Skip to main content
Top
Published in: Journal of Translational Medicine 1/2009

Open Access 01-12-2009 | Methodology

Combined intermittent hypoxia and surface muscle electrostimulation as a method to increase peripheral blood progenitor cell concentration

Authors: Ginés Viscor, Casimiro Javierre, Teresa Pagès, Josep-Lluis Ventura, Antoni Ricart, Gregorio Martin-Henao, Carmen Azqueta, Ramon Segura

Published in: Journal of Translational Medicine | Issue 1/2009

Login to get access

Abstract

Background

Our goal was to determine whether short-term intermittent hypoxia exposure, at a level well tolerated by healthy humans and previously shown by our group to increase EPO and erythropoiesis, could mobilize hematopoietic stem cells (HSC) and increase their presence in peripheral circulation.

Methods

Four healthy male subjects were subjected to three different protocols: one with only a hypoxic stimulus (OH), another with a hypoxic stimulus plus muscle electrostimulation (HME) and the third with only muscle electrostimulation (OME). Intermittent hypobaric hypoxia exposure consisted of only three sessions of three hours at barometric pressure 540 hPa (equivalent to an altitude of 5000 m) for three consecutive days, whereas muscular electrostimulation was performed in two separate periods of 25 min in each session. Blood samples were obtained from an antecubital vein on three consecutive days immediately before the experiment and 24 h, 48 h, 4 days and 7 days after the last day of hypoxic exposure.

Results

There was a clear increase in the number of circulating CD34+ cells after combined hypobaric hypoxia and muscular electrostimulation. This response was not observed after the isolated application of the same stimuli.

