Heterogeneity in Studies of Mesenchymal Stromal Cells to Treat or Prevent Graft-versus-Host Disease: A Scoping Review of the Evidence

Biology of Blood and Marrow Transplantation

Volumn 22, Issue 8, 2016, Pages 1416-1423

  Rizk, Mina ^a   Monaghan, Madeline ^a   Shorr, Risa ^a   Kekre, Natasha ^a   Bredeson, Christopher N ^a   Allan, David S ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

Graft versus host disease; Hematopoietic cell transplantation; Mesenchymal stromal cell; Prevention; Systematic review; Treatment

Indexed keywords

ADIPOSE TISSUE; ARTICLE; BONE MARROW; CELL CULTURE; CRYOPRESERVATION; GRAFT VERSUS HOST REACTION; HLA MATCHING; HUMAN; INTERVENTION STUDY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; PREVENTION STUDY; SYSTEMATIC REVIEW; TREATMENT RESPONSE; UMBILICAL CORD BLOOD; CLINICAL PROTOCOL; CLINICAL TRIAL (TOPIC); CYTOLOGY; PROCEDURES; STANDARD; STANDARDS;

CLINICAL PROTOCOLS; CLINICAL TRIALS AS TOPIC; GRAFT VS HOST DISEASE; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; REFERENCE STANDARDS;

EID: 84973885518     PISSN: 10838791     EISSN: 15236536     Source Type: Journal    
DOI: 10.1016/j.bbmt.2016.04.010     Document Type: Article

References (63)

