Dystonic Pseudo Foot Drop

Abstract

The most common presentation of foot dystonia in patients with Parkinson's disease (PD) or dystonia is inversion of the foot accompanied by flexion of the toes, with or without extension of the hallux. Less commonly, foot dystonia may mimic foot drop, as occurs with weakness of the dorsiflexors muscles, resulting in a pseudo foot drop. This has rarely been reported in the literature and has been poorly recognized, often leading to misdiagnosis and unnecessary investigations and treatment. We report 5 patients with dystonic pseudo foot drop, one of them diagnosed with early‐onset PD, 2 with sporadic PD, and 2 with dystonia. Despite the steppage gait, their physical exam revealed normal strength, and no other explanation for a “foot drop” was found. It is important to recognize this phenomenology, which can be a clue to the diagnosis of early‐onset PD, and may be responsive to levodopa in selected patients.

Patients with lower‐limb dystonia often complain of “dragging the foot.” This is particularly common in patients with Parkinson's disease (PD)1 and in children with dystonia.2 The most common presentation is inversion of the foot (equinovarus) accompanied by flexion (curling) of the toes, with or without extension of the hallux (striatal toe).3 Less commonly, foot dystonia may mimic foot drop as occurs with weakness of ankle dorsiflexion in neuromuscular or pyramidal syndromes. Foot dystonia mimicking foot drop is a poorly recognized phenomenon, which can lead to misdiagnosis and unnecessary investigation and treatment.

We report on 5 patients (Table 1) with foot dystonia mimicking a foot drop, emphasizing the phenomenology of this presentation and clinical diagnosis. We propose the terms “dystonic pseudo foot drop” or “foot drop dystonia” for this presentation, which, to our knowledge, has rarely been described in the literature.

Table 1.

Clinical characteristics of patients presenting dystonic pseudo foot drop

Case	Diagnosis	Gender, Age of Onset	Gait Phenomenology
1	Juvenile parkinsonism	Male, 14	High stepping with mild hip abduction on the right, loss of dorsiflexion of the ankle, and tendency to turn the anterior portion of the right foot inward
2	PD	Male, 75	Mild high stepping and hip abduction on the right, scraping the ball and lateral portion of the foot on the floor, inversion of the ankle
3	PD	Male, 60	Stiff right lower limb, dragging the toes on the floor; in the ON phase tends to high stepping
4	Familial dystonia	Male, 64	Plantar flexion of the right ankle and hallux, hip adduction and knee flexion (Achilles tendon transfer surgery on the right)
5	Acquired dystonia		Plantar flexion and inversion of the right foot while stepping forward. High and long stepping on the right. Right toes tend to scrape the floor.

Case Series

Patient 1

A right‐handed man started experiencing falls and walking difficulties at the age of 14 preceded by a history of learning disability and autism. He gradually developed generalized bradykinesia and hypophonia. By age 15, juvenile parkinsonism was diagnosed. During the disease course, he developed depression and anxiety, as well as impulse control disorder secondary to dopamine agonist therapy. At age 19, L‐dopa was started with a good response, but rapid development of dyskinesia. Physical exam at age 21 revealed limited downward gaze, blepharospasm, moderate hypomimia, hypophonia, and dysarthria. There was mild bradykinesia and rigidity throughout, choreiform dyskinesia in the upper limbs and trunk, and lack of postural reflexes. His strength was normal throughout. There was no spasticity in the lower limbs. Deep tendon reflexes were brisk throughout. Gait was steppage with loss of dorsiflexion and tendency to turn the right foot inward (see Video 1). He was able to walk on heel and on toes.

Brain MRI revealed generalized volume loss involving cerebral hemispheres and cerebellum, with no metal deposition or corticospinal involvement. MRI of the cervical and thoracic spine revealed only reversal of the physiological lordosis of the cervical spine, with no spinal cord atrophy or signal abnormalities. He was found to be a carrier of heterozygous mutations in PINK1 and ATP13A genes. At last evaluation at age 30, motor UPDRS score was 43. As the result of progression of disease, he developed increasingly gait problems, with additional spasticity, and became wheelchair bound.

