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Robotics and Autonomous Systems

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A proprioceptive neuromuscular facilitation integrated roboticanklefoot system for post stroke rehabilitationZhihao Zhou a, Yuan Zhou b, Ninghua Wang b, Fan Gao c, Kunlin Wei d, Qining Wang a,a The Robotics Research Group, College of Engineering, Peking University, Beijing 100871, Chinab Department of Rehabilitation Medicine, First Hospital, Peking University, Beijing 100034, Chinac Department of Health Care Sciences, University of Texas Southwestern Medical Center, Dallas, USAd Department of Psychology, Peking University, Beijing 100871, China

h i g h l i g h t s

We developed a proprioceptive neuromuscular facilitation (PNF) integrated robotic anklefoot system for post stroke rehabilitation. It is the first time that PNF method has been used in ankle spasticity/contracture rehabilitation. Five able-bodied subjects participated in the experiments and five stroke patients were recruited with a six-week PNF treatment. The proposed system can offer more effective treatment than passive stretching in improvement of both passive and active joint properties.

a r t i c l e i n f o

Article history:Available online xxxx

Keywords:Proprioceptive neuromuscular facilitationRobotic anklefoot systemAnkle rehabilitationSpasticity/contractureStroke

a b s t r a c t

Ankle joint with spasticity and/or contracture can severely disable the mobility and the independence ofstroke survivors. In this paper, we developed a proprioceptive neuromuscular facilitation (PNF) integratedrobotic anklefoot system for post stroke rehabilitation. The system consists of a robotic platform and acontrol system with graphic user interface. We employ five normal subjects to test the reliability andfeasibility of the proposed system. To validate the effectiveness of the PNF integrated robotic system, werecruit five stroke patients and carry out a six-week PNF treatment. Treatment outcome was evaluatedquantitatively in passive and active joint properties. The passive hysteresis loop shows that themaximumdorsiflexion angle increases from 32.9 1.5 to 42.0 3.2 (p = 0.014) while the resistance torquedecreases from 45.6 Nm 5.8 N m to 29.8 N m 4.4 N m (p = 0.019). The active joint properties areimproved significantly with the training score increasing from 5.7 0.9 to 8.1 0.6, and getting closeto that of normal subjects (9.5 0.3). In addition, muscle strength has a rising trend as time goes on. Theresults demonstrate that the proposed PNF integrated robotic anklefoot rehabilitation system is effectivein improving ankle spasticity and/or contracture and is a promising solution in clinical rehabilitation.

2014 Elsevier B.V. All rights reserved.

1. Introduction

Human ankle joint as a very flexible and complex skeletal struc-ture plays an important role in providing forward propulsion forceduring terminal stance phase and maintaining body balance andsmooth gait during the whole gait cycle [1]. Cerebrovascular ac-cident (CVA), or stroke, is one of the leading causes of ankle dis-ability [2,3]. For those patients, the ankle joint with spasticityand/or contracture can severely disable the mobility and the in-dependence of stroke survivors [48]. The spasticity is resulted

Corresponding author. Tel.: +86 10 6276 9138; fax: +86 10 6276 9138.E-mail address: qiningwang@pku.edu.cn (Q. Wang).

from the hypertonus and reflex hyperactivity of skeleton muscles[9,10]. Such spasticity in flexormuscles of stroke patients is amorecommon syndrome than extensor muscles. It reduces the range ofmotion (ROM) of ankle joint and may cause severe physical pain.Moreover, lack of mobilization and prolonged spasticity may fur-ther change the structure of muscle fibers and connective tissuesand finally lead to permanent contracture as a result. About 34%of stroke survivors have developed ankle contracture [8,11,12].Therefore, one of the greatest challenges in stroke survivors re-habilitation is to improve their ankle spasticity and/or contracture,which can seriously influence its normal functional activities.

In clinic, the ankle joint with spasticity and/or contractureis generally rehabilitated via physiotherapy [1315]. During thetreatment, patients ankle is manually moved within its ROM by

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2 Z. Zhou et al. / Robotics and Autonomous Systems ( )

a physical therapist. Physical rehabilitation is in need of a long-termcontinuous operation as short-term treatment is less effectiveand usually insufficient to make patients fully recuperation [16].Even if the patients have temporarily recovered from short-termtreatment, they tend to relapse and have future problems [13,17].In addition, for some severe patients, their ankle joints have a veryhigh stiffness and can hardly be stretched by therapists, even withstrong arms. Above all, manual stretching is very time-consuming,strenuous and laborious to physical therapists. Therefore, manualrehabilitation may not last long, partly due to the limitation ofstretching frequency and duration time.

In view of shortcomings of physiotherapy, a robotic an-klefoot rehabilitation system has been proposed to supportphysicians in providing a high-intensity therapy for the strokepatients [18]. Robotic technology can transform rehabilitationfrom labor-intensive operations to robot-assisted operations,which can implement different kinds of rehabilitation meth-ods [19]. The robotic system can offer an adequate stretching forceand sustaining long-term training, which can cover the limita-tion of manual stretching [20]. It can also record rich information,such as velocity, ROM, joint torque, electromyography (EMG) sig-nals. Those useful signals can facilitate patient diagnosis, functionalassessment, therapy customization and rehabilitation historyrecording. Thus, robotic rehabilitation is gradually being thoughtto be as good as or even better thanmanual therapy [21]. There aremainly two kinds of robotic anklefoot rehabilitation systems [20]:one kind is mobile systems, e.g. [2224], mainly focusing on im-proving walking gait and the other one is platform-based systemsaiming at improvement of ankle performance. For ankle joint withspasticity/contracture induced by the hypertonus and reflex hy-peractivity of flexor muscles, the primary work is to alleviate thespasticity of crus muscle [5,6]. Before walking rehabilitation usingwearable systems, patients with ankle joint spasticity/contracture,especially those severe patients, have to use a platform-based sys-tem to ensure reliability and improve current performance.

