Prognostic factors of macrophage activation syndrome, at the time of diagnosis, in adult patients affected by autoimmune disease: Analysis of 41 cases collected in 2 rheumatologic centers

Autoimmunity Reviews

Volumn 16, Issue 1, 2017, Pages 16-21

  Ruscitti, Piero ^a   Cipriani, Paola ^a   Ciccia, Francesco ^b   Masedu, Francesco ^a   Liakouli, Vasiliki ^a   Carubbi, Francesco ^a   Berardicurti, Onorina ^a   Guggino, Giuliana ^b   Di Benedetto, Paola ^a   Di Bartolomeo, Salvatore ^a   Valenti, Marco ^a   Triolo, Giovanni ^b   Giacomelli, Roberto ^a  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

Author keywords

Adult onset Still's disease; Hyperferritinemic syndrome; Macrophage activation syndrome

Indexed keywords

FERRITIN; IMMUNOSUPPRESSIVE AGENT;

ADULT; AUTOIMMUNE DISEASE; CLINICAL ARTICLE; CLINICAL OUTCOME; CLINICAL STUDY; COHORT ANALYSIS; DEATH; DISEASE ASSOCIATION; FEMALE; FERRITIN BLOOD LEVEL; FOLLOW UP; HEALTH CENTER; HUMAN; MACROPHAGE ACTIVATION SYNDROME; MALE; MORTALITY; PROGNOSIS; REVIEW; RHEUMATIC DISEASE; AUTOIMMUNE DISEASES; CLINICAL TRIAL; MIDDLE AGED; MULTICENTER STUDY; OUTPATIENT DEPARTMENT; RETROSPECTIVE STUDY; TREATMENT OUTCOME;

ADULT; AMBULATORY CARE FACILITIES; AUTOIMMUNE DISEASES; FEMALE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MACROPHAGE ACTIVATION SYNDROME; MALE; MIDDLE AGED; PROGNOSIS; RETROSPECTIVE STUDIES; TREATMENT OUTCOME;

EID: 84992061046     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2016.09.016     Document Type: Review

References (58)

