Therapeutic implications of extracorporeal photopheresis for rheumatic diseases

REVIEW ARTICLE

Therapeutic implications of extracorporeal photopheresis for rheumatic diseases

Ewa Morgiel 1 , Jarosław Dybko 2 , Marta Madej 1 , Grzegorz Mazur 3

1. Department and Clinic of Rheumatology and Internal Medicine, Wroclaw Medical University, Wroclaw, Poland,
2. Department of Cancer Prevention and Therapy, Wroclaw Medical University, Wroclaw, Poland,
3. Department and Clinic of Internal and Occupational Diseases and Hypertension, Wroclaw Medical University, Wroclaw, Poland,

Published: 2020-09-22
DOI: 10.5604/01.3001.0014.4117
GICID: 01.3001.0014.4117
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2020; 74 : 391-398

 

Abstract

Extracorporeal photopheresis (ECP) procedure is based on mononuclear cells (MNC) apheresis and their extracorporeal UVA exposure. It has been applied mainly in hematology and transplantation. Over thirty years of experience confirmed its effectiveness, outstanding safety profile and good tolerance. These observations encourage the implementation of ECP in the treatment of autoimmune connective tissue diseases. The procedure might be considered in refractory cases, when the first line treatment strategies do not control disease activity or immunosuppressants are contraindicated and in the group of patients with high risk of infections. Current literature about using ECP in rheumatology is scarce and most data come from case reports and small observational studies. Systemic sclerosis is the most studied rheumatic disease in the field of ECP use. The disease appeared on the list of clinical applications of ECP therapy according to American Society for Apheresis. However, no European or American guidelines, or recommendations for the treatment in rheumatology suggest ECP as the treatment option. There are no standards in performing ECP in rheumatic diseases concerning indications, length of therapy, concomitant immunosuppressive treatment, follow up or patients characteristic. In this review, we have searched literature concerning ECP use in rheumatic diseases.

