CASE SERIES
CLINICAL PRACTICE
Post-Traumatic Shoulder Movement Disorders: A Challenging Differential Diagnosis Between Organic and Functional Sanjay Pandey, MD, DM,1,2 Fatta Nahab, MD,3 Jason Aldred, MD,4 John Nutt, MD,5 Mark Hallett, MD2,*
Abstract: Peripheral trauma may be a trigger for the development of various movement disorders, though the pathophysiology remains controversial and some of these patients have a functional (psychogenic) disorder. We report on 3 cases of shoulder movement disorders subsequent to trauma to the shoulder region. Physiology was done in all the patients to extend the physical examination. Two patients had a history of recurrent shoulder dislocation and were diagnosed with Ehlers-Danlos syndrome. One patient had shoulder injury after repeated falls while performing as a cheerleader. In 2 patients, there were some clinical features suggesting a functional etiology, but physiological studies in all 3 failed to produce objective evidence of a functional nature. Shoulder movement after trauma is uncommon. Diagnosis in such cases is challenging, considering the complex pathophysiology. The movements can be associated with prolonged pain and handicap, and once established, they appear resistant to treatment.
The first report of movement disorders subsequent to peripheral trauma was by Gowers.1 He reported abnormal involuntary movements after an injury of the neck and thumb. Types of peripherally induced movement disorders (PIMDs) are dystonia, tremor, myoclonus, and tics. A commonly suggested mechanism is altered afferent traffic leading to central nervous system changes. Many cases, however, are clearly functional (psychogenic), making it challenging to diagnose such patients. Shoulder movement disorders are not common, and some of the cases have been associated with peripheral trauma.2 Here, we present 3 cases of involuntary, tremulous shoulder movements that seem directly related to repetitive shoulder injury.
Case 1 A 15-year-old right-handed female had marked joint laxity throughout her life and experienced numerous joint dislocations. She was diagnosed with Ehlers-Danlos Syndrome (EDS) type 3 (hypermobility subtype). After multiple episodes of right shoulder dislocation, she experienced pain and paresthesias that improved once the dislocation was reduced. To minimize dislo-
cations, the patient underwent arthroscopic surgery. The patient experienced a poor outcome and developed a neuropathic pain syndrome associated with hyperalgesia, sweating changes, and decreased range of motion consistent with complex regional pain syndrome per Budapest diagnostic criteria.3 The patient underwent rehabilitation and recovered completely within weeks and continued to do well until another right shoulder dislocation. The joint could not be reduced, and the arm was put in a sling for 3 months. When the arm was taken out of the sling, the humerus dislocated and a movement disorder gradually developed over a period of 1 week and then became static. The movement was a repetitive forward-backward motion at the shoulder with a grinding sound (see Video, Case 1). No exacerbating factors were known, and the movements only stopped during sleep. A trial of bupivicaine injections into the affected muscles slightly worsened the spasms. Physical examination showed the persistent rhythmic right shoulder tremor with anterior-posterior motion of the humeral head. The movements were not distractible with other tasks, such as tapping different frequencies with the left hand. MRI of the brain and cervical spine were normal.
1
Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA; Govind Ballabh Pant Hospital, New Delhi, India; 3University of California San Diego, San Diego, California, USA; 4Department of Neurology, Gundersen Health System, La Crosse, Wisconsin, USA; 5Department of Neurology, Oregon Health & Science University, Portland, Orgeon, USA
2
* Correspondence to: Dr. Mark Hallett, Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 10 Center Drive, MSC 1428, Building 10, Room 7D37, Bethesda, MD 20892, USA; E-mail: [email protected]
Keywords: shoulder, movement, physiology, tremor, functional, psychogenic. Relevant disclosures and conflicts of interest are listed at the end of this article. Received 2 January 2014; revised 27 February 2014; accepted 5 March 2014. Published online 19 May 2014 in Wiley InterScience (www.interscience.wiley.com). DOI:10.1002/mdc3.12016
102
© 2014 International Parkinson and Movement Disorder Society doi:10.1002/mdc3.12016
CASE SERIES
Pandey et al.
Surface electromyography (EMG) of proximal right arm muscles captured a 2- to 3-Hz tremor that did not change during cognitive tasks and did not entrain with tapping of the left hand at different frequencies and also did not pause with ballistic movements of the left hand. She was treated with topiramate, clonazepam, gabapentin, and injections of botulinum neurotoxin (BoNT) without any benefit.