1. 1 Jagasia, M., Arora, M., Flowers, M.E.D., et al. Risk factors for acute GVHD and survival after hematopoietic cell transplantation. Blood 119 (2012), 296–307.
2. 2 Sung, A.D., Chao, N.J., Concise review: acute graft-versus-host disease: immunobiology, prevention, and treatment. Stem Cells Transl Med 2 (2013), 25–32.
3. 3 MacMillan, M.L., Weisdorf, D.J., Wagner, J.E., et al. Response of 443 patients to steroids as primary therapy for acute graft-versus-host disease: comparison of grading systems. Biol Blood Marrow Transplant 8 (2002), 387–394.
4. 4 Martin, P.J., Rizzo, J.D., Wingard, J.R., et al. First and second-line systemic treatment of acute graft-versus-host disease: recommendations of the American Society of Blood and Marrow Transplantation. Biol Blood Marrow Transplant 18 (2012), 1150–1163.
5. 5 Pittenger, M.F., Mackay, A.M., Beck, S.C., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999), 143–147.
6. 6 Bartholomew, A., Sturgeon, C., Siatskas, M., et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 30 (2002), 42–48.
7. 7 Yagi, H., Soto-Gutierrez, A., Parekkadan, B., et al. Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transplant 19 (2010), 667–679.
8. 8 Aggarwal, S., Pittenger, M.F., Human mesenchymal stem cells modulate allogeneic immune responses. Blood 105 (2005), 1815–1822.
9. 9 Augello, A., Tasso, R., Negrini, S.M., et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 35 (2005), 1482–1490.
10. 10 Akiyama, K., Chen, C., Wang, D., et al. Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 10 (2012), 544–555.
11. 11 Ren, G., Zhao, X., Zhang, L., et al. Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J Immunol 184 (2010), 2321–2328.
12. 12 Saldanha-Araujo, F., Ferreira, F.I., Palma, P.V., et al. Mesenchymal stromal cells up-regulate CD39 and increase adenosine production to suppress activated T-lymphocytes. Stem Cell Res 7 (2011), 66–74.
13. 13 Rasmusson, I., Ringden, O., Sundberg, B., Le Blanc, K., Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76 (2003), 1208–1213.
14. 14 Kordelas, L., Rebmann, V., Ludwig, A.-K., et al. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus host disease. Leukemia 28 (2014), 970–973.
15. 15 Dominici, M., Le Blanc, K., Mueller, I., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8 (2006), 315–317.
16. 16 Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med, 6, 2009, e1000097.
17. 17 Ringden, O., Uzunel, M., Rasmusson, I., et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 81 (2006), 1390–1397.
18. 18 Fang, B., Song, Y., Liao, L., et al. Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant Proc 39 (2007), 3358–3362.
19. 19 Le Blanc, K., Frassoni, F., Ball, L., et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371 (2008), 1579–1586.
20. 20 Kebriaei, P., Isola, L., Bahceci, E., et al. Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease. Biol Blood Marrow Transplant 15 (2009), 804–811.
21. 21 von Bonin, M., Stolzel, F., Goedecke, A., et al. Treatment of refractory acute GVHD with third-party MSC expanded in platelet lysate-containing medium. Bone Marrow Transplant 43 (2009), 245–251.
22. 22 Weng, J.Y., Du, X., Geng, S.X., et al. Mesenchymal stem cell as salvage treatment for refractory chronic GVHD. Bone Marrow Transplant 45 (2010), 1732–1740.
23. 23 Lucchini, G., Introna, M., Dander, E., et al. Platelet-lysate-expanded mesenchymal stromal cells as a salvage therapy for severe resistant graft-versus-host disease in a pediatric population. Biol Blood Marrow Transplant 16 (2010), 1293–1301.
24. 24 Herrmann, R., Sturm, M., Shaw, K., et al. Mesenchymal stromal cell therapy for steroid-refractory acute and chronic graft versus host disease: a phase 1 study. Int J Hematol 95 (2012), 182–188.
25. 25 Perez-Simon, J.A., Lopez-Villar, O., Andreu, E.J., et al. Mesenchymal stem cells expanded in vitro with human serum for the treatment of acute and chronic graft-versus-host disease: results of a phase I/II clinical trial. Haematologica 96 (2011), 1072–1076.
26. 26 Prasad, V.K., Lucas, K.G., Kleiner, G.I., et al. Efficacy and safety of ex vivo cultured adult human mesenchymal stem cells (Prochymal) in pediatric patients with severe refractory acute graft-versus-host disease in a compassionate use study. Biol Blood Marrow Transplant 17 (2011), 534–541.
