appliedsciences
ArticleBiomechanical Analysis of Gait Compensation Strategies as a
Result of Muscle Restriction
Jessica Beltran Ullauri 1 , Yasuhiro Akiyama 1, *, Shogo Okamoto 2 and Yoji Yamada 1
12*
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Citation: Ullauri, J.B.; Akiyama, Y.;
Okamoto, S.; Yamada, Y.
Biomechanical Analysis of Gait
Compensation Strategies as a Resultof Muscle Restriction. Appl. Sci. 2021,

Department of Mechanical Systems Engineering, Mechano-Informatics and Systems, Nagoya University,
Nagoya 464-8603, Japan; Gabriela.Hoerig@ottobock.de (J.B.U.); yoji.yamada@mae.nagoya-u.ac.jp (Y.Y.)
Department of Computer Sciences, Tokyo Metropolitan University, Hino, Tokyo 191-0065, Japan;
okamotos@tmu.ac.jp
Correspondence: akiyama-yasuhiro@mech.nagoya-u.ac.jp

Abstract: The loss of muscle mass with aging and consequent muscle weakness results in compensatory gait motions. Although these compensatory motions increase the cost of walking, they appear
to be an attempt by the elderly to maintain safe ambulation. However, the relationship between theaffected muscles and compensatory motions in the gait cycle is unclear. This study examined gait
compensation in young subjects whose muscles were weakened with Muscle Activity Restriction Taping Technique, which restricts the muscle’s belly by tightening the lower limb(s). The study included
different walking speeds (regular/slow) and restrictions (calf muscles/both calf and thigh muscles).
It revealed that there was an active kinematic compensation chain, in which the non-restricted or
less-restricted joints compensated for the affected joint to prevent foot drop, knee hyperextension
in the terminal stance phase, and knee hyperflexion in the loading response phase, and to maintainthe step length. Furthermore, joints could compensate for themselves when the muscles acting on
the other joints were unable to assist, as observed on an ankle joint that compensated for itself toprevent foot drop when the knee and hip flexor muscles were restricted. Moreover, the observed
compensation strategies agreed with a previously reported simulation on the gait compensations
appearing along with muscle weakness. This study includes a comparison of these compensation
strategies with those reported for the elderly. The results of this study provide an understanding of
the mechanisms of gait compensation against limitations of gait ability.

11, 8344. https://doi.org/10.3390/
app11188344

Keywords: muscle restriction; joint compensation; gait analysis

Academic Editor: Arkady Voloshin
Received: 28 July 2021
Accepted: 2 September 2021
Published: 8 September 2021

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Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

1. Introduction
Human physical ability deteriorates with aging. An important cause is the reduction in muscle strength, mainly owing to the loss of muscle fibers and muscle crosssectional area [1–4]. In fact, a loss of at least 30% of muscle mass is expected by the ageof 80 years [5,6]; this loss is greater in the lower limbs than in the upper limbs [7]. For
instance, with regard to the lower limbs, significant reductions in the muscle areas of thegluteus maximus, gluteus medius, psoas major, rectus femoris (RF), vastii (VAS), biceps
femoris short head (BFS), and gastrocnemius (GAS) muscles have been reported in theelderly when compared to the young [8].
With the reduction of the lower-limb muscle mass, the gait suffers from several
impairments because the loss of mass causes changes in the activity magnitude of theaffected muscles and their periods of action along the gait cycle. For instance, a shorter
range of activity of the GAS muscle has been reported in elderly with recurrent falls [9],and a lower activity of the same muscle has been found in the elderly during the latestance phase [10]. This last might explain the elderly less-powered ankle push-off [11].
Aniansson et al. [12] reported a reduction of 25–35% in the muscle strength of the leg
extensors in 70–80-year-old men. In addition, a peroneal nerve disfunction, that is aperipheral neuropathy commonly seen in the elderly, causes a lower activity or paralysis ofAppl. Sci. 2021, 11, 8344. https://doi.org/10.3390/app11188344

