Int J Stem Cells.  2021 Feb;14(1):21-32. 10.15283/ijsc20088.

Autologous Bone-Marrow vs.Peripheral Blood Mononuclear Cells Therapy for Peripheral Artery Disease in Diabetic Patients

Affiliations
  • 1Department of Internal Medicine, Dr. Cipto Mangunkusumo National General Hospital, Faculty of Medicine Universitas Indonesia, Jakarta, Indonesia
  • 2Metabolic Disorder, Cardiovascular, and Aging Cluster, Indonesian Medical Education and Research Institute, Faculty of Medicine Universitas Indonesia, Jakarta, Indonesia
  • 3Department of Radiology, Dr. Cipto Mangunkusumo National General Hospital, Faculty of Medicine Universitas Indonesia, Jakarta, Indonesia

Abstract

Diabetes mellitus (DM) remains one of the most important risk factors for peripheral artery disease (PAD), with approximately 20% of DM patients older than 40 years old are affected with PAD. The current standard management for severe PAD is endovascular intervention with or without surgical bypass. Unfortunately, up to 40% of patients are unable to undergo these revascularization therapies due to excessive surgical risk or adverse vascular side effects. Stem cell therapy has emerged as a novel therapeutic strategy for these ‘no-option’ patients. Several types of stem cells are utilized for PAD therapy, including bone marrow mononuclear cells (BMMNC) and peripheral blood mononuclear cells (PBMNC). Many studies have reported the safety of BMMNC and PBMNC, as well as its efficacy in reducing ischemic pain, ulcer size, pain-free walking distance, ankle-brachial index (ABI), and transcutaneous oxygen pressure (TcPO2). However, the capacity to establish the efficacy of reducing major amputation rates, amputation free survival, and all-cause mortality is limited, as shown by several randomized placebo-controlled trials. The present literature review will focus on comparing safety and efficacy between BMMNC and PBMNC as cell-based management in diabetic patients with PAD who are not suitable for revascularization therapy.

Keyword

Peripheral artery disease; Diabetes mellitus; Stem cell therapy; Bone marrow mononuclear cells; Peripheral blood mononuclear cells

Figure

  • Fig. 1 A schematic diagram of angiogenesis process following stem cell injection of the affected area of PAD. EC: Endothelial Cells. Adapted from: Lawall H, et al. Thromb Haemost; 2010.


Reference

References

1. Hirsch AT, Haskal ZJ, Hertzer NR, Bakal CW, Creager MA, Halperin JL, Hiratzka LF, Murphy WR, Olin JW, Puschett JB, Rosenfield KA, Sacks D, Stanley JC, Taylor LM Jr, White CJ, White J, White RA, Antman EM, Smith SC Jr, Adams CD, Anderson JL, Faxon DP, Fuster V, Gibbons RJ, Halperin JL, Hiratzka LF, Hunt SA, Jacobs AK, Nishimura R, Ornato JP, Page RL, Riegel B. 2006; ACC/AHA 2005 guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): executive summary a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease) endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and Vascular Disease Foundation. J Am Coll Cardiol. 47:1239–1312. DOI: 10.1016/j.jacc.2005.10.009. PMID: 16545667.
2. Fowkes FG, Rudan D, Rudan I, Aboyans V, Denenberg JO, McDermott MM, Norman PE, Sampson UK, Williams LJ, Mensah GA, Criqui MH. 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. DOI: 10.1016/S0140-6736(13)61249-0. PMID: 23915883.
Article
3. Marso SP, Hiatt WR. 2006; Peripheral arterial disease in patients with diabetes. J Am Coll Cardiol. 47:921–929. DOI: 10.1016/j.jacc.2005.09.065. PMID: 16516072.
Article
4. Kamil S, Sehested TSG, Carlson N, Houlind K, Lassen JF, N Bang C, Dominguez H, Pedersen CT, Gislason GH. 2019; Diabetes and risk of peripheral artery disease in patients undergoing first-time coronary angiography between 2000 and 2012- a nationwide study. BMC Cardiovasc Disord. 19:234. DOI: 10.1186/s12872-019-1213-1. PMID: 31651241. PMCID: PMC6813965.
5. Maulahela H. 2013. Clinical outcome of percutaneus transluminal angioplasty in type 2 diabetic patient with peripheral arterial disease and distribution of factors that influenced clinical success [thesis]. Universitas Indonesia;Depok:
Article
6. Thiruvoipati T, Kielhorn CE, Armstrong EJ. 2015; Peripheral artery disease in patients with diabetes: epidemiology, mechanisms, and outcomes. World J Diabetes. 6:961–969. DOI: 10.4239/wjd.v6.i7.961. PMID: 26185603. PMCID: PMC4499529.
Article
7. Nehler MR, Duval S, Diao L, Annex BH, Hiatt WR, Rogers K, Zakharyan A, Hirsch AT. 2014; Epidemiology of peripheral arterial disease and critical limb ischemia in an insured national population. J Vasc Surg. 60:686–695. e. DOI: 10.1016/j.jvs.2014.03.290. PMID: 24820900.