Patient 2

A 75‐year‐old man had a 5‐year history of resting tremor and reduced arm swing on the right. His parkinsonism gradually progressed and he developed gait difficulty resulting from inversion of the right foot and freezing of gait. He received a diagnosis of PD, and started treatment with l‐dopa up to 600 mg/daily, with suboptimal response. By the time of our assessment, his main concerns were related to dragging of his foot, curling of his toes, and difficulty writing. Physical exam showed masked face and hypophonia. Tremor at rest was prominent in the right hand and also intermittently observed in the lower lip. There was moderate bradykinesia and rigidity, worse on the right. He had mirroring of voluntary movements of the right hand in the left. Strength was normal throughout, including in tibialis anterior bilaterally. Gait was characterized by plantar flexion of the right foot, with inversion of the ankle and flexion of the toes. Arm swing was reduced on the right, and rest tremor was appreciated. He was able to walk on his heels (see Video 2). Motor UPDRS score was 45.

A brain MRI disclosed small high‐signal foci within the deep white matter bilaterally (T2‐weighted and fluid‐attenuated inversion recovery [FLAIR] axial images) suggestive of microangiopathy. Because of the typical presentation and lack of other relevant abnormalities on physical exam, we recommended a further increase in the dose of l‐dopa, and he continued to be managed by his primary neurologist.

Patient 3

A 60‐year‐old man noted tremor in the right thumb gradually progressing to the whole hand, followed by reduced dexterity and slowness. He was diagnosed with PD and was treated with a dopamine agonist, followed by l‐dopa and amantadine. Over the period of 5 years, he developed progressive gait difficulties, with dragging of the right foot, in addition to motor fluctuations and dyskinesia. Because of a subacute worsening of ambulation, he was investigated with brain and spinal MRI. The brain MRI revealed nonspecific high‐signal lesions in T2‐weighted and FLAIR images, involving periventricular white matter, as well as brainstem. The spinal MRI revealed stenosis of the cervical spine resulting from severe spondylosis with possible compressive myelopathy, which motivated a spinal surgery with decompression and fusion C3 to C7. He had a gradual recovery of the symptoms, but the baseline gait difficulties related to PD and dragging of the foot persisted. Two years later, his physical exam in the off medication phase revealed facial hypomimia and hypophonia. Tremor was noticed in the right hand at rest. He had moderate‐to‐severe bradykinesia and rigidity throughout, worse on the right side. Strength was preserved throughout. Gait was marked by dragging of the right toes, as well as slapping the ball of the right foot on the floor (see Video 3, Segment 1). After administration of l‐dopa, plantar flexion of the right foot improved; however, dyskinesia affecting the upper and lower limbs developed (see Video 3, Segment 2).

This patient received a bilateral DBS implant within the globus pallidus (GP), but, unfortunately, the electrodes were removed shortly after the surgery because of infection. Electrodes were more recently reimplanted with improvement of dyskinesia, but no improvement of foot posturing and gait.

Patient 4

A 64‐year‐old man had a history of breech delivery after prolonged labor, but normal childhood developmental milestones. During childhood/adolescence, handwriting was sloppy, with difficulties playing the piano with the right hand. At the age of 27, tremor developed in the right arm. He remained stable for approximately 5 years, but then the right foot started turning during walking, to the point that a decade later, a tendon transfer surgery was performed. Three of eight siblings had a similar movement disorder with no history of consanguinity. Physical exam revealed a mild rotation of the head to the right. At rest, there were no obvious involuntary movements. With arms elevated, he developed rhythmic involuntary movements at the right shoulder at 2 Hz, resembling myorhythmia, worse with the arms flexed at the elbows. There was also mild scooping posture at the left wrist. There was inversion of the left foot with dorsiflexion spasms of the toes. The right leg was stiff, and the right foot tended to drag with the toes curled under (see Video 4). Abnormal plantar flexion of the foot improved by walking on the spot.

Electromyography (EMG) showed no spontaneous activity in the median gastrocnemius. There were a few motor units active from time to time in the right soleus, and there was intermittent dystonic activity in the right extensor halluces longus. Surface electrodes were used to record from tibilais anterior and soleus during walking on the spot. Alternate activity was recorded from these muscles during the stepping cycle. There was no evidence that the soleus was overactive during the swing phase.

There was an initial good response to trihexyphenidyl. Trials of botulinum toxin (BoTN) injections were performed with limited benefit. The patient was followed from 1985 until death in 1996. No brain tissue was available for pathology and genetic testing was not available at the time.

Patient 5

A 43‐year‐old right‐handed Filipino man without history of perinatal injury presented with a 3‐year history of abnormal foot posturing on ambulation. A diagnosis of a psychogenic or functional disorder was being entertained by his referring physician owing to the unusual nature of his gait and lack of explanatory clues. Medical history was significant for learning disability diagnosed in kindergarten, bipolar affective disorder diagnosed at age 30, atrial fibrillation, and right adrenalectomy resulting from Cushing syndrome at age 35. Medications included amiodarone, digoxin, risperidone, and trazodone (unknown doses and duration of treatment). Pharmacy records revealed a previous exposure to haloperidol. His mother had noticed gradual development of abnormal posture in the left hand for 15 years with minimal functional impairment. Family history included primary biliary cirrhosis in the mother and Goodpasture's disease in the sister. On examination, there were no Kayser‐Fleischer rings. He had a slightly dysarthic speech. Facial movements appeared reduced on the right side. Dystonic movements were present in the face, with episodic frowning, pouting movement of the lips, and writhing of the tongue. Muscle tone was normal throughout. He had mild high‐frequency tremor with posture of his arms. There was dystonic posturing of the left hand with digits extended at the metacarpophalangeal and flexed at the interphalangeal joints. Dystonia was not obvious at the lower limbs at rest. Mirror movements were noted in the left foot during right‐foot tapping. Gait showed right dystonic foot drop, which improved with running and walking backward (see Video 5). He was not able to walk on toes on the right side, but, at times, he was able to walk on heels, however with difficulty.

The patient is currently under investigation. His brain MRI was unrevealing. The spinal MRI disclosed a small likely asymptomatic syrinx from T4 to T10 measuring less than 2 mm. Copper and ceruloplasmin levels were normal. The results of genetic tests for DYT 1 and DYT 6 were negative.

Discussion

In our series, patients 1, 2, and 3 presented with dystonic pseudo foot drop associated with parkinsonism. Although the phenomenology can be confused with neuromuscular or pyramidal foot drop, physical exam revealed normal strength and reflexes. Patient 1 had juvenile parkinsonism and was found to carry heterozygous mutations in PINK1 and ATP13A genes. Patient 3 had a history of cervical spinal stenosis and surgery; however, the pseudo foot drop was at least partially responsive to l‐dopa and there was no explanatory weakness or spasticity.

Dystonia is frequently observed in patients with PD and can present in a variety of forms.4 The involvement of distal lower limbs is particularly common, sometimes preceding other parkinsonian symptoms by a decade.5, 6 Dystonia can be paroxysmal, most often triggered by prolonged walking, which has been referred to as kinesigenic foot dystonia,6 probably better termed “exercise‐induced foot dystonia.” In advancing PD, foot dystonia can occur with motor fluctuations (e.g., at the end of dose), which is sometimes painful and disabling, particularly early in the morning.7, 8 Foot dystonia has been considered a hallmark of juvenile and young onset forms of PD,9 as in patient 1. However, patients with sporadic and late‐onset forms, such as patients 2 and 3, can also present with foot dystonia as an early symptom.

Foot dystonia was the primary complaint in patients 4 and 5. In case 4, dystonia began during childhood, and in patient 5, in early adulthood. Both cases had a slowly progressive course. In patient 4, the strong family history of similar symptoms suggested a genetic etiology. Patient 5 may have either inherited or acquired dystonia. Importantly, owing to the lack of recognition of the dystonic pseudo foot drop, this patient had been previously considered to have a psychogenic/functional foot drop.

Dystonic foot drop has been previously reported in a patient with manganism, who presented with an unusual gait,10 distinct from the typical “cock gait” described in acquired and inherited manganism. Another interesting gait pattern with foot drop was reported in a patient with l‐dopa‐responsive/exercise‐induced alternating leg‐paresis/hypotonia and hemidystonia diagnosed with hemiparkinsonism‐hemiatrophy syndrome, who had no evidence of weakness or peripheral nerve abnormalities between the attacks.11 To our knowledge, the pathophysiology of dystonic pseudo foot drop has not been previously explored in neurophysiological studies. We hypothesize that this is an action‐induced dystonia, which behaves similarly to “task specific dystonia,” resulting in plantar flexion with (or without) inversion of the ankle triggered by stepping forward in the swing phase of walking, although we could not confirm this using surface electrodes in patient 4. Patients then tend to lift their legs higher in order to avoid scraping their toes on the floor, similarly to what happens in patients with distal weakness.

