ORIGINAL CONTRIBUTION. Transcranial Brain Sonography Findings in Discriminating Between Parkinsonism and Idiopathic Parkinson Disease
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1 ORIGINAL CONTRIBUTION Transcranial Brain Sonography Findings in Discriminating Between Parkinsonism and Idiopathic Parkinson Disease Uwe Walter, MD; Dirk Dressler, MD; omas Probst, MD; Alexander Wolters, MD; Mazen Abu-Mugheisib, MD; Matthias Wittstock, MD; Reiner Benecke, MD Background: In several pilot studies, transcranial brain sonography findings of substantia nigra and lenticular nucleus discriminated between idiopathic Parkinson disease () and atypical parkinsonian disorders. Objective: To study the use of transcranial brain sonography in excluding the diagnosis of idiopathic in patients with sporadic parkinsonism. Design and Setting: All patients with parkinsonism admitted to our movement disorder clinic from January 1, 2003, through December 31, 2005, who fulfilled clinical diagnostic criteria for definite, probable parkinsonian variant of multiple-system atrophy (MSA-P), or probable progressive supranuclear palsy (PSP) were prospectively studied with transcranial brain sonography by an investigator blinded to clinical diagnoses. Patients: Eligible patients included 138 with sporadic idiopathic (82 men and 56 women; mean±sd age, 67.1±9.8 years; mean±sd disease duration, 7.5±6.3 years; mean±sd motor score on the Unified Parkinson Disease Rating Scale, 32.6±18.1), 21 with MSA-P (10 men and 11 women; mean±sd age, 65.4±9.5 years; mean±sd duration of disease, 3.1±2.0 years; mean±sd motor score, 33.5±16.1), and 22 with PSP (13 men and 9 women; mean±sd age, 71.2±5.5 years; mean±sd duration of disease, 3.4±2.4 years; mean±sd motor score, 46.2±18.9). In 7 patients, transcranial brain sonography was not possible owing to insufficient temporal acoustic bone windows. Main Outcome Measures: Sensitivity, specificity, and predictive value of transcranial brain sonography in indicating an atypical parkinsonian syndrome rather than idiopathic in patients with sporadic parkinsonism. Results: Normal echogenic substantia nigra indicated MSA-P rather than (sensitivity, 90%; specificity, 98%; positive predictive value, 86%), whereas third-ventricle dilatation of more than 10 mm in combination with lenticular nucleus hyperechogenicity indicated PSP rather than (sensitivity, 84%; specificity, 98%; positive predictive value, 89%). Normal echogenic substantia nigra combined with lenticular nucleus hyperechogenicity indicated MSA-P or PSP (sensitivity, 59%; specificity, 100%; positive predictive value, 100%). In parkinsonism with age at onset younger than 60 years, normal echogenic substantia nigra alone indicated MSA-P or PSP (sensitivity, 75%; specificity, 100%; positive predictive value, 100%). Conclusions: Distinct transcranial brain sonography findings can exclude the diagnosis of in patients with sporadic parkinsonism. Sonographic discrimination of atypical parkinsonian syndromes from is clearer in patients with onset of parkinsonism at younger than 60 years. Arch Neurol. 2007;64(11): Author Affiliations: Departments of Neurology, University of Rostock, Rostock, Germany (Drs Walter, Dressler, Probst, Wolters, Abu-Mugheisib, Wittstock, and Benecke), and District Hospital Mainkofen, Deggendorf, Germany (Dr Probst). IDIOPATHIC PARKINSON DISEASE () and atypical parkinsonian syndromes such as the parkinsonian variant of multiple-system atrophy (MSA-P) and progressive supranuclear palsy (PSP) differ in their prognosis and treatment options but may be difficult to differentiate clinically, especially in the early course of the disease. 1,2 Also, levodopa sensitivity is not always conclusive in differentiating these diseases. Sophisticated neuroimaging methods such as routine magnetic resonance imaging, singlephoton emission computed tomography, and positron emission tomography may help to discriminate between and atypical parkinsonian syndromes. Despite the high technical demands and costs of these techniques, sensitivity and specificity are not sufficiently high. 3,4 Recently, transcranial brain sonography (TCS) was reported to discriminate from MSA-P and PSP. 5,6 e TCS finding of substantia nigra hyperechogenicity is characteristic of, 5-9 whereas normal substantia nigra echogenicity in combination with lenticular nucleus hyperechogenicity suggests atypical parkinsonian syndromes. 5,6,10 Substantia nigra hyperechogenicity is thought to reflect 1635
2 Table 1. Demographic Data of Patients Undergoing TCS Patient Group Demographic Data 60 (n=59) 60 (n=79) MSA-P (n=21) PSP (n=22) Sex, M/F 34/25 48/31 10/11 13/9 Age, y Mean±SD 60.1± ± ± ±5.5 Range Age at disease onset, y Mean±SD 49.9± ± ± ±4.7 Range Disease duration, y Mean±SD 10.1± ± ± ±2.4 Range URS-III score, mean±sd 34.6± ± ± ±18.9 Patients not assessable, No. (%) a 2(3) 2(3) 0 2(9) Abbreviations: MSA-P, multiple-system atrophy, parkinsonian variant; 60, idiopathic Parkinson disease with onset at younger than 60 years; 60, idiopathic Parkinson disease with onset at 60 years or older; PSP, progressive supranuclear palsy; TCS, transcranial sonography; URS-III, motor part of the Unified Parkinson Disease Rating Scale. a Patients could not undergo TCS owing to bilateral insufficient acoustic temporal bone windows. A B C D SN a f r d r SN Figure 1. Magnetic resonance imaging (MRI) and transcranial sonography (TCS) studies of axial transsections of the brain at midbrain level in 1 patient with multiple-system atrophy (A and B) and 1 patient with idiopathic Parkinson disease (C and D). A, e MRI corresponding to the image in part B. e square denotes the area to be evaluated in sonography of midbrain structures, as shown in parts B and D. B, e TCS image shows normal substantia nigra (SN) echogenicity in multiple-system atrophy. Within the midbrain (encircled area), only some small echogenic dots in the area of the bilateral SN (arrows) can be visualized. C, Schematic illustration of the area shown in part D (a indicates aqueduct; d, dorsal; f, frontal; and r, raphe). D, e TCS image shows abnormal SN in Parkinson disease. In the area of the bilateral SN (arrows), a marked hyperechogenicity can be seen. 1636
3 increased amounts of iron, bound to proteins other than ferritin in the substantia nigra, and remains unchanged during the course of Also, lenticular nucleus hyperechogenicity is most likely to be caused by increased trace metal content. 5,14,15 Because patients with and substantia nigra hyperechogenicity ( 90% of all patients with ) were found to have a younger age at disease onset (mean±sd, 54±7 years) compared with patients with and normal substantia nigra echogenicity ( 10%; mean±sd, 65±6 years), 7 we hypothesized that sonographic discrimination from atypical parkinsonian syndromes might be clearer in patients with who have onset at younger than 60 years compared with patients with later onset. To further assess the discriminative value of TCS, we studied a larger group of patients with, randomly mixed with patients with MSA-P or PSP. METHODS STUDY POPULATION We prospectively studied all patients with sporadic parkinsonism admitted to our movement disorder clinic from January 1, 2003, through December 31, 2005, who fulfilled the British Brain Bank criteria for definite 16 or the clinical consensus criteria for probable MSA-P or PSP. 1,17 Computed tomography and/or magnetic resonance imaging of the brain and laboratory workup were performed in all patients to exclude other causes of parkinsonism. Altogether, we included the following 181 patients: 138 with idiopathic, 21 with MSA-P, and 22 with PSP. Fifty-nine patients with had disease onset at younger than 60 years (60 patients), and 79, at 60 years or older (60 patients). e TCS findings of some of these patients (60, n=10; 60, n=15; MSA, n=9; PSP, n=6) had contributed to results of a previously published study. 5 Table 1 shows demographic data of the patients studied. TRANSCRANIAL BRAIN SONOGRAPHY We performed TCS through the preauricular acoustic bone windows using a phased-array ultrasound system with a 2.5- MHz transducer (Sonoline; Siemens, Erlangen, Germany). e ultrasound variables chosen were penetration depth of 16 cm, dynamic range of 50 db, and high persistence. Substantia nigra echogenic size measurements were performed on axial TCS images automatically after manually encircling the outer circumference of the echogenic area of the substantia nigra. According to the normal values of substantia nigra echogenic size, obtained by examining 300 healthy adults, the substantia nigra echogenicity was classified into the following 3 groups: group 1, normal substantia nigra echogenicity (echogenic size, 75th percentile of the healthy control group, ie, 0.20 cm 2 ); group 2, moderate substantia nigra hyperechogenicity (echogenic size, 75th-90th percentile); and group 3, marked substantia nigra hyperechogenicity (echogenic size, 90th percentile, ie, 0.25 cm 2 ). 5,7 For classification of patients with respect to their substantia nigra echogenicity, the greater value of bilateral measurements was used. For intergroup comparisons, bilateral substantia nigra echogenic sizes in each individual were used. In addition, echogenicity of the lenticular nucleus was investigated and classified as hyperechogenic when it was more intense than the surrounding white matter. 5,6 Classification of patients with respect to lenticular nucleus echogenicity was based on the more affected side. Because third-ventricle dilatation was previously reported as a TCS finding characteristic of PSP, 10 the minimal width of the third Patients, % SN markedly hyperechogenic SN moderately hyperechogenic MSA-P PSP Clinical Diagnosis ventricle was measured. All TCS examinations were performed by 1 experienced sonographer (U.W.) who was unaware of the clinical diagnosis of the patients. e TCS images of brain structures of all patients were stored and analyzed off-line by a second investigator (T.P. or M.A.-M.) blinded to the diagnoses and clinical data. A given structure was regarded as abnormal on TCS only if the findings of both investigators agreed. STATISTICS Descriptive statistics are given as medians with lower (25th percentile) and upper (75th percentile) quartiles. For group comparison of substantia nigra echogenic sizes, we used the Mann- Whitney test. We analyzed categorial data by means of the 2 test. For comparison of echogenic sizes with age, disease duration, and disease severity, we performed the Spearman rank correlation test. RESULTS SN normal Figure 2. Diagram showing the frequency of normal echogenic substantia nigra (SN), moderately and markedly hyperechogenic SN in patients with idiopathic Parkinson disease () with disease onset at younger than 60 years (60 ), idiopathic with disease onset at 60 years or older (60 ), the parkinsonian variant of multiple-system atrophy (MSA-P), and progressive supranuclear palsy (PSP). None of the 60 patients exhibited normal SN echogenicity. A temporal bone window sufficient for an adequate sonographic analysis of the substantia nigra at least on 1 side was found in 57 of patients, 77 of patients, 21 of 21 patients with MSA-P, and 19 of 22 patients with PSP (96% of all patients). Lenticular nucleus TCS was possible in 54 of patients, 71 of patients, 20 of 21 patients with MSA-P, and 19 of 22 patients with PSP (91% of all patients). ird-ventricle measurement was possible in 57 of patients, 73 of patients, 19 of 21 patients with MSA-P, and 20 of 22 patients with PSP (93% of all patients). In the patients with sufficient temporal acoustic bone windows, moderate or marked substantia nigra hyperechogenicity was found in all 60 patients, patients (96%), 2 patients with MSA-P (10%), and 9 patients with PSP (47%) (Figure 1 and Figure 2). Substantia nigra echogenic sizes were larger in patients with than in those with MSA-P (Mann- Whitney test, P.001) and PSP (P.001). ere was no correlation of substantia nigra echogenic sizes with age, disease severity, or disease duration in either group 1637