Article
8. Sigvant B, Lundin F, Wahlberg E. 2016; The risk of disease progression in peripheral arterial disease is higher than expected: a meta-analysis of mortality and disease progression in peripheral arterial disease. Eur J Vasc Endovasc Surg. 51:395–403. DOI: 10.1016/j.ejvs.2015.10.022. PMID: 26777541.
Article
9. Duff S, Mafilios MS, Bhounsule P, Hasegawa JT. 2019; The burden of critical limb ischemia: a review of recent literature. Vasc Health Risk Manag. 15:187–208. DOI: 10.2147/VHRM.S209241. PMID: 31308682. PMCID: PMC6617560.
10. Mills JL. 2016; Lower limb ischaemia in patients with diabetic foot ulcers and gangrene: recognition, anatomic patterns and revascularization strategies. Diabetes Metab Res Rev. 32 Suppl 1:239–245. DOI: 10.1002/dmrr.2753. PMID: 26455728.
Article
11. Gerhard-Herman MD, Gornik HL, Barrett C, Barshes NR, Corriere MA, Drachman DE, Fleisher LA, Fowkes FG, Hamburg NM, Kinlay S, Lookstein R, Misra S, Mureebe L, Olin JW, Patel RA, Regensteiner JG, Schanzer A, Shishehbor MH, Stewart KJ, Treat-Jacobson D, Walsh ME. 2017; 2016 AHA/ACC guideline on the management of patients with lower extremity peripheral artery disease: executive summary: a report of the American college of cardiology/American Heart Association task force on clinical practice guidelines. Circulation. 135:e686–e725. DOI: 10.1161/CIR.0000000000000470. PMCID: PMC5479414. PMID: 27840332.
Article
12. Adam DJ, Beard JD, Cleveland T, Bell J, Bradbury AW, Forbes JF, Fowkes FG, Gillepsie I, Ruckley CV, Raab G, Storkey H. 2005; Bypass versus angioplasty in severe ischaemia of the leg (BASIL): multicentre, randomised controlled trial. Lancet. 366:1925–1934. DOI: 10.1016/S0140-6736(05)67704-5. PMID: 16325694.
Article
13. Kalra K, Tomar PC. 2014; Stem cell: basics, classification and applications. Am J Phytomed Clin Ther. 2:919–930.
14. Barky AR, Ali EMM, Mohamed TM. 2017; Stem cells, classifications and their clinical applications. Am J Pharmacol Ther. 1:1–7.
15. Volarevic V, Markovic BS, Gazdic M, Volarevic A, Jovicic N, Arsenijevic N, Armstrong L, Djonov V, Lako M, Stojkovic M. 2018; Ethical and safety issues of stem cell-based therapy. Int J Med Sci. 15:36–45. DOI: 10.7150/ijms.21666. PMID: 29333086. PMCID: PMC5765738.
Article
16. Silvestre JS, Mallat Z, Tedgui A, Lévy BI. 2008; Post-ischaemic neovascularization and inflammation. Cardiovasc Res. 78:242–249. DOI: 10.1093/cvr/cvn027. PMID: 18252762.
Article
17. Tuomisto TT, Rissanen TT, Vajanto I, Korkeela A, Rutanen J, Ylä-Herttuala S. 2004; HIF-VEGF-VEGFR-2, TNF- alpha and IGF pathways are upregulated in critical human skeletal muscle ischemia as studied with DNA array. Atherosclerosis. 174:111–120. DOI: 10.1016/j.atherosclerosis.2004.01.015. PMID: 15135259.
Article
18. Urbich C, Dimmeler S. 2004; Endothelial progenitor cells: characterization and role in vascular biology. Circ Res. 95:343–353. DOI: 10.1161/01.RES.0000137877.89448.78. PMID: 15321944.
19. Kolluru GK, Bir SC, Kevil CG. 2012; Endothelial dysfunction and diabetes: effects on angiogenesis, vascular remodeling, and wound healing. Int J Vasc Med. 2012:918267. DOI: 10.1155/2012/918267. PMID: 22611498. PMCID: PMC3348526.
Article
20. Mendoza MG, Robles HV, Romo E, Rios A, Escalante B. 2007; Nitric oxide-dependent neovascularization role in the lower extremity disease. Curr Pharm Des. 13:3591–3596. DOI: 10.2174/138161207782794103. PMID: 18220796.
Article
21. Santarelli JG, Udani V, Yung YC, Cheshier S, Wagers A, Brekken RA, Weissman I, Tse V. 2006; Incorporation of bone marrow-derived Flk-1-expressing CD34 cells in the endothelium of tumor vessels in the mouse brain. Neuro-surgery. 59:374–382. discussion 374–382. DOI: 10.1227/01.NEU.0000222658.66878.CC. PMID: 16883178.
Article
22. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. 1997; Isolation of putative progenitor endothelial cells for angio-genesis. Science. 275:964–967. DOI: 10.1126/science.275.5302.964. PMID: 9020076.
Article
23. Gnecchi M, Zhang Z, Ni A, Dzau VJ. 2008; Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 103:1204–1219. DOI: 10.1161/CIRCRESAHA.108.176826. PMID: 19028920. PMCID: PMC2667788.
Article
24. Xie J, March KL, Murphy MP. Mohler ER, Annex BH, editors. 2016. Bone marrow- derived cells: From the laboratory to the clinic. Regenerative Medicine for Peripheral Artery Disease. Elsevier Inc.;San Diego: p. 27–42. DOI: 10.1016/B978-0-12-801344-1.00003-6. PMCID: PMC4795089.
25. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. 2003; Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 348:593–600. DOI: 10.1056/NEJMoa022287. PMID: 12584367.
Article
26. Bompais H, Chagraoui J, Canron X, Crisan M, Liu XH, Anjo A, Tolla-Le Port C, Leboeuf M, Charbord P, Bikfalvi A, Uzan G. 2004; Human endothelial cells derived from circulating progenitors display specific functional properties compared with mature vessel wall endothelial cells. Blood. 103:2577–2584. DOI: 10.1182/blood-2003-08-2770. PMID: 14630797.
Article
27. Romagnani P, Annunziato F, Liotta F, Lazzeri E, Mazzinghi B, Frosali F, Cosmi L, Maggi L, Lasagni L, Scheffold A, Kruger M, Dimmeler S, Marra F, Gensini G, Maggi E, Romagnani S. 2005; CD14CD34low cells with stem cell phenotypic and functional features are the major source of circulating endothelial progenitors. Circ Res. 97:314–322. DOI: 10.1161/01.RES.0000177670.72216.9b. PMID: 16020753.
Article
28. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC. 2004; Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 104:2752–2760. DOI: 10.1182/blood-2004-04-1396. PMID: 15226175.
Article
29. Fadini GP, Losordo D, Dimmeler S. 2012; Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res. 110:624–637. DOI: 10.1161/CIRCRESAHA.111.243386. PMID: 22343557. PMCID: PMC3382070.
Article
30. Yoder MC. 2013; Endothelial progenitor cell: a blood cell by many other names may serve similar functions. J Mol Med (Berl). 91:285–295. DOI: 10.1007/s00109-013-1002-8. PMID: 23371317. PMCID: PMC3704045.
Article
31. Thirumala S, Goebel WS, Woods EJ. 2013; Manufacturing and banking of mesenchymal stem cells. Expert Opin Biol Ther. 13:673–691. DOI: 10.1517/14712598.2013.763925. PMID: 23339745.
Article
32. Nakagami H, Maeda K, Morishita R, Iguchi S, Nishikawa T, Takami Y, Kikuchi Y, Saito Y, Tamai K, Ogihara T, Kaneda Y. 2005; Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler Thromb Vasc Biol. 25:2542–2547. DOI: 10.1161/01.ATV.0000190701.92007.6d. PMID: 16224047.
Article
33. Iwashima S, Ozaki T, Maruyama S, Saka Y, Kobori M, Omae K, Yamaguchi H, Niimi T, Toriyama K, Kamei Y, Torii S, Murohara T, Yuzawa Y, Kitagawa Y, Matsuo S. 2009; Novel culture system of mesenchymal stromal cells from human subcutaneous adipose tissue. Stem Cells Dev. 18:533–543. DOI: 10.1089/scd.2008.0358. PMID: 19055360.
Article
34. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. 2000; Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A. 97:13625–13630. DOI: 10.1073/pnas.240309797. PMID: 11087820. PMCID: PMC17626.
35. Tomokiyo A, Yoshida S, Hamano S, Hasegawa D, Sugii H, Maeda H. 2018; Detection, characterization, and clinical application of mesenchymal stem cells in periodontal ligament tissue. Stem Cells Int. 2018:5450768. DOI: 10.1155/2018/5450768. PMID: 30224921. PMCID: PMC6129323.
Article
36. Ukai R, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. 2007; Mesenchymal stem cells derived from peripheral blood protects against ischemia. J Neurotrauma. 24:508–520. DOI: 10.1089/neu.2006.0161. PMID: 17402856. PMCID: PMC2605398.
Article
37. Kim SW, Han H, Chae GT, Lee SH, Bo S, Yoon JH, Lee YS, Lee KS, Park HK, Kang KS. 2006; Successful stem cell therapy using umbilical cord blood-derived multipotent stem cells for Buerger's disease and ischemic limb disease animal model. Stem Cells. 24:1620–1626. DOI: 10.1634/stemcells.2005-0365. PMID: 16497946.
Article
38. Romanov YA, Svintsitskaya VA, Smirnov VN. 2003; Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells. 21:105–110. DOI: 10.1634/stemcells.21-1-105. PMID: 12529557.
Article
39. Xu Y, Meng H, Li C, Hao M, Wang Y, Yu Z, Li Q, Han J, Zhai Q, Qiu L. 2010; Umbilical cord-derived mesenchymal stem cells isolated by a novel explantation technique can differentiate into functional endothelial cells and promote revascularization. Stem Cells Dev. 19:1511–1522. DOI: 10.1089/scd.2009.0321. PMID: 20170363.
Article
40. Oliveira MS, Barreto-Filho JB. 2015; Placental-derived stem cells: culture, differentiation and challenges. World J Stem Cells. 7:769–775. DOI: 10.4252/wjsc.v7.i4.769. PMID: 26029347. PMCID: PMC4444616.
Article
41. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Horwitz E. Prockop Dj. 2006; Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 8:315–317. DOI: 10.1080/14653240600855905. PMID: 16923606.
Article
42. Petrini M, Pacini S, Trombi L, Fazzi R, Montali M, Ikehara S, Abraham NG. 2009; Identification and purification of mesodermal progenitor cells from human adult bone marrow. Stem Cells Dev. 18:857–866. DOI: 10.1089/scd.2008.0291. PMID: 18991503. PMCID: PMC3085824.
Article
43. D'Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC. 2004; Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci. 117(Pt 14):2971–2981. DOI: 10.1242/jcs.01103. PMID: 15173316.
44. Subrammaniyan R, Amalorpavanathan J, Shankar R, Rajkumar M, Baskar S, Manjunath SR, Senthilkumar R, Murugan P, Srinivasan VR, Abraham S. 2011; Application of autologous bone marrow mononuclear cells in six patients with advanced chronic critical limb ischemia as a result of diabetes: our experience. Cytotherapy. 13:993–999. DOI: 10.3109/14653249.2011.579961. PMID: 21671823.
Article
45. Ponemone V, Gupta S, Sethi D, Suthar M, Sharma M, Powell RJ, Harris KL, Jungla N, Arambam P, Kaul U, Seth A, Bukhari S. 2017; Safety and effectiveness of bone marrow cell concentrate in the treatment of chronic critical limb ischemia utilizing a rapid point-of-care system. Stem Cells Int. 2017:4137626. DOI: 10.1155/2017/4137626. PMID: 28194186. PMCID: PMC5282442.
Article
46. Baker PK, Rhodes EG, Duguid JK. 1992; Effective concentration of bone marrow mononuclear cells using density gradient separation within an automated cell separator. Transfus Sci. 13:353–356. DOI: 10.1016/0955-3886(92)90147-9. PMID: 10148131.
Article
47. Aktas M, Radke TF, Strauer BE, Wernet P, Kogler G. 2008; Separation of adult bone marrow mononuclear cells using the automated closed separation system Sepax. Cyto-therapy. 10:203–211. DOI: 10.1080/14653240701851324. PMID: 18368599.
Article
48. Hermann PC, Huber SL, Herrler T, von Hesler C, Andrassy J, Kevy SV, Jacobson MS, Heeschen C. 2008; Concentration of bone marrow total nucleated cells by a point-of-care device provides a high yield and preserves their functional activity. Cell Transplant. 16:1059–1069. DOI: 10.3727/000000007783472363. PMID: 18351022.
Article
49. Autissier P, Soulas C, Burdo TH, Williams KC. 2010; Evaluation of a 12-color flow cytometry panel to study lymphocyte, monocyte, and dendritic cell subsets in humans. Cytometry A. 77:410–419. DOI: 10.1002/cyto.a.20859. PMID: 20099249.
Article
50. Bogoslovsky T, Wang D, Maric D, Scattergood-Keepper L, Spatz M, Auh S, Hallenbeck J. 2013; Cryopreservation and enumeration of human endothelial progenitor and endothelial cells for clinical trials. J Blood Disord Transfus. 4:158. DOI: 10.4172/2155-9864.1000158. PMID: 25309814. PMCID: PMC4193669.
Article
51. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. 1999; Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 5:434–438. DOI: 10.1038/7434. PMID: 10202935.
Article
52. Shepherd RM, Capoccia BJ, Devine SM, Dipersio J, Trinkaus KM, Ingram D, Link DC. 2006; Angiogenic cells can be rapidly mobilized and efficiently harvested from the blood following treatment with AMD3100. Blood. 108:3662–3667. DOI: 10.1182/blood-2006-06-030577. PMID: 16912220. PMCID: PMC1895468.
Article
53. Honold J, Lehmann R, Heeschen C, Walter DH, Assmus B, Sasaki K, Martin H, Haendeler J, Zeiher AM, Dimmeler S. 2006; Effects of granulocyte colony simulating factor on functional activities of endothelial progenitor cells in patients with chronic ischemic heart disease. Arterioscler Thromb Vasc Biol. 26:2238–2243. DOI: 10.1161/01.ATV.0000240248.55172.dd. PMID: 16902165.
Article
54. Bhattacharya P, Thiruppathi M, Elshabrawy HA, Alharshawi K, Kumar P, Prabhakar BS. 2015; GM-CSF: an immune modulatory cytokine that can suppress autoimmunity. Cytokine. 75:261–271. DOI: 10.1016/j.cyto.2015.05.030. PMID: 26113402. PMCID: PMC4553090.
Article
55. Gazitt Y. 2000; Immunologic profiles of effector cells and peripheral blood stem cells mobilized with different hematopoietic growth factors. Stem Cells. 18:390–398. DOI: 10.1634/stemcells.18-6-390. PMID: 11072026.
Article
56. Huang P, Li S, Han M, Xiao Z, Yang R, Han ZC. 2005; Autologous transplantation of granulocyte colony-stimulating factor-mobilized peripheral blood mononuclear cells improves critical limb ischemia in diabetes. Diabetes Care. 28:2155–2160. DOI: 10.2337/diacare.28.9.2155. PMID: 16123483.
Article
57. Ozturk A, Kucukardali Y, Tangi F, Erikci A, Uzun G, Bashekim C, Sen H, Terekeci H, Narin Y, Ozyurt M, Ozkan S, Sayan O, Rodop O, Nalbant S, Sıldıroglu O, Yalnız FF, Senkal IV, Sabuncu H, Oktenli C. 2012; Therapeutical potential of autologous peripheral blood mononuclear cell transplantation in patients with type 2 diabetic critical limb ischemia. J Diabetes Complications. 26:29–33. DOI: 10.1016/j.jdiacomp.2011.11.007. PMID: 22240264.
Article
58. Minamino K, Adachi Y, Okigaki M, Ito H, Togawa Y, Fujita K, Tomita M, Suzuki Y, Zhang Y, Iwasaki M, Nakano K, Koike Y, Matsubara H, Iwasaka T, Matsumura M, Ikehara S. 2005; Macrophage colony-stimulating factor (M- CSF), as well as granulocyte colony-stimulating factor (G- CSF), accelerates neovascularization. Stem Cells. 23:347–354. DOI: 10.1634/stemcells.2004-0190. PMID: 15749929.
Article
59. Lane TA, Law P, Maruyama M, Young D, Burgess J, Mullen M, Mealiffe M, Terstappen LW, Hardwick A, Moubayed M, Oldham F, Corringham RET, Ho AD. 1995; Harvesting and enrichment of hematopoietic progenitor cells mobilized into the peripheral blood of normal donors by granulocyte-mac-rophage colony-stimulating factor (GM-CSF) or G-CSF: potential role in allogeneic marrow transplantation. Blood. 85:275–282. DOI: 10.1182/blood.V85.1.275.bloodjournal851275. PMID: 7528570.
Article
60. Fischmeister G, Kurz M, Haas OA, Micksche M, Buchinger P, Printz D, Ressmann G, Stroebel T, Peters C, Fritsch G, Gadner H. 1999; G-CSF versus GM-CSF for stimulation of peripheral blood progenitor cells (PBPC) and leukocytes in healthy volunteers: comparison of efficacy and tolerability. Ann Hematol. 78:117–123. DOI: 10.1007/s002770050487. PMID: 10211753.
Article
61. Duong HK, Savani BN, Copelan E, Devine S, Costa LJ, Wingard JR, Shaughnessy P, Majhail N, Perales MA, Cutler CS, Bensinger W, Litzow MR, Mohty M, Champlin RE, Leather H, Giralt S, Carpenter PA. 2014; Peripheral blood progenitor cell mobilization for autologous and allogeneic hematopoietic cell transplantation: guidelines from the American Society for Blood and Marrow Transplantation. Biol Blood Marrow Transplant. 20:1262–1273. DOI: 10.1016/j.bbmt.2014.05.003. PMID: 24816581.
Article
62. Hsu JW, Wingard JR, Logan BR, Chitphakdithai P, Akpek G, Anderlini P, Artz AS, Bredeson C, Goldstein S, Hale G, Hematti P, Joshi S, Kamble RT, Lazarus HM, O'Donnell PV, Pulsipher MA, Savani BN, Schears RM, Shaw BE, Confer DL. 2015; Race and ethnicity influences collection of granulocyte colony-stimulating factor-mobilized peripheral blood progenitor cells from unrelated donors, a Center for International Blood and Marrow Transplant Research analysis. Biol Blood Marrow Transplant. 21:165–171. DOI: 10.1016/j.bbmt.2014.10.007. PMID: 25316111. PMCID: PMC4272878.
Article
63. Poole J, Mavromatis K, Binongo JN, Khan A, Li Q, Khayata M, Rocco E, Topel M, Zhang X, Brown C, Corriere MA, Murrow J, Sher S, Clement S, Ashraf K, Rashed A, Kabbany T, Neuman R, Morris A, Ali A, Hayek S, Oshinski J, Yoon YS, Waller EK, Quyyumi AA. 2013; Effect of progenitor cell mobilization with granulocyte-macrophage colony-stimulating factor in patients with peripheral artery disease: a randomized clinical trial. JAMA. 310:2631–2639. DOI: 10.1001/jama.2013.282540. PMID: 24247554.
Article
64. Huang PP, Yang XF, Li SZ, Wen JC, Zhang Y, Han ZC. 2007; Randomised comparison of G-CSF-mobilized peripheral blood mononuclear cells versus bone marrow-mononuclear cells for the treatment of patients with lower limb arteriosclerosis obliterans. Thromb Haemost. 98:1335–1342. DOI: 10.1160/TH07-02-0137. PMID: 18064333.
Article
65. Dubsky M, Jirkovska A, Bem R, Fejfarova V, Pagacova L, Sixta B, Varga M, Langkramer S, Sykova E, Jude EB. 2013; Both autologous bone marrow mononuclear cell and peripheral blood progenitor cell therapies similarly improve ischaemia in patients with diabetic foot in comparison with control treatment. Diabetes Metab Res Rev. 29:369–376. DOI: 10.1002/dmrr.2399. PMID: 23390092.
Article
66. Hess DC, Hill WD, Martin-Studdard A, Carroll J, Brailer J, Carothers J. 2002; Bone marrow as a source of endothelial cells and NeuN-expressing cells after stroke. Stroke. 33:1362–1368. DOI: 10.1161/01.STR.0000014925.09415.C3. PMID: 11988616.
Article
67. Werner N, Priller J, Laufs U, Endres M, Böhm M, Dirnagl U, Nickenig G. 2002; Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition. Arterioscler Thromb Vasc Biol. 22:1567–1572. DOI: 10.1161/01.ATV.0000036417.43987.D8. PMID: 12377731.
Article
68. Reddy K, Zhou Z, Schadler K, Jia SF, Kleinerman ES. 2008; Bone marrow subsets differentiate into endothelial cells and pericytes contributing to Ewing's tumor vessels. Mol Cancer Res. 6:929–936. DOI: 10.1158/1541-7786.MCR-07-2189. PMID: 18567797. PMCID: PMC2441901.
Article
69. Göthert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, Green AR, Göttgens B, Izon DJ, Begley CG. 2004; Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood. 104:1769–1777. DOI: 10.1182/blood-2003-11-3952. PMID: 15187022.
Article
70. Purhonen S, Palm J, Rossi D, Kaskenpää N, Rajantie I, Ylä-Herttuala S, Alitalo K, Weissman IL, Salven P. 2008; Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc Natl Acad Sci U S A. 105:6620–6625. DOI: 10.1073/pnas.0710516105. PMID: 18443294. PMCID: PMC2365563.
Article
71. Attwell D, Mishra A, Hall CN, O'Farrell FM, Dalkara T. 2016; What is a pericyte? J Cereb Blood Flow Metab. 36:451–455. DOI: 10.1177/0271678X15610340. PMID: 26661200. PMCID: PMC4759679.
Article
72. Bergers G, Song S. 2005; The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol. 7:452–464. DOI: 10.1215/S1152851705000232. PMID: 16212810. PMCID: PMC1871727.
Article
73. Caporarello N, D'Angeli F, Cambria MT, Candido S, Giallongo C, Salmeri M, Lombardo C, Longo A, Giurdanella G, Anfuso CD, Lupo G. 2019; Pericytes in microvessels: from "mural" function to brain and retina regeneration. Int J Mol Sci. 20:6351. DOI: 10.3390/ijms20246351. PMID: 31861092. PMCID: PMC6940987.
Article
74. Rajantie I, Ilmonen M, Alminaite A, Ozerdem U, Alitalo K, Salven P. 2004; Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood. 104:2084–2086. DOI: 10.1182/blood-2004-01-0336. PMID: 15191949. PMCID: PMC2698665.
Article
75. Ziegelhoeffer T, Fernandez B, Kostin S, Heil M, Voswinckel R, Helisch A, Schaper W. 2004; Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res. 94:230–238. DOI: 10.1161/01.RES.0000110419.50982.1C. PMID: 14656934.
Article
76. Kamihata H, Matsubara H, Nishiue T, Fujiyama S, Tsutsumi Y, Ozono R, Masaki H, Mori Y, Iba O, Tateishi E, Kosaki A, Shintani S, Murohara T, Imaizumi T, Iwasaka T. 2001; Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation. 104:1046–1052. DOI: 10.1161/hc3501.093817. PMID: 11524400.
Article
77. Rehman J, Li J, Orschell CM, March KL. 2003; Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation. 107:1164–1169. DOI: 10.1161/01.CIR.0000058702.69484.A0. PMID: 12615796.
Article
78. Dokun AO, Annex BH. 2011; The VEGF165b "ICE-o-form" puts a chill on the VEGF story. Circ Res. 109:246–247. DOI: 10.1161/CIRCRESAHA.111.249953. PMID: 21778432. PMCID: PMC3196354.
Article
79. Carmeliet P, Jain RK. 2011; Molecular mechanisms and clinical applications of angiogenesis. Nature. 473:298–307. DOI: 10.1038/nature10144. PMID: 21593862. PMCID: PMC4049445.
Article
80. Montesano R, Vassalli JD, Baird A, Guillemin R, Orci L. 1986; Basic fibroblast growth factor induces angiogenesis in vitro. Proc Natl Acad Sci U S A. 83:7297–7301. DOI: 10.1073/pnas.83.19.7297. PMID: 2429303. PMCID: PMC386703.
Article
81. Murakami M, Simons M. 2008; Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol. 15:215–220. DOI: 10.1097/MOH.0b013e3282f97d98. PMID: 18391788. PMCID: PMC2745288.
Article
82. Xin X, Yang S, Ingle G, Zlot C, Rangell L, Kowalski J, Schwall R, Ferrara N, Gerritsen ME. 2001; Hepatocyte growth factor enhances vascular endothelial growth factor-induced angiogenesis in vitro and in vivo. Am J Pathol. 158:1111–1120. DOI: 10.1016/S0002-9440(10)64058-8. PMID: 11238059. PMCID: PMC1850376.
Article
83. Sanada F, Taniyama Y, Azuma J, Yuka II, Kanbara Y, Iwabayashi M, Rakugi H, Morishita R. 2014; Therapeutic angiogenesis by gene therapy for critical limb ischemia: choice of biological agent. Immunol Endocr Metab Agents Med Chem. 14:32–39. DOI: 10.2174/1871522213999131231105139. PMID: 26005508. PMCID: PMC4435566.
