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01-08-2021 | Niemann-Pick Disease | Review Article

Neuropsychological assessment in Niemann-Pick disease type C: a systematic review

Authors: Giuseppa Maresca, Caterina Formica, Vanessa Nocito, Desiree Latella, Simona Leonardi, Maria Cristina De Cola, Giuseppe Triglia, Placido Bramanti, Francesco Corallo

Published in: Neurological Sciences | Issue 8/2021

Abstract

Background

The neuropsychological profile of Niemann-Pick type C (NP-C) patients is characterized by an early deterioration in executive functions and attention. There are few studies on cognitive impairment and on neuropsychological assessment of NP-C disease. The purpose of this review is to analyze the studies on a psychological assessment for NP-C patients.

Method

This review aims to identify a neuropsychological assessment to evaluate cognitive domains and neuropsychological changes in these patients. There were a total of 73 articles. The search terms were identified as titles and abstracts. All articles were evaluated by title, abstract, and text.

Results

Only four of the 73 articles were included because they met the criteria of our review. Furthermore, in these studies, possible diagnostic protocols are proposed on NP-C subjects.

Discussion and conclusion

The cognitive impairment in NP-C has a negative impact on daily functioning and quality of life. Early diagnosis could identify cognitive deficits and promote cognitive interventions to improve the neuropsychological profile. The management of NP-C disease should be based on a multidisciplinary approach, to treating symptoms, preserving neurological functions, and guaranteeing the best possible quality of life. Early identification of neurological and psychological symptoms of the disease is necessary in order to decrease the progression of neurological disease and improve patient care and treatment outcomes. Furthermore, research should focus more on cognitive aspects, not only in the diagnostic process but also in the rehabilitation process.

Kheder A, Scott C, Olpin S, Hadjivassiliou M (2013) Niemann–Pick type C: a potentially treatable disorder? Practical neurology. 13(6):382–385CrossRef

Patterson MC, Hendriksz CJ, Walterfang M, Sedel F, Vanier MT, Wijburg F (2012) Recommendations for the diagnosis and management of Niemann-Pick disease type C: an update. Mol Genet Metab 106:330–344CrossRef

Vanier MT (2015) Complex lipid trafficking in Niemann-Pick disease type C. J Inherit Metab Dis. 38:187–199CrossRef

Ca W, Cross JL, Iben J, Sanchez-Pulido L, Cougnoux A, Platt FM et al (2015) High incidence of unrecognized visceral/neurological late-onset Niemann-Pick disease, type C1, predicted by analysis of massively parallel sequencing data sets. Genet Med 18:41–48

Geberhiwot T, Moro A, Dardis A, Ramaswami U, Sirrs S, Marfa MP et al (2018) Consensus clinical management guidelines for Niemann-pick disease type C. Orphanet J Rare Dis. 13:50CrossRef

Bonnot O, Klünemann H-H, Velten C, Torres Martin JV, Walterfang M (2018) Systematic review of psychiatric signs in Niemann-Pick disease type C. World J Biol Psychiatry.

Fecarotta S, Romano A, Della Casa R, del Giudice E, Bruschini D, Mansi G, Bembi B, Dardis A, Fiumara A, di Rocco M, Uziel G (2015) Long term follow-up to evaluate the efficacy of miglustat treatment in Italian patients with Niemann-Pick disease type C. Orphanet J Rare Dis 10:22CrossRef

Stampfer M, Theiss S, Amraoui Y, Jiang X, Keller S, Ory DS et al (2013) Niemann-Pick disease type C clinical database: cognitive and coordination deficits are early disease indicators. Orphanet J Rare Dis. 8:35CrossRef

Bergeron D, Poulin S, Laforce R Jr (2018) Cognition and anatomy of adult Niemann–Pick disease type C: insights for the Alzheimer field. Cognitive neuropsychology. 35(3-4):209–222CrossRef

10.

Hinton V, Vecchio D, Prady H, Wraith E, Patterson M, York N et al (2005) The cognitive phenotype of Niemann-Pick type C (NPC): neuropsychological characteristics of patients at baseline in a clinical trial with oral miglustat. J Neurol Sci 238:S77

11.