In clinical practice, patients presenting with dystonic pseudo foot drop are often submitted to EMG and nerve conduction studies, spinal imaging, and, occasionally, orthopedic surgery. A careful evaluation of the dorsiflexor musculature, reflexes, and sensory exam are essential to correctly differentiate between true foot drop and dystonic pseudo foot drop. In addition, an assessment of gait, including walking on toes and heels, running, and walking backward, will provide the most important clues for the correct diagnosis. Patients with dorsiflexor weakness would likely be unable to perform heel‐walking, and dystonia tends to improve with backward gait, running, and even marching on the spot, as in patient 4, whereas weakness does not.

It is important to recognize this form of dystonia in order to avoid unnecessary investigations and invasive treatments. The paucity of information in the literature precludes recommendation for management of dystonic pseudo foot drop. Etiology will clearly influence treatment response. Some patients may respond to l‐dopa (PD and dopa‐responsive dystonia), or to anticholinergic agents, as illustrated in cases 3 and 4. BoTN injections have been applied in PD patients with OFF dystonia12 and might be beneficial in selected patients with dystonic pseudo foot drop, targeting the ankle plantar flexors. In other refractory patients, orthotic fitting might be considered.13 To our knowledge, the effects of DBS, for example, targeting the internal segment of the GP, have not been reported to date. In our case 3, it was not successful, but this patient had several complications, including removal of electrodes because of infection, in addition to a history of spinal surgery. Further studies on pathophysiology of dystonic pseudo foot drop might help to guide therapeutics.

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.

C.C.A.: 1A, 1B, 1C, 3A

E.S.: 1C, 3A, 3C

A.E.L.: 1A, 1B, 3C

Disclosures

Funding Sources and Conflict of Interest: The authors report no sources of funding and no conflicts of interest.

Financial Disclosures for previous 12 months: C.C.A. received a fellowship grant from Parkinson Society Canada; scholarship from the CAPES Foundation, the Brazilian Ministry of Education; and support from Mohammad Al Zaibak Fellowships in Parkinson's Disease. A.E.L. has served as an advisor for AbbVie, Allon Therapeutics, Avanir Pharmaceuticals, Biogen Idec, Boerhinger Ingelheim, Ceregene, Lilly, Medtronic, Merk, Novartis, NeuroPhage Pharmaceuticals, Teva, and UCB; received honoraria from Medtronic, Teva, UCB, and AbbVie; received grants from Brain Canada, Canadian Institutes of Health Research, the Edmond J Safra Philantropic Foundation, the Michael J. Fox Foundation, the Ontario Brain Institute, the National Parkinson Foundation, Parkinson Society Canada, and the Tourette Syndrome Association; received publishing royalties from Saunders, Wiley‐Blackwell, Johns Hopkins Press, and Cambridge University Press; and has served as an expert witness in cases related to the welding industry.

Supporting information

Videos accompanying this article are available in the supporting information here.

Video 1. Patient 1 walking forward presents dystonic pseudo foot drop on the right, accompanied by absence of arm swing on the same side. Heel‐walking and strength of the dorsiflexors of the ankles were normal.

Video 2. Patient 2 has plantar flexion and inversion of the right foot while walking forward. The arm swing is reduced ipsilaterally.

Video 3. Segment 1: Patient 3 in the off medication phase presenting dystonic foot drop and resting tremor on the right side. Segment 2: After l‐dopa infusion, dystonia and resting tremor improves, and the patient developed dyskinesia in the right upper and lower extremities.

Video 4. Patient 4 has dystonia in the right ankle and toes, dragging his toes on the floor while walking forward. Marching in place, walking on heels and on toes, there is no evidence of foot drop. Exam of the upper limbs demonstrated proximal movement on the right side suggestive of myorhythmia.

Video 5. Patient 5 has dystonic posture of the left hand. Walking forward, he has dystonic pseudo foot drop, which improves with walking backward and running. Strength of the dorsiflexors of the ankle is normal bilaterally.