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Appl. Sci. 2021, 11, 8344

2 of 12the tibialis anterior (TA) muscle that in turn leads to foot drops (a gait abnormality where
the forefoot drops when getting closer to the ground) [13].
Thus, the motion pattern of the lower-limb joints deviates from the normal gait pattern,partially because of the effects of muscle weakness, and partially as a result of unconscious
compensation measures that the human takes to minimize the effects of muscle weakness
and maintain safe ambulation [14]. For instance, an increased hip power has been reported
in the elderly during the stance phase and has been suggested as a compensation for theirlower-powered push-off in the late stance phase [15]. Owing to a weak TA muscle during
the swing phase, the elderly exert a reduced ankle dorsal flexion; however, to maintain asafe ground clearance, the knee and/or hip joints compensate with a higher flexion [16].
According to the simulations of Van der Krogt [17] regarding the effects of muscle
weakness on a lower limb, a weakened muscle can compensate for itself by exerting higher
activity (as measured by electromyography), or can be compensated for by other muscles.
For instance, the main leg muscle groups can compensate in the following manner: (a)The weakness of the GAS and soleus (SO) muscle groups increases the activity of the BFS
muscle and decreases the activity of the TA muscle. Both the GAS and BFS muscles are
responsible for knee flexion; thus, the BFS compensates for the GAS function. Additionally,
the GAS and the SO muscles are responsible for plantar flexion, and the disability toexert plantar flexion is compensated by lowering the activity of the TA muscle that is
responsible for the ankle dorsal flexion. (b) The weakness of the hamstring (HAM) and
VAS muscles (which are responsible for knee flexion/hip extension and knee extension,respectively) increases the activity of these same muscle groups, and decreases the activityof the iliopsoas (ILPS) muscle (responsible for hip flexion). (c) The weakness of the RF
muscle, which is responsible for knee extension and hip flexion, increases the activity of
the ILPS and VAS muscles, and decreases the activity of the BFS muscle.
However, joint compensation motions vary widely, and the mechanisms for explaining
how and when they occur have not been sufficiently investigated. Furthermore, theobservation and analysis of such compensation motions are necessary to understand themechanisms of human motion with aging.
In a previous study, we developed the Muscle Activity Restriction Taping Technique(MARTT) that restricts the transversal area of the muscle belly where it is applied andweakens the muscle activity [18]. We hypothesized that the young whose lower-limb
muscles are restricted by MARTT would show compensation motions during walking suchthe ones seen as effect of muscle weakness that come with aging.
In this study, the compensations in the gait motion exhibited by young subjects while
walking with MARTT were observed and classified, to investigate the compensation strategies. The differences in the compensation motions across the walking speeds, muscle
restriction conditions, and subjects were compared and analyzed. The identified characteristics of the compensation strategies were validated based on the reported effects ofmuscle weakness in the gait simulations of Van der Krogt [17]. Furthermore, similarities tothe compensation motions reported in the elderly were considered. Figure 1 depicts themuscles and muscles groups that are referred in this study.

Appl. Sci. 2021, 11, 8344

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ILPS

RF

VAS

TA

HAM

GAS, SO

Figure 1. Location and abbreviations of muscles referred in this study. ILPS: iliopsoas muscle, RF:
rectus femoris muscle, VAS: vastii muscle group, HAM: hamstring muscle group, GAS: gastrocnemius
muscle, SO: soleus muscle, TA: tibialis anterior.

2. Materials and Methods
This study was performed with the permission of the Institutional Review Board of
Nagoya University, Japan, with Approval Number 14-4. This experiment was originallyperformed to validate the performance of the MARTT, a wearable device that aims tomodify the gait motion to that of the elderly [18].
2.1. Subjects
Ten healthy male young adults with a mean age of 22 years participated in this study.
The mean value and standard deviation of their weights and heights were 63.9 ± 8.9 and1.72 ± 0.05 m, respectively. Their dominant leg was the right leg.
2.2. Apparatus
Every gait experiment was conducted on a treadmill with a 1.4 × 0.5 m2 walking
surface (OMEGA3, Johnson Health Tech Co., Ltd., Taichung City, Taiwan). A motion
capture system (MAC 3D system, Motion Analysis Corporation, Rohnert Park, CA, USA)was used to record the gait motion at a frequency of 100 Hz. The joint patterns and subjects’postures were calculated by fitting the positions of reflective markers attached to thesubject to a motion module of Software for Interactive Musculoskeletal Modeling (SIMM,
Musculographics Inc., Santa Rosa, CA, USA). Furthermore, four flexible force-sensing
resistors (FSR-400, Interlink Electronics, Lake Forest, CA, USA) were embedded at eachshoe tip and shoe sole of comfortable sport shoes, to detect heel contact (HC) and toe off(TO) events.
The MARTT, which is a wearable device, that basically incorporates belts and force
sensors, for restricting lower-limb muscles by tightening the limb [18], was used in thisexperiment. With MARTT, the muscle contraction was disturbed by limiting the expansionof the cross section area of the muscle. The MARTT mainly restricted the GAS and TA
muscles, when it was used on the calf, and the HAM, VAS, and RF muscles, when it
was used on the thigh. The same restriction force was applied to each leg, which wasmonitored with the incorporated force sensors in MARTT. The applied force corresponded
to a pressure of approximately 180 mmHg, that is in the range of safe blood flow restriction(160–230 mmHg [19]) and below 200 mmHg that could cause muscle fatigue [20].

