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Intention Tremor of the Legs in Essential Tremor: Prevalence and Clinical Correlates

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Authors: Meir Kestenbaum MD, Monika Michalec MPH, Qiping Yu PhD, Seth L. Pullman MD andElan D. Louis MD, MSc

Article first published online:  23 OCT 2014 | DOI: 10.1002/mdc3.12099


Abstract

The aim of this study was to estimate the prevalence and assess the clinical correlates of intention tremor in the legs in essential tremor (ET) patients. The cerebellar features of ET are of growing interest to clinical neurologists. Arm tremor has an intentional component in many ET patients. Intention tremor in the legs, however, has never been systematically evaluated. One hundred twenty-eight ET patients were enrolled in a clinical-epidemiological study at Columbia University (New York, NY). A videotaped neurological examination included 10 toe-to-target movements with each foot. Videotapes were independently reviewed by two movement disorder neurologists who noted the presence versus absence of intentional leg tremor. Two patients underwent quantitative computerized tremor analysis to study the physiological characteristics of the tremor. Thirty-five patients (27.3%) had intentional leg tremor; in 21, tremor was unilateral and in 14 it was bilateral. The 35 patients with intentional leg tremor did not differ from the remaining 93 in their clinical characteristics. Analyses comparing the 14 patients with bilateral intentional leg tremor to the 93 with no intentional leg tremor showed trends toward longer disease duration and more-severe intentional arm tremor in the former. Tremor analysis showed a 3-fold increase in average tremor amplitude from movement onset to the point just before touching the target. Our data suggest that intentional leg tremor, another cerebellar feature, is common in ET patients. The tremor may be associated with longer disease duration and more-severe intentional arm tremor, but these preliminary trends need to be assessed in larger study samples.

Essential tremor (ET), the most common tremor disorder,[1, 2] is characterized by kinetic and postural tremors, affecting mainly the arms and hands. Current clinical, neuroimaging, and postmortem data indicate cerebellar involvement in ET.[3-6] The identification and characterization of additional cerebellar features on neurological examination provides further evidence to support this. With this in mind, the cerebellar features of ET are of growing interest to clinical neurologists. Interestingly, the kinetic arm tremor in ET often has an intentional component. Intention tremor is defined as tremor that increases in amplitude as the target is approached during visually guided movements.[7-11] Intention tremor in the arms occurs in 44% to 58% of ET patients.[10, 11] Intention tremor is not limited to the arms, and it occurs in the head in approximately 10% of ET patients.[12] Some forms of tremor in ET are limited to specific body regions (i.e., in ET, rest tremor occurs in the arms, but is not observed in the legs),[13] so we posed the clinical question of whether intention tremor of the legs was a feature of ET. To our knowledge, this has never been assessed formally, and we could find no published data that addressed this question. The aims of this study were to (1) estimate the prevalence of intention tremor in the legs in ET patients and (2) assess its clinical correlates.

 

Patients and Methods

Study Participants and Diagnoses

As described previously, ET patients were enrolled in an ongoing clinical-epidemiological study of ET at Columbia University (New York, NY), which began in 2000.[14] All provided written informed consent approved by the Columbia University Internal Review Board. After a thorough assessment of both questionnaire-derived data and a videotaped neurological examination, ET diagnoses were confirmed by a senior movement disorder neurologist (E.D.L.) based on reliable and validated diagnostic criteria (moderate or greater amplitude kinetic tremor during at least three activities or a head tremor in the absence of Parkinson's disease [PD], dystonia, or another known cause, e.g., thyroid disease, medications, or Wilson's disease).[2]

As described previously,[15] assessment of leg tremor by videotaped neurological examination, began in August 2007. For the current analyses, we selected the 128 patients who had had a digitized videotaped neurological examination after that date. There were also 74 age- and gender-matched controls enrolled in the same study during the same time period who had a digitized videotaped neurological examination; data on intention tremor in the legs in these controls were used as a comparison point.

Study Evaluation

Cases underwent a comprehensive tremor questionnaire. During the questionnaire, age of onset and duration of tremor symptoms were assessed, as well as complaints of leg tremor (“Do you often have an uncontrollable tremor in your leg?”) and family history of tremor (first- and second-degree relatives). Reported frequency of falls in the last year was assessed (“How many falls have you had in the past year?”).

The videotaped neurological examination included detailed assessments of postural, kinetic, and intention tremor in the arms. The severity of postural and kinetic tremor in the arms (total tremor score: range = 0–36) was based on the 0 to 3 ratings of six tasks with each arm. As in previous studies,[10] intention tremor (i.e., tremor that occurs with goal-directed movement [finger-nose-finger movement] and worsens when approaching the target) was rated as 0 (absent), 0.5 (probable), and 1 (definite); severity of intention tremor (two arms combined) was therefore graded from 0 to 2. Presence of head and voice tremor was assessed during the videotaped neurological examination.

