Olfactory identification in LRRK2 G2019S mutation carriers: a relevant marker?

Annals of Clinical and Translational Neurology

Volumn 1, Issue 9, 2014, Pages 670-678

  Saunders Pullman, Rachel ^a,b,c   Mirelman, Anat ^d   Wang, Cuiling ^c   Alcalay, Roy N ^e,f   San Luciano, Marta ^g   Ortega, Robert ^a   Raymond, Deborah ^a   Mejia Santana, Helen ^e,f   Ozelius, Laurie ^b   Clark, Lorraine ^e,f   Orr Utreger, Avi ^d   Marder, Karen ^e,f,h   Giladi, Nir ^d   Bressman, Susan B ^a,b  

^a BETH ISRAEL MEDICAL CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d TEL AVIV UNIVERSITY   (Israel)

^e New York Presbyterian Columbia University Medical Center   (United States)

^f Department of Medicine   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h Vagelos College of Physicians and Surgeons   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; LEUCINE RICH REPEAT KINASE 2;

ADULT; ARTICLE; CONTROLLED STUDY; DISEASE CARRIER; FEMALE; GENE; GENE MUTATION; HUMAN; HYPOSMIA; LRRK2 GENE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; OLFACTION SCORE; PARKINSON DISEASE; PRIORITY JOURNAL; SCORING SYSTEM; SMELLING; UPSIT SCORE;

EID: 84936993750     PISSN: None     EISSN: 23289503     Source Type: Journal    
DOI: 10.1002/acn3.95     Document Type: Article

References (46)

1. Stern MB, Doty RL, Dotti M, et al. Olfactory function in Parkinson's disease subtypes. Neurology 1994;44:266–268.
2. Doty RL. Olfactory dysfunction in Parkinson's disease. Nat Rev Neurosci 2012;8:329–339.
3. Duda JE. Olfactory system pathology as a model of Lewy body neurodegenerative disease. J Neurol Sci 2010;289:49–54.
4. Khan NL, Katzenschlager R, Watt H, et al. Olfaction differentiates parkin disease from early-onset parkinsonism and PD. Neurology 2004;62:1224–1226.
5. Alcalay RN, Caccappolo E, Mejia-Santana H, et al. Cognitive performance of GBA mutation carriers with early-onset PD: The CORE-PD study. Neurology 2012;78:1434–1440.
6. Khan NL, Jain S, Lynch JM, et al. Mutations in the gene LRRK2 encoding dardarin (PARK8) cause familial Parkinson's disease: clinical, pathological, olfactory and functional imaging and genetic data. Brain 2005;128:2786–2796.
7. Silveira-Moriyama L, Guedes LC, Kingsbury A, et al. Hyposmia in G2019S LRRK2-related parkinsonism: clinical and pathologic data. Neurology 2008;71:1021–1026.
8. Trinh J, Amouri R, Duda JE, et al. A comparative study of Parkinson's disease and leucine-rich repeat kinase 2 p. G2019S parkinsonism. Neurobiol Aging 2014;35:1125–1131.
9. Healy DG, Falchi M, O'Sullivan SS, et al. Phenotype, genotype, and worldwide genetic penetrance of LRRK2-associated Parkinson's disease: a case–control study. Lancet Neurol 2008;7:583–590.
10. Saunders-Pullman R, Stanley K, Wang C, et al. Olfactory dysfunction in LRRK2 G2019S mutation carriers. Neurology 2011;77:319–324.
11. Silveira-Moriyama L, Munhoz RP, de J Carvalho M, et al. Olfactory heterogeneity in LRRK2 related Parkinsonism. Mov Disord 2010; 25: 2879–2883.
12. Marras C, Schuele B, Munhoz RP, et al. Phenotype in parkinsonian and nonparkinsonian LRRK2 G2019S mutation carriers. Neurology 2011;77:325–333.
13. 123I-MIBG cardiac uptake and smell identification in parkinsonian patients with LRRK2 mutations. J Neurol 2011;258:1126–1132.
14. Sierra M, Sánchez-Juan P, Martínez-Rodríguez MI, et al. Olfaction and imaging biomarkers in LRRK2 G2019S-associated PD. Neurology 2013;80:621–626.
15. Johansen KK, Warø BJ, Aasly JO. Olfactory dysfunction in sporadic Parkinson's disease and LRRK2 carriers. Acta Neurol Scand 2014;129:300–306; DOI: 10.1111/ane.12172.
16. Ross GW, Petrovitch H, Abbott RD, et al. Association of olfactory dysfunction with risk for future Parkinson's disease. Ann Neurol 2008;63:167–173.
17. Ponsen MM, Stoffers D, Wolters EC, et al. Olfactory testing combined with dopamine transporter imaging as a method to detect prodromal Parkinson's disease. J Neurol Neurosurg Psychiatry 2010;81:396–399.
18. Clark LN, Wang Y, Karlins E, et al. Frequency of LRRK2 mutations in early- and late-onset PD. Neurology 2006;67:1786–1791.
19. Ozelius LJ, Senthil G, Saunders-Pullman R, et al. LRRK2 G2019S as a cause of Parkinson's disease in Ashkenazi Jews. N Engl J Med 2006;354:424–425.
20. Ferreira JJ, Guedes LC, Rosa MM, et al. High prevalence of LRRK2 mutations in familial and sporadic Parkinson's disease in Portugal. Mov Disord 2007;22:1194–1201.
21. Alcalay RN, Mirelman A, Saunders-Pullman R, et al. PD phenotype in Ashkenazi Jews with and without LRRK2 G2019S mutations. Mov Disord 2013;28:1966–1971.
22. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinic-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992;55:181–184.
23. Gan-Or Z, Bar-Shira A, Gurevich T, et al. Homozygosity for the MTX1 c.184T>A (p. S63T) alteration modifies the age of onset in GBA-associated Parkinson's disease. J Neurogenet 2011;12:325–332.
24. Barrett MJ, Hagenah J, Dhawan V, et al. Transcranial sonography and functional imaging in glucocerebrosidase mutation PD. Parkinsonism Relat Disord 2013;19:186–191.
25. Doty RL. The Smell Identification Test™ administration manual. 3rd ed. Haddon Heights, NJ: Sensonics, Inc.; 1995.
26. Fahn S, Marsden CD, Calne DB, et al. Recent developments in Parkinson's disease. 1st ed. Florham Park, NJ: Mcmillan Healthcare Information; 1987. p. 153–163.
27. Nasreddine ZS, Phillips NA, Bédirian V, et al. The Montreal Cognitive Assessment (MoCA): a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005;53:695–699.
28. Laird NM, Ware JH. Random effects models for longitudinal data. Biometrics 1982;38:963–974.
29. Vuong QH. Likelihood ratio tests for model selection and non-nested hypotheses. Econometrica 1898;57:307–333.
30. Silveira-Moriyama L, Holton JL, Kingsbury A, et al. Regional differences in the severity of Lewy body pathology across the olfactory cortex. Neurosci Lett 2009;453:77–80.
31. Brockmann K, Srulijes K, Hauser AK, et al. GBA-associated PD presents with non-motor characteristics. Neurology 2011;77:276–280.
32. Saunders-Pullman R, Hagenah J, Dhawan V, et al. Gaucher disease ascertained through a Parkinson's center: imaging and clinical characterization. Mov Dis 2010;25:1364–1372.
33. Houlden H, Singleton A. The genetics and neuropathology of Parkinson's disease. Acta Neuropathol 2012;124:325–338.
34. Poulopoulos M, Cortes E, Vonsattel JP, et al. Clinical and pathological characteristics of LRRK2 G2019S patients with PD. J Mol Neurosci 2012;47:139–143.
35. Braak H, Del TK, Rub U, et al. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003;24:197–211.
36. Siderowf A, Jennings D, Connolly J, et al. Risk factors for Parkinson's disease and impaired olfaction in relatives of patients with Parkinson's disease. Mov Disord 2007;22:2249–2255.
37. Siderowf A, Jennings D, Eberly S, et al. Impaired olfaction and other prodromal features in the Parkinson At-Risk Syndrome Study. Mov Disord 2012;27:406–412.
38. Thaler A, Mirelman A, Helmich RC, et al. Neural correlates of executive functions in healthy G2019S LRRK2 mutation carriers. Cortex 2013;49:2501–2511.
39. Berg D, Godau J, Seppi K, et al. The PRIPS study: screening battery for subjects at risk for Parkinson's disease. Eur J Neurol 2013;20:102–108.
40. Postuma RB, Aarsland D, Barone P, et al. Identifying prodromal Parkinson's disease: pre-motor disorders in Parkinson's disease. Mov Disord 2012;27:617–626.
41. Mirelman A, Gurevich T, Giladi N, et al. Gait alterations in healthy carriers of the LRRK2 G2019S mutations. Ann Neurol 2011;69:193–197.
42. Ortega R, Deik A, Battista J, et al. Progression of motor dysfunction in elderly LRRK2 carriers, including prior to phenoconversion to PD [abstract]. Neurology 2013;80IN2-2-005.
43. Lo Y, Mendell NR, Rubin DB. Testing the number of components in a normal mixture. Biometrika 2001;88:767–778.
44. Klein C, Chuang R, Marras C, Lang AE. The curious case of phenocopies in families with genetic Parkinson's disease. Mov Disord 2011;26:1793–1802.
45. Quinn TP, Alcalay RN, Saunders-Pullman R, et al. The Montreal Cognitive Assessment across English and Hebrew. World Parkinson's Congress, Montreal, 2013.
46. Djaldetti R, Nageris BI, Lorberboym M, et al. [123-I]-FP-CIT SPECT and olfaction test in patients with combined postural and rest tremor. J Neural Transm 2008;115:469–472.