Rego T, Farrand S, Goh AM, Eratne D, Kelso W, Mangelsdorf S, Velakoulis D, Walterfang M (2019) Psychiatric and cognitive symptoms associated with Niemann-Pick type C disease: neurobiology and management. CNS drugs. 33(2):125–142CrossRef

12.

Sevin M, Lesca G, Baumann N, Millat G, Lyon-Caen O, Vanier MT et al (2007) The adult form of Niemann-Pick disease type C. Brain 130(Pt 1):120–133PubMed

13.

Sedel F, Chabrol B, Audoin B, Kaphan E, Tranchant C, Burzykowski T, Tourbah A, Vanier MT, Galanaud D (2016) Normalisation of brain spectroscopy findings in Niemann-Pick disease type C patients treated with miglustat. J Neurol. 263:927–936CrossRef

14.

Heitz C, Epelbaum S, Nadjar Y (2017) Cognitive impairment profile in adult patients with Niemann pick type C disease. Orphanet journal of rare diseases. 12(1):166CrossRef

15.

Klarner B, Klünemann HH, Lürding R, Aslanidis C, Rupprecht R (2007) Neuropsychological profile of adult patients with Niemann–Pick C1 (NPC1) mutations. Journal of inherited metabolic disease. 30(1):60–67CrossRef

16.

Maubert A, Hanon C, Sedel F (2016) Psychiatric disorders in adult form of Niemann-Pick disease type C. Encephale. 42:208–213CrossRef

17.

Patterson MC, Clayton P, Gissen P, Anheim M, Bauer P, Bonnot O, Dardis A, Dionisi-Vici C, Klünemann HH, Latour P, Lourenço CM (2017) Recommendations for the detection and diagnosis of Niemann-pick disease type C: an update. Neurology: Clinical Practice. 7(6):499–511

18.

Nadjar Y, Hütter-Moncada AL, Latour P, Ayrignac X, Kaphan E, Tranchant C, Cintas P, Degardin A, Goizet C, Laurencin C, Martzolff L (2018) Adult Niemann-Pick disease type C in France: clinical phenotypes and long-term miglustat treatment effect. Orphanet journal of rare diseases. 13(1):175CrossRef

19.

Evans WR, Hendriksz CJ (2017) Niemann-Pick type C disease–the tip of the iceberg? A review of neuropsychiatric presentation, diagnosis and treatment. BJPsych bulletin. 41(2):109–114CrossRef

20.

Fu R, Yanjanin NM, Elrick MJ, Ware C, Lieberman AP, Porter FD (2012) Apolipoprotein E genotype and neurological disease onset in Niemann-Pick disease, type C1. Am J Med Genet A. 158A(11):2775–2780. https://doi.org/10.1002/ajmg.a.35395 Epub 2012 Sep 28. PMID: 23023945; PMCID: PMC3477305CrossRefPubMedPubMedCentral

21.

Manganelli F, Dubbioso R, Iodice R, Topa A, Dardis A, Russo CV, Ruggiero L, Tozza S, Filla A, Santoro L (2014) Central cholinergic dysfunction in the adult form of Niemann Pick disease type C: a further link with Alzheimer’s disease? J Neurol. 261(4):804–808. https://doi.org/10.1007/s00415-014-7282-2 Epub 2014 Feb 26CrossRefPubMed

22.

Cologna SM, Cluzeau CV, Yanjanin NM, Blank PS, Dail MK, Siebel S, Toth CL, Wassif CA, Lieberman AP, Porter FD (2014) Human and mouse neuroinflammation markers in Niemann-Pick disease, type C1. J Inherit Metab Dis 37(1):83–92. https://doi.org/10.1007/s10545-013-9610-6 Epub 2013 May 8. PMID: 23653225; PMCID: PMC3877698CrossRefPubMed

23.

Mattsson N, Olsson M, Gustavsson MK, Kosicek M, Malnar M, Månsson JE, Blomqvist M, Gobom J, Andreasson U, Brinkmalm G, Vite C, Hecimovic S, Hastings C, Blennow K, Zetterberg H, Portelius E (2012) Amyloid-β metabolism in Niemann-Pick C disease models and patients. Metab Brain Dis. 27(4):573–585. https://doi.org/10.1007/s11011-012-9332-8 Epub 2012 Sep 1CrossRefPubMed

24.

Kågedal K, Kim WS, Appelqvist H, Chan S, Cheng D, Agholme L, Barnham K, McCann H, Halliday G, Garner B (2010) Increased expression of the lysosomal cholesterol transporter NPC1 in Alzheimer’s disease. Biochim Biophys Acta. 1801(8):831–838. https://doi.org/10.1016/j.bbalip.2010.05.005 Epub 2010 May 16CrossRefPubMed

25.

Benussi A, Cotelli MS, Cosseddu M, Bertasi V, Turla M, Salsano E, Dardis A, Padovani A, Borroni B (2017) Preliminary results on long-term potentiation-like cortical plasticity and cholinergic dysfunction after miglustat treatment in Niemann-Pick disease type C. JIMD Rep 36:19–27. https://doi.org/10.1007/8904_2016_33 Epub 2017 Jan 17. PMID: 28092091; PMCID: PMC5680283CrossRefPubMedPubMedCentral

26.

Di Lorenzo F, Ponzo V, Bonnì S, Motta C, Negrão Serra PC, Bozzali M, Caltagirone C, Martorana A, Koch G (2016) Long-term potentiation-like cortical plasticity is disrupted in Alzheimer’s disease patients independently from age of onset. Ann Neurol. 80(2):202–210. https://doi.org/10.1002/ana.24695 Epub 2016 Jul 8CrossRefPubMed

27.

Benussi A, Cosseddu M, Filareto I, Dell’Era V, Archetti S, Sofia Cotelli M, Micheli A, Padovani A, Borroni B (2016) Impaired long-term potentiation-like cortical plasticity in presymptomatic genetic frontotemporal dementia. Ann Neurol. 80(3):472–476. https://doi.org/10.1002/ana.24731 Epub 2016 Aug 10CrossRefPubMed

28.

Esposito M, Dubbioso R, Tozza S, Iodice R, Aiello M, Nicolai E, Cavaliere C, Salvatore M, Santoro L, Manganelli F (2019) In vivo evidence of cortical amyloid deposition in the adult form of Niemann Pick type C. Heliyon 5(11):e02776. https://doi.org/10.1016/j.heliyon.2019.e02776 PMID: 31844711; PMCID: PMC6895717CrossRefPubMedPubMedCentral

29.

Bowman EA, Walterfang M, Abel L, Desmond P, Fahey M, Velakoulis D (2015) Longitudinal changes in cerebellar and subcortical volumes in adult-onset Niemann-Pick disease type C patients treated with miglustat. J Neurol. 262:2106–2114CrossRef

30.

Sedel F (2010) Clinical diagnosis of the adult form of Niemann-Pick type C disease. Archives de pediatrie: organe officiel de la Societe francaise de pediatrie. 17:S50–S53CrossRef

31.

Tozza S, Dubbioso R, Iodice R, Topa A, Esposito M, Ruggiero L, Spina E, De Rosa A, Saccà F, Santoro L, Manganelli F (2018) Long-term therapy with miglustat and cognitive decline in the adult form of Niemann-Pick disease type C: a case report. Neurol Sci. 39(6):1015–1019. https://doi.org/10.1007/s10072-018-3314-5 Epub 2018 Mar 13CrossRefPubMed

32.

Mengel E, Klünemann HH, Lourenço CM, Hendriksz CJ, Sedel F, Walterfang M, Kolb SA (2013) Niemann-Pick disease type C symptomatology: an expert-based clinical description. Orphanet journal of rare diseases. 8(1):166CrossRef

33.

Thurm A, Farmer C, Farhat NY, Wiggs E, Black D, Porter FD (2016) Cohort study of neurocognitive functioning and adaptive behaviour in children and adolescents with Niemann-Pick disease type C1. Developmental Medicine & Child Neurology. 58(3):262–269CrossRef

34.

Abela L, Plecko B, Palla A, Burda P, Nuoffer JM, Ballhausen D, Rohrbach M (2014) Early co-occurrence of a neurologic-psychiatric disease pattern in Niemann-Pick type C disease: a retrospective Swiss cohort study. Orphanet J Rare Dis 9:176. https://doi.org/10.1186/s13023-014-0176-7 PMID: 25425405; PMCID: PMC4253629CrossRefPubMedPubMedCentral

35.