The study began in 2000; however, assessment of leg tremor during the videotaped neurological examination did not begin until August 2007. Starting at that point, the videotaped neurological examination included an assessment of postural tremor of the legs, as previously described,[15] as well as 10 repetitive toe-to-target movements with each foot. Patients were examined while seated and asked to remove their shoes and socks, although a few preferred to keep their socks on. They were asked to raise their foot from the ground to reach the target (a tongue blade) and touch it with their big toe. The tongue blade was placed at least 16 inches from the ground level (see Videos 1 and 2). The videotapes were reviewed independently by two movement disorder neurologists (M.K. and E.D.L.), who noted the presence versus absence of intention tremor in the legs (i.e., tremor that worsened terminally as the patient's foot was in close proximity to the target). The more junior of the two neurologists (M.K.) was trained by the more senior neurologist (E.D.L.) to conservatively mark the presence of intention tremor in the legs. In the case of disagreements between the neurologists, the videotapes were coreviewed until a consensus was reached. There were 37 instances in which the junior neurologist marked the presence of intention tremor of the legs, but on further assessment by the senior neurologist, the tremor was deemed to be no more than kinetic tremor. There were no other sources of disagreement between the two neurologists.

A 9-m walk was assessed by asking the patient to walk that distance.[16] This task was performed twice and the average time was calculated.

Two subjects with intention tremor of the legs (1 male and 1 female, both with intention tremor of the arms as well) were selected to undergo computerized quantitative tremor analysis using an ultralight piezoresistive miniature accelerometer (±25 g; weight, 1.2 g) with linear sensitivities of approximately 4.5 mV/g in the biological tremor range (0–25 Hz). The accelerometer was attached to the distal phalanx of the great toe. Movement signals were obtained while performing a targeting task with the foot, moving from the floor to a pressure sensitive target cue 80 cm in height.

The tremor acquisition setup allowed for relatively unrestrained activity of the leg and foot throughout testing, approximating the clinical state. Six 10-second trials were obtained per patient. Data from the more affected foot were used in the calculations of averages. Total testing time was approximately 1 hour.

Two channels recorded the accelerometric and target sensor signals. Recordings were digitized at 700 Hz with a 16-bit A/D board, smoothed, and processed. Displacement (tremor amplitude) was derived offline by double integration of accelerometric data after filtering out low-frequency voluntary movements (less than 2 Hz) and averaging. Displacement data were calculated from 0.5-second epochs taken from 100 ms after movement onset and 100 ms before reaching the target sensor. Tremor frequencies were calculated from accelerometry using a fast Fourier transform (FFT) to generate auto spectra.

Statistical Analyses

Statistical analyses were performed using SPSS software (version 21.0; SPSS, Inc., Chicago, IL). Differences between groups were evaluated using Student's t and chi-square tests. Ninety-five percent confidence intervals (CIs) were calculated.

 

Results

Thirty-five (27.3%) of 128 ET patients had intention tremor in the legs (95% CI = 20.3–35.7); by comparison, only 2 (2.7%) of 74 age- and gender-matched controls had such tremor (chi-square test = 19.0; P < 0.001). In 21 (16.4%) of 128 ET patients, tremor was unilateral (in 9 affecting the right leg and in 12 affecting the left leg) and in 14 (10.9%) of 128 it was bilateral. Four (3.1%) ET patients had postural tremor of the legs; 3 of these had intention tremor of the legs. Subject characteristics are summarized in Table 1.
Table 1. Demographic and clinical characteristics of 128 ET patients
Demographics/Characteristics Total Patients Intention Tremor of the Legs No Intention Tremor of the Legs PValue
  1. Values represent means ± standard deviations or numbers (percentages). The P value reports the difference between 35 patients with intention tremor of the legs and 93 without intention tremor of the legs.

  2. a

    Student's t test.

  3. b

    Chi-square test.

No. of ET patients 128 35 93  
Age, years 71.5 ± 12.9 70.5 ± 12.5 71.8 ± 13.1 0.61a
Female gender 66 (51.6) 15 (42.9) 51 (54.8) 0.23a
Duration of symptoms, years 32.5 ± 18.9 35.1 ± 19.6 31.5 ± 18.6 0.36a
Family history of tremor 85 (66.4) 24 (68.6) 61 (65.6) 0.75b
Severity of action tremor in the arms, total tremor score 20.4 ± 6.1 19.9 ± 5.3 20.6 ± 6.4 0.56a
Severity of intention tremor in the arms 0.9 ± 0.7 1.0 ± 0.65 0.85 ± 0.7 0.27a
Presence of head tremor on examination 55 (43.6) 14 (40) 41 (45.0) 0.23b
Presence of voice tremor on examination 35 (27.8) 9 (25.7) 26 (28.6) 0.75b
Complaint of leg tremor by history 16 (12.5) 5 (14.3) 11 (11.8) 0.76b
Reported frequency of falls in the last year 1.0 ± 3.2 1.8 ± 5.6 0.7 ± 1.2 0.26a
9-m walk, seconds 9.6 ± 4.1 9.1 ± 3.6 9.7 ± 4.3 0.55a
 

The 35 patients with intention tremor in the legs did not differ from the remaining 93 patients in age, gender, duration of symptoms, family history of tremor, severity of action tremor in the arms, severity of intention tremor in the arms, presence of head tremor on examination, presence of voice tremor on examination, complaint of leg tremor by history, reported frequency of falls in the last year, or 9-m walk (Table 1). Additional analysis that compared the 14 patients with bilateral intention tremor of the legs to the 93 patients with no intention tremor of the legs showed nonsignificant trends toward longer disease duration (39.4 ± 16.4 vs. 31.5 ± 18.6 years; P = 0.15) and more-severe intentional arm tremor (1.2 ± 0.7 vs. 0.85 ± 0.7; P = 0.09). There was no difference in the reported frequency of falls in the last year (3.6 ± 8.5 vs. 0.7 ± 1.2; P = 0.23).

Computerized tremor analysis showed a 3-fold increase in average tremor amplitude from just after movement onset to just before touching the target. Foot frequency tremor had a peak of approximately 7.0 to 8.5 Hz, reflecting the oscillations in foot position. The frequency is typical of ET range. Tremor analysis findings are summarized in Figure 1.

Tremor analysis findingsFigure 1. (A) Upper panel: movement tracing from 1 patient showing foot position from rest to target. Accelerometric data are sampled at 700 Hz, digitized with a 16-bit A/D board, smoothed, and processed to give displacement. Displacement data are calculated from 0.5-second epochs (solid lines A and B) from just after movement onset (indicated by single arrow) and just before reaching the target sensor (indicated by double arrow). Lower panel: An FFT with a peak of approximately 7.0 to 8.5 Hz at the asterisk (*) reflecting the oscillations in the upper panel in the ET range. Large, low-frequency peak reflects foot movement. (B) Bar graph showing data from 0.5-second epochs from six complete trials showing a 3-fold increase in average tremor amplitude from just after movement onset (corresponding to A) to just before touching the target (corresponding to B).

 

Discussion

Although we have previously studied postural and kinetic tremor in the legs in ET,[15] to our knowledge, this is the first study to assess the prevalence of intention tremor of the legs and its clinical correlates in ET. Our data suggest that intention tremor of the legs is common in ET patients (27.3%), but less common than intentional tremor in the arms (approximately 50%). The 35 patients with intention tremor of the legs did not differ from the remaining 93 in terms of demographics and most clinical features. It is worth mentioning that in the patients with intention tremor of the legs, only a small minority (14.3%) were aware of their leg tremor, suggesting the absence of functional impairment caused by this tremor. The lack of difference in the 9-m walking time also supports this lack of a functional correlate. Tremor analysis showed a significant 3-fold increase in tremor amplitude from movement onset to just before touching the target, thus supporting the clinical observation of an intentional component to the tremor.

A subgroup of 14 patients with bilateral intentional tremor showed nonsignificant trends toward longer disease duration and more-severe intentional arm tremor, when compared to the 93 ET patients without intention tremor of the legs. This finding would be consistent with the view that ET is a progressive disease with the development of other forms of tremor (rest tremor and intention tremors) over time.[17] This needs to be further explored in a longitudinal study, which would allow us to follow individuals over time and assess the change in the prevalence of intention tremor of the legs with time. Furthermore, these preliminary trends need to be assessed in larger study samples.

This article had limitations. First, the tremor analysis was performed on only 2 cases, and though the findings support the clinical results, it would be of value to study a larger number of subjects in order to make a more general set of statements about the physiological properties of this type of tremor in ET. Also, a study of intention tremor of the legs in other disorders, such as tremor predominant PD, would further extend the study of this clinical phenomenology to other settings.

In summary, intention tremor of the legs may be unrecognized, but is common in ET patients, among whom intentional tremors can occur in a variety of other body regions (e.g., arms and head). This and other cerebellar signs may serve as markers of an underlying disorder of cerebellar function in this disease. Whether the intention tremors of ET worsen over time similar to other ET tremors is not known, but this is worthy of study.

 

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