1. [1] Bode, S.F., Lehmberg, K., Maul-Pavicic, A., Vraetz, T., Janka, G., Stadt, U.Z., Ehl, S., Recent advances in the diagnosis and treatment of hemophagocytic lymphohistiocytosis. Arthritis Res Ther, 14, 2012, 213.
2. [2] Filipovich, A.H., Hemophagocytic lymphohistiocytosis (HLH) and related disorders. Hematology Am Soc Hematol Educ Program, 127-31, 2009.
3. [3] Ramos-Casals, M., Brito-Zerón, P., López-Guillermo, A., Khamashta, M.A., Bosch, X., Adult haemophagocytic syndrome. Lancet 383 (2014), 1503–1516.
4. [4] Ravelli, A., Davì, S., Minoia, F., Martini, A., Cron, R.Q., Macrophage activation syndrome. Hematol Oncol Clin North Am 29 (2015), 927–941.
5. [5] Grom, A.A., Horne, A., De Benedetti, F., Macrophage activation syndrome in the era of biologic therapy. Nat Rev Rheumatol 12 (2016), 259–268.
6. [6] Janka, G.E., Lehmberg, K., Hemophagocytic lymphohistiocytosis: pathogenesis and treatment. Hematology Am Soc Hematol Educ Program 2013 (2013), 605–611.
7. [7] Batu, E.D., Erden, A., Seyhoğlu, E., Kilic, L., Büyükasık, Y., Karadag, O., Bilginer, Y., Bilgen, S.A., Akdogan, A., Kiraz, S., Ertenli, A.I., Özen, S., Kalyoncu, U., Assessment of the HScore for reactive haemophagocytic syndrome in patients with rheumatic diseases. Scand J Rheumatol 30 (Jun 2016), 1–5 [Epub ahead of print].
8. [8] Arlet, J.B., Le, T.H., Marinho, A., Amoura, Z., Wechsler, B., Papo, T., Piette, J.C., Reactive haemophagocytic syndrome in adult-onset Still's disease: a report of six patients and a review of the literature. Ann Rheum Dis 65 (2006), 1596–1601.
9. [9] Arceci, R.J., When T cells and macrophages do not talk: the hemophagocytic syndromes. Curr Opin Hematol 15 (2008), 359–367.
10. [10] Chen, M., Felix, K., Wang, J., Critical role for perforin and Fas-dependent killing of dendritic cells in the control of inflammation. Blood 119 (2012), 127–136.
11. [11] Canna, S.W., Behrens, E.M., Not all hemophagocytes are created equally: appreciating the heterogeneity of the hemophagocytic syndromes. Curr Opin Rheumatol 24 (2012), 113–118.
12. [12] Lykens, J.E., Terrell, C.E., Zoller, E.E., Risma, K., Jordan, M.B., Perforin is a critical physiologic regulator of T-cell activation. Blood 118 (2011), 618–626 [54].
13. [13] Behrens, E.M., Canna, S.W., Slade, K., Rao, S., Kreiger, P.A., Paessler, M., Kambayashi, T., Koretzky, G.A., Repeated TLR9 stimulation results in macrophage activation syndrome-like disease in mice. J Clin Invest 121 (2011), 2264–2277.
14. [14] Rosário, C., Zandman-Goddard, G., Meyron-Holtz, E.G., D'Cruz, D.P., Shoenfeld, Y., The hyperferritinemic syndrome: macrophage activation syndrome, Still's disease, septic shock and catastrophic antiphospholipid syndrome. BMC Med, 11, 2013, 185.
15. [15] Henter, J.I., Elinder, G., Ost, A., Diagnostic guidelines for hemophagocytic lymphohistiocytosis. The FHL Study Group of the Histiocyte Society. Semin Oncol 18 (1991), 29–33.
16. [16] Henter, J.I., Horne, A., Aricó, M., Egeler, R.M., Filipovich, A.H., Imashuku, S., Ladisch, S., McClain, K., Webb, D., Winiarski, J., Janka, G., HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 48 (2007), 124–131.
17. [17] Klabunde, C.N., Potosky, A.L., Legler, J.M., Warren, J.L., Development of a comorbidity index using physician claims data. J Clin Epidemiol 53 (2000), 1258–1267.
18. [18] Charlson, M.E., Pompei, P., Ales, K.L., MacKenzie, C.R., A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40 (1987), 373–383.
19. [19] Vilaiyuk, S., Sirachainan, N., Wanitkun, S., Pirojsakul, K., Vaewpanich, J., Recurrent macrophage activation syndrome as the primary manifestation in systemic lupus erythematosus and the benefit of serial ferritin measurements: a case-based review. Clin Rheumatol 32 (2013), 899–904.
20. [20] Carvalheiras, G., Anjo, D., Mendonça, T., Vasconcelos, C., Farinha, F., Hemophagocytic syndrome as one of the main primary manifestations in acute systemic lupus erythematosus—case report and literature review. Lupus 19 (2010), 756–761.
21. [21] Tochihara, M., Kasai, M., Katsumata, Y., Sato, E., Ishiguro, N., Kazama, H., Sugimoto, N., Ichida, H., Kawaguchi, Y., Yamanaka, H., Erythematosus plaques with macrophage infiltration as an initial manifestation of macrophage activation syndrome in a patient with systemic lupus erythematosus. Mod Rheumatol 18 (Jul 2014), 1–2 [Epub ahead of print].
22. [22] Efthimiou, P., Kadavath, S., Mehta, B., Life-threatening complications of adult-onset Still's disease. Clin Rheumatol 33 (2014), 305–314.
23. [23] Behrens, E.M., Beukelman, T., Paessler, M., Cron, R.Q., Occult macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis. J Rheumatol 34 (2007), 1133–1138.
24. [24] Bae, C.B., Jung, J.Y., Kim, H.A., Suh, C.H., Reactive hemophagocytic syndrome in adult-onset Still disease: clinical features, predictive factors, and prognosis in 21 patients. Medicine (Baltimore), 94, 2015, e451.
25. [25] Kalyoncu, U., Buyukasik, Y., Akdogan, A., Karadag, O., Bilgen, S.A., Kiraz, S., Ertenli, I., Calguneri, M., Increased serum vitamin B12 levels are associated with adult-onset Still's disease with reactive macrophage activation syndrome. Joint Bone Spine 77 (2010), 131–134.
26. [26] Lenert, A., Yao, Q., Macrophage activation syndrome complicating adult onset Still's disease: a single center case series and comparison with literature. Semin Arthritis Rheum 45 (2016), 711–716.
27. [27] Kaito, K., Kobayashi, M., Katayama, T., Otsubo, H., Ogasawara, Y., Sekita, T., Saeki, A., Sakamoto, M., Nishiwaki, K., Masuoka, H., Shimada, T., Yoshida, M., Hosoya, T., Prognostic factors of hemophagocytic syndrome in adults: analysis of 34 cases. Eur J Haematol 59 (1997), 247–253.
28. [28] Takahashi, N., Chubachi, A., