Share This Article:
Review Paper

Review of the adaptation of skeletal muscle in intermittent claudication

Abstract Full-Text HTML Download Download as PDF (Size:572KB) PP. 347-360
DOI: 10.4236/wjcd.2013.34055    2,941 Downloads   4,441 Views   Citations

ABSTRACT

Background: Despite awareness about the impact of intermittent claudication (IC) on mobility, balance and quality of life; the underlying pathophysiology and alterations in muscle architecture secondary to the disease are often overlooked. This review aimed to summarize the pathophysiological muscle changes present secondary to IC. Methods: The electronic databases, Medline, EMBASE, Cinahl and AMED, were searched for studies from 1967 to August 2011. Search terms included exercise, intermittent claudication and muscle. Studies about IC which were focused on muscle histology, muscle architecture, blood flow or changes with exercise were included. Results: Of 434 studies identified, 135 unique results were found. Only 78 of these were suitable from abstract review, of which 15 were unobtainable and a further nine were identified from hand-searching references. Studies in animal models demonstrated a predominance of type II muscle fibres and an improvement in animal exercise tolerance secondary to training. Exercise alone was never able to improve distances to that of healthy controls, however a lower limb fistula along with exercise did. Lower limb blood flow was demonstrated to be affected regionally, and most evident during exercise with a prolonged return to normal in patients with IC. At a cellular level, the myocytes metabolism increased in those with IC, but returned to normal post-revascularization. Conclusion: Treatment for claudicants includes either revascularization or exercise. Successful revascularization has demonstrated a return to normal muscle metabolism; the underlying physiological improvement secondary to exercise still requires clarification.


Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Gohil, R. , Lane, T. and Coughlin, P. (2013) Review of the adaptation of skeletal muscle in intermittent claudication. World Journal of Cardiovascular Diseases, 3, 347-360. doi: 10.4236/wjcd.2013.34055.

References

[1] Lambert, J. and Lambert, P.J. (1967) Untoward hemodynamic effects of intra-arterial injections of vasodilator drugs on the muscle circulation in the dog hind limb with experimental arterial occlusion. Angiology, 18, 415-27. doi:10.1177/000331976701800702
[2] Link, R.P., Pedersoli, W.M. and Safanie, A.H. (1972) Effect of exercise on development of atherosclerosis in swine. Atherosclerosis, 15, 107-22. doi:10.1016/0021-9150(72)90044-5
[3] Makitie, J. and Teravainen, H. (1977) Histochemical changes in striated muscle in patients with intermittent claudication. Archives of Pathology & Laboratory Medicine, 101, 658-663.
[4] Dahllof, A.G., Holm, J., Kral, J. and Schersten, T. (1975) The relationship between glycogen content of leg muscles and working capacity in patients with intermittent claudication. Acta Chirurgica Scandinavica, 141, 329-332.
[5] Holm, J., Dahllof, A.G. and Schersten, T. (1975) Metabolic activity of skeletal muscle in patients with peripheral arterial insufficiency. Effect of arterial reconstructive surgery. Scandinavian Journal of Clinical & Laboratory Investigation, 35, 81-86. doi:10.3109/00365517509068009
[6] Askew, C.D., Green, S., Walker, P.J., Kerr, G.K., Green, A.A., Williams, A.D., et al. (2005) Skeletal muscle phenotype is associated with exercise tolerance in patients with peripheral arterial disease. Journal of Vascular Surgery, 41, 802-807. doi:10.1016/j.jvs.2005.01.037
[7] Clyne, C.A., Weller, R.O., Bradley, W.G., Silber, D.I., O’Donnell Jr., T.F. and Callow, A.D. (1982) Ultrastructural and capillary adaptation of gastrocnemius muscle to occlusive peripheral vascular disease. Surgery, 92, 434440.
[8] Hedberg, B., Angquist, K.A. and Sjostrom, M. (1988) Peripheral arterial insufficiency and the fine structure of the gastrocnemius muscle. International Journal of Angiology, 7, 50-59.