4 Table 2. TCS Findings Indicating an Atypical Parkinsonian Syndrome (MSA-P or PSP) Rather an Idiopathic TCS Finding Sensitivity, % a Specificity, % PPV, % P Value b Assessability, % c All Patients (n=181) Normal echogenic SN 72 (90 d ) Normal echogenic SN with hyperechogenic LN 59 (65 d ) Normal/moderately hyperechogenic SN with hyperechogenic LN 77 (79 e ) ird-ventricle width 10 mm and hyperechogenic LN 54 (84 e ) Normal echogenic SN or third-ventricle width 10 mm with hyperechogenic LN Patients With Onset of Parkinsonism at Younger an 60 Years (n=71) Normal echogenic SN Abbreviations: LN, lenticular nucleus; MSA-P, multiple-system atrophy, parkinsonian variant;, Parkinson disease; PPV, positive predictive value; PSP, progressive supranuclear palsy; SN, substantia nigra; TCS, transcranial sonography. a e first percentage refers to discrimination of from the combined group of MSA-P and PSP, whereas the percentage in parentheses refers to discrimination of from only 1 diagnostic group (either MSA-P or PSP, as specified by accompanying footnote). b Calculated by means of the 2 test. c Indicates percentage of patients with adequate bilateral acoustic temporal bone windows for TCS. d Discrimination of MSA from idiopathic. e Discrimination of PSP from idiopathic. Patients, % MSA-P PSP Clinical Diagnosis Figure 3. Diagram showing the frequency of the combined sonographic finding of normal echogenic substantia nigra (SN) and hyperechogenic lenticular nucleus in patients with idiopathic Parkinson disease () with disease onset at younger than 60 years (60 ), idiopathic with disease onset at 60 years or older (60 ), the parkinsonian variant of multiple-system atrophy (MSA-P), and progressive supranuclear palsy (PSP). None of the patients with exhibited this combined finding. (Spearman rank correlation coefficients). Because the 60 patients had a mean disease duration 3 times longer than that of those with MSA-P and PSP, we also compared substantia nigra echogenic sizes of 60 patients with a duration of no longer than 5 years and those with a duration of longer than 5 years and did not find a difference (Spearman rank correlation, P=.20). e finding of normal substantia nigra echogenicity indicated the clinical diagnosis of MSA-P or PSP (ie, not being diagnosed as having ) with a positive predictive value of 91% (Table 2). Normal substantia nigra echogenicity best discriminated MSA-P from (sensitivity, 90%; specificity, 98%; positive predictive value, 86%). In patients with assessable windows and onset of parkinsonism at younger than 60 years (60, n=57; MSA-P, n=10; PSP, n=2), normal substantia nigra echogenicity indicated MSA-P or PSP with a positive predictive value of 100%. Lenticular nucleus hyperechogenicity was found in patients (19%), patients (30%), 15 patients with MSA-P (75%), and 19 patients with PSP (100%). e patients with with and without lenticular nucleus hyperechogenicity did not differ with respect to disease duration, disease severity, age at onset, or motor subtype. Lenticular nucleus hyperechogenicity in combination with normal substantia nigra echogenicity was detected only in 13 patients with MSA-P (65%) and 10 patients with PSP (53%) (Figure 3). Lenticular nucleus hyperechogenicity in combination with normal or moderately hyperechogenic substantia nigra was seen in none of the 60 patients, 4 60 patients (6%), 15 patients with PSP (79%), and 15 patients with MSA-P (75%). ird-ventricle dilatation of more than 10 mm was found in 5 60 patients (9%), 9 60 patients (12%), 4 patients with MSA-P (21%), and 17 patients with PSP (85%). Combination of thirdventricle width of more than 10 mm with lenticular nucleus hyperechogenicity was exhibited in 1 60 patient (2%), 1 60 patient (1%), 4 patients with MSA-P (21%), and 16 patients with PSP (84%) (Figure 4 and Figure 5). ird-ventricle width of more than 10 mm in combination with hyperechogenic lenticular nucleus discriminated PSP from with a positive predictive value of 89% (sensitivity, 84%; specificity, 98%). e finding of hyperechogenic lenticular nucleus in combination with normal echogenic substantia nigra or third-ventricle dilatation of more than 10 mm indicated MSA-P or PSP rather than, with a positive predictive value of 94% (Table 2). e flow diagram in Figure 6 displays the diagnostic algorithm and accuracy of substantia nigra and lenticular nucleus TCS for excluding the diagnosis of idiopathic in patients with sporadic parkinsonism. COMMENT Data obtained in this study show that the combined TCS finding of normal substantia nigra echogenicity 1638