Article
84. Lawall H, Bramlage P, Amann B. 2010; Stem cell and progenitor cell therapy in peripheral artery disease. A critical appraisal. Thromb Haemost. 103:696–709. DOI: 10.1160/TH09-10-0688. PMID: 20174766.
85. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, Amano K, Kishimoto Y, Yoshimoto K, Akashi H, Shimada K, Iwasaka T, Imaizumi T. 2002; Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet. 360:427–435. DOI: 10.1016/S0140-6736(02)09670-8. PMID: 12241713.
Article
86. Persiani F, Paolini A, Camilli D, Mascellari L, Platone A, Magenta A, Furgiuele S. 2018; Peripheral blood mononuclear cells therapy for treatment of lower limb ischemia in diabetic patients: a single-center experience. Ann Vasc Surg. 53:190–196. DOI: 10.1016/j.avsg.2018.05.036. PMID: 30053546.
Article
87. Horie T, Yamazaki S, Hanada S, Kobayashi S, Tsukamoto T, Haruna T, Sakaguchi K, Sakai K, Obara H, Morishita K, Saigo K, Shintani Y, Kubo K, Hoshino J, Oda T, Kaneko E, Nishikido M, Ioji T, Kaneda H, Fukushima M. 2018; Outcome from a randomized controlled clinical trial- improvement of peripheral arterial disease by granulocyte colony-stimulating factor-mobilized autologous peripheral-blood-mononuclear cell transplantation (IMPACT). Circ J. 82:2165–2174. DOI: 10.1253/circj.CJ-17-1220. PMID: 29877199.
Article
88. Liew A, Bhattacharya V, Shaw J, Stansby G. 2016; Cell therapy for critical limb ischemia: a meta-analysis of randomized controlled trials. Angiology. 67:444–455. DOI: 10.1177/0003319715595172. PMID: 26195561.
89. Wen Y, Meng L, Gao Q. 2011; Autologous bone marrow cell therapy for patients with peripheral arterial disease: a meta-analysis of randomized controlled trials. Expert Opin Biol Ther. 11:1581–1589. DOI: 10.1517/14712598.2011.626401. PMID: 21973046.
Article
90. Ai M, Yan CF, Xia FC, Zhou SL, He J, Li CP. 2016; Safety and efficacy of cell-based therapy on critical limb ischemia: a meta-analysis. Cytotherapy. 18:712–724. DOI: 10.1016/j.jcyt.2016.02.009. PMID: 27067609.
Article
91. Rigato M, Monami M, Fadini GP. 2017; Autologous cell therapy for peripheral arterial disease: systematic review and meta-analysis of randomized, nonrandomized, and noncontrolled studies. Circ Res. 120:1326–1340. DOI: 10.1161/CIRCRESAHA.116.309045. PMID: 28096194.
Article
92. Xie B, Luo H, Zhang Y, Wang Q, Zhou C, Xu D. 2018; Autologous stem cell therapy in critical limb ischemia: a meta-analysis of randomized controlled trials. Stem Cells Int. 2018:7528464. DOI: 10.1155/2018/7528464. PMID: 29977308. PMCID: PMC5994285.
Article
93. Pan T, Wei Z, Fang Y, Dong Z, Fu W. 2018; Therapeutic efficacy of CD34 cell-involved mononuclear cell therapy for no-option critical limb ischemia: a meta-analysis of randomized controlled clinical trials. Vasc Med. 23:219–231. DOI: 10.1177/1358863X17752556. PMID: 29457540.
Article
94. Gao W, Chen D, Liu G, Ran X. 2019; Autologous stem cell therapy for peripheral arterial disease: a systematic review and meta-analysis of randomized controlled trials. Stem Cell Res Ther. 10:140. DOI: 10.1186/s13287-019-1254-5. PMID: 31113463. PMCID: PMC6528204.
Article
95. Peeters Weem SM, Teraa M, de Borst GJ, Verhaar MC, Moll FL. 2015; Bone marrow derived cell therapy in critical limb ischemia: a meta-analysis of randomized placebo controlled trials. Eur J Vasc Endovasc Surg. 50:775–783. DOI: 10.1016/j.ejvs.2015.08.018. PMID: 26460286.
Article
96. Ii M, Takenaka H, Asai J, Ibusuki K, Mizukami Y, Maruyama K, Yoon YS, Wecker A, Luedemann C, Eaton E, Silver M, Thorne T, Losordo DW. 2006; Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ Res. 98:697–704. DOI: 10.1161/01.RES.0000209948.50943.ea. PMID: 16484619.
Article
97. Fadini GP, Sartore S, Albiero M, Baesso I, Murphy E, Menegolo M, Grego F, Vigili de Kreutzenberg S, Tiengo A, Agostini C, Avogaro A. 2006; Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy. Arterioscler Thromb Vasc Biol. 26:2140–2146. DOI: 10.1161/01.ATV.0000237750.44469.88. PMID: 16857948.
Article
98. Tecilazich F, Dinh T, Pradhan-Nabzdyk L, Leal E, Tellechea A, Kafanas A, Gnardellis C, Magargee ML, Dejam A, Toxavidis V, Tigges JC, Carvalho E, Lyons TE, Veves A. 2013; Role of endothelial progenitor cells and inflammatory cytokines in healing of diabetic foot ulcers. PLoS One. 8:e83314. DOI: 10.1371/journal.pone.0083314. PMID: 24358275. PMCID: PMC3865213.
Article
99. Zafar N, Krishnasamy SS, Shah J, Rai SN, Riggs DW, Bhatnagar A, O'Toole TE. 2018; Circulating angiogenic stem cells in type 2 diabetes are associated with glycemic control and endothelial dysfunction. PLoS One. 13:e0205851. DOI: 10.1371/journal.pone.0205851. PMID: 30321232. PMCID: PMC6188890.
Article
100. Zhou B, Bi YY, Han ZB, Ren H, Fang ZH, Yu XF, Poon MC, Han ZC. 2006; G-CSF-mobilized peripheral blood mononuclear cells from diabetic patients augment neovascula-rization in ischemic limbs but with impaired capability. J Thromb Haemost. 4:993–1002. DOI: 10.1111/j.1538-7836.2006.01906.x. PMID: 16689750.
Article
101. Losordo DW, Kibbe MR, Mendelsohn F, Marston W, Driver VR, Sharafuddin M, Teodorescu V, Wiechmann BN, Thompson C, Kraiss L, Carman T, Dohad S, Huang P, Junge CE, Story K, Weistroffer T, Thorne TM, Millay M, Runyon JP, Schainfeld R. 2012; A randomized, controlled pilot study of autologous CD34 cell therapy for critical limb ischemia. Circ Cardiovasc Interv. 5:821–830. DOI: 10.1161/CIRCINTERVENTIONS.112.968321. PMID: 23192920. PMCID: PMC3549397.
Article
102. Klepanec A, Mistrik M, Altaner C, Valachovicova M, Olejarova I, Slysko R, Balazs T, Urlandova T, Hladikova D, Liska B, Tomka J, Vulev I, Madaric J. 2012; No difference in intra-arterial and intramuscular delivery of autologous bone marrow cells in patients with advanced critical limb ischemia. Cell Transplant. 21:1909–1918. DOI: 10.3727/096368912X636948. PMID: 22472173.
Article
103. Gu YQ, Zhang J, Guo LR, Qi LX, Zhang SW, Xu J, Li JX, Luo T, Ji BX, Li XF, Yu HX, Cui SJ, Wang ZG. 2008; Transplantation of autologous bone marrow mononuclear cells for patients with lower limb ischemia. Chin Med J (Engl). 121:963–967. DOI: 10.1097/00029330-200806010-00001. PMID: 18706241.
Article
104. Patiño B, Espinosa D, Solano MH, Abello V, Casas C. 2018; Morbidity and mortality associated with performing bone marrow aspiration and biopsy. Int Phys Med Rehab J. 3:65–70. DOI: 10.15406/ipmrj.2018.03.00077.
Article
105. Hölig K. 2013; G-CSF in healthy allogeneic stem cell donors. Transfus Med Hemother. 40:225–235. DOI: 10.1159/000354196. PMID: 24179471. PMCID: PMC3776391.
Article
106. Balaguer H, Galmes A, Ventayol G, Bargay J, Besalduch J. 2004; Splenic rupture after granulocyte-colony-stimulating factor mobilization in a peripheral blood progenitor cell donor. Transfusion. 44:1260–1261. DOI: 10.1111/j.1537-2995.2004.00413.x. PMID: 15265137.
Article
107. Azoulay E, Attalah H, Harf A, Schlemmer B, Delclaux C. 2001; Granulocyte colony-stimulating factor or neutrophil-induced pulmonary toxicity: myth or reality? Systematic review of clinical case reports and experimental data. Chest. 120:1695–1701. DOI: 10.1378/chest.120.5.1695. PMID: 11713155.
Article
108. Falanga A, Marchetti M, Evangelista V, Manarini S, Oldani E, Giovanelli S, Galbusera M, Cerletti C, Barbui T. 1999; Neutrophil activation and hemostatic changes in healthy donors receiving granulocyte colony-stimulating factor. Blood. 93:2506–2514. DOI: 10.1182/blood.V93.8.2506. PMID: 10194429.
Article
109. Matoba S, Tatsumi T, Murohara T, Imaizumi T, Katsuda Y, Ito M, Saito Y, Uemura S, Suzuki H, Fukumoto S, Yamamoto Y, Onodera R, Teramukai S, Fukushima M, Matsubara H. 2008; Long-term clinical outcome after intramuscular implantation of bone marrow mononuclear cells (Therapeutic Angiogenesis by Cell Transplantation [TACT] trial) in patients with chronic limb ischemia. Am Heart J. 156:1010–1018. DOI: 10.1016/j.ahj.2008.06.025. PMID: 19061721.
Article
110. Onodera R, Teramukai S, Tanaka S, Kojima S, Horie T, Matoba S, Murohara T, Matsubara H, Fukushima M. 2011; Bone marrow mononuclear cells versus G-CSF-mobilized peripheral blood mononuclear cells for treatment of lower limb ASO: pooled analysis for long-term prognosis. Bone Marrow Transplant. 46:278–284. DOI: 10.1038/bmt.2010.110. PMID: 20479708.
Article
Full Text Links
  • IJSC
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr