ORIGINAL ARTICLE
Effects of Treadmill Inclination on the Gait of Individuals
With Chronic Hemiparesis
Cinthia C. Moreno, MSc, Luciana A. Mendes, MSc, Ana R. Lindquist, PhD ABSTRACT. Moreno CC, Mendes LA, Lindquist AR.
Ef-fects of treadmill inclination on the gait of individuals with chronic hemiparesis. Arch Phys Med Rehabil 2011;92: 1675-80.
Objective:To analyze the effects of electric treadmill incli-nation on the gait of individuals with chronic hemiparesis.
Design:Descriptive, observational study.
Setting:Laboratory for human movement analyses of UFRN.
Participants: Individuals (N⫽18) with a mean age of 55.3⫾9.3 years and a lesion time of 36⫾22.8 months.
Interventions:Not applicable.
Main Outcome Measures:Subjects were assessed for func-tional independence (FIM) and balance (Berg Balance Scale). Spatial-temporal variables were observed as well as the angular variation of the hip, knee, and ankle in the sagittal plane, while the individuals walked on the treadmill at 3 different inclina-tions (0%, 5%, and 10%).
Results:There was an increase in stance time between 0% and 5% (0.83⫾0.21 vs 0.87⫾0.20; P⫽.011) and 0% and 10% (0.83⫾0.21 vs 0.88⫾0.23; P⫽.021). The other spatial-tempo-ral variables did not change. During initial contact there was an increase in the hip, knee, and ankle flexion angle. An increase in hip amplitude was also observed between 0% and 10% (37.83⫾5.23 vs 41.12⫾5.63; P⬍.001) and 5% and 10% (38.80⫾5.96 vs 41.12⫾5.63; P⫽.002) and in knee amplitude between 0% and 10% (47.51⫾15.07 vs 50.30⫾12.82;
P⫽.040), as well as decreased hip extension and increased
dorsiflexion.
Conclusions:Treadmill inclination promoted angular altera-tions such as an increase in hip, knee, and ankle angle during initial contact and the swing phase and an increase in the amplitude of movement of the hip and knee, as well as an increase in stance time of the paretic lower limb.
Key Words: Biomechanics; Exercise test; Rehabilitation;
Stroke.
© 2011 by the American Congress of Rehabilitation
Medicine
S
TROKE, ONE OF THE MAIN causes of disability in adults, may cause serious difficulties in the performance of seemingly simple tasks.1In developed countries, stroke is the third most common cause of death.2 When the individuals do not die, they are left with functional consequences that result in a sedentary lifestyle with a number of limitations in the activ-ities of daily living.1The motor impairment caused by stroke is related to spasticity, abnormal muscle activation, alterations in sensation, reduced strength, and abnormal muscle extensibility. These factors gen-erate a series of modifications in the spatial-temporal charac-teristics of gait, such as reduced velocity, stride length, ca-dence, stance phase of the paretic leg, and cycle length symmetry.3-7Furthermore, the following modifications in an-gular displacement of the affected limb occur: a decrease in hip flexion, an increase in both knee and plantar flexion at initial contact (IC), a decrease in hip and knee flexion, and an increase in plantar flexion during the swing phase.3,5,8 All of these alterations in the gait pattern lead to the adoption of compen-satory strategies that increase the energy cost of gait.6
Considering that the pattern of human locomotion is highly adaptable to environmental differences, many researchers have studied the changes that inclined surfaces provoke in the gait of healthy individuals,9-16but few have assessed this condition in hemiparetic subjects. One such investigation was conducted by Leroux et al,10 who identified the existence of adaptation strategies in subjects with spinal cord lesion, even though electromyographic activity had been minimally affected by inclination. Moreover, we underscore the study by Werner et al,16who observed a number of alterations in spatial-temporal variables in the gait of individuals with hemiparesis, but who also determined that electromyographic activity was also min-imally affected. Even though we recognize the importance of this study, the kinematic responses that inclination may pro-mote in the gait of these subjects were not assessed, which could justify the presence of alterations in spatial-temporal variables.
It should also be pointed out that, in addition to the impor-tance of better understanding control strategies for walking on inclined surfaces, inclined treadmills have been widely used in clinical practice17-26 to promote the rehabilitation of subjects with hemiparesis, reduce the number of falls, and enable their access to urban environments. Thus, it is important to know the effect of inclination on hemiparetic gait to enhance clinical practice, make it well directed, and based on scientific evi-dence. Accordingly, the aim of this study was to observe if there would be alterations in the gait patterns of these individ-uals while they walked on the treadmill at inclinations of 5% and 10%, and if there is a difference between these 2 inclina-tion percentages. Our hypothesis is that treadmill walking on
From the Department of Physical Therapy, Federal University of Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil.
Supported by the Fundação de Apoio à Pesquisa do Estado do Rio Grande do Norte (Foundation for the Support of Research in the State of Rio Grande do Norte) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (National Research Council [grant no. 477462/2007-3]).
No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organi-zation with which the authors are associated.
Clinical trial registration number: ACTRN 12610000429055
Correspondence to Ana Raquel Rodrigues Lindquist, PhD, Av. Senador Salgado Filho, 3000, Caixa Postal 1524, CEP: 59072-970, Natal, RN, Brazil, e-mail:
araquel@ufrnet.br. Reprints are not available from the author. 0003-9993/11/9210-01040$36.00/0
doi:10.1016/j.apmr.2011.05.016
List of Abbreviations
ROM range of motion IC initial contact
inclined surfaces produces alterations in the kinematic patterns and spatial-temporal variables of hemiparetic individuals.
METHODS Participants
The sample was composed of individuals with chronic hemi-paresis after ischemic or hemorrhagic stroke and who were undergoing physical therapy treatment. The inclusion criteria were as follows: spasticity classified between levels 0 and 2 on the Modified Ashworth Scale of muscle spasticity27 for the
lower limb affected; ambulatory capacity classified between levels 3 and 5 on the Functional Ambulatory Classification27;
minimum sequela time of 6 months; absence of clinical signs of cardiac alterations (New York Heart Association, degree I)28;
absence of other orthopedic or neurologic impairment that caused gait alterations; not using orthotics on the paretic lower limb; and capacity to obey simple verbal commands. Exclusion criteria were: individuals whose systolic blood pressure rose 10mmHg during the treadmill test29 or whose heart rate
ex-ceeded 75% of the age-adjusted maximum heart rate according to the formula proposed by Tanaka et al,30and those who had
a fear of falling while walking on the treadmill. All the indi-viduals signed an informed consent form, and the study was approved by the institutional research ethics committee.
Measuring Instruments
Functional independence in the activities of daily living was assessed using the FIM.31 To evaluate balance, we used the Berg Balance Scale,32 which has proved to be an effective instrument for assessing the balance of hemiparetic individu-als.33-35
Gait analysis was conducted with the subjects walking on a Gait Trainer System 2 treadmill.aA Biodex Unweighting Sys-temawas used, but no weight was supported by the system. It was used for safety purposes only, to avoid falls or false steps. The data were captured using the Qualisys Motion Capture System.b Three Qualisys ProReflex MCU-240 cameras that emit infrared light and spherical passive markers were used. The data were captured at a frequency of 120Hz.
Experimental Protocol
After initial assessment, where clinical and demographic data, anthropometric measures, and vital signs (heart rate and blood pressure) were collected, functional independence and balance assessments were made to characterize the sample.
We conducted gait analysis with barefoot individuals, plac-ing reflective markers on the followplac-ing bone structures: greater trochanter, medial and lateral epicondyle of the femur, medial and lateral malleolus, calcaneus, and the 5th and 1st metatarsal head. Markers were used to trace the segments in space during movement and were placed on the middle third and lateral surface of the thigh and leg. These consisted of 4 markers noncollinearly placed on a square base fixed with Velcro to an elastic neoprene strip. Markers were also placed on the calca-neous and 1st metatarsal head of the nonparetic foot.36-38
The speed used on the treadmill was calculated using a chronometer during overground walking on a 10-m long walk-way.16The mean velocity obtained from the 3 passes on the
walkway was used, disregarding the acceleration and deceler-ation phases. Later, the individuals were instructed on the correct trunk posture and upper limb position and transfer weight over the hemiplegic limb to be used during the treadmill protocol. All the individuals were capable of understanding this command and walked satisfactorily on the treadmill.
Static collection was conducted with the individuals in the orthostatic position (position of reference) in order to provide data for the future creation of their biomechanical model. The data were collected for 5 seconds.
The treadmill was then turned on and the speed gradually increased until it reached the velocity calculated during the 10-m test. After 2 minutes, a 30-second video capture was made (dynamic collection). All the individuals were submitted to collections on the treadmill with inclinations of 0%, 5%, and 10%, according to earlier studies.10-12 To avoid fatigue, a
3-minute rest period was given between the different condi-tions.16
Data Analysis
The data generated by Qualisys were exported to Visual 3D version Basic/RT 3.99.25.8.cThis system enables the construc-tion of a biomechanic model and the assessment of the spatial-temporal variables of gait, as well as angular variation. Angular displacements of each joint were obtained according to the angle sequence proposed by Cardan.39The reference or
ortho-static position was considered the neutral position.
To eliminate the noise caused by the movement of markers, a low-pass Butterworth filter was used at a cutoff frequency of 6Hz.40
Hip, knee, and ankle angular displacements were represented in percentage over the course of the gait cycle (0%–100%). To determine the start and end of the cycle, 2 consecutive IC events of the paretic foot were needed. This was achieved by observing the markers placed on the calcaneus or head of the 5th metatarsus. Raising the foot off the treadmill was deter-mined by the marker placed on the head of the 5th metatarsus. The events were defined based on the graphic representation of these markers on the y axis.41 These definitions were also
determined for the nonparetic foot to provide data for the analysis of gait-related variables.
Only the 5 best cycles were selected for analysis. The spatial and temporal gait variables investigated were: velocity (m/s), cadence (steps/min), step length (m), cycle time (s), step time of the paretic and nonparetic leg (s), support time and swing time of the paretic leg (s), and interlimb symmetry ratio. To calculate the symmetry ratio, the following formula was used42:
interlimb symmetry ratio⫽
2(NP step time) ⁄ (NP step time⫹ P step time), where NP stands for nonparetic and P stands for paretic.
In relation to angular variables, we investigated the angular displacements and range of motion (ROM), in degrees, of the hip, knee, and ankle in the sagittal plane. ROM was obtained by subtracting the minimum from the maximum value reached. Hip and knee joint angles were analyzed in the following events: IC, maximum stance extension, and maximum swing flexion. For the ankle, the events were IC, maximum stance, and swing dorsiflexion and maximum plantar flexion.11,14,42
Statistical Analysis
Data analysis was conducted using Statistica 7.0dat a 95% confidence interval.
Descriptive analysis was performed using central tendency and SD. The Shapiro-Wilk test was used to test normality. The parametric analysis of variance test with a randomized block design was also used. The Tukey post hoc test was used to detect statistically different measures. When the data did not show normative distribution, the Friedman and Wilcoxon tests
were used. The variables that showed normative distribution were cycle time, stride time in the paretic and nonparetic limb, stance time, intralimb symmetry, and maximum ankle dorsi-flexion in the swing phase. The other variables analyzed did not exhibit normative distribution.
RESULTS
Out of a total of 23 individuals, 18 took part in this study (10 men and 8 women): 8 with left hemiparesis and 10 with right hemiparesis. Five subjects were excluded owing to alterations in blood pressure, heart rate, and fear of falling off the tread-mill. The clinical and demographic characteristics were de-scribed (table 1).
Spatial-Temporal Variables
There was a decrease in cadence between 0% and 10% (91.12⫾18.29 vs 88.14⫾18.68) and between 5% and 10% (92.13⫾20.94 vs 88.14⫾18.68), but no significant differences were found (P⫽.160). Stance time increased with inclination and the differences were seen using the Wilcoxon test, com-paring 0% and 5% (0.83⫾0.21 vs 0.87⫾0.20; P⫽.011) and 0% and 10% (0.83⫾0.21 vs 0.88⫾0.23; P⫽.021). Step length (P⫽.230), cycle time (P⫽.153), step time of the paretic (P⫽.150) and nonparetic limb (P⫽.330), paretic limb swing time (P⫽.118), and the interlimb symmetry ratio (P⫽.219) were minimally affected and showed no significant difference (table 2).
Angular Variables
The graphic representation of the hip, knee, and ankle joint angles in the sagittal plane during the gait cycle of the indi-viduals assessed was made for each of the 3 treadmill condi-tions (fig 1).
Analysis of the hip joint, using Tukey ad hoc test, showed significant differences at IC, maximum extension, and
maxi-mum swing flexion. With an increase in inclination, there was an increase in flexion at IC at 0%, 5%, and 10% (P⬍.001) and in swing at 0%, 5%, and 10% (P⬍.001). There was a decrease in maximum extension during the terminal stance between 0% and 5% inclination (P⫽.021), 0% and 10% (P⬍.001), and 5%
Table 1: Clinical and Demographic Characteristics of the Individuals (Nⴝ18)
Characteristics Mean⫾ SD Range
Age (y) 55.33⫾9.37 39–76
Body mass (kg) 70.39⫾10.16 50.0–91.5 Height (m) 1.61⫾0.09 1.47–1.76 Lesion time (mo) 34.00⫾22.80 8–84 Speed (m/s) 0.71⫾0.28 0.22–1.14
FIM 79.50⫾5.89 70–88
BBS 47.11⫾8.69 22–54
Abbreviation: BBS, Berg Balance Scale.
Table 2: Spatial-Temporal Variables During Treadmill Walking
Spatial-Temporal Variables 0% 5% 10% Cadence (steps/min) 91.12⫾18.29 92.13⫾20.94 88.14⫾18.68 Stride length (m) 0.84⫾0.26 0.86⫾0.26 0.85⫾0.25 Cycle time (s) 1.26⫾0.23 1.28⫾0.23 1.29⫾0.26 P step time (s) 0.69⫾0.16 0.69⫾0.16 0.71⫾0.17 NP step time (s) 0.57⫾0.09 0.58⫾0.10 0.58⫾0.11 Stance time (s) 0.83⫾0.21*† 0.87⫾0.20* 0.88⫾0.23† Swing time (s) 0.40⫾0.07 0.41⫾0.07 0.42⫾0.07
Interlimb symmetry ratio 0.91⫾0.09 0.92⫾0.09 0.90⫾0.09 NOTE: Values are presented as mean⫾ SD.
Abbreviations: NP, nonparetic lower limb; P, paretic lower limb. *P⫽.011;†P⫽.021.
Fig 1. Mean angular variation of the (A) hip, (B) knee, (C) and ankle in the sagittal plane during treadmill walking at inclinations of 0%, 5%, and 10%. The positive representation indicates flexion (or dor-siflexion) and the negative indicates extension (or plantar flexion).
and 10% (P⫽.031). An increase was also observed in ROM between 0% and 10% (P⬍.001) and 5% and 10% (P⫽.002) (table 3).
In the knee, no differences were found in the maximum stance extension and the maximum swing flexion. According to the Tukey test, at IC, differences occurred between 0% and 10% and between 5% and 10% (both with P⬍.001). At max-imum stance flexion, the differences occurred between 0% and 10% (P⬍.001) and between 5% and 10% (P⫽.004). ROM was different only between 0% and 10% (P⫽.040) (seetable 3).
In the ankle, no significant maximum dorsiflexion differ-ences were observed during stance or maximum plantar flex-ion. At IC there were differences only between 0% and 10% (Tukey ad hoc test P⫽.021). Maximum swing dorsiflexion only showed a difference between 5% and 10% (Wilcoxon test
P⫽.040). No differences were found in ROM (seetable 3).
DISCUSSION Spatial-Temporal Variables
The spatial-temporal gait variables showed that higher de-grees of inclination resulted in an increased stance time, whereas the other variables showed no significant alterations. Studies that compared the overground and treadmill gait of hemiparetic individuals showed that the treadmill promoted an increase in stance time, likely owing to better body alignment resulting from the partial body-weight support system.4,42 In
this study, the harness support was used only for safety pur-poses; however, the fact that the subjects held onto the front bar while walking may have interfered in body alignment. Further-more, it was observed that stance time increased linearly as a function of the inclination percentage. Thus, it is believed that inclination was an additional factor that contributed to the increase of this variable and that the absence of alterations in the remaining variables may be explained by the constant speed and speed variability of individuals who walked at a comfort-able, self-selected speed (0.22-1.14m/s).10-12,14
Werner et al16 assessed individuals with hemiparesis and
observed an increase in stance time, a decrease in swing time, an increase in stride length, and decreased cadence. According to Visintin,43and Hesse44,45and colleagues, the use of partial
weight support on the treadmill produces an improvement in spatial-temporal gait variables such as speed, cadence, cycle length, and symmetry. However, in the present study, speed was maintained constant and body weight was not supported, a fact that may have interfered in cadence and in the other variables analyzed.
Angular Variables
In relation to the angular variables, it was observed that at IC and in the swing phase that there was an increase in hip and knee flexion and in ankle dorsiflexion only during IC. In healthy individuals, according to Leroux,10,12and Lay14and
colleagues, higher degrees of inclination caused an increase in hip and knee flexion and in ankle dorsiflexion during IC and in the swing phase. Prentice et al13also observed an increase in
flexion in the same joints during the swing phase. These authors explained that the aforementioned characteristics result from the need to elevate the lower limb and thrust the body forward while ascending. Similar results were found by Leroux et al.10in a study investigating the effects of treadmill
incli-nation on individuals with sequela from spinal cord lesion in the hip joint. The other joints, however, showed no alterations, possibly owing to the limitations in knee and ankle joint adaptation caused by neural or biomechanic factors.
Leroux et al11also observed that in healthy individuals, the
increase in hip flexion was used as adaptation to treadmill inclination, resulting in an increased stride length. In our study, the increase in hip flexion was not accompanied by an increase in stride length, but the increased flexion suggests that individ-uals with hemiparesis also use adaptation strategies to change limb trajectory and ensure IC on a more elevated surface.13
Stride length did not increase with inclination, likely because of the reduced hip extension.
The decrease in hip extension and increase in flexion found in our study also may be explained by the need to elevate the limb to ensure contact at a higher level, as observed by Lay et al.14It is important to point out that even though there was a
reduction in extension, hip joint amplitude increased between 0% and 10% and between 5% and 10%. Given that individuals with hemiparesis show a decrease in hip flexion on IC and in swing and a consequent reduced amplitude,3,5 the increase in
Table 3: Angular Variables of the Hip, Knee, and Ankle During Treadmill Walking at Inclinations of 0%, 5%, and 10%
Angular Variables 0% 5% 10%
Hip
IC 23.11⫾4.33* 26.12⫾4.86* 29.99⫾3.97*
Maximum stance extension ⫺12.41⫾5.60*† ⫺10.79⫾6.14†‡ ⫺9.28⫾5.36*‡
Maximum stance flexion 25.42⫾4.76* 28.02⫾4.94* 31.84⫾4.82*
ROM 37.83⫾5.23* 38.80⫾5.96§ 41.12⫾5.63*§
Knee
IC 17.59⫾8.58* 18.52⫾8.31储 22.16⫾7.82*储
Maximum stance flexion 17.36⫾11.14* 18.01⫾10.73储 21.08⫾11.24*储
Maximum stance extension 3.20⫾9.87 3.10⫾10.36 2.79⫾9.75 Maximum swing flexion 50.71⫾13.65 51.53⫾12.40 53.09⫾10.53
ROM 47.51⫾15.07¶ 48.43⫾14.24 50.30⫾12.82¶
Ankle
IC ⫺1.83⫾8.08† ⫺1.51⫾8.11 ⫺0.59⫾7.29†
Maximum stance dorsiflexion 5.80⫾5.11 6.13⫾5.40 6.63⫾5.38 Maximum plantar flexion ⫺5.41⫾8.57 ⫺6.20⫾8.17 ⫺4.66⫾8.48 Maximum swing dorsiflexion 1.45⫾8.08 1.74⫾7.95¶ 2.50⫾7.42¶
ROM 11.21⫾7.90 12.33⫾7.77 11.29⫾7.82
NOTE: Values are presented as mean⫾ SD.
