Functional Assessment of Lower Extremities in Hereditary Spastic Paraplegia

Article Outline

• Abstract
• Methods
  • Statistical Analysis
• Results
• Discussion
  • Study Limitations
• Conclusions
• References
• Suppliers
• Copyright

Abstract 

Braschinsky M, Parts K, Maamägi H, Gross-Paju K, Haldre S. Functional assessment of lower extremities in hereditary spastic paraplegia.

Objectives

To characterize the spasticity and range of motion (ROM) in patients with hereditary spastic paraplegia (HSP) and to correlate these parameters with walking speed.

Design

An observational population-based cohort study.

Setting

Patient data were acquired from a population-based epidemiologic study performed earlier in Estonia.

Participants

Persons (N=46) (mean age, 50.1y) with clinically confirmed HSP diagnosis (mean duration, 20.9y) participated in the study.

Interventions

Active and passive ROMs were measured with a plastic 360° goniometer. Spasticity was evaluated by using the modified Ashworth scale (MAS). The time it took a patient to walk 10m was recorded.

Main Outcome Measures

Measurements included testing of active and passive ROM as a marker for mobility, the MAS for spasticity, and time to complete a 10-m walk.

Results

A higher degree of spasticity in hip muscles was associated with lower values of active ROM and slower walking. Walking speed was negatively correlated to disease duration and participant age.

Conclusions

The present study provides analysis of the contributions of spasticity and ROM to walking speed in HSP, both factors negatively influence gait in persons with HSP.

Key Words: Gait, Muscle spasticity, Range of motion, articular, Rehabilitation, Spastic paraplegia, hereditary

List of Abbreviations: CC, correlation coefficient, cHSP, complex hereditary spastic paraplegia, HSP, hereditary spastic paraplegia, MAS, modified Ashworth scale, pHSP, pure hereditary spastic paraplegia, ROM, range of motion

HEREDITARY SPASTIC PARAPLEGIA is a neurodegenerative disorder characterized by progressive spasticity, hyperreflexia, and motor deficit of the legs. The reported prevalence of HSP varies from 0.5 to 12 per 100,000.¹, ², ³ Recently, the prevalence of HSP in Estonia was estimated to be 4.4 per 100,000.⁴ The severity and age of onset are mainly determined by genetic background.⁵ To date, more than 30 different loci for HSP, termed spastic paraplegia genes, have been identified. HSP is classified clinically into “pure” (pHSP) and “complex” (cHSP) forms. The pHSP forms present with spasticity and motor deficit in the legs, brisk reflexes, and Babinski sign, are often accompanied by deep sensory impairment and sphincter disturbances. A number of other neurologic or extraneurologic features are associated with cHSP. Although HSP is generally considered a mild disease, its clinical course varies greatly from severe congenital presentation to mild involvement in old age. Although HSP does not shorten the life expectancy, it does interfere with the quality of life of the patient. This topic is poorly investigated. It was somewhat looked into as a part of interventional studies only.⁶, ⁷ To date, there are no specifically disease-oriented descriptive studies in HSP.

Gait disturbance in HSP is characterized by shortened strides caused by limited hip flexion and foot dorsiflexion.⁸ Lower-limb spasticity is particularly observed in the hamstrings, quadriceps, dorsiflexors, and thigh adductors.⁸, ⁹ The clinical peculiarity of HSP that separates it from other causes of spastic paraparesis is that the spasticity contributes to gait disturbance disproportionally more than the paresis, with a notable discrepancy between the degrees of spasticity and muscle weakness. This is shown by HSP patients who use wheelchairs because of spasticity but have nearly normal muscular power.⁹ This phenomenon and the detailed pathophysiologic mechanisms and causative factors of the disease have not been adequately explained.

Assistive devices, such as walkers, canes, or wheelchairs, may be required as the disease progresses, depending on its clinical course.¹⁰ Common treatments focus on reducing spasticity through antispastic medications, including botulinum toxin and physical therapy. Such therapies reduce the symptoms without treating the underlying cause and unfortunately are not effective in all cases.⁷ Hence, one of the main cornerstones in the management of persons with HSP is an appropriate physical therapy, which by itself relies on a knowledge of a clinical presentation and gait features of the disease. Considering its clinical uniqueness, there is a need for a detailed functional evaluation of HSP progression. To date, only a few analyses of gait in HSP have been published.¹¹, ¹²

The goal of this descriptive study was to evaluate the role of spasticity and ROM in gait disturbance in HSP, considering the duration of the disease and the age of the patient. The main question aimed to be answered was do spasticity and ROM influence gait in persons with HSP.