Recently, several research groups have developed differentrobotic platform-based anklefoot rehabilitation devices [2533].Continuous passive motion (CPM) is mainly applied in those de-vices. It has been confirmed in their studies that passive stretch-ing is effective in treating the ankle joint with spasticity and/orcontracture. CPM devices can provide regular and consistent pas-sive stretching. The ankle joint is moved between two predefinedpositions which usually not cover the whole ankle ROM. There-fore, calf muscle may not be fully stretched into the extreme po-sition of dorsiflexion where the spasticity and/or contracture issignificant. In addition, most of the ankle CPM devices run at a setvelocity and do not provide motions with velocity change duringone reciprocation. Different from those devices, Zhang et al. hasdeveloped an intelligent stretching device for the patients withcontracture/spasticity and the stretching velocity is inversely pro-portional to the joint resistance torque [2527]. However, duringpassive stretching since lower limb is totally relaxed, the improve-ment of muscle strength and coordination are limited and patientscanhardly get functional recovery. In addition, passive stretching isonly a kind of mechanically reciprocating motion without involv-ing patients active participation, which makes their acceptanceand initiative not high.

To address these problems, we choose an active rehabilitationmethod, namely proprioceptive neuromuscular facilitation (PNF)technique. Different from the passive stretching, here the activemethod is specified from the subject point of view, which meansthe active participation of the patient. Common PNF stretchinginvolves a shortening contraction of the opposing muscle to placethe target muscle on stretch. It was firstly proposed by Kabat andKnott for the rehabilitation of polio patients with paralysis [34].Klein et al. reported that PNF treatment in elderly will significantly

improve flexibility, ROM, muscle strength and ADL function [35].The PNF is even found effective to increase muscle volume andalter muscle fiber types [36]. Thus, PNF is widely used for physicaltherapist and athletic trainers [37]. Above all, PNF technique cancover the problems in the previous treatment and ismore effectivethan passive stretching [38]. Moreover, the active participation inPNF treatment can improve their compliance and initiative.

In this paper, we develop a PNF integrated robotic anklefootsystem for ankle joint with spasticity/contracture of post strokerehabilitation. The robotic system can provide the required mo-tion of plantar flexion and dorsiflexion, and has nine degrees offreedom (DOFs) to conveniently adjust the position of footplate forthe sake of avoiding misalignment between biological ankle axisand robotic system axis [39]. A graphic user interface (GUI) de-veloped in the Labview environment is customized friendly andconcisely for both patients and operators. Moreover, in consid-eration of the safety in humanmachine interaction (HMI) [40],protection on control system andGUI,mechanical limits and emer-gency switches are all designed in the proposed system. Five poststroke patients participate in our pilot experiment and accept acourse of six-week PNF rehabilitation treatment using the roboticanklefoot system. Experimental results including changes of bothpassive and active properties of ankle joint after training show theimprovement of spasticity and/or contracture.

This paper is organized as follows. Section 2 presents the detailsof the robotic anklefoot rehabilitation system. PNF technique,experiment protocol and evaluation methods are illustratedin Section 3. Performance of the proposed robotic anklefootrehabilitation system and results of PNF rehabilitation for five poststroke patients are shown in Section 4. Finally, wemake discussionin Section 5 and conclude in Section 6.

2. Robotic anklefoot system

This section presents themain technical solutions of the roboticanklefoot system (see Fig. 1) which is functionally divided intotwo parts: GUI (top layer) and hardware (bottom layer). Threesubsystems are implemented on the platform and describedhereafter. They contains the mechanical design, the sensory andcontrol system, and the graphical user interface. Safety of patientsfor the rehabilitation devices is placed at the first place. Once thedanger happens, it would cause a destructive injury to patients.Therefore, protection on control system and GUI, mechanical stopsand emergency switches are redundantly designed to ensure theabsolute safety of patient in our system.

2.1. Mechanical design

The proposed robotic anklefoot rehabilitation system consistsof an immobile base that contains a comfortable seat, a motorsuite (dunkermotoren Inc.), an adjustable sliding platform in threedegrees of freedom which is used to move the motor bracket toan appropriate position, an adjustable leg support and a controlcabinet (see Fig. 2). The motor and the footplate are fixed on thesliding platform. The leg support can be adjusted in four degreesof freedom and the leg was strapped to the leg support by theleg belt. The adjustable sliding platform and leg support togetherensure that ankle axis is aligned with the motor shaft while kneeis flexed at a fixed degree for each training. They are all lockedby the lock plungers after being adjusted to the desired position.Since the rehabilitation technique that we are adopted is a kind ofactive method which need the patient to perform his maximumforce during the treatment, the hardware structure must havehigh mechanical strength and stiffness to make the patient andguarantee the device to be at a relative standstill. Therefore the

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Fig. 1. The overall structure of the proposed robotic anklefoot rehabilitation system. The top layer is the GUI and the bottom layer is the hardware.