Conclusion

Our results open a new application field for hypobaric systems as a way to increase efficiency in peripheral HSC collection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Asahara T, Murohara T, Sullivan A, Silver M, Zee van der R, Li T, Witzenbichler B, Schatteman G, Isner JM: Isolation of putative progenitor endothelial cells for angiogenesis. Science (New York, N Y). 1997, 275: 964-967.CrossRef Asahara T, Murohara T, Sullivan A, Silver M, Zee van der R, Li T, Witzenbichler B, Schatteman G, Isner JM: Isolation of putative progenitor endothelial cells for angiogenesis. Science (New York, N Y). 1997, 275: 964-967.CrossRef
2.
go back to reference Ferrario M, Massa M, Rosti V, Campanelli R, Ferlini M, Marinoni B, De Ferrari GM, Meli V, De Amici M, Repetto A, Verri A, Bramucci E, Tavazzi L: Early haemoglobin-independent increase of plasma erythropoietin levels in patients with acute myocardial infarction. Eur Heart J. 2007, 28: 1805-1813. 10.1093/eurheartj/ehm065.CrossRefPubMed Ferrario M, Massa M, Rosti V, Campanelli R, Ferlini M, Marinoni B, De Ferrari GM, Meli V, De Amici M, Repetto A, Verri A, Bramucci E, Tavazzi L: Early haemoglobin-independent increase of plasma erythropoietin levels in patients with acute myocardial infarction. Eur Heart J. 2007, 28: 1805-1813. 10.1093/eurheartj/ehm065.CrossRefPubMed
3.
go back to reference Theiss HD, David R, Engelmann MG, Barth A, Schotten K, Naebauer M, Reichart B, Steinbeck G, Franz WM: Circulation of CD34+ progenitor cell populations in patients with idiopathic dilated and ischaemic cardiomyopathy (DCM and ICM). Eur Heart J. 2007, 28: 1258-1264. 10.1093/eurheartj/ehm011.CrossRefPubMed Theiss HD, David R, Engelmann MG, Barth A, Schotten K, Naebauer M, Reichart B, Steinbeck G, Franz WM: Circulation of CD34+ progenitor cell populations in patients with idiopathic dilated and ischaemic cardiomyopathy (DCM and ICM). Eur Heart J. 2007, 28: 1258-1264. 10.1093/eurheartj/ehm011.CrossRefPubMed
4.
go back to reference Roberts N, Xiao Q, Weir G, Xu Q, Jahangiri M: Endothelial Progenitor Cells are Mobilized After Cardiac Surgery. Ann Thorac Surg. 2007, 83: 598-605. 10.1016/j.athoracsur.2006.09.087.CrossRefPubMed Roberts N, Xiao Q, Weir G, Xu Q, Jahangiri M: Endothelial Progenitor Cells are Mobilized After Cardiac Surgery. Ann Thorac Surg. 2007, 83: 598-605. 10.1016/j.athoracsur.2006.09.087.CrossRefPubMed
5.
go back to reference Steiner S, Niessner A, Ziegler S, Richter B, Seidinger D, Pleiner J, Penka M, Wolzt M, Huber K, Wojta J, Minar E, Kopp CW: Endurance training increases the number of endothelial progenitor cells in patients with cardiovascular risk and coronary artery disease. Atherosclerosis. 2005, 181: 305-310. 10.1016/j.atherosclerosis.2005.01.006.CrossRefPubMed Steiner S, Niessner A, Ziegler S, Richter B, Seidinger D, Pleiner J, Penka M, Wolzt M, Huber K, Wojta J, Minar E, Kopp CW: Endurance training increases the number of endothelial progenitor cells in patients with cardiovascular risk and coronary artery disease. Atherosclerosis. 2005, 181: 305-310. 10.1016/j.atherosclerosis.2005.01.006.CrossRefPubMed
6.
go back to reference Hoetzer GL, Van Guilder GP, Irmiger HM, Keith RS, Stauffer BL, DeSouza CA: Aging, exercise, and endothelial progenitor cell clonogenic and migratory capacity in men. J Appl Physiol. 2007, 102: 847-852. 10.1152/japplphysiol.01183.2006.CrossRefPubMed Hoetzer GL, Van Guilder GP, Irmiger HM, Keith RS, Stauffer BL, DeSouza CA: Aging, exercise, and endothelial progenitor cell clonogenic and migratory capacity in men. J Appl Physiol. 2007, 102: 847-852. 10.1152/japplphysiol.01183.2006.CrossRefPubMed
7.
go back to reference Meng X, Ichim T, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan K, Thebaud B, Riordan N: Endometrial regenerative cells: A novel stem cell population. Journal of Translational Medicine. 2007, 5: 57-10.1186/1479-5876-5-57.PubMedCentralCrossRefPubMed Meng X, Ichim T, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan K, Thebaud B, Riordan N: Endometrial regenerative cells: A novel stem cell population. Journal of Translational Medicine. 2007, 5: 57-10.1186/1479-5876-5-57.PubMedCentralCrossRefPubMed
8.
