Effect Of Motor Neuromuscular Electrical Stimulation On .

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Research ReportEffect of Motor Neuromuscular ElectricalStimulation on Microvascular Perfusion ofStimulated Rat Skeletal MuscleF Rlchard ClementeDanlel H MatullonlsKirk W BarronDean P CurrlerThe puqose of this study was to determine the efect of neuromuscular electricalstimulation (NMES) (2,500-ppssine wave interrupted at 50 bps) on the degree ofmicrovascularp d i i o n in stimulated skeletal muscle. The tibialis anterior (TA)and m t m r di'itorum longus (EDL) muscles of 3 6 male rats were treated withNMES for 3 0 minutes at current amplitudes suficient to produce a sustainedmuscle contraction (motor NMES). Muscle tissue was removed at 0, 5, 10, 15, and30 minutes afrer NMES. The perfused vessel/musclefiberratio (PV/q of the stimulated animak; at time 0 minutes was greater than that of the unstimulated controlanimaki. A gradual decrease in the magnitude of the PV/F increase was notedover time. Depending on the muscle'sjber-type composition, the PV/F values returned to control levels by 10 to 30 minutes afier motor NMES. The results indicate (I) that motor NMES signzficantly increases the degree of microvascular perfusion in stimulated rat skeletal muscle and (2)that the increased degree ofperfusion perskits for various lengths of time, depending on rhe ber-type composition of the muscle. Thus, if responses in an animal model can be used as indicators of similar human responses, then the results of this study suggest that NMEScan be used to increase the degree of microvascular perfusion in human skeletalmuscle. [Clemente FR, Matulionis DH, B a m n KW, Cum'er DP. Effect of motorneuromzlscular electrical stimulation on microvascularperfmUS1onof stimulatedrat skeletal muscle. Pbys Tber 1991;71:397406]Key Words: Electrotherapy, electrical stimulation; Hemodynamics; Musculoskeletalsystem; Perjiciion; Rats.FR Clemente, PhD, PT,is Associate Professor, School of Physical Therapy, Slippery Rock University,S l i p- e.nRock.,PA 16057-1326 (USA).,, Address all corres ondenceto Dr Clemente.D Matulionis, PhD, is Associate Professor, Department of Anatomy and Neurob ology,College ofMedicine, University of Kentucky, Lexington, KY 40536.K Barron, PhD, is Assistant Professor, Department of Physiology, University of Oklahoma, HealthSciences Center, Oklahoma City, OK 73190.D Currier, PhD, PT,is Professor, Division of Physical Therapy, College of Allied Health Professions,University of Kentucky.This research was supported in pan by National Institutes of Health Grant #HW6552.The protocol outlining the use of animals in this study was approved by the Institution AnimalCare and Use Committee of the University of Kentucky.The application of electric current tohuman tissues to alleviate or improvevarious maladies dates back to 400BC.' Since that time, electrotherapyhas experienced a fluctuating popularihr as a treatment anent.In the earlv"1980s, there was a resurgence of interest in electrotherapy or neuromuscular electrical stimulation (NMES) asa therapeutic modality. This resurgence has stimulated interest in research of the efficacy of NMES. Somereports in the literature indicate thatthe application of NMES will alter peripheral hemodynamics. Investigatorshave shown an increased blood flowTh& article was submitred April 3, 1990, and was accepted December 21, 19.90.52 / 397Physical Therapy/Volume 71, Number 51May 1991

velocity in the arteries that supply thestimulated muscles24 and a decreasedblood flow in the arteries of nonstimulated extremities.5 Even thoughblood flow appears to be increased inthe vessels supplying the stimulatedmuscle, nothing is known regardingthe specific response of the microvascular bed in these muscles.The volume of blood that flows past agiven point in a vascular bed in agiven period of time (Q) is related toblood flow velocity (V) and perfusedvascular cross-sectional area (A), according to the equation6This equation can be rewritten asBased on this relationship, bloodflow can be increased by increasingeither the blood flow velocity o r theperfused vascular cross-sectionalarea. The blood flow velocity is indicative of how fast blood is movingthrough the blood vessels, but itdoes not necessarily reflect the spatial relationship between the bloodand the parenchymal tissue. Theperfused vascular cross-sectionalarea or the degree of microvascularperfusion is an indicator of the diffusion distance, the spatial relationship between the blood and the parenchymal tissue.The degree of muscle microvascularperfusion is an indicator of the diffusion distance for oxygen, nutrients,and metabolites to and from the paAn increased derenchymalgree of microvasculature perfusionreduces the diffusion distance, whichimproves the availability of oxygenand nutrients to and enhances theremoval of metabolites from the parenchymal muscle tissue. The diffusion distance between the blood supply and the muscle tissue markedlyinfluences the function of the muscle.If treatment with NMES does increasethe degn:e of microvascular perfusion, then NMES should decrease thediffusion distance. This decrease inexchange distance could enhance thePhysical Therapy /Volume 71, Numberefficiency of muscle contraction, promote healing of damaged muscles,and improve metabolic exchange inareas of impaired circulation.Currently, no definitive studies address the microvascular response inskeletal muscle subsequent to NMES.An understanding of microvascularresponse to NMES is important because tissue function is dependent onan accessible blood supply in the microvascular bed and NMES is usedclinically without a clear understanding of its possible effects on the tissuemicrovascular bed. Thus, the purposeof this investigation was to test thehypothesis that NMES of 2,500 ppsfrequency modulated to 50 bursts persecond (bps) increases the degree ofperfusion in the microvascular bed ofstimulated skeletal muscle.Method and MaterialsSampleThirty-six male, 12- to 16-week-oldSprague-Dawley rats weighing 300to 450 g were used in this study. Allanimals were housed in quarters atthe University of Kentucky Tobaccoand Health Research Institute. Theambient environment was maintained at 22 C and 48% relative humidity with a 12-hour light/dark cycle. Food and water were providedad libitum. In order to ensureproper health, all animals werequarantined for 10 days prior totheir use in the study.ProcedureAll animals were weighed and subsequently anesthetized by intraperitoneal injection (65 m a g ) of sodium pentobarbital. Sodiumpentobarbital was selected becauseit has been shown to have little o rno effect on the vascular resistancein skeletal muscle.9J0 Appropriateanesthesia was maintained for 30minutes o r for the duration of theexperimental period for all animals,including the controls. The temperature of each animal was monitoredby a rectal probe and maintained at37 C by radiant heat. After each ani-mal was anesthetized, cannulas wereinserted into the right jugular vein,the trachea, and the left commoncarotid artery. The jugular cannulawas used for administration of thevascular label, and the endotrachealtube was inserted to maintain apatent airway. The mean arterialblood pressure and heart rate weremeasured via the carotid artery cannula and recorded on a strip-chartrecorder. These cardiovascular variables were used to monitor the status of the peripheral circulatory system of each animal under resting,nonstimulated conditions and during experimental manipulations.Each of the 36 animals was randomly assigned to one of sixgroups. Group 1 consisted of animals that were untreated (absolutecontrols). Because of their accessibility and distinct muscle fiber-typedistributions, the right tibialis anterior (TA) and extensor digitorumlongus (EDL) muscles were chosenfor stimulation. These muscles ofthe group 2, 3, 4, 5, and 6 animalswere electrically stimulated to evokea sustained tetanic contraction.Groups 2, 3, 4, 5, and 6 were defined based on the tissue samplingtimes of 0, 5, 10, 15, and 30 minutesafter NMES, respectively.Electrical StimulationAll animals except the absolute controls received NMES