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Methods 

Patient data were acquired from an epidemiologic study.⁴ A diagnosis of HSP, based on previously published criteria¹³, ¹⁴ was the main and obligatory inclusion citerion. All persons who either did not have HSP diagnosis or did not consent for participation in the study were excluded. Forty-six subjects with a clinical diagnosis of HSP consented to be included in the study, including 29 men and 17 women. The demographic data of the participants are presented in table 1. The mean age of the participants was 50.1 years (range, 11–75y). The mean age at onset was 29.2 years (range, 3–57y), and the mean disease duration was 20.9 years (range, 3–42y). Assistive devices were used by 22 patients; 14 participants used a unilateral cane, 5 used bilateral crutches, and 3 used a wheelchair because of the severity of the disease.

Table 1. Characteristics of Patients With HSP

Pt	Sex	Age (y)	Age at Onset (y)	Disease Duration (y)	SPG4	Family History	Assistive Device	MAS Hip Fl. Right/Left	MAS Hip Abd. Right/Left	MAS Ft. Dors. Right/Left
1	M	52	41	11	Negative	Present	Unilateralcane	2/2	1/1	3/3
2	F	62	40	22	Negative	Absent	Unilateralcane	2/2	2/2	2/2
3	M	58	44	14	Negative	Absent	None	2/0	0/0	2/2
4	F	39	13	26	Negative	Present	None	3/3	3/3	4/4
5	F	17	13	4	Negative	Present	None	1/0	1/0	2/2
6	M	56	17	39	Negative	Present	None	1/0	0/0	0/2
7	M	22	15	7	Negative	Present	None	1/1	0/0	1/1
8	M	52	28	24	Negative	Present	Bilateralcrutches	2/2	2/3	2/2
9	M	49	28	21	Positive	Present	Bilateralcrutches	2/2	3/3	3/2
10	M	33	5	28	Negative	Present	None	2/1	2/2	3/1
11	F	11	8	3	Negative	Present	None	0/0	0/0	1/1
12	M	75	38	37	Positive	Present	Wheelchair	2/3	3/3	2/2
13	M	51	45	6	Negative	Absent	None	1/1	0/0	1/1
14	M	42	13	29	Negative	Present	None	1/1	2/2	1/1
15	F	59	24	35	Negative	Absent	None	2/2	2/2	3/3
16	F	55	28	27	Negative	Present	Unilateralcane	4/4	4/4	4/4
17	M	26	3	23	Positive	Absent	None	0/0	0/0	0/0
18	M	39	29	10	Negative	Absent	None	0/0	3/3	3/3
19	M	45	18	27	Negative	Present	Unilateralcane	3/3	1/1	2/2
20	M	54	40	14	Negative	Present	Unilateralcane	1/1	2/2	2/2
21	M	33	21	12	Positive	Present	Bilateralcrutches	0/0	1/1	3/3
22	F	58	40	18	Negative	Present	Unilateralcane	2/1	2/2	3/3
23	F	40	12	28	Negative	Present	Bilateralcrutches	3/4	4/4	4/4
24	M	67	29	38	Negative	Absent	Unilateralcane	4/4	4/4	4/4
25	F	60	30	30	Negative	Present	Unilateralcane	0/0	2/2	3/3
26	M	56	30	26	Negative	Absent	None	2/2	1/1	2/2
27	M	70	35	35	Negative	Absent	Unilateralcane	1/1	2/2	2/2
28	M	55	40	15	Negative	Present	None	0/0	0/0	0/0
29	F	60	18	42	Negative	Present	None	0/0	2/2	2/2
30	F	53	28	25	Negative	Present	None	3/3	0/0	2/2
31	M	58	31	27	Negative	Absent	Wheelchair	3/3	3/4	4/4
32	M	65	36	29	Negative	Present	Bilateralcrutches	0/0	0/0	0/0
33	M	60	50	10	Negative	Absent	Unilateralcane	0/0	0/0	1/1
34	F	50	30	20	Positive	Present	None	0/0	1/1	1/1
35	F	49	35	14	Positive	Present	None	1/1	1/1	2/1
36	F	18	10	8	Positive	Present	None	1/1	1/1	1/1
37	M	45	35	10	Negative	Absent	None	1/2	3/3	4/4
38	F	56	46	10	Positive	Present	Unilateralcane	0/0	0/0	0/0
39	M	53	37	16	Negative	Absent	Unilateralcane	3/3	4/4	4/4
40	M	61	28	33	Negative	Absent	Unilateralcane	2/2	3/3	3/2
41	F	34	30	4	Negative	Present	None	2/3	1/1	4/4
42	M	61	40	21	Negative	Present	Wheelchair	3/3	4/4	4/4
43	M	56	40	16	Positive	Present	None	1/1	2/2	4/3
44	M	66	35	31	Negative	Present	Unilateralcane	3/3	3/3	3/3
45	F	64	57	7	Negative	Present	None	2/1	2/1	1/1
46	M	60	32	28	Negative	Present	None	1/1	1/1	4/4