go back to reference Kondo T, Hayashi M, Takeshita K, Numaguchi Y, Kobayashi K, Iino S, Inden Y, Murohara T: Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler Thromb Vasc Biol. 2004, 24: 1442-1447. 10.1161/01.ATV.0000135655.52088.c5.CrossRefPubMed Kondo T, Hayashi M, Takeshita K, Numaguchi Y, Kobayashi K, Iino S, Inden Y, Murohara T: Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler Thromb Vasc Biol. 2004, 24: 1442-1447. 10.1161/01.ATV.0000135655.52088.c5.CrossRefPubMed
9.
go back to reference Zhu Ll, Zhao T, Li Hs, Zhao H, Wu Ly, Ding As, Fan Wh, Fan M: Neurogenesis in the adult rat brain after intermittent hypoxia. Brain Res. 2005, 1055: 1-6. 10.1016/j.brainres.2005.04.075.CrossRefPubMed Zhu Ll, Zhao T, Li Hs, Zhao H, Wu Ly, Ding As, Fan Wh, Fan M: Neurogenesis in the adult rat brain after intermittent hypoxia. Brain Res. 2005, 1055: 1-6. 10.1016/j.brainres.2005.04.075.CrossRefPubMed
10.
go back to reference Qiang Xu, Penka M, Wolzt M, Huber K, Wojta J, Minar E, Kopp CW: Hypoxia-Induced Astrocytes Promote the Migration of Neural Progenitor Cells Via Vascular Endothelial Factor, Stem Cell Factor, Stromal-Derived Factor-1alpha and Monocyte Chemoattractant Protein-1 Upregulation in Vitro. Clin Exp Pharmacol Physiol. 2007, 34: 624-631. 10.1111/j.1440-1681.2007.04619.x.CrossRef Qiang Xu, Penka M, Wolzt M, Huber K, Wojta J, Minar E, Kopp CW: Hypoxia-Induced Astrocytes Promote the Migration of Neural Progenitor Cells Via Vascular Endothelial Factor, Stem Cell Factor, Stromal-Derived Factor-1alpha and Monocyte Chemoattractant Protein-1 Upregulation in Vitro. Clin Exp Pharmacol Physiol. 2007, 34: 624-631. 10.1111/j.1440-1681.2007.04619.x.CrossRef
11.
go back to reference Grayson W, Zhao F, Bunnell B, Ma T: Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun. 2007, 358: 948-953. 10.1016/j.bbrc.2007.05.054.CrossRefPubMed Grayson W, Zhao F, Bunnell B, Ma T: Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun. 2007, 358: 948-953. 10.1016/j.bbrc.2007.05.054.CrossRefPubMed
12.
go back to reference Flames N, Pla R, Gelman DM, Rubenstein JLR, Puelles L, Marin O: Delineation of Multiple Subpallial Progenitor Domains by the Combinatorial Expression of Transcriptional Codes. J Neurosci. 2007, 27: 9682-9695. 10.1523/JNEUROSCI.2750-07.2007.CrossRefPubMed Flames N, Pla R, Gelman DM, Rubenstein JLR, Puelles L, Marin O: Delineation of Multiple Subpallial Progenitor Domains by the Combinatorial Expression of Transcriptional Codes. J Neurosci. 2007, 27: 9682-9695. 10.1523/JNEUROSCI.2750-07.2007.CrossRefPubMed
13.
go back to reference Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Böhm M, Nickenig G: Circulating Endothelial Progenitor Cells and Cardiovascular Outcomes. N Engl J Med. 2005, 353: 999-1007. 10.1056/NEJMoa043814.CrossRefPubMed Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Böhm M, Nickenig G: Circulating Endothelial Progenitor Cells and Cardiovascular Outcomes. N Engl J Med. 2005, 353: 999-1007. 10.1056/NEJMoa043814.CrossRefPubMed
14.
go back to reference Miller-Kasprzak E, Jagodzinski PP: Endothelial progenitor cells as a new agent contributing to vascular repair. Arch Immunol Ther Exp (Warsz). 2007, 55: 247-259. 10.1007/s00005-007-0027-5.CrossRef Miller-Kasprzak E, Jagodzinski PP: Endothelial progenitor cells as a new agent contributing to vascular repair. Arch Immunol Ther Exp (Warsz). 2007, 55: 247-259. 10.1007/s00005-007-0027-5.CrossRef
15.
go back to reference Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C, Klinge H, Schümichen C, Nienaber CA, Freund M, Steinhoff G: Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet. 2003, 361: 45-46. 10.1016/S0140-6736(03)12110-1.CrossRefPubMed Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C, Klinge H, Schümichen C, Nienaber CA, Freund M, Steinhoff G: Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet. 2003, 361: 45-46. 10.1016/S0140-6736(03)12110-1.CrossRefPubMed
16.
go back to reference Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, Silva GV, Belém L, Vivacqua R, Rangel FO, Esporcatte R, Geng YJ, Vaughn WK, Assad JA, Mesquita ET, Willerson JT: Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation. 2003, 107: 2294-2302. 10.1161/01.CIR.0000070596.30552.8B.CrossRefPubMed Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, Silva GV, Belém L, Vivacqua R, Rangel FO, Esporcatte R, Geng YJ, Vaughn WK, Assad JA, Mesquita ET, Willerson JT: Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation. 2003, 107: 2294-2302. 10.1161/01.CIR.0000070596.30552.8B.CrossRefPubMed