Fig. 2. The proposed robotic anklefoot rehabilitation system. It consists of the immobile base, the sliding platform, the leg support, the control and power supply cabinetand the sensory system including the inclinometer and the EMG acquisition system. The sliding platform has three DOFs of translation along x, y and z. The leg support hasfour DOFs of translation along x, y and z and rotation along y.

mechanical structure of the device will be more difficult andcomplex than CPM devices.

As shown in Fig. 3, the motor is fixed on the motor bracketand the footplate is fixed on the motor shaft through the sideplate. Themotor suite consists of a DCmotor and an inline gearboxwith a 250:1 gear ratio which increases the loading capacity of themotor up to 100 N m. It also has an inline rotation encoder forspeed-closed control. Considering interaction between human andmachine, the safety of the robotic platform is quite important. Inthis study, rotation limits of the footplate are set both in the motordrive and control module. The system will stop running if theobliquity of the footplate is out of the prescribed range. In addition,a mechanical limit stop is set to constrain the range of motion.The motor bracket with location holes on the perimeter is usedto place the mechanical limit stops in our system. The separationangle of two adjacent location holes is 5. Two stop pins on themotor bracket are used for limiting the rotation range of the swingpin, which is fixed on themotor shaft. Besides, the operator and thepatient all have their own handhold emergency switch and eitherof them could shut down the motor by pressing their own switch.

The footplate can move along the side plate to ensure thatthe rotating axis of footplate is aligned with biological ankle axis

(see Fig. 3). The two DOFs can satisfy the foot size for differentpatient. In experimental protocol, we firstly measure the heightof foot (distance from the bottom of foot to the lateral malleolus)which is represented by D0 and the length of foot (distance fromthe heel of foot to the lateralmalleolus)which is represented byD1.Before the ankle is placed on the footplate, we adjust the footplateposition depending on D0 and D1 to avoid the misalignment in theprocess of rotation. Then the foot is secured on the footplate byvelcro at the dorsal foot and the heel.

2.2. Control system

To obtain as much useful information as possible, placementpositions of sensors used in the system are carefully determined(see Figs. 1 and 2). One uni-axial torque sensor (TransducerTechniques, Inc.) ismounted on the shaft tomeasure the resistancetorque. An inclinometer is attached to the underneath of footplatewhich can record the joint angle with the reference to the ground.It is self-designed and its output range is 90. Two-channelsEMG system (Delsys Inc.) is used to measure EMG signals ofgastrocnemius muscle and soleus muscle. In addition, an inline

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Fig. 3. Schematic diagram of the motor suite and the footplate. The footplate hastwo DOFs of translation along x and z which is adjusted according to D0 and D1 .

rotation encoder can calculate rotational speed of footplate. Allof those signals are fed into the Labview program through a USBdata acquisition (DAQ) card (NI Inc.) with the sampling rate at1 kHz. Thereinto, the resistance torque and the joint angle aresimply processed through a second order Butterworth low-passfilter with a cut-off frequency of 20 Hz. The raw EMG signals arefirstly bandpass filtered through a fourth order Butterworth filterwith a cutoff frequency of 20 and 450 Hz, then full-wave rectified,and low-pass filtered through another fourth order Butterworthfilter with a cutoff frequency of 5 Hz. Then it is filtered by movingaverage with a window length of two hundred sample points. Theprocessed EMG signals also need to subtracts the measured offsetwhen the muscles are relaxed. The relationship between torqueand EMG signals of gastrocnemius and soleus is shown in Fig. 4. Thecorrelation coefficient between torque and EMG of gastrocnemiusis 0.4392 while the correlation coefficient between torque andEMG of soleus is 0.9576. The gastrocnemius muscle runs from itstwo heads above the knee to the heel, so we choose soleus muscleas feedback in our treatment also due to its high correlation. It candemonstrate that the filter method can make soleus EMG signalbeing accurately in correspondence with joint torque.

The proposed robotic anklefoot rehabilitation system ismodeled as a double pendulum using NewtonEuler formulation.The combined dynamics of robotic system and human subject isgiven by

Js (t) + Bs (t) + Ks(t) = Tm(t) + Tgrav(t) + Tank(t) (1)

where Js, Bs and Ks are the inertia, damping and stiffness of thesystem which are estimated according to the motor specificationand themechanicalmodel in the Solidworks Software. (t)was thejoint flexion angle. Tm(t), Tgrav(t) and Tank(t) are the motor outputtorque, gravitational torque and ankle joint torque, respectively.

The joint torque when the muscles are relaxed can be obtainedby

Tank(t) = Tres(t) = Ja (t) + Ba (t) + Ka(t) (2)

where Ja, Ba and Ka are joint stiffness, viscous damping and footinertia of ankle. And the joint torque when the muscles arecontracted can be obtained by

Tank(t) = Tmuscle(t). (3)

The system is driven by a DC motor controlled by a customizeddriver. As shown in Fig. 5, the control strategy implements a doubleclosed-loop system with the current control as the inner-loop andthe speed control or position control as the outer-loop which isswitched based on motor status.