transcutaneously. The method of stimulationwas designed to alter peripheralblood circulation based on protocols used clinically and during experimentation on animals.2,5-11,12Theanimals were positioned supine ona surgery board and secured inplace. Carbon silicone electrodes,1.0 x 1.5 cm, were used to adaptthe electrical stimulator to the hindlimb of the rats. After shaving theright leg, one electrode was positioned over the lateral aspect of theright knee and another was placedanteriorly, just proximal to the rightankle. These electrodes were heldin place by rubber strips, whichwere glued to the skin. The electrical current was produced with an

Electostima 180-2i stimulator.* Thecharacteristics of the Electrostim@180-2i stimulator's current havebeen described and illustrated previo sly.2 5J J3This stimulator emitsa continuous sine-wave output witha carrier frequency of 2,500 pps.The carrier frequency was interrupted at 50 bps. The stimulatordelivered 12-second bursts of stimuli that were finely ramped s o thatthe current gradually increased overa 5-second period but had anabrupt ramp decline. Each 12second burst was followed by a 10second rest interval, producing a12-/lo-second "on/offU ratio.The NMES was applied at three timesthe amplitude needed to produce aminimal, visible contraction of the TAmuscle (motor NMES).l3 The currentamplitudes were monitored with amultimeter. In all cases, motor NMESwas applied for 30 minutes.Muscle Prepantion andData CollectionAt various times after completion ofthe NMES (ie, 0, 5, 10, 15, and 30minutes), the TA and EDL muscleswere removed quickly by sharp dissection. These muscles were thendipped in talcum powder, coveredwith O C P (ornithine carbamoyltransferase) compound? pinned to a pieceof cork, and frozen in isopentanecooled over liquid nitrogen.14J5 Thetissue was transversely sectioned (10pm) at the midpoint of the musclebelly.Muscle fiber types and perfused microvessels were identified on serialsections. Identification of muscle fibertypes was achieved by staining themuscle sections for myosin ATPase@reincubation pH 4.4).14.16 For eachTA muscle, 72 nonoverlapping fields(0.057 mm2field) were sampled ineach section. These sampled sectionsincluded 36 fields in the area in whichmuscle fiber types were most hetemgeneous and 36 in the area in whichmuscle fiber types were most homogeneous. Twenty-seven nonoverlappingfields were sampled in each EDL muscle section. Fibers that partially protruded from the reference area (0.057mm2/field) were counted as one-halffibers." The proportion of each fibertype was calculated as a percentage ofthe total number of muscle fiberscounted per reference area.ls Percentages were calculated for the entireEDL and TA muscle sections and forthe two dilferent fiber-type regions ofthe TA muscle sections.Fluorescein isothiocyanate conjugatedto bovine serum albumin (FITC-BSA)was used according to the methodol-ogy of McDonagh and Williams19 tolabel the perfused microvessels. TheFITC-BSA solution was continuouslyinfused over a 1-minute periodthrough the jugular vein cannula. Theinfusion was started 2.5 minutes priorto collection of the muscle tissue, allowing the FITC-BSA to circulate for1.5 minutes. To visualize the perfusedmicrovasculature, the tissue, whichhad been labeled with FITC-BSA, wasprocessed according to a previouslydescribed method.20 The degree ofmicrovascular perfusion was evaluatedvia fluorescent microscopy using aphotomicroscope with xenon epiillumination and a 490-nm barrierfilter. The same sampling procedurewas used for this assessment as described previously for the assessmentof fiber-type composition.Perfused microvessels were definedas microvessels (ie, terminal arterioles, capillaries, and postcapillaryvenules), 5 to 20 pm in diameter,21s22which contained the fluorescent label.The perfused microvessels and muscle fibers present in each field werecounted at a magnification of X400. Avalue of one-half was given to anymuscle fiber o r microvessel locatedon the field perimeter line." The perfused microvesseVmuscle fiber ratio(W/F ratio) was calculated as the total*Electrostim@USA Ltd, 1851 Black Rd, Joliet, ILnumber of perfused microvessels inan area divided by the total numberof muscle fibers in the same area.This ratio was used as an indicator ofthe density o r degree of microvascular perfusion in the skeletal mu cle. 3The W/F ratio was calculated for thewhole TA muscle section, for its heterogeneous and homogeneous muscle fiber-type regions, and for thewhole EDL muscle section.Data AnalysisThe mean values of the WIF ratiowere determined for the TA and EDLmuscles for all animal groups. Theseratios were statistically assessed usingthe Fisher's Protected LSD Test tomake all possible pair-wise comparisons. Significance was set at the alphalevel of .05, and all data are reportedas means 1 standard error of themean.Cardiovascular monitoring indicatedthat mean arterial blood pressureand heart rate were consistent withphysiologic normative values for theanimal model throughout the experimental recording period. Thesecardiovascular variables remainedconsistent with physiologic normative values during all experimentalprocedures.Myosin ATPase staining of the TAmuscle sections revealed two distinctregions of dilferent fiber-type composition. These results are shown inTable 1. The nearly homogeneoussuperficial region, up to approximately 0.81 mm from the surface, wascomposed of 1.1% 0.4% type I (oxidative) and 98.9% 0.4% type I1 (glycolytic) fibers. The deeper, more heterogeneous region of the TA muscle,greater than 0.81 mm from the surface, contained approximately8.3% 0.6% type I and 91.7% 0.6%type I1 fibers. The EDL muscle wasintermediate between these two regions of the TA muscle, being composed of 96.4% 0.4% type I1 fiberswith a uniform distribution of3.7% 0.4% type I muscle fibers. Miles Inc, Diagnostics Div, 1025 Michigan St, Elkhan, IN 46515.54 / 399Physical Therapy / Volume 71, Number 5 / May 1991

Table 1. Fiber-Type Composition ofTibialis Anterior (TA) and ExtensorDigitorum Longus (EDL) Muscles(MeanSEM)1.40*1.12-.-0Whole TA5.2a0.494.220.4dSuperficial TA1.120.498.920.4&Deep TA8.320.691.7t0.6Whole EDL3.720.496.450.420.840.560.28The W/F ratio for the whole TA muscle of the control animals was0.954k0.036. The nearly homogeneous type I1 superficial TA muscleregion had a W/F ratio ofmore0.904*0.0231 and theheterogeneous TA muscle region hada ratio of 1.010 0.050.In the EDLmuscle of the control animals, a PV/Fratio of 0.970k0.024 was calculated.These data are shown in Table 2 andin Figures 1 through 4.In the motor NMES-time 0 minutesspecimens, PV/F ratios were1.271L0.019for the whole TA muscle,1.132 0 . 0 4 9for the superficial TAmuscle region, and 1.366k0.027 forthe deep TA muscle region (Tab. 2,Figs. 1-3). Statistical analysis indicatedthat motor NMES increased the PV/Fratios of the whole TA muscle and ofboth the superficial and the deep TAmuscle regions at time 0 minutes(Figs. 1-3). In the EDL muscle at time0.00Time (min)130Figure 1. Perfused vesselImuscleJiberratios (PVIF) of whole tibialis anterior muscleat 0 to 30 minutes after motor neuromuscular electrical stimulation (open bars).Striped bar represents PVIF of unstimulated control animals. Asterisk indicates statistically sign@cant increase when compared with control levels. (Mean 2SEM.)0 minutes after motor NMES, the PV/Fratio was 1.229 -0.038(Tab. 2). ThisPV/F ratio represents a statistically significant increase when compared withcontrol levels (Fig. 4).The degree of perfusion (W/F ratio)was also determined at time intervalsof 5, 10, 15, and 30 minutes aftertermination of the motor NMES ofthe TA and EDL muscles (Tab. 2,Figs. 1-4). Over time, a gradual returnto control values was observed. ThePV/F ratio for the whole TA musclereturned to values similar to controllevels by 15 minutes post-motorNMES (1.049 0.020) (Fig. 1). In thesuperficial TA muscle region, andW/F ratio returned to control levelsby 10 minutes after motor NMES(0.930 0.037) (Fig. 2). The W/F ratiosin the deep TA muscle region decreased to a value equivalent to control levels by 30 minutes after motorNMES (1.002 k0.009) (Fig. 3). Degreeof perfusion in the EDL muscle followed a similar pattern to that of thedeep TA muscle region, with the PV/Fratio returning to control values by30 minutes post-motor NMES(0.901k0.020) (Fig. 4).Table 2. Mean (2SEM) of Pegused VessellFiber Ratio for Tibialis Anterior (TA) and Extensor Digitorum Longus (EDL) Muscles atVarious Times (in Minutes) gfter Motor Neurornuscular Electrical Stimulation (Motor NMES)Petfused VesselIFiber RatloSourceWhole TASupetflclal TADeep TAEDLControlMotor NMES-0Motor NMES-5Motor NMES-10Motor NMES-15Motor NMES-30Physical Therapy /Volume 71, Number 5 /May 1991400 / 55

1.20reflex arc can be activated by musclecontraction31-33 and that the activationof the group 111 and IV fibers can produce a pressor resp0nse3 slo r a deand an increasepressor re ponse35.3 in blood flow.2393'3*0.96.-0CdClement and Shepherd37 reportedthat muscle contraction can markedlyattenuate the vasoconstrictor effects ofefferent sympathetic outflow to theactive muscle. They suggested that theinteraction between the influences ofmuscle contraction and sympatheticoutflow acts to maintain the most efficient and effective ratio of blood flowto oxygen consumption.0.72QZ a0.480.240.0001051530Time (min)Flgure 2. Pefised vesseI/musclejber ratios (PVIF) of superJicialtibialis anteriormuscle region at 0 to 3 0 minutes after motor neuromuscular electrical stimulation(open bars). Striped bar represents PVIF of unstimulated control animals. Asterisk indicates statistically signij5cant increase when compared with control values. (MeankSEM)DiscussionThe primary goal of this study was totest the hypothesis that transcutaneousNMES, applied at a frequency of 2,500pps and modulated at 50 bps, increases the microvascular perfusion ofstimulated skeletal muscle. At time0 minutes, motor NMES produced asignificant (PS.05) increase in thedegree of microvascular perfusion inall muscles analyzed. Although noprevious reports of the effects of transcutaneous NMES on microvascularperfusion of skeletal muscle werefound, the results of this study are inagreement with the increased degreeof perfusion described by otherinvestigators,' 23-27who used directmuscle stimulation with indwellingelectrodes. The increase in degree ofmicrovascular perfusion described inthis study supports the view that theblood supply increases during highmetabolic demand, such as duringmuscle contra tion. 6 RMuscle contraction has also beennoted to cause acute alterations ofblood flow. Reports29.30in the literature suggest that these changes mightbe mediated via a reflex arc. The afferent limb of the suggested arc consists of group I11 and group IV so56 / 401matic fibers, which innervatemammalian skeletal muscle.29 31-33The efferent component of the proposed reflex arc is the sympatheticoutflow to the vasculature of the contracting mu cle.3 34Investigators have demonstrated thatthe afferent limb of this suggestedOther investigators have proposedadditional mechanisms for increasingthe degree of microvascular perfusionsuch as a myogenic reflex?8 low oxygen tension in the parenchymal tissue,2739z40unspecified metabolites ofincreased conmuscle ontraction,4l- and thecentration of adenosine:-5release of a neuromodulator o r neuropeptide.6 Many of these mechanisms have been studied in somedetail; however, the actual role thateach plays in the response of the microvasculature to muscle contractionis still not certain.1.601.28.-0.96QZ a0.64.-0d0.320.00Time (min)Figure 3. Perfused vesellmusclejber ratios (PVIF)of deep tibialis anterior muscleregion at 0 to 3 0 minutes after motor neuromuscu arelectrical stimulation (openbars). Striped bar represents PVIF of unstimulated control animals. Asterisk indicatesstatistically signiJca

fields were sampled in each EDL mus- cle section. Fibers that partially pro- truded from the reference area (0.057 mm2/field) were counted as one-half fibers." The proportion of each fiber type was calculated as a percentage of the total number of muscle fibers counted per reference area.ls Percent- ages were calculated for the entire

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