Appl. Sci. 2021, 11, 8344

4 of 122.3. Protocol
After an informed consent procedure, every subject wore a well-fitted sport suit andmarkers for the motion capture system. Next, the subjects were instructed to walk for ashort period of time to get accustomed to the shoes and the walking path on the treadmill.
The recording trials, each with a duration of 6 min, were initiated.
In this experiment, two walking speeds (regular/slow) and two muscle restriction
conditions (calf/calf and thigh) were investigated. The regular speed was set at 1.11 m/s(4 km/h), which is regarded as the natural walking speed of young adults [21], and theslow speed was set at 0.97 m/s (3.5 km/h), which is close to the average walking speed ofthe elderly [22]. The restriction of the calf and thigh was applied using the MARTT. In thefirst condition, the MARTT was applied on the calf. It was named as the calf restriction
condition (referred to as C-restriction). In the other condition, MARTT was applied on boththe calf and the thigh. It was named as the calf and thigh restriction condition (referred toas CT-restriction). In total, four walking conditions were investigated, i.e., the combinationsof the two levels of walking speeds and two types of restriction conditions.
In the recording session, six walking trials were recorded for each subject: the above
mentioned four restricted trials, and two non-restricted trials at both walking speeds. First,
the results of the non-restricted trials at the two levels of walking speeds were recorded in
random order. Then, the results from the four types of restricted conditions were recorded,
also in random order. Hereon, the non-restricted condition is referred to as the normal
walking condition. The restriction forces applied to the muscles were monitored online toensure that the magnitude of the restriction force applied to both legs was the same, andthat it remained stable throughout the restricted trials.
2.4. Data Processing
The first minute of the recorded gait motion of each trial was excluded from theanalysis, as it was considered as an adaptation time to the experimental conditions. Then,the position data of all markers were smoothed using a 6 Hz Butterworth filter. The timingof the gait events (HC and TO) were determined according to the ground reaction force
observed at the foot soles. Every gait cycle was determined as the gait motion occurring
between two consecutive HCs of the same leg.
The angles of the lower-limb joints in every gait cycle were calculated with the human motion analysis software SIMM; this software obtains the position of markers placedalong the body, as recorded by the motion capture system. The joint motion patterns werenormalized to a 0–100% gait cycle, and were separated into the following gait sections:loading response (first 10%), middle stance (10–30%), terminal stance (30–50%), pre-swing(50–62%), initial swing (62–75%), middle swing (75–85%), and terminal swing (85–100%)[23]. Each section of the gait cycle is shown in Figure 2. Furthermore, the joint angles in every gait section were analyzed across subjects to determine the characteristics (differences)of the restricted gait (C-restriction and CT-restriction) in comparison to the normal gait.
Several of the found characteristics occurred at the beginning or end of the mentioned gait
sections. In that case, the first or last 5% of the corresponding section, respectively, wastaken for further statistical analysis. In the section where a characteristic was identified, therespective joint angle was averaged for every subject and walking condition. The statisticalsignificance within subjects of the characteristics in comparison to the normal gait wastested using a two-tailed paired t-test and compensated with the Bonferroni method.
The Institutional Review Board of Nagoya University, Japan, approved the study
and registered it under approval Number, 14-4.

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Loading
Response

0%

Mid-Stance12%

Terminal Stance

31%

Pre-Swing Initial Swing

50%

62%

Mid-Swing75%

Terminal
Swing

87%

100%

Gait Cycle [%]Figure 2. Human gait cycle.

