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Role of Skeletal Muscle Angiogenesis in Peripheral Artery Disease

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Biochemical Basis and Therapeutic Implications of Angiogenesis

Part of the book series: Advances in Biochemistry in Health and Disease ((ABHD,volume 6))

Abstract

Peripheral artery disease is a major circulatory disorder, which is characterized by obstruction of arteries mainly due to atherosclerosis and thrombosis, leading to reduced blood supply and ischemia in the hind limb. On the basis of their actions on blood constituents and blood vessels, several interventions such as antiatherosclerotic, antithrombolytic, antihypertensive, antidiabetic, and vasodilating agents are commonly used for the treatment of this disease but none of these drugs are satisfactory. Since angiogenesis is an adaptive process, which is concerned with promoting blood flow in different organs, it is plausible that the development of angiogenesis in the skeletal muscle may serve as a novel target for the treatment of peripheral artery disease. Because the formation of several factors such as vascular endothelial growth factor and nitric oxide as well as reduction of oxidative stress and inflammatory cytokines is known to promote angiogenesis, manipulation of these mechanisms by newer interventions including stem cell therapy can be seen to produce beneficial effects. In this context, both exercise training and CO2-bath therapy have been shown to induce angiogenesis and increase blood flow in the ischemic limb. Thus the development of angiogenesis-based therapies is suggested for improving blood flow in the treatment of peripheral arterial disease.

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References

  1. Hudlicka O, Brown M, Egginton S (1992) Angiogenesis in skeletal and cardiac muscle. Physiol Rev 72:369–417

    CAS  PubMed  Google Scholar 

  2. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9:653–660

    Article  CAS  PubMed  Google Scholar 

  3. Troidl K, Schaper W (2012) Arteriogenesis versus angiogenesis in peripheral artery disease. Diabetes Metal Res Rev 28:27–29

    Article  Google Scholar 

  4. Egginton S (2008) Invited review: activity-induced angiogenesis. Pflugers Arch 457:963–977

    Article  PubMed  CAS  Google Scholar 

  5. Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146:873–887

    Article  CAS  PubMed  Google Scholar 

  6. Risau W (1997) Mechanisms of angiogenesis. Nature 386:671–674

    Article  CAS  PubMed  Google Scholar 

  7. Hertig A (1935) Angiogenesis in the early human chorion and in the primary plascenta of the macque monkey. Contrib Embryol 25:37–81

    Google Scholar 

  8. Sandison JC (1932) Contraction of blood vessels and observations on the circulation in the transparent chamber in the rabbit’s ear. Anat Rec 24:105–127

    Article  Google Scholar 

  9. Hudlicka O, Wright AJ, Ziada AM (1986) Angiogenesis in the heart and skeletal muscle. Can J Cardiol 2:120–123

    CAS  PubMed  Google Scholar 

  10. Kawamata T, Speliotes EK, Finklestein SP (1997) The role of polypeptide growth factors in recovery from stroke. Adv Neurol 73:377–382

    CAS  PubMed  Google Scholar 

  11. Kumar S, West D, Shahabuddin S et al (1983) Angiogenesis factor from human myocardial infarcts. Lancet 322:364–368

    Article  Google Scholar 

  12. Burgos H, Herd A, Bennett JP (1989) Placental angiogenic and growth factors in the treatment of chronic varicose ulcers: preliminary communication. J R Soc Med 82:598–599

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Folkman J, Merler E, Abernathy C et al (1971) Isolation of a tumor factor responsible for angiogenesis. J Exp Med 133:275–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other diseases. Nat Med 1:27–31

    Article  CAS  PubMed  Google Scholar 

  15. Christou H, Yoshida A, Arthur V et al (1998) Increased vascular endothelial growth factor production in the lungs of rats with hypoxia-induced pulmonary hypertension. Am J Respir Cell Mol Biol 18:768–776

    Article  CAS  PubMed  Google Scholar 

  16. Patz A (1978) Current concepts in ophthalmology. Retinal vascular diseases. N Engl J Med 298:1451–1454

    Article  CAS  PubMed  Google Scholar 

  17. Latroche C, Gitiaux C, Chretien F et al (2015) Skeletal muscle microvasculature: a highly dynamic lifeline. Phys Ther 30:417–427

    CAS  Google Scholar 

  18. Limbourg A, Korff T, Napp LC et al (2009) Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia. Nat Protoc 4:1737–1746