[9] Jansson, E., Johansson, J., Sylven, C. and Kaijser, L. (1988) Calf muscle adaptation in intermittent claudication. Side-differences in muscle metabolic characteristics in patients with unilateral arterial disease. Clinical Physiology, 8, 17-29.
[10] Teravainen, H. and Makitie, J. (1977) Striated muscle ultrastructure in intermittent claudication. Archives of Pathology & Laboratory Medicine, 101, 230-235.
[11] Angquist, K.A. and Sjostrom, M. (1980) Intermittent claudication and muscle fiber fine structure: Morphometric data on mitochondrial volumes. Ultrastructural Pathology, 1, 461-470. doi:10.3109/01913128009140552
[12] Schocke, M.F.H., Esterhammer, R., Ostermann, S., Santner, W., Gorny, O., Fraedrich, G., et al. (2006) High-energy phosphate metabolism during calf ergometry in patients with isolated aorto-iliac artery stenoses. Investigative Radiology, 41, 874-882. doi:10.1097/01.rli.0000246148.09129.42
[13] Eto, D., Yamano, S., Kasashima, Y., Sugiura, T., Nasu, T., Tokuriki, M., et al. (2003) Effect of controlled exercise on middle gluteal muscle fibre composition in Thoroughbred foals. Equine Veterinary Journal, 35, 676-680. doi:10.2746/042516403775696276
[14] Lane, R.J., Barrett, M.C., Woodrow, D., Moss, J., Fletcher, R. and Archard, L.C. (1998) Muscle fibre characteristics and lactate responses to exercise in chronic fatigue syndrome. Journal of Neurology, Neurosurgery & Psychiatry, 64, 362-367. doi:10.1136/jnnp.64.3.362
[15] Brackenbury, J.H. and Holloway, S.A. (1991) Age and exercise effects on mitochondrial density and capillary fibre ratio in bird leg muscle. British Poultry Science, 32, 645-653. doi:10.1080/00071669108417389
[16] Dingboom, E.G., Dijkstra, G., Enzerink, E., van Oudheusden, H.C. and Weijs, W.A. (1999) Postnatal muscle fibre composition of the gluteus medius muscle of Dutch Warmblood foals; maturation and the influence of exercise. Equine Veterinary Journal, 31, 95-100. doi:10.1111/j.2042-3306.1999.tb05320.x
[17] Pipinos, I.I., Swanson, S.A., Zhu, Z., Nella, A.A., Weiss, D.J., Gutti, T.L., et al. (2008) Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage. American Journal of Physiology—Regulatory Integrative and Comparative Physiology, 295, R290-R296. doi:10.1152/ajpregu.90374.2008
[18] Hain, B.A., Dodd, S.L. and Judge, A.R. (2011) IBalpha degradation is necessary for skeletal muscle atrophy associated with contractile claudication. American Journal of Physiology—Regulatory Integrative and Comparative Physiology, 300, R595-R604. doi:10.1152/ajpregu.00728.2010
[19] Egan, B., Carson, B.P., Garcia-Roves, P.M., Chibalin, A.V., Sarsfield, F.M., Barron, N., et al. (2010) Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor coactivator-1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. The Journal of Physiology, 588, 1779-1790. doi:10.1113/jphysiol.2010.188011
[20] Daugaard, J.R. and Richter, E.A. (2001) Relationship between muscle fibre composition, glucose transporter protein 4 and exercise training: possible consequences in non-insulin-dependent diabetes mellitus. Acta Medica Scandinavica, 171, 267-276. doi:10.1046/j.1365-201x.2001.00829.x
[21] Frisk-Holmberg, M., Jorfeldt, L., Juhlin-Dannfelt, A. and Karlsson, J. (1981) Leg blood flow during exercise in man in relation to muscle fibre composition. Acta Medica Scandinavica, 112, 339-342. doi:10.1111/j.1748-1716.1981.tb06825.x
[22] Hammarsten, J., Bylund-Fellenius, C. and Holm, J. (1980) Capillary supply and muscle fibre types in patients with intermittent claudication: Relationships between morphology and metabolism. European Journal of Clinical Investigation, 10, 301-305. doi:10.1111/j.1365-2362.1980.tb00037.x
[23] Green, H.J., Smith, D., Murphy, P. and Fraser, I. (1990) Training-induced alterations in muscle glycogen utilization in fibre-specific types during prolonged exercise. Canadian Journal of Physiology and Pharmacology, 68, 1372-1376. doi:10.1139/y90-208
[24] Magal, M., Dumke, C.L., Urbiztondo, Z.G., Cavill, M.J., Triplett, N.T., Quindry, J.C., et al. (2010) Relationship between serum creatine kinase activity following exercise-induced muscle damage and muscle fibre composition. Journal of Sports Science and Medicine, 28, 257266.
[25] Pernow, B., Saltin, B., Wahren, J., Cronestrand, R. and Ekestroom, S. (1975) Leg blood flow and muscle metabolism in occlusive arterial disease of the leg before and after reconstructive surgery. Clinical Science & Molecular Medicine, 49, 265-275.
[26] Karlsson, J., Sjodin, B., Jacobs, I. and Kaiser, P. (1981) Relevance of muscle fibre type to fatigue in short intense and prolonged exercise in man. Ciba Foundation Symposium, 82, 59-74.
[27] Barker, G.A., Green, S. and Walker, P.J. (2004) Effect of carbohydrate supplementation on walking performance in peripheral arterial disease: A preliminary physiologic study. Journal of Vascular Surgery, 40, 932-938. doi:10.1016/j.jvs.2004.07.047
[28] Brevetti, G., Chiariello, M., Ferulano, G., Policicchio, A., Nevola, E., Rossini, A., et al. (1988) Increases in walking distance in patients with peripheral vascular disease treated with L-carnitine: A double-blind, cross-over study. Circulation, 77, 767-773. doi:10.1161/01.CIR.77.4.767
[29] Lieber, R.L. (1993) Skeletal muscle architecture: Implications for muscle function and surgical tendon transfer. Journal of Hand Therapy, 6, 105-113. doi:10.1016/S0894-1130(12)80291-2
[30] Lieber, R.L. and Friden, J. (2000) Functional and clinical significance of skeletal muscle architecture. Muscle Nerve, 23, 1647-1666. doi:10.1002/1097-4598(200011)23:11<1647::AID-MUS1>3.0.CO;2-M
[31] Kemp, G.J., Roberts, N., Bimson, W.E., Bakran, A., Harris, P.L., Gilling-Smith, G.L., et al. (2001) Mitochondrial function and oxygen supply in normal and in chronically ischemic muscle: A combined 31P magnetic resonance spectroscopy and near infrared spectroscopy study in vivo. Journal of Vascular Surgery, 34, 1103-1110. doi:10.1067/mva.2001.117152
[32] Nicholson, C.D., Angersbach, D. and Wilke, R. (1992) The effect of physical training on rat calf muscle, oxygen tension, blood flow, metabolism and function in an animal model of chronic occlusive peripheral vascular disease. International Journal of Sports Medicine, 13, 60-64. doi:10.1055/s-2007-1021236
[33] Yang, H.T., Ogilvie, R.W. and Terjung, R.L. (1991) Low-intensity training produces muscle adaptations in rats with femoral artery stenosis. Journal of Applied Physiology, 71, 1822-1829.
[34] Afaq, A., Montgomery, P.S., Scott, K.J., Blevins, S.M., Whitsett, T.L. and Gardner, A.W. (2008) The effect of hypercholestrolemia on calf muscle hemoglobin oxygen saturation in patients with intermittent claudication. Angiology, 59, 534-541.
[35] Depairon, M., De Landsheere, C., Merlo, P., Del Fiore, G., Quaglia, L., Peters, J.M., et al. (1988) Effect of exercise on the leg distribution of C15O2 and 15O2 in normals and in patients with peripheral ischemia: A study using positron tomography. International Journal of Angiology, 7, 254-257.
[36] Appleberg, M. and Lewis, J.D. (1975) Evaluation of aorto-iliac disease with Doppler ultrasound and isotope clearance techniques. South African Medical Journal, 49, 1744-1746.
[37] Alpert, J.S., Larsen, O.A. and Lassen, N.A. (1969) Exercise and intermittent claudication. Blood flow in the calf muscle during walking studied by the xenon-133 clearance method. Circulation, 39, 353-359. doi:10.1161/01.CIR.39.3.353
[38] McCully, K.K., Halber, C. and Posner, J.D. (1994) Exercise-induced changes in oxygen saturation in the calf muscles of elderly subjects with peripheral vascular disease. Journal of Gerontology, 49, B128-B134. doi:10.1093/geronj/49.3.B128
[39] Dorigo, B., Bartoli, V., Grisillo, D., Beconi, D. and Zanini, A. (1980) Exercise hyperemia for the study of peripheral circulation. Angiology, 31, 50-57. doi:10.1177/000331978003100108
[40] Weiss, T., Fujita, Y., Kreimeier, U. and Messmer, K. (1992) Effect of intensive walking exercise on skeletal muscle blood flow in intermittent claudication. Angiology, 43, 63-71. doi:10.1177/000331979204300108
[41] Bostrom, P.A., Diemer, H., Leide, S., Lilja, B. and Bergqvist, D. (1993) 99Tcm-sestamibi uptake in the leg muscles and in the myocardium in patients with intermittent claudication. Angiology, 44, 971-976. doi:10.1177/000331979304401208
[42] Depairon, M., Depresseux, J.C., De, C., Merlo, P., Del, G., Quaglia, L., et al. (1988) Quantitation of regional muscle blood flow and oxygen uptake in peripheral arterial insufficiency using positron emission tomography. Journal des Maladies Vasculaires, 13, 107-115.
[43] Jussila, E., Niinikoski, J. and Inberg, M.V. (1979) Tissue gas tensions in the calf muscles of patients with lower limb arterial ischaemia. Scandinavian Cardiovascular Journal, 13, 77-82. doi:10.3109/14017437909101791
[44] Erney, T.P., Mathien, G.M. and Terjung, R.L. (1991) Muscle adaptations in trained rats with peripheral arterial insufficiency. American Journal of Physiology-Heart and Circulatory Physiology, 260, H445-H452.
[45] Prior, B.M., Lloyd, P.G., Ren, J., Li, H., Yang, H.T., Laughlin, M.H., et al. (2004) Time course of changes in collateral blood flow and isolated vessel size and gene expression after femoral artery occlusion in rats. American Journal of Physiology Heart Circulatory Physiology, 287, H2434-H2447. doi:10.1152/ajpheart.00398.2004
[46] Yang, H.T., Laughlin, M.H. and Terjung, R.L. (2000) Prior exercise training increases collateral-dependent blood flow in rats after acute femoral artery occlusion. American Journal of Physiology Heart Circulatory Physiology, 279, H1890-H1897.
[47] Yang, H.T., Ogilvie, R.W. and Terjung, R.L. (1995) Training increases collateral-dependent muscle blood flow in aged rats. American Journal of Physiology Heart and Circulatory Physiology, 268, H1174-H1180.
