Olfaction and Parkinson's syndromes: Its role in differential diagnosis

Current Opinion in Neurology

Volumn 17, Issue 4, 2004, Pages 417-423

  Katzenschlager, Regina ^a,b,c   Lees, Andrew J ^a,b  

^a NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Donauspital/SMZ Ost ^*  (Austria)

Author keywords

Differential diagnosis; Early detection; Olfactory function; Parkinsonian syndromes

Indexed keywords

DOPAMINE; NEUROLEPTIC AGENT; PARKIN; TYROSINE 3 MONOOXYGENASE;

BRAIN LEVEL; CEREBELLUM DISEASE; CORTICOBASAL DEGENERATION; DIFFERENTIAL DIAGNOSIS; DIFFUSE LEWY BODY DISEASE; DISEASE ASSOCIATION; EARLY DIAGNOSIS; ESSENTIAL TREMOR; GENETIC DISORDER; HUMAN; NEUROLOGIC EXAMINATION; NEUROPHYSIOLOGY; OLFACTORY BULB; PARKIN DISEASE; PARKINSON DISEASE; PARKINSONISM; PATHOGENESIS; PATHOPHYSIOLOGY; PROGRESSIVE SUPRANUCLEAR PALSY; PSYCHOMETRY; REVIEW; SHY DRAGER SYNDROME; SMELLING; SMELLING DISORDER; SNIFFING; SPINOCEREBELLAR DEGENERATION; TREMOR; VASCULAR PARKINSONISM;

CEREBELLAR DISEASES; DIAGNOSIS, DIFFERENTIAL; DOPAMINE; HUMANS; OLFACTION DISORDERS; OLFACTORY BULB; PARKINSONIAN DISORDERS; SMELL;

EID: 4043098888     PISSN: 13507540     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.wco.0000137531.76491.c2     Document Type: Review

References (80)

1. Constandinidis J, de Ajuriaguerra J. Familial syndrome with parkinsonian tremor and anosmia and its therapy with L-dopa associated with a decarboxylase inhibitor. Therapeutique 1970; 46:263-269.
2. Ansari KA, Johnson A. Olfactory function in patients with Parkinson's disease. J Chron Dis 1975; 28:493-497.
3. Doty RL, Shaman P, Dann M. Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav 1984; 32:489-502.
4. Doty RL, Bromley SM, Stern MB. Olfactory testing as an aid in the diagnosis of Parkinson's disease: development of optimal discrimination criteria. Neurodegeneration 1995; 4:93-97.
5. Hawkes CH. Olfaction in neurodegenerative disease. Mov Disord 2003; 18:364-372. A valuable overview of the topic, which summarizes research results and focuses on their application in clinical practice.
6. Khan NL, Katzenschlager R, Watt H, et al. Olfaction differentiates parkin disease from early-onset parkinsonism and Parkinson's disease. Neurology 2004; 62:1224-1226.
7. Katzenschlager R, Zijlmans J, Evans A, et al. Olfactory function distinguishes vascular parkinsonism from Parkinson's disease. J Neurol Neurosurg Psychiatry 2004; in press.
8. Wenning GK, Shephard B, Hawkes C, et al. Olfactory function in atypical parkinsonian syndromes. Acta Neurol Scand 1995; 91:247-250.
9. Gray AJ, Staples V, Murren K, et al. Olfactory identification is impaired in clinic-based patients with vascular dementia and senile dementia of Alzheimer type. Int J Geriatric Psychiatry 2001; 16:513-517.
10. Parola S, Liberini P. Assessing olfaction in the Italian population: methodology and clinical application. Ital J Neurol Sci 1999; 20:287-296.
11. Doty RL, Marcus A, Lee WW. Development of the 12-item Cross-Cultural Smell Identification Test (CC-SIT). Laryngoscope 1996; 106:353-356.
12. Gouldsmit N, Coleman E, Seckinger RA, et al. A brief smell identification test discriminates between deficit and non-deficit schizophrenia. Psychiatry Res 2003; 120:155-164.
13. Doty RL, Marcus A, Lee WW. Development of the 12-item Cross-Cultural Smell Identification Test (CC-SIT). Laryngoscope 1996; 106:353-356.
14. Double KL, Rowe DB, Hayes M, et al. Identifying the pattern of olfactory deficits in Parkinson disease using the Brief Smell Identification Test. Arch Neurol 2003; 60:545-549.
15. Hummel T, Sekinger B, Wolf SR, et al. 'Sniffin' Sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 1997; 22:39-52.
16. Hawkes CH, Shephard BC. Olfactory evoked responses and identification tests in neurological disease. Ann NY Acad Sci 1998; 855:608-615.
17. Hummel T. Olfactory evoked potentials as a tool to measure progression of Parkinson's disease. In: Chase T, Bedard B, editors. Focus on medicine, vol. 14. New developments in the drug therapy of Parkinson's disease. Oxford: Blackwell Science; 1999; pp. 47-53.
18. Doty RL, Stern MB, Pfeiffer C, et al. Bilateral olfactory dysfunction in early stage treated and untreated idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry 1992; 55:138-142.
19. Doty RL, Deems DA, Stellar S. Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage or disease duration. Neurology 1988; 38:1237-1244.
20. Stern MB, Doty RL, Dotti M, et al. Olfactory function in Parkinson's disease subtypes. Neurology 1994; 44:266-268.
21. Müller A, Reichmann H, Livermore A, Hummel T. Olfactory function in idiopathic Parkinson's disease (IPD): results from cross-sectional studies in IPD patients and long-term follow-up of de-novo IPD patients. J Neural Transm 2002; 109:805-811.
22. Tissingh G, Berendse HW, Bergmans P, et al. Loss of olfaction in de novo and treated Parkinson's disease: possible implications for early diagnosis. Mov Disord 2001; 16:41-46.
23. Sobel N, Prabhakaran V, Hartley CA, et al. Odorant-induced and sniff-induced activation in the cerebellum of the human. J Neurosci 1998; 18:8990-9001.
24. Sobel N, Thomason ME, Stappen I, et al. An impairment in sniffing contributes to the olfactory impairment in Parkinson's disease. Proc Natl Acad Sci U S A 2001; 98:4154-4159.
25. Sobel N, Prabhakaran V, Desmond JE, et al. Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 1998; 392:282-286.
26. Pearce RK, Hawkes CH, Daniel SE. The anterior olfactory nucleus in Parkinson's disease. Mov Disord 1995; 10:283-237.
27. Daniel SE, Hawkes CH. Preliminary diagnosis of Parkinson's disease using olfactory bulb pathology [letter]. Lancet 1992; 340:186.
28. Braak H, Del Tredici K, Rüb U, et al. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003; 24:197-211.
