Niemann–Pick type C: focus on the adolescent/adult onset form

References

• Carstea ED, Morris JA, Coleman KG, et al. Niemann–Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997;277(5323):228–31.
   PubMed Web of Science ®Google Scholar
• Naureckiene S, Sleat DE, Lackland H, et al. Identification of HE1 as the second gene of Niemann–Pick C disease. Science 2000;290(5500):2298–301.
   PubMed Web of Science ®Google Scholar
• Patterson MC, Hendriksz CJ, Walterfang M, et al. Recommendations for the diagnosis and management of Niemann–Pick disease type C: an update. Mol Genet Metab 2012;106(3):330–44.
   PubMed Web of Science ®Google Scholar
• Sevin M, Lesca G, Baumann N, et al. The adult form of Niemann–Pick disease type C. Brain 2007;130(Pt 1):120–33.
   PubMed Web of Science ®Google Scholar
• Vanier MT, Duthel S, Rodriguez-Lafrasse C, et al. Genetic heterogeneity in Niemann–Pick C disease: a study using somatic cell hybridization and linkage analysis. Am J Hum Genet 1996;58(1):118–25.
   PubMed Web of Science ®Google Scholar
• Wraith JE, Guffon N, Rohrbach M, et al. Natural history of Niemann–Pick disease type C in a multicentre observational retrospective cohort study. Mol Genet Metab 2009;98(3):250–4.
   PubMed Web of Science ®Google Scholar
• Group N-CGW, Wraith JE, Baumgartner MR, et al. Recommendations on the diagnosis and management of Niemann–Pick disease type C. Mol Genet Metab 2009;98(1–2):152–65.
   PubMed Web of Science ®Google Scholar
• Vanier MT. Niemann–Pick disease type C. Orphanet J Rare Dis 2010;5:16.
   PubMed Web of Science ®Google Scholar
• Patterson MC, Mengel E, Wijburg FA, et al. Disease and patient characteristics in NP-C patients: findings from an international disease registry. Orphanet J Rare Dis 2013;8:12.
   PubMed Web of Science ®Google Scholar
• Jahnova H, Dvorakova L, Vlaskova H, et al. Observational, retrospective study of a large cohort of patients with Niemann-Pick disease type C in the Czech Republic: a surprisingly stable diagnostic rate spanning almost 40 years. Orphanet J Rare Dis 2014;9(1):140.
   PubMed Web of Science ®Google Scholar
• Wenger DA, Barth G, Githens JH. Nine cases of sphingomyelin lipidosis, a new variant in Spanish–American Children. Juvenile variant of Niemann–Pick disease with foamy and sea-blue histiocytes. Am J Dis Child 1977;131(9):955–61.
   PubMedGoogle Scholar
• Winsor EJ, Welch JP. Genetic and demographic aspects of Nova Scotia Niemann–Pick disease (type D). Am J Hum Genet 1978;30(5):530–8.
   PubMed Web of Science ®Google Scholar
• Maubert A, Hanon C, Metton JP. [Adult onset Niemann-Pick type C disease and psychosis: literature review]. L'Encephale 2013;39(5):315–9.
   PubMed Web of Science ®Google Scholar
• Bonnot O, Klunemann HH, Sedel F, et al. Diagnostic and treatment implications of psychosis secondary to treatable metabolic disorders in adults: a systematic review. Orphanet J Rare Dis 2014;9:65.
   PubMed Web of Science ®Google Scholar
• Klunemann HH, Santosh PJ, Sedel F. Treatable metabolic psychosis that go undetecd: what Niemann Pick type C can teach us. Int J Psychiatry Clin Pract 2012;16:1–8.
   PubMed Web of Science ®Google Scholar
• Wassif CA, Cross JL, Iben J, et al. High incidence of unrecognized visceral/neurological late-onset Niemann–Pick disease, type C1, predicted by analysis of massively parallel sequencing data sets. Genet Med 2015;18:41–7
   PubMed Web of Science ®Google Scholar
• Davies JP, Ioannou YA. Topological analysis of Niemann–Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein. J Biol Chem 2000;275(32):24367–74.