[48] Kojda, G. and Hambrecht, R. (2005) Molecular mechanisms of vascular adaptations to exercise. Physical activeity as an effective antioxidant therapy? Cardiovasc Research, 67, 187-197. doi:10.1016/j.cardiores.2005.04.032
[49] Troidl, K., Ruding, I., Cai, W.J., Mucke, Y., Grossekettler, L., Piotrowska, I., et al. (2009) Actin-binding rho activating protein (Abra) is essential for fluid shear stressinduced arteriogenesis. Arteriosclerosis Thrombosis Vascular Biology, 29, 2093-2101. doi:10.1161/ATVBAHA.109.195305
[50] Schierling, W., Troidl, K., Troidl, C., Schmitz-Rixen, T., Schaper, W. and Eitenmuller, I.K. (2009) The role of angiogenic growth factors in arteriogenesis. Journal of Vascular Research, 46, 365-374. doi:10.1159/000189797
[51] Schierling, W., Troidl, K., Mueller, C., Troidl, C., Wustrack, H., Bachmann, G., et al. (2009) Increased intravascular flow rate triggers cerebral arteriogenesis. Journal of Cerebral Blood Flow & Metabolism, 29, 726-737. doi:10.1038/jcbfm.2008.165
[52] Prior, B.M., Ren, J., Terjung, R.L. and Yang, H.T. (2011) Significant, but limited collateral blood flow increases occur with prolonged training in rats with femoral artery occlusion. Journal of Physiology and Pharmacology, 62, 197-205.
[53] Ferrara, N. (2004) Vascular endothelial growth factor: Basic science and clinical progress. Endocrine Reviews, 25, 581-611. doi:10.1210/er.2003-0027
[54] Allen, L.A., Terjung, R.L. and Yang, H.T. (2006) Exogenous basic fibroblast growth factor increases collateral blood flow in female rats with femoral artery occlusion. Journal of Cardiovascular Pharmacology, 47, 146154. doi:10.1097/01.fjc.0000199145.54220.58
[55] Troidl, K., Tribulova, S., Cai, W.J., Eitenmuller, I., Wustrack, H., Schierling, W., et al. (2009) Effects of endogenous NO and of DETA NONOate in Arteriogenesis. Journal of cardiovascular pharmacology, 2, 153-160.
[56] Henriksson, J., Nygaard, E., Andersson, J. and Eklof, B. (1980) Enzyme activities, fibre types and capillarization in calf muscles of patients with intermittent claudication. Scandinavian Journal of Clinical and Laboratory Investigation, 40, 361-369. doi:10.3109/00365518009092656
[57] Yang, H.T., Ogilvie, R.W. and Terjung, R.L. (1994) Peripheral adaptations in trained aged rats with femoral ar-tery stenosis. Circulation Research, 74, 235-243. doi:10.1161/01.RES.74.2.235
[58] Deschenes, M.R. and Ogilvie, R.W. (1999) Exercise stimulates neovascularization in occluded muscle without affecting bFGF content. Medicine & Science in Sports & Exercise, 31, 1599-1604. doi:10.1097/00005768-199911000-00016
[59] Wang, J., Zhou, S., Bronks, R., Graham, J. and Myers, S. (2009) Effects of supervised treadmill walking training on calf muscle capillarization in patients with intermittent claudication. Angiology, 60, 36-41. doi:10.1177/0003319708317337
[60] Birot, O.J., Koulmann, N., Peinnequin, A. and Bigard, X.A. (2003) Exercise-induced expression of vascular endothelial growth factor mRNA in rat skeletal muscle is dependent on fibre type. Journal of Physiology, 552, 213221. doi:10.1113/jphysiol.2003.043026
[61] Palmer-Kazen, U., Religa, P. and Wahlberg, E. (2009) Exercise in patients with intermittent claudication elicits signs of inflammation and angiogenesis. European Journal of Vascular and Endovascular Surgery, 38, 689-696. doi:10.1016/j.ejvs.2009.08.005
[62] Chinsomboon, J., Ruas, J., Gupta, R.K., Thom, R., Shoag, J., Rowe, G.C., et al. (2009) The transcriptional coactivator PGC-1alpha mediates exercise-induced angiogenesis in skeletal muscle. Proceeding of the National Academy of Sciences of the United States of America, 106, 21401-21406. doi:10.1073/pnas.0909131106
[63] Mathien, G.M. and Terjung, R.L. (1990) Muscle blood flow in trained rats with peripheral arterial insufficiency. American Journal of Physiology-Heart and Circulatory Physiology, 258, H759-H765.
[64] Mathien, G.M. and Terjung, R.L. (1986) Influence of training following bilateral stenosis of the femoral artery in rats. American Journal of Physiology, 250, H1050H1059.