29. Berendse HW, Booij J, Francot CMJE, et al. Subclinical dopaminergic dysfunction in asymptomatic Parkinson's disease patients' relatives with a decreased sense of smell. Ann Neurol 2001; 50:34-41.
30. Harding AJ, Stimson E, Henderson JM, Halliday GM. Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease. Brain 2002; 125:2431-2445.
31. Huisman E, Uylings HBM, Hoogland PV. A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson's disease. Mov Disord 2004; 19:687-692. An interesting study that adds new insights to our incomplete understanding of the pathophysiological basis underlying smell loss in PD.
32. Duchamp-Viret P, Coronas V, Delaleu JC, et al. Dopaminergic modulation of mitral cell activity in the frog olfactory bulb: a combined radioligand binding-electrophysiological study. Neuroscience 1997; 79:203-216.
33. Hsia AY, Vincent JD, Lledo PM. Dopamine depresses synaptic inputs into the olfactory bulb. J Neurophysiol 1999; 82:1082-1085.
34. Barz S, Hummel T, Pauli E, et al. Chemosensory event-related potentials in response to trigeminal and olfactory stimulation in idiopathic Parkinson's disease. Neurology 1997; 49:1424-1431.
35. Hudry J, Thobois S, Broussolle E, et al. Evidence for deficiencies in perceptual and semantic olfactory processes in Parkinson's disease. Chem Senses 2003; 28:537-543. One of the very few studies investigating the central processes involved in olfactory perception in PD.
36. Ondo WG. Olfaction testing in patients with tremor dominant Parkinson's disease: is this a distinct condition? [abstract]. Mov Disord 2003; 18:1093.
37. Kovacs T, Papp MI, Cairns NJ, et al. Olfactory bulb in multiple system atrophy. Mov Disord 2003; 18:938-942.
38. Wenning GK, Shephard B, Magalhaes M, et al. Olfactory function in multiple system atrophy. Neurodegeneration 1993; 2:169-171.
39. Wenning GK, Shephard B, Hawkes C, et al. Olfactory function in progressive supranuclear palsy and corticobasal degeneration. J Neurol Neurosurg Psychiatry 1995; 57:251-252.
40. Abele M, Riet A, Hummel T, et al. Olfactory dysfunction in cerebellar ataxia and multiple system atrophy. J Neurol 2003; 250:1453-1455. This paper adds to our knowledge of cerebellar involvement in olfaction by showing a small but similar magnitude of dysfunction in MSA-c and cerebellar ataxia of unknown aetiology.
41. McShane RH, Nagy Z, Esiri MM, et al. Anosmia in dementia is associated with Lewy bodies rather than Alzheimer's pathology. J Neurol Neurosurg Psychiatry 2001; 70:739-743.
42. Hawkes CH, Shephard BC, Daniel SE. Olfactory dysfunction in Parkinson's disease. J Neurol Neurosurg Psychiatry 1997; 62:436-446.
43. Liberini P, Parola S, Spano PF, Antonini L. Olfaction in Parkinson's disease: methods of assessment and clinical relevance. J Neurol 2000; 247:88-96.
44. Westervelt HJ, Stern RA, Tremonet G. Odor identification deficits in diffuse Lewy body disease. Cogn Behav Neurol 2003; 16:93-99. This paper was the first to use an odour identification test, and provides a valuable contribution to the data available on olfaction in this condition.
45. McKeith I, Mintzer J, Aarsland D, et al. International Psychogeriatric Association Expert Meeting on DLB. Dementia with Lewy bodies. Lancet Neurology 2004; 3:19-28.
46. Richard IH, Papka M, Rubio A, Kurlan R. Parkinson's disease and dementia with Lewy bodies: one disease or two? Mov Disord 2002; 17:1161-1165.
47. Doty RL, Golbe LI, McKeown DA, et al. Olfactory testing differentiates between progressive supranuclear palsy and idiopathic Parkinson's disease. Neurology 1993; 43:962-965.
48. Tsuboi Y, Wszolek ZK, Graff-Radford NR, et al. Tau pathology in the olfactory bulb correlates with Braak stage, Lewy body pathology and apolipoprotein epsilon4. Neuropathol Appl Neurobiol 2003; 29:503-510. An important contribution to the neuropathological literature that helps to explain some of the differences in olfaction found in the Parkinsonian syndromes.
49. Markopoulou K, Larsen KW, Wszolek EK, et al. Olfactory dysfunction in familial parkinsonism. Neurology 1997; 49:1262-1267.
50. Bostanjopoulou S, Katsarou Z, Papdimitriou A, et al. Clinical features of parkinsonian patients with the alpha synuclein (G209A) mutation. Mov Disord 2001; 16:1007-1013.
51. Nordin S, Paulsen JS, Murphy C. Sensory- and memory-mediated olfactory dysfunction in Huntington's disease. J Int Neuropsychol Soc 1995; 1:281-290.
52. Bylsma FW, Moberg PJ, Doty RL, Brandt J. Odor identification in Huntington's disease patients and asymptomatic gene carriers. J Neuropsychiatry Clin Neurosci 1997; 9:598-600.
