Research ArticlePhysiology of Thermal Therapy

Heat therapy improves body composition and muscle function but does not affect capillary or collateral growth in a model of obesity and hindlimb ischemia

REFERENCES

  • 1. Lee AJ, Price JF, Russell MJ, Smith FB, van Wijk MC, Fowkes FG. Improved prediction of fatal myocardial infarction using the ankle brachial index in addition to conventional risk factors: the Edinburgh Artery Study. Circulation 110: 3075–3080, 2004. doi:10.1161/01.CIR.0000143102.38256.DE.
    Crossref | PubMed | Web of Science | Google Scholar
  • 2. Sampson UK, Fowkes FG, McDermott MM, Criqui MH, Aboyans V, Norman PE, Forouzanfar MH, Naghavi M, Song Y, Harrell FE Jr., Denenberg JO, Mensah GA, Ezzati M, Murray C. Global and regional burden of death and disability from peripheral artery disease: 21 world regions, 1990 to 2010. Glob Heart 9: 145–158, 2014. e121. doi:10.1016/j.gheart.2013.12.008.
    Crossref | PubMed | Google Scholar
  • 3. Fowkes FG, Aboyans V, Fowkes FJ, McDermott MM, Sampson UK, Criqui MH. Peripheral artery disease: epidemiology and global perspectives. Nat Rev Cardiol 14: 156–170, 2017. doi:10.1038/nrcardio.2016.179.
    Crossref | PubMed | Web of Science | Google Scholar
  • 4. Belch J, MacCuish A, Campbell I, Cobbe S, Taylor R, Prescott R, Lee R, Bancroft J, MacEwan S, Shepherd J, Macfarlane P, Morris A, Jung R, Kelly C, Connacher A, Peden N, Jamieson A, Matthews D, Leese G, McKnight J, O’Brien I, Semple C, Petrie J, Gordon D, Pringle S, MacWalter R, Prevention of Progression of Arterial Disease and Diabetes Study Group; Diabetes Registry Group; Royal College of Physicians Edinburgh. The prevention of progression of arterial disease and diabetes (POPADAD) trial: factorial randomised placebo controlled trial of aspirin and antioxidants in patients with diabetes and asymptomatic peripheral arterial disease. BMJ 337: a1840, 2008. doi:10.1136/bmj.a1840.
    Crossref | PubMed | Google Scholar
  • 5. Low Wang CC, Blomster JI, Heizer G, Berger JS, Baumgartner I, Fowkes FGR, Held P, Katona BG, Norgren L, Jones WS, Lopes RD, Olin JW, Rockhold FW, Mahaffey KW, Patel MR, Hiatt WR, EUCLID Trial Executive Committee ETE and Investigators. Cardiovascular and Limb Outcomes in Patients With Diabetes and Peripheral Artery Disease: The EUCLID Trial. J Am Coll Cardiol 72: 3274–3284, 2018. doi:10.1016/j.jacc.2018.09.078.
    Crossref | PubMed | Web of Science | Google Scholar
  • 6. Collins TC, Lunos S, Carlson T, Henderson K, Lightbourne M, Nelson B, Hodges JS. Effects of a home-based walking intervention on mobility and quality of life in people with diabetes and peripheral arterial disease: a randomized controlled trial. Diabetes Care 34: 2174–2179, 2011. doi:10.2337/dc10-2399.
    Crossref | PubMed | Web of Science | Google Scholar
  • 7. Gardner AW, Parker DE, Montgomery PS, Blevins SM. Diabetic women are poor responders to exercise rehabilitation in the treatment of claudication. J Vasc Surg 59: 1036–1043, 2014. doi:10.1016/j.jvs.2013.10.058.
    Crossref | PubMed | Web of Science | Google Scholar
  • 8. DeRubertis BG, Pierce M, Ryer EJ, Trocciola S, Kent KC, Faries PL. Reduced primary patency rate in diabetic patients after percutaneous intervention results from more frequent presentation with limb-threatening ischemia. J Vasc Surg 47: 101–108, 2008. doi:10.1016/j.jvs.2007.09.018.