[65] Melichna, J., Mackova, E.V., Semiginovsky, B., Tolar, M., Stichova, J., Slavicek, A., et al. (1987) Effect of exercise on muscle fibre composition and enzyme activities of skeletal muscles in young rats. Physiol Bohemoslov, 36, 321-328.
[66] Pipinos, I.I., Shepard. A.D., Anagnostopoulos, P.V., Katsamouris, A. and Boska, M.D. (2000) Phosphorus 31 nuclear magnetic resonance spectroscopy suggests a mitochondrial defect in claudicating skeletal muscle. Journal of Vascular Surgery, 31, 944-952. doi:10.1067/mva.2000.106421
[67] Zatina, M.A., Berkowitz, H.D., Gross, G.M., Maris, J.M. and Chance, B. (1986) 31P nuclear magnetic resonance spectroscopy: Noninvasive biochemical analysis of the ischemic extremity. Journal of Vascular Surgery, 3, 411420.
[68] Elander, A., Sjostrom, M., Lundgren, F., Schersten, T. and Bylund-Fellenius, A.C. (1985) Biochemical and morphometric properties of mitochondrial populations in human muscle fibres. Clinical Science (Lond), 69, 153164.
[69] Thaveau, F., Zoll, J., Rouyer, O., Chafke, N., Kretz, J.G., Piquard, F., et al. (2007) Ischemic preconditioning specifically restores complexes I and II activities of the mitochondrial respiratory chain in ischemic skeletal muscle. Journal of Vascular Surgery, 46, 541-547. doi:10.1016/j.jvs.2007.04.075
[70] Maass, U. (1983) Experimental design in angiological clinical therapeutic research, interand intraindividual comparison in patients with intermittent claudication. [German] Zur Methodik in der Angiologisch-TherapeutischKlinischen Forschung. interund Intraindividueller Vergleich bei Arterieller Verschlusskrankheit. Fortschritte der Medizin, 101, 1831-1837.
[71] Kramer, C.M. (2007) Peripheral arterial disease assessment: Wall, perfusion, and spectroscopy. Topics in Magnetic Resonance Imaging, 18, 357-369. doi:10.1097/rmr.0b013e31815d064c
[72] Rexroth, W., Semmler, W., Guckel, F., Stadlander, M., Weicker, H., Hild, R., et al. (1989) Assessment of muscular metabolism in peripheral arterial occlusive disease using 31P nuclear magnetic resonance spectroscopy. Klinische Wochenschrift, 67, 804-812. doi:10.1007/BF01725196
[73] Schunk, K., Kersjes, W., Schadmand-Fischer, S., Thelen, M. (1997) Dynamic 31phosphorus magnetic resonance spectroscopy of the quadriceps muscle: Metabolic changes resulting from two different forms of exercise. Rofo, 166, 317-323. doi:10.1055/s-2007-1015432
[74] Keller, U., Oberhansli, R., Huber, P., Widmer, L.K., Aue, W.P., Hassink, R.I., et al. (1985) Phosphocreatine content and intracellular pH of calf muscle measured by phosphorus NMR spectroscopy in occlusive arterial disease of the legs. European Journal of Clinical Investigation, 15, 382-388. doi:10.1111/j.1365-2362.1985.tb00289.x
[75] Schunk, K., Romaneehsen, B., Mildenberger, P., Kersjes, W., Schadmand-Fischer, S. and Thelen, M. (1997) Dynamic phosphorus-31 magnetic resonance spectroscopy in arterial occlusive disease. Correlation with clinical and angiographic findings and comparison with healthy volunteers. Investigative Radiology, 32, 651-659. doi:10.1097/00004424-199711000-00001
[76] Schunk, K., Romaneehsen, B., Dahm, M., Dietz, U., Kersjes, W., Schadmand-Fischer, S., et al. (1997) Dynamic 31-phosphorus magnetic resonance spectroscopy of the m. quadriceps: Therapy-induced changes in arterial occlusive disease. Rofo, 167, 139-146. doi:10.1055/s-2007-1015507