Case 2 A 15-year-old female diagnosed with EDS (hypermobility subtype 3) had several episodes of bilateral shoulder dislocation leading to chronic bilateral shoulder pain. In this setting, she developed the gradual onset of rhythmic movement of the right shoulder lasting for 4 months. The movement remitted after relocation of the shoulder. After 2 months, the abnormal movement reappeared, gradually involving both shoulder regions with increased shoulder pain and shoulder dislocation and has persisted. The movements remitted during sleep. There was no family history of movement disorders. Examination was remarkable only for the bilateral semirhythmic anterior-posterior movement of the shoulders (see Video, Case 2). They were intermittently synchronous, and the abnormal movements were decreased by the voluntary effort to reposition her hair. The movements were more jerky and irregular during the postural test. Distraction while doing serial subtraction reduced the amplitude of movements. These features of her movements were suggestive of a functional movement disorder. Sensation and strength were normal in the shoulders. Surface EMG of proximal right and left shoulder muscles captured 3- to 4-Hz tremors that were synchronous in the bilateral pectoral muscles. The patient had poor task performance when asked to tap at different frequencies. A ballistic movement test was difficult to perform because of bilateral movement. She failed trials of BoNT injection, propranolol, primidone, clonazepam, baclofen, cyclobenzaprine, gabapentin, topirimate, and levetiracetam.
Case 3 A 17-year-old female cheerleader in her school had multiple falls leading to shoulder injury and pain in the last 2 years. One year ago, she developed left-sided involuntary shoulder movement after a fall, injuring that shoulder. Movements gradually developed over 1 month, but have been continuous since then. They did not occur during sleep and there was no history of urge. On clinical examination, there was semirhythmic shoulder movement on the left side predominantly in the scapular region (see Video, Case 3). The movement was variable over time, and the video captured a moment with relatively slow irregular movement, but there were also periods of regular movements (1–2 Hz). Physiology experiments were done at a time of regular tremor, which would make it clearer as to whether there might be entrainment or disruption by voluntary movement. Surface EMG of proximal left arm muscles captured a 1- to 2-Hz tremor that did not entrain with right-hand tapping at
different frequencies and did not pause with right ballistic arm movement (Fig. 1A–C). She was treated with BoNT injection without relief.
Discussion The movement disorders in the 3 patients were all semirhythmic shoulder tremors after injury to the shoulder region. The first 2 cases had EDS with a chronic history of shoulder dislocation. The third patient had history of repeated shoulder injury during falls while performing as a cheerleader. There were no features of functional movement disorder in case 1. In case 2, periods of bilateral synchrony and some modification with distraction were suggestive of a functional disorder. The variability of the movement over time in case 3 is also a feature observed in functional disorders. Tremor in all 3 patients was analyzed by surface EMG studies, which objectify what might be discerned clinically. The tremors were not completely rhythmic and did not exhibit significant changes in frequency at different times, even with distraction (although there were changes in amplitude in case 2). In case 2, EMG documented that the tremors were intermittently bilaterally synchronous in the pectoralis muscles, a finding usually indicative of a functional origin. The entrainment test, where a patient is asked to tap at various frequencies using an unaffected body part, is often helpful in differentiating functional and organic tremors. The tremor is modified in functional patients, often taking up the frequency of voluntary tapping. In a study where patients with functional tremor were compared with essential tremor, the tapping task was sensitive (72.7%) and specific (73.3%).4 Tremor could not be entrained in all 3 cases, giving no evidence for a functional disorder. In case 2, however, she was not able to perform the tapping consistently at the given frequency. The failure to be able to tap at requested frequencies can also be a sign of a functional abnormality.4 Tremor monitoring while a patient is making sudden rapid (ballistic) movement using the unaffected part is another way of differentiating organic and psychogenic tremor. In psychogenic tremor, there can be a pause in the tremor activity while doing the ballistic movement. No pause was observed in cases 1 and 3, giving no evidence for a functional abnormality. In case 2, again the patient was not able to do the ballistic movement consistently, so no clear interpretation could be made. Thus, whereas clinical observations in cases 2 and 3 were suggestive of a functional disorder, physiological testing in all 3 cases was unable to add objective evidence other than to confirm some of the clinical observations. There has been published literature on PIMD, including different types of abnormal shoulder movements, but none are similar to ours (Table 1). Criteria have been proposed to diagnose PIMD, and although arbitrary, they do have some heuristic value.7 These criteria include trauma causing local symptoms for at least 2 weeks, initial movement disorder manifestation should anatomically relate to the injury site, and onset of the movement must occur within 1 year after the injury. All our cases had a history of trauma and fulfill these diagnostic criteria. MOVEMENT DISORDERS CLINICAL PRACTICE
doi:10.1002/mdc3.12016
103
CASE SERIES
Shoulder Movement Disorder TABLE 1 Published case series of shoulder movement disorders Case series
Number (male: female)
Side of involvement
Associated illnesses
Abdo et al.6
3 (3:0)
Lee (1999)2
3 (2:1)
Unilateral: 2 Bilateral: 1 Unilateral: 3
Wali (1999)2 Wali (1999)2
2 (2:0) 1 (1:0)
Caviness et al.5
5 (4:1)
Neuralgic amyotrophy Cerebral infarct in 2 patients Cerebral infarct Lower esophagus surgery Wrist injury: 2 Head injury: 1
Unilateral: 2 Right shoulder Unilateral: 2 Bilateral: 3
Please note that the Lee (1999) and Wali (1999) series are both described in detail in reference 2.