Andrade GN, Molholm S, Butler JS, Brandwein AB, Walkley SU, Foxe JJ (2014) Atypical multisensory integration in Niemann-Pick type C disease– towards potential biomarkers. Orphanet J Rare Dis 9:149. https://doi.org/10.1186/s13023-014-0149-x PMID: 25239094; PMCID: PMC4173006CrossRefPubMedPubMedCentral

36.

Benussi A, Alberici A, Premi E, Bertasi V, Cotelli MS, Turla M, Dardis A, Zampieri S, Marchina E, Paghera B, Gallivanone F, Castiglioni I, Padovani A, Borroni B (2015) Phenotypic heterogeneity of Niemann-Pick disease type C in monozygotic twins. J Neurol. 262(3):642–647. https://doi.org/10.1007/s00415-014-7619-x Epub 2014 Dec 24CrossRefPubMed

37.

Benussi A, Cotelli MS, Cantoni V, Bertasi V, Turla M, Dardis A, Biasizzo J, Manenti R, Cotelli M, Padovani A, Borroni B (2019) Clinical and neurophysiological characteristics of heterozygous <i>NPC1</i> carriers. JIMD Rep 49(1):80–88. https://doi.org/10.1002/jmd2.12059 PMID: 31497485; PMCID: PMC6718120CrossRefPubMedPubMedCentral

38.

Bremova-Ertl T, Sztatecsny C, Brendel M, Moser M, Möller B, Clevert DA, Beck-Wödl S, Kun-Rodrigues C, Bras J, Rominger A, Ninov D, Strupp M, Schneider SA (2020) Clinical, ocular motor, and imaging profile of Niemann-Pick type C heterozygosity. Neurology. 94(16):e1702–e1715. https://doi.org/10.1212/WNL.0000000000009290 Epub 2020 Mar 31CrossRefPubMed

39.

Chamova T, Kirov A, Guergueltcheva V, Todorov T, Bojinova V, Zhelyazkova S, Samuel J, Radionova M, Sarafov S, Cherninkova S, Krastev S, Todorova A, Tournev I (2016) Clinical spectrum and genetic variability in Bulgarian patients with Niemann-Pick disease type C. Eur Neurol. 75(3-4):113–123. https://doi.org/10.1159/000444480 Epub 2016 Feb 25CrossRefPubMed

40.

Chien YH, Lee NC, Tsai LK, Huang AC, Peng SF, Chen SJ, Hwu WL (2007) Treatment of Niemann-Pick disease type C in two children with miglustat: initial responses and maintenance of effects over 1 year. J Inherit Metab Dis. 30(5):826. https://doi.org/10.1007/s10545-007-0630-y Epub 2007 Jun 21CrossRefPubMed

41.

Dagan E, Schlesinger I, Ayoub M, Mory A, Nassar M, Kurolap A, Peretz-Aharon J, Gershoni-Baruch R (2015) The contribution of Niemann-Pick SMPD1 mutations to Parkinson disease in Ashkenazi Jews. Parkinsonism Relat Disord. 21(9):1067–1071. https://doi.org/10.1016/j.parkreldis.2015.06.016 Epub 2015 Jun 19CrossRefPubMed

42.

Farmer CA, Thurm A, Farhat N, Bianconi S, Keener LA, Porter FD (2019) Long-term neuropsychological outcomes from an open-label phase I/IIa trial of 2-hydroxypropyl-β-cyclodextrins (VTS-270) in Niemann-Pick disease, type C1. CNS Drugs 33(7):677–683. https://doi.org/10.1007/s40263-019-00642-2 PMID: 31187454; PMCID: PMC7448545CrossRefPubMedPubMedCentral

43.

Hassan SS, Trenado C, Elben S, Schnitzler A, Groiss SJ (2018) Alteration of cortical excitability and its modulation by Miglustat in Niemann-Pick disease type C. J Clin Neurosci. 47:214–217. https://doi.org/10.1016/j.jocn.2017.10.011 Epub 2017 Oct 23CrossRefPubMed

44.

Johnen A, Pawlowski M, Duning T (2018) Distinguishing neurocognitive deficits in adult patients with NP-C from early onset Alzheimer’s dementia. Orphanet J Rare Dis 13(1):91. https://doi.org/10.1186/s13023-018-0833-3 PMID: 29871644; PMCID: PMC5989447CrossRefPubMedPubMedCentral

45.

