Freezing of gait in patients with advanced Parkinson s disease

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1 J Neural Transm (2001) 108: Freezing of gait in patients with advanced Parkinson s disease N. Giladi, T. A. Treves, E. S. Simon, H. Shabtai, Y. Orlov, B. Kandinov, D. Paleacu, and A. D. Korczyn Movement Disorders Unit, Department of Neurology, Tel-Aviv Medical Center, Sackler Faculty of Medicine, Tel-Aviv University, Israel Received April 19, 2000; accepted June 6, 2000 Summary. Background. Freezing of Gait (FOG) is one of the most disturbing and least understood symptom in advanced stage of Parkinson s disease (PD). The contribution of the underlying pathological process and the antiparkinsonian treatment to the development of FOG are controversial. Objective. To study the relationships between clinical features of PD and therapeutic modalities in patients with advanced PD and FOG. Methods. Consecutive patients with 5 years or more of PD symptoms (n 172) (99 men) with mean age at symptoms onset of years and mean symptoms duration of years were studied. Clinical data were collected during the last office visit through physical examination, detailed history, review of patients charts, and other documents. A patient was considered as freezer if he/she reported recent experience that the legs got stuck to the ground while trying to walk. The presence of dyskinesia, early morning dystonia or significant postural reflex abnormalities were assessed through history and neurological examination. Duration of treatment with antiparkinsonian drugs was calculated from history charts. Chi square and t test were used to compare the patients with and without FOG. Logistic regression was used for the comparison of association between the presence of FOG (dependent variable) disease duration and disease stage (explanatory variables) and duration of treatment with anti-parkinsonian drugs. Results. The study population consisted of 45 patients at Hoehn and Yahr (H&Y) stage 2.5 (26%), 104 patients at stage 3 (60.5%), and 23 patients at H&Y stages 4 5 (13.5%). Ninety one patients (53%) reported FOG at the time of the study. Severity of the disease expressed by H&Y stage at off was a significant contributing factor for FOG with a significant trend (z 4.38, p ), as was longer duration of levodopa treatment, and confirmed by FOG using the multivariate logistic regression (p 0.01 and p 0.004, respectively). Using a univariate model, longer duration of treatment with dopamine agonists contribute to the appearance of FOG (p 0.07) while longer duration of amantadine treatment decreased the appearance of FOG

2 54 N. Giladi et al. (p 0.09). There was a significant association between FOG and the presence of dyskinesia (p 0.002), early morning foot dystonia (p 0.003) and significant postural instability (p ). Conclusion. FOG is a common symptom in advanced PD. It is mainly related to disease progression and levodopa treatment. Keywords: Parkinson s disease, freezing of gait, complication, advanced stage. Introduction The modern therapeutic approach to Parkinson s disease (PD) has enabled patients to remain ambulatory and mobile throughout most of the disease course. However, the progression of the disease in conjunction with long term side effects of antiparkinsonian medications created a complex motor disturbances. Gait disturbances are playing an important role in the clinical picture of advanced PD cases affecting the degree of ambulating ability and independence of the patients. These include choreic or dystonic gait as well as festinating gait at the on state while shuffling gait or hypokinetic bradykinetic gait pattern frequently accompanied by dystonia are seen during the off state. Freezing of gait (FOG) is one of the common and most disabling gait disturbances accompanied the clinical syndrome in advanced stages of PD. FOG has been reported at the early stages of the disease even prior to anti-parkinsonian treatment but it is relatively rare and usually short in duration (1 2 seconds) with minor functional disability (Giladi et al., 1992, 1996; Lamberti et al., 1996). FOG is rare as the presenting symptom of PD (Lamberti et al., 1997) and if it is the major disturbing symptom in the early stages of the disease one should suspect the diagnosis of other parkinsonian syndromes like progressive supranuclear palsy (PSP) or vascular parkinsonism (Giladi et al., 1997; Giladi and Fahn, 1998). In contrast, at the advanced stages of the disease FOG is a very disabling symptom lasting seconds to minutes and frequently associated with falls and injuries. It appears at initiation of gait (start hesitation), at doorways, narrow spaces or in stressful situations (Giladi et al., 1992; Lamberti et al., 1997). FOG may become the most disabling symptom which force the patient to stay at home or use a wheelchair. The basic mechanism responsible for FOG is unclear. Disease progression by itself is playing an important role as shown in the DATATOP study (Giladi et al., 1996) but clearly dopaminergic, therapies are playing an important role (Ambani and Van Woert, 1973; Barbeau, 1972, 1976). The purpose of the present study was to assess the frequency of FOG at the advanced stages of PD and to associate it with other parkinsonian symptoms or therapeutic modalities. Such study even if retrospective in nature is of importance trying to understand the role of the disease itself and the contribution of current treatment modalities to the development of FOG. In order to look at a relatively homogeneous group of PD patients we excluded patients with less than five years of parkinsonian symptoms.