TABLE 2 Diagnostic workout to differentiate between organic and psychogenic tremor
Figure 1 (A) Surface EMG of case 3 showing 1- to 2-Hz tremors in the left shoulder. (B) Surface EMG of case 3 showing no entrainment in tremor activity while patient is tapping at 4 Hz using her right hand (R_hand). (C) Surface EMG of case 3 showing no change in tremor activity while doing a ballistic movement using her right hand (R_hand). EMG producing the ballistic movement is indicated with a line under the EMG burst. Left anterior deltoid (L_AntD); supra-spinatus (L_SupS); levator scapulae (L_Lev); rhomboid (L_Rhom); and infra-spinatus (L_infrasp).
Four cases of unusual movement involving the shoulder were reported, characterized by semirhythmic shoulder movements that were attenuated by voluntary activity.5 Emotional stress tended to exacerbate the movement, and, occasionally, the 104
History
Sudden onset or remission; paroxysmal; pain, fatigue, and disability apparently out of proportion to objective findings; variability in body part affected, type of movement, or severity
Physical examination
Variability of the movement; distractibility; entrainment; tremor becoming more severe when visual attention is toward the involved limb
Physiological studies with surface EMG and/or accelerometry
Variability in frequency during distracting cognitive task, such as counting; bilateral synchrony; entrainment of the involuntary movement while tapping using the normal limb at different specified frequencies; poor task performance of the unaffected body part when tapping at specified frequencies; pause in tremor while doing contralateral ballistic movement; increase in tremor frequency on weight loading; coactivation
movements could be completely suppressed, suggesting psychogenicity. Three cases of peripherally induced shoulder movement disorders have also been reported after neuralgic amyotrophy.6 Movement in these patients was slow, and prolonged muscle contractions were similar to dystonia. In a series of patients with surgically corrected cervical radiculopathy, shoulder pain and fixed dystonia later developed. Surprisingly, transcranial sonography revealed hyperechogenic lesions in the lentiform nucleus in the majority of these patients. The proposed mechanism for the development of dystonia in these patients was an interaction between the peripheral nervous system and increased susceptibility to dystonia.8 Task-specific dystonia affecting the shoulder of petanque players resulting in freezing of shoulder flexion was also reported.9 The pathogenesis of PIMD is unknown, but pain and limb immobility have both been considered important, leading to secondary changes in spinal and supraspinal sensorimotor circuits, causing sensory impairments and abnormal central motor response.2 The explanation in a number of patients is clearly
MOVEMENT DISORDERS CLINICAL PRACTICE doi:10.1002/mdc3.12016
CASE SERIES
Pandey et al.
functional, and the differential diagnosis is often challenging. In a review, 713 patients with PIMD were summarized from 133 publications.2 The most common PIMD was fixed dystonia and 15% were thought to be psychogenic, but many authorities would consider this an underestimate. Presence of significant variability, entrainment of the movements, distractibility, and spontaneous recovery should alert the clinicians regarding the possibility of psychogenicity.10 Clinical neurophysiology (Table 2), which can be valuable, is useful only when positive, and firm conclusions cannot be drawn when testing is negative. We still need better methods for definitive diagnosis of functional movement disorders.
Author Roles (1) Research Project: A. Conception, B. Organization, C. Execution; (2) Statistical Analysis: A. Design, B. Execution, C. Review and Critique; (3) Manuscript: A. Writing of the First Draft, B. Review and Critique. S.P.: 1C, 3A, 3B F.N.: 1C, 3B J.A.: 1C, 3B J.N.: 1C, 3B M.H.: 1C, 3B
revenue on US Patent #6 780 413 B2 (issued 24 August 2004): Immunotoxin (MAB-Ricin) for the treatment of focal movement disorders; and US Patent #7 407 478 (issued 5 August 2008): Coil for Magnetic Stimulation and methods for using the same (H-coil); in relation to the latter, he has received license fee payments from the NIH (from Brainsway) for licensing of this patent. He is on the editorial board of 20 journals and received royalties from publishing from Cambridge University Press, Oxford University Press, John Wiley & Sons, Wolters Kluwer, and Elsevier and has received honoraria for lecturing from Columbia University and the Parkinson and Aging Research Foundation. Dr. Hallett’s research at the NIH is largely supported by the NIH Intramural Program. Supplemental research funds came from the Kinetics Foundation, for studies of instrumental methods to monitor Parkinson’s disease, and BCN Peptides, S.A., for treatment studies of blepharospasm.
References 1. Van Rooijen DE, Geraedts EJ, Marinus J, Jankovic J, van Hilten JJ. Peripheral trauma and movement disorders: a systematic review of reported cases. J Neurol Neurosurg Psychiatry 2011 Aug;82:892–898. 2. Aggarwal A, Thompson PD. Unusual focal dyskinesias. Handb Clin Neurol 2011;100:617–628. 3. Harden RN. Objectification of the diagnostic criteria for CRPS. Pain Med 2010;11:1212–1215. 4. Edwards MJ, Bhatia KP. Functional (psychogenic) movement disorders: merging mind and brain. Lancet Neurol 2012;11:250–260.
Acknowledgments The authors are thankful to the patients for participating in these studies.
5. Caviness JN, Gabellini A, Kneebone CS, Thompson PD, Lees AJ, Marsden CD. Unusual focal dyskinesias: the ears, the shoulders, the back, and the abdomen. Mov Disord 1994;9:531–538. 6. Abdo WF, Bloem BR, Eijk JJ, Geurts AC, van Alfen N, van de Warrenburg BP. Atypical dystonic shoulder movements following neuralgic amyotrophy. Mov Disord 2009;24:293–296.
Disclosures
7. Jankovic J. Peripherally induced movement disorders. Neurol Clin 2009;27:821–832.
Funding Sources and Conflicts of Interest: This study was supported by the National Institute of Neurological Disorders and Stroke Intramural Program. The Indo-US Science Technology Forum awarded a fellowship to Dr. Sanjay Pandey to do research in Parkinson’s disease and Movement Disorders at the Human Motor Control Section, National Institute of Neurological Disorders and Stroke, and the National Institutes of Health. The work of Dr. Jason Aldred was supported by a Parkinson’s Disease Research, Education, and Clinical Centers clinical research fellowship through the Department of Veterans Affairs. The authors report no conflicts of interest. Financial Disclosures for previous 12 months: J.A. consulted for Abvvie and received honoraria from Allergan, Ipsen, and Teva Neuroscience. J.N. receives research funding from the Michael J. Fox Foundation, The National Parkinson Foundation, and the National Institutes of Health (NIH). M.H. serves as chair of the medical advisory board for, and receives honoraria and funding for travel from, the Neurotoxin Institute; may accrue
8. Becker G, Berg D, Kruse N, et al. Evidence for shoulder girdle dystonia in selected patients with cervical disc prolapse. Mov Disord 2002;17:710– 716. 9. Lagueny A, Burbaud P, Dubos JL, et al. Freezing of shoulder flexion impeding boule throwing: a form of task-specific focal dystonia in petanque players. Mov Disord 2002;17:1092–1095. 10. Lang AE, Angel M, Bhatia K, et al. Myoclonus in complex regional pain syndrome. Mov Disord 2009;24:314–316.
Supporting Information A video accompanying this article is available in the supporting information here. Video. Case 1: Right shoulder semirhythmic tremor with anterior-posterior motion of humeral head; the movements are not distractible. Case 2: Bilateral semirhythmic anterior-posterior movement of the shoulder: distraction slightly reduced the amplitude of movement. Case 3: Semirhythmic shoulder movement on the left side predominantly in the scapular region.
MOVEMENT DISORDERS CLINICAL PRACTICE doi:10.1002/mdc3.12016
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CLINICAL PRACTICE
Post-Traumatic Shoulder Movement Disorders: A Challenging Differential Diagnosis Between Organic and Functional Sanjay Pandey, MD, DM,1,2 Fatta Nahab, MD,3 Jason Aldred, MD,4 John Nutt, MD,5 Mark Hallett, MD2,*
Abstract: Peripheral trauma may be a trigger for the development of various movement disorders, though the pathophysiology remains controversial and some of these patients have a functional (psychogenic) disorder. We report on 3 cases of shoulder movement disorders subsequent to trauma to the shoulder region. Physiology was done in all the patients to extend the physical examination. Two patients had a history of recurrent shoulder dislocation and were diagnosed with Ehlers-Danlos syndrome. One patient had shoulder injury after repeated falls while performing as a cheerleader. In 2 patients, there were some clinical features suggesting a functional etiology, but physiological studies in all 3 failed to produce objective evidence of a functional nature. Shoulder movement after trauma is uncommon. Diagnosis in such cases is challenging, considering the complex pathophysiology. The movements can be associated with prolonged pain and handicap, and once established, they appear resistant to treatment.
The first report of movement disorders subsequent to peripheral trauma was by Gowers.1 He reported abnormal involuntary movements after an injury of the neck and thumb. Types of peripherally induced movement disorders (PIMDs) are dystonia, tremor, myoclonus, and tics. A commonly suggested mechanism is altered afferent traffic leading to central nervous system changes. Many cases, however, are clearly functional (psychogenic), making it challenging to diagnose such patients. Shoulder movement disorders are not common, and some of the cases have been associated with peripheral trauma.2 Here, we present 3 cases of involuntary, tremulous shoulder movements that seem directly related to repetitive shoulder injury.
Case 1 A 15-year-old right-handed female had marked joint laxity throughout her life and experienced numerous joint dislocations. She was diagnosed with Ehlers-Danlos Syndrome (EDS) type 3 (hypermobility subtype). After multiple episodes of right shoulder dislocation, she experienced pain and paresthesias that improved once the dislocation was reduced. To minimize dislo-
cations, the patient underwent arthroscopic surgery. The patient experienced a poor outcome and developed a neuropathic pain syndrome associated with hyperalgesia, sweating changes, and decreased range of motion consistent with complex regional pain syndrome per Budapest diagnostic criteria.3 The patient underwent rehabilitation and recovered completely within weeks and continued to do well until another right shoulder dislocation. The joint could not be reduced, and the arm was put in a sling for 3 months. When the arm was taken out of the sling, the humerus dislocated and a movement disorder gradually developed over a period of 1 week and then became static. The movement was a repetitive forward-backward motion at the shoulder with a grinding sound (see Video, Case 1). No exacerbating factors were known, and the movements only stopped during sleep. A trial of bupivicaine injections into the affected muscles slightly worsened the spasms. Physical examination showed the persistent rhythmic right shoulder tremor with anterior-posterior motion of the humeral head. The movements were not distractible with other tasks, such as tapping different frequencies with the left hand. MRI of the brain and cervical spine were normal.
1
Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA; Govind Ballabh Pant Hospital, New Delhi, India; 3University of California San Diego, San Diego, California, USA; 4Department of Neurology, Gundersen Health System, La Crosse, Wisconsin, USA; 5Department of Neurology, Oregon Health & Science University, Portland, Orgeon, USA
2
* Correspondence to: Dr. Mark Hallett, Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 10 Center Drive, MSC 1428, Building 10, Room 7D37, Bethesda, MD 20892, USA; E-mail: [email protected]
Keywords: shoulder, movement, physiology, tremor, functional, psychogenic. Relevant disclosures and conflicts of interest are listed at the end of this article. Received 2 January 2014; revised 27 February 2014; accepted 5 March 2014. Published online 19 May 2014 in Wiley InterScience (www.interscience.wiley.com). DOI:10.1002/mdc3.12016
102
© 2014 International Parkinson and Movement Disorder Society doi:10.1002/mdc3.12016
CASE SERIES
Pandey et al.