    Crossref | PubMed | Web of Science | Google Scholar
  • 9. Malmstedt J, Leander K, Wahlberg E, Karlström L, Alfredsson L, Swedenborg J. Outcome after leg bypass surgery for critical limb ischemia is poor in patients with diabetes: a population-based cohort study. Diabetes Care 31: 887–892, 2008. doi:10.2337/dc07-2424.
    Crossref | PubMed | Web of Science | Google Scholar
  • 10. Regensteiner JG, Hiatt WR, Coll JR, Criqui MH, Treat-Jacobson D, McDermott MM, Hirsch AT. The impact of peripheral arterial disease on health-related quality of life in the Peripheral Arterial Disease Awareness, Risk, and Treatment: New Resources for Survival (PARTNERS) Program. Vasc Med 13: 15–24, 2008. doi:10.1177/1358863X07084911.
    Crossref | PubMed | Web of Science | Google Scholar
  • 11. Garg PK, Liu K, Tian L, Guralnik JM, Ferrucci L, Criqui MH, Tan J, McDermott MM. Physical activity during daily life and functional decline in peripheral arterial disease. Circulation 119: 251–260, 2009. doi:10.1161/CIRCULATIONAHA.108.791491.
    Crossref | PubMed | Web of Science | Google Scholar
  • 12. Garg PK, Tian L, Criqui MH, Liu K, Ferrucci L, Guralnik JM, Tan J, McDermott MM. Physical activity during daily life and mortality in patients with peripheral arterial disease. Circulation 114: 242–248, 2006. doi:10.1161/CIRCULATIONAHA.105.605246.
    Crossref | PubMed | Web of Science | Google Scholar
  • 13. Hiatt WR, Armstrong EJ, Larson CJ, Brass EP. Pathogenesis of the limb manifestations and exercise limitations in peripheral artery disease. Circ Res 116: 1527–1539, 2015. doi:10.1161/CIRCRESAHA.116.303566.
    Crossref | PubMed | Web of Science | Google Scholar
  • 14. Askew CD, Green S, Walker PJ, Kerr GK, Green AA, Williams AD, Febbraio MA. Skeletal muscle phenotype is associated with exercise tolerance in patients with peripheral arterial disease. J Vasc Surg 41: 802–807, 2005. doi:10.1016/j.jvs.2005.01.037.
    Crossref | PubMed | Web of Science | Google Scholar
  • 15. Regensteiner JG, Wolfel EE, Brass EP, Carry MR, Ringel SP, Hargarten ME, Stamm ER, Hiatt WR. Chronic changes in skeletal muscle histology and function in peripheral arterial disease. Circulation 87: 413–421, 1993. doi:10.1161/01.CIR.87.2.413.
    Crossref | PubMed | Web of Science | Google Scholar
  • 16. Herman SD, Liu K, Tian L, Guralnik JM, Ferrucci L, Criqui MH, Liao Y, McDermott MM. Baseline lower extremity strength and subsequent decline in functional performance at 6-year follow-up in persons with lower extremity peripheral arterial disease. J Am Geriatr Soc 57: 2246–2252, 2009. doi:10.1111/j.1532-5415.2009.02562.x.
    Crossref | PubMed | Web of Science | Google Scholar
  • 17. McDermott MM, Ferrucci L, Guralnik J, Tian L, Liu K, Hoff F, Liao Y, Criqui MH. Pathophysiological changes in calf muscle predict mobility loss at 2-year follow-up in men and women with peripheral arterial disease. Circulation 120: 1048–1055, 2009. doi:10.1161/CIRCULATIONAHA.108.842328.
    Crossref | PubMed | Web of Science | Google Scholar
  • 18. McDermott MM, Liu K, Tian L, Guralnik JM, Criqui MH, Liao Y, Ferrucci L. Calf muscle characteristics, strength measures, and mortality in peripheral arterial disease: a longitudinal study. J Am Coll Cardiol 59: 1159–1167, 2012. doi:10.1016/j.jacc.2011.12.019.
    Crossref | PubMed | Web of Science | Google Scholar
  • 19. Singh N, Liu K, Tian L, Criqui MH, Guralnik JM, Ferrucci L, Liao Y, McDermott MM. Leg strength predicts mortality in men but not in women with peripheral arterial disease. J Vasc Surg 52: 624–631, 2010. doi:10.1016/j.jvs.2010.03.066.
    Crossref | PubMed | Web of Science | Google Scholar
  • 20. Akasaki Y, Miyata M, Eto H, Shirasawa T, Hamada N, Ikeda Y, Biro S, Otsuji Y, Tei C. Repeated thermal therapy up-regulates endothelial nitric oxide synthase and augments angiogenesis in a mouse model of hindlimb ischemia. Circ J 70: 463–470, 2006. doi:10.1253/circj.70.463.
    Crossref | PubMed | Web of Science | Google Scholar
  • 21. Kim K, Reid BA, Ro B, Casey CA, Song Q, Kuang S, Roseguini BT. Heat therapy improves soleus muscle force in a model of ischemia-induced muscle damage. J Appl Physiol 127: 215–228, 2019. doi:10.1152/japplphysiol.00115.2019.
    Link | Web of Science | Google Scholar
  • 22. Archer AE, Rogers RS, Von Schulze AT, Wheatley JL, Morris EM, McCoin CS, Thyfault JP, Geiger PC. Heat shock protein 72 regulates hepatic lipid accumulation. Am Physiol Regul Integr Comp Physiol 315: R696–R707, 2018. doi:10.1152/ajpregu.00073.2018.
    Link | Web of Science | Google Scholar
  • 23. Chung J, Nguyen AK, Henstridge DC, Holmes AG, Chan MH, Mesa JL, Lancaster GI, Southgate RJ, Bruce CR, Duffy SJ, Horvath I, Mestril R, Watt MJ, Hooper PL, Kingwell BA, Vigh L, Hevener A, Febbraio MA. HSP72 protects against obesity-induced insulin resistance. Proc Natil Acad Sci USA 105: 1739–1744, 2008. doi:10.1073/pnas.0705799105.
    Crossref | PubMed | Web of Science | Google Scholar
  • 24. Gupte AA, Bomhoff GL, Swerdlow RH, Geiger PC. Heat treatment improves glucose tolerance and prevents skeletal muscle insulin resistance in rats fed a high-fat diet. Diabetes 58: 567–578, 2009. doi:10.2337/db08-1070.
    Crossref | PubMed | Web of Science | Google Scholar
  • 25. Kokura S, Adachi S, Manabe E, Mizushima K, Hattori T, Okuda T, Nakabe N, Handa O, Takagi T, Naito Y, Yoshida N, Yoshikawa T. Whole body hyperthermia improves obesity-induced insulin resistance in diabetic mice. Int J Hyperthermia 23: 259–265, 2007. doi:10.1080/02656730601176824.
    Crossref | PubMed | Web of Science | Google Scholar
  • 26. Rogers RS, Morris EM, Wheatley JL, Archer AE, McCoin CS, White KS, Wilson DR, Meers GM, Koch LG, Britton SL, Thyfault JP, Geiger PC. Deficiency in the heat stress response could underlie susceptibility to metabolic disease. Diabetes 65: 3341–3351, 2016. doi:10.2337/db16-0292.
    Crossref | PubMed | Web of Science | Google Scholar
  • 27. DiStasi MR, Mund JA, Bohlen HG, Miller SJ, Ingram DA, Dalsing MC, Unthank JL. Impaired compensation to femoral artery ligation in diet-induced obese mice is primarily mediated via suppression of collateral growth by Nox2 and p47phox. Am J Physiology Heart Circ Physiol 309: H1207–H1217, 2015. doi:10.1152/ajpheart.00180.2015.
    Link | Web of Science | Google Scholar
  • 28. Ryan TE, Schmidt CA, Green TD, Spangenburg EE, Neufer PD, McClung JM. Targeted expression of catalase to mitochondria protects against ischemic myopathy in high-fat diet-fed mice. Diabetes 65: 2553–2568, 2016. doi:10.2337/db16-0387.
    Crossref | PubMed | Web of Science | Google Scholar
  • 29. Eshima H, Tamura Y, Kakehi S, Kurebayashi N, Murayama T, Nakamura K, Kakigi R, Okada T, Sakurai T, Kawamori R, Watada H. Long-term, but not short-term high-fat diet induces fiber composition changes and impaired contractile force in mouse fast-twitch skeletal muscle. Physiol Rep 5: e13250, 2017. doi:10.14814/phy2.13250.
    Crossref | Web of Science | Google Scholar
  • 30. Tallis J, Hill C, James RS, Cox VM, Seebacher F. The effect of obesity on the contractile performance of isolated mouse soleus, EDL, and diaphragm muscles. J Appl Physiol 122: 170–181, 2017. doi:10.1152/japplphysiol.00836.2016.
    Link | Web of Science | Google Scholar
  • 31. D’Souza DM, Trajcevski KE, Al-Sajee D, Wang DC, Thomas M, Anderson JE, Hawke TJ. Diet-induced obesity impairs muscle satellite cell activation and muscle repair through alterations in hepatocyte growth factor signaling. Physiol Rep 3: e12506, 2015. doi:10.14814/phy2.12506.
    Crossref | Google Scholar
  • 32. Fu X, Zhu M, Zhang S, Foretz M, Viollet B, Du M. Obesity impairs skeletal muscle regeneration through inhibition of AMPK. Diabetes 65: 188–200, 2016.
    Crossref | PubMed | Web of Science | Google Scholar
  • 33. Brown LA, Lee DE, Patton JF, Perry RA Jr, Brown JL, Baum JI, Smith-Blair N, Greene NP, Washington TA. Diet-induced obesity alters anabolic signalling in mice at the onset of skeletal muscle regeneration. Acta Physiol 215: 46–57, 2015. doi:10.1111/apha.12537.
    Crossref | Web of Science | Google Scholar
  • 34. Hesketh K, Shepherd SO, Strauss JA, Low DA, Cooper RJ, Wagenmakers AJM, Cocks M. Passive heat therapy in sedentary humans increases skeletal muscle capillarization and eNOS content but not mitochondrial density or GLUT4 content. Am J Physiol Heart Circ Physiol 317: H114–H123, 2019. doi:10.1152/ajpheart.00816.2018.
    Link | Web of Science | Google Scholar
  • 35. Kim K, Reid BA, Casey CA, Bender BE, Ro B, Song Q, Trewin AJ, Petersen AC, Kuang S, Gavin TP, Roseguini BT. Effects of repeated local heat therapy on skeletal muscle structure and function in humans. J Appl Physiol (1985) 128: 483–492, 2020. doi:10.1152/japplphysiol.00701.2019.
    Link | Web of Science | Google Scholar
  • 36. Hafen PS, Abbott K, Bowden J, Lopiano R, Hancock CR, Hyldahl RD. Daily heat treatment maintains mitochondrial function and attenuates atrophy in human skeletal muscle subjected to immobilization. J Appl Physiol 127: 47–57, 2019. doi:10.1152/japplphysiol.01098.2018.
    Link | Web of Science | Google Scholar
  • 37. Hafen PS, Preece CN, Sorensen JR, Hancock CR, Hyldahl RD. Repeated exposure to heat stress induces mitochondrial adaptation in human skeletal muscle. J Appl Physiol (1985) 125: 1447–1455, 2018. doi:10.1152/japplphysiol.00383.2018.
    Link | Web of Science | Google Scholar
  • 38. Tamura Y, Matsunaga Y, Masuda H, Takahashi Y, Takahashi Y, Terada S, Hoshino D, Hatta H. Postexercise whole body heat stress additively enhances endurance training-induced mitochondrial adaptations in mouse skeletal muscle. Am J Physiol Regul Integr Comp Physiol 307: R931–R943, 2014. doi:10.1152/ajpregu.00525.2013.
    Link | Web of Science | Google Scholar
  • 39. Distasi MR, Case J, Ziegler MA, Dinauer MC, Yoder MC, Haneline LS, Dalsing MC, Miller SJ, Labarrere CA, Murphy MP, Ingram DA, Unthank JL. Suppressed hindlimb perfusion in Rac2-/- and Nox2-/- mice does not result from impaired collateral growth. Am J Physiol Heart Circ Physiology 296: H877–H886, 2009. doi:10.1152/ajpheart.00772.2008.
    Link | Web of Science | Google Scholar
  • 40. Hoefer IE, van Royen N, Rectenwald JE, Bray EJ, Abouhamze Z, Moldawer LL, Voskuil M, Piek JJ, Buschmann IR, Ozaki CK. Direct evidence for tumor necrosis factor-alpha signaling in arteriogenesis. Circulation 105: 1639–1641, 2002. doi:10.1161/01.CIR.0000014987.32865.8E.
    Crossref | PubMed | Web of Science | Google Scholar
  • 41. Mees B, Wagner S, Ninci E, Tribulova S, Martin S, van Haperen R, Kostin S, Heil M, de Crom R, Schaper W. Endothelial nitric oxide synthase activity is essential for vasodilation during blood flow recovery but not for arteriogenesis. Arterioscler Thromb Vasc Biol 27: 1926–1933, 2007. [Erratum in Arterioscler Thromb Vasc Biol. 2013 Mar;33(3):e102]. doi:10.1161/ATVBAHA.107.145375.
    Crossref | PubMed | Web of Science | Google Scholar
  • 42. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31: 1116–1128, 2006. doi:10.1016/j.neuroimage.2006.01.015.
    Crossref | PubMed | Web of Science | Google Scholar
  • 43. Goto A, Egawa T, Sakon I, Oshima R, Ito K, Serizawa Y, Sekine K, Tsuda S, Goto K, Hayashi T. Heat stress acutely activates insulin-independent glucose transport and 5'-AMP-activated protein kinase prior to an increase in HSP72 protein in rat skeletal muscle. Physiol Rep 3: e12601, 2015. doi:10.14814/phy2.12601.
    Crossref | PubMed | Google Scholar
  • 44. Miyauchi T, Miyata M, Ikeda Y, Akasaki Y, Hamada N, Shirasawa T, Furusho Y, Tei C. Waon therapy upregulates Hsp90 and leads to angiogenesis through the Akt-endothelial nitric oxide synthase pathway in mouse hindlimb ischemia. Circ J 76: 1712–1721, 2012. doi:10.1253/circj.CJ-11-0915. doi:10.1253/circj.cj-11-0915.
    Crossref | PubMed | Web of Science | Google Scholar
  • 45. Nwadozi E, Rudnicki M, De Ciantis M, Milkovich S, Pulbere A, Roudier E, Birot O, Gustafsson T, Ellis CG, Haas TL. High-fat diet pre-conditioning improves microvascular remodelling during regeneration of ischaemic mouse skeletal muscle. Acta Physiol 229: e13449, 2020. doi:10.1111/apha.13449.
    Crossref | Web of Science | Google Scholar
  • 46. Thomas MM, Trajcevski KE, Coleman SK, Jiang M, Di Michele J, O’Neill HM, Lally JS, Steinberg GR, Hawke TJ. Early oxidative shifts in mouse skeletal muscle morphology with high-fat diet consumption do not lead to functional improvements. Physiol Rep 2: e12149, 2014. doi:10.14814/phy2.12149.
    Crossref | Google Scholar
  • 47. Ziegler MA, Distasi MR, Bills RG, Miller SJ, Alloosh M, Murphy MP, Akingba AG, Sturek M, Dalsing MC, Unthank JL. Marvels, mysteries, and misconceptions of vascular compensation to peripheral artery occlusion. Microcirculation 17: 3–20, 2010. doi:10.1111/j.1549-8719.2010.00008.x.
    Crossref | PubMed | Web of Science | Google Scholar
  • 48. Roberts KC, Nixon C, Unthank JL, Lash JM. Femoral artery ligation stimulates capillary growth and limits training-induced increases in oxidative capacity in rats. Microcirculation 4: 253–260, 1997. doi:10.3109/10739689709146788.
    Crossref | PubMed | Web of Science | Google Scholar
  • 49. Arpino JM, Nong Z, Li F, Yin H, Ghonaim N, Milkovich S, Balint B, O’Neil C, Fraser GM, Goldman D, Ellis CG, Pickering JG. Four-dimensional microvascular analysis reveals that regenerative angiogenesis in ischemic muscle produces a flawed microcirculation. Circ Res 120: 1453–1465, 2017. doi:10.1161/CIRCRESAHA.116.310535.
    Crossref | PubMed | Web of Science | Google Scholar
  • 50. Helisch A, Wagner S, Khan N, Drinane M, Wolfram S, Heil M, Ziegelhoeffer T, Brandt U, Pearlman JD, Swartz HM, Schaper W. Impact of mouse strain differences in innate hindlimb collateral vasculature. ATVB 26: 520–526, 2006. doi:10.1161/01.ATV.0000202677.55012.a0.
    Crossref | Web of Science | Google Scholar
  • 51. Eshima H, Tamura Y, Kakehi S, Kakigi R, Hashimoto R, Funai K, Kawamori R, Watada H. A chronic high-fat diet exacerbates contractile dysfunction with impaired intracellular Ca(2+) release capacity in the skeletal muscle of aged mice. J Appl Physiol 128: 1153–1162, 2020. doi:10.1152/japplphysiol.00530.2019.
    Link | Web of Science | Google Scholar
  • 52. Geiger PC, Gupte AA. Heat shock proteins are important mediators of skeletal muscle insulin sensitivity. Exerc Sport Sci Rev 39: 34–42, 2011. doi:10.1097/JES.0b013e318201f236.
    Crossref | PubMed | Web of Science | Google Scholar
  • 53. Harris MB, Blackstone MA, Ju H, Venema VJ, Venema RC. Heat-induced increases in endothelial NO synthase expression and activity and endothelial NO release. Am J Physiol Heart Circ Physiol 285: H333–H340, 2003. doi:10.1152/ajpheart.00726.2002.
    Link | Web of Science | Google Scholar
  • 54. Ives SJ, Andtbacka RH, Kwon SH, Shiu YT, Ruan T, Noyes RD, Zhang QJ, Symons JD, Richardson RS. Heat and alpha1-adrenergic responsiveness in human skeletal muscle feed arteries: the role of nitric oxide. J Appl Physiol 113: 1690–1698, 2012. doi:10.1152/japplphysiol.00955.2012.
    Link | Web of Science | Google Scholar
  • 55. Ikeda Y, Biro S, Kamogawa Y, Yoshifuku S, Eto H, Orihara K, Kihara T, Tei C. Repeated thermal therapy upregulates arterial endothelial nitric oxide synthase expression in Syrian golden hamsters. Jpn Circ J 65: 434–438, 2001. doi:10.1253/jcj.65.434.
    Crossref | PubMed | Google Scholar
  • 56. Frisbee JC. Reduced nitric oxide bioavailability contributes to skeletal muscle microvessel rarefaction in the metabolic syndrome. Am J Physiol Regul Integr Comp Physiol 289: R307–R316, 2005. doi:10.1152/ajpregu.00114.2005.
    Link | Web of Science | Google Scholar
  • 57. Yan J, Tie G, Park B, Yan Y, Nowicki PT, Messina LM. Recovery from hind limb ischemia is less effective in type 2 than in type 1 diabetic mice: roles of endothelial nitric oxide synthase and endothelial progenitor cells. J Vasc Surg 50: 1412–1422, 2009. doi:10.1016/j.jvs.2009.08.007.