3. Results
3.1. Joint Compensation
The compensation action of a joint is considered as the increment in its flexion or
extension range in comparison to its normal range of motion, and works to overcome theeffects of muscle weakness. The majority of the subjects (8 out of 10 subjects) compensatedfor the joint restriction with the non-restricted or less-restricted joints. This compensation
behavior appeared to be independent of the order of the experimental trials and walking
speeds.
In the C-restriction case, the subjects compensated for the restricted ankle motion with
the non-restricted hip and/or knee joints. In the CT-restriction case, where the ankle, knee,
and hip joints were restricted, the majority of subjects compensated for the ankle joint. In
the remaining two subjects, one subject always compensated for the hip joint regardless of
the restricted muscles, and the other exhibited no compensation and a permanent lower
hip range of motion. Figure 3 shows the joint motion for the C- and CT-restrictions of theleft leg of a subject; this represents the motions seen in the majority of the subjects.
In this section, the joint motion characteristics seen in every restriction type andwalking speed will be described, along with the number of subjects that showed eachcharacteristic and the significance evaluated in every subject (as specified with p-values).
3.2. Joint Motion in C-Restriction
In the ankle joint, the majority of subjects exhibited (a) higher plantar flexion at the
beginning of the loading response phase, (b) higher dorsal flexion in the terminal stancephase, and (c) lower dorsal flexion during the swing phase (see these characteristics inFigure 3a). At the speed of 3.5 km/h, (a) seven (p < 0.01), (b) eight (p < 0.01), and (c) seven(p < 0.01) subjects presented these characteristics, respectively. Furthermore, at the speedof 4 km/h, (a) six (five with p < 0.01 and one with p < 0.05), (b) nine (p < 0.01), and (c)seven (six with p < 0.01 and one with p < 0.05) subjects showed the same characteristics.
In the knee joint, all subjects showed higher knee flexion, mainly in the (a) loading
response and (b) terminal stance phases, and (c) from the initial to middle swing phase (seeFigure 3c). At the speed of 3.5 km/h, (a) eight (six with p < 0.01 and two with p < 0.05), (b)seven (p < 0.01), and (c) seven (p < 0.01) subjects presented this characteristic, respectively.
Furthermore, at the speed of 4 km/h, (a) eight (p < 0.01), (b) seven (p < 0.01), and (c) seven(p < 0.01) subjects showed this characteristic.
In the hip joint, the subjects mainly exhibited (a) higher hip extension in the middle
stance (see Figure 3e), (b) higher hip extension in the terminal stance (see Figure 3e), (c)higher hip flexion in the initial swing and (d) higher hip flexion in middle swing. At awalking speed of 3.5 km/h, (a) four (p < 0.01), (b) six (five with p < 0.01 and one with p< 0.05), (c) five (four with p < 0.01 and one with p < 0.05), and (d) six (p < 0.01) subjects
presented these characteristics, respectively. At the speed of 4 km/h, the same trend wasobserved in (a) ten (eight with p < 0.01 and two with p < 0.05), (b) nine (p < 0.01), (c) seven(p < 0.01), and (d) eight (p < 0.01) subjects, respectively.

Appl. Sci. 2021, 11, 8344

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-

-

-

-

-

-

-

-

-

ー

ー

ー-

ー

ー

ー

Figure 3. Joint motion of a representative subject, showing the typical motion seen in the majority of the subjects.

3.3. Joint Motion in CT-Restriction
In the ankle joint, the subjects mainly presented higher dorsal flexion in the (a) terminal
stance (see Figure 3b) and (b) initial and terminal swing. At the speed of 3.5 km/h, (a) eight(p < 0.01) and (b) seven (p < 0.01) subjects presented higher dorsal flexion, respectively. At

Appl. Sci. 2021, 11, 8344

7 of 12the speed of 4 km/h, the same trend appeared in (a) ten (p < 0.01) and (b) eight (p < 0.01)
subjects, respectively. The higher dorsal flexion in the terminal stance phase was also seenin the C-restriction in the same eight subjects at the speed of 3.5 km/h and in nine subjects
at 4 km/h.
In the knee joint, seven (six with p < 0.01 and one with p < 0.05) subjects presented ahigher extended knee in the terminal swing phase (see Figure 3d) at the walking speed of
3.5 km/h, and nine (p < 0.01) subjects at the speed of 4 km/h.
In the hip joint, the majority of the subjects exhibited (a) higher hip extension at the
beginning of the pre-swing phase (see Figure 3f), (b) lower hip flexion during the initialand middle swing phases, and (c) lower hip flexion in the terminal swing phase. At thewalking speed of 3.5 km/h, (a) eight (seven with p < 0.01 and one with p < 0.05), (b) seven(p < 0.01), and (c) ten subjects (nine with p < 0.01 and one with p < 0.05) presented thesecompensations, respectively. At the walking speed of 4 km/h, these compensation motions
appeared in (a) nine (p < 0.01), (b) nine (eight with p < 0.01 and one with p < 0.05), and (c)seven (p < 0.01) subjects, respectively.
3.4. Gait Timing
The gait timing characteristics between subjects is shown in Table 1. As discussed ina previous article [18], the majority of subjects with the MARTT adapted their gait witha significantly lower single support phase. Several subjects also presented a significantly
lower step length. However, no significant change in cadence was found.
Table 1. Gait timing between subjects. Median ± IQR among subjects. The step length was normalized to the subject height. The
information in parentheses indicates the number of subjects that experienced a significant reduction in the respective gait parameter.
* p < 0.05 indicates a significant reduction in comparison with normal walking.

Parameter

Walking
Speed [km/h]

Normal Walking

C-Restriction

CT-Restriction

Cadence[steps/min]

3.5
4

102.71 ± 12.34
107.97 ± 7.70

101.37 ± 6.42
104.15 ± 7.38

100.35 ± 8.89
105.46 ± 7.79

Step Length
[m]

3.5
4

0.57 ± 0.03
0.60 ± 0.03

0.57 ± 0.05 (5∗ )0.61 ± 0.03 (3∗ )0.57 ± 0.04 (4∗ )0.60 ± 0.05 (5∗ )Single Support Phase[% stride]3.5
4

64.20 ± 5.43
66.36 ± 4.25

63.45 ± 3.14 (8∗ )63.93 ± 4.32 (8∗ )64.13 ± 3.42 (8∗ )64.55 ± 3.11 (9∗ )4. Discussion
4.1. Compensation Strategies
As a result of the muscle restriction with the MARTT, the majority of subjects exhibitedmotion compensation in the non-restricted joints. This compensation behavior agrees withthe results reported in the gait simulations of Van der Krogt [17], who studied the effects
of muscle weakness on human gait. The simulations suggested that a weakened muscle
might react by decreasing or increasing its own activity, or the activity of other muscles.
In this section, we discuss the changes in the motion patterns of each joint (as mentioned
in the results section) by comparing them with the compensation strategies reported in
the simulations of Van der Krogt, i.e., those reported as a consequence of the weakness ofcertain muscles or muscle groups.

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8 of 124.1.1. C-Restriction
In C-restriction, the mainly restricted muscles are the GAS and TA.
Effect on the ankle motion:
According to Van der Krogt’s simulations, when the TA and GAS muscles are weakened, their activity level reduces as the weakness increases. Additionally, when the GAS
and SO muscle groups are weakened, the TA muscle activity decreases. The compensation
motion observed in our study as shown in Figure 3a agrees with the decay in the TAmuscle activity during the loading response and swing phases, where, in a normal gait,
the TA muscle is known to have its most prominent activity in generating a dorsal-flexion
moment [23]. The higher plantar flexion during the loading response phase observed inour experiment suggests that the movement of the foot toward plantar flexion after HC
is not decelerated by a weak TA muscle, as it occurs in the normal gait. Thus, the ankle
reaches a higher plantar flexion than normal before a sufficient dorsal-flexion moment iscreated at the ankle that moves the tibia forward over the articular surface of the talus(known as ankle rollover). During the swing phase, we observed that the ankle exhibited alower dorsal flexion, resulting in a lower foot clearance.
The weakness of the GAS muscle was noticeable in the majority of subjects from the
mid-stance to terminal stance, when the GAS in the normal gait is most active in controllingthe dorsal flexion of the ankle before TO [23]. At the end of the rollover, we observed thatthe ankle reached a higher dorsal-flexion angle before initiating plantar flexion to prepare
for TO. This agrees with the concept of a weakened GAS muscle that could not decelerate
the dorsal flexion of the ankle as normal.
Effect on the knee motion:
An increased knee flexion from the loading response to mid-stance was observed in
the majority of subjects (see Figure 3c), that suggests a weakness in the VAS muscles. In
the normal gait, these muscles prevent knee hyperflexion in the loading response phase,and extend the knee until the middle of mid-stance [23]. Moreover, the observed higher
knee flexion in the terminal stance and initial swing suggests compensation from the BFS
muscle as reported in the simulations of Van der Krogt, i.e., as a compensation for the weak
GAS and SO muscles. The higher activity of the BFS muscle in a terminal stance could help
prevent knee hyperextension, and the higher activity in the initial swing could compensate
for the lower dorsal flexion of the ankle and ensure sufficient foot clearance.
Effect on the hip motion:
Van der Krogt’s simulations reported increased activity in the HAM muscles ascompensation for the weakness of the GAS muscle. In agreement with this compensation,
we observed a higher hip extension from the loading response to the middle of the midstance (see Figure 3e), where in normal gait the semimembranosus and semitendinosus
muscles (HAM muscles) are active to extend the hip. In addition, we observed an increased
hip extension at the end of the terminal stance phase, which suggests a weakness in thetensor fascia lata that limits the hip extension before the hip starts to flex in the pre-swing
in the normal gait. Moreover, the increased hip flexion observed in the initial swing
suggests increased activity in the ILPS muscle, also seen in Van der Krogt’s simulations, asa compensation for the GAS muscle weakness. This could be an action to compensate forthe lack of the hip flexion moment that is normally generated in pre-swing and is usually
enough to drive the hip passively during the initial swing phase [23]. As a result, the extra
hip flexion would support the above-mentioned compensation of the knee, and contributeto the foot clearance.
Summary of C-restriction: When the muscles at the calf area were restricted (Crestriction), the weakness of the ankle in reaching the normal dorsal flexion angle during
the swing phase was compensated for by a higher knee and hip flexion, showing a priority in compensating for foot drop. The knee also compensated to protect itself fromhyperextension in the terminal stance phase. The hip compensated for itself during theinitial swing phase by flexing more to create the necessary moment, normally generated in
the terminal stance phase, to advance the leg forward. The hip also compensated for theAppl. Sci. 2021, 11, 8344