27. 27 Resnick, I.B., Barkats, C., Shapira, M.Y., et al. Treatment of severe steroid resistant acute GVHD with mesenchymal stromal cells (MSC). Am J Blood Res 3 (2013), 225–238.
28. 28 Ball, L.M., Bernardo, M.E., Roelofs, H., et al. Multiple infusions of mesenchymal stromal cells induce sustained remission in children with steroid-refractory, grade III-IV acute graft-versus-host disease. Br J Haematol 163 (2013), 501–509.
29. 29 Muroi, K., Miyamura, K., Ohashi, K., et al. Unrelated allogeneic bone marrow-derived mesenchymal stem cells for steroid-refractory acute graft-versus-host disease: a phase I/II study. Int J Hematol 98 (2013), 206–213.
30. 30 Peng, Y., Chen, X., Liu, Q., et al. Alteration of naive and memory B-cell subset in chronic graft-versus-host disease patients after treatment with mesenchymal stromal cells. Stem Cells Transl Med 3 (2014), 1023–1031.
31. 31 Sanchez-Guijo, F., Caballero-Velazquez, T., Lopez-Villar, O., et al. Sequential third-party mesenchymal stromal cell therapy for refractory acute graft-versus-host disease. Biol Blood Marrow Transplant 20 (2014), 1580–1585.
32. 32 Introna, M., Lucchini, G., Dander, E., et al. Treatment of graft versus host disease with mesenchymal stromal cells: a phase I study on 40 adult and pediatric patients. Biol Blood Marrow Transplant 20 (2014), 375–381.
33. 33 Kurtzberg, J., Prockop, S., Teira, P., et al. Allogeneic human mesenchymal stem cell therapy (Remestemcel-L, Prochymal) as a rescue agent for severe refractory acute graft-versus-host disease in pediatric patients. Biol Blood Marrow Transplant 20 (2014), 229–235.
34. 34 Zhao, K., Lou, R., Huang, F., et al. Immunomodulation effects of mesenchymal stromal cells on acute graft-versus-host disease after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 21 (2015), 97–104.
35. 35 Peng, Y., Chen, X., Liu, Q., et al. Mesenchymal stromal cells infusions improve refractory chronic graft versus host disease through an increase of CD5+ regulatory B cells producing interleukin 10. Leukemia 29 (2015), 636–646.
36. 36 Lazarus, H.M., Koc, O.M., Devine, S.M., et al. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol Blood Marrow Transplant 11 (2005), 389–398.
37. 37 Gonzalo, D.R., Regidor, C., Martin, D.T., et al. Results of a pilot study on the use of third-party donor mesenchymal stromal cells in cord blood transplantation in adults. Cytotherapy 11 (2009), 278–288.
38. 38 Baron, F., Lechanteur, C., Willems, E., et al. Cotransplantation of mesenchymal stem cells might prevent death from graft-versus-host disease (GVHD) without abrogating graft-versus-tumor effects after HLA-mismatched allogeneic transplantation following nonmyeloablative conditioning. Biol Blood Marrow Transplant 16 (2010), 838–847.
39. 39 Bernardo, M.E., Ball, L.M., Cometa, A.M., et al. Co-infusion of ex vivo-expanded, parental MSCs prevents life-threatening acute GVHD, but does not reduce the risk of graft failure in pediatric patients undergoing allogeneic umbilical cord blood transplantation. Bone Marrow Transplant 46 (2011), 200–207.
40. 40 Kuzmina, L.A., Petinati, N.A., Parovichnikova, E.N., et al. Multipotent mesenchymal stromal cells for the prophylaxis of acute graft-versus-host disease- a phase II study. Stem Cells Int, 2012, 2012, 968213.
41. 41 Wang, H., Yan, H., Wang, Z., et al. Cotransplantation of allogeneic mesenchymal and hematopoietic stem cells in children with aplastic anemia. Pediatrics, 129, 2012, e1612.
42. 42 Wu, Y., Wang, Z., Cao, Y., et al. Cotransplantation of haploidentical hematopoietic and umbilical cord mesenchymal stem cells with a myeloablative regimen for refractory/relapsed hematologic malignancy. Ann Hematol, 92, 2013, 1675.
43. 43 Li, X.H., Gao, C.J., Da, W.M., et al. Reduced intensity conditioning, combined transplantation of haploidentical hematopoietic stem cells and mesenchymal stem cells in patients with severe aplastic anemia. PloS One, 9, 2014, e89666.
44. 44 Shipounova, I.N., Petinati, N.A., Bigildeev, A.E., et al. Analysis of results of acute graft-versus-host disease prophylaxis with donor multipotent mesenchymal stromal cells in patients with hemoblastoses after allogeneic bone marrow transplantation. Biochemistry 79 (2014), 1363–1370.
