- Email: [email protected]
Assessment of hand functions in patients with idiopathic cervical dystonia
Human Movement Science 70 (2020) 102581
Contents lists available at ScienceDirect
Human Movement Science journal homepage: www.elsevier.com/locate/humov
Full Length Article
Assessment of hand functions in patients with idiopathic cervical dystonia
T
Pelin Oktayoglua, , Abdullah Acarb, Ibrahim Gunduzc, Mehmet Caglayana, Muhittin Cenk Akbostancid ⁎
a
Dicle University, Faculty of Medicine, Department of Physical Medicine and Rehabilitation, Diyarbakir, Turkey Dicle University, Faculty of Medicine, Department of Neurology, Diyarbakir, Turkey c Health Sciences University, Diyarbakir Gazi Yasargil Training and Research Hospital, Department of Physical Medicine and Rehabilitation, Diyarbakir, Turkey d Ankara University Faculty of Medicine, Department of Neurology, Ankara, Turkey b
ARTICLE INFO
ABSTRACT
Keywords: Cervical dystonia Hand functions Grip strength Pinch strength Fingertip dexterity Quality of life
Cervical dystonia (CD) is the most common form of focal dystonia characterized by involuntary contractions of the neck muscles, causing abnormal rotation of the head into specific directions. Studies report that idiopathic dystonia is a developmental disorder of the sensorimotor circuits, involving both the cortico-striatal and thalamo-cortical pathways. It is also suggested that enhanced cortical plasticity extends beyond the clinically affected region and may also be detected in the unaffected upper limbs of the patient with CD. In the present study, we aimed at exploring if patients with CD had hand motor dysfunctions. Forty patients with idiopathic CD and 40 healthy controls were included in this study. Dystonic symptoms were assessed by means of The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS). Stanford Health Assessment Questionnaire (HAQ) was used to assess functional status. Quality of life (QoL) was assessed by using the Medical Outcomes Study Short Form 36-Item Health Survey (SF 36). Grip strength was assessed by using hand dynamometers. Tip pinch, lateral pinch and chuck pinch of the hand were assessed by using a pinchmeter. Fingertip dexterity and hand coordination was assessed using Purdue Pegboard. Duruoz Hand Index (DHI) was used for the assessment of hand functions. There were no significant differences between the groups in grip and pinch strengths of hands and fingers. As to the fingertip dexterity, patients with CD had a mean Pin 1 and Pin 2 test score of 10.6 ± 2.8 and 10.8 ± 3.2 respectively and a mean assembling test score of 5.2 ± 2.0. These results were significantly worse than those of the healthy controls. As to the SF 36 sub-scores, there were significant differences between the groups in all SF 36 sub-scores (p < .001). This study indicates that patients with CD suffer a deteriorated fine motor coordination of hands without dystonic involvement of upper extremities. Furthermore, lower SF 36 scores in patients with CD suggest poorer health-related quality of life.
1. Introduction Dystonia is a condition characterized by sustained muscle contractions, frequently causing twisting and repeated movements or abnormal postures which lead to failure in proper performance of motor tasks (Breakefield et al., 2008). This abnormality can
⁎
Corresponding author at: Dicle University, Faculty of Medicine, Department of Physical Medicine and Rehabilitation, Diyarbakir, Turkey. E-mail address: [email protected] (P. Oktayoglu).
https://doi.org/10.1016/j.humov.2020.102581 Received 8 September 2019; Received in revised form 23 November 2019; Accepted 8 January 2020 Available online 15 January 2020 0167-9457/ © 2020 Elsevier B.V. All rights reserved.
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
manifest itself in the form of excessive use of the primary muscles that are employed for producing a movement, overflow activation of additional muscles that are not necessary for a given movement, or simultaneous activation of muscles that antagonize the primary muscles. The clinical expression of dystonia is determined according to the severity and distribution of muscles involved (Jinnah, 2015). When classified according to the distribution of muscles, patients are categorized as having focal, segmental, multifocal, generalized, or hemidystonia (Fahn, Bressman, & Marsden, 1988). Cervical dystonia (CD) is the most frequently observed form of focal dystonia that is defined as involuntary and sustained contractions of the neck muscles, causing abnormal rotation or tilt of the head into certain directions (Stacy, 2000). Prevalence estimates vary from 5.7/100000 to 0.4% of the population (Jankovic, Tsui, & Bergeron, 2007). The pathophysiology of CD and other focal dystonias has yet to be fully elucidated. Recently, it has become clear that the role of basal ganglia extends beyond motor control into cognitive and sensory functions and sensorimotor integration (Tinazzi, Fiorio, Fiaschi, Rothwell, & Bhatia, 2009. Data from neuroimaging and electrophysiological experiments in dystonic patients also point to functional impairments in premotor and primary sensorimotor cortical areas as well as aberrant sensorimotor integration, which is believed to be a significant element in the occurrence of focal dystonia (Hinkley, Webster, Byl, & Nagarajan, 2009; Tinazzi, Fiorio, et al., 2009; Tinazzi, Squintani, & Berardelli, 2009). It has been shown that patients with idiopathic dystonia show sensorimotor dysfunction associated with sensorimotor circuits, involving both the cortico-striatal and thalamo-cortical pathways. (Peterson, Sejnowski, & Poizner, 2010; Tinazzi, Fiorio, et al., 2009). Additionally, it has been indicated that abnormalities affect a region that is beyond the sensorimotor circuits that control the affected body (Kanovsky et al., 1998; Pelosin, Bove, Marinelli, Abbruzzese, & Ghilardi, 2009; Walsh & Hutchinson, 2007). Therefore, considering the suggestion that patients with CD show altered sensory motor processing in both clinically affected and non-affected segments of the body, one might find impairments in hand functions despite the absence of clinical involvement of the upper limb muscles. In the light of all these data, we aimed at assessing fine and gross motor dexterity and coordination of hands and fingers and quality of life in patients with isolated idiopathic cervical dystonia. 2. Patients and methods Forty five patients with pure idiopathic cervical dystonia, who were admitted to neurology outpatient clinic between January 2017 and January 2018, and 47 sex- and age-matched healthy controls, who were recruited, based on the date of admission, from among the inpatients' relatives accompanying them in the physical therapy and rehabilitation clinic, were included in this study. Before recruitment, the potential healthy controls were subject to inclusion and exclusion criteria. Clinical evaluations were performed right away in drug-naive patients and at least 3 months after the administration of the last botulinum toxin when complaints reached their peak in the rest of the patients. A withdrawal period of 3 months was employed in order to avoid effects of botulinum toxin that is known to last about three months (Münchau & Bhatia, 2000). None of the study participants, all of whom were examined by an experienced neurologist (AA), had a cognitive impairment or any other psychiatric disease. Exclusion criteria were as follows: being younger than 18 years of age, exhibiting head tremor or dystonia outside the cervical region, not receiving any medication that could affect dystonic symptoms (e.g. benzodiazepines), and having anterocollis, retrocollis, polyneuropathies, radiculopathies, contractures or peripheric nerve entrapments of upper extremities, inflammatory rheumatic diseases, thyroid dysfunctions, hypermobility syndromes, or a history of cerebrovascular accidents. Five female patients in the dystonia group were excluded from the study because of reception of benzodiazepines, and seven patients in the control group withdrew voluntarily because of individual reasons. As a result, forty patients with idiopathic cervical dystonia (28 females and 12 males) and 40 healthy controls (30 females and 10 males) were included in this study. Stanford Health Assessment Questionnaire (HAQ) was used to assess the functional status (Fries, Spitz, Kraines, & Holman, 1980). This scale is used for assessing daily activities. The HAQ is composed of 20 items that include eight functional categories with a score range of 0–3 (index), with higher scores indicating more disability. Activities are marked as 0: no limitation; 1: mild limitation; 2: severe limitation; and 3: complete limitation. Quality of life (QoL) was assessed by using generic questionnaire the Medical Outcomes Study Short Form 36-Item Health Survey (SF 36). (Ware & Sherbourne, 1992). In SF 36 survey, physical functioning, physical health, emotional health, energy, emotional well-being, social functioning, pain and general health sub-scores were calculated. All patients with CD completed The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS) at the time of experimental visit (Consky, Basinki, Belle, Ranawaya, & Lang, 1990). TWSTRS is a standardized assessment tool measuring torticollis severity scale as well as disability and pain scales associated with CD. It is commonly used in clinical trials to assess any change in the severity of CD (Novac, Campbell, Boyce, & Fung, 2010). The severity section is composed of the following six items that are rated by the examiner: maximal excursion, duration, effect of sensory tricks, shoulder elevation/anterior displacement, range of motion, and time. The score range for the severity section is 0 to 38, where zero indicates no dystonia, and 38 indicates severe dystonia. The disability and pain sections consist of self-rated questions related to the extent to which the CD affects the person's ability to work, drive, read, watch television, and conduct activities of daily living (Comella, Bressman, Goetz, & Lang, 1990). 2.1. Assessment of hand functions and fingertip dexterity Grip strength was assessed in both dominant and non-dominant hands for each patient by means of SAEHAN hand dynamometers (Saehan Corp, Masan, Korea). Tip pinch, lateral pinch and chuck pinch of the hand were assessed by means of SAEHAN pinchmeter. The measurements were made in the sitting position, with shoulders adducted and naturally rotated. Elbows were flexed at 90° and forearms were positioned in neutral position. Grip and pinch strengths were measured three times at 30-s intervals for both hands and the average measurement was noted down for each patient (Duruöz, Cerrahoglu, Dincer-Turhan, & Kürsat, 2003; Mathiowetz, 2