    Crossref | PubMed | Web of Science | Google Scholar
  • 58. Hoefer IE, van Royen N, Jost MM. Experimental models of arteriogenesis: differences and implications. Lab Anim 35: 36–44, 2006. . doi:10.1038/laban0206-36.
    Crossref | Web of Science | Google Scholar
  • 59. Carter HH, Spence AL, Atkinson CL, Pugh CJ, Naylor LH, Green DJ. Repeated core temperature elevation induces conduit artery adaptation in humans. Eur J Appl Physiol 114: 859–865, 2014. doi:10.1007/s00421-013-2817-2.
    Crossref | PubMed | Web of Science | Google Scholar
  • 60. Green DJ, Carter HH, Fitzsimons MG, Cable NT, Thijssen DH, Naylor LH. Obligatory role of hyperaemia and shear stress in microvascular adaptation to repeated heating in humans. J Physiol 588: 1571–1577, 2010. doi:10.1113/jphysiol.2010.186965.
    Crossref | PubMed | Web of Science | Google Scholar
  • 61. Naylor LH, Carter H, FitzSimons MG, Cable NT, Thijssen DH, Green DJ. Repeated increases in blood flow, independent of exercise, enhance conduit artery vasodilator function in humans. Am J Physiol Heart Circ Physiol 300: H664–H669, 2011. doi:10.1152/ajpheart.00985.2010.
    Link | Web of Science | Google Scholar
  • 62. Schaper W. Collateral circulation: past and present. Basic Res Cardiol 104: 5–21, 2009. doi:10.1007/s00395-008-0760-x.
    Crossref | PubMed | Web of Science | Google Scholar
  • 63. Yang HT, Laughlin MH, Terjung RL. Prior exercise training increases collateral-dependent blood flow in rats after acute femoral artery occlusion. Am J Physiol Heart Circ Physiol 279: H1890–1897, 2000. doi:10.1152/ajpheart.2000.279.4.H1890.
    Link | Web of Science | Google Scholar
  • 64. Colleran PN, Li Z, Yang HT, Laughlin MH, Terjung RL. Vasoresponsiveness of collateral vessels in the rat hindlimb: influence of training. J Physiol 588: 1293–1307, 2010. . doi:10.1113/jphysiol.2009.186247.
    Crossref | PubMed | Web of Science | Google Scholar
  • 65. Mohiuddin M, Lee NH, Moon JY, Han WM, Anderson SE, Choi JJ, Shin E, Nakhai SA, Tran T, Aliya B, Kim DY, Gerold A, Hansen LM, Taylor WR, Jang YC. Critical Limb Ischemia Induces Remodeling of Skeletal Muscle Motor Unit. Sci Rep 9: 9551, 2019. doi:10.1038/s41598-019-45923-4.
    Crossref | PubMed | Web of Science | Google Scholar
  • 66. Johansen LB, Jensen TU, Pump B, Norsk P. Contribution of abdomen and legs to central blood volume expansion in humans during immersion. J Appl Physiol (1985) 83: 695–699, 1997. doi:10.1152/jappl.1997.83.3.695.
    Link | Web of Science | Google Scholar
  • 67. Miyata S, Koyama Y, Takemoto K, Yoshikawa K, Ishikawa T, Taniguchi M, Inoue K, Aoki M, Hori O, Katayama T, Tohyama M. Plasma corticosterone activates SGK1 and induces morphological changes in oligodendrocytes in corpus callosum. PLoS One 6: e19859, 2011. doi:10.1371/journal.pone.0019859.
    Crossref | PubMed | Web of Science | Google Scholar
  • 68. Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Chui DH, Tabira T. Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 20: 1568–1574, 2000. doi:10.1523/JNEUROSCI.20-04-01568.2000.