References

  • 1. Abreu M.T., von Tirpitz C., Hardi R., Kaatz M., Van Assche G.,Rutgeerts P., Bisaccia E., Goerdt S., Hanauer S., Knobler R., MannonP., Mayer L., Ochsenkuhn T., Sandborn W.J., Parenti D., et al.: Extracorporealphotopheresis for the treatment of refractory Crohn’sdisease: Results of an open-label pilot study. Inflamm. Bowel Dis.,2009; 15: 829–836
    Google Scholar
  • 2. Akay B.N., Sanli H., Kutlay S.: Treatment of ankylosing spondylitisby extracorporeal photochemotherapy given for mycosisfungoides: a potential treatment option? J. Clin. Rheumatol., 2011;17: 278–280
    Google Scholar
  • 3. Andreu G., Achkar A., Couetil J.P., Guillemain R., Heshmati F.,Amrein C., Chevalier P., Guinvarch A., Dore M.F., Capron F., LaabanJ.P., Carpentier A.: Extracorporeal photochemotherapy treatmentfor acute lung rejection episode. J. Heart Lung Transplant., 1995;14: 793–796
    Google Scholar
  • 4. Berger C.L., Hanlon D., Kanada D., Girardi M., Edelson R.L.:Transimmunization, a novel approach for tumor immunotherapy.Transfus. Apher. Sci., 2002; 26: 205–216
    Google Scholar
  • 5. Calore E., Calò A., Tridello G., Cesaro S., Pillon M., Varotto S.,Gazzola M.V., Destro R., Marson P., Trentin L., Carli M., Messina C.:Extracorporeal photochemotherapy may improve outcome in childrenwith acute GVHD. Bone Marrow Transplant., 2008; 42: 421–425
    Google Scholar
  • 6. Cho A., Jantschitsch C., Knobler R.: Extracorporeal photopheresis– an overview. Front. Med., 2018; 5: 236
    Google Scholar
  • 7. Cribier B., Faradji T., Le Coz C., Oberling F., Grosshans E.: Extracorporealphotochemotherapy in systemic sclerosis and severemorphea. Dermatology, 1995; 191: 25–31
    Google Scholar
  • 8. Dall’Amico R., Murer L., Montini G., Andreetta B., Zanon G.F.,Zacchello G., Zacchello F.: Successful treatment of recurrent rejectionin renal transplant patients with photopheresis. J. Am. Soc.Nephrol., 1998; 9: 121–127
    Google Scholar
  • 9. De Wilde A., DiSpaltro F.X., Geller A., Szer I.S., Klainer A.S., BisacciaE.: Extracorporeal photochemotherapy as adjunctive treatmentin juvenile dermatomyositis: A case report. Arch. Dermatol., 1992;128: 1656–1657
    Google Scholar
  • 10. Edelson R., Berger C., Gasparro F., Jegasothy B., Heald P., WintroubB., Vonderheid E., Knobler R., Wolff K., Plewig G., McKiernanG., Christiansen I., Oster M., Honigsmann H., Wilford H., etal.: Treatment of cutaneous T-cell lymphoma by extracorporealphotochemotherapy. Preliminary results. N. Engl. J. Med., 1987;316: 297–303
    Google Scholar
  • 11. Enomoto D.N., Mekkes J.R., Bossuyt P.M., Yong S.L., Out T.A.,Hoekzema R., de Rie M.A., Schellekens P.T., ten Berge I.J., de Borgie C.A., Bos J.D.: Treatment of patients with systemic sclerosis withextracorporeal photochemotherapy (photopheresis). J. Am. Acad.Dermatol., 1999; 41: 915–922
    Google Scholar
  • 12. Fimiani M., Rubegni P., Flori M.L., Mazzatenta C., D’Ascenzo G.,Andreassi L.: Three cases of progressive systemic sclerosis treatedwith extracorporeal photochemotherapy. Arch. Dermatol. Res.,1997; 289: 120–122
    Google Scholar
  • 13. Flowers M.E., Apperley J.F., van Besien K., Elmaagacli A., GriggA., Reddy V., Bacigalupo A., Kolb H.J., Bouzas L., Michallet M., PrinceH.M., Knobler R., Parenti D., Gallo J., Greinix H.T.: A multicenterprospective phase 2 randomized study of extracorporeal photopheresisfor treatment of chronic graft-versus-host disease. Blood,2008; 112: 2667–2674
    Google Scholar
  • 14. Gandelman J.S., Song D.J., Chen H., Engelhardt B.G., Chen Y.B.,Clark W.B., Giver C.R., Waller E.K., Jung D.K., Jagasia M.: A prospectivetrial of extracorporeal photopheresis for chronic graft–versushostdisease reveals significant disease response and no associationwith frequency of regulatory T cells. Biol. Blood Marrow Transplant.,2018; 24: 2373–2380