Surface electromyography (EMG) of proximal right arm muscles captured a 2- to 3-Hz tremor that did not change during cognitive tasks and did not entrain with tapping of the left hand at different frequencies and also did not pause with ballistic movements of the left hand. She was treated with topiramate, clonazepam, gabapentin, and injections of botulinum neurotoxin (BoNT) without any benefit.
Case 2 A 15-year-old female diagnosed with EDS (hypermobility subtype 3) had several episodes of bilateral shoulder dislocation leading to chronic bilateral shoulder pain. In this setting, she developed the gradual onset of rhythmic movement of the right shoulder lasting for 4 months. The movement remitted after relocation of the shoulder. After 2 months, the abnormal movement reappeared, gradually involving both shoulder regions with increased shoulder pain and shoulder dislocation and has persisted. The movements remitted during sleep. There was no family history of movement disorders. Examination was remarkable only for the bilateral semirhythmic anterior-posterior movement of the shoulders (see Video, Case 2). They were intermittently synchronous, and the abnormal movements were decreased by the voluntary effort to reposition her hair. The movements were more jerky and irregular during the postural test. Distraction while doing serial subtraction reduced the amplitude of movements. These features of her movements were suggestive of a functional movement disorder. Sensation and strength were normal in the shoulders. Surface EMG of proximal right and left shoulder muscles captured 3- to 4-Hz tremors that were synchronous in the bilateral pectoral muscles. The patient had poor task performance when asked to tap at different frequencies. A ballistic movement test was difficult to perform because of bilateral movement. She failed trials of BoNT injection, propranolol, primidone, clonazepam, baclofen, cyclobenzaprine, gabapentin, topirimate, and levetiracetam.
Case 3 A 17-year-old female cheerleader in her school had multiple falls leading to shoulder injury and pain in the last 2 years. One year ago, she developed left-sided involuntary shoulder movement after a fall, injuring that shoulder. Movements gradually developed over 1 month, but have been continuous since then. They did not occur during sleep and there was no history of urge. On clinical examination, there was semirhythmic shoulder movement on the left side predominantly in the scapular region (see Video, Case 3). The movement was variable over time, and the video captured a moment with relatively slow irregular movement, but there were also periods of regular movements (1–2 Hz). Physiology experiments were done at a time of regular tremor, which would make it clearer as to whether there might be entrainment or disruption by voluntary movement. Surface EMG of proximal left arm muscles captured a 1- to 2-Hz tremor that did not entrain with right-hand tapping at
different frequencies and did not pause with right ballistic arm movement (Fig. 1A–C). She was treated with BoNT injection without relief.
Discussion The movement disorders in the 3 patients were all semirhythmic shoulder tremors after injury to the shoulder region. The first 2 cases had EDS with a chronic history of shoulder dislocation. The third patient had history of repeated shoulder injury during falls while performing as a cheerleader. There were no features of functional movement disorder in case 1. In case 2, periods of bilateral synchrony and some modification with distraction were suggestive of a functional disorder. The variability of the movement over time in case 3 is also a feature observed in functional disorders. Tremor in all 3 patients was analyzed by surface EMG studies, which objectify what might be discerned clinically. The tremors were not completely rhythmic and did not exhibit significant changes in frequency at different times, even with distraction (although there were changes in amplitude in case 2). In case 2, EMG documented that the tremors were intermittently bilaterally synchronous in the pectoralis muscles, a finding usually indicative of a functional origin. The entrainment test, where a patient is asked to tap at various frequencies using an unaffected body part, is often helpful in differentiating functional and organic tremors. The tremor is modified in functional patients, often taking up the frequency of voluntary tapping. In a study where patients with functional tremor were compared with essential tremor, the tapping task was sensitive (72.7%) and specific (73.3%).4 Tremor could not be entrained in all 3 cases, giving no evidence for a functional disorder. In case 2, however, she was not able to perform the tapping consistently at the given frequency. The failure to be able to tap at requested frequencies can also be a sign of a functional abnormality.4 Tremor monitoring while a patient is making sudden rapid (ballistic) movement using the unaffected part is another way of differentiating organic and psychogenic tremor. In psychogenic tremor, there can be a pause in the tremor activity while doing the ballistic movement. No pause was observed in cases 1 and 3, giving no evidence for a functional