourtant cette maladie génétique n'atteint que le cerveau. Le dommage à ce niveau est souvent confondu avec les manifestations cliniques et radiologiques d'une encéphalopathie hypoxique-ischémique sévère.

Type
Original Articles
Information
Canadian Journal of Neurological Sciences , Volume 41 , Issue 1 , January 2014 , pp. 42 - 48
Copyright
Copyright © The Canadian Journal of Neurological 2014

References

1. Rosenblum, WI. Neuropathologic changes in a case of sulfite oxidase deficiency. Neurology. 1968 Dec; 18 (12): 1187–96.CrossRefGoogle Scholar
2. Barbot, C, Martins, E, Vilarinho, L, Dorche, C, Cardoso, ML. A mild form of infantile isolated sulphite oxidase deficiency. Neuropediatrics. 1995 Dec; 26 (6): 322–4.CrossRefGoogle Scholar
3. Touati, G, Rusthoven, E, Depondt, E, et al. Dietary therapy in two patients with a mild form of sulphite oxidase deficiency. Evidence for clinical and biological improvement. J Inherit Metab Dis. 2000 Feb; 23 (1): 45–53.CrossRefGoogle ScholarPubMed
4. Sass, JO, Gunduz, A, Araujo Rodrigues Funayama, C, et al. Functional deficiencies of sulfite oxidase: Differential diagnoses in neonates presenting with intractable seizures and cystic encephalomalacia. Brain Dev. 2010 Aug; 32 (7): 544–9.CrossRefGoogle ScholarPubMed
5. Reiss, J, Johnson, JL. Mutations in the molybdenum cofactor biosynthetic genes MOCS1, MOCS2, and GEPH. Hum Mutat. 2003 Jun; 21 (6): 569–76.CrossRefGoogle ScholarPubMed
6. Mudd, SH, Irreverre, F, Laster, L. Sulfite oxidase deficiency in man: demonstration of the enzymatic defect. Science. 1967 Jun 23; 156 (3782): 1599–602.CrossRefGoogle ScholarPubMed
7. Rupar, CA, Gillett, J, Gordon, BA, et al. Isolated sulfite oxidase deficiency. Neuropediatrics. 1996 Dec; 27 (6): 299–304.CrossRefGoogle ScholarPubMed
8. Rashed, MS, Saadallah, AA, Rahbeeni, Z, et al. Determination of urinary S-sulphocysteine, xanthine and hypoxanthine by liquid chromatography-electrospray tandem mass spectrometry. Biomed Chromatogr. 2005 Apr; 19 (3): 223–30.CrossRefGoogle ScholarPubMed
9. Seidahmed, MZ, Alyamani, EA, Rashed, MS, et al. Total truncation of the molybdo-pterin/dimerization domains of SUOX protein in an Arab family with isolated sulfite oxidase deficiency. Am J Med Genet A. 2005 Jul 15; 136 (2): 205–9.CrossRefGoogle Scholar
10. Salih, MA, Bosley, TM, Alorainy, IA, et al. Preimplantation genetic diagnosis in isolated sulfite oxidase deficiency. Can J Neurol Sci. 2013 Jan; 40 (1): 109–12.CrossRefGoogle ScholarPubMed
11. Eyaid, WM, Al-Nouri, DM, Rashed, MS, Al-Rifai, MT, Al-Wakeel, AS. An inborn error of metabolism presenting as hypoxic-ischemic insult. Pediatr Neurol. 2005 Feb; 32 (2): 134–6.CrossRefGoogle ScholarPubMed
12. Sass, JO. Laboratory diagnosis of sulphite oxidase deficiency. Eur J Pediatr. 2006 Oct; 165 (10): 739; author reply 40.CrossRefGoogle ScholarPubMed
13. Edwards, MC, Johnson, JL, Marriage, B, et al. Isolated sulfite oxidase deficiency: review of two cases in one family. Ophthalmology. 1999 Oct; 106 (10): 1957–61.CrossRefGoogle ScholarPubMed
14. Enns, GM. Inborn Errors of Metabolism Masquerading as Hypoxic-Ischemic Encephalopathy. NeoReviews. 2005; 6: e549–e57.CrossRefGoogle Scholar