53. Reuter I, Hu MTM, Andrews TC, et al. Late onset levodopa responsive Huntington's disease with minimal chorea masquerading as Parkinson plus syndrome. J Neurol Neurosurg Psychiatry 2000; 68:238-241.
54. Payami H, Nutt J, Gancher S, et al. SCA2 may present as levodopa-responsive parkinsonism. Mov Disord 2003; 18:425-429.
55. Lu CS, Wu Chou YHW, Yen TC, et al. Dopa-responsive parkinsonism phenotype of spinocerebellar ataxia type 2. Mov Disord 2002; 17:1046-1051.
56. Buhmann C, Bussopulos A, Oechsner M. Dopaminergic response in Parkinsonian phenotype of Machado-Joseph disease. Mov Disord 2003; 18:219-221.
57. Connelly T, Farmer JM, Lynch DR, Doty RL. Olfactory dysfunction in degenerative ataxias. J Neurol Neurosurg Psychiatry 2003; 74:1435-1437. A study undertaken based on the recent recognition of the role of the cerebellum in olfaction. Despite small patient numbers in some diagnostic categories, the results are of interest overall.
58. Hensiek AE, Bhatia K, Hawkes CH. Olfactory function in drug induced parkinsonism. J Neurol 2000; 247 (Suppl.):P303.
59. Booij J, Speelman JD, Horstink MW, et al. The clinical benefit of imaging striatal dopamine transporters with [123I]FP-CIT SPECT in differentiating patients with presynaptic parkinsonism from those with other forms of parkinsonism. Eur J Nucl Med 2001; 28:266-272.
60. Geddes J, Huws R, Pratt P. Olfactory acuity in the positive and negative syndromes of schizophrenics. Biol Psychiatry 1991; 29:774-778.
61. Zijlmans JCM, Thijssen HOM, Vogels OJM, et al. MRI in patients with suspected vascular parkinsonism. Neurology 1995; 45:2183-2188.
62. Zijlmans JCM, Daniel SE, Hughes AJ, et al. A clinico-pathological investigation of vascular parkinsonism (VP), including clinical criteria for the diagnosis of VP. Mov Disord 2004; 19:630-640.
63. Winikates J, Jankovic J. Clinical correlates of vascular parkinsonism. Arch Neurol 1999; 56:98-102.
64. Müller A, Müngersdorf M, Reichmann H, et al. Olfactory function in parkinsonian syndromes. J Clin Neurosci 2002; 9:521-524.
65. Busenbark KL, Huber SJ, Greer G, et al. Olfactory function in essential tremor. Neurology 1992; 42:1631-1632.
66. Louis ED, Jurewicz EC. Olfaction in essential tremor patients with and without isolated rest tremor. Mov Disord 2003; 18:1387-1389. A study comprising a large number of patients, which is in contrast to the previous literature by showing mild olfactory dysfunction in essential tremor.
67. Wills AJ, Jenkins IH, Thompson PD, et al. A positron emission tomography study of cerebral activation associated with essential and writing tremor. Arch Neurol 1995; 52:299-305.
68. Louis ED, Bromley SM, Jurewicz EC, Watner D. Olfactory dysfunction in essential tremor: a deficit unrelated to disease duration or severity. Neurology 2002; 59:1631-1633.
69. Boroojerdi B, Ferbert A, Foltys H, et al. Evidence for a non-orthostatic origin of orthostatic tremor. J Neurol Neurosurg Psychiatry 1999; 66:284-288.
70. Katzenschlager R, Costa D, Gerschlager W, et al. FP-CIT SPECT demonstrates dopaminergic deficit in orthostatic tremor. Ann Neurol 2003; 53:489-496.
71. Olson EJ, Boeve BF, Silber MH. Rapid eye movement sleep behaviour disorder: demographic, clinical and laboratory findings in 93 cases. Brain 2000; 123:331-339.
72. Montgomery EB, Baker KB, Lyons K, Koller WC. Abnormal performance on the PD test battery by asymptomatic first-degree relatives. Neurology 1999; 52:757-762.
73. Jones RD, Donaldson IM. Fractionation of visuoperceptual dysfunction in Parkinson's disease. J Neurol Sci 1995; 131:43-50.
74. Henderson JM, Lu Y, Wang S, et al. Olfactory deficits and sleep disturbances in Parkinson's disease: a case-control survey. J Neurol Neurosurg Psychiatry 2003; 74:956-958.
75. Camicioli R, Grossman SJ, Spencer PS, et al. Discriminating mild parkinsonism: methods for epidemiological research. Mov Disord 2001; 16:33-40.
76. Montgomery EB, Koller WC, LaMantia TJK, et al. Early detection of probable idiopathic Parkinson's disease: I. Development of a diagnostic test battery. Mov Disord 2000; 15:467-473.
77. Montgomery EB, Lyons K, Koller WC. Early detection of probable idiopathic Parkinson's disease: II. A prospective evaluation of a diagnostic test battery. Mov Disord 2000; 15:474-478.
78. Sommer U, Hummel T, Cormann K, et al. Detection of presymptomatic Parkinson's disease: combining smell tests, transcranial sonography, and SPECT. Mov Disord 2004; in press.
79. Leenders KL. Significance of non-presynaptic SPECT tracer methods in Parkinson's disease. Mov Disord 2003; 18 (Suppl. 7):S39-S42.
80. Vodusek DB. Sphincter EMG and differential diagnosis of multiple system atrophy. Mov Disord 2001; 16:600-607.