The velocity is controlled in such a way that it was inverselyproportional to the resistance torque [27]. Thus, when the positionof the ankle joint gets closed to the extreme position of ROM, theincreasing resistance slows down the motor gradually and at thesame time the muscletendons involved are stretched slowly andsafely. In the middle of ROM where the resistance is usually low,the motor stretches the slack muscles at higher speed. Certainly, ifthe resistance is high in the middle, the movement would also beslowed down accordingly. Specifically, d and p are the extremeposition of the joint ROM in ankle dorsiflexion and plantar flexion,respectively (both are positive numbers). Tp is a specified peakresistance torque when the motor reaches the mechanical stops.If Tres(t) is beyond the Tp, the system will shut down immediatelyas a kind of self-protection. It can serve as a safe value to protect thepatient and the system. vmin and vmax (two positive numbers) arethe minimum and maximum speeds (for stretching in the middleof ROM) which are predetermined, respectively. C1 and C2 aretwo constants and are empirically selected according to the rangeof velocity and resistance torque. C2 scales the 1/Tres(t) to theappropriate stretching velocity.

When the position (t) is in the middle of ROM, the motorvelocity v(t) is calculated by

v(t) =

vmin vt 6 vmin

C1 +C2

|T (t)|vmin < vt < vmax

vmax vt > vmax

(4)

where vmin and vmax (two positive numbers) are the minimumandmaximum speeds (for stretching in the middle of ROM) whichare predetermined, respectively. C1 and C2 are two constantsand are empirically selected according to the range of velocityand resistance torque. C2 scales the 1/Tres(t) to the appropriate

Fig. 4. Relationship between torque and EMG signals of gastrocnemius (Gas) and soleus (Sol). All of them were filtered.

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Fig. 5. Control flow diagram of the ankle rehabilitation system.

Fig. 6. The main interface (or homepage) of the customized graphical user interface developed in the Labview environment.

stretching velocity. In our system, C1 and C2 are 7.5 and 0.05respectively.

When the position (t) reaches the end of ROM, namely d orp, the motor velocity v(t) is zero. The motor driver implementsa position close-loop by PID controller and current closed-loopserves as the inner-loop.

2.3. Graphical user interface

A customized GUI is developed in Labview environment forthe robotic anklefoot rehabilitation system. All interfaces areconcise and friendly so that the patients can easily understand.They are also convenient to operate by the therapist. As shownin Fig. 6, it is the main interface (or called homepage) of ourGUI, where we can operate patients database and enter into eachtraining interface according to the rehabilitation protocol. Someindividual information like name, age and height needs to inputwhen adding a new patient. Also we can choose a previous patientfrom patients database and set wanted paths of saving data.According to the rehabilitation protocol in the homepage, we canenter into corresponding sub interfaces in sequence.

PNF stretching as the key interface during treatment is shownin Fig. 7. Two windows display to the operator and the patient,like Fig. 7(a) and (b). ROM of dorsiflexion and maximum voluntarycontraction (MVC) of EMG have been recorded in the step of ROMMeasurement and MVC Measurement, which are the defaultvalue in PNF stretching. Total trials number, hold time, relax timeand target need to set by the operator. Those parameters all canbe updated when the software is running. The patient is asked to

perform isometric contraction with the soleus muscle activatedand maintains the soleus EMG in the target percentage range ofMVC for seconds (Hold time). A countdown clock is used to displaythe remaining time of relax time and hold time. And each trialwill have a training score to the patient which will be explainedin Section 3.

3. Method

3.1. Proprioceptive neuromuscular facilitation (PNF)

PNF stretching is commonly used in clinical environments toenhance both active and passive ROM with the ultimate goalbeing to optimize motor performance and rehabilitation. Propri-oception means sense of self. In human limbs, the propriocep-tor provides information about joint angles, muscle length, andmuscle tension, which give information about the position of thelimb in space. The Golgi tendon organs (GTO) serves as one kind ofproprioceptive sensory receptor organs in our body. It can provideinformation about changes in muscle tension. One end of GTO isconnected to the muscle fibers and the other end merges into thetendon bundles.When the central nervous system sends amessageto the agonist muscle to contract, (here the agonist muscles aregastrocnemius and soleus muscle), these target muscles developactive force. Due to the applied force, GTO gets compressed, andtriggers Golgi tendon reflex (GT reflex), which can relax andlengthen the target muscle (here the target muscles are also gas-trocnemius and soleus muscle). So the patient actively contractshis gastrocnemius and soleus muscle, meanwhile makes these

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(a) Interface for operators.

(b) Interface for patients1. (c) Interface for patients2.

Fig. 7. Sub interface: PNF stretching. (a) is the interface for operator. (b) is the interface for patients when patients relax muscles in neural position and (c) is the one whenpatients contract muscles to step the footplate.

(a) Direct hold-relax PNF.

(b) Indirect hold-relax PNF.

Fig. 8. Principles of two kind of PNF methods. Direct hold-relax PNF and indirect hold-relax PNF are shown in subfigure (a) and (b), respectively.

muscles get further relaxed. The repetition of this process facili-tates the patient to further contract and relax his ankle joint. Sincethe targetmuscle is also the agonist, this technique is usually calleddirect hold-relax PNF [41,42] (see Fig. 8(a)).

On the other hand, there is an indirect hold-relax PNF tech-nique (see Fig. 8(b)). In human body, there exists a neural phe-nomenon called reciprocal inhibition. When the agonist muscle(muscle causing movement) starts to contract, the tension in theantagonist muscle (muscle opposing movement) is inhibited byimpulses frommotor neurons, and thusmust simultaneously relax.With reciprocal inhibition as one muscle contracts, the opposing(antagonist) muscle will relax and allow more movement aroundthe joint. In this case the target muscle is the opposingmuscle (an-tagonist) and this technique is called indirect hold-reflex PNF.