45. 45 Si, Y., Yang, K., Qin, M., et al. Efficacy and safety of human umbilical cord derived mesenchymal stem cell therapy in children with severe aplastic anemia following allogeneic hematopoietic stem cell transplantation: a retrospective case series of 37 patients. Pediatr Hematol Oncol 31 (2014), 39–49.
46. 46 Wu, Y., Cao, Y., Li, X., et al. Cotransplantation of haploidentical hematopoietic and umbilical cord mesenchymal stem cells for severe aplastic anemia: successful engraftment and mild GVHD. Stem Cell Res 12 (2014), 132–138.
47. 47 Bacigalupo, A., Ballen, K., Rizzo, D., et al. Defining the intensity of conditioning regimens: working definitions. Biol Blood Marrow Transplant 15 (2009), 1628–1633.
48. 48 Wang, L., Gu, Z.Y., Zhao, X.L., et al. Role of mesenchymal stem cells in preventing GVHD: a meta-analysis. Zhongguo Shi Yan Xue Ye Xue Zhi 23 (2015), 1125–1132.
49. 49 Verneris, M.R., Lee, S.J., Ahn, K.W., et al. HLA mismatch is associated with worse outcomes after unrelated donor reduced-intensity conditioning hematopoietic cell transplantation: an analysis from them Center for International Blood and Marrow Transplant Research. Biol Blood Marrow Transplant 21 (2015), 1783–1789.
50. 50 Walker, I., Panzarella, T., Couban, S., et al. Pretreatment with anti-thymocyte globulin versus no anti-thymocyte globulin in patients with haematological malignancies undergoing haemopoietic cell transplantation from unrelated donors: a randomised, controlled, open-label, phase 3, multicentre trial. Lancet Oncol 17 (2016), 164–173.
51. 51 Finke, J., Bethge, W.A., Schmoor, C., et al. Standard graft-versus-host disease prophylaxis with or without anti-T-cell globulin in haematopoietic cell transplantation from matched unrelated donors: a randomised, open-label, multicentre phase 3 trial. Lancet Oncol 10 (2009), 855–864.
52. 52 Le Blanc, K., Rasmusson, I., Sundberg, B., et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363 (2004), 1439–1441.
53. 53 Lalu, M.M., McIntyre, L., Pugliese, C., et al. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS One, 7, 2012, e47559.
54. 54 Hashmi, S., Ahmed, M., Murad, M.H., et al. Survival after mesenchymal stromal cell therapy in steroid-refractory acute graft-versus-host-disease: systematic review and meta-analysis. Lancet Haematol 3 (2016), e45–e52.
55. 55 Kallekleiv, M., Larun, L., Bruserud, O., Hatfield, K.J., Co-transplantation of multipotent mesenchymal stromal cells in allogeneic hematopoietic stem cell transplantation: a systematic review. Cytotherapy 18 (2016), 172–185.
56. 56 Chen, X., Wang, C., Yin, J., et al. Efficacy of mesenchymal stem cell therapy for steroid-refractory acute graft-versus-host disease following allogeneic hematopoietic stem cell transplantation: a systematic review and meta-analysis. PLoS One, 10, 2015, e0136991.
57. 57 Martin, P.J., Uberti, J.P., Soiffer, R.J., et al. Prochymal improves response rates in patients with steroid-refractory acute graft versus-host disease (SR-GVHD) involving the liver and gut: results of a randomized, placebo-controlled, multicenter phase III trial in GVHD. Biol Blood Marrow Transplant 16 (2010), S169–S170 [abstract].
58. 58 Osiris therapeutics announces preliminary results for Prochymal phase III GvHD trials. Available at: http://investor.osiris.com/releasedetail.cfm?releaseid=407404. Accessed January 7, 2016.
59. 59 Galipeau, J., The mesenchymal stromal cells dilemma – does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road?. Cytotherapy 15 (2013), 2–8.
60. 60 Kaipe, H., Erkers, T., Sadeghi, B., Ringden, O., Stromal cells – are they really useful for GVHD?. Bone Marrow Transplant 49 (2014), 737–743.
61. 61 Copland, I.B., Qayed, M., Garcia, M.A., et al. Bone marrow mesenchymal stromal cells from patients with acute and chronic graft-versus-host disease deploy normal phenotype, differentiation plasticity, and immune-suppressive activity. Biol Blood Marrow Transplant 21 (2015), 934–940.
62. 62 Jagasia, M.H., Greinix, H.T., Arora, M., et al. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. The 2014 diagnosis and staging working group report. Biol Blood Marrow Transplant 21 (2015), 389–401.
63. 63 Lee, S.J., Wolff, D., Kitko, C., et al. Measuring therapeutic response in chronic graft-versus-host disease. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: IV. The 2014 response criteria working group report. Biol Blood Marrow Transplant 21 (2015), 984–999.