   PubMed Web of Science ®Google Scholar
• Ioannou YA. The structure and function of the Niemann–Pick C1 protein. Mol Genet Metab 2000;71(1–2):175–81.
   PubMed Web of Science ®Google Scholar
• Liscum L, Sturley SL. Intracellular trafficking of Niemann-Pick C proteins 1 and 2: obligate components of subcellular lipid transport. Biochim Biophys Acta 2004;1685(1–3):22–7.
   PubMed Web of Science ®Google Scholar
• Kwon HJ, Abi-Mosleh L, Wang ML, et al. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 2009;137(7):1213–24.
   PubMed Web of Science ®Google Scholar
• Sleat DE, Wiseman JA, El-Banna M, et al. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc Natl Acad Sci U S A 2004;101(16):5886–91.
   PubMed Web of Science ®Google Scholar
• Bu B, Li J, Davies P, et al. Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann–Pick type C murine model. J Neurosci 2002;22(15):6515–25.
   PubMed Web of Science ®Google Scholar
• Sturley SL, Patterson MC, Balch W, et al. The pathophysiology and mechanisms of NP-C disease. Biochim Biophys Acta 2004;1685(1-3):83–7.
   PubMed Web of Science ®Google Scholar
• Walkley SU. Cellular pathology of lysosomal storage disorders. Brain Pathol 1998;8(1):175–93.
   PubMed Web of Science ®Google Scholar
• Suzuki K, Parker CC, Pentchev PG, et al. Neurofibrillary tangles in Niemann–Pick disease type C. Acta Neuropathol 1995;89(3):227–38.
   PubMed Web of Science ®Google Scholar
• Love S, Bridges LR, Case CP. Neurofibrillary tangles in Niemann–Pick disease type C. Brain 1995;118(Pt 1):119–29.
   PubMed Web of Science ®Google Scholar
• Williams DR. Tauopathies. Classification and clinical update on neurodegenerative diseases associated with microtubule-associated protein tau. Intern Med J 2006;36(10):652–60.
   PubMed Web of Science ®Google Scholar
• Mattsson N, Zetterberg H, Bianconi S, et al. Gamma-secretase-dependent amyloid-beta is increased in Niemann-Pick type C: a cross-sectional study. Neurology 2011;76(4):366–72.
   PubMed Web of Science ®Google Scholar
• Manganelli F, Dubbioso R, Iodice R, et al. Central cholinergic dysfunction in the adult form of Niemann–Pick disease type C: a further link with Alzheimer's disease? J Neurol 2014;261(4):804–8.
   PubMed Web of Science ®Google Scholar
• Walterfang M, Fietz M, Fahey M, et al. The neuropsychiatry of Niemann–Pick type C disease in adulthood. J Neuropsychiatry Clin Neurosci 2006;18(2):158–70.
   PubMed Web of Science ®Google Scholar
• Webber D, Klünemann HH. Psychiatric manifestations of Niemann-Pick disease. J Inherit Metab Dis 2011;4(1):25–31.
   Google Scholar
• Imrie J, Galani C, Gairy K, et al. Cost of illness associated with Niemann-Pick disease type C in the UK. J Med Econ 2009;12(3):219–29.
   PubMedGoogle Scholar
• Imrie J, Vijayaraghaven S, Whitehouse C, et al. Niemann-Pick disease type C in adults. J Inherit Metab Dis 2002;25(6):491–500.
   PubMed Web of Science ®Google Scholar
• Anheim M, Lagha-Boukbiza O, Fleury-Lesaunier MC, et al. Heterogeneity and frequency of movement disorders in juvenile and adult-onset Niemann–Pick C disease. J Neurol 2014;261(1):174–9.
   PubMed Web of Science ®Google Scholar
• Trendelenburg G, Vanier MT, Maza S, et al. Niemann-Pick type C disease in a 68-year-old patient. J Neurol Neurosurg Psychiatry 2006;77(8):997–8.
   PubMed Web of Science ®Google Scholar
• Wherret JR, Rewcastle NB. Adult neurovisceral lipidosis. Clin Res 1969;17:665 (Abstract).