    Google Scholar
  • 15. Gatza E., Rogers C.E., Clouthier S.G., Lowler K.P., Tawara I., LiuC., Reddy P., Ferrara J.L.: Extracorporeal photopheresis reversesexperimental graft-versus-host disease through regulatory T cells.Blood, 2008; 112: 1515–1521
    Google Scholar
  • 16. Greinix H.T., Knobler R.M., Worel N., Schneider B., SchneebergerA., Hoecker P., Mitterbauer M., Rabitsch W., SchulenburgA., Kalhs P.: The effect of intensified extracorporeal photochemotherapyon long-term survival in patients with severe acute graftversus-host disease. Haematologica, 2006; 91: 405–408
    Google Scholar
  • 17. Greinix H.T., Volc-Platzer B., Rabitsch W., Gmeinhart B., Guevara-Pineda C., Kalhs P., Krutmann J., Hönigsmann H., Ciovica M.,Knobler R.M.: Successful use of extracorporeal photochemotherapyin the treatment of severe acute and chronic graft-versus-hostdisease. Blood, 1998; 92: 3098–3104
    Google Scholar
  • 18. Greinix H.T., Worel N., Just U., Knobler R.: Extracorporeal photopheresisin acute and chronic graft-versus-host disease. Transfus.Apher. Sci., 2014; 50: 349–357
    Google Scholar
  • 19. Greinix H.T., Worel N., Knobler R.: Role of extracorporeal photopheresis(ECP) in treatment of steroid-refractory acute graftversus-host disease. Biol. Blood Marrow Transplant., 2010; 16:1747–1749
    Google Scholar
  • 20. Hautmann A.H., Wolff D., Hahn J., Edinger M., Schirmer N., AmmerJ., Holler B., Landfried K., Hautmann M.G., Ahrens N., UgocsaiP., Andreesen R., Holler E.: Extracorporeal photopheresis in 62 patientswith acute and chronic GVHD: Results of treatment with theCOBE Spectra System. Bone Marrow Transplant., 2013; 48: 439–445
    Google Scholar
  • 21. Jagasia M., Greinix H., Robin M., Das-Gupta E., Jacobs R., SavaniB.N., Engelhardt B.G., Kassim A., Worel N., Knobler R., Russell N.,Socie G.: Extracorporeal photopheresis versus anticytokine therapyas a second-line treatment for steroid-refractory acute GVHD: Amulticenter comparative analysis. Biol. Blood Marrow Transplant.,2013; 19: 1129–1133
    Google Scholar
  • 22. Knobler R., Berlin G., Calzavara-Pinton P., Greinix H., Jaksch P.,Laroche L., Ludvigsson J., Quaglino P., Reinisch W., Scarisbrick J.,Schwarz T., Wolf P., Arenberger P., Assaf C., Bagot M., et al.: Guidelineson the use of extracorporeal photopheresis. J. Eur. Acad. Dermatol.Venereol., 2014; 28: 1–37
    Google Scholar
  • 23. Knobler R.M., French L.E., Kim Y., Bisaccia E., Graninger W.,Nahavandi H., Strobl F.J., Keystone E., Mehlmauer M., Rook A.H.,Braverman I., Systemic Sclerosis Study Group: A randomized, double-blind, placebo-controlled trial of photopheresis in systemicsclerosis. J. Am. Acad. Dermatol., 2006; 54: 793–799
    Google Scholar
  • 24. Knobler R.M., Graninger W., Graninger W., Lindmaier A., TrautingerF., Smolen J.S.: Extracorporeal photochemotherapy for thetreatment of systemic lupus erythematosus. A pilot study. ArthritisRheum., 1992; 35: 319–324
    Google Scholar
  • 25. Krasagakis K., Dippel E., Ramaker J., Owsianowski M., OrfanosC.E.: Management of severe scleroderma with long-term extracorporealphotopheresis. Dermatology, 1998; 196: 309–315
    Google Scholar
  • 26. Lamioni A., Parisi F., Isacchi G., Giorda E., Di Cesare S., LandolfoA., Cenci F., Bottazzo G.F., Carsetti R.: The immunological effects ofextracorporeal photopheresis unraveled: Induction of tolerogenicdendritic cells in vitro and regulatory T cells in vivo. Transplantation,2005; 79: 846–850
    Google Scholar
  • 27. Maeda A., Schwarz A., Bullinger A., Morita A., Peritt D., SchwarzT.: Experimental extracorporeal photopheresis inhibits the sensitizationand effector phases of contact hypersensitivity via twomechanisms: Generation of IL-10 and induction of regulatoryT cells. J. Immunol., 2008; 181: 5956–5962