17.
go back to reference Cashen AF, Lazarus HM, Devine SM: Mobilizing stem cells from normal donors: is it possible to improve upon G-CSF?. Bone Marrow Transplant. 2007, 39: 577-588. 10.1038/sj.bmt.1705616.CrossRefPubMed Cashen AF, Lazarus HM, Devine SM: Mobilizing stem cells from normal donors: is it possible to improve upon G-CSF?. Bone Marrow Transplant. 2007, 39: 577-588. 10.1038/sj.bmt.1705616.CrossRefPubMed
18.
go back to reference Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grünwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM: Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation. 2002, 106: 3009-3017. 10.1161/01.CIR.0000043246.74879.CD.CrossRefPubMed Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grünwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM: Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation. 2002, 106: 3009-3017. 10.1161/01.CIR.0000043246.74879.CD.CrossRefPubMed
19.
go back to reference Valina C, Pinkernell K, Song YH, Bai X, Sadat S, Campeau RJ, Le Jemtel TH, Alt E: Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J. 2007, 28: 2667-2677. 10.1093/eurheartj/ehm426.CrossRefPubMed Valina C, Pinkernell K, Song YH, Bai X, Sadat S, Campeau RJ, Le Jemtel TH, Alt E: Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction. Eur Heart J. 2007, 28: 2667-2677. 10.1093/eurheartj/ehm426.CrossRefPubMed
20.
go back to reference Bahlmann FH, de Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D: Erythropoietin regulates endothelial progenitor cells. Blood. 2004, 103: 921-926. 10.1182/blood-2003-04-1284.CrossRefPubMed Bahlmann FH, de Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D: Erythropoietin regulates endothelial progenitor cells. Blood. 2004, 103: 921-926. 10.1182/blood-2003-04-1284.CrossRefPubMed
21.
go back to reference Westenbrink BD, Lipsic E, Meer van der P, Harst van der P, Oeseburg H, Du Marchie Sarvaas GJ, Koster J, Voors AA, van Veldhuisen DJ, van Gilst WH, Schoemaker RG: Erythropoietin improves cardiac function through endothelial progenitor cell and vascular endothelial growth factor mediated neovascularization. Eur Heart J. 2007, 28: 2018-2027. 10.1093/eurheartj/ehm177.CrossRefPubMed Westenbrink BD, Lipsic E, Meer van der P, Harst van der P, Oeseburg H, Du Marchie Sarvaas GJ, Koster J, Voors AA, van Veldhuisen DJ, van Gilst WH, Schoemaker RG: Erythropoietin improves cardiac function through endothelial progenitor cell and vascular endothelial growth factor mediated neovascularization. Eur Heart J. 2007, 28: 2018-2027. 10.1093/eurheartj/ehm177.CrossRefPubMed
22.
go back to reference Serebrovskaya TV: Intermittent hypoxia research in the former Soviet Union and the Commonwealth of independent states: History and review of the concept and selected applications. High Alt Med Biol. 2002, 3: 205-221. 10.1089/15270290260131939.CrossRefPubMed Serebrovskaya TV: Intermittent hypoxia research in the former Soviet Union and the Commonwealth of independent states: History and review of the concept and selected applications. High Alt Med Biol. 2002, 3: 205-221. 10.1089/15270290260131939.CrossRefPubMed
23.
go back to reference Levine BD: Intermittent Hypoxic Training: Fact and Fancy. High Alt Med Biol. 2002, 3: 177-193. 10.1089/15270290260131911.CrossRefPubMed Levine BD: Intermittent Hypoxic Training: Fact and Fancy. High Alt Med Biol. 2002, 3: 177-193. 10.1089/15270290260131911.CrossRefPubMed
24.
go back to reference Levine BD, Stray-Gundersen J: "Living high-training low": effect of moderate-altitude acclimatization with low-altitude training on performance. J Appl Physiol. 1997, 83: 102-112.PubMed Levine BD, Stray-Gundersen J: "Living high-training low": effect of moderate-altitude acclimatization with low-altitude training on performance. J Appl Physiol. 1997, 83: 102-112.PubMed
25.