5 A B C CN LN CN LN CN LN Figure 4. Magnetic resonance imaging (MRI) and transcranial sonography (TCS) images of axial transsections of the brain at the thalamus level in 1 patient with idiopathic Parkinson disease (A and B) and 1 patient with progressive supranuclear palsy (C). A, e MRI corresponding to the image in part B. B, e TCS image shows normal width of the third ventricle (double arrow) and normal lenticular nucleus (LN) echogenicity (arrow). C, e TCS image shows characteristic abnormal findings in progressive supranuclear palsy, namely, dilatation of the third ventricle (double arrow) and LN hyperechogenicity in the region of the globus pallidus internus (arrow). CN indicates caudate nucleus;, thalamus Patients with parkinsonism referred to TCS Patients, % MSA-P PSP Clinical Diagnosis Figure 5. Diagram showing the frequency of the combined sonographic finding of third-ventricle dilatation of more than 10 mm and hyperechogenic lenticular nucleus in patients with idiopathic Parkinson disease () with disease onset at younger than 60 years (60 ), idiopathic with disease onset at 60 years or older (60 ), the parkinsonian variant of multiple-system atrophy (MSA-P), and progressive supranuclear palsy (PSP). is combined finding was rare in patients with but frequent in those with PSP. and lenticular nucleus hyperechogenicity excludes the diagnosis of, indicating MSA-P or PSP, with a positive predictive value of 100%. In patients with onset of parkinsonism at younger than 60 years, normal substantia nigra echogenicity alone indicates MSA-P or PSP rather than, with a sensitivity of 75% and a positive predictive value of 100%. We found that MSA-P is best discriminated from by normal substantia nigra echogenicity, whereas PSP is best discriminated from by the combined finding of third-ventricle dilatation of more than 10 mm and lenticular nucleus hyperechogenicity. A limitation of this study is that the diagnosis of MSA-P or PSP in our patients could not be confirmed by postmortem investigation, which is the diagnostic gold standard. We aimed to minimize the liability of a misdiagnosis by including only patients with clinically probable MSA-P or PSP according to current consensus criteria. 1,17 On the basis of the findings of 2 pilot studies that identified the substantia nigra, lenticular nucleus, and third ventricle as the brain structures of most value for sonographic syndrome discrimination, 5,10 in the present study 174 Had TCS 7 With transcranial insonability 145 With age < 60 y 25 With age < 60 y 4 Had an at onset of parkinsonism and hyperechogenic SN, or age 60 y at onset and hyperechogenic SN, or age 60 y at onset and normal echogenic SN combined with normal echogenic LN at onset of parkinsonism and normal echogenic SN or age 60 y at onset and normal echogenic SN combined with hyperechogenic LN inconclusive result: normal echogenic SN and only unilateral assessability of SN and LN 145 Had a clinical 25 Had a clinical 4 Had a clinical diagnosis diagnosis diagnosis 133 With 12 Without 0 With 25 Without 1 With 3 Without Figure 6. Flow diagram showing diagnostic algorithm and accuracy of transcranial sonography (TCS) for excluding the diagnosis of idiopathic Parkinson disease () in patients with sporadic parkinsonism. In each patient, substantia nigra (SN) and lenticular nucleus (LN) echogenicity were assessed bilaterally on TCS. e applied sonographic criteria had a sensitivity of 62% and positive predictive value of 100% in excluding the diagnosis of (ie, indicating an atypical parkinsonian syndrome). these structures were systematically studied in a large sample of patients. In a recent study, only the substantia nigra and lenticular nucleus were investigated, and patients with clinically possible MSA-P and PSP were included. 6 Frequency and distribution of TCS abnormalities of the substantia nigra, lenticular nucleus, and third ventricle found in the present study are in line with previous findings in patients with, MSA-P, and PSP e group of patients with was subdivided according to onset of parkinsonism before 60 years or at 60 years or older because this cutoff value was found to differentiate patients with who had normal and hyperechogenic substantia nigra. 7 Our hypothesis, namely that in 1639