9 of 12hyperflexion of the knee in the loading response phase by extending more. In this muscle
restriction condition, the weakness of the joint was always compensated for within the
kinematic chain, either by the joint itself or by others.
4.1.2. CT-Restriction
For the following discussion, it is important to consider that the CT-restriction restricts
the RF, HAM, and VAS muscles in addition to muscles restricted by the C-restriction.
Effect on the ankle motion:
We observed an increased ankle dorsal flexion during the swing phase (see Figure 3b),which suggests an increased activity of the TA muscle, that is a compensation for the
restricted HAM muscles in Van der Krogt’s simulations. This action might serve to safely
clear the ground, as the knee and hip may not be able to compensate with a higher flexion
as they did in C-restriction. The higher ankle dorsal flexion observed in the terminal stancesuggests a weak GAS muscle, as also seen in the C-restriction, but in this case, the flexion ishigher. The weak GAS is one of the reported effects from restricting the RF muscle in Van
der Krogt’s simulations.
Effect on the knee motion:
We observed a higher knee extension in the terminal swing phase (see Figure 3d).
This might be caused by the decreased activity in the HAM muscles and/or increased
activity in the VAS muscles, as reported by Van der Krogt during the swing phase when
the VAS muscles are weakened. During the swing phase in the normal gait, the HAM
muscles modulate the rate of knee extension, and the VAS muscles act to ensure a complete
extension, so as to prepare for the abrupt weight transfer at HC. Weak HAM muscles would
fail to regulate the knee extension, and a higher activated VAS would produce a higher
knee extension, and compensate for the lower hip flexion that we observed in the majorityof subjects at terminal swing (section below). This would otherwise significantly reduce
the step length.
Effect on the hip motion:
We observed a lower hip flexion at pre-swing (see Figure 3f), suggesting weakness
in the RF and gracilis (GRA) muscles. These contribute to flexing the hip, to prepare forthe swing phase in the normal gait. This partially agrees with Van der Krogt’s results, asin that study, a higher activity in the RF muscle during pre-swing and a lower activity in
the GRA muscles along the gait cycle were reported as effects of the RF muscle restriction.
The observed reduced hip flexion during the initial and middle swing phases also suggests
lower activity in the GRA muscle, which normally supports the flexion at this time. This
would mean that the hip cannot compensate to clear the ground, as it did in C-restriction.
However, as mentioned in the compensations for the ankle, the TA muscle compensates
to clear the ground. The observed higher extended hip in the terminal swing phase is theresult of the previously mentioned lack of the flexion action of the GRA muscle. As a resultof the weak hip flexion during the swing phase, the step length would be shorter thannormal.
By comparing the compensation actions manifested in the C- and CT-restrictions,
we see a more dynamic compensation activity in C-restriction; this is because the ankle,
knee, and hip joints (kinematic chain) are able to compensate for each other, and in somecases even themselves. One of the reasons for this is the severity of the restriction. As
the knee and hip joints are minimally affected in C-restriction, they can supply what theoverall kinematic chain needs. However, in CT-restriction, the muscle restriction affects thecomplete kinematic chain; therefore, the body has to prioritize what to compensate. We
found that the prioritization includes the prevention of foot drop, knee hyperextension
in the terminal stance phase, and knee hyperflexion in the loading response phase, as
well as the preservation of the step length. This suggests that the priority is to adapt the
gait patterns for safe walking, as also seen in the elderly [24]. Moreover, the evaluationof the significance of every joint motion characteristic in every subject showed that thesignificance increased at a faster walking speed of 4 km/h in both C- and CT-restriction.