    Google Scholar
  • 28. Malawista S.E., Trock D.H., Edelson R.L.: Treatment of rheumatoidarthritis by extracorporeal photochemotherapy. A pilotstudy. Arthritis Rheum., 1991; 34: 646–654
    Google Scholar
  • 29. Marques M.B., Tuncer H.H.: Photopheresis in solid organ transplantrejection. J. Clin. Apher., 2006; 21: 72–77
    Google Scholar
  • 30. Merlin E., Jacomet F., D’Incan M., Halle P., Berger M., GandemerV., Piguet C., Souteyrand P., Deméocq F., Kanold J.: Use of cryopreservedautologous cells for extracorporeal photochemotherapy:Clinical applications. Transfusion, 2011; 51: 1296–1299
    Google Scholar
  • 31. Messina C., Locatelli F., Lanino E., Uderzo C., Zacchello G.,Cesaro S., Pillon M., Perotti C., Del Fante C., Faraci M., RivabellaL., Calore E., De Stefano P., Zecca M., Giorgiani G., et al.: Extracorporealphotochemotherapy for paediatric patients with graft-versus-host disease after haematopoietic stem cell transplantation.Br. J. Haematol., 2003; 122: 118–127
    Google Scholar
  • 32. Morelli A.E., Larregina A.T., Shufesky W.J., Zahorchak A.F.,Logar A.J., Papworth G.D., Wang Z., Watkins S.C., Falo L.D.Jr., ThomsonA.W.: Internalization of circulating apoptotic cells by splenicmarginal zone dendritic cells: Dependence on complement receptorsand effect on cytokine production. Blood, 2003; 101: 611–620
    Google Scholar
  • 33. Muellegger R.R., Hofer A., Salmhofer W., Soyer H.P., Kerl H.,Wolf P.: Extended extracorporeal photochemotherapy with extracorporealadministration of 8-methoxypsoralen in systemicsclerosis. An Austrian single-center study. Photodermatol. Photoimmunol.Photomed., 2000; 16: 216–223
    Google Scholar
  • 34. Padmanabhan A., Connelly-Smith L., Aqui N., Balogun R.A.,Klingel R., Meyer E., Pham H.P., Schneiderman J., Witt V., Wu Y.,Zantek N.D., Dunbar N.M., Schwartz J.: Guidelines on the use oftherapeutic apheresis in clinical practice – Evidence-based approachfrom the writing committee of the American Society forApheresis: The eighth special issue. J. Clin. Apher., 2019; 34: 171–354
    Google Scholar
  • 35. Papp G., Horvath I.F., Barath S., Gyimesi E., Vegh J., SzodorayP., Zeher M.: Immunomodulatory effects of extracorporeal photochemotherapyin systemic sclerosis. Clin. Immunol., 2012; 142:150–159
    Google Scholar
  • 36. Perotti C., Del Fante C., Tinelli C., Viarengo G., Scudeller L.,Zecca M., Locatelli F., Salvaneschi L.: Extracorporeal photochemotherapyin graft-versus-host disease: A longitudinal study on factorsinfluencing the response and survival in pediatric patients.Transfusion, 2010; 50: 1359–1369
    Google Scholar
  • 37. Pierelli L., Perseghin P., Marchetti M., Messina C., Perotti C.,Mazzoni A., Bacigalupo A., Locatelli F., Carlier P., Bosi A., SocietàItaliana di Emaferesi and Manipolazione Cellulare (SIdEM); GruppoItaliano Trapianto Midollo Osseo (GITMO): Extracorporeal photopheresisfor the treatment of acute and chronic graft-versus-hostdisease in adults and children: Best practice recommendationsfrom an Italian Society of Hemapheresis and Cell Manipulation (SIdEM)and Italian Group for Bone Marrow Transplantation (GITMO)Consensus Process. Transfusion, 2013; 53: 2340–2352
    Google Scholar
  • 38. Reich S., Gambichler T., Altmeyer P., Kreuter A.: Extracorporealphotopheresis in systemic sclerosis: Effects on organ involvement?J. Am. Acad. Dermatol., 2007; 56: 348–349
    Google Scholar
  • 39. Richter H.I., Krutmann J., Goerz G.: Extracorporeal photopheresisin therapy-refractory disseminated discoid lupus erythematosus.Hautarzt., 1998; 49: 487–491
    Google Scholar