    Crossref | PubMed | Web of Science | Google Scholar
  • 69. Akerman AP, Thomas KN, van Rij AM, Body ED, Alfadhel M, Cotter JD. Heat therapy vs. supervised exercise therapy for peripheral arterial disease: a 12-wk randomized, controlled trial. Am J Physiol Heart Circ Physiol 316: H1495–H1506, 2019. doi:10.1152/ajpheart.00151.2019.
    Link | Web of Science | Google Scholar
  • 70. Pellinger TK, Neighbors CB, Simmons GH. Acute lower leg heating increases exercise capacity in patients with peripheral artery disease. J Cardiovasc Nurs 34: 130–133, 2019. doi:10.1097/JCN.0000000000000510.
    Crossref | PubMed | Web of Science | Google Scholar
  • 71. Shinsato T, Miyata M, Kubozono T, Ikeda Y, Fujita S, Kuwahata S, Akasaki Y, Hamasaki S, Fujiwara H, Tei C. Waon therapy mobilizes CD34+ cells and improves peripheral arterial disease. J Cardiol 56: 361–366, 2010. doi:10.1016/j.jjcc.2010.08.004.
    Crossref | PubMed | Web of Science | Google Scholar
  • 72. Tei C, Shinsato T, Kihara T, Miyata M. Successful thermal therapy for end-stage peripheral artery disease. J Cardiology 47: 163–164, 2006. ]
    PubMed | Google Scholar
  • 73. Tei C, Shinsato T, Miyata M, Kihara T, Hamasaki S. Waon therapy improves peripheral arterial disease. J Am Coll Cardiol 50: 2169–2171, 2007. doi:10.1016/j.jacc.2007.08.025.
    Crossref | PubMed | Web of Science | Google Scholar
  • 74. Oishi Y, Hayashida M, Tsukiashi S, Taniguchi K, Kami K, Roy RR, Ohira Y. Heat stress increases myonuclear number and fiber size via satellite cell activation in rat regenerating soleus fibers. J Appl Physiol (1985) 107: 1612–1621, 2009. doi:10.1152/japplphysiol.91651.2008.
    Link | Web of Science | Google Scholar
  • 75. Shibaguchi T, Hoshi M, Yoshihara T, Naito H, Goto K, Yoshioka T, Sugiura T. Impact of different temperature stimuli on the expression of myosin heavy chain isoforms during recovery from bupivacaine-induced muscle injury in rats. J Appl Physiol 127: 178–189, 2019. doi:10.1152/japplphysiol.00930.2018.
    Link | Web of Science | Google Scholar
  • 76. Ohira T, Higashibata A, Seki M, Kurata Y, Kimura Y, Hirano H, Kusakari Y, Minamisawa S, Kudo T, Takahashi S, Ohira Y, Furukawa S. The effects of heat stress on morphological properties and intracellular signaling of denervated and intact soleus muscles in rats. Physiol Rep 5: e13350, 2017. doi:10.14814/phy2.13350.
    Crossref | Web of Science | Google Scholar
  • 77. Selsby JT, Dodd SL. Heat treatment reduces oxidative stress and protects muscle mass during immobilization. Am J Physiol Regul Integr Comp Physiol 289: R134–R139, 2005. doi:10.1152/ajpregu.00497.2004.
    Link | Web of Science | Google Scholar
  • 78. Tamura Y, Kitaoka Y, Matsunaga Y, Hoshino D, Hatta H. Daily heat stress treatment rescues denervation-activated mitochondrial clearance and atrophy in skeletal muscle. J Physiol 593: 2707–2720, 2015. doi:10.1113/JP270093.
    Crossref | PubMed | Web of Science | Google Scholar
  • 79. Koutakis P, Myers SA, Cluff K, Ha DM, Haynatzki G, McComb RD, Uchida K, Miserlis D, Papoutsi E, Johanning JM, Casale GP, Pipinos II. Abnormal myofiber morphology and limb dysfunction in claudication. J Surg Res 196: 172–179, 2015. doi:10.1016/j.jss.2015.02.011.
    Crossref | PubMed | Web of Science | Google Scholar