3 Freezing of gait in patients with advanced Parkinson s disease 55 Methods Patient population and data collection Our study population was based on 172 consecutive PD patients, seen between December 1996 and June 1997 at the Movement Disorders Unit of Tel-Aviv Sourasky Medical Center. The diagnosis of idiopathic PD was based on the United Kingdom Brain Bank clinical criteria (Hughes et al., 1992) which was confirmed by a movement disorders specialist at the last office visit. We excluded from the study all patients with less than 5 years of parkinsonian symptoms, in order to minimize the inclusion of patients with atypical parkinsonism. We specifically looked for and excluded patients with a possible or probable diagnosis of Multiple System Atrophy (MSA) according to Quinn s criteria (Quinn, 1994), as well as those patients in whom dementia had occurred before the motor symptomatology or in the first year after parkinsonism was diagnosed. In addition, patients with marked postural instability or significant orthostatism occurring during the first year after the appearance of motor symptoms, and patients with a history of strokes, significant head trauma or encephalitis were excluded. Data collection Patients and their caregivers were interviewed by a neurologist specializing in movement disorders, and patients were examined in order to confirm the diagnosis of PD. A specific questionnaire was completed by the physician during the last office visit and missing historical data were retrieved from the hospital chart or by telephone interview with the primary care physician or family members. FOG was considered to be present if actual freezing episodes were observed during the office visit or reported by the patient, his/her family member or the caregiver to be of any functional significance during the last 3 months. In addition, we reviewed the chart to see if FOG was mentioned to be of any significant functional importance during the last 3 months prior to the last office visit. In order to assess FOG we explained to the patients and their caregivers what we meant by FOG saying that we evaluate those episodes when the feet get glued to the ground blocking the initiation or continuance of walking as well as turning in place. If this description was not clear we imitated FOG of all types, during the office visit. The presence of early morning foot dystonia was assessed by history only in a similar fashion as FOG but in this case specifying the involuntary appearance of spasm of the foot prior to the first morning dose of levodopa. Dyskinesia and significant postural reflexes abnormalities were evaluated in a similar way during the exam as well as by history from the patient or the caregivers. We did not subclassified FOG nor dyskinesias to the different subtypes. All patients were scored according to the Hoehn and Yahr (H&Y) motor clinical staging (Hoehn and Yahr, 1967) modified by Fahn et al. (1987). In order to assess the relationships between disease progression and the presence of FOG, we divided the study population into three sub-groups according to the H&Y stage (1 2.5, 3, 4 5). The common therapeutic strategy in practice at the Movement Disorders Unit over the period of the study was to delay levodopa treatment mainly in patients with young age of symptoms onset, to add dopamine agonist drugs only if daily dose of 500mg levodopa did not give satisfactory relief or if response fluctuations appeared. Amantadine was prescribed in many cases throughout the entire disease course. Selegiline was introduced in the late 1980 s or early 1990 in most patients and was continued unless side effects developed. Statistical analysis Chi-square and z-tests for linear trend for proportions (Snedecor and Cochran, 1980) were used to analyze the distribution of FOG among the various severity subgroups