  • 40. Romano C., Rubegni P., De Aloe G., Stanghellini E., D’AscenzoG., Andreassi L., Fimiani M.: Extracorporeal photochemotherapyin the treatment of eosinophilic fasciitis. J. Eur. Acad. Dermatol.Venereol., 2003; 17: 10–13
    Google Scholar
  • 41. Rook A.H., Freundlich B., Jegasothy B.V, Perez M.I., Barr W.G.,Jimenez S.A., Rietschel R.L., Wintroub B., Kahaleh M.B., Varga J.,Heald P.W., Steen V., Massa M.C., Murphy G.F., Perniciaro C., et al.:Treatment of systemic sclerosis with extracorporeal photochemotherapy.Results of a multicenter trial. Arch. Dermatol., 1992;128: 337–346
    Google Scholar
  • 42. Schwartz J., Padmanabhan A., Aqui N., Balogun R.A., Connelly-Smith L., Delaney M., Dunbar N.M., Witt V., Wu Y., Shaz B.H.:Guidelines on the use of therapeutic apheresis in clinical practice-evidence-based approach from the writing committee of theAmerican Society for Apheresis: The seventh special issue. J. Clin.Apher., 2016; 31: 149–162
    Google Scholar
  • 43. Schwartz J., Winters J.L., Padmanabhan A., Balogun R.A., DelaneyM., Linenberger M.L., Szczepiorkowski Z.M., Williams M.E.,Wu Y., Shaz B.H.: Guidelines on the use of therapeutic apheresisin clinical practice – Evidence-based approach from the writingcommittee of the American Society for Apheresis: The sixth specialissue. J. Clin. Apher., 2013; 28: 145–284
    Google Scholar
  • 44. Shaz B.H., Linenberger M.L., Bandarenko N., Winters J.L., KimH.C., Marques M.B., Sarode R., Schwartz J., Weinstein R., WirkA., Szczepiorkowski Z.M.: Category IV indications for therapeuticapheresis: ASFA fourth special issue. J. Clin. Apher., 2007; 22:176–180
    Google Scholar
  • 45. Szczepiorkowski Z.M., Bandarenko N., Kim H.C., LinenbergerM.L., Marques M.B., Sarode R., Schwartz J., Shaz B.H., Weinstein R.,Wirk A., Winters J.L., American Society for Apheresis, ApheresisApplications Committee of the American Society for Apheresis:Guidelines on the use of therapeutic apheresis in clinical practice:Evidence-based approach from the Apheresis ApplicationsCommittee of the American Society for Apheresis. J. Clin. Apher.,2007; 22: 106–175
    Google Scholar
  • 46. Szczepiorkowski Z.M., Winters J.L., Bandarenko N., Kim H.C.,Linenberger M.L., Marques M.B., Sarode R., Schwartz J., WeinsteinR., Shaz B.H., Apheresis Applications Committee of the AmericanSociety for Apheresis: Guidelines on the use of therapeutic apheresisin clinical practice – Evidence-based approach from the apheresisapplications committee of the American Society for Apheresis.J. Clin. Apher., 2010; 25: 83–177
    Google Scholar
  • 47. Urbani L., Mazzoni A., Colombatto P., Biancofiore G., Bindi L.,Tascini C., Menichetti F., Brunetto M., Scatena F., Filipponi F.: Potentialapplications of extracorporeal photopheresis in liver transplantation.Transplant. Proc., 2008; 40: 1175–1178
    Google Scholar
  • 48. Vahlquist C., Larsson M., Ernerudh J., Berlin G., Skogh T., VahlquistA.: Treatment of psoriatic arthritis with extracorporeal photochemotherapyand conventional psoralen-ultraviolet A irradiation.Arthritis Rheum., 1996; 39: 1519–1523
    Google Scholar
  • 49. Villanueva J., Bhorade S.M., Robinson J.A., Husain A.N., GarrityE.R.Jr.: Extracorporeal photopheresis for the treatment of lung allograftrejection. Ann. Transplant., 2000; 5: 44–47
    Google Scholar
  • 50. Ward D.M.: Extracorporeal photopheresis: How, when, andwhy. J. Clin. Apher., 2011; 26: 276–285
    Google Scholar
  • 51. Wollina U., Looks A.: Extracorporeal photochemotherapy incutaneous lupus erythematosus. J. Eur. Acad. Dermatol. Venereol.,1999; 13: 127–30
    Google Scholar
  • 52. Zhou X.A., Choi J.: Photopheresis: Advances and use in systemicsclerosis. Curr. Rheumatol. Rep., 2017; 19: 31
    Google Scholar

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