go back to reference Koutedakis Y, Frischknecht R, Vrbova G, Sharp NC, Budgett R: Maximal voluntary quadriceps strength patterns in Olympic overtrained athletes. Med Sci Sports Exerc. 1995, 27: 566-572.CrossRefPubMed Koutedakis Y, Frischknecht R, Vrbova G, Sharp NC, Budgett R: Maximal voluntary quadriceps strength patterns in Olympic overtrained athletes. Med Sci Sports Exerc. 1995, 27: 566-572.CrossRefPubMed
26.
go back to reference Crameri RM, Weston A, Climstein M, Davis GM, Sutton JR: Effects of electrical stimulation-induced leg training on skeletal muscle adaptability in spinal cord injury. Scand J Med Sci Sports. 2002, 12: 316-322. 10.1034/j.1600-0838.2002.20106.x.CrossRefPubMed Crameri RM, Weston A, Climstein M, Davis GM, Sutton JR: Effects of electrical stimulation-induced leg training on skeletal muscle adaptability in spinal cord injury. Scand J Med Sci Sports. 2002, 12: 316-322. 10.1034/j.1600-0838.2002.20106.x.CrossRefPubMed
27.
go back to reference Brocherie F, Babault N, Cometti G, Maffiuletti N, Chatard JC: Electrostimulation training effects on the physical performance of ice hockey players. Med Sci Sports Exerc. 2005, 37: 455-460. 10.1249/01.MSS.0000155396.51293.9F.CrossRefPubMed Brocherie F, Babault N, Cometti G, Maffiuletti N, Chatard JC: Electrostimulation training effects on the physical performance of ice hockey players. Med Sci Sports Exerc. 2005, 37: 455-460. 10.1249/01.MSS.0000155396.51293.9F.CrossRefPubMed
28.
go back to reference Panisello P, Torrella JR, Pages T, Viscor G: Capillary Supply and Fiber Morphometry in Rat Myocardium after Intermittent Exposure to Hypobaric Hypoxia. High Alt Med Biol. 2007, 8: 322-330. 10.1089/ham.2007.1030.CrossRefPubMed Panisello P, Torrella JR, Pages T, Viscor G: Capillary Supply and Fiber Morphometry in Rat Myocardium after Intermittent Exposure to Hypobaric Hypoxia. High Alt Med Biol. 2007, 8: 322-330. 10.1089/ham.2007.1030.CrossRefPubMed
29.
go back to reference Panisello P, Torrella JR, Esteva S, Pages T, Viscor G: Capillary supply, fibre types and fibre morphometry in rat tibialis anterior and diaphragm muscles after intermittent exposure to hypobaric hypoxia. Eur J Appl Physiol. 2008, 103: 203-213. 10.1007/s00421-008-0691-0.CrossRefPubMed Panisello P, Torrella JR, Esteva S, Pages T, Viscor G: Capillary supply, fibre types and fibre morphometry in rat tibialis anterior and diaphragm muscles after intermittent exposure to hypobaric hypoxia. Eur J Appl Physiol. 2008, 103: 203-213. 10.1007/s00421-008-0691-0.CrossRefPubMed
30.
go back to reference Rodriguez FA, Ventura JL, Casas M, Casas H, Pages T, Rama R, Ricart A, Palacios L, Viscor G: Erythropoietin acute reaction and haematological adaptations to short, intermittent hypobaric hypoxia. Eur J Appl Physiol. 2000, 82: 170-177. 10.1007/s004210050669.CrossRefPubMed Rodriguez FA, Ventura JL, Casas M, Casas H, Pages T, Rama R, Ricart A, Palacios L, Viscor G: Erythropoietin acute reaction and haematological adaptations to short, intermittent hypobaric hypoxia. Eur J Appl Physiol. 2000, 82: 170-177. 10.1007/s004210050669.CrossRefPubMed
31.
go back to reference Bennie SD, Petrofsky JS, Nisperos J, Tsurudome M, Laymon M: Toward the optimal waveform for electrical stimulation of human muscle. Eur J Appl Physiol. 2002, 88: 13-19. 10.1007/s00421-002-0711-4.CrossRefPubMed Bennie SD, Petrofsky JS, Nisperos J, Tsurudome M, Laymon M: Toward the optimal waveform for electrical stimulation of human muscle. Eur J Appl Physiol. 2002, 88: 13-19. 10.1007/s00421-002-0711-4.CrossRefPubMed
32.
go back to reference Keeney M, Chin-Yee I, Weir K, Popma J, Nayar R, Sutherland DR: Single platform flow cytometric absolute CD34+ cell counts based on the ISHAGE guidelines. International Society of Hematotherapy and Graft Engineering. Cytometry. 1998, 34: 61-70. 10.1002/(SICI)1097-0320(19980415)34:2<61::AID-CYTO1>3.0.CO;2-F.CrossRefPubMed Keeney M, Chin-Yee I, Weir K, Popma J, Nayar R, Sutherland DR: Single platform flow cytometric absolute CD34+ cell counts based on the ISHAGE guidelines. International Society of Hematotherapy and Graft Engineering. Cytometry. 1998, 34: 61-70. 10.1002/(SICI)1097-0320(19980415)34:2<61::AID-CYTO1>3.0.CO;2-F.CrossRefPubMed
33.