abnormality. In case 2, again the patient was not able to do the ballistic movement consistently, so no clear interpretation could be made. Thus, whereas clinical observations in cases 2 and 3 were suggestive of a functional disorder, physiological testing in all 3 cases was unable to add objective evidence other than to confirm some of the clinical observations. There has been published literature on PIMD, including different types of abnormal shoulder movements, but none are similar to ours (Table 1). Criteria have been proposed to diagnose PIMD, and although arbitrary, they do have some heuristic value.7 These criteria include trauma causing local symptoms for at least 2 weeks, initial movement disorder manifestation should anatomically relate to the injury site, and onset of the movement must occur within 1 year after the injury. All our cases had a history of trauma and fulfill these diagnostic criteria. MOVEMENT DISORDERS CLINICAL PRACTICE
doi:10.1002/mdc3.12016
103
CASE SERIES
Shoulder Movement Disorder TABLE 1 Published case series of shoulder movement disorders Case series
Number (male: female)
Side of involvement
Associated illnesses
Abdo et al.6
3 (3:0)
Lee (1999)2
3 (2:1)
Unilateral: 2 Bilateral: 1 Unilateral: 3
Wali (1999)2 Wali (1999)2
2 (2:0) 1 (1:0)
Caviness et al.5
5 (4:1)
Neuralgic amyotrophy Cerebral infarct in 2 patients Cerebral infarct Lower esophagus surgery Wrist injury: 2 Head injury: 1
Unilateral: 2 Right shoulder Unilateral: 2 Bilateral: 3
Please note that the Lee (1999) and Wali (1999) series are both described in detail in reference 2.
TABLE 2 Diagnostic workout to differentiate between organic and psychogenic tremor
Figure 1 (A) Surface EMG of case 3 showing 1- to 2-Hz tremors in the left shoulder. (B) Surface EMG of case 3 showing no entrainment in tremor activity while patient is tapping at 4 Hz using her right hand (R_hand). (C) Surface EMG of case 3 showing no change in tremor activity while doing a ballistic movement using her right hand (R_hand). EMG producing the ballistic movement is indicated with a line under the EMG burst. Left anterior deltoid (L_AntD); supra-spinatus (L_SupS); levator scapulae (L_Lev); rhomboid (L_Rhom); and infra-spinatus (L_infrasp).
Four cases of unusual movement involving the shoulder were reported, characterized by semirhythmic shoulder movements that were attenuated by voluntary activity.5 Emotional stress tended to exacerbate the movement, and, occasionally, the 104
History
Sudden onset or remission; paroxysmal; pain, fatigue, and disability apparently out of proportion to objective findings; variability in body part affected, type of movement, or severity
Physical examination
Variability of the movement; distractibility; entrainment; tremor becoming more severe when visual attention is toward the involved limb
Physiological studies with surface EMG and/or accelerometry
Variability in frequency during distracting cognitive task, such as counting; bilateral synchrony; entrainment of the involuntary movement while tapping using the normal limb at different specified frequencies; poor task performance of the unaffected body part when tapping at specified frequencies; pause in tremor while doing contralateral ballistic movement; increase in tremor frequency on weight loading; coactivation
movements could be completely suppressed, suggesting psychogenicity. Three cases of peripherally induced shoulder movement disorders have also been reported after neuralgic amyotrophy.6 Movement in these patients was slow, and prolonged muscle contractions were similar to dystonia. In a series of patients with surgically corrected cervical radiculopathy, shoulder pain and fixed dystonia later developed. Surprisingly, transcranial sonography revealed hyperechogenic lesions in the lentiform nucleus in the majority of these patients. The proposed mechanism for the development of dystonia in these patients was an interaction between the peripheral nervous system and increased susceptibility to dystonia.8 Task-specific dystonia affecting the shoulder of petanque players resulting in freezing of shoulder flexion was also reported.9 The pathogenesis of PIMD is unknown, but pain and limb immobility have both been considered important, leading to secondary changes in spinal and supraspinal sensorimotor circuits, causing sensory impairments and abnormal central motor response.2 The explanation in a number of patients is clearly
MOVEMENT DISORDERS CLINICAL PRACTICE doi:10.1002/mdc3.12016
CASE SERIES
Pandey et al.
functional, and the differential diagnosis is often challenging. In a review, 713 patients with PIMD were summarized from 133 publications.2 The most common PIMD was fixed dystonia and 15% were thought to be psychogenic, but many authorities would consider this an underestimate. Presence of significant variability, entrainment of the movements, distractibility, and spontaneous recovery should alert the clinicians regarding the possibility of psychogenicity.10 Clinical neurophysiology (Table 2), which can be valuable, is useful only when positive, and firm conclusions cannot be drawn when testing is negative. We still need better methods for definitive diagnosis of functional movement disorders.