Abbreviations: Pt, patient; M, male; F, female; Hip Fl., hip flexion; Hip Abd., hip abduction; Ft. Dors., foot dorsiflexion.

Active and passive ROMs of hip flexion, hip abduction, and foot dorsiflexion were measured with a plastic 360° JAMAR Goniometer.^15,a For all ROM measurements, the participants were asked to lie supine. To measure the active hip flexion, the legs were extended and the pelvis stabilized by the therapist, who placed the goniometer pin on the greater trochanter of the femur. The value was recorded upon slow hip flexion (with the knee flexed) by the patient. To measure the passive hip flexion, the femur was moved to the limit of hip flexion by the therapist, who applied a slight overpressure at the end of this movement.

To measure the active hip abduction, the goniometer axis was placed on the hip. The patient moved his/her leg to the side while the therapist recorded the value. To measure the passive hip abduction, the same movement was performed and documented by the therapist. Ankle dorsiflexion was measured with a roll placed under the knee of the measured leg to maintain a knee flexion of ∼ 20° to 30°. One axis was placed under the lateral malleolus, and the initial goniometer position had to indicate 90°. After this measurement, the degree of active flexion of the foot was recorded. The passive value was documented by the therapist, who applied traction to the calcaneus and moved the dorsal part of the foot toward the anterior aspect of the lower leg to the limit of the ankle dorsiflexion.

All movements were measured 3 times with a 1-minute rest between measurements, and the best result was documented by 1 physiotherapist. The reliability of repetitive goniometric measurements performed in standardized conditions by the same investigator has been shown.¹⁶ The normal active ROM for hip flexion is 0° to 120°, for hip abduction it is 0° to 45°, and for foot dorsiflexion it is 0° to 20°.¹⁷

Spasticity was evaluated by using the MAS to assess the following antagonist muscles: hamstrings, thigh adductor, gastrocnemius, and soleus. A 0 to 5 grading system¹⁸, ¹⁹ was applied as follows: 0, no increase in muscle tone; 1, a slight increase in tone with a catch and release or minimal resistance at the end of the range; 2, similar to 1 but with minimal resistance through the range following catch; 3, more markedly increased tone through ROM; 4, considerable increase in muscle tone, passive movement difficult; and 5, affected part rigid.

The time it took a patient to walk 10m was also recorded²⁰ by 1 physiotherapist in all participants except 2 patients who were unable to walk and used a wheelchair because of their disability. The patients were permitted to use their regular assistive device to perform the walk. They were asked to perform the walk at their possible best. One attempt was documented. This study was approved by Ethics Review Committee on Human Research of the University of Tartu.

Statistical Analysis 

The data were tested for normality. The continuous data are expressed as the mean ± SD if distributed normally or otherwise by medians with 25th and 75th percentile ranges. To compare active and passive ROMs, a Wilcoxon signed rank test for medians was performed after checking for the normal distribution of the data. Associations between variables (ROM, MAS, walking speed) were examined by using univariate and regression analyses. A correlation analysis was applied to determine the effects of ROM and spasticity on the walking speed. Free software R (version 2.2.0)^b was used for all statistical analyses. Significance was defined as P<.05.

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Results 

The median scores for active and passive ROMs are shown in table 2. The active and passive ROMs were below normal values in all joints except for the passive hip flexion, and the described differences were statistically significant.

Table 2. Active and Passive ROM of Subjects, Normal ROM, MAS of the Antagonist Muscles, and Relationship Between Active ROM and Spasticity in Measured Motor Functions

NOTE. Significance is defined as P<.05.

Abbreviation: IQR, interquartile range.