15. Haider, N, Salih, MA, Al-Rasheed, S, Al-Mofada, S, Krahn, PM, Kabiraj, M. Nonketotic hyperglycinemia: A life-threatening disorder in Saudi newborns. Ann Saudi Med. 1996 Jul; 16 (4): 400–4.CrossRefGoogle ScholarPubMed
16. Salih, MAM, Kabiraj, M, Gascon, GG, Al Jarallah, AS, Al Zamil, FA. Typical and atypical presentations of pyridoxine-dependent seizures. Saudi Medical J. 1995; 16: 347–51.Google Scholar
17. Salih, MA, Abdel-Gader, AG, Zahraa, JN, et al. Stroke due to mitochondrial disorders in Saudi children. Saudi Med J. 2006 Mar; 27 Suppl 1: S81–90.Google ScholarPubMed
18. Mohamed, S. Recognition and diagnostic approach to acute metabolic disorders in the neonatal period. Sudan J Paediatr. 2011; 11: 20–8.Google ScholarPubMed
19. Dublin, AB, Hald, JK, Wootton-Gorges, SL. Isolated sulfite oxidase deficiency: MR imaging features. AJNR Am J Neuroradiol. 2002 Mar; 23 (3): 484–5.Google ScholarPubMed
20. Hoffmann, C, Ben-Zeev, B, Anikster, Y, et al. Magnetic resonance imaging and magnetic resonance spectroscopy in isolated sulfite oxidase deficiency. J Child Neurol. 2007 Oct; 22 (10): 1214–21.CrossRefGoogle ScholarPubMed
21. Hobson, EE, Thomas, S, Crofton, PM, Murray, AD, Dean, JC, Lloyd, D. Isolated sulphite oxidase deficiency mimics the features of hypoxic ischaemic encephalopathy. Eur J Pediatr. 2005 Nov; 164 (11): 655–9.CrossRefGoogle ScholarPubMed
22. Brown, GK, Scholem, RD, Croll, HB, Wraith, JE, McGill, JJ. Sulfite oxidase deficiency: clinical, neuroradiologic, and biochemical features in two new patients. Neurology. 1989 Feb; 39 (2 Pt 1): 252–7.CrossRefGoogle ScholarPubMed
23. Per, H, Gumus, H, Ichida, K, Caglayan, O, Kumandas, S. Molybdenum cofactor deficiency: clinical features in a Turkish patient. Brain Dev. 2007 Jul; 29 (6): 365–8.CrossRefGoogle Scholar
24. Olsen, WO, Noffsinger, D, Carhart, R. Masking level differences encountered in clinical populations. Audiology. 1976 Jul–Aug; 15 (4): 287–301.CrossRefGoogle ScholarPubMed
25. Bofill, M, Borthwick, NJ, Simmonds, HA. Novel mechanism for the impairment of cell proliferation in HIV-1 infection. Immunol Today. 1999 Jun; 20 (6): 258–61.CrossRefGoogle ScholarPubMed
26. Hong, YC, Lee, JT, Kim, H, Kwon, HJ. Air pollution: a new risk factor in ischemic stroke mortality. Stroke. 2002 Sep; 33 (9): 2165–9.Google Scholar
27. Sang, N, Yun, Y, Yao, GY, Li, HY, Guo, L, Li, GK. SO(2)-induced neurotoxicity is mediated by cyclooxygenases-2-derived prostaglandin E(2) and its downstream signaling pathway in rat hippocampal neurons. Toxicol Sci. 2011 Dec; 124 (2): 400–13.CrossRefGoogle Scholar
28. Sharma, DR, Sunkaria, A, Bal, A, et al. Neurobehavioral impairments, generation of oxidative stress and release of proapoptotic factors after chronic exposure to sulphur mustard in mouse brain. Toxicol Appl Pharmacol. 2009 Oct 15; 240 (2): 208–18.CrossRefGoogle ScholarPubMed
29. Morrison, JP, Ton, TV, Collins, JB, et al. Gene expression studies reveal that DNA damage, vascular perturbation, and inflammation contribute to the pathogenesis of carbonyl sulfide neurotoxicity. Toxicol Pathol. 2009 Jun; 37 (4): 502–11.CrossRefGoogle Scholar