In this study, we currently only adopt the direct hold-relax PNFtechnique in our system. We can intuitively discover that directhold-relax PNF is more easy to take in than indirect hold-relax PNFbecause it can directly improve the lost or deficient dorsiflexion

motion. But considering hypertonus of backmuscle due to spastic-ity and/or contracture, the patient is very hard to actively dorsiflex-ion according to indirect hold-reflex PNF. Therefore indirect PNF ismore suitable for their primary rehabilitation. When spasticity hasbeen largely alleviated, indirect hold-relax PNF maybe be needed.

3.2. Subjects and experiment protocol

Five chronic stroke patients with ankle spasticity and/orcontracture (Ashworth scale >1 around ankle joint) participatedin the study. Detail information was shown in Table 1. The strokesubjects age was 65.6 9.0 years, height was 170.4 11.0 cmand weight was 71.0 12.6 kg. Two of them were left impairedside and others were right. Their first stroke occurred 42.8 13.3months ago. All the stroke patients were able to walk in anabnormal gait without any mechanical aid, and able to generateplantar flexion using the calf muscles. They were all from theDepartment of Rehabilitation Medicine, First Hospital, Peking

Z. Zhou et al. / Robotics and Autonomous Systems ( ) 7

Table 1Subject data.

Patient no. Age (year) Gender (M/F) Height (cm) Weight (kg) Impaired side (L/R) Injury duration (Month)

1 77 M 156 51 L 502 65 M 170 85 L 593 72 M 165 69 R 264 58 M 185 76 R 465 56 M 176 74 R 33Mean Std 65.6 9.0 / 170.4 11.0 71.0 12.6 / 42.8 13.3

University and they gave written and informed consent beforethe experiment. All procedures were approved by the institutionalreview board of the First Hospital, Peking University. The trainingwas carried out 3 times a week and lasted for 6 weeks. In addition,we also recruited five normal subjects to check the system beforepatients experiments. Their age was 27.2 1.8 years, height was165.6 8.7 cm and weight was 65.8 9.9 kg, and two of themwere female. Test data of both sides were measured. The purposeof those normal subjects was to evaluation the feasibility of theoverall system.

The experiment protocol mainly involved three steps, namelypreparation, initialization and stretching:

3.2.1. Step I: preparationD0 and D1 of the subjects foot were measured in order to prop-

erly adjust the position of the device. It could ensure that the an-kle joint was able to align with the axis of the motor shaft. Thesubject seated comfortably with knee flexed at 30which was de-termined after multiple comparison. The lower leg was strappedto the leg support and the foot was attached to the footplate. Theskin was cleaned and conditioned with warmwater before attach-ing the electrode pads. Surface EMG electrodes were placed ac-cording to the recommendation of the SENIAM Protocol (SurfaceElectroMyoGraphy for the Non-Invasive Assessment ofMuscles) todetect soleus muscle EMG [43].

3.2.2. Step II: initializationAt the beginning of each stretching, the extreme position in an-

kle dorsiflexion was measured which was the maximum angle thepatient was able to reach. At first, subjects foot was moved pas-sively to its dorsiflexion. When the extreme position was reachedaccording to real-time feedback of patient, the operatorwould shutdown themotor and the systemwould record themaximum anglevalue. With the ankle at the extreme dorsiflexion position, subjectwas asked to perform maximum voluntary contraction (MVC) inplantar flexion direction by activating the soleus muscle and theEMG signal was collected at the same time.MVC value of EMG gen-erally needed to be measured up to three times. The peak value ofMVC was recorded for normalization in the PNF stretching.

3.2.3. Step III: stretchingDuring the PNF stretching, the ankle joint was passively rotated

from its neutral position to the extremedorsiflexionposition. Then,the subject was asked to perform isometric contraction with thesoleus muscle activated and maintained the soleus EMG in therange of 50% 10% MVC for 15 s. The target range and the holdduration time were adjusted based on actual condition of differentsubjects and the rehabilitation phase. The processed EMG feedbackand the target range were provided through a customized GUI inthe patient monitor. After the 15 s muscle activation, ankle jointwas moved back to its neutral position to relax the muscle. Thebreak between each PNF stretching was 10 s. Each training sessionwas 30min including about 30 trails. Before and after each training,ankle joint was passively rotated between its neutral position andextremedorsiflexion position for about 1min towarmup and relaxthe soleus and gastrocnemius muscle, respectively.

3.3. Evaluation

The robotic anklefoot system can be available not only to treatthe ankle joint with spasticity and/or contracture but also to quan-titatively evaluate the effectiveness based on the rehabilitation-induced changes in joint biomechanical properties. Improvementof passive and active properties of ankle joint will be describedhereafter.

3.3.1. Passive properties of ankle jointSince spasticity and/or contracture can reduce the joint ROM

(mainly in dorsiflexion direction) and largely increase dorsiflex-ion resistance torque (plantar flexor muscle resistance torque),changes of them are effectively physical size improvements.Throughout the stretching treatment, the robotic systemmeasuresthe passive ROM and the resistance torque. The ROM measureswere divided into dorsiflexion ROM, plantar flexion ROM and to-tal ROM. Here we only pay more attention to the dorsiflexion ROMsince spasticity/contracture can cause drop-foot and we do notwant them to do some plantar flexion motion within its ROM.

Passive joint dynamic properties in terms of joint stiffness andviscosity before/after PNF rehabilitation are evaluated quantita-tively. They are measured as the slope of the torqueangle rela-tionship (hysteresis loop) and the slope of torquevelocity rela-tionship [4,25]. In hysteresis loop, the ascending curve representsthe passive dorsiflexion phase and the descend curve representsthe plantar flexion phase, as show in Fig. 9. and repre-sent the torqueangle relationship before and after rehabilitation,respectively. The changes of them can reflect improvement of pas-sive biomechanical properties.