Appl. Sci. 2021, 11, 8344

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Summary of CT-restriction: When the muscles at the calf and thigh area were restricted (CT-restriction), the ankle compensated for itself during the swing phase with ahigher dorsal flexion, thereby preventing foot drop. The knee and hip were not able to aid
in this task as they did in C-restriction. The hip did not reach the normal flexion range during the swing phase, which reduced the step length. However, some subjects compensatedfor the higher extended knee in the terminal swing phase to keep the step length. In thismuscle restriction condition, the active compensation chain of the C-restriction was notseen. However, the subjects’ gait motion appeared to always prioritize safe ambulation, as
also seen in the elderly.
4.2. Joint Motion Compensation and Weakness: Similarities and Differences with the Elderly
The resultant joint motion of the young adults with the MARTT in C-restriction
agreed with several compensation motions and weaknesses seen in the healthy elderly. For
instance, the young adults presented a lower ankle plantar flexion in the terminal stance atthe time of push-off, as seen in the elderly [11,25]. In addition, a lower dorsal flexion of
the ankle during the swing phase was seen in the young adults, which is also commonly
known in the elderly as foot drop [26].
Öberg et al. [27] reported the following joint motion changes with aging: increment ofknee flexion in the middle stance phase, reduction of knee flexion in the swing phase, andan increment in the hip flexion in the mid-swing phase. In agreement, the young adults
with C-restriction showed these motion changes, except for the lower knee flexion during
the swing phase. However, the higher knee flexion during the swing phase (as seen inthese young adults) has also been found in other studies of the elderly [26,28] as a safetymeasure to compensate for foot drop.
4.3. Limitations
The subject sample that participated in this study is relatively small, and it is possiblethat there exist other compensation patterns not seen in our analysis. Thus, it is necessary
to observe the compensation motions in a much larger subject sample to investigate theuniversal trend of compensation strategies. Furthermore, a muscle activity analysis is
missing to validate what has been discussed in this study regarding which muscles areactive or weak, at the moment the observed compensation strategies occur.
To investigate the relationship between the restriction of certain muscle groups andcompensation motions, we used MARTT to cause the muscle restriction artificially. However, the congruence between the compensation motions that result from this artificial
restriction and the ones that result from natural muscle weakness have to be further
analyzed and validated.
5. Conclusions
The compensation strategies in human gait appearing under restrictions of the lowerlimb muscles were observed and analyzed in this study. The muscle restriction wasachieved using the MARTT, which includes wearable belts for restricting lower-limb
muscles. The gait motion was investigated under various conditions of walking speed andmuscle restrictions.
The compensation behavior did not appear to be dependent on the walking speed, but
the significance of the compensation as evaluated among the subjects increased with the
speed. The joint motion weaknesses and compensations seen in the C-restriction agreed
with those seen in the elderly, suggesting that human compensation behaviors againstmuscle weakness have similar purposes, regardless of age. The results of this study provide
an essential inspection for understanding the mechanisms of gait compensation against
limitations of gait ability.
Author Contributions: Conceptualization, Y.Y., Y.A., S.O. and J.B.U.; methodology, Y.A., S.O. and
J.B.U.; software, Y.A. and J.B.U.; validation, Y.A., S.O. and Y.Y.; formal analysis, J.B.U., Y.A. and
S.O.; investigation, J.B.U., Y.A. and S.O.; resources, Y.Y.; data curation, J.B.U.; writing—original draft

Appl. Sci. 2021, 11, 8344

11 of 12preparation, J.B.U., Y.A.; writing—review and editing, Y.A., J.B.U.; visualization, J.B.U.; supervision,
Y.A., S.O., Y.Y.; project administration, Y.Y.; funding acquisition, Y.Y. All authors have read and agreed
to the published version of the manuscript.
Funding: This research was funded by JSPS KAKENHI grant number 26750121.
Institutional Review Board Statement: The study was conducted according to the guidelines of the
Declaration of Helsinki, and approved by the Institutional Review Board of Nagoya University, Japan(approval number 14-4 and date of approval).
Informed Consent Statement: Written informed consent was obtained from all subjects involved in
the study.
Data Availability Statement: The subjects’ joint angles in every gait section analyzed in this study
are compiled and available in the submitted supplementary material; as well as, the statistical analysisof the relevance of the found compensatory motions.
Conflicts of Interest: The authors declare no conflicts of interest. The funders had no role in thedesign of the study; in the collection, analysis, or interpretation of data; in the writing of themanuscript, or in the decision to publish the results.

Abbreviations
The following abbreviations are used in this manuscript:
RF
VAS
BFS
GAS
SO
TA
HAM
ILPS
MARTT
MTC
HC
TO
C-restriction
CT-restriction

rectus femoris
vastiibiceps femoris short headgastrocnemius
soleustibialis anterior
hamstringiliopsoas
Muscle Activity Restriction Taping Techniqueminimum toe clearance
heel contact
toe off
calf restriction
calf and thigh restriction

References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.

Hollmann, W.; Strüder, H.; Tagarakis, C.; King, G. Physical activity and the elderly. Eur. J. Cardiovasc. Prev. Rehabil. 2007, 14,
730–739.
Lamoureux, E.L.; Sparrow, W.A.; Murphy, A.; Newton, R.U. Differences in the neuromuscular capacity and lean muscle tissue inold and older community-dwelling adults. J. Gerontol. A. Biol. Sci. Med. Sci. 2001, 56, M381–M385.
Frontera, W.R.; Hughes, V.A.; Fielding, R.A.; Fiatarone, M.A.; Evans, W.J; Roubenoff, R. Aging of skeletal muscle: A 12-year
longitudinal study. J. Appl. Physiol. 2000, 88, 1321–1326.
Hayashida, I.; Tanimoto, Y.; Takahashi, Y.; Kusabiraki, T.; Tamaki, J. Correlation between muscle strength and muscle mass, andtheir association with walking speed, in community-dwelling elderly Japanese individuals. PLoS ONE 2014, 9, e111810.
McCormick, R.; Vasilaki, A. Age-related changes in skeletal muscle: changes to life-style as a therapy. Biogerontology 2018, 19,
519–536.
Akima, H.; Kano, Y.; Enomoto, Y.; Ishizu, M.; Okada, M.; Oishi, Y.; Katsuta, S; Kuno, S. Muscle function in 164 men and women
aged 20–84 year. Med. Sci. Sports Exerc. 2001, 33, 220–226.
Janssen, I.; Heymsfield, S.B.; Wang, Z.M.; Ross, R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 year.
J. Appl. Physiol. 2000, 89, 81–88.
Ikezoe, T.; Mori, N.; Nakamura, M.; Ichihashi, N. Age-related muscle atrophy in the lower extremities and daily physical activity
in elderly women. Arch. Gerontol. Geriatr. 2011, 53, 153–157.
Kirkwood, R.N.; Trede, R.G.; Moreira, B.; Kirkwood, S.A.; Pereira, L.S. Decreased gastrocnemius temporal muscle activation
during gait in elderly women with history of recurrent falls. Gait Posture 2011, 34, 60–64.
Schmitz, A.; Silder, A.; Heiderscheit, B.; Mahoney, J; Thelen, D. Differences in lower-extremity muscular activation during walking
between healthy older and young adults. J. Electromyogr. Kinesiol. 2009, 19, 1085–1091.

