421
Journal of Parkinson’s Disease 4 (2014) 421–430 DOI 10.3233/JPD-130233 IOS Press
Research Report
Kinematic Analysis in Patients with Parkinson’s Disease and SWEDD Myung Jun Lee, Sha Lom Kim, Chul Hyoung Lyoo and Myung Sik Lee∗ Department of Neurology, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea
Abstract. Background and Objectives: The differential diagnosis between mild Parkinson’s disease (PD) and Scan Without Evidence of Dopaminergic Deficit(SWEDD) is challenging. Progressive reduction in amplitude and speed of finger tapping (sequence effect) has been considered as the most useful sign for discriminating PD from SWEDD. However, a video analysis reported that sequence effect is a major confounding factor for the misdiagnosis of PD. Our objective was to perform a kinematic analysis of finger tapping to explore parameters for distinguishing between patients with PD and SWEDD. Methods: We enrolled 14 patients with PD, 17 patients with SWEDD and 18 age- and sex-matched healthy controls. Amplitude, speed and frequency of finger tapping were measured using gyroscopes, and the means, decrement and variability in kinematic parameters for specific tapping duration were calculated. Results: Compared to SWEDD group, PD group showed more decrement in amplitude and speed of the first 20 taps, more decrement in frequency after 20 taps and more variability in speed of 15 seconds of taps. However, none of parameters was a practically useful indicator distinguishing individual patients with PD from those with SWEDD. Conclusions: Analysis of finger tapping, even using an apparatus, is not useful for distinguishing mild PD and SWEDD. Keywords: Parkinson’s disease, SWEDD, finger tapping, kinematic analysis
INTRODUCTION Up to 15% of patients clinically diagnosed by movement disorders specialists with early Parkinson’s disease (PD) may show no evidence of nigrostriatal dopaminergic neuronal loss on functional imaging studies. This neurological condition has been called ‘Scan Without Evidence of Dopaminergic Deficit’ (SWEDD) [1–3]. SWEDD is associated with a variety of neurological conditions, including atypical tremor syndrome, dopa responsive dystonia, vascular parkinsonism, drug induced parkinsonism, postsynaptic parkinsonism, depression, functional parkinsonism, posttraumatic parkinsonism, and Fahr syndrome [3–7]. However, ∗ Correspondence
to: Myung-Sik Lee, MD, Department of Neurology, Gangnam Severance Hospital, Yonsei University College of Medicine, 211 Eonjuro, Gangnam-gu, Seoul, Republic of Korea. Tel.: +82 2 2019 3322; Fax: +82 2 3462 5904; E-mail: mslee@ yuhs.ac.
studies by Schwingenschuh et al. analyzed clinical and electrophysiological features in SWEDD patients, and their results suggest that SWEDD shares similarities with primary dystonia [4, 6]. There has also been report that dystonic tremor mimics PD [8]. Reductions in movement amplitude and speed can be observed in patients with PD, as well as those with pyramidal, extrapyramidal, cerebellar, spinal and lower motor neuron disorders [9, 10]. Thus, UK PD Brain Bank defined true parkinsonian bradykinesia as a combination of slowness of initiation of voluntary movement and progressive reduction in amplitude and speed of repetitive movements (so called ‘decrement and fatigue’ or ‘sequence effect’) [6, 11–13]. The sequence effect is widely accepted as one of the most useful indicators for discriminating PD from SWEDD [6, 7, 14, 15]. The sequence effect can be elicited by various motor tasks, including finger tapping, opening and closing of the hand, hand rolling, hand writing and drawing,
ISSN 1877-7171/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved
422
M.J. Lee et al. / Kinematic Analysis in PD and SWEDD
peg board task, foot tapping and walking [12, 16, 17]. Among them, because of its high sensitivity and specificity for PD, finger tapping is the most commonly used motor examination in the clinic [13, 18, 19]. However, of the Unified PD Rating Scale (UPDRS) items, finger tapping has a low inter- and intra-rater reliability with a Kappa coefficient ranging from 0.4 to 0.6 [20, 21]. A physician’s observation of finger tapping is subjective and insensitive to subtle changes, with greater insensitivity to changes in speed and rhythm than in amplitude [14, 21, 22]. In a blinded video analysis study of 38 patients with uncertain PD, about a third and a half of patients judged as to have true bradykinesia respectively by the two movement disorders specialists showed normal striatal dopamine transporter uptake in functional imaging studies. It was determined that the sequence effect of finger tapping was the most important factor leading to the false positive diagnosis of PD [5]. The analysis of kinematic parameters of finger tapping using a mechanical apparatus should clear off the chaos caused by inherent limitation of human naked eye observation on rapid repetitive movements [10, 21, 22]. However, differences in objective kinematic parameters for finger tapping have not been previously investigated between patients with mild PD and SWEDD. Using gyroscopes, we analyzed finger tapping to determine kinematic parameters for distinguishing between patients with mild PD from SWEDD. SUBJECTS AND METHODS Subjects We recruited 17 patients who were clinically diagnosed with PD, but showed no evidence of dopaminergic deficit on [18 F]–N--fluoro-propyl2-carbomethoxy-3-(4-iodophenyl) nortopane (FPCIT) positron emission tomography (PET) imaging. All of them had very mild dystonic posture changes (10 patients in the neck; three patients in the neck and hands; and four patients in the hand), but did not exhibit other etiologies of parkinsonism such as cerebral infarction, hydrocephalus, brain tumor, drugs or metabolic disorders. We also included 14 de novo PD patients fulfilling UK PD brain bank criteria [11]. Clinical diagnoses was confirmed by reduced putaminal [18 F]-FP CIT uptake in PET studies. Patients were excluded if their action hand tremor interfered with the kinematic analysis of finger tapping. Patients were also excluded if they had a significant medi-
cal comorbidities, cognitive impairment (Mini-Mental State Examination score
Journal of Parkinson’s Disease 4 (2014) 421–430 DOI 10.3233/JPD-130233 IOS Press
Research Report
Kinematic Analysis in Patients with Parkinson’s Disease and SWEDD Myung Jun Lee, Sha Lom Kim, Chul Hyoung Lyoo and Myung Sik Lee∗ Department of Neurology, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea
Abstract. Background and Objectives: The differential diagnosis between mild Parkinson’s disease (PD) and Scan Without Evidence of Dopaminergic Deficit(SWEDD) is challenging. Progressive reduction in amplitude and speed of finger tapping (sequence effect) has been considered as the most useful sign for discriminating PD from SWEDD. However, a video analysis reported that sequence effect is a major confounding factor for the misdiagnosis of PD. Our objective was to perform a kinematic analysis of finger tapping to explore parameters for distinguishing between patients with PD and SWEDD. Methods: We enrolled 14 patients with PD, 17 patients with SWEDD and 18 age- and sex-matched healthy controls. Amplitude, speed and frequency of finger tapping were measured using gyroscopes, and the means, decrement and variability in kinematic parameters for specific tapping duration were calculated. Results: Compared to SWEDD group, PD group showed more decrement in amplitude and speed of the first 20 taps, more decrement in frequency after 20 taps and more variability in speed of 15 seconds of taps. However, none of parameters was a practically useful indicator distinguishing individual patients with PD from those with SWEDD. Conclusions: Analysis of finger tapping, even using an apparatus, is not useful for distinguishing mild PD and SWEDD. Keywords: Parkinson’s disease, SWEDD, finger tapping, kinematic analysis
INTRODUCTION Up to 15% of patients clinically diagnosed by movement disorders specialists with early Parkinson’s disease (PD) may show no evidence of nigrostriatal dopaminergic neuronal loss on functional imaging studies. This neurological condition has been called ‘Scan Without Evidence of Dopaminergic Deficit’ (SWEDD) [1–3]. SWEDD is associated with a variety of neurological conditions, including atypical tremor syndrome, dopa responsive dystonia, vascular parkinsonism, drug induced parkinsonism, postsynaptic parkinsonism, depression, functional parkinsonism, posttraumatic parkinsonism, and Fahr syndrome [3–7]. However, ∗ Correspondence
to: Myung-Sik Lee, MD, Department of Neurology, Gangnam Severance Hospital, Yonsei University College of Medicine, 211 Eonjuro, Gangnam-gu, Seoul, Republic of Korea. Tel.: +82 2 2019 3322; Fax: +82 2 3462 5904; E-mail: mslee@ yuhs.ac.
studies by Schwingenschuh et al. analyzed clinical and electrophysiological features in SWEDD patients, and their results suggest that SWEDD shares similarities with primary dystonia [4, 6]. There has also been report that dystonic tremor mimics PD [8]. Reductions in movement amplitude and speed can be observed in patients with PD, as well as those with pyramidal, extrapyramidal, cerebellar, spinal and lower motor neuron disorders [9, 10]. Thus, UK PD Brain Bank defined true parkinsonian bradykinesia as a combination of slowness of initiation of voluntary movement and progressive reduction in amplitude and speed of repetitive movements (so called ‘decrement and fatigue’ or ‘sequence effect’) [6, 11–13]. The sequence effect is widely accepted as one of the most useful indicators for discriminating PD from SWEDD [6, 7, 14, 15]. The sequence effect can be elicited by various motor tasks, including finger tapping, opening and closing of the hand, hand rolling, hand writing and drawing,
ISSN 1877-7171/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved
422
M.J. Lee et al. / Kinematic Analysis in PD and SWEDD
peg board task, foot tapping and walking [12, 16, 17]. Among them, because of its high sensitivity and specificity for PD, finger tapping is the most commonly used motor examination in the clinic [13, 18, 19]. However, of the Unified PD Rating Scale (UPDRS) items, finger tapping has a low inter- and intra-rater reliability with a Kappa coefficient ranging from 0.4 to 0.6 [20, 21]. A physician’s observation of finger tapping is subjective and insensitive to subtle changes, with greater insensitivity to changes in speed and rhythm than in amplitude [14, 21, 22]. In a blinded video analysis study of 38 patients with uncertain PD, about a third and a half of patients judged as to have true bradykinesia respectively by the two movement disorders specialists showed normal striatal dopamine transporter uptake in functional imaging studies. It was determined that the sequence effect of finger tapping was the most important factor leading to the false positive diagnosis of PD [5]. The analysis of kinematic parameters of finger tapping using a mechanical apparatus should clear off the chaos caused by inherent limitation of human naked eye observation on rapid repetitive movements [10, 21, 22]. However, differences in objective kinematic parameters for finger tapping have not been previously investigated between patients with mild PD and SWEDD. Using gyroscopes, we analyzed finger tapping to determine kinematic parameters for distinguishing between patients with mild PD from SWEDD. SUBJECTS AND METHODS Subjects We recruited 17 patients who were clinically diagnosed with PD, but showed no evidence of dopaminergic deficit on [18 F]–N--fluoro-propyl2-carbomethoxy-3-(4-iodophenyl) nortopane (FPCIT) positron emission tomography (PET) imaging. All of them had very mild dystonic posture changes (10 patients in the neck; three patients in the neck and hands; and four patients in the hand), but did not exhibit other etiologies of parkinsonism such as cerebral infarction, hydrocephalus, brain tumor, drugs or metabolic disorders. We also included 14 de novo PD patients fulfilling UK PD brain bank criteria [11]. Clinical diagnoses was confirmed by reduced putaminal [18 F]-FP CIT uptake in PET studies. Patients were excluded if their action hand tremor interfered with the kinematic analysis of finger tapping. Patients were also excluded if they had a significant medi-
cal comorbidities, cognitive impairment (Mini-Mental State Examination score