Before the whole rehabilitation treatment, we measure andrecord the maximum dorsiflexion angle m which the patient canbe ability to reach passively. Meanwhile, corresponding resistancetorque m at the position m is also measured. We did not directlycompare (m, m) and ( m,

m) between before and after the PNF

rehabilitation treatment and it may be meaningless, becauseobviously the larger joint angle, and the larger resistance torque.Therefore, maximum dorsiflexion angle and m under the sameresistance torque m before and after rehabilitation are comparedand so are maximum resistance torque m and at the same angleposition m, as shown in Fig. 9.

3.3.2. Active properties of ankle jointFor stroke patients, because of brain dysfunctions related to dis-

ease of the blood vessels supplying the brain, it leads to loss ofmuscle inhibition and cause spasticity. PNF can improve patientscontrol for their back muscles through reconstruction of nervefunction because the treatment needs patients to perform isomet-ric contraction with the soleus muscle activated and to track tar-get curve. In addition, PNF as a active rehabilitation therapy canstrengthen the muscle force indicated by the active output torqueof ankle joint. Those advantages are what the passive stretchingdoes not have.

We propose a training Score to quantitatively evaluate theoutcome of PNF stretching. It can reflect active properties of anklejoint comprehensively. We assume that P is the feedback value

8 Z. Zhou et al. / Robotics and Autonomous Systems ( )

Fig. 9. Torqueangle relationship (hysteresis loop) during ankle stretching in dorsi- and plantar flexion, obtained from subject 3. The x-axis is the dorsiflexion angle and theY -axis is the resistance torque. (, ) and ( , ) represent the torqueangle relationship before and after rehabilitation, respectively. The variable with subscript m refersto the maximum value.

Table 2Comparison of maximum dorsiflexion angle and m under the same resistance torque

m andmaximum resistance torque m and at the same position m between before

and after PNF rehabilitation.

Patient no. m (deg) m (N m) (N m) m (deg) m (N m) (deg)

1 43.8 45.4 20.7 51.5 35.6 37.42 40.1 61.3 36.5 44.0 42.9 30.43 37.0 55.6 43.2 39.0 46.7 32.54 31.5 31.7 28.1 32.0 27.5 29.35 35.9 33.8 21.4 43.7 34.4 35.1Mean SE 37.6 2.1 45.6 5.8 29.8 4.4 42.0 3.2 37.4 3.4 32.9 1.5

for patient during PNF training, which refers to the ratio betweencurrentmeasured EMGvalue andMVCor the ratio between currenttorque and maximum active joint torque. Pt refers to the targetratio and the target range is PtEr in our systemwhich are showedin GUI (Fig. 7). Patients are asked to perform isometric contractionto reach Pt and maintain P within the target range during thepredefined time T . Then we calculate the average value across Tand the training Score of each trial is defined as

Score = mean(sgn(P Pt)) (5)

where sgn(x) is defined as

sgn(x) =

1 |x| < EdEr |x|Er Ed

Ed 6 |x| 6 Er

0 |x| > Er

(6)

where Ed (>0) is the value of deadband around 0 and Er (>0) isthe value of target range around 0 (Fig. 10). They are empiricallydetermined to be 0.02(2%) and 0.1(10%), respectively. Finally wemultiply Score by 10.0 to map it from 01 to 010. In our experi-ment, default value of T and Pt are 15 s and 50%, respectively. Forinstance, if real-time P is 56% or 44%, sgn (P Pt ) equals to 0.5.

To avoid some disturbance, data including two seconds of start-ing and ending respectively during each stretching are discardedand not counted for the score. Each treatment is 30min containingabout 2030 trials PNF stretching. Final score for one treatment iscalculated through averaging all trials score in the day.

4. Experimental results

4.1. Changes in passive properties of ankle joint

The increase in ankle ROM and the decrease in resistancetorque were consistently observed, indicating that ankle joint was

Fig. 10. Function sgn(x). Ed (>0) is the value of deadband around 0 and Er (>0) isthe value of target range around 0.

more compliant than before and spasticity/contracture had beenalleviated effectively. Comparison of the maximum dorsiflexionangle and m under the same resistance torque

m before and

after the treatment were shown in 6th and 4th columns of Table 2.And we also conducted a comparison of the maximum resistancetorque m and in the same position m before and after thePNF rehabilitation treatment, as shown in 2nd and 3rd columns ofTable 2. Over multiple patients, the dorsiflexion angle increasedfrom 32.9 1.5 to 42.0 3.2 while the resistance torquedecreased from 45.6 N m 5.8 N m to 29.8 N m 4.4 N m.Furthermore, the showed significantly lower than m (p = 0.019)while the m showed significantly larger than (p = 0.014).Those can demonstrate that PNF is effective for treatment for anklespasticity and contracture.