Appl. Sci. 2021, 11, 8344

11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.

12 of 12Begg, R.K; Sparrow, W.A. Ageing effects on knee and ankle joint angles at key events and phases of the gait cycle. J. Med. Eng.
Technol. 2006, 30, 382–389.
Aniansson, A.; Grimby, G.; Hedberg, M. Compensatory muscle fiber hypertrophy in elderly men. J. Appl. Physiol. 1992, 73,
812–816.
Stewart, J.D. Foot drop: Where, why and what to do? Pract. Neurol. 2008, 8, 158–169.
Pirker, W.; Katzenschlager, R. Gait disorders in adults and the elderly: A clinical guide Wien Klin. Wochenschr. 2017, 129, 81–95.
DeVita, P.; Hortobagyi, T. Age causes a redistribution of joint torques and powers during gait. J. Appl. Physiol. 2000, 88, 1804–1811.
Mill, P.; Barret, R.S. Swing phase mechanics of healthy young and elderly men. Hum. Mov. Sci. 2001, 20, 427–446.
Van der Krogt, M.M.; Delp, S.L.; Schwartz, M.H. How robust is human gait to muscle weakness? Gait Posture 2012, 36, 113–119.
Ullauri, J.B.; Akiyama, Y.; Okamoto, S.; Yamada, Y. Technique to reduce the minimum toe clearance of young adults during
walking to simulate the risk of tripping of the elderly. PLoS ONE 2019, 14, e0217336.
Abe, T.; Kearns, C.; Sato, Y. Muscle size and strength are increased following walk training with restricted venous blood flowfrom the leg muscle, Kaatsu-walk training. J. Appl. Physiol. 2006, 100, 1460–1466.
Abe, T.; Sakamaki, M.; Fujita, S.; Ozaki, H.; Sugaya, M.; Sato, Y. Effects of low-intensity walk training with restricted leg bloodflow on muscle strength and aerobic capacity in older adults. J. Geriatr. Phys. Ther. 2010, 33, 34–40.
Karst, G.M.; Hageman, P.A.; Jones, T.F.; Bunner, S.H. Reliability of foot trajectory measures within and between testing sessions. J.
Gerontol. 1999, 54, 343–347.
Hamacher, D.; Hamacher, D.; Schega, L. Towards the importance of minimum toe clearance in level ground walking in a healthyelderly population. Gait Posture 2014, 40, 727–729.
Perry, J.; Burnfield, J.M. Gait Analysis: Normal and Pathological Function, 2nd ed.; Slack Inc.: Thorofare, NJ , USA, 2010; pp. 53–119.
Winter, D.A.; Patla, A.E.; Frank, J.S; Walt, S.E. Biomechanical walking pattern changes in the fit and healthy elderly. Phys. Ther.
1990, 70, 340–347.
Kerrigan, D.C.; Todd, M.K.; Della Croce, U.; Lipsitz, L.A.; Collins, J.J. Biomechanical gait alterations independent of speed in thehealthy elderly: evidence for specific limiting impairments. Arch. Phys. Med. Rehabil. 1998, 79, 317–322.
Mills, P.; Barrett, R.; Morrison, S. Toe clearance variability during walking in young and elderly men. Gait Posture 2008, 28,
101–107.
Oberg, T.; Karsznia, A.; Oberg, K. Joint angle parameters in gait: reference data for natural subjects, 10–79 of age. J. Rehabil. Res.
Dev. 1994, 31, 199–213.
Prince, F.; Corriveau, H.; Hebert, R; Winter, D.A. Gait in the elderly. Gait Posture 1997, 5, 128–135.