these parameters, which occurred at inclinations of 5% and 10%, may be a positive factor in promoting and stimulating a near-normative amplitude.5Improving these parameters is the desired goal in the rehabilitation of hemiparetic individuals, given that such an outcome increases their ability to move body mass forward, thereby enhancing gait quality.
The knee joint showed that the individuals made IC with excessive flexion (17.59⫾8.58 at 0%, 18.52⫾8.31 at 5%, and 22.16⫾7.82 at 10%), possibly owing to ischiotibial or plantar flexor muscle spasticity or knee extensor weakness, which leads to flexion posture in the swing phase as well.3,8,10,46 There was no significant difference in maximum extension or maximum swing flexion, but inclination promoted a beneficial effect, given the significant increase in amplitude between 0% and 10%.
Qualitative analysis of IC showed that 10 of the 18 individ-uals made contact with the ankle plantar flexed, but with an increase in inclination to 10%, there was a significant decrease. In other words, there was a tendency toward the neutral posi-tion, which approaches the normative pattern seen in healthy individuals.3,6,8 According to Leroux et al,11the increase in
dorsiflexion occurs to accommodate the vertical orientation of the torso and the pelvis during the ascent phase, and this also may have occurred in hemiparetic individuals. This factor is positive, because it may contribute to improving dorsiflexion activation or mechanical properties (decreased stiffness) of muscles involved in plantar flexion and might also promote a decrease in the need to perform hip circumduction during the swing phase.
It is known that inclined surfaces pose significant challenges to the locomotor control system, in addition to resulting in substantial complications for subjects with pathologic gait caused by neurologic impairment. Thus, kinematic alterations and possible adjustments in limb trajectory may lead to a decrease in compensatory strategies and, in turn, to a decrease in energetic cost, greater access to certain environments, and reduced risk of falling.
Study Limitations
The small number of cameras used in this study precluded kinematic analysis of the hip and the nonparetic limb and small number of subjects. Additionally, no electromyographic assess-ment was performed, which could indicate the strategies used in the angular alterations occurred at 5% and 10% inclination.
CONCLUSIONS
According to these findings, we conclude that treadmill inclination promotes alterations in the angular variables of gait such as an increase in hip, knee, and ankle angle during IC and the swing phase, as well as an increase in ROM of the hip and knee. With respect to spatial-temporal variables, we conclude that inclination promotes minimal alterations, because only the stance time of the paretic lower limb was altered, evidenced by the increase of this variable. These results support further studies on the use of inclined treadmill walking in stroke rehabilitation and whether inclined walking training is effective in improving any of the functional limitations of patients post-stroke.
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Suppliers
a. Biodex Medical Systems Inc, 20 Ramsay Rd, Shirley, NY 11967-4704.
b. Qualisys Medical AB, Packhusgatan 6, 411 13 Gothenburg, Swe-den.
c. C-Motion Inc, 20030 Century Blvd, Ste 104A, Germantown, MD 20874.