4 56 N. Giladi et al. according to H&Y as well as for the association between FOG and clinical features. Statistical significance was determined for alpha level of 0.05, with Bonferroni correction for multiple comparisons. Because the exact time of onset of FOG, dyskinesia, dystonia or postural instability was not always clearly recorded, the effect of drugs on FOG was evaluated in a cross sectional (rather than incidence) approach. Therefore, the relationship between the presence of FOG (dependent variables) and duration of treatment with levodopa, dopamine agonist drugs, selegeline, amantadine or anticholinergic medications (explanatory variables) were examined using backward stepwise logistic regression with age at onset, and motor severity as covariates. In order to be able to evaluate the relative magnitude of the beta coefficients generated by the model (the exponents of which reflect odds ratios), standardized beta were also looked for. Results Of 172 PD patients, 73 were women and 99 men, with a mean age of years at symptoms onset, and a mean disease duration of years (Table 1). Tremor was the presenting symptom in 69.4% of our patients, while 94% of them had rest tremor recorded at least once during the course of the disease. Bradykinesia at disease onset was reported by 44.7% of the patients while rigidity was present in 25.3% and gait disturbances in 18.2% (Table 1). When we divided the study group according to disease stage, as reflected by the H&Y clinical stage state, 45 patients had mild disease at stage 2.5 (26%), 104 patients with moderate progression at stage 3 (60.5%) and 23 advanced patients at stage 4 5 (13.5%). Age of symptoms onset was similar in these 3 groups, , and years, respectively (p 0.05). Table 1. Clinical characteristics of 172 patients with Parkinson s disease Gender Women 73 Men 99 Present age (years) Mean age of symptoms onset (years) Mean disease duration (years) Mean levodopa dose (mg/day) Hoehn & Yahr clinical staging at off state (26%) (60.5%) (13.4%) Therapeutic profile Drug % of patients treated Duration of treatment Levodopa n 171 (99%) Dopa agonist n 117 (68%) Selegiline n 107 (62%) Amantadine n 95 (55%)

5 Freezing of gait in patients with advanced Parkinson s disease 57 Table 2. Association between clinical features and freezing of gait Freezers Non-Freezers test p (n 92) (n 83) Duration of PD symptoms t Duration of Levodopa t treatment n 92 n 79 Duration of dopamine t agonist treatment n 83 n 78 Duration of amantadine t treatment n 42 n 48 Duration of selegiline t treatment n 81 n 78 Presence of dyskinesia n 49 n 25 χ Presence of early morning n 28 n 10 χ dystonia Presence of significant n 77 n 50 χ postural instability χ 2 square; PD Parkinson s disease Ninety nine percent of the patients were treated with levodopa with a mean duration of treatment of years. At the last visit, the mean levodopa dose was mg/day. Duration of levodopa treatment was significantly shorter in the group with milder disease (H&Y 3): years as compared to and years for more advanced patients [H&Y 3 and H&Y 3 subgroups, respectively (F 6.9, p 0.001)]. Dopamine agonists were taken at any point in time throughout the disease by 68% of the patients for a mean duration of years. Selegiline and amantadine were taken during the course of the disease by 62% and 55% of the patients, respectively (Table 1). FOG occurred in 53% of all patients (92 patients). Severity of the disease expressed by H&Y stage was a significant contributing factor for the presence of FOG (p ) with a significant trend (z 4.38). Ten patients with H&Y stage had FOG (22%), 65 of patients with H&Y stage 3 had FOG (62%) while 69% of patients with H&Y stage 4 5 experienced FOG. FOG was significantly associated with higher H&Y stage X , p Similarly, longer duration of PD symptoms was significantly associated with the presence of FOG (p 0.05). FOG was significantly associated with longer duration of levodopa treatment (p 0.007), and a trend towards an association was found with longer duration of treatment with dopamine agonist drugs (p 0.07) (Table 2). We also observed negative association between duration of amantadine treatment and the appearance of FOG but this relationship did not reach statistical significant level (p 0.09) (Table 2). Levodopa induced dyskinesia, early

6 58 N. Giladi et al. morning dystonia and clinically significant postural reflex abnormalities were all significantly associated with the presence of FOG (p 0.002, p 0.003, p , respectively) (Table 2). Due to the retrospective nature of this study and the possible interrelationships between the different clinical features, we performed a backward stepwise logistic regression with the multivariate model. Such analysis demonstrated that disease severity expressed by H&Y stage and duration of treatment with levodopa were the only clinical features that were significant contributing factors for the appearance of FOG (β 0.96, p 0.001; β 0.06, p 0.067, respectively). Discussion FOG has long been associated with parkinsonism, even before levodopa was introduced for the treatment of PD (Charcot, 1877; Martin, 1967; Schwab et al., 1959). However, its exact frequency at the pre-levodopa period is unknown. Shortly after the introduction of levodopa for the treatment of PD, Barbau and later Ambani and Van Woert have reported about the increase in FOG frequency, a phenomenon which they considered as another late complication of levodopa treatment (Ambani and Van Woert, 1973; Barbeau, 1972). The FOG at the early stages of the disease prior to the introduction of levodopa seems to be mild, short lasting and with minor effect on gait in general. At the advanced stages of PD, FOG is much more disturbing and disabling symptom, lasts longer, highly associated with the on\off phenomenon and frequently leads to falls. The present study confirmed previous retrospective studies that disease progression as reflected on the H&Y clinical staging, is a major contributing factor for the appearance of FOG (Giladi et al., 1992, 1996). In addition, we confirmed previous reports that duration of levodopa treatment is a significant contributing factor for the development of FOG (Giladi et al., 1992; Lamberti et al., 1997). We propose that the relationships between FOG and H&Y stage should be looked in light of the association we observed between FOG and significant postural reflexes abnormalities. The majority of our patients were in H&Y stage 3 or higher. The difference between H&Y and 3 is the appearance of clinically significant postural reflexes abnormalities. In other words, we propose that the tight relationships between FOG and H&Y stage is not just an association with disease progression in general but specifically with the development of postural reflexes abnormalities. This overlap between postural reflexes abnormalities and H&Y score is the result of the over representation of postural abnormalities in that specific clinical staging. For example, tremor which has significant contribution to disease severity in tremor predominant PD was found to be a protective factor for FOG (Giladi et al., 1992, 1996; Lamberti et al., 1997). Following this line of thoughts, we suggest that there might be an interaction between postural reflexes disturbances and locomotor centers which are

7 Freezing of gait in patients with advanced Parkinson s disease 59 degenerated simultaneously to cause FOG as well as the falls associated with it. At the present study we observed a possible contribution of duration of treatment with dopamine agonists to the appearance of FOG. Such relationship between FOG and dopamine agonists have also been suggested by Weiner et al. (1993) and Ahlskog et al. (1992). Recently, in two large scale prospective double-blind studies, which assessed Ropinirole (Rascol et al., 2000) and primipaxol (Holloway et al., 2000) a trend was observed for higher FOG frequency in patients treated with the two dopamine agonists. Considering the fact that over 68% of our advanced PD patients were treated with dopamine agonist drugs and the increasing role of these agents as a substitution to levodopa in all stages of the disease, our present observation as well as others, should lead to greater caution using dopamine agonists in patients with gait disturbances as a major disabling symptom and especially FOG. This is the first study, which looked at the relationship between selegeline or amantadine and FOG in advanced patients. This was of special interest in light of previous observation that selegeiline was an effective symptomatic treatment for FOG in the prelevodopa period (Giladi et al., 1996). We did not see any relationship between duration of treatment with selegilinge or amantadine and FOG in the multivariate analysis. Our results are in the same line as previous prospective study which looked at the possible protective effect of selegiline treatment on the development of FOG and did not find any effect (Parkinson Study Group, 1996). The pathophysiology of FOG is unclear as well as the mechanism associated with levodopa treatment or dopamine agonists. However, FOG has repeatedly been associated with levodopa induced dyskinesia (Giladi et al., 1992) and in this study for the first time with early morning foot dystonia. Such an association can be the result of advanced disease and possibly of similar pathophysiology. Support for the idea of common pathophysiology comes from several physiological studies which showed co-activation of antagonist muscles during a freezing episode (Andrews, 1973; Ueno et al., 1993). In other words, all three motor disturbances are caused by dissynchronized, involuntary co-activation of limb muscles. We suggest that FOG is a dystonic like phenomenon which is action induced, task (gait) specific, responses to motor and cognitive tricks and associated with coactivation of antagonist muscles. However, FOG is not a typical dystonia mainly because it is transient. We suggest the term paroxismal dyskinetic freezing episode. This study raises several important clinical issues in relation to FOG in PD. The retrospective nature of our research did not let us conclude about risk factors and to clearly separate between the different contributing factors. Only a prospective study will be able to identify risk factors for FOG. However, the strength of the present study is the relatively large and clean group of PD patients we had. FOG was assessed by a direct question. This was done as a result of lack of any objective assessment for FOG at the time of the