The rehabilitation treatment of our system can result in consid-erable changes in joint properties characterized by joint stiffnessand viscosity. They are calculated from the relationship between

Z. Zhou et al. / Robotics and Autonomous Systems ( ) 9

Fig. 11. Changes in torqueangle relationship (1st row), stiffnessangle relationship (2nd row), and viscosityangle relationship (3rd row) of spastic ankles caused bythe six-week PNF treatment in two stroke patients. The blue and red line correspond evaluations done immediately before and after treatment, respectively. Each columncorresponds to a stroke patient. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 12. Changes of active torque of ankle joint during six weeks. The x-axis is the trial number (about 3 times per week) and the y-axis is the increment of active jointtorque relative to the maximum torque before treatment.

the joint angle and resistance torque (hysteresis loop). As shownin the representative cases (Fig. 11), such as the subject 1 (the 1stcolumn), joint stiffness is reduced remarkably after rehabilitationacross the range of muscle contraction (2nd row of Fig. 11). At thesame time, the treatment also reduces the joint viscosity (3rd rowof Fig. 11). Other subjects except subject 4 are similar to the sub-ject 1, having significant improvement. For subject 4 (the 2nd col-umn), we do not see increase in maximum dorsiflexion angle andjust find decrease in resistance torque. Also, stiffness and viscos-ity also do not decrease evidently. Since he suffered from one timecerebrovascular disease in the third week, this maybe result thatthe effect of rehabilitation was not obvious for him.

4.2. Change of active properties of ankle joint

As shown in Fig. 12, we can see that the maximum activetorque of every subject was showing a rising trend as time goeson. For a representative case, such as subject 5, his joint torque hasincreased 24.24 Nm after treatment which was a large promotion.Other subjects are also similar. On the whole, increment of jointtorque is 15.3 N m 5.9 N m. As shown in Fig. 13, the Scoreof before/after six weeks rehabilitation and normal subjects were5.7 0.9, 8.1 0.6 and 9.5 0.3 respectively. Over multiplepatients, the increase in training Score is observed, and it is close tothat of the healthy subjects. Thereinto, the normal value are fromfive normal subjects about 20 trials per subject andwe can find that

10 Z. Zhou et al. / Robotics and Autonomous Systems ( )

Fig. 13. Comparison of training Score of patients before and after rehabilitation andnormal subjects. The Scores are 5.7 0.9, 8.1 0.6 and 9.5 0.3 respectively.

the task is relatively easy for all normal subjects. The result presentthat the patients were becoming faster to track the target line afterthe PNF rehabilitation.

5. Discussion

We proposed a PNF integrated robotic anklefoot system forrehabilitation of ankle joint with spasticity/contracture in poststroke patients. Different from existing treatments, PNF is a kindof method based on proprioceptionwith the ultimate goal being tooptimizemotor performance and rehabilitation. The proposed sys-tem intelligently stretches the ankle forcefully and safely to its ex-treme positions where spasticity and contracture are significant. Itis reliable and convenient for patients and therapists. Furthermore,rehabilitation effectiveness is verified in two aspects includingactive and passive joint properties. Our system is considerable im-provement over previous study andmore importantly, it is promis-ing for treatment of ankle joint with spasticity/contracture inclinical rehabilitation.

The proposed system has following advantages over previousrobotic devices for post stroke rehabilitation. First, the PNF is veryeffectiveness for post stroke rehabilitation over passive stretch-ing. In PNF treatment, the ankle is stretched to its extreme po-sitions where spasticity and contracture are significant and thenthe patient performs isometric contraction with the soleus mus-cle according to biological feedback. For spasticity/contracture re-habilitation, the barrier to further progress lies not in developingnew hardware but rather in finding the most effective way to en-hance neuro-recovery [44]. It is clear that PNF can be qualified tocarry the neurologic recovery. Active joint properties are improvedsignificantly with the training score increasing from 5.7 0.9 to8.1 0.6, and getting close to that of normal subjects (9.5 0.3)after treatment (Fig. 13). The results indicate that neural control isimproved by the PNF training. In addition, muscle strength has arising trend as time goes on (Fig. 12) and increment of joint torqueis 15.3 N m 5.9 N m. Those are what the passive stretching doesnot have.

To verify the effectiveness of our system with passive stretch-ing, we can compare some common indicators. In our results, thepassive hysteresis loop shows that the maximum dorsiflexion an-gle increases from 32.9 1.5 to 42.0 3.2 (p = 0.014)while the resistance torque decreases from 45.6 N m 5.8 N mto 29.8 N m 4.4 N m (p = 0.019) (Table 2). All these changesare quite evident. In addition, changes in joint stiffness and viscos-ity are also significantly improved (Fig. 11). However, in [25], dor-siflexion range increased from 11.9 to 16.5 at the same torque(10 N m) after stretching. Changes in joint stiffness and viscosityare not significant. In [27], the resistance torque was 11.9 N m and10.5 N m and the stiffness was 0.60 N m/ and 0.49 N m/ at 20dorsiflexion, pre- and post-intervention, respectively. In [29], the

dorsiflexion angle increases of 5. Above all, we can find that theproposed PNFmethod ismore effective than the passive stretching.Now, there are several commercial products called isokinetic ma-chines (e.g. BIODEX, CYBEX NORM) whose working modes includecontinuous passive motion (CPM) and resistance training. Differ-ent from them, the working mode of our system is originated fromPNF technique as a kind of neurophysiological technique most of-ten used to inhibit spasticity based on two inhibitory conceptsAutogenic inhibition and Reciprocal inhibition which is respond todirect hold-relax and indirect hold-relax respectively. The prelimi-nary clinical results demonstrate its effectiveness on rehabilitationof spasticity and/or contracture.

Second, the proposed system can raise compliance and ini-tiative of patients which are key points to make them trainingzealously and persistently [45,46]. Stroke rehabilitation is in needof a long-term continuous operation as short-term treatment isless effective and usually insufficient to make patients fully recu-peration [13,16,17]. In our system, the friendly GUI can providebiological feedback and the patient needs to perform isometriccontraction with the soleus muscle according to the biomedicalfeedback, which have formed a reasonable humanmachine inter-action. From behaviors and experiences of all subject, it is foundthat they showmore interested in training than passive stretching.Thus, our system can make the patients persevere in a long-termtreatment with better initiative.

Moreover, our device stretches the ankle joint forcefully andsafely. The stretching velocity is controlled similar to Zhanget al. [25] and the control method can enhance safety. The systemcan cover the limitation of stretching frequency and force in phys-ical therapist and do not have the shortcoming of labor, so it canmake long-term and sufficient treatment [20]. Safety of HMI [40]is ensured by redundantly design of mechanical limit, emergencyswitch and control strategy. In addition, multi-DOFs of platformcan be adjusted to avoid misalignment between biological ankleaxis and robotic device rotation axis [39].

The robotic anklefoot rehabilitation system, though beingpromising, has some limitations in this paper and future improve-ments are needed. Firstly, the small sample of patients takes part inthe pilot experiments and we will verify more subjects to achievemore comprehensive and reliable evaluation of our system andthe rehabilitation therapy comparingwith different trainingmeth-ods. Secondly, only a six-week rehabilitation was done for thosepatients and we will continue the long-term treatment for thosepatients and to further investigate the effectiveness of PNF treat-ment. Thirdly, we will try more effective methods integrated withrobotics for stroke rehabilitation in future, such as other neuro-physiologic techniques or motor learning techniques [47].

6. Conclusion

In this paper, we have proposed a PNF integrated roboticanklefoot system for rehabilitation of ankle joint with spastic-ity/contracture induced by stroke. The proposed system is in-telligent and reliable, and can offer more effective treatmentthan passive stretching in improvement of both passive and ac-tive joint properties. We verify its effectiveness through clini-cal experiments. The system can be a good solution for anklespasticity/contracture. Future endeavors should further improveits performance and make it widely used in clinical rehabilitation.

Acknowledgments

This work was supported by the National Natural ScienceFoundation of China (61005082, 31000456, 31371020, J1103602,61020106005), theBeijingNova Program (No. Z141101001814001)and the PKU-Biomedical Engineering Joint Seed Grant 2014.

Z. Zhou et al. / Robotics and Autonomous Systems ( ) 11

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Zhihao Zhou received his Bachelor degree in Mechani-cal Engineering fromChinaUniversity of Geosciences (Bei-jing). He is currently working towards the Ph.D. degreeunder the supervision of Prof. Qining Wang in the Col-lege of Engineering, Peking University, China. His researchinterests include biomedical engineering and robotics forhealthcare.

Yuan Zhou received her Bachelor degree from Peking Uni-versity, China and the Ph.D. degree from theDepartment ofRehabilitation Medicine, First Hospital, Peking University,China. Her research interests include stroke rehabilitationand robotics.

Ninghua Wang received her Bachelor degree from Bei-jing Medical University, China and Ph.D. degree from TheHong Kong Polytechnic University, Hong Kong. She is cur-rently a full professor and the Dean of the Departmentof Rehabilitation Medicine, First Hospital, Peking Univer-sity, China. Her research interests include rehabilitationmedicine, stroke rehabilitation and rehabilitation devices.

Fan Gao received his Bachelor degree in MechanicalEngineering from Peking University, China and Ph.D.degree inMechanical Engineering fromPennsylvania StateUniversity, USA.He is currently anAssistant Professor fromDepartment of Health Care Sciences, University of TexasSouthwestern Medical Center, Dallas, USA. His researchinterests include rehabilitation device, muscle mechanics,orthotics and prosthetics.

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12 Z. Zhou et al. / Robotics and Autonomous Systems ( )

Kunlin Wei received his two M.A. degrees (in Kinesi-ology and Electrical Engineering, respectively) and Ph.D.degree in Kinesiology from the Pennsylvania State Uni-versity, USA. Before that, he obtained his B.E. in Biome-chanics from Beijing Sports University, China. He is anAssociate Professor from Department of Psychology,Peking University, Beijing, China. Dr. Weis research inter-ests include sensorimotor control, robotics, biomechanics,humanmachine interaction, and motor rehabilitation.

Qining Wang received his Bachelor degree in ComputerScience and Technology from China University of Geo-sciences (Beijing) in 2004, and the Ph.D. degree in Dynam-ics and Control from Peking University in 2009. He was anAssistant Professor in the Center for Systems and Control,College of Engineering, Peking University, from July 2009to July 2012. He is currently an Associate Professor in theCollege of Engineering, Peking University, and the Directorof the Beijing Engineering Research Center of IntelligentRehabilitation Engineering. He is the Project Leader of theRobotic Prosthesis R&D Group, Peking University. His re-

search interests are in the fields of bio-inspired robots and rehabilitation systems.

A proprioceptive neuromuscular facilitation integrated robotic ankle--foot system for post stroke rehabilitationIntroductionRobotic ankle--foot systemMechanical designControl systemGraphical user interface

MethodProprioceptive neuromuscular facilitation (PNF)Subjects and experiment protocolStep I: preparationStep II: initializationStep III: stretching

EvaluationPassive properties of ankle jointActive properties of ankle joint

Experimental resultsChanges in passive properties of ankle jointChange of active properties of ankle joint

DiscussionConclusionAcknowledgmentsReferences