Koens LH, Kuiper A, Coenen MA, Elting JW, de Vries JJ, Engelen M, Koelman JH, van Spronsen FJ, Spikman JM, de Koning TJ, Tijssen MA (2016) Ataxia, dystonia and myoclonus in adult patients with Niemann-Pick type C. Orphanet J Rare Dis 11(1):121. https://doi.org/10.1186/s13023-016-0502-3 PMID: 27581084; PMCID:PMC5007743CrossRefPubMedPubMedCentral

46.

Maresca G, Nocito V, De Salvo S, Formica C, Leonardi S, Bramanti P, de Cola MC, Corallo F (2021) Assessment and rehabilitation of cognitive deficit in a Niemann-Pick type C disease patient. Neurocase.:1–4. https://doi.org/10.1080/13554794.2020.1864409 Epub ahead of print

47.

Pineda M, Perez-Poyato MS, O’Callaghan M, Vilaseca MA, Pocovi M, Domingo R, Portal LR, Pérez AV, Temudo T, Gaspar A, Peñas JJ, Roldán S, Fumero LM, de la Barca OB, Silva MT, Macías-Vidal J, Coll MJ (2010) Clinical experience with miglustat therapy in pediatric patients with Niemann-Pick disease type C: a case series. Mol Genet Metab. 99(4):358–366. https://doi.org/10.1016/j.ymgme.2009.11.007 Epub 2009 Nov 29CrossRefPubMed

48.

Santos ML, Raskin S, Telles DS, Löhr A Jr (2008) Lib Long-term therapy with miglustat and cognitive decline in the adult form of Niemann-Pick disease type C: a case report. eralesso PB, Vieira SC, Cordeiro ML. Treatment of a child diagnosed with Niemann-Pick disease type C with miglustat: a case report in Brazil. J Inherit Metab Dis 31(Suppl 2):S357-61. https://doi.org/10.1007/s10545-008-0923-9 Epub 2008 Oct 21CrossRefPubMed

49.

Sylvain M, Arnold DL, Scriver CR, Schreiber R, Shevell MI (1994) Magnetic resonance spectroscopy in Niemann-Pick disease type C: correlation with diagnosis and clinical response to cholestyramine and lovastatin. Pediatr Neurol. 10(3):228–232. https://doi.org/10.1016/0887-8994(94)90028-0CrossRefPubMed

50.

Villemagne VL, Velakoulis D, Doré V, Bozinoski S, Masters CL, Rowe CC, Walterfang M (2019) Imaging of tau deposits in adults with Niemann-Pick type C disease: a case-control study. Eur J Nucl Med Mol Imaging. 46(5):1132–1138. https://doi.org/10.1007/s00259-019-4273-7 Epub 2019 Jan 28CrossRefPubMed

51.

Walterfang M, Fietz M, Fahey M, Sullivan D, Leane P, Lubman DI (2006 Spring) Velakoulis. The neuropsychiatry of Niemann-Pick type C disease in adulthood. J Neuropsychiatry Clin Neurosci. 18(2):158–170. https://doi.org/10.1176/jnp.2006.18.2.158CrossRefPubMed

52.

Higgins JJ, Patterson MC, Dambrosia JM, Pikus AT, Pentchev PG, Sato S, Brady RO, Barton NW (1992) A clinical staging classification for type C Niemann-Pick disease. Neurology 42(12):2286CrossRef

Title: Neuropsychological assessment in Niemann-Pick disease type C: a systematic review
Authors: Giuseppa Maresca
Caterina Formica
Vanessa Nocito
Desiree Latella
Simona Leonardi
Maria Cristina De Cola
Giuseppe Triglia
Placido Bramanti
Francesco Corallo
Publication date: 01-08-2021
Publisher: Springer International Publishing
Keywords: Niemann-Pick Disease
Niemann-Pick Disease
Published in: Neurological Sciences / Issue 8/2021
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-021-05337-5

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Neuropsychological assessment in Niemann-Pick disease type C: a systematic review

Abstract

Background

Method

Results

Discussion and conclusion

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Method

Results

Discussion and conclusion

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