[77] Schunk, K., Romaneehsen, B., Rieker, O., Duber, C., Kersjes, W., Schadmand-Fischer, S., et al. (1998)Dynamic phosphorus-31 magnetic resonance spectroscopy in arterial occlusive disease: Effects of vascular therapy on spectroscopic results. Investigative Radiology, 33, 329335. doi:10.1097/00004424-199806000-00003
[78] Ecochard, L., Lhenry, F., Sempore, B. and Favier, R. (2000) Skeletal muscle HSP72 level during endurance training: Influence of peripheral arterial insufficiency. Pflugers Archiv, 440, 918-924. doi:10.1007/s004240000362
[79] Pellegrin, M., Miguet-Alfonsi, C., Bouzourene, K., Aubert, J.F., Deckert, V., Berthelot, A., et al. (2009) Longterm exercise stabilizes atherosclerotic plaque in ApoE knockout mice. Medicine & Science in Sports & Exercise, 41, 2128-2135. doi:10.1249/MSS.0b013e3181a8d530
[80] Russell, A.P., Somm, E., Praz, M., Crettenand, A., Hartley, O., Melotti, A., et al. (2003) UCP3 protein regulation in human skeletal muscle fibre types I, IIa and IIx is dependent on exercise intensity. Journal of Physiology, 550, 855-861. doi:10.1113/jphysiol.2003.040162
[81] Karlsson, J., Diamant, B., Folkers, K. and Lund, B. (1991) Muscle fibre types, ubiquinone content and exercise capacity in hypertension and effort angina. Annals Medicine, 23, 339-344. doi:10.3109/07853899109148070
[82] Melchert, U.H., Brinkmann, G., Forger, K., Gleim, M., Wunsch-Binder, F., Maier, C., et al. (1992) In vivo 31phosphorus MR spectroscopy of the calf musculature in arterial occlusive diseases. [German] In-vivo-31Phosphor MR-Spektroskopie der Wadenmuskulatur bei arterieller VerschluBkrankheit. RoFo, 156, 346-352. doi:10.1055/s-2008-1032899
[83] Taylor, D.J., Amato, A., Hands, L.J., Kemp, G.J., Ramaswami, G., Nicolaides, A., et al. (1996) Changes in energy metabolism of calf muscle in patients with intermittent claudication assessed by 31P magnetic resonance spectroscopy: A phase II open study. Vascular Medicine, 1, 241-245.
[84] Allegra, C., Antignani, P.L., Schachter, I., Koverech, A., Messano, M. and Virmani, A. (2008) Propionyl-L-carnitine in Leriche-Fontaine stage II peripheral arterial obstructive disease. Annals of Vascular Surgery, 22, 552-558. doi:10.1016/j.avsg.2008.02.010
[85] Ren, J., Li, H., Prior, B.M. and Yang, H.T. (2008) Angiotensin converting enzyme inhibition enhances collateral artery remodeling in rats with femoral artery occlusion. The American Journal of the Medical Sciences, 335, 177-187. doi:10.1097/MAJ.0b013e318142b978
[86] Taylor, J.C., Li, Z., Yang, H.T., Laughlin, M.H. and Terjung, R.L. (2008) Alpha-adrenergic inhibition increases collateral circuit conductance in rats following acute occlusion of the femoral artery. Journal of Physiology, 586, 1649-1667. doi:10.1113/jphysiol.2007.149567
[87] Nicholson, C.D. (1996) Experimental models of chronic lower extremity arterial occlusive disease: Lessons for drug development. Vascular Medicine, 1, 43-49.
[88] Loizidis, T., Sioga, A., Economou, L., Frosinis, A., Kyparos, A., Zotou, A., et al. (2007) The role of ascorbic acid and exercise in chronic ischemia of skeletal muscle in rats. Journal of Applied Physiology, 102, 321-330. doi:10.1152/japplphysiol.00251.2005

  
comments powered by Disqus

Copyright © 2019 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.