   Google Scholar
• Campo JV, Stowe R, Slomka G, et al. Psychosis as a presentation of physical disease in adolescence: a case of Niemann–Pick disease, type C. Dev Med Child Neurol 1998;40(2):126–9.
   PubMed Web of Science ®Google Scholar
• Shulman LM, David NJ, Weiner WJ. Psychosis as the initial manifestation of adult-onset Niemann–Pick disease type C. Neurology 1995;45(9):1739–43.
   PubMed Web of Science ®Google Scholar
• Josephs KA, Van Gerpen MW, Van Gerpen JA. Adult onset Niemann–Pick disease type C presenting with psychosis. J Neurol Neurosurg Psychiatry 2003;74(4):528–9.
   PubMed Web of Science ®Google Scholar
• Sandu S, Jackowski-Dohrmann S, Ladner A, et al. Niemann–Pick disease type C1 presenting with psychosis in an adolescent male. Eur Child Adolesc Psychiatry 2009;18(9):583–5.
   PubMed Web of Science ®Google Scholar
• Sedel F. [Clinical diagnosis of the adult form of Niemann–Pick type C disease]. Arch Pediatr 2010;17(suppl 2):S50–3.
   PubMed Web of Science ®Google Scholar
• Klarner B, Klunemann HH, Lurding R, et al. Neuropsychological profile of adult patients with Niemann–Pick C1 (NPC1) mutations. J Inherit Metab Dis 2007;30(1):60–7.
   PubMed Web of Science ®Google Scholar
• Bauer P, Balding DJ, Klunemann HH, et al. Genetic screening for Niemann–Pick disease type C in adults with neurological and psychiatric symptoms: findings from the ZOOM study. Hum Mol Genet 2013;22(21):4349–56.
   PubMed Web of Science ®Google Scholar
• Kheder A, Scott C, Olpin S, et al. Niemann–Pick type C: a potentially treatable disorder? Pract Neurol 2013;13(6):382–5.
   PubMedGoogle Scholar
• Schicks J, Muller Vom Hagen J, Bauer P, et al. Niemann–Pick type C is frequent in adult ataxia with cognitive decline and vertical gaze palsy. Neurology 2013;80(12):1169–70.
   PubMed Web of Science ®Google Scholar
• Walterfang M, Fahey M, Abel L, et al. Size and shape of the corpus callosum in adult Niemann–Pick type C reflects state and trait illness variables. AJNR Am J Neuroradiol 2011;32(7):1340–6.
   PubMed Web of Science ®Google Scholar
• Synofzik M, Harmuth F, Stampfer M, et al. NPC1 is enriched in unexplained early onset ataxia: a targeted high-throughput screening. J Neurol 2015;262(11):2557–63.
   PubMed Web of Science ®Google Scholar
• Hendriksz CJ, Pineda M, Fahey M, et al. The Niemann-Pick disease type C suspicion index: development of a revised tool with improved predictive ability. J Inherit Metab Dis 2014;37(suppl 7):P–372.
   Google Scholar
• Hendriksz CJ, Pineda M, Fahey M, et al. Improving NP-C screening: identification of seven key discriminatory signs and symptoms. J Inherit Metab Dis 2014;37(suppl 7):P–371.
   Google Scholar
• Wijburg FA, Sedel F, Pineda M, et al. Development of a suspicion index to aid diagnosis of Niemann–Pick disease type C. Neurology 2012;78(20):1560–7.
   PubMed Web of Science ®Google Scholar
• Wijburg FA, Sedel F, Pineda M, et al. Suspicion index to aid diagnosis of Niemann–Pick type C disease (NP-C), as autosomal recessive neurovisceral disorder. J Inherit Metab Dis 2011;34(3):S191.
   Google Scholar
• Garver WS, Francis GA, Jelinek D, et al. The National Niemann–Pick C1 disease database: report of clinical features and health problems. Am J Med Genet A 2007;143A(11):1204–11.
   PubMed Web of Science ®Google Scholar
• Strupp M, Kremmyda O, Adamczyk C, et al. Central ocular motor disorders, including gaze palsy and nystagmus. J Neurol 2014;261(suppl 2):S542–58.
   PubMed Web of Science ®Google Scholar
• Salsano E, Umeh C, Rufa A, et al. Vertical supranuclear gaze palsy in Niemann–Pick type C disease. Neurol Sci 2012;33(6):1225–32.
   PubMed Web of Science ®Google Scholar
• Goldberg ME, Walker MF. The control of gaze. In: Kandel ER, Schwartz JH, Jessel TM, et al., editors. Principles of neural science. 5th ed. New York: McGraw-Hill; 2013:984–16.
   Google Scholar
• Rottach KG, von Maydell RD, Das VE, et al. Evidence for independent feedback control of horizontal and vertical saccades from Niemann-Pick type C disease. Vis Res 1997;37(24):3627–38.
   PubMed Web of Science ®Google Scholar
• Abel LA, Walterfang M, Fietz M, et al. Saccades in adult Niemann-Pick disease type C reflect frontal, brainstem, and biochemical deficits. Neurology 2009;72(12):1083–6.
   PubMed Web of Science ®Google Scholar
• Solomon D, Winkelman AC, Zee DS, et al. Niemann-Pick type C disease in two affected sisters: ocular motor recordings and brain-stem neuropathology. Ann N Y Acad Sci 2005;1039:436–45.
   PubMed Web of Science ®Google Scholar
• Fink JK, Filling-Katz MR, Sokol J, et al. Clinical spectrum of Niemann-Pick disease type C. Neurology 1989;39(8):1040–9.
   PubMed Web of Science ®Google Scholar
• King KA, Gordon-Salant S, Yanjanin N, et al. Auditory phenotype of Niemann-Pick disease, type C1. Ear Hear 2014;35(1):110–7.
   PubMed Web of Science ®Google Scholar
• Grau AJ, Brandt T, Weisbrod M, et al. Adult Niemann-Pick disease type C mimicking features of multiple sclerosis. J Neurol Neurosurg Psychiatry 1997;63(4):552.
   PubMed Web of Science ®Google Scholar
• Walterfang M, Fahey M, Desmond P, et al. White and gray matter alterations in adults with Niemann-Pick disease type C: a cross-sectional study. Neurology 2010;75(1):49–56.
   PubMed Web of Science ®Google Scholar
• Walterfang M, Patenaude B, Abel LA, et al. Subcortical volumetric reductions in adult Niemann-Pick disease type C: a cross-sectional study. AJNR Am J Neuroradiol 2013;34(7):1334–40.
   PubMed Web of Science ®Google Scholar
• Walterfang M, van de Warrenburg BP. Cognitive impairment in “Other” movement disorders: hidden defects and valuable clues. Mov Disord 2014;29(5):694–703.
   PubMed Web of Science ®Google Scholar
• Hendriksz CJ, Pineda M, Fahey M, et al. The Niemann-Pick disease Type C suspicion index: development of a new tool to aid diagnosis. J Rare Disord Diagn Therapy 2015;1(1):11.
   Google Scholar
• Patterson MC, Mengel E, Vanier MT, et al. Stable or improved neurological manifestations during miglustat therapy in patients from the international disease registry for Niemann-Pick disease type C: an observational cohort study. Orphanet J Rare Dis 2015;10:65.
   PubMed Web of Science ®Google Scholar
• Tint GS, Pentchev P, Xu G, et al. Cholesterol and oxygenated cholesterol concentrations are markedly elevated in peripheral tissue but not in brain from mice with the Niemann-Pick type C phenotype. J Inherit Metab Dis 1998;21(8):853–63.
   PubMed Web of Science ®Google Scholar
• Boenzi S, Deodato F, Taurisano R, et al. A new simple and rapid LC-ESI-MS/MS method for quantification of plasma oxysterols as dimethylaminobutyrate esters. Its successful use for the diagnosis of Niemann-Pick type C disease. Clin Chim Acta 2014;437:93–100.
   PubMed Web of Science ®Google Scholar
• Jiang X, Sidhu R, Porter FD, et al. A sensitive and specific LC-MS/MS method for rapid diagnosis of Niemann-Pick C1 disease from human plasma. J Lipid Res 2011;52(7):1435–45.
   PubMed Web of Science ®Google Scholar
• Porter FD, Scherrer DE, Lanier MH, et al. Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease. Sci Transl Med 2010;2(56):56–81.
   Web of Science ®Google Scholar
• Giese AK, Mascher H, Grittner U, et al. A novel, highly sensitive and specific biomarker for Niemann-Pick type C1 disease. Orphanet J Rare Dis 2015;10:78.
   PubMed Web of Science ®Google Scholar
• Welford RW, Garzotti M, Marques Lourenco C, et al. Plasma lysosphingomyelin demonstrates great potential as a diagnostic biomarker for Niemann-Pick disease type C in a retrospective study. PLoS ONE 2014;9(12):e114669.
   PubMed Web of Science ®Google Scholar
• te Vruchte D, Lloyd-Evans E, Veldman RJ, et al. Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport. J Biol Chem 2004;279(25):26167–75.
   PubMed Web of Science ®Google Scholar
• Bremova T, Malinova V, Amraoui Y, et al. Acetyl-dl-leucine in Niemann-Pick type C: a case series. Neurology 2015;85(16):1368–75.
   PubMed Web of Science ®Google Scholar
• Platt FM, Neises GR, Dwek RA, et al. N-butyldeoxynojirimycin is a novel inhibitor of glycolipid biosynthesis. J Biol Chem 1994;269(11):8362–5.
   PubMed Web of Science ®Google Scholar
• Treiber A, Morand O, Clozel M. The pharmacokinetics and tissue distribution of the glucosylceramide synthase inhibitor miglustat in the rat. Xenobiotica 2007;37(3):298–314.
   PubMed Web of Science ®Google Scholar
• Patterson MC, Vanier MT, Suzuki K, et al. Niemann-pick disease type C: a lipid trafficking disorder. In: Scriver ALB, C.R., Sly, W.S., Valle, D., et al., editors. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill; 2001:3611–33.
   Google Scholar
• Fecarotta S, Romano A, Della Casa R, et al. Long term follow-up to evaluate the efficacy of miglustat treatment in Italian patients with Niemann-Pick disease type C. Orphanet J Rare Dis 2015;10:22.
   PubMed Web of Science ®Google Scholar
• Walterfang M, Chien YH, Imrie J, et al. Dysphagia as a risk factor for mortality in Niemann-Pick disease type C: systematic literature review and evidence from studies with miglustat. Orphanet J Rare Dis 2012;7:76.
   PubMed Web of Science ®Google Scholar
• Wraith JE, Vecchio D, Jacklin E, et al. Miglustat in adult and juvenile patients with Niemann-Pick disease type C: long-term data from a clinical trial. Mol Genet Metab 2010;99(4):351–7.
   PubMed Web of Science ®Google Scholar
• Pineda M, Wraith JE, Mengel E, et al. Miglustat in patients with Niemann-Pick disease Type C (NP-C): a multicenter observational retrospective cohort study. Mol Genet Metab 2009;98(3):243–9.
   PubMed Web of Science ®Google Scholar
• Bowman EA, Walterfang M, Abel L, . Longitudinal changes in cerebellar and subcortical volumes in adult-onset Niemann-Pick disease type C patients treated with miglustat. J Neurol 2015;262(9):2106–14.
   PubMed Web of Science ®Google Scholar
• Galanaud D, Tourbah A, Lehericy S, et al. 24 month-treatment with miglustat of three patients with Niemann-Pick disease type C: follow up using brain spectroscopy. Mol Genet Metab 2009;96(2):55–8.
   PubMed Web of Science ®Google Scholar
• Sedel F, Chabrol B, Audoin B, et al. Normalization of brain spectroscopy in Niemann-Pick disease type C patients treated with miglustat. J Neurol in press.
   Web of Science ®Google Scholar
• Abel LA, Walterfang M, Stainer MJ, et al. Longitudinal assessment of reflexive and volitional saccades in Niemann-Pick type C disease during treatment with miglustat. Orphanet J Rare Dis 2015;10(1):160.
   PubMed Web of Science ®Google Scholar
• Brand M, Muller A, Alsop J, et al. Results from a 9-year Intensive Safety Surveillance Scheme (IS(3)) in miglustat (Zavesca((R)))-treated patients. Pharmacoepidemiol Drug Saf 2015;24(3):329–33.
   PubMed Web of Science ®Google Scholar
• Hollak CE, Hughes D, van Schaik IN, et al. Miglustat (Zavesca) in type 1 Gaucher disease: 5-year results of a post-authorisation safety surveillance programme. Pharmacoepidemiol Drug Saf 2009;18(9):770–7.
   PubMed Web of Science ®Google Scholar
• Champion H, Ramaswami U, Imrie J, et al. Dietary modifications in patients receiving miglustat. J Inherit Metab Dis 2010;33(3):S379–83.
   PubMed Web of Science ®Google Scholar
• Actelion. Miglustat (Zavesca) summary of product characteristics: EMA (EudraPharm) 2014. Available from: http://www.ema.europa.eu/ema/index.jsp?curl=pages/medicines/human/medicines/000435/human_med_001171.jsp&murl=menus/medicines/medicines.jsp&mid=WC0b01ac058001d125. [last accessed 6 May 2014].
   Google Scholar
• Belmatoug N, Burlina A, Giraldo P, et al. Gastrointestinal disturbances and their management in miglustat-treated patients. J Inherit Metab Dis 2011;34(5):991–1001.
   PubMed Web of Science ®Google Scholar
• Dechelotte P. [Type 1 Gaucher's disease in the adult. Nutritional management during initiation of treatment with miglustat]. Presse Med 2004;33(7):494–6.
   PubMed Web of Science ®Google Scholar
• Remenova T, Morand O, Amato D, et al. A double-blind, randomized, placebo-controlled trial studying the effects of Saccharomyces boulardii on the gastrointestinal tolerability, safety, and pharmacokinetics of miglustat. Orphanet J Rare Dis 2015;10(1):81.
   PubMed Web of Science ®Google Scholar
• Peake KB, Vance JE. Normalization of cholesterol homeostasis by 2-hydroxypropyl-beta-cyclodextrin in neurons and glia from Niemann-Pick C1 (NPC1)-deficient mice. J Biol Chem 2012;287(12):9290–8.
   PubMed Web of Science ®Google Scholar
• Ramirez CM, Liu B, Taylor AM, et al. Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr Res 2010;68(4):309–15.
   PubMed Web of Science ®Google Scholar
• Matsuo M, Togawa M, Hirabaru K, et al. Effects of cyclodextrin in two patients with Niemann-Pick type C disease. Mol Genet Metab 2013;108(1):76–81.
   PubMed Web of Science ®Google Scholar
• Aqul A, Liu B, Ramirez CM, et al. Unesterified cholesterol accumulation in late endosomes/lysosomes causes neurodegeneration and is prevented by driving cholesterol export from this compartment. J Neurosci 2011;31(25):9404–13.
   PubMed Web of Science ®Google Scholar
• Williams IM, Wallom KL, Smith DA, et al. Improved neuroprotection using miglustat, curcumin and ibuprofen as a triple combination therapy in Niemann-Pick disease type C1 mice. Neurobiol Dis 2014;67:9–17.
   PubMed Web of Science ®Google Scholar
• Pipalia NH, Cosner CC, Huang A, et al. Histone deacetylase inhibitor treatment dramatically reduces cholesterol accumulation in Niemann-Pick type C1 mutant human fibroblasts. Proc Natl Acad Sci U S A 2011;108(14):5620–5.
   PubMed Web of Science ®Google Scholar
• Alam MS, Getz M, Haldar K. Chronic administration of an HDAC inhibitor treats both neurological and systemic Niemann-Pick type C disease in a mouse model. Sci Transl Med 2016;8(326):326–23.
   Web of Science ®Google Scholar
• Mengel E, Klunemann HH, Lourenco CM, et al. Niemann-Pick disease type C symptomatology: an expert-based clinical description. Orphanet J Rare Dis 2013;8:166.
   PubMed Web of Science ®Google Scholar