6 parkinsonian patients with age at onset younger than 60 years, the value of normal substantia nigra echogenicity in predicting MSA-P or PSP is higher than in patients with later onset, was confirmed by the present findings. Substantia nigra echogenicity in our patients with was independent of disease duration, which agrees with the findings of a previously reported 5-year follow-up study that demonstrated stable substantia nigra echogenic sizes in patients with. 12 In recent studies, normal substantia nigra echogenicity also separated posttraumatic parkinsonism and essential tremor from idiopathic. 18,19 However, the value of substantia nigra hyperechogenicity alone in predicting the diagnosis of idiopathic in parkinsonian patients is less specific because substantia nigra hyperechogenicity is also frequent in patients with corticobasal degeneration, 10 dementia with Lewy bodies, 20 and parkin-related hereditary parkinsonism. 21,22 In these entities, the additional TCS findings of more pronounced and bilateral symmetric substantia nigra hyperechogenicity or of lenticular nucleus hyperechogenicity may be obtained and may help to discriminate them from. 10,20 Data in this study suggest that distinct TCS findings in parkinsonian patients indicate an atypical parkinsonian syndrome rather than, with a high positive predictive value. Further studies are necessary that compare TCS findings with postmortem histopathological findings in parkinsonian patients. As TCS has the advantages of wide availability, noninvasiveness, and short investigation times, this method might become useful to improve diagnostic accuracy. Accepted for Publication: April 5, Correspondence: Uwe Walter, MD, Department of Neurology, University of Rostock, Gehlsheimer Str 20, D Rostock, Germany (uwe.walter@med.uni-rostock.de). Author Contributions: Study concept and design: Walter. Acquisition of data: Walter, Dressler, Probst, Wolters, Wittstock, and Benecke. Analysis and interpretation of data: Walter, Abu-Mugheisib, and Benecke. Drafting of the manuscript: Walter. Critical revision of the manuscript for important intellectual content: Walter, Dressler, Probst, Wolters, Abu-Mugheisib, Wittstock, and Benecke. Financial Disclosure: None reported. REFERENCES 1. Litvan I, Agid Y, Calne D, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology. 1996;47(1): Wenning GK, Ben-Shlomo Y, Hughes A, Daniel SE, Lees A, Quinn NP. What clinical features are most useful to distinguish definite multiple system atrophy from Parkinson s disease? J Neurol Neurosurg Psychiatry. 2000;68(4): Schrag A, Good CD, Miszkiel K, et al. Differentiation of atypical parkinsonian syndromes with routine MRI. Neurology. 2000;54(3): Ravina B, Eidelberg D, Ahlskog JE, et al. e role of radiotracer imaging in Parkinson disease. Neurology. 2005;64(2): Walter U, Niehaus L, Probst T, Benecke R, Meyer BU, Dressler D. Brain parenchyma sonography discriminates Parkinson s disease and atypical parkinsonian syndromes. Neurology. 2003;60(1): Behnke S, Berg D, Naumann M, Becker G. Differentiation of Parkinson s disease and atypical parkinsonian syndromes by transcranial ultrasound. 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J Neurol Sci. 1999;163(1): Kivi A, Trottenberg T, Kupsch A, Plotkin M, Felix R, Niehaus L. Levodoparesponsive posttraumatic parkinsonism is not associated with changes of echogenicity of the substantia nigra. Mov Disord. 2005;20(2): Stockner H, Sojer M, K KS, et al. Midbrain sonography in patients with essential tremor. Mov Disord. 2007;22(3): Walter U, Dressler D, Wolters A, Wittstock M, Greim B, Benecke R. Sonographic discrimination of dementia with Lewy bodies and Parkinson s disease with dementia. J Neurol. 2006;253(4): Walter U, Klein C, Hilker R, Benecke R, Pramstaller PP, Dressler D. Brain parenchyma sonography detects preclinical parkinsonism. Mov Disord. 2004;19 (12): Hagenah JM, Hedrich K, Becker B, Pramstaller PP, Seidel G, Klein C. Distinguishing early-onset from dopa-responsive dystonia with transcranial sonography. Neurology. 2006;66(12):
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