    Article  CAS  PubMed  Google Scholar 

  19. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298–307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Olfert IM, Baum O, Hellsten Y, Egginton S (2015) Advances and challenges in skeletal muscle angiogenesis. Am J Physiol Heart Circ Physiol 310:H326–H336

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hiatt WR, Goldstone J, Smith SC et al (2008) Atherosclerotic peripheral vascular disease symposium II: nomenclature for vascular diseases. Circulation 118:2826–2829

    Article  PubMed  Google Scholar 

  22. Krishna S, Moxon J, Golledge J (2015) A review of the pathophysiology and potential biomarkers for peripheral artery disease. Int J Mol Sci 16:11294–11322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Cooke JP, Losordo DW (2015) Modulating the vascular response to limb ischemia: Angiogenic and cell therapies. Circ Res 116:1561–1578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Grote K, Schütt H, Schieffer B (2013) Toll-like receptor-linked signal transduction in angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 139–157

    Chapter  Google Scholar 

  25. Hoier B, Hellsten Y (2014) Exercise-induced capillary growth in human skeletal muscle and the dynamics of VEGF. Microcirculation 21:301–314

    Article  CAS  PubMed  Google Scholar 

  26. Von Tell D, Armulik A, Betsholtz C (2006) Pericytes and vascular stability. Exp Cell Res 312:623–629

    Article  CAS  Google Scholar 

  27. Vandekeere S, Dewerchin M, Carmeliet P (2015) Angiogenesis revisited: an overlooked role of endothelial cell metabolism in vessel sprouting. Microcirculation 22:509–517

    Article  PubMed  Google Scholar 

  28. Gerhardt H (2008) VEGF and endothelial guidance in angiogenic sprouting. Organogenesis 4:241–246

    Article  PubMed  PubMed Central  Google Scholar 

  29. Thal MA, Kishore R (2013) Role of cytokines in angiogenesis: turning it on and off. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 47–61

    Chapter  Google Scholar 

  30. Viloria-Petit A, Richard A, Zours S et al (2013) Role of transforming growth factor beta in angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 23–45

    Chapter  Google Scholar 

  31. Gerhardt H, Golding M, Fruttiger M et al (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Barnabas O, Wang H, Gao XM (2013) Role of estrogen in angiogenesis in cardiovascular diseases. J Geriatr Cardiol 10:377–382

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Schaun MI, Eibel B, Kristocheck M et al (2016) Cell therapy in ischemic heart disease: interventions that modulate cardiac regeneration. Stem Cells Int 2016:1–21. doi:10.1155/2016/2171035

    Article  Google Scholar 

  34. Ribatti D, Crivellato E (2012) “Sprouting angiogenesis”, a reappraisal. Dev Biol 372:157–165

    Article  CAS  PubMed  Google Scholar 

  35. Pradhan-Nabzdyk L, Nabzdyk C (2013) Neuropeptides and angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 63–77

    Chapter  Google Scholar 

  36. Hughes CCW (2008) Endothelial-stromal interactions in angiogenesis. Curr Opin Hematol 15:204–209

    Article  PubMed  Google Scholar 

  37. Lorier G, Touriño C, Kalil R (2011) Coronary angiogenesis as an endogenous response to myocardial ischemia in adults. Arq Bras Cardiol 97:140–148

    Article  Google Scholar 

  38. Tabatabai G, Weller M (2013) Role of integrins in angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 79–91

    Chapter  Google Scholar 

  39. Cross MJ, Claesson-Welsh L (2001) FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 22:201–207

    Article  CAS  PubMed  Google Scholar 

  40. Kehler DS, Dhalla NS, Duhamel TA (2013) Biochemical mechanisms of exercise-induced angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 181–206

    Chapter  Google Scholar 

  41. Crivellato E, Ribatti D (2013) Role of mast cells in angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 107–121

    Chapter  Google Scholar 

  42. Fowkes FGR, Rudan D, Rudan I et al (2013) Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis. Lancet 382:1329–1340

    Article  PubMed  Google Scholar 

  43. Hernando FJS, Conejero AM (2007) Peripheral artery disease: pathophysiology, diagnosis, and treatment. Rev Esp Cardiol 60:969–982

    Article  Google Scholar 

  44. Criqui MH, Aboyans V (2015) Epidemiology of peripheral artery disease. Circ Res 116:1509–1526

    Article  CAS  PubMed  Google Scholar 

  45. Allison MA, Ho E, Denenberg JO et al (2007) Ethnic-specific prevalence of peripheral arterial disease in the United States. Am J Prev Med 32:328–333

    Article  PubMed  Google Scholar 

  46. Haas TL, Lloyd PG, Yang H-T, Terjung RL (2012) Exercise training and peripheral arterial disease. Compr Physiol 2:2933–3017

    PubMed  PubMed Central  Google Scholar 

  47. Norgren L, Hiatt WR, Dormandy JA et al (2007) Inter-society consensus for the management of peripheral arterial disease (TASC II). Int Angiol 26:82–157

    Google Scholar 

  48. Raval Z, Losordo DW (2013) Cell therapy of peripheral arterial disease: from experimental findings to clinical trials. Circ Res 112:1288–1302

    Article  CAS  PubMed  Google Scholar 

  49. Hardman RL, Jazaeri O, Yi J et al (2014) Overview of classification systems in peripheral artery disease. Semin Intervent Radiol 31:378–388

    Article  PubMed  PubMed Central  Google Scholar 

  50. Shanmugasundaram M, Ram VK, Luft UC et al (2011) Peripheral arterial disease-what do we need to know? Clin Cardiol 34:478–482

    Article  PubMed  Google Scholar 

  51. Hegele RA (1997) The genetic basis of atherosclerosis. Int J Clin Lab Res 27:2–13

    Article  CAS  PubMed  Google Scholar 

  52. Mallika V, Goswami B, Rajappa M (2007) Atherosclerosis pathophysiology and the role of novel risk factors: a clinicobiochemical perspective. Angiology 58:513–522

    Article  CAS  PubMed  Google Scholar 

  53. Dashwood MR, Timm M, Muddle JR et al (1998) Regional variations in endothelin-1 and its receptor subtypes in human coronary vasculature: pathophysiological implications in coronary disease. Endothelium 6:61–70

    Article  CAS  PubMed  Google Scholar 

  54. Kobayashi T, Miyauchi T, Iwasa S et al (2000) Corresponding distributions of increased endothelin-B receptor expression and increased endothelin-1 expression in the aorta of apolipoprotein E-deficient mice with advanced atherosclerosis. Pathol Int 50:929–936

    Article  CAS  PubMed  Google Scholar 

  55. Rudijanto A (2007) The role of vascular smooth muscle cells on the pathogenesis of atherosclerosis. Acta Med Indones 39:86–93

    PubMed  Google Scholar 

  56. Plasschaert H, Heeneman S, Daemen MJ (2009) Progression in atherosclerosis: histological features and pathophysiology of atherosclerotic lesions. Top Magn Reson Imaging 20:227–237

    Article  PubMed  Google Scholar 

  57. Singh RB, Mengi SA, Xu YJ et al (2002) Pathogenesis of atherosclerosis: a multifactorial process. Exp Clin Cardiol 7:40–53

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Kim Y, Byzova TV (2015) Oxidative stress in angiogenesis and vascular disease. Blood 123:625–631

    Article  CAS  Google Scholar 

  59. Moore KJ, Tabas I (2011) Macrophages in the pathogenesis of atherosclerosis. Cell 145:341–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Sakakura K, Nakano M, Otsuka F et al (2013) Pathophysiology of atherosclerosis plaque progression. Heart Lung Circ 22:399–411

    Article  PubMed  Google Scholar 

  61. Idris NM, Haider HK, Goh MW, Sim EK (2004) Therapeutic angiogenesis for treatment of peripheral vascular disease. Growth Factors 22:269–279

    Article  CAS  PubMed  Google Scholar 

  62. Singla S, Mehta JL (2013) Trials of angiogenesis therapy in patients with ischemic heart disease. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 313–334

    Chapter  Google Scholar 

  63. Li WW, Li VW, Casey R et al (1998) Clinical trials of angiogenesis-based therapies: overview and new guiding principles. In: Maragoudakis M (ed) Angiogenesis: models, modulators and clinical application. Plenum Press, New York, pp 475–492

    Chapter  Google Scholar 

  64. Badimon L, Oñate B, Vilahur G (2013) Adipose tissue-derived mesenchymal stem cell and angiogenesis in ischemic heart disease. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 285–311