go back to reference Valgimigli M, Rigolin GM, Cittanti C, Malagutti P, Curello S, Percoco G, Bugli AM, Della Porta M, Bragotti LZ, Ansani L, Mauro E, Lanfranchi A, Giganti M, Feggi L, Castoldi G, Ferrari R: Use of granulocyte-colony stimulating factor during acute myocardial infarction to enhance bone marrow stem cell mobilization in humans: clinical and angiographic safety profile. Eur Heart J. 2005, 26: 1838-1845. 10.1093/eurheartj/ehi289.CrossRefPubMed Valgimigli M, Rigolin GM, Cittanti C, Malagutti P, Curello S, Percoco G, Bugli AM, Della Porta M, Bragotti LZ, Ansani L, Mauro E, Lanfranchi A, Giganti M, Feggi L, Castoldi G, Ferrari R: Use of granulocyte-colony stimulating factor during acute myocardial infarction to enhance bone marrow stem cell mobilization in humans: clinical and angiographic safety profile. Eur Heart J. 2005, 26: 1838-1845. 10.1093/eurheartj/ehi289.CrossRefPubMed
34.
go back to reference Falanga A, Marchetti M, Evangelista V, Manarini S, Oldani E, Giovanelli S, Galbusera M, Cerletti C, Barbui T: Neutrophil activation and hemostatic changes in healthy donors receiving granulocyte colony-stimulating factor. Blood. 1999, 93: 2506-2514.PubMed Falanga A, Marchetti M, Evangelista V, Manarini S, Oldani E, Giovanelli S, Galbusera M, Cerletti C, Barbui T: Neutrophil activation and hemostatic changes in healthy donors receiving granulocyte colony-stimulating factor. Blood. 1999, 93: 2506-2514.PubMed
35.
go back to reference Gutierrez-Delgado F, Bensinger W: Safety of granulocyte colony-stimulating factor in normal donors. Curr Opin Hematol. 2001, 8: 155-160. 10.1097/00062752-200105000-00005.CrossRefPubMed Gutierrez-Delgado F, Bensinger W: Safety of granulocyte colony-stimulating factor in normal donors. Curr Opin Hematol. 2001, 8: 155-160. 10.1097/00062752-200105000-00005.CrossRefPubMed
36.
go back to reference Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T: Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation. 2001, 103: 2776-2779. 10.1161/hc2301.092122.CrossRefPubMed Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T: Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation. 2001, 103: 2776-2779. 10.1161/hc2301.092122.CrossRefPubMed
37.
go back to reference Adams V, Lenk K, Linke A, Lenz D, Erbs S, Sandri M, Tarnok A, Gielen S, Emmrich F, Schuler G, Hambrecht R: Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arterioscler Thromb Vasc Biol. 2004, 24: 684-690. 10.1161/01.ATV.0000124104.23702.a0.CrossRefPubMed Adams V, Lenk K, Linke A, Lenz D, Erbs S, Sandri M, Tarnok A, Gielen S, Emmrich F, Schuler G, Hambrecht R: Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arterioscler Thromb Vasc Biol. 2004, 24: 684-690. 10.1161/01.ATV.0000124104.23702.a0.CrossRefPubMed
38.
go back to reference Laufs U, Urhausen A, Werner N, Scharhag J, Heitz A, Kissner G, Böhm M, Kindermann W, Nickenig G: Running exercise of different duration and intensity: effect on endothelial progenitor cells in healthy subjects. Eur J Cardiovasc Prev Rehabil. 2005, 12: 407-414. 10.1097/01.hjr.0000174823.87269.2e.CrossRefPubMed Laufs U, Urhausen A, Werner N, Scharhag J, Heitz A, Kissner G, Böhm M, Kindermann W, Nickenig G: Running exercise of different duration and intensity: effect on endothelial progenitor cells in healthy subjects. Eur J Cardiovasc Prev Rehabil. 2005, 12: 407-414. 10.1097/01.hjr.0000174823.87269.2e.CrossRefPubMed
39.
go back to reference Wahl P, Brixius K, Bloch W: Exercise-induced stem cell activation and its implication for cardiovascular and skeletal muscle regeneration. Minim Invasive Ther Allied Technol. 2008, 17: 91-99. 10.1080/13645700801969816.CrossRefPubMed Wahl P, Brixius K, Bloch W: Exercise-induced stem cell activation and its implication for cardiovascular and skeletal muscle regeneration. Minim Invasive Ther Allied Technol. 2008, 17: 91-99. 10.1080/13645700801969816.CrossRefPubMed
Metadata
Title
Combined intermittent hypoxia and surface muscle electrostimulation as a method to increase peripheral blood progenitor cell concentration
Authors
Ginés Viscor
Casimiro Javierre
Teresa Pagès
Josep-Lluis Ventura
Antoni Ricart
Gregorio Martin-Henao
Carmen Azqueta
Ramon Segura
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2009
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/1479-5876-7-91

Other articles of this Issue 1/2009

Journal of Translational Medicine 1/2009 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.