Effects Of Cyclic Stretching Exercise On Long-Lasting .
Physiol. Res. 69: 861-870, cts of Cyclic Stretching Exercise on Long-Lasting Hyperalgesia,Joint Contracture, and Muscle Injury Following Cast Immobilizationin RatsKazuhiro HAYASHI1,2*, Saori FUKUYASU-MATSUO3*, Takayuki INOUE4, MitsuhiroFUJIWARA5,6, Yuji ASAI7, Masahiro IWATA6,7, Shigeyuki SUZUKI8* These authors contributed equally to this work.1Multidisciplinary Pain Center, Aichi Medical University, Nagakute, Japan, 2Department ofRehabilitation, Aichi Medical University Hospital, Nagakute, Japan, 3Division of Rehabilitation,Gifu University Hospital, Gifu, Japan, 4Department of Rehabilitation, Nagoya University Hospital,Nagoya, Japan, 5Department of Rehabilitation, Kamiiida Rehabilitation Hospital, Nagoya, Japan,6Department of Physical and Occupational Therapy, Nagoya University Graduate School ofMedicine, Nagoya, Japan, 7Department of Rehabilitation, Faculty of Health Sciences, NihonFukushi University, Handa, Japan, 8Department of Health and Sports Sciences, School of HealthSciences, Asahi University, Mizuho, JapanReceived January 20, 2020Accepted June 9, 2020Epub Ahead of Print September 9, 2020SummaryKey wordsThe effects of exercise on mechanical hyperalgesia, jointStretchingcontracture, and muscle injury resulting from immobilization areImmobilizationexercise Hyperalgesia Muscledamage not completely understood. This study aimed to investigate theeffects of cyclic stretching on these parameters in a rat model ofCorresponding authorchronic post-cast pain (CPCP). Seventeen 8-week-old Wistar ratsM. Iwata, Department of Rehabilitation, Faculty of Healthwere randomly assigned to (1) control group, (2) immobilizationSciences, Nihon Fukushi University, 26-2 Higashihaemi-cho,(CPCP) group, or (3) immobilization and stretching exerciseHanda, Aichi 475-0012, Japan. Fax: 81-569-20-0127. E-mail:(CPCP STR) group. In the CPCP and CPCP STR groups, bothiwata-m@n-fukushi.ac.jphindlimbs of each rat were immobilized in full plantar flexion witha plaster cast for a 4-week period. In the CPCP STR group,Introductioncyclic stretching exercise was performed 6 days/week for2 weeks, beginning immediately after cast removal prior toreloading. Although mechanical hyperalgesia in the plantar skinand calf muscle, ankle joint contracture, and gastrocnemiusmuscle injury were observed in both immobilized groups, thesechanges were significantly less severe in the CPCP STR groupthan in the CPCP group. These results clearly demonstrate thebeneficial effect of cyclic stretching exercises on widespreadmechanical hyperalgesia, joint contracture, and muscle injury ina rat model of CPCP.Chronic periods of reduced physical activity canoccur following traumatic injury, with prolongedimmobilization, and as a part of aging. The primaryeffects of muscle disuse in such situations includeprogressive skeletal muscle atrophy (Honda et al. 2015),loss of muscle extensibility (Honda et al. 2018), and jointcontracture (Inoue et al. 2007, Morimoto et al. 2013).Studies have confirmed that 4 weeks of hindlimb castimmobilization causes disuse muscle atrophy in rats(Okita et al. 2009), with decreased capillary-to-myofiberratios in the hindlimb muscles after 2 weeks (KataokaPHYSIOLOGICAL RESEARCH ISSN 1802-9973 (online) 2020 Institute of Physiology of the Czech Academy of Sciences, Prague, Czech RepublicFax 420 241 062 164, e-mail: physres@fgu.cas.cz, www.biomed.cas.cz/physiolres