8 60 N. Giladi et al. assessment. However, such data could not give us the severity of FOG, its relation to on or off neither the exact time when FOG was developed in the course of the disease. Future studies using our recently developed FOG questionnaire will be able to answer some of the questions which were left open in the present study (Giladi et al., 2000). In conclusion, FOG is a very common symptom in the advanced stages of PD which has a significant impact on patients ambulation and independence. There are increasing evidences that levodopa as well as dopamine agonists treatment contributing to the development of FOG in conjunction with the underlying neurodegenerative process and normal aging. We suggest that levodopa or dompamine agonists contribute to the development of FOG in a similar mechanism they cause dyskinesia at the on state and dystonia at the on or off states. Future studies will have to look prospectively at FOG and define the population at risk in order to prevent these disabling symptoms. Acknowledgment This work was supported in part by a research grant by Merz Pharmaceutical Ltd. References Ahlskog J (1992) Dopamine agonist treatment of flucturating parkinsonism. D-2 (controlled release MK-458) vs combined D-1 and D-2 (pergolide). Arch Neurol 49: Ambani L, Van Woert M (1973) Start hesitation a side effect of long-term levodopa therapy. N Eng J Med 24: Andrews CJ (1973) Influence of dystonia on the response to long-term L-dopa therapy in Parkinson s disease. J Neurol Neurosurg Psychiatry 36: Barbeau A (1972) Long term appraisal of levodopa therapy. Neurology 22: Barbeau A (1976) Six years of high level levodopa therapy in severely akinetic parkinosnian patients. Arch Neurol 33: Charcot J (1877) Clinical lectures on disease of the nervous system. Sydenham Society, pp Fahn H, Marsden C, Calne D (1987) Recent developments in Parkinson s disease. Macmillan Health Care Information, Florham Park, pp Giladi N, Fahn S (1998) Freezing phenomenon, the fifth cardinal sign of parkinsonism. In: Fisher A, Hanin I, Yoshida M (eds) Progress in Alzheimer s and Parkinson s diseases. Plenum Press, New York London, pp Giladi N, McMahon, Przedborski S, Flaster E, Guillory S, Kostic V, Fahn S (1992) Motor blocks in Parkinson s disease. Neurology 42: Giladi N, McDermott M, Fahn S, Przedborski S, Parkinson Study Group (1996) Freezing of gait in Parkinson s disease. Neurology 46: A377(Abstract) Giladi N, Kao R, Fahn S (1997) Freezing phenomenon in patients with parkinsonian syndromes. Mov Disord 12: Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn AD (2000) Construction of freezing of gait questionnaire for patients with parkinsonism. Parkinsonism and Related Disorders 6: Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression, and mortality. Neurology 17: Holloway R and the Parkinson Study Group (2000) Pramipexole versus Levodopa in early Parkinson s disease: a randomized clinical trial. Neurology 54: A89 A89 (Abstract)

9 Freezing of gait in patients with advanced Parkinson s disease 61 Hughes A, Daniel S, Kilford L, Lees A (1992) Accuracy of clinical diagnosis of idiopathic Parkinson s disease a clinico pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55: Lamberti P, Armenise S, Castaldo V, de Mari M, Iliceto G, Tronci P, Serlenga L (1997) Freezing gait in Parkinson s disease. Eur Neurol 38: Martin J (1967) Disorder of locomotion associated with disease of the basal ganglia. In: Anonymous: The basal ganglia and posture. JB Lippincott, Philadelphia, pp Parkinson Study Group (1996) Impact of Deprenyl and tocopehrol treatment on Parkinson s disease in DATATOP subjects requiring levodopa. Anal Neurol 39(1): Quinn N (1994) Multiple system atrophy. In: Marsden CD, Fahn S (eds) Movement disorders 3. Butterworth-Heinemann, Oxford, pp Rascol O, Brooks D, Korczyn A, De Deyn P, Clarke C, Lang A (2000) A five-year study of the incidence of dyskinesia in patients with early Parkinson s disease who were treated with ropinirole or levodopa. N Engl J Med 342: Schwab R, England A, Peterson E (1959) Akinesia in Parkinson s disease. Neurology 9: Snedecor G, Cochran W (1980) Analysis of frequencies. In: Anonymous: Statistical methods. The Iowa State University Press, Ames, pp Ueno E, Yanagisawa N, Takami M (1993) Gait disorders in parkinsonism. A study with floor reaction forces and EMG. Adv Neurol 60: Weiner WJ, Factor SA, Sanchez RJ, Singer C, Sheldon C, Cornelius L, Ingenito A (1993) Early combination therapy (bromocriptine and levodopa) does not prevent motor fluctuations in Parkinson s disease. Neurology 43: Authors address: Dr. N. Giladi, Movement Disorders Unit, Department of Neurology, Tel-Aviv Sourasky Medical Center, 6 Weizmann Street, Tel Aviv, Israel 64239, Fax 972/3/

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