    Chapter  Google Scholar 

  65. Botham CM, Bennett WL, Cooke JP (2013) Clinical trials of adult stem cell therapy for peripheral artery disease. Methodist Debakey Cardiovasc J 9:201–205

    Article  PubMed  PubMed Central  Google Scholar 

  66. Høier B, Olsen K, Nyberg M et al (2010) Contraction-induced secretion of VEGF from skeletal muscle cells is mediated by adenosine. Am J Physiol Heart Circ Physiol 299:H857–H862

    Article  PubMed  CAS  Google Scholar 

  67. Baum O, Da Silva-Azevedo L, Willerding G et al (2004) Endothelial NOS is main mediator for shear stress-dependent angiogenesis in skeletal muscle after prazosin administration. Am J Physiol Heart Circ Physiol 287:H2300–H2308

    Article  CAS  PubMed  Google Scholar 

  68. Haas TL, Milkiewicz M, Davis SJ et al (2000) Matrix metalloproteinase activity is required for activity-induced angiogenesis in rat skeletal muscle. Am J Physiol Heart Circ Physiol 279:H1540–H1547

    CAS  PubMed  Google Scholar 

  69. Rullman E, Rundqvist H, Wågsäter D et al (2007) A single bout of exercise activates matrix metalloproteinase in human skeletal muscle. J Appl Physiol 102:2346–2351

    Article  CAS  PubMed  Google Scholar 

  70. Hoier B, Prats C, Qvortrup K et al (2013) Subcellular localization and mechanism of secretion of vascular endothelial growth factor in human skeletal muscle. FASEB J 27:3496–3504

    Article  CAS  PubMed  Google Scholar 

  71. Milkiewicz M, Hudlicka O, Brown MD, Silgram H (2005) Nitric oxide, VEGF, and VEGFR-2: interactions in activity-induced angiogenesis in rat skeletal muscle. Am J Physiol Circ Physiol 289:H336–H343

    Article  CAS  Google Scholar 

  72. O’Lone R, Knorr K, Jaffe IZ et al (2007) Estrogen receptors alpha and beta mediate distinct pathways of vascular gene expression, including genes involved in mitochondrial electron transport and generation of reactive oxygen species. Mol Endocrinol 21:1281–1296

    Article  PubMed  CAS  Google Scholar 

  73. Araujo AB, Kupelian V, Page ST et al (2007) Sex steroids and all-cause and cause-specific mortality in men. Arch Intern Med 167:1252–1260

    Article  CAS  PubMed  Google Scholar 

  74. Sieveking DP, Lim P, Chow RWY et al (2010) A sex-specific role for androgens in angiogenesis. J Exp Med 207:345–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kelly DM, Jones TH (2013) Testosterone: a vascular hormone in health and disease. J Endocrinol 217:R47–R71

    Article  CAS  PubMed  Google Scholar 

  76. Lecce L, Lam YT, Ng MKC (2013) Role of sex steroids in angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 159–180

    Chapter  Google Scholar 

  77. Chen L, Endler A, Shibasaki F (2009) Hypoxia and angiogenesis: regulation of hypoxia-inducible factors via novel binding factors. Exp Mol Med 41:849–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Logsdon EA, Finley SD, Popel AS, MacGabhann F (2014) A systems biology view of blood vessel growth and remodelling. J Cell Mol Med 18:1491–1508

    Article  PubMed  Google Scholar 

  79. Lu J, Pompili VJ, Das H (2013) Vascular stem cells in regulation of angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 123–138

    Chapter  Google Scholar 

  80. Jewell UR, Kvietikova I, Scheid A et al (2001) Induction of HIF-1alpha in response to hypoxia is instantaneous. FASEB J 15:1312–1314

    CAS  PubMed  Google Scholar 

  81. Kuwano M, Fukushi J, Okamoto M et al (2001) Angiogenesis factors. Intern Med 40:565–572

    Article  CAS  PubMed  Google Scholar 

  82. Hayakawa H, Shibasaki F (2013) Regulation of angiogenesis by hypoxia-inducible factors. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 93–106

    Chapter  Google Scholar 

  83. Ouma GO, Jonas RA, Usman MHU, Mohler ER (2012) Targets and delivery methods for therapeutic angiogenesis in peripheral artery disease. Vasc Med 17:174–192