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Rennells, & Donahoe, 1985). Pinch strength was measured for both hands using a pinchmeter. Lateral, tip and chuck pinch strengths were measured as in the handgrip strength measurement procedure. The doctor showed the suitable position first, and then the participants pinched as strong as they could for all three forms of pinch strengths (Mathiowetz, Weber, Volland, & Kashman, 1984). Fingertip dexterity and hand coordination was assessed by using the Purdue Pegboard Model # 32020 (Lafayette Instrument Company, IN, USA). Assessments by the Purdue Pegboard were carried out in three parts. First part included picking up the pins with the dominant hand (Pin 1 test) and placing them in grooves in 30 s starting from the top groove. The same procedure was repeated with the non-dominant hand (Pin 2 test) in the second part and finally, the third part included the assembling test. Participants were allowed to practice each test four or five times to make sure they understood the procedure completely. In the first and second parts of the test, the number of pins that were picked up and placed in the grooves was noted. Pins, collars and washers were used in the assembling test. One pin was picked up with the dominant hand and placed in the top groove on the dominant hand side, and then a washer was picked up with the non-dominant hand and placed over the pin. A collar was picked up with the dominant hand and dropped over the pin. While the collar was being dropped over the pin, another washer was picked up with the non-dominant hand and dropped over the collar. This was counted as the first assembling, and then the same procedure was repeated for the next groove. The patients were given 60 s for the assembling test and the number of assemblings was noted down as the assembling test score (Duruöz et al., 2003); (Oktayoglu et al., 2014). Duruoz Hand Index (DHI) was used for the assessment of hand functions (Duruöz et al., 1996). The index consists of 18 questions about activities of daily living that are categorized into 3 groups. The first group represents activities requiring force and rotational motions, the second group represents activities requiring dexterity and precision and the third group represents dynamic activities requiring flexibility of the first 3 fingers. Each item is scored on a 6-point Likert scale (0–5) and the patients are asked about their experience related to these questions during the last week (Duruöz et al., 1996) The study was approved by Dicle University Faculty of Medicine Ethics Committee with the approval no. 30 in 12th January 2017 and conducted in accordance with the Declaration of Helsinki. All participants gave their written informed consent to the study. 2.2. Statistical analysis Student's t-test was used for the comparison of study parameters that met the parametric test criteria. Chi-square test was used to determine the frequency differences between the categorical groups. Correlation analyses were performed by using the Pearson's rank correlation test. A p value smaller than 0.05 was considered statistically significant. All statistical computations were performed with SPSS (Statistical Package for Social Sciences) for Windows Version 18.0 software package. 2.2.1. Statistical power analysis Mean score of dominant hand pin test was determined as 10.6 ± 2.8 and 13.2 ± 2.4 respectively in patient and control groups. The power of statistical analysis for this study was 99.4% according to the given effect size (group means of 10.6 vs. 13.2), SD (2.8 vs 2.4), sample sizes (40 and 40) and alpha (0.050, two tailed). 3. Results The dominant hand was the left hand in two patients with CD. In the control group, on the other hand, there was only one patient with a dominant left hand. There was no significant difference in age (p = .488), gender (p = .446), body mass index (p = .430) and number of menopausal patients (p = .960) between the two groups. Table 1 shows demographic characteristics of the patients and healthy controls. Five of the patients were Botilinum toxin-naive. The groups showed no significant difference in educational levels (p = .612). Nineteen patients had isolated right torticollis whereas 14 had isolated left, and the rest of the patients had both torticollis and laterocollis on opposite or the same sides. TWSTRS scores of the patients with CD are shown in Table 2. The mean right handgrip strength was 47.85 ± 22.48 and 57.10 ± 25.13 kg respectively in patients with CD and healthy controls. There was no significant difference between the two groups in right grip strength (p = .087). On the other hand, the mean left handgrip strength was Table 1 Demographic characteristics of patients with CD and healthy controls.
Age Gender F/M Body mass index Duration of disease (year) Duration of Botilinum toxin treatment (year) Number of menopausal patients Number of patients with left torticollis Number of patients with right torticollis Number of patients with both left torticollis and left laterocollis Number of patients with both right torticollis and right laterocollis Number of patients with one side torticollis and opposite site laterocollis
3
Cervical dystonia
Healthy controls
38.8 ± 12.5 28/12 24.6 ± 3.7 11.6 ± 11.5 4.7 ± 4.0 4/24 14/40 19/40 3/40 1/40 3/40
36.8 ± 12 31/9 25.3 ± 4.6 – – 4/27
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Table 2 Functional characteristics of patients with CD and healthy controls. Clinical parameters
Cervical Dystonia
Healthy Controls
P
Right handgrip strength (mean ± SD) kg/force Left handgrip strength (mean ± SD) Right hand lateral strength (mean ± SD) kg/force Left hand lateral strength (mean ± SD) kg/force Right hand tip strength (mean ± SD) kg/force Left hand tip strength (mean ± SD) kg/force Right hand chuck strength (mean ± SD) kg/force Left hand chuck strength (mean ± SD) kg/force Dominant Hand Pin test score (Pin 1) Non-dominant Hand Pin test score(Pin 2) Assembling test score Duruoz hand index HAQ TWSTRS Torticollis Severity Scale TWSTRS Disability Scale TWSTRS Pain Scale
47.85 ± 22.48 44.65 ± 23.30 12.64 ± 4.42 11.46 ± 3.93 8.21 ± 3.35 7.80 ± 3.04 13.04 ± 4.82 11.89 ± 4.69 10.6 ± 2.8 10.8 ± 3.2 5.2 ± 2.0 19.60 ± 13.28 11.85 ± 8.27 14.42 ± 7.25 16.22 ± 7.31 9.2 ± 3.54
57.10 ± 25.13 54.28 ± 24.42 13.21 ± 5.52 12.33 ± 5.32 9.28 ± 3.56 7.93 ± 2.94 13.87 ± 5.52 12.50 ± 5.41 13.2 ± 2.4 12.8 ± 2.3 7.5 ± 1.3 1.20 ± 1.80 1.05 ± 1.58 – – –
0.087 0.075 0.612 0.408 0.173 0.847 0.475 0.587 0.001⁎ 0.001⁎ 0.001⁎ 0.001⁎ 0.001⁎ – – –
SD: Standard deviation; TWSTRS: The Toronto Western Spasmodic Torticollis Rating Scale; HAQ: Stanford Health Assessment Questionnaire; SD: standard deviation. ⁎ p < .05.
44.65 ± 23.30 and 54.28 ± 24.42 kg respectively in patients with CD and healthy controls. There was no significant difference between the groups in the left handgrip strength, either (p = .075). Similarly, no significant difference was found between the groups in pinch strengths of right and left hands (Table 2). As to the fingertip dexterity, patients with CD had a mean Pin 1 and Pin 2 test score of 10.6 ± 2.8 and 10.8 ± 3.2 respectively and a mean assembling test score of 5.2 ± 2.0. These results were significantly different than those in the healthy controls (Table 2). Moreover, DHI Scores (p < .001) and HAQ scores of the patients with CD were found to be significantly different than those of the healthy controls. Age was found to correlate negatively with the scores of dominant hand pin test (r = −0.340, p = .032), non-dominant hand pin test (r = −0.430 p = .006) and assembling test (r = −0.347, p = .028) in patients with CD. On the other hand, assembling test score correlated positively with right hand lateral strength (r = 0.370 p = .019) and right hand chuck strength (r = 0.365, p = .020) in these patients. There was a correlation between torticollis severity scale (r = 0.301, p = .059) and assembling test score. Duration of disease correlated negatively with scores of both dominant (r = −0.441, p = .004) and non-dominant pin tests (r = 0.552, p < .001). Assembling test score also correlated negatively with duration of disease (r = −0.563, p < .001). Torticollis severity scale (r = −0.335, p = .035) and disability scale (r = −0.324 p = .041) correlated negatively with dominant hand pin test score. There was a strong correlation between torticollis severity scale and DHI (r = 0.463 p = .003). DHI also correlated with disability scale (r = 0.607 p < .001), pain scale (r = 0.328 p = .039), and HAQ (r = 0.800 p < .001). Pain scale showed a correlation with HAQ scores (r = 0.368 p = .019). Correlations among dominant hand pin test, non-dominant hand pin test, assembling test, DHI and HAQ are shown in Table 3. As to the SF 36 sub-scores, all the SF 36 sub-scores showed significant differences between the groups (p < .001). Correlation analysis resulted in the observation of a negative correlation between torticollis severity scale and PF (r = −0.385, p = .014), pain (r = −0.387, p = .014) and general health (r = −0.376, p = .017) sub-scores. There were correlations among disability scale, DHI, HAQ and PF, PH, energy, emotional well-being, SF, pain and general health scores, which are indicated in Table 4. Pain scale did not correlate with any other SF 36 sub-scores than emotional well-being (r = −0.308, p = .053) and pain sub-scores (r = −0.495, p = .001). 4. Discussion This study suggests that patients with CD might suffer impaired fine motor coordination in both upper extremities without experiencing motor weakness despite the absence of clinical involvement of upper extremity muscles. Table 3 Correlations Among Purdue Pegboard Test, DHI and HAQ Scores.
DHI HAQ
Dominant hand pin test score
Non-dominant hand pin test score
Assembling test score
r = −0.429 p = .006⁎ r = −0.342 p = .031⁎
r = −0.369 p = .019⁎ r = −0.335 p = .031⁎
r = −0.481 p = .002⁎ r = −0.355 p = .025⁎
DHI:Duruoz Hand Index; HAQ: Stanford Health Assessment Questionnaire; ⁎p < .05; r: Pearson's correlation coefficient. 4
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Table 4 Correlations Among SF 36, DHI, HAQ and disability scale. SF 36 Sub-scores
DHI
HAQ
Disability Scale
Physical Functioning
r = −0.555 p = .001⁎ r = −0.331 p = .040⁎ r = −0.372 p = .020⁎ r = −0.370 p = .020⁎ r = −0.550 p = .001⁎ r = −0.232 p = .149 r = −0.443 p = .004⁎ r = −0.324 p = .041⁎
r = −0.745 p = .001⁎ r = −0.373 p =−0.019⁎ r = −0.380 p = .017⁎ r = −0.465 p = .003⁎ r = −0.564 p = .001⁎ r = −0.382 p = .015⁎ r = −0.382 p = .005⁎ r = −0.339 p = −0.032⁎
r = −0.452 p = .003⁎ r = −0.242 p = .132 r = −0.361 p = .022⁎ r = −0.384 p = .014⁎ r = −0.383 p = .015⁎ r = −0.395 p = .012⁎ r = −0.589 p = .001⁎ r = −0.508 p = .001⁎
Physical Health Energy Social Functioning Emotional well-being Pain General health Health Change
DHI: Duruoz Hand Index; HAQ: Health Assessment Questionnaire; SF 36:Short Form 36;
⁎
p < .05; r: Pearson's correlation coefficient.
In their study, Thickbroom et al. reported that a reversible reorganization of the corticomotor representation of the clinically unaffected hand muscle might be due to the existence of a more widespread abnormality of motor control in patients with CD (Thickbroom, Byrnes, Stell, & Mastaglia, 2003). It is possible that kinematic impairment is not confined to the dystonic segments as abnormal processing of information from muscle spindles and misinterpretation of positional information is present in both symptomatic and asymptomatic regions in the patients with focal dystonia (Grunewald, Yoneda, Shipman, & Sagar, 1997; Rome & Grunewald, 1999). Results of a recent imaging study provide further support to the hypothesis of a generalized impairment of motor control in patients with CD, showing that the apparently normal execution of hand movements in patients with CD is associated with abnormal patterns of cerebral activation (de Vries et al., 2008). Alterations of sensory motor processing in both clinically affected and unaffected segments might cause abnormalities in hand functions in patients with CD especially in reaching movements similar to those observed in patients with upper limb dystonia. Paracka et al. investigated sensory alterations in patients with isolated idiopathic dystonia and detected subtle sensory impairments in patients' hands. They suggested that clinically silent sensory alterations might be present in patients with dystonia regardless of the presence of overt dystonia in a specific region of the body (Paracka et al., 2017). Pelosin et al. studied trajectory formation of out and back arm reaching movements in patients with CD to see if movements that employed non-dystonic segments showed kinematic abnormalities. They found that patients with CD showed significant trajectory abnormalities when compared to healthy controls. Patients' trajectories were more curved with asymmetrical temporal velocity profiles and increased hand path areas and had longer reversal lags between the out and back segments. They reported that movements performed with non-dystonic segments were abnormal in patients with CD (Pelosin et al., 2009). This result is in agreement with a recent contribution to the literature suggesting a general disorganization of cerebral motor control in patients with CD (de Vries et al., 2008). Delnooz et al. explored if patients with CD had altered functional brain connectivity compared to healthy controls by investigating 10 resting state networks by means of resting state functional MRI that assessed disease related cerebral activity. (Delnooz, Pasman, Beckmann, & van de Warrenburg, 2013). Comparing dystonic patients to healthy controls, they observed reduced functional connectivity in the sensorimotor and primary visual networks as well as increased functional connectivity in the executive network. All these data suggest that reduced connectivity within the sensorimotor and primary visual networks might cause neural substrate to expect defective motor planning and disturbed spatial cognition (Delnooz et al., 2013). Furthermore, increased connectivity within the executive control network is suggestive of excessive attentional control contributing to abnormal motor control, which might alternatively serve as a compensatory function in order to mitigate the consequences of the motor planning defect inflicted by the other network abnormalities (Delnooz et al., 2013). On the other hand, abnormalities of sensorimotor topography were found on both affected and unaffected sides in patients with CD, suggesting the presence of widespread hand muscle abnormalities that might cause a pathophysiological predisposition to the development of dystonic symptoms (Tamburin, Manganotti, Marzi, Fiaschi, & Zanette, 2002). A few previous studies provide evidence of non-motor symptoms in patients with CD in the domain of visuospatial processing. Duane conducted attentional visual search in 108 patients with torticollis and found attentional impairments in nearly half of the patients. (Duane, 1991). Visuospatial attention was also investigated in 23 CD patients by using a line bisection task. Patients with CD were asked to bisect horizontal lines by using their left or right hand. They bisected more to the left of the true center when using their left hand compared to their right hand. (Chillemi et al., 2017). The authors attributed this result to the presence of biased visuospatial attention in patients with CD (Chillemi et al., 2017). Similarly, Leplow and Stubinger found marked deficits of orientation in extrapersonal space in patients with spasmodic torticollis when they followed a specific path drawn on a map (routewalking test) (Leplow & Stubinger, 1994). In addition, patients made atypical displacement errors as they tended to go to the right side when requested to align a rod along an apparent subjective vertical line (Leplow & Stubinger, 1994). 5
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
All of the previously stated findings and alterations of sensory motor processing in both clinically affected and unaffected segments might cause abnormalities in hand functions in patients with CD especially in reaching movements similar to those observed in patients with upper limb dystonia, which may explain delays in placing the pins in the groves and disruptions in assembling test that normally requires attention and fine motor coordination. This may also point to the presence of generalized subclinical sensory abnormalities in patients with dystonia, independent from the region that is clinically involved by dystonia. Patients with idiopathic dystonia experience loss of sensitivity not only in temporal and spatial discrimination but also in unaffected regions of the body (Bradley et al., 2012; Breakefield et al., 2008; Bara-Jimenez, Pm, & Hallett, 2000; Bradley et al., 2012; Fiorio et al., 2008; Molloy, Carr, Zeuner, Dambrosia, & Hallett, 2003; Putzki et al., 2006). The present study indicated a significantly poorer quality of life in patients with CD. All SF-36 sub-scores were found to be poorer in patients with CD. Many physical and emotional factors accompanying cervical dystonia can affect the patient's quality of life (QoL), including pain, abnormal head and neck posture, low self-confidence, depression, anxiety and limited social interaction (Mordin, Masaqeul, Abbott, & Copley-Merriman, 2014). All SF 36 sub-scores, except for physical function, correlated with disability scale. The disability of dystonia may act as a nonspecific stressor and combine with other factors to cause a reduced quality of life. Some authors regard pain caused by cervical dystonia as a contributor to a poorer quality of life but disregard severity and associated disability as significant contributors (Kiss et al., 2007). Physical, social and emotional factors are considered to be the most affected aspects of the quality of life in these patients (Werle, Takeda, Zonta, Guimaraes, & Teive, 2014). An important limitation of the present study was the absence of botulinum toxin injections. Therefore, a ‘before and after injection’ comparison could not be made for fine motor coordination, and potential effects of the given toxin on the motor coordination of the hands could not be observed. We are convinced that patients with isolated cervical dystonia might suffer fine motor impairments in daily life. These impairments can be ignored if the patient's vocation does not require fine motor coordination. On the other hand, this situation might be important in patients engaging in such vocations as microsurgery, handcrafting, playing stringed instruments and hairdressing, which inherently require fine motor coordination of the hands. Further studies employing botulinum toxin injections may shed light on the potential effects of the given toxin on fine motor coordination of the hands in patients with CD. Financial disclosure The authors received no financial support for the research and/or authorship of this article. Authors' roles PO and AA designed the study. PO and IG collected the data. PO and MC analysed the data. PO, AA, IG, MCA interpreted the data. PO drafted the manuscript. PO, AA, IG, MC, MCA critically evaluated and revised the manuscript. Ethical publication statement We confirm that we read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. Declaration of Competing Interest The authors report no conflict of interest. Acknowledgement We would like to extend our gratitude to Sebnem S. Oktayoglu for her contributions to the study planning and typesetting. References Bara-Jimenez, W., Pm, S., & Hallett, M. (2000). Spatial discrimination is abnormal in focal hand dystonia. Neurology, 55(12), 1869–1873. Bradley, D., Whelan, R., Kimmich, O., O’Riordan, S., Mulrooney, N., Brady, P., ... Hutchinson, M. (2012). Temporal discrimination thresholds in adult-onset primary torsion dystonia: An analysis by task type and by dystonia phenotype. Journal of Neurology, 259, 77–82. Breakefield, X. O., Blood, A. J., Li, Y., Hallet, M., Hanson, P. I., & Standaert, E. G. (2008). The pathophysiological basis of dystonias. Nature Reviews. Neuroscience, 9(3), 222–234. Chillemi, G., Formica, C., Salatino, A., Calamuneri, A., Girlanda, P., Morgante, F., ... Ricci, R. (2017). Biased visuospatial attention in cervical dystonia. Journal of the International Neuropsychological Society, 24(1), 22–32. Comella, C., Bressman, S., Goetz, C. G., & Lang, A. E. (1990). The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS) training videotape. Move Disord Soc. Consky, E., Basinki, A., Belle, L., Ranawaya, R., & Lang, A. E. (1990). The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS): Assessment of validity and inter-rater reliability. Neurology, 40(1), 445. Delnooz, C. C., Pasman, J. W., Beckmann, C. F., & van de Warrenburg, B. P. (2013). Task-free functional MRI in cervical dystonia reveals multi-network changes that partially normalize with botulinum toxin. PLoS One, 8(5), e62877. Duane, D. D. (1991). Treatment of spasmodic torticollis. Mayo Clinic Proceedings, 66(9), 969–971. Duruöz, M. T., Cerrahoglu, L., Dincer-Turhan, Y., & Kürsat, S. (2003). Hand function assessment in patients receiving haemodialysis. Swiss Medical Weekly, 133(31−32), 433–438.
6
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Duruöz, M. T., Poiraudeau, S., Fermanian, J., Menkes, C. J., Amor, B., Dougados, M., & Revel, M. (1996). Development and validation of a rheumatoid hand functional disability scale that assesses functional handicap. The Journal of Rheumatology, 23(7), 1167–1172. Fahn, S., Bressman, S. B., & Marsden, C. D. (1988). Classification of dystonia. Advances in Neurology, 78, 1–10. Fiorio, M., Tinazzi, M., Scontrini, A., Stanzani, C., Gambarin, M., Fiaschi, A., ... Berardelli, A. (2008). Tactile temporal discrimination in patients with blepharospasm. Journal of Neurology, Neurosurgery, and Psychiatry, 79, 796–798. Fries, J. F., Spitz, P., Kraines, R., & Holman, H. R. (1980). Measurement of patient outcome in arthritis. Arthritis and Rheumatism, 23(2), 137–145. Grunewald, R. A., Yoneda, Y., Shipman, J. M., & Sagar, H. J. (1997). Idiopathic focal dystonia: A disorder of muscle spindle afferent processing? Brain, 120(Pt 12), 2179–2185. Hinkley, L. B., Webster, R. L., Byl, N. N., & Nagarajan, S. S. (2009). Neuroimaging characteristics of patients with focal hand dystonia. Journal of Hand Therapy, 22(2), 125–134. Jankovic, J., Tsui, J., & Bergeron, C. (2007). Prevalence of cervical dystonia and spasmodic torticollis in the United States general population. Parkinsonism & Related Disorders, 13(7), 411–416. Jinnah, H. A. (2015). Diagnosis & treatment of dystonia. Neurologic Clinics, 33(1), 77–100. Kanovsky, P., Streitova, H., Dufek, J., Znojil, V., Daniel, P., & Rektor, I. (1998). Change in lateralization of the P22/N30 cortical component of median nerve somatosensory evoked potentials in patients with cervical dystonia after successful treatment with botulinum toxin a. Movement Disorders, 13(1), 108–117. Kiss, Z. H., Doig-Beyaert, K., Eliasziw, M., Tsui, J., Haffenden, A., & Suchowersky, O. (2007). The Canadian multicentre study of deep brain stimulation for cervical dystonia. Brain, 130, 2879–2886 Pt 11. Leplow, B., & Stubinger, C. (1994). Visuospatial functions in patients with spasmotic torticollis. Perceptual and Motor Skills, 78(3 Pt 2), 1363–1375. Mathiowetz, V., Rennells, C., & Donahoe, L. (1985). Effect of the elbow position on grip and key pinch strength. Hand Surg (Am), 10(5), 694–697. Mathiowetz, V., Weber, K., Volland, G., & Kashman, N. (1984). Reliability and validity of hand strength evaluations. The Journal of Hand Surgery, 9(2), 222–226. Molloy, F. M., Carr, T. D., Zeuner, K. E., Dambrosia, J. M., & Hallett, M. (2003). Abnormalities of spatial discrimination in focal and generalized dystonia. Brain, 126(Pt 10), 2175–2182. Mordin, M., Masaqeul, C., Abbott, C., & Copley-Merriman, C. (2014). Factors affecting the health-related quality of life of patients with cervical dystonia and impact of treatment with abobotulinumtoxin A (Dysport): Results from a randomized, double-blind, placebocontrolled study. BMJ Open, 16(4), 10. Münchau, A., & Bhatia, K. P. (2000). Uses of botulinum toxin injection in medicine today. BMJ, 320(7228), 161–165. Novac, I., Campbell, L., Boyce, M., & Fung, V. S. C. (2010). Botulinum toxin assessment, intervention and aftercare for cervical dystonia and other causes hypertonia of the neck: International consensus statement. European Journal of Neurology, 17(2), 94e108. Oktayoglu, P., Bozkurt, M., Em, S., Yıldız, M., Uçmak, F., & Nas, K. (2014). Assessment of hand functions in patients with hepatitis B. Erciyes Med J, 36(2), 58–61. Paracka, L., Wegner, F., Blahak, C., Abdallat, M., Saryyeva, A., Dressler, D., ... Krauss, J. K. (2017). Sensory alterations in patients with isolated idiopathic dystonia: An exploratory quantitative sensory testing analysis. Frontiers in Neurology, 17(8), 553. Pelosin, E., Bove, M., Marinelli, L., Abbruzzese, G., & Ghilardi, M. F. (2009). Cervical dystonia affects aimed movements of nondystonic segments. Movement Disorders, 24(13), 1955–1961. Peterson, D. A., Sejnowski, T. J., & Poizner, H. (2010). Convergent evidence for abnormal striatal synaptic plasticity in dystonia. Neurobiology of Disease, 37(3), 558–573. Putzki, N., Stude, P., Konczak, J., Graf, K., Diener, H. C., & Maschke, M. (2006). Kinesthesia is impaired in focal dystonia. Movement Disorders, 21(6), 754–760. Rome, S., & Grunewald, R. A. (1999). Abnormal perception of vibrationinduced illusion of movement in dystonia. Neurology, 53(8), 1794–1800. Stacy, M. (2000). Idiopathic cervical dystonia: an overview. Neurology, 12(5), 2–8. Tamburin, S., Manganotti, P., Marzi, C. A., Fiaschi, A., & Zanette, G. (2002). Abnormal somatotropic arrangement of sensorimotor interactions in dystonic patients. Brain, 125(Pt12), 2719–2730. Thickbroom, G. W., Byrnes, M. L., Stell, R., & Mastaglia, F. L. (2003). Reversible reorganisation of the motor cortical representation of the hand in cervical dystonia. Movement Disorders, 18(4), 395–402. Tinazzi, M., Fiorio, M., Fiaschi, A., Rothwell, J. C., & Bhatia, K. P. (2009). Sensory functions in dystonia: Insights from behavioral studies. Movement Disorders, 24(10), 1427–1436. Tinazzi, M., Squintani, G., & Berardelli, A. (2009). Does neurophysiological testing provide the information we need to improve the clinical management of primary dystonia? Clinical Neurophysiology, 120(8), 1424–1432. de Vries, P. M., Johnson, K. A., de Jong, B. M., Gieteling, E. W., Bohning, D. E., George, M. S., & Leenders, K. L. (2008). Changed patterns of cerebral activation related to clinically normal hand movement in cervical dystonia. Clinical Neurology and Neurosurgery, 110(2), 120–128. Walsh, R., & Hutchinson, M. (2007). Molding the sensory cortex: Spatial acuity improves after botulinum toxin treatment for cervical dystonia. Movement Disorders, 22(16), 2443–2446. Ware, J. E., & Sherbourne, C. D. (1992). The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Medical Care, 30(6), 473–483. Werle, R. W., Takeda, S. Y., Zonta, M. B., Guimaraes, A. T., & Teive, H. A. (2014). The physical, social and emotional aspects are the most affected in the quality of life of the patients with cervical dystonia. Arquivos de Neuro-Psiquiatria, 72(6), 405–410.
7
Contents lists available at ScienceDirect
Human Movement Science journal homepage: www.elsevier.com/locate/humov
Full Length Article
Assessment of hand functions in patients with idiopathic cervical dystonia
T
Pelin Oktayoglua, , Abdullah Acarb, Ibrahim Gunduzc, Mehmet Caglayana, Muhittin Cenk Akbostancid ⁎
a
Dicle University, Faculty of Medicine, Department of Physical Medicine and Rehabilitation, Diyarbakir, Turkey Dicle University, Faculty of Medicine, Department of Neurology, Diyarbakir, Turkey c Health Sciences University, Diyarbakir Gazi Yasargil Training and Research Hospital, Department of Physical Medicine and Rehabilitation, Diyarbakir, Turkey d Ankara University Faculty of Medicine, Department of Neurology, Ankara, Turkey b
ARTICLE INFO
ABSTRACT
Keywords: Cervical dystonia Hand functions Grip strength Pinch strength Fingertip dexterity Quality of life
Cervical dystonia (CD) is the most common form of focal dystonia characterized by involuntary contractions of the neck muscles, causing abnormal rotation of the head into specific directions. Studies report that idiopathic dystonia is a developmental disorder of the sensorimotor circuits, involving both the cortico-striatal and thalamo-cortical pathways. It is also suggested that enhanced cortical plasticity extends beyond the clinically affected region and may also be detected in the unaffected upper limbs of the patient with CD. In the present study, we aimed at exploring if patients with CD had hand motor dysfunctions. Forty patients with idiopathic CD and 40 healthy controls were included in this study. Dystonic symptoms were assessed by means of The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS). Stanford Health Assessment Questionnaire (HAQ) was used to assess functional status. Quality of life (QoL) was assessed by using the Medical Outcomes Study Short Form 36-Item Health Survey (SF 36). Grip strength was assessed by using hand dynamometers. Tip pinch, lateral pinch and chuck pinch of the hand were assessed by using a pinchmeter. Fingertip dexterity and hand coordination was assessed using Purdue Pegboard. Duruoz Hand Index (DHI) was used for the assessment of hand functions. There were no significant differences between the groups in grip and pinch strengths of hands and fingers. As to the fingertip dexterity, patients with CD had a mean Pin 1 and Pin 2 test score of 10.6 ± 2.8 and 10.8 ± 3.2 respectively and a mean assembling test score of 5.2 ± 2.0. These results were significantly worse than those of the healthy controls. As to the SF 36 sub-scores, there were significant differences between the groups in all SF 36 sub-scores (p < .001). This study indicates that patients with CD suffer a deteriorated fine motor coordination of hands without dystonic involvement of upper extremities. Furthermore, lower SF 36 scores in patients with CD suggest poorer health-related quality of life.
1. Introduction Dystonia is a condition characterized by sustained muscle contractions, frequently causing twisting and repeated movements or abnormal postures which lead to failure in proper performance of motor tasks (Breakefield et al., 2008). This abnormality can
⁎
Corresponding author at: Dicle University, Faculty of Medicine, Department of Physical Medicine and Rehabilitation, Diyarbakir, Turkey. E-mail address: [email protected] (P. Oktayoglu).
https://doi.org/10.1016/j.humov.2020.102581 Received 8 September 2019; Received in revised form 23 November 2019; Accepted 8 January 2020 Available online 15 January 2020 0167-9457/ © 2020 Elsevier B.V. All rights reserved.
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
manifest itself in the form of excessive use of the primary muscles that are employed for producing a movement, overflow activation of additional muscles that are not necessary for a given movement, or simultaneous activation of muscles that antagonize the primary muscles. The clinical expression of dystonia is determined according to the severity and distribution of muscles involved (Jinnah, 2015). When classified according to the distribution of muscles, patients are categorized as having focal, segmental, multifocal, generalized, or hemidystonia (Fahn, Bressman, & Marsden, 1988). Cervical dystonia (CD) is the most frequently observed form of focal dystonia that is defined as involuntary and sustained contractions of the neck muscles, causing abnormal rotation or tilt of the head into certain directions (Stacy, 2000). Prevalence estimates vary from 5.7/100000 to 0.4% of the population (Jankovic, Tsui, & Bergeron, 2007). The pathophysiology of CD and other focal dystonias has yet to be fully elucidated. Recently, it has become clear that the role of basal ganglia extends beyond motor control into cognitive and sensory functions and sensorimotor integration (Tinazzi, Fiorio, Fiaschi, Rothwell, & Bhatia, 2009. Data from neuroimaging and electrophysiological experiments in dystonic patients also point to functional impairments in premotor and primary sensorimotor cortical areas as well as aberrant sensorimotor integration, which is believed to be a significant element in the occurrence of focal dystonia (Hinkley, Webster, Byl, & Nagarajan, 2009; Tinazzi, Fiorio, et al., 2009; Tinazzi, Squintani, & Berardelli, 2009). It has been shown that patients with idiopathic dystonia show sensorimotor dysfunction associated with sensorimotor circuits, involving both the cortico-striatal and thalamo-cortical pathways. (Peterson, Sejnowski, & Poizner, 2010; Tinazzi, Fiorio, et al., 2009). Additionally, it has been indicated that abnormalities affect a region that is beyond the sensorimotor circuits that control the affected body (Kanovsky et al., 1998; Pelosin, Bove, Marinelli, Abbruzzese, & Ghilardi, 2009; Walsh & Hutchinson, 2007). Therefore, considering the suggestion that patients with CD show altered sensory motor processing in both clinically affected and non-affected segments of the body, one might find impairments in hand functions despite the absence of clinical involvement of the upper limb muscles. In the light of all these data, we aimed at assessing fine and gross motor dexterity and coordination of hands and fingers and quality of life in patients with isolated idiopathic cervical dystonia. 2. Patients and methods Forty five patients with pure idiopathic cervical dystonia, who were admitted to neurology outpatient clinic between January 2017 and January 2018, and 47 sex- and age-matched healthy controls, who were recruited, based on the date of admission, from among the inpatients' relatives accompanying them in the physical therapy and rehabilitation clinic, were included in this study. Before recruitment, the potential healthy controls were subject to inclusion and exclusion criteria. Clinical evaluations were performed right away in drug-naive patients and at least 3 months after the administration of the last botulinum toxin when complaints reached their peak in the rest of the patients. A withdrawal period of 3 months was employed in order to avoid effects of botulinum toxin that is known to last about three months (Münchau & Bhatia, 2000). None of the study participants, all of whom were examined by an experienced neurologist (AA), had a cognitive impairment or any other psychiatric disease. Exclusion criteria were as follows: being younger than 18 years of age, exhibiting head tremor or dystonia outside the cervical region, not receiving any medication that could affect dystonic symptoms (e.g. benzodiazepines), and having anterocollis, retrocollis, polyneuropathies, radiculopathies, contractures or peripheric nerve entrapments of upper extremities, inflammatory rheumatic diseases, thyroid dysfunctions, hypermobility syndromes, or a history of cerebrovascular accidents. Five female patients in the dystonia group were excluded from the study because of reception of benzodiazepines, and seven patients in the control group withdrew voluntarily because of individual reasons. As a result, forty patients with idiopathic cervical dystonia (28 females and 12 males) and 40 healthy controls (30 females and 10 males) were included in this study. Stanford Health Assessment Questionnaire (HAQ) was used to assess the functional status (Fries, Spitz, Kraines, & Holman, 1980). This scale is used for assessing daily activities. The HAQ is composed of 20 items that include eight functional categories with a score range of 0–3 (index), with higher scores indicating more disability. Activities are marked as 0: no limitation; 1: mild limitation; 2: severe limitation; and 3: complete limitation. Quality of life (QoL) was assessed by using generic questionnaire the Medical Outcomes Study Short Form 36-Item Health Survey (SF 36). (Ware & Sherbourne, 1992). In SF 36 survey, physical functioning, physical health, emotional health, energy, emotional well-being, social functioning, pain and general health sub-scores were calculated. All patients with CD completed The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS) at the time of experimental visit (Consky, Basinki, Belle, Ranawaya, & Lang, 1990). TWSTRS is a standardized assessment tool measuring torticollis severity scale as well as disability and pain scales associated with CD. It is commonly used in clinical trials to assess any change in the severity of CD (Novac, Campbell, Boyce, & Fung, 2010). The severity section is composed of the following six items that are rated by the examiner: maximal excursion, duration, effect of sensory tricks, shoulder elevation/anterior displacement, range of motion, and time. The score range for the severity section is 0 to 38, where zero indicates no dystonia, and 38 indicates severe dystonia. The disability and pain sections consist of self-rated questions related to the extent to which the CD affects the person's ability to work, drive, read, watch television, and conduct activities of daily living (Comella, Bressman, Goetz, & Lang, 1990). 2.1. Assessment of hand functions and fingertip dexterity Grip strength was assessed in both dominant and non-dominant hands for each patient by means of SAEHAN hand dynamometers (Saehan Corp, Masan, Korea). Tip pinch, lateral pinch and chuck pinch of the hand were assessed by means of SAEHAN pinchmeter. The measurements were made in the sitting position, with shoulders adducted and naturally rotated. Elbows were flexed at 90° and forearms were positioned in neutral position. Grip and pinch strengths were measured three times at 30-s intervals for both hands and the average measurement was noted down for each patient (Duruöz, Cerrahoglu, Dincer-Turhan, & Kürsat, 2003; Mathiowetz, 2
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Rennells, & Donahoe, 1985). Pinch strength was measured for both hands using a pinchmeter. Lateral, tip and chuck pinch strengths were measured as in the handgrip strength measurement procedure. The doctor showed the suitable position first, and then the participants pinched as strong as they could for all three forms of pinch strengths (Mathiowetz, Weber, Volland, & Kashman, 1984). Fingertip dexterity and hand coordination was assessed by using the Purdue Pegboard Model # 32020 (Lafayette Instrument Company, IN, USA). Assessments by the Purdue Pegboard were carried out in three parts. First part included picking up the pins with the dominant hand (Pin 1 test) and placing them in grooves in 30 s starting from the top groove. The same procedure was repeated with the non-dominant hand (Pin 2 test) in the second part and finally, the third part included the assembling test. Participants were allowed to practice each test four or five times to make sure they understood the procedure completely. In the first and second parts of the test, the number of pins that were picked up and placed in the grooves was noted. Pins, collars and washers were used in the assembling test. One pin was picked up with the dominant hand and placed in the top groove on the dominant hand side, and then a washer was picked up with the non-dominant hand and placed over the pin. A collar was picked up with the dominant hand and dropped over the pin. While the collar was being dropped over the pin, another washer was picked up with the non-dominant hand and dropped over the collar. This was counted as the first assembling, and then the same procedure was repeated for the next groove. The patients were given 60 s for the assembling test and the number of assemblings was noted down as the assembling test score (Duruöz et al., 2003); (Oktayoglu et al., 2014). Duruoz Hand Index (DHI) was used for the assessment of hand functions (Duruöz et al., 1996). The index consists of 18 questions about activities of daily living that are categorized into 3 groups. The first group represents activities requiring force and rotational motions, the second group represents activities requiring dexterity and precision and the third group represents dynamic activities requiring flexibility of the first 3 fingers. Each item is scored on a 6-point Likert scale (0–5) and the patients are asked about their experience related to these questions during the last week (Duruöz et al., 1996) The study was approved by Dicle University Faculty of Medicine Ethics Committee with the approval no. 30 in 12th January 2017 and conducted in accordance with the Declaration of Helsinki. All participants gave their written informed consent to the study. 2.2. Statistical analysis Student's t-test was used for the comparison of study parameters that met the parametric test criteria. Chi-square test was used to determine the frequency differences between the categorical groups. Correlation analyses were performed by using the Pearson's rank correlation test. A p value smaller than 0.05 was considered statistically significant. All statistical computations were performed with SPSS (Statistical Package for Social Sciences) for Windows Version 18.0 software package. 2.2.1. Statistical power analysis Mean score of dominant hand pin test was determined as 10.6 ± 2.8 and 13.2 ± 2.4 respectively in patient and control groups. The power of statistical analysis for this study was 99.4% according to the given effect size (group means of 10.6 vs. 13.2), SD (2.8 vs 2.4), sample sizes (40 and 40) and alpha (0.050, two tailed). 3. Results The dominant hand was the left hand in two patients with CD. In the control group, on the other hand, there was only one patient with a dominant left hand. There was no significant difference in age (p = .488), gender (p = .446), body mass index (p = .430) and number of menopausal patients (p = .960) between the two groups. Table 1 shows demographic characteristics of the patients and healthy controls. Five of the patients were Botilinum toxin-naive. The groups showed no significant difference in educational levels (p = .612). Nineteen patients had isolated right torticollis whereas 14 had isolated left, and the rest of the patients had both torticollis and laterocollis on opposite or the same sides. TWSTRS scores of the patients with CD are shown in Table 2. The mean right handgrip strength was 47.85 ± 22.48 and 57.10 ± 25.13 kg respectively in patients with CD and healthy controls. There was no significant difference between the two groups in right grip strength (p = .087). On the other hand, the mean left handgrip strength was Table 1 Demographic characteristics of patients with CD and healthy controls.
Age Gender F/M Body mass index Duration of disease (year) Duration of Botilinum toxin treatment (year) Number of menopausal patients Number of patients with left torticollis Number of patients with right torticollis Number of patients with both left torticollis and left laterocollis Number of patients with both right torticollis and right laterocollis Number of patients with one side torticollis and opposite site laterocollis
3
Cervical dystonia
Healthy controls
38.8 ± 12.5 28/12 24.6 ± 3.7 11.6 ± 11.5 4.7 ± 4.0 4/24 14/40 19/40 3/40 1/40 3/40
36.8 ± 12 31/9 25.3 ± 4.6 – – 4/27
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Table 2 Functional characteristics of patients with CD and healthy controls. Clinical parameters
Cervical Dystonia
Healthy Controls
P
Right handgrip strength (mean ± SD) kg/force Left handgrip strength (mean ± SD) Right hand lateral strength (mean ± SD) kg/force Left hand lateral strength (mean ± SD) kg/force Right hand tip strength (mean ± SD) kg/force Left hand tip strength (mean ± SD) kg/force Right hand chuck strength (mean ± SD) kg/force Left hand chuck strength (mean ± SD) kg/force Dominant Hand Pin test score (Pin 1) Non-dominant Hand Pin test score(Pin 2) Assembling test score Duruoz hand index HAQ TWSTRS Torticollis Severity Scale TWSTRS Disability Scale TWSTRS Pain Scale
47.85 ± 22.48 44.65 ± 23.30 12.64 ± 4.42 11.46 ± 3.93 8.21 ± 3.35 7.80 ± 3.04 13.04 ± 4.82 11.89 ± 4.69 10.6 ± 2.8 10.8 ± 3.2 5.2 ± 2.0 19.60 ± 13.28 11.85 ± 8.27 14.42 ± 7.25 16.22 ± 7.31 9.2 ± 3.54
57.10 ± 25.13 54.28 ± 24.42 13.21 ± 5.52 12.33 ± 5.32 9.28 ± 3.56 7.93 ± 2.94 13.87 ± 5.52 12.50 ± 5.41 13.2 ± 2.4 12.8 ± 2.3 7.5 ± 1.3 1.20 ± 1.80 1.05 ± 1.58 – – –
0.087 0.075 0.612 0.408 0.173 0.847 0.475 0.587 0.001⁎ 0.001⁎ 0.001⁎ 0.001⁎ 0.001⁎ – – –
SD: Standard deviation; TWSTRS: The Toronto Western Spasmodic Torticollis Rating Scale; HAQ: Stanford Health Assessment Questionnaire; SD: standard deviation. ⁎ p < .05.
44.65 ± 23.30 and 54.28 ± 24.42 kg respectively in patients with CD and healthy controls. There was no significant difference between the groups in the left handgrip strength, either (p = .075). Similarly, no significant difference was found between the groups in pinch strengths of right and left hands (Table 2). As to the fingertip dexterity, patients with CD had a mean Pin 1 and Pin 2 test score of 10.6 ± 2.8 and 10.8 ± 3.2 respectively and a mean assembling test score of 5.2 ± 2.0. These results were significantly different than those in the healthy controls (Table 2). Moreover, DHI Scores (p < .001) and HAQ scores of the patients with CD were found to be significantly different than those of the healthy controls. Age was found to correlate negatively with the scores of dominant hand pin test (r = −0.340, p = .032), non-dominant hand pin test (r = −0.430 p = .006) and assembling test (r = −0.347, p = .028) in patients with CD. On the other hand, assembling test score correlated positively with right hand lateral strength (r = 0.370 p = .019) and right hand chuck strength (r = 0.365, p = .020) in these patients. There was a correlation between torticollis severity scale (r = 0.301, p = .059) and assembling test score. Duration of disease correlated negatively with scores of both dominant (r = −0.441, p = .004) and non-dominant pin tests (r = 0.552, p < .001). Assembling test score also correlated negatively with duration of disease (r = −0.563, p < .001). Torticollis severity scale (r = −0.335, p = .035) and disability scale (r = −0.324 p = .041) correlated negatively with dominant hand pin test score. There was a strong correlation between torticollis severity scale and DHI (r = 0.463 p = .003). DHI also correlated with disability scale (r = 0.607 p < .001), pain scale (r = 0.328 p = .039), and HAQ (r = 0.800 p < .001). Pain scale showed a correlation with HAQ scores (r = 0.368 p = .019). Correlations among dominant hand pin test, non-dominant hand pin test, assembling test, DHI and HAQ are shown in Table 3. As to the SF 36 sub-scores, all the SF 36 sub-scores showed significant differences between the groups (p < .001). Correlation analysis resulted in the observation of a negative correlation between torticollis severity scale and PF (r = −0.385, p = .014), pain (r = −0.387, p = .014) and general health (r = −0.376, p = .017) sub-scores. There were correlations among disability scale, DHI, HAQ and PF, PH, energy, emotional well-being, SF, pain and general health scores, which are indicated in Table 4. Pain scale did not correlate with any other SF 36 sub-scores than emotional well-being (r = −0.308, p = .053) and pain sub-scores (r = −0.495, p = .001). 4. Discussion This study suggests that patients with CD might suffer impaired fine motor coordination in both upper extremities without experiencing motor weakness despite the absence of clinical involvement of upper extremity muscles. Table 3 Correlations Among Purdue Pegboard Test, DHI and HAQ Scores.