Author Roles (1) Research Project: A. Conception, B. Organization, C. Execution; (2) Statistical Analysis: A. Design, B. Execution, C. Review and Critique; (3) Manuscript: A. Writing of the First Draft, B. Review and Critique. S.P.: 1C, 3A, 3B F.N.: 1C, 3B J.A.: 1C, 3B J.N.: 1C, 3B M.H.: 1C, 3B
revenue on US Patent #6 780 413 B2 (issued 24 August 2004): Immunotoxin (MAB-Ricin) for the treatment of focal movement disorders; and US Patent #7 407 478 (issued 5 August 2008): Coil for Magnetic Stimulation and methods for using the same (H-coil); in relation to the latter, he has received license fee payments from the NIH (from Brainsway) for licensing of this patent. He is on the editorial board of 20 journals and received royalties from publishing from Cambridge University Press, Oxford University Press, John Wiley & Sons, Wolters Kluwer, and Elsevier and has received honoraria for lecturing from Columbia University and the Parkinson and Aging Research Foundation. Dr. Hallett’s research at the NIH is largely supported by the NIH Intramural Program. Supplemental research funds came from the Kinetics Foundation, for studies of instrumental methods to monitor Parkinson’s disease, and BCN Peptides, S.A., for treatment studies of blepharospasm.
References 1. Van Rooijen DE, Geraedts EJ, Marinus J, Jankovic J, van Hilten JJ. Peripheral trauma and movement disorders: a systematic review of reported cases. J Neurol Neurosurg Psychiatry 2011 Aug;82:892–898. 2. Aggarwal A, Thompson PD. Unusual focal dyskinesias. Handb Clin Neurol 2011;100:617–628. 3. Harden RN. Objectification of the diagnostic criteria for CRPS. Pain Med 2010;11:1212–1215. 4. Edwards MJ, Bhatia KP. Functional (psychogenic) movement disorders: merging mind and brain. Lancet Neurol 2012;11:250–260.
Acknowledgments The authors are thankful to the patients for participating in these studies.
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Disclosures
7. Jankovic J. Peripherally induced movement disorders. Neurol Clin 2009;27:821–832.
Funding Sources and Conflicts of Interest: This study was supported by the National Institute of Neurological Disorders and Stroke Intramural Program. The Indo-US Science Technology Forum awarded a fellowship to Dr. Sanjay Pandey to do research in Parkinson’s disease and Movement Disorders at the Human Motor Control Section, National Institute of Neurological Disorders and Stroke, and the National Institutes of Health. The work of Dr. Jason Aldred was supported by a Parkinson’s Disease Research, Education, and Clinical Centers clinical research fellowship through the Department of Veterans Affairs. The authors report no conflicts of interest. Financial Disclosures for previous 12 months: J.A. consulted for Abvvie and received honoraria from Allergan, Ipsen, and Teva Neuroscience. J.N. receives research funding from the Michael J. Fox Foundation, The National Parkinson Foundation, and the National Institutes of Health (NIH). M.H. serves as chair of the medical advisory board for, and receives honoraria and funding for travel from, the Neurotoxin Institute; may accrue
8. Becker G, Berg D, Kruse N, et al. Evidence for shoulder girdle dystonia in selected patients with cervical disc prolapse. Mov Disord 2002;17:710– 716. 9. Lagueny A, Burbaud P, Dubos JL, et al. Freezing of shoulder flexion impeding boule throwing: a form of task-specific focal dystonia in petanque players. Mov Disord 2002;17:1092–1095. 10. Lang AE, Angel M, Bhatia K, et al. Myoclonus in complex regional pain syndrome. Mov Disord 2009;24:314–316.
Supporting Information A video accompanying this article is available in the supporting information here. Video. Case 1: Right shoulder semirhythmic tremor with anterior-posterior motion of humeral head; the movements are not distractible. Case 2: Bilateral semirhythmic anterior-posterior movement of the shoulder: distraction slightly reduced the amplitude of movement. Case 3: Semirhythmic shoulder movement on the left side predominantly in the scapular region.
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