862Vol. 69Hayashi et al.et al. 2014) and 4 weeks (Matsumoto et al. 2014) ofimmobilization. Other studies have shown that castimmobilization induces muscle fibrosis, whichcontributes to limb contracture (Honda et al. 2015,Maezawa et al. 2017, Yoshimura et al. 2017). A 4-weekperiod of hindlimb cast immobilization was shown toincrease the vulnerability of rats to muscle damage atreloading because of alterations in mobility andmovement (Inoue et al. 2009).In addition to physical and functional changes,recent studies in healthy human subjects and animalmodels have found that prolonged immobilizationinduces pain hypersensitivity (Terkelsen et al. 2008,Nakano et al. 2012, Ohmichi et al. 2012, Morimoto et al.2013, Sekino et al. 2014, Hamaue et al. 2015, Nakagawaet al. 2018) and may contribute to the development ofcomplex regional pain syndrome (Allen et al. 1999).A study of healthy rats with 2-week cast immobilizationof one hindlimb found long-lasting skin and musclehyperalgesia in the immobilized and contralateral limbs(chronic post-cast pain; CPCP) (Ohmichi et al. 2012).Immobilization-induced hyperalgesia and jointcontracture affect the recovery of muscle functionality afterimmobilization, limit activities of daily living, and increasehealthcare costs. Various therapeutic strategies forreducing CPCP and joint contracture, including treadmillexercises (Morimoto et al. 2013), vibration exercises(Hamaue et al. 2015), and static stretching (Morimotoet al. 2013), have been evaluated in animal models.However, the effects of stretching exercise on postimmobilization pain and joint contracture remain unclear.Some studies have found that stretching reduces jointcontracture (Kaneguchi et al. 2019), whereas others havenot found a clinically relevant effect (Harvey et al. 2017).Continuous passive motion on a stretching machine wasshown to decrease markers of inflammation and mitigatehyperalgesia in a rat model of arthritis (Nakabayashi et mmation and improved pain in rats with subcutaneousinflammation induced by carrageenan (Corey et al. 2012).One recent animal study reported that static stretchingdecreased pain and increased joint range of motion (ROM)in a rat model of CPCP (Morimoto et al. 2013). However,to our knowledge, no studies have evaluated the effect ofcyclic stretching initiated immediately after cast removalon post-immobilization muscle pain in a rat model ofCPCP. The hypothesis of this study was that cyclicstretching exercises initiated immediately after castremoval would decrease long-lasting post-immobilizationmechanical hyperalgesia in rats. We also evaluated theeffect of cyclic stretching on post-immobilization jointcontracture and muscle damage.MethodsAnimalsAll experiments were approved by the EthicsCommittee for Animal Experimentation at the NagoyaUniversity School of Health Science. This study wasperformed in compliance with the ethical guidelines ofthe International Association for the Study of Pain andthe European Guidelines on Laboratory Animal Care.Seventeen 8-week-old male Wistar rats werepurchased from Japan SLC (Hamamatsu, Japan) andhoused under a 12-h light/dark cycle with free access tofood and water. The rats were randomly divided into thefollowing three groups: CPCP without cyclic stretchingexercises (CPCP, n 6), CPCP with cyclic stretchingexercises (CPCP STR, n 6), and age-matched naïvecontrols (CON, n 5; Fig. 1A).Fig. 1A. Schematic diagram and photos of experimental protocol and representative photomicrographs of muscle tissue (hematoxylin-eosinstaining). Treatment groups and treatment schedule. Rats were divided into three groups: age-matched naïve controls (CON, n 5), chronicpost-cast pain (CPCP) without cyclic stretching exercise (CPCP, n 6), and CPCP with cyclic stretching exercise (CPCP STR, n 6).
2020Immobilization and reloadingCPCP was generated through 4 weeks ofhindlimb cast immobilization (Nakagawa et al. 2018).Rats in the CPCP and CPCP STR groups wereanesthetized with intraperitoneal pentobarbital sodium(40 mg/kg). The bilateral hindlimbs were encased for4 weeks in plaster casts (Alcare, Tokyo, Japan) in fullplantar flexion from just above the knee to the distal foot.Casts were replaced every 2 to 3 days to preventloosening and hindpaw edema. When the immobilizedrats were anesthetized, the age-matched controls(CON group) were also anesthetized to avoid possibleconfounding. Pentobarbital sodium was the onlymedication administered during the study period. Afterthe 4-week immobilization period, casts were removedand animals were allowed to ambulate freely in theircages.Effect of Stretching Exercise on Immobilized Rat Hindlimbs863Stretching exercisesStretching exercises were modified from Inoueet al. (2009). Rats in the CPCP STR group wereanesthetized as above and the bilateral gastrocnemiusmuscles were stretched with a custom-built apparatus(Fig. 1B). The hindlimb was stabilized with hip and kneeextended by taping the foot to the platform, which wasconnected to a movable board attached to a shaft. Theamplitude and frequency of cyclical stretches werecontrolled with a stepping motor. Stretching exerciseswere performed at a frequency of once every 4 s witha range of 40 from maximum dorsiflexion, as measuredwith a goniometer. The cyclical stretching was performedfor 30 min/day, 6 days/week, beginning immediately aftercast removal (prior to reloading) and continuing for2 weeks (12 sessions total).Fig. 1B-F. Schematic diagram andphotos of experimental protocol matoxylin-eosinstaining). (B) Photograph showingapplicationofstretchingexercise.Stretching was performed cyclically in thedirection of plantar and dorsiflexion (inthe range of 40 from maximumdorsiflexion) using a stretch apparatus ata frequency of once every 4 s for30 min/day, 6 days/week. (C) Mechanicalsensitivity of the gastrocnemius musclewas evaluated with a Randall-Selittoapparatus. (D) Mechanical sensitivity ofthe glabrous skin of the hindpaw wasevaluated with von Frey filaments.(E, F) Representative photomicro-graphsof infiltrated muscle fiber (E) andcentrally nucleated muscle fiber (F). Blackand white arrows indicate infiltratedfibers and centrally nucleated fibers,respectively. Scale bar, 100 µm.Behavior testsBehavior tests to assess mechanical sensitivity inthe calf muscle and hindpaw skin were performed beforecast immobilization (baseline), prior to reloadingimmediately after cast removal (Day 0), and on Days 1, 3,5, 7, 10, and 14 after cast removal. The tests were
864Vol. 69Hayashi et al.performed prior to stretching on each testing day. Duringthese tests, rats were wrapped individually in a clothrestrainer because ankle joint contracture prevented thosein the immobilized groups from walking on theirhindlimbs. As shown in Figures 1C and D, the restrainerallowed the animal to dangle safely with the legspositioned to be free and under no loading, as describedby Nakano et al. (2012).A Randall-Selitto analgesiometer (Ugo Basile,Comerio, Italy) equipped with a probe with a 2.6-mm tipdiameter was used to measure the withdrawal thresholdof the right gastrocnemius muscle (Fig. 1C). Use ofa large-diameter probe enabled measurement of thewithdrawal threshold of deep tissue (Nasu et al. 2010).The nociceptive threshold was defined as the force thatinduced a withdrawal response to an increasing pressurestimulus from 0 to 250 g. Measurements were repeatedseven times at 2- to 3-min intervals; the mean value ineach session was taken as the withdrawal threshold.The glabrous skin of the right hindpaw wasprobed six times with 2- and 7-g von Frey filaments(VFFs; North Coast Medical, Morgan Hill, CA, USA) at10-s intervals (Fig. 1D). Lifting or pulling back the pawwas counted as a paw withdrawal response. The 2- and7-g filaments were used to ascertain mechanical allodyniaand mechanical hyperalgesia, respectively (Peleshok andRibeiro-da-Silva 2011). This procedure was performedprior to the Randall-Selitto test on each testing day.Joint contractureDorsiflexion ROM of the bilateral ankle jointswas measured with a goniometer (Inoue et al. 2007).Following the pain behavior tests, the rat wasanesthetized and laid on its side with the knee flexed to90 . The ankle was passively dorsiflexed maximally andthe angle formed by the intersection of the lineconnecting the fifth metatarsal with the malleolus lateralisand that connecting the malleolus lateralis with the centerof the knee joint was measured (0 -180 ).Histological analysisAt the end of the experiment, the rightgastrocnemius muscle of each animal was excised underanesthesia with intraperitoneal pentobarbital sodium(50 mg/kg). The muscles were embedded in an optimalcutting temperature compound (TissueTek ; SakuraFinetek, Tokyo, Japan), quickly frozen by immersion inisopentane precooled in liquid nitrogen, and processed forsectioning on a cryostat (CM1510-11; Leica, Wetzlar,Germany). Serial transverse sections (7 µm) were cutfrom the muscle mid-belly and stained with hematoxylineosin to assess muscle injury. Digital images of thestained sections were acquired with an optical microscope(BZ-9000; Keyence, Osaka, Japan) at 400 magnification(Fig. 1E, F). Five image files were selected witha random number table. Injured muscle fibers weredefined as those displaying infiltration by more than twonucleated inflammatory cells (Fig. 1E) (Koh et al. 2003).Central nuclei were defined as those located more thanone nuclear diameter from the fiber border; myofiberswith central nuclei were termed centrally nucleated fibers(Fig. 1F) (Zschüntzsch et al. 2016). A total of10,000 muscle fibers contained in five images (imagearea, 1.5 1.2 mm) were analyzed with Image J software(National Institutes of Health, Bethesda, MD, USA). Thenumber of infiltrated muscle fibers and the number ofcentrally nucleated fibers per 10,000 fibers were used asindices of muscle injury.Statistical analysisSigma Plot 13 (Systat Software, San Jose, CA,USA) was used for analyses. Because some dependentvariables were not normally distributed according toShapiro-Wilk testing, non-parametric tests were appliedto all variables. The Friedman test was applied tocompare differences in outcome measures betweentimepoints within each group. When a significantdifference was found, a Dunnett’s post hoc test wasperformed to identify a significant difference from thebaseline value. Differences between groups wereanalyzed with the Kruskal-Wallis test followed bya Dunn-Bonferroni post hoc test for all pairwise multiplecomparisons. P 0.05 were considered significant. Graphsplot mean standard error of the mean (SEM), unlessnoted otherwise.ResultsWithdrawal thresholds of gastrocnemius muscleWithdrawal thresholds immediately after castremoval in the CPCP and CPCP STR groups were morethan 20 % lower than baseline values (from 216 to 165 gin CPCP group and from 217 to 158 g in the CPCP STRgroup). These threshold values were significantly lowerthan that of the CON group (P 0.035 vs. CPCP andP 0.013 vs. CPCP STR; Fig. 2). The threshold reductionin the CPCP group was maintained over the 14-day studyperiod and this threshold was always significantly lower
2020than that of the CON group (P 0.002 on Days 1, 3, and10; P 0.001 on Day 5; P 0.004 on Days 7 and 14).Conversely, the threshold reduction observed in theCPCP STR group gradually recovered. By Day 1 aftercast removal, there was no significant difference inEffect of Stretching Exercise on Immobilized Rat Hindlimbs865threshold level between the CPCP STR and CONgroups. The threshold value of the CPCP STR group wassignificantly higher than that of the CPCP group at14 days after cast removal (P 0.036).Fig. 2. Time course of changes inwithdrawal thresholds of gastrocnemius muscle. Horizontal axis indicatesmeasurement time points. Data arepresented as mean SEM (n 5 or 6).* P 0.05 relative to associatedbaseline values; # P 0.05 relative toCON group; † P 0.05 relative to CPCPgroup.Paw-withdrawal responsesThe number of paw-withdrawal responseselicited with 2-g VFFs is presented in Figure 3A. Thenumber of responses after cast removal did notsignificantly differ from the number at baseline in anygroup at any point during the experimental period.However, the number of responses in the CPCP groupwas significantly higher than that in the CON group onDay 5 after cast removal (P 0.044).The number of paw-withdrawal responseselicited with a 7-g VFF is presented in Figure 3B. Thenumber of responses in the CPCP group was significantlyhigher on Days 5 (P 0.001) and 7 (P 0.030) after castremoval compared with the number at baseline and washigher than the number in the CON group on Days 1(P 0.008), 5 (P 0.001), 7 (P 0.002), 10 (P 0.002), and14 (P 0.006) after cast removal. The number ofresponses in the CPCP STR group was slightly butsignificantly increased on Day 5 after cast removalcompared with baseline (P 0.018); however, this valuewas not significantly different than that in theCON group.Range of motion of ankle dorsiflexionThe ROM of bilateral ankle dorsiflexion ispresented in Figures 4A and B. The ROM in bothhindlimbs immediately after cast removal was significantlylower than at baseline in the CPCP and CPCP STR groupsFig. 3. Time course of changes in number of paw-withdrawalresponses. (A) Measurement of mechanical allodynia with 2-gvon Frey filament (VFF). (B) Measurement of mechanicalhyperalgesia with 7-g VFF. Horizontal axis indicates measurementtime points. Data are presented as mean SEM (n 5 or 6).* P 0.05 relative to baseline values; # P 0.05 relative toCON group.
866Vol. 69Hayashi et al.(P 0.001 in both hindlimbs in each group). The ROMgradually recovered over the study period. The ROM in theCPCP group was significantly lower than that in theCON group over the 14-day period (right: P 0.037 on Day0, P 0.003 on Day 1, P 0.004 on Day 3, P 0.001 on Days5, 7, 10, and 14; left: P 0.018 on Day 0, P 0.006 onDay 1, P 0.001 on Days 3, 5, 7, 10, and 14). Conversely,the ROM in the CPCP STR group did not significantlydiffer from than in the CON group on Day 3 or later.central nuclei, we evaluated the number of myofiberswith these findings per 10,000 fibers in each group. Asshown in Figures 5A and B, the number of fibers withinfiltration and the number with central nuclei were bothsignificantly higher in the CPCP group than in theCON group (both P 0.004). Conversely, the number offibers with infiltration and the number with central nucleiin the CPCP STR group did not significantly differ fromnumbers in the CON group.DiscussionFig. 4. Time course of changes in range of motion (ROM) ofankle dorsiflexion. (A) ROM of right ankle dorsiflexion. (B) ROMof left ankle dorsiflexion. Horizontal axis indicates measurementtime points. Data are presented as mean SEM (n 5 or 6).* P 0.05 relative to associated baseline values; # P 0.05 relativeto CON group.Histological observationsThe gastrocnemius muscles of age-matched nonimmobilized control rats (CON group) displayed fewmyofibers with inflammatory infiltration or centralnuclei. Conversely, cellular infiltration and central nucleiwere evident in the immobilized gastrocnemius muscles(CPCP group) at 14 days following cast removal.To assess the effects of stretching exercises onthe number of fibers with inflammatory infiltration andLimb immobilization can cause prolonged jointcontracture, muscle injury, and hyperalgesia, which canaffect quality of life and increase healthcare costs. Thepresent study revealed that cyclic stretching afterhindlimb cast immobilization alleviated hyperalgesia,improved ROM, and limited muscle injury in a rat modelof CPCP.In this study, we used withdrawal responses toevaluate CPCP. Both immobilization groups (CPCP andCPCP STR) had significantly lower pain thresholds onDay 0 after cast removal than at baseline, which confirmspost-immobilization hyperalgesia in our model. However,the group treated with cyclic stretching had rapidamelioration of CPCP, with levels not significantlydifferent from those in the control group by Day 1 aftercast removal. Conversely, the CPCP group that was nottreated with cyclic stretching had persistently low painthresholds throughout the 2-week study period. Theseresults are consistent with those of Morimoto et al.(2013), who reported that stretching ameliorated longlasting hyperalgesia, joint limitation, and muscle atrophyinduced by cast immobilization in rats. However, ourstudy differed from that of Morimoto in the followingrespects. First, rats in the present study had a 4-weekperiod of bilateral immobilization from just above theknee to the distal paw, whereas the previous studyapplied 2 weeks of unilateral immobilization from thetrunk to the mid-hindpaw. Second, the present study usedcyclic stretching applied six times/week for 2 weekswhereas the previous study used static stretching appliedthree times/week for 2 weeks. In a preliminaryunpublished study, we compared the effects of staticversus cyclic stretching on muscle atrophy (fiber crosssectional area) and injury (necrotic fiber number) afterimmobilization (Supplementary Methods section andSupplementary Tables 1 and 2). We found that cyclicstretching was superior to static stretching in ameliorating
2020these conditions. Finally, stretching in the present studywas initiated on the day of cast removal, before reloading,whereas stretching was initiated on Day 3 after castremoval in the study of Morimoto et al. (2013). The veryEffect of Stretching Exercise on Immobilized Rat Hindlimbs867early application of passive stretching resulted insignificant amelioration in CPCP within 1 day of castremoval in the present study.Fig. 5. Effects of stretching exerciseson number of muscle fibers withinflammatory infiltration and centralnuclei. Histological findings wereconfirmed with quantitative analysiscomparingage-matchednaïvecontrols (CON, n 5), CPCP ratswithout cyclic stretching exercise(CPCP, n 6), and CPCP rats withcyclic stretching exercise (CPCP STR,n 6). (A) Number of infiltratedmuscle fibers. (B) Number of centrallynucleated fibers. Values are expressedas box-and-whisker plots (highest,third quartile, median, first quartile,and lowest values). Dotted linesindicate mean values. # P 0.05relative to CON group.Joint contracture occurs during immobilizationbecause of structural alterations, including musclefibrosis and joint capsule changes (Wong et al. 2015).Studies have reported conflicting evidence regarding theefficacy of stretching in the treatment of immobilizationinduced joint contracture. Several studies in animalmodels have found that stretching significantly improvesjoint ROM after immobilization (Inoue et al. 2007,Morimoto et al. 2013). However, a recent systematicreview of 18 studies found that stretching did not haveclinically important effects on joint contracture caused byvarious etiologies (Harvey et al. 2017). The presentresults support the efficacy of cyclic stretching inincreasing the ROM of joints with immobilizationinduced contracture.In the present study, we used the presence ofcentral nuclei and inflammatory cells within myofibers asmarkers of muscle injury. We found higher numbers ofinfiltrated and centrally nucleated muscle fibers in thegastrocnemius muscles of rats who underwent a 4-weekimmobilization period than in control rats. Central nucleiare a sign of muscle repair and are seen in various typesof muscular dystrophy and after muscle injury (Folkerand Baylies 2013). The calf muscles of CPCP rats showdisuse atrophy (Inoue et al. 2007); reloading of muscleswith disuse atrophy induces inflammatory changes(Frenette et al. 2002). Therefore, the muscle injury in thepresent study may have resulted from reloading of theatrophic calf muscle. We found that early uatedimmobilization-induced muscle injury. This finding isconsistent with that of Inoue et al. (2009), whodemonstrated that stretching exercises performed soonafter cast removal in rats decreased muscle injury(assessed based on inflammatory infiltration and heatshock proteins) in the cast-immobilized hindlimb.Similarly, Gomes et al. (2007) demonstrated thatstretching exercises protected rat gastrocnemius musclesfrom atrophy and muscle damage during disuse.Although the relationship between muscle injury andCPCP is not clear, our finding that stretching decreasedmuscle injury and alleviated pain suggests that muscledamage may play a role in the development of CPCP.Further studies are needed to clarify this relationship.This study has several limitations. First, it didnot investigate the epidermis, spinal plasticity, oroxidative stress. Second, muscle injury was assessed withtwo parameters on hematoxylin-eosin staining only.Evaluation of additional histopathologic and systemicparameters could enhance our understanding of theeffects of stretching on CPCP. Further detailedinvestigation of these aspects will be useful to elucidatethe mechanisms by which stretching exercises decreasethe pain associated with cast immobilization. In addition,Schwann cells and muscle spindles could also bepotential targets for exploring the mechanisms.In conclusion, early implementation of cyclicstretching exercises ameliorated cutaneous and muscular
868Vol. 69Hayashi et al.mechanical hyperalgesia, joint contracture, andimmobilization-induced muscle injury in a rat model ofCPCP. Stretching exercises may decrease long-lastinghyperalgesia in patients undergoing rehabilitationfollowing cast immobilization.Conflict of InterestThere is no conflict of interest.AcknowledgementsThe authors are grateful to Yuji Takahashi (ShowaUniversity Koto Toyosu Hospital, Japan) for technicalassistance in performing the experiments. This work wassupported by JSPS KAKENHI Grant Number 22500455from the Japan Society for the Promotion of Science. Wethank Rebecca Tollefson, DVM, from Edanz Group(https://en-author-services.edanzgroup.com/) for editinga draft of this manuscript.ReferencesALLEN G, GALER BS, SCHWARTZ L: Epidemiology of complex regional pain syndrome: a retrospective chartreview of 134 patients. Pain 80: 539-544, 1999. https://doi.org/10.1016/s0304-3959(98)00246-2COREY SM, VIZZARD MA, BOUFFARD NA, BADGER GJ, LANGEVIN HM: Stretching of the back improves gait,mechanical sensitivity and connective tissue inflammation in a rodent model. PLoS One 7: e29831, OLKER E, BAYLIES M: Nuclear positioning in muscle development and disease. Front Physiol 363: 4, TTE J, ST-PIERRE M, CÔTÉ CH, MYLONA E, PIZZA FX: Muscle impairment occurs rapidly and precedesinflammatory cell accumulation after mechanical loading. Am J Physiol Regul Integr Comp Physiol 282:R351-R357, 2002. https://doi.org/10.1152/ajpregu.00189.2001GOMES AR, CORNACHIONE A, SALVINI TF, MATTIELLO-SVERZUT AC: Morphological effects of twoprotocols of passive stretch over the immobilized rat soleus muscle. J Anat 210: 328-335, 7.xHAMAUE Y, NAKANO J, SEKINO Y, CHUGANJI S, SAKAMOTO J, YOSHIMURA T, OKITA M, ORIGUCHI T:Effects of vibration therapy on immobilization-induced hypersensitivity in rats. Phys Ther 95: 1015-1026,2015. https://doi.org/10.2522/ptj.20140137HARVEY LA, KATALINIC OM, HERBERT RD, MOSELEY AM, LANNIN NA, SCHURR K: Stretch for the treatmentand prevention of contracture: an abridged republication of a Cochrane systematic review. J Physiother 63: 67-75,2017. https://doi.org/10.1016/j.jphys.2017.02.014HONDA Y, SAKAMOTO J, NAKANO J, KATAOKA H, SASABE R, GOTO K, TANAKA M, ORIGUCHI T,YOSHIMURA T, OKITA M: Upregulation of interleukin-1β/transforming growth factor-β1 and hypoxia relateto molecular mechanisms underlying immobilization-induced muscle contracture. Muscle Nerve 52: 419-427,2015. https://doi.org/10.1002/mus.24558HONDA Y, TANAKA M, TANAKA N, SASABE R, GOTO K, KATAOKA H, SAKAMOTO J, NAKANO J, OKITAM: Relationship between extensibility and collagen expression in immobilized rat skeletal muscle. MuscleNerve 57: 672-678, 2018. https://doi.org/10.1002/mus.26011INOUE T, OKITA M, TAKAHASHI Y, HARADA Y, SUZUKI S: Effect of intermittent stretching on limitation ofankle joint mobility and disuse muscle atrophy in immobilized rat soleus muscle. (In Japanese) RigakuRyōhōgaku 34: 1-9, 2007.INOUE T, SUZUKI S, HAGIWARA R, IWATA M, BANNO Y, OKITA M: Effects of passive stretching on muscleinjury and HSP expression during recovery after immobilization in rats. Pathobiology 76: 253-259, 2009.https://doi.org/10.1159/000228901KANEGUCHI A, OZAWA J, YAMAOKA K: Intra-articular injection of mitomycin C prevents progression ofimmobilization-induced arthrogenic contracture in the remobilized rat knee. Physiol Res 69: 145-156, 2020.https://doi.org/10.33549/physiolres.934149