The median spasticity value was calculated based on the measured MAS parameters. The median MAS scores and interquartile ranges are shown in table 2. A higher degree of spasticity was associated with lower values of active ROMs. The strongest correlation between ROM and spasticity was observed for the hip abduction. Foot dorsiflexion showed the least correlation with spasticity.

The mean gait speed determined from a 10-m walk was 0.96 m/s (range, 0.2–2.3 m/s). A higher active ROM correlated with a faster speed for all joints (table 3). As with spasticity, the strongest correlation between ROM and walking speed was observed in the hip abduction (CC=.62, P<.001). The correlation with foot dorsiflexion (CC=.31, P<.05) did not reach statistical significance after adjusting for age and symptom duration, although a trend did remain (P<.10). A higher degree of spasticity correlated with a slower walking speed (CC=−.55, P<.0001). The walking speed was also influenced by the age of participants (CC=−.49, P<.0001) and the duration of symptoms (CC=−.32, P=.03).

Table 3. Relationship Between Active ROM of Measured Motor Functions and 10-m Walk Time

NOTE. Significance is defined as P<.05.

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Discussion 

The main goal of this study was to evaluate the influence of spasticity and ROM on gait in persons with HSP. To our knowledge, there have been no published analyses of the relationships between ROM, spasticity, and walking speed in patients with HSP, which makes the direct and complete comparison of our results with others impossible. There are some interventional studies, which were oriented toward the analysis of the effect of different treatment options upon the dysfunction in HSP.⁶, ⁷ Within the few available descriptional studies, like the present one, Klebe et al¹¹ conducted 3-dimensional gait analysis but did not investigate the influences of ROM and spasticity on gait. Comparable in both studies were the walking speed and some kinematic variables, which can be used for indirect comparisons only. However, the complementation of 1 study by another, using different approaches to the same clinical problem, is what possible comparative analysis of both works could and should represent.

We investigated ROM and MAS because they are routinely used in physiotherapeutic assessments. In normal gait, hip flexion and foot dorsiflexion play important roles at the beginning and end of the swing phase. Our results showed markedly limited foot dorsiflexion in HSP. Spasticity was increased in all muscles, as measured by MAS, consistent with the nature of the disease. Similar results have been reported by others.⁸, ²¹ Increased spasticity correlated with the active ROMs of the hip flexion and abduction and foot dorsiflexion. Limited active ROMs and increased spasticity on MAS both correlated with a reduced walking speed.

The evaluation of walking speed is widely used in physiotherapy assessment for patients with neurologic diseases.¹² A gait speed of less than 1m/s identifies persons at high risk for negative health-related outcomes.²² Hence, our results (a walking speed of 0.96m/s) indicate that persons with HSP represent a high-risk group for the aforementioned outcomes. According to our correlation analysis, walking speed in HSP was more influenced by the ROM of the hip muscles than by the ROM of the foot muscles.

In our study, walking speed was also influenced by the age of participants and the duration of symptoms. Not all studies have reached the same conclusions, which probably reflects the clinical variability and heterogeneity of the disease.¹¹

Study Limitations 

Nevertheless, there are some limitations of this study. Based on the evaluations performed within this particular work, it is inconclusive if the described changes actually influence the quality of life of persons with HSP. To determine if this is the case, specific studies are needed that use widely recognized measurement tools specifically designed to estimate the quality of life. Although our study team actually performed quality of life measurements, these are outside of the scope of the present publication and are to be published elsewhere. Another limitation to our study is related to the well-known fact that gait is also influenced by muscle strength. Because the clinical peculiarity of HSP is the clear dominance of spasticity, it was not the aim of this study to evaluate the degree of paresis itself, which is usually minor when compared with the influence of spasticity. Nevertheless, measuring muscle strength could further broaden our detailed understanding of gait in HSP, and it is important to continue research in this area.

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Conclusions 

In conclusion, we have shown that ROM and spasticity influence gait in persons with HSP. We have also shown that such analyses, particularly of the hip muscles, may provide a more complete functional analysis of the motor limitations in HSP than walking speed alone. Hence, the practical implications of these results suggest clinical applicability in everyday practice; physiotherapeutic evaluation of persons with HSP should always include measurements of ROM, MAS, and walking speed. These measurements could also be useful when performing longitudinal studies to observe disease progression or treatment studies to evaluate treatment effects. Further investigations are needed to combine the data to provide a more complete overview of the functional disabilities associated with HSP.

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