DHI HAQ
Dominant hand pin test score
Non-dominant hand pin test score
Assembling test score
r = −0.429 p = .006⁎ r = −0.342 p = .031⁎
r = −0.369 p = .019⁎ r = −0.335 p = .031⁎
r = −0.481 p = .002⁎ r = −0.355 p = .025⁎
DHI:Duruoz Hand Index; HAQ: Stanford Health Assessment Questionnaire; ⁎p < .05; r: Pearson's correlation coefficient. 4
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Table 4 Correlations Among SF 36, DHI, HAQ and disability scale. SF 36 Sub-scores
DHI
HAQ
Disability Scale
Physical Functioning
r = −0.555 p = .001⁎ r = −0.331 p = .040⁎ r = −0.372 p = .020⁎ r = −0.370 p = .020⁎ r = −0.550 p = .001⁎ r = −0.232 p = .149 r = −0.443 p = .004⁎ r = −0.324 p = .041⁎
r = −0.745 p = .001⁎ r = −0.373 p =−0.019⁎ r = −0.380 p = .017⁎ r = −0.465 p = .003⁎ r = −0.564 p = .001⁎ r = −0.382 p = .015⁎ r = −0.382 p = .005⁎ r = −0.339 p = −0.032⁎
r = −0.452 p = .003⁎ r = −0.242 p = .132 r = −0.361 p = .022⁎ r = −0.384 p = .014⁎ r = −0.383 p = .015⁎ r = −0.395 p = .012⁎ r = −0.589 p = .001⁎ r = −0.508 p = .001⁎
Physical Health Energy Social Functioning Emotional well-being Pain General health Health Change
DHI: Duruoz Hand Index; HAQ: Health Assessment Questionnaire; SF 36:Short Form 36;
⁎
p < .05; r: Pearson's correlation coefficient.
In their study, Thickbroom et al. reported that a reversible reorganization of the corticomotor representation of the clinically unaffected hand muscle might be due to the existence of a more widespread abnormality of motor control in patients with CD (Thickbroom, Byrnes, Stell, & Mastaglia, 2003). It is possible that kinematic impairment is not confined to the dystonic segments as abnormal processing of information from muscle spindles and misinterpretation of positional information is present in both symptomatic and asymptomatic regions in the patients with focal dystonia (Grunewald, Yoneda, Shipman, & Sagar, 1997; Rome & Grunewald, 1999). Results of a recent imaging study provide further support to the hypothesis of a generalized impairment of motor control in patients with CD, showing that the apparently normal execution of hand movements in patients with CD is associated with abnormal patterns of cerebral activation (de Vries et al., 2008). Alterations of sensory motor processing in both clinically affected and unaffected segments might cause abnormalities in hand functions in patients with CD especially in reaching movements similar to those observed in patients with upper limb dystonia. Paracka et al. investigated sensory alterations in patients with isolated idiopathic dystonia and detected subtle sensory impairments in patients' hands. They suggested that clinically silent sensory alterations might be present in patients with dystonia regardless of the presence of overt dystonia in a specific region of the body (Paracka et al., 2017). Pelosin et al. studied trajectory formation of out and back arm reaching movements in patients with CD to see if movements that employed non-dystonic segments showed kinematic abnormalities. They found that patients with CD showed significant trajectory abnormalities when compared to healthy controls. Patients' trajectories were more curved with asymmetrical temporal velocity profiles and increased hand path areas and had longer reversal lags between the out and back segments. They reported that movements performed with non-dystonic segments were abnormal in patients with CD (Pelosin et al., 2009). This result is in agreement with a recent contribution to the literature suggesting a general disorganization of cerebral motor control in patients with CD (de Vries et al., 2008). Delnooz et al. explored if patients with CD had altered functional brain connectivity compared to healthy controls by investigating 10 resting state networks by means of resting state functional MRI that assessed disease related cerebral activity. (Delnooz, Pasman, Beckmann, & van de Warrenburg, 2013). Comparing dystonic patients to healthy controls, they observed reduced functional connectivity in the sensorimotor and primary visual networks as well as increased functional connectivity in the executive network. All these data suggest that reduced connectivity within the sensorimotor and primary visual networks might cause neural substrate to expect defective motor planning and disturbed spatial cognition (Delnooz et al., 2013). Furthermore, increased connectivity within the executive control network is suggestive of excessive attentional control contributing to abnormal motor control, which might alternatively serve as a compensatory function in order to mitigate the consequences of the motor planning defect inflicted by the other network abnormalities (Delnooz et al., 2013). On the other hand, abnormalities of sensorimotor topography were found on both affected and unaffected sides in patients with CD, suggesting the presence of widespread hand muscle abnormalities that might cause a pathophysiological predisposition to the development of dystonic symptoms (Tamburin, Manganotti, Marzi, Fiaschi, & Zanette, 2002). A few previous studies provide evidence of non-motor symptoms in patients with CD in the domain of visuospatial processing. Duane conducted attentional visual search in 108 patients with torticollis and found attentional impairments in nearly half of the patients. (Duane, 1991). Visuospatial attention was also investigated in 23 CD patients by using a line bisection task. Patients with CD were asked to bisect horizontal lines by using their left or right hand. They bisected more to the left of the true center when using their left hand compared to their right hand. (Chillemi et al., 2017). The authors attributed this result to the presence of biased visuospatial attention in patients with CD (Chillemi et al., 2017). Similarly, Leplow and Stubinger found marked deficits of orientation in extrapersonal space in patients with spasmodic torticollis when they followed a specific path drawn on a map (routewalking test) (Leplow & Stubinger, 1994). In addition, patients made atypical displacement errors as they tended to go to the right side when requested to align a rod along an apparent subjective vertical line (Leplow & Stubinger, 1994). 5
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
All of the previously stated findings and alterations of sensory motor processing in both clinically affected and unaffected segments might cause abnormalities in hand functions in patients with CD especially in reaching movements similar to those observed in patients with upper limb dystonia, which may explain delays in placing the pins in the groves and disruptions in assembling test that normally requires attention and fine motor coordination. This may also point to the presence of generalized subclinical sensory abnormalities in patients with dystonia, independent from the region that is clinically involved by dystonia. Patients with idiopathic dystonia experience loss of sensitivity not only in temporal and spatial discrimination but also in unaffected regions of the body (Bradley et al., 2012; Breakefield et al., 2008; Bara-Jimenez, Pm, & Hallett, 2000; Bradley et al., 2012; Fiorio et al., 2008; Molloy, Carr, Zeuner, Dambrosia, & Hallett, 2003; Putzki et al., 2006). The present study indicated a significantly poorer quality of life in patients with CD. All SF-36 sub-scores were found to be poorer in patients with CD. Many physical and emotional factors accompanying cervical dystonia can affect the patient's quality of life (QoL), including pain, abnormal head and neck posture, low self-confidence, depression, anxiety and limited social interaction (Mordin, Masaqeul, Abbott, & Copley-Merriman, 2014). All SF 36 sub-scores, except for physical function, correlated with disability scale. The disability of dystonia may act as a nonspecific stressor and combine with other factors to cause a reduced quality of life. Some authors regard pain caused by cervical dystonia as a contributor to a poorer quality of life but disregard severity and associated disability as significant contributors (Kiss et al., 2007). Physical, social and emotional factors are considered to be the most affected aspects of the quality of life in these patients (Werle, Takeda, Zonta, Guimaraes, & Teive, 2014). An important limitation of the present study was the absence of botulinum toxin injections. Therefore, a ‘before and after injection’ comparison could not be made for fine motor coordination, and potential effects of the given toxin on the motor coordination of the hands could not be observed. We are convinced that patients with isolated cervical dystonia might suffer fine motor impairments in daily life. These impairments can be ignored if the patient's vocation does not require fine motor coordination. On the other hand, this situation might be important in patients engaging in such vocations as microsurgery, handcrafting, playing stringed instruments and hairdressing, which inherently require fine motor coordination of the hands. Further studies employing botulinum toxin injections may shed light on the potential effects of the given toxin on fine motor coordination of the hands in patients with CD. Financial disclosure The authors received no financial support for the research and/or authorship of this article. Authors' roles PO and AA designed the study. PO and IG collected the data. PO and MC analysed the data. PO, AA, IG, MCA interpreted the data. PO drafted the manuscript. PO, AA, IG, MC, MCA critically evaluated and revised the manuscript. Ethical publication statement We confirm that we read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. Declaration of Competing Interest The authors report no conflict of interest. Acknowledgement We would like to extend our gratitude to Sebnem S. Oktayoglu for her contributions to the study planning and typesetting. References Bara-Jimenez, W., Pm, S., & Hallett, M. (2000). Spatial discrimination is abnormal in focal hand dystonia. Neurology, 55(12), 1869–1873. Bradley, D., Whelan, R., Kimmich, O., O’Riordan, S., Mulrooney, N., Brady, P., ... Hutchinson, M. (2012). Temporal discrimination thresholds in adult-onset primary torsion dystonia: An analysis by task type and by dystonia phenotype. Journal of Neurology, 259, 77–82. Breakefield, X. O., Blood, A. J., Li, Y., Hallet, M., Hanson, P. I., & Standaert, E. G. (2008). The pathophysiological basis of dystonias. Nature Reviews. Neuroscience, 9(3), 222–234. Chillemi, G., Formica, C., Salatino, A., Calamuneri, A., Girlanda, P., Morgante, F., ... Ricci, R. (2017). Biased visuospatial attention in cervical dystonia. Journal of the International Neuropsychological Society, 24(1), 22–32. Comella, C., Bressman, S., Goetz, C. G., & Lang, A. E. (1990). The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS) training videotape. Move Disord Soc. Consky, E., Basinki, A., Belle, L., Ranawaya, R., & Lang, A. E. (1990). The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS): Assessment of validity and inter-rater reliability. Neurology, 40(1), 445. Delnooz, C. C., Pasman, J. W., Beckmann, C. F., & van de Warrenburg, B. P. (2013). Task-free functional MRI in cervical dystonia reveals multi-network changes that partially normalize with botulinum toxin. PLoS One, 8(5), e62877. Duane, D. D. (1991). Treatment of spasmodic torticollis. Mayo Clinic Proceedings, 66(9), 969–971. Duruöz, M. T., Cerrahoglu, L., Dincer-Turhan, Y., & Kürsat, S. (2003). Hand function assessment in patients receiving haemodialysis. Swiss Medical Weekly, 133(31−32), 433–438.