2020Effect of Stretching Exercise on Immobilized Rat Hindlimbs869KATAOKA H, NAKANO J, MORIMOTO Y, HONDA Y, SAKAMOTO J, ORIGUCHI T, OKITA M, YOSHIMURA T:Hyperglycemia inhibits recovery from disuse-induced skeletal muscle atrophy in rats. Physiol Res 63: 465-474,2014.KOH TJ, PETERSON JM, PIZZA FX, BROOKS SV: Passive stretches protect skeletal muscle of adult and old micefrom lengthening contraction-induced injury. J Gerontol A Biol Sci Med Sci 58: 592-597, WA T, TANAKA M, KANAZASHI M, MAESHIGE N, KONDO H, ISHIHARA A, FUJINO H: Astaxanthinsupplementation attenuates immobilization-induced skeletal muscle fibrosis via suppression of oxidative stress.J Physiol Sci 67: 603-611, 2017. https://doi.org/10.1007/s12576-016-0492-xMATSUMOTO Y, NAKANO J, OGA S, KATAOKA H, HONDA Y, SAKAMOTO J, OKITA M: The non-thermaleffects of pulsed ultrasound irradiation on the development of disuse muscle atrophy in rat gastrocnemiusmuscle. Ultrasound Med Biol 40: 1578-1586, 2014. MORIMOTO A, WINAGA H, SAKURAI H, OHMICHI M, YOSHIMOTO T, OHMICHI Y, MATSUI T, USHIDA T,OKADA T, SATO J: Treadmill running and static stretching improve long-lasting hyperalgesia, jointlimitation, and muscle atrophy induced by cast immobilization in rats. Neurosci Lett 534: 295-300, AKABAYASHI K, SAKAMOTO J, KATAOKA H, KONDO Y, HAMAUE Y, HONDA Y, NAKANO J, OKITA M:Effect of continuous passive motion initiated after the onset of arthritis on inflammation and secondaryhyperalgesia in rats. Physiol Res 65: 683-691, 2016. https://doi.org/10.33549/physiolres.933214NAKAGAWA T
862 Hayashi et al. Vol. 69 et al. 2014) and 4 weeks (Matsumoto 2014) of et al. immobilization. Other studies have shown that cast immobilization induces muscle fibrosis, which contributes to limb contracture (Honda 2015, et a
INDEX PRESENTATION 5 THE THUMB 7 MECHANICAL EXERCISES 8 SECTION 1 THUMB Exercise 1 12 Exercise 2 13 Exercise 3 - 4 14 Exercise 5 15 Estudio 1 16 SECTION 2 THUMB WITH JUMPS Exercise 6 17 Exercise 7 - 8 18 Exercise 9 19 Exercise 10 20 Exercise 11 - 12 21 Estudio 6 22 SECTION 3 GOLPE Exercise 13 23 Exercise 14 24 Exercise 15 25 Exercise 16 - 17 26 Exercise 18 27 .
Chapter 1 Exercise Solutions Exercise 1.1 Exercise 1.2 Exercise 1.3 Exercise 1.4 Exercise 1.5 Exercise 1.6 Exercise 1.7 Exercise 1.8 Exercise 1.9 Exercise 1.10 Exercise 1.11 Exercise 1.12 Fawwaz T. Ulaby and Umberto Ravaioli, Fundamentals of Applied Electromagnetics c 2019 Prentice Hall
PNF stretching utilizes static stretching and isometric contractions of the target muscle (TM) in a consecutive style. Static and PNF stretching are preferred to improve flexibility, while dynamic stretching good for warm-up (Costa et al., 2014; D. Medeiros & Martini, 2017). PNF is
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Stretching Manual Author’s Choice “Best Pick” Aaron Mattes Active Isolated Stretching (AIS) The Active Isolated Stretching (AIS) method of muscle lengthening and fascial release is a type of Athletic Stretching Technique that provides effective, dynamic, facilitated stretching of
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Basic homological complexes 9 2. H-unitality and excision 14 3. Homology of di erential graded algebras 16 4. Cyclic cohomology 16 5. The Hochschild cochain complex 17 . Introduction 49 2. Action of the Lie algebra cochain complex of C (A;A) 49 3. Rigidity of periodic cyclic homology 51 4. Construction of cyclic cocycles 53 5. The .
5.3 Cyclic Voltammetry of Ferrocene Carboxylic Acid 5.3.1 Switch the current range to 10 µA. 5.3.2 From the techniques menu select Cyclic Voltammetry. This opens the Staircase Cyclic Voltammetry dialog box, which is used to set the limits and ramp rate of the voltage waveform applied to the working electrode. In the dialog box, select the .