    Article  PubMed  PubMed Central  Google Scholar 

  84. Tekin D, Dursun AD, Xi L (2010) Hypoxia inducible factor 1 (HIF-1) and cardioprotection. Acta Pharmacol Sin 31:1085–1094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Kelly BD, Hackett SF, Hirota K et al (2003) Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res 93:1074–1081

    Article  CAS  PubMed  Google Scholar 

  86. Madanecki P, Kapoor N, Bebok Z et al (2013) Regulation of angiogenesis by hypoxia: the role of microRNA. Cell Mol Biol Lett 18:47–57

    Article  CAS  PubMed  Google Scholar 

  87. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9:677–684

    Article  CAS  PubMed  Google Scholar 

  88. Roy H, Bhardwaj S, Ylä-Herttuala S (2006) Biology of vascular endothelial growth factors. FEBS Lett 580:2879–2887

    Article  CAS  PubMed  Google Scholar 

  89. Melly LF, Marsano A, Frobert A et al (2012) Controlled angiogenesis in the heart by cell-based expression of specific vascular endothelial growth factor levels. Hum Gene Ther Methods 23:346–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Zachary I, Morgan RD (2011) Therapeutic angiogenesis for cardiovascular disease: biological context, challenges, prospects. Heart 97:181–189

    Article  CAS  PubMed  Google Scholar 

  91. Oka T, Akazawa H, Naito AT, Komuro I (2014) Angiogenesis and cardiac hypertrophy: maintenance of cardiac function and causative roles in heart failure. Circ Res 114:565–571

    Article  CAS  PubMed  Google Scholar 

  92. Ferrara N, Davis-Smyth T (2006) The biology of vascular endothelial growth factor. Endocr Rev 19:61–69

    Google Scholar 

  93. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 7:359–371

    Article  CAS  PubMed  Google Scholar 

  94. Bates DO, Harper SJ (2002) Regulation of vascular permeability by vascular endothelial growth factors. Vascul Pharmacol 39:225–237

    Article  CAS  PubMed  Google Scholar 

  95. Ylä-Herttuala S, Rissanen TT, Vajanto I, Hartikainen J (2007) Vascular endothelial growth factors: biology and current status of clinical applications in cardiovascular medicine. J Am Coll Cardiol 49:1015–1026

    Article  PubMed  CAS  Google Scholar 

  96. Fujita Y, Asahara T, Kawamoto A (2013) Angiogenesis in myocardial ischemia. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 261–283

    Chapter  Google Scholar 

  97. Tammela T, Enholm B, Alitalo K, Paavonen K (2005) The biology of vascular endothelial growth factors. Cardiovasc Res 65:550–563

    Article  CAS  PubMed  Google Scholar 

  98. Hartmann BR, Bassenge E, Hartmann M (1997) Effects of serial percutaneous application of carbon dioxide in intermittent claudication: results of a controlled trial. Angiology 48:957–963

    Article  CAS  PubMed  Google Scholar 

  99. Bruce DJ, Tan PH (2013) Endothelial growth factor receptors in angiogenesis. In: Mehta JL, Dhalla NS (eds) Biochemical basis and therapeutic implications of angiogenesis. Springer Science+Business Media, LLC, New York, pp 3–22

    Chapter  Google Scholar 

  100. Lähteenvuo J, Rosenzweig A (2012) Effects of aging on angiogenesis. Circ Res 110:1252–1263

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Prabhakar NR, Seneza GL (2015) Oxygen sensing and homeostasis. Phys Ther 30:340–348

    CAS  Google Scholar 

  102. Schmidt KL (2009) Carbon dioxide bath (Carbon dioxide spring). http://www.nutecint.com/Docs/Carbon%20Dioxide%20Bath.pdf. Accessed 20 Sept 2009

  103. Schott A (1928) Carbon-dioxide thermo-saline springs in the light of modern research. Proc R Soc Med 21(4):589–597

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Falagas ME, Zarkadoulia E, Rafailidis PI (2009) The therapeutic effect of balneotherapy: evaluation of the evidence from randomised controlled trials. Int J Clin Pract 63:1068–1084

    Article  CAS  PubMed  Google Scholar 

  105. Hartmann BR, Bassenge E, Pittler M (1997) Effect of carbon dioxide-enriched water and fresh water on the cutaneous microcirculation and oxygen tension in the skin of the foot. Angiology 48:337–343

    Article  CAS  PubMed  Google Scholar 

  106. Pagourelias ED, Zorou PG, Tsaligopoulos M et al (2011) Carbon dioxide balneotherapy and cardiovascular disease. Int J Biometeorol 55:657–663

    Article  PubMed  Google Scholar 

  107. Nishimura N, Sugenoya J, Matsumoto T et al (2002) Effects of repeated carbon dioxide-rich water bathing on core temperature, cutaneous blood flow and thermal sensation. Eur J Appl Physiol 87:337–342

    Article  CAS  PubMed  Google Scholar 

  108. Ernst E (1989) Peripheral vascular disease. BMJ 299:873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Irie H, Tatsumi T, Takamiya M et al (2005) Carbon dioxide-rich water bathing enhances collateral blood flow in ischemic hindlimb via mobilization of endothelial progenitor cells and activation of NO-cGMP system. Circulation 111:1523–1529

    Article  PubMed  Google Scholar 

  110. Hashimoto M, Yamamoto N (2004) Decrease in heart rates by artificial CO2 hot spring bathing is inhibited by beta1-adrenoceptor blockade in anesthetized rats. J Appl Physiol 96:226–232

    Article  CAS  PubMed  Google Scholar 

  111. Izumi Y, Yamaguchi T, Yamazaki T et al (2015) Percutaneous carbon dioxide treatment using a gas mist generator enhances the collateral blood flow in the ischemic hindlimb. J Atheroscler Thromb 22:38–51

    Article  PubMed  Google Scholar 

  112. Nonaka K, Akiyama J, Tatsuta N et al (2013) Carbon dioxide water bathing enhances myogenin but not MyoD protein expression after skeletal muscle injury. J Phys Ther Sci 25:709–711

    Article  PubMed  PubMed Central  Google Scholar 

  113. Bloor CM (2005) Angiogenesis during exercise and training. Angiogenesis 8:263–271

    Article  PubMed  Google Scholar 

  114. Dhalla NS (2015) CO2-enriched water bath as a novel therapy for peripheral vascular disease. J Heart Dis 12:38

    Google Scholar 

  115. Dhalla NS (2015) Molecular basis for the beneficial effects of CO2-water bath therapy in peripheral artery disease. Curr Res Cardiol 2:115

    Google Scholar 

  116. Elimban V, Xu YJ, Dhalla NS (2014) Beneficial effects of CO2-enriched water bath treatment on blood flow and angiogenesis in ischemic hind limbs. Curr Res Cardiol 1:40

    Google Scholar 

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Acknowledgements

The financial support for this project was provided by Mitsubishi Rayon Cleansui Co., Ltd., Tokyo, Japan. The infrastructural support was provided by the St. Boniface Hospital Research Foundation.

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Authors and Affiliations

  1. Institute of Cardiovascular Sciences, St. Boniface Hospital Albrechtsen Research Centre, Department of Physiology and Pathophysiology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, 351 Tache Avenue, Winnipeg, Manitoba, Canada, R2H 2A6

    Naranjan S. Dhalla, Rebeca O. Camargo, Vijayan Elimban, Ravideep S. Dhadial & Yan-Jun Xu

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  1. Naranjan S. Dhalla
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  2. Rebeca O. Camargo
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Correspondence to Naranjan S. Dhalla .

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Editors and Affiliations

  1. Divison of Cardiovascular Medicine, University of Arkansas for Medical Sciences, Central Arkansas Veterans Healthcare System, Little Rock, Arkansas, USA

    Jawahar L. Mehta

  2. Department of Medicine, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA

    Pankaj Mathur

  3. Institute of Cardiovascular Sciences, St. Boniface Hospital Albrechtsen Research Centre, Department of Physiology and Pathophysiology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba, Canada

    Naranjan S. Dhalla

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Dhalla, N.S., Camargo, R.O., Elimban, V., Dhadial, R.S., Xu, YJ. (2017). Role of Skeletal Muscle Angiogenesis in Peripheral Artery Disease. In: Mehta, J., Mathur, P., Dhalla, N. (eds) Biochemical Basis and Therapeutic Implications of Angiogenesis. Advances in Biochemistry in Health and Disease, vol 6. Springer, Cham. https://doi.org/10.1007/978-3-319-61115-0_23

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