6
Human Movement Science 70 (2020) 102581
P. Oktayoglu, et al.
Duruöz, M. T., Poiraudeau, S., Fermanian, J., Menkes, C. J., Amor, B., Dougados, M., & Revel, M. (1996). Development and validation of a rheumatoid hand functional disability scale that assesses functional handicap. The Journal of Rheumatology, 23(7), 1167–1172. Fahn, S., Bressman, S. B., & Marsden, C. D. (1988). Classification of dystonia. Advances in Neurology, 78, 1–10. Fiorio, M., Tinazzi, M., Scontrini, A., Stanzani, C., Gambarin, M., Fiaschi, A., ... Berardelli, A. (2008). Tactile temporal discrimination in patients with blepharospasm. Journal of Neurology, Neurosurgery, and Psychiatry, 79, 796–798. Fries, J. F., Spitz, P., Kraines, R., & Holman, H. R. (1980). Measurement of patient outcome in arthritis. Arthritis and Rheumatism, 23(2), 137–145. Grunewald, R. A., Yoneda, Y., Shipman, J. M., & Sagar, H. J. (1997). Idiopathic focal dystonia: A disorder of muscle spindle afferent processing? Brain, 120(Pt 12), 2179–2185. Hinkley, L. B., Webster, R. L., Byl, N. N., & Nagarajan, S. S. (2009). Neuroimaging characteristics of patients with focal hand dystonia. Journal of Hand Therapy, 22(2), 125–134. Jankovic, J., Tsui, J., & Bergeron, C. (2007). Prevalence of cervical dystonia and spasmodic torticollis in the United States general population. Parkinsonism & Related Disorders, 13(7), 411–416. Jinnah, H. A. (2015). Diagnosis & treatment of dystonia. Neurologic Clinics, 33(1), 77–100. Kanovsky, P., Streitova, H., Dufek, J., Znojil, V., Daniel, P., & Rektor, I. (1998). Change in lateralization of the P22/N30 cortical component of median nerve somatosensory evoked potentials in patients with cervical dystonia after successful treatment with botulinum toxin a. Movement Disorders, 13(1), 108–117. Kiss, Z. H., Doig-Beyaert, K., Eliasziw, M., Tsui, J., Haffenden, A., & Suchowersky, O. (2007). The Canadian multicentre study of deep brain stimulation for cervical dystonia. Brain, 130, 2879–2886 Pt 11. Leplow, B., & Stubinger, C. (1994). Visuospatial functions in patients with spasmotic torticollis. Perceptual and Motor Skills, 78(3 Pt 2), 1363–1375. Mathiowetz, V., Rennells, C., & Donahoe, L. (1985). Effect of the elbow position on grip and key pinch strength. Hand Surg (Am), 10(5), 694–697. Mathiowetz, V., Weber, K., Volland, G., & Kashman, N. (1984). Reliability and validity of hand strength evaluations. The Journal of Hand Surgery, 9(2), 222–226. Molloy, F. M., Carr, T. D., Zeuner, K. E., Dambrosia, J. M., & Hallett, M. (2003). Abnormalities of spatial discrimination in focal and generalized dystonia. Brain, 126(Pt 10), 2175–2182. Mordin, M., Masaqeul, C., Abbott, C., & Copley-Merriman, C. (2014). Factors affecting the health-related quality of life of patients with cervical dystonia and impact of treatment with abobotulinumtoxin A (Dysport): Results from a randomized, double-blind, placebocontrolled study. BMJ Open, 16(4), 10. Münchau, A., & Bhatia, K. P. (2000). Uses of botulinum toxin injection in medicine today. BMJ, 320(7228), 161–165. Novac, I., Campbell, L., Boyce, M., & Fung, V. S. C. (2010). Botulinum toxin assessment, intervention and aftercare for cervical dystonia and other causes hypertonia of the neck: International consensus statement. European Journal of Neurology, 17(2), 94e108. Oktayoglu, P., Bozkurt, M., Em, S., Yıldız, M., Uçmak, F., & Nas, K. (2014). Assessment of hand functions in patients with hepatitis B. Erciyes Med J, 36(2), 58–61. Paracka, L., Wegner, F., Blahak, C., Abdallat, M., Saryyeva, A., Dressler, D., ... Krauss, J. K. (2017). Sensory alterations in patients with isolated idiopathic dystonia: An exploratory quantitative sensory testing analysis. Frontiers in Neurology, 17(8), 553. Pelosin, E., Bove, M., Marinelli, L., Abbruzzese, G., & Ghilardi, M. F. (2009). Cervical dystonia affects aimed movements of nondystonic segments. Movement Disorders, 24(13), 1955–1961. Peterson, D. A., Sejnowski, T. J., & Poizner, H. (2010). Convergent evidence for abnormal striatal synaptic plasticity in dystonia. Neurobiology of Disease, 37(3), 558–573. Putzki, N., Stude, P., Konczak, J., Graf, K., Diener, H. C., & Maschke, M. (2006). Kinesthesia is impaired in focal dystonia. Movement Disorders, 21(6), 754–760. Rome, S., & Grunewald, R. A. (1999). Abnormal perception of vibrationinduced illusion of movement in dystonia. Neurology, 53(8), 1794–1800. Stacy, M. (2000). Idiopathic cervical dystonia: an overview. Neurology, 12(5), 2–8. Tamburin, S., Manganotti, P., Marzi, C. A., Fiaschi, A., & Zanette, G. (2002). Abnormal somatotropic arrangement of sensorimotor interactions in dystonic patients. Brain, 125(Pt12), 2719–2730. Thickbroom, G. W., Byrnes, M. L., Stell, R., & Mastaglia, F. L. (2003). Reversible reorganisation of the motor cortical representation of the hand in cervical dystonia. Movement Disorders, 18(4), 395–402. Tinazzi, M., Fiorio, M., Fiaschi, A., Rothwell, J. C., & Bhatia, K. P. (2009). Sensory functions in dystonia: Insights from behavioral studies. Movement Disorders, 24(10), 1427–1436. Tinazzi, M., Squintani, G., & Berardelli, A. (2009). Does neurophysiological testing provide the information we need to improve the clinical management of primary dystonia? Clinical Neurophysiology, 120(8), 1424–1432. de Vries, P. M., Johnson, K. A., de Jong, B. M., Gieteling, E. W., Bohning, D. E., George, M. S., & Leenders, K. L. (2008). Changed patterns of cerebral activation related to clinically normal hand movement in cervical dystonia. Clinical Neurology and Neurosurgery, 110(2), 120–128. Walsh, R., & Hutchinson, M. (2007). Molding the sensory cortex: Spatial acuity improves after botulinum toxin treatment for cervical dystonia. Movement Disorders, 22(16), 2443–2446. Ware, J. E., & Sherbourne, C. D. (1992). The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Medical Care, 30(6), 473–483. Werle, R. W., Takeda, S. Y., Zonta, M. B., Guimaraes, A. T., & Teive, H. A. (2014). The physical, social and emotional aspects are the most affected in the quality of life of the patients with cervical dystonia. Arquivos de Neuro-Psiquiatria, 72(6), 405–410.
7