30. Chen-Plotkin, AS, Vossel, KA, Samuels, MA, Chen, MH. Encephalopathy, stroke, and myocardial infarction with DMSO use in stem cell transplantation. Neurology. 2007 Mar 13; 68 (11): 859–61.CrossRefGoogle ScholarPubMed
31. Zhang, X, Vincent, AS, Halliwell, B, Wong, KP. A mechanism of sulfite neurotoxicity: direct inhibition of glutamate dehydrogenase. J Biol Chem. 2004 Oct 8; 279 (41): 43035–45.CrossRefGoogle ScholarPubMed
32. van Gennip, AH, de Abreu, RA, van Lenthe, H, et al. Dihydropyrimidinase deficiency: confirmation of the enzyme defect in dihydropyrimidinuria. J Inherit Metab Dis. 1997 Jul; 20 (3): 339–42.CrossRefGoogle ScholarPubMed
33. Van Kuilenburg, AB, Van Lenthe, H, Wanders, RJ, Van Gennip, AH. Subcellular localization of dihydropyrimidine dehydrogenase. Biol Chem. 1997 Sep; 378 (9): 1047–53.CrossRefGoogle ScholarPubMed
34. Volpe, JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009 Jan; 8 (1): 110–24.CrossRefGoogle ScholarPubMed
35. Olney, JW, Misra, CH, de Gubareff, T. Cysteine-S-sulfate: brain damaging metabolite in sulfite oxidase deficiency. J Neuropathol Exp Neurol. 1975 Mar; 34 (2): 167–77.CrossRefGoogle ScholarPubMed
36. Matute, C, Domercq, M, Sanchez-Gomez, MV. Glutamate-mediated glial injury: mechanisms and clinical importance. Glia. 2006 Jan 15; 53 (2): 212–24.CrossRefGoogle ScholarPubMed
37. Shroff, MM, Soares-Fernandes, JP, Whyte, H, Raybaud, C. MR imaging for diagnostic evaluation of encephalopathy in the newborn. Radiographics. 2010 May; 30 (3): 763–80.CrossRefGoogle ScholarPubMed
38. Lueder, GT, Steiner, RD. Ophthalmic abnormalities in molybdenum cofactor deficiency and isolated sulfite oxidase deficiency. J Pediatr Ophthalmol Strabismus. 1995 Sep–Oct; 32 (5): 334–7.CrossRefGoogle ScholarPubMed
39. Vally, H, Misso, NL, Madan, V. Clinical effects of sulphite additives. Clin Exp Allergy. 2009 Nov; 39 (11): 1643–51.CrossRefGoogle ScholarPubMed
40. Barrero, AF, Herrador, MM, Quilez, JF, et al. Bioactive sesquiterpenes from Santolina rosmarinifolia subsp. Canescens. A conformational analysis of the germacrane ring. Phytochemistry. 1999 Jun; 51 (4): 529–41.CrossRefGoogle ScholarPubMed
41. Shi, X. Generation of SO3.- and OH radicals in SO3(2-) reactions with inorganic environmental pollutants and its implications to SO3(2-) toxicity. J Inorg Biochem. 1994 Nov 15; 56 (3): 155–65.CrossRefGoogle ScholarPubMed
42. Follett, PL, Deng, W, Dai, W, et al. Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci. 2004 May 5; 24 (18): 4412–20.CrossRefGoogle ScholarPubMed
43. Frade, J, Pope, S, Schmidt, M, et al. Glutamate induces release of glutathione from cultured rat astrocytes–a possible neuroprotective mechanism? J Neurochem. 2008 May; 105 (4): 1144–52.CrossRefGoogle ScholarPubMed
44. Puka-Sundvall, M, Eriksson, P, Nilsson, M, Sandberg, M, Lehmann, A. Neurotoxicity of cysteine: interaction with glutamate. Brain Res. 1995 Dec 24; 705 (1–2): 65–70.CrossRefGoogle ScholarPubMed
45. Birdsall, TC. Therapeutic applications of taurine. Altern Med Rev. 1998 Apr; 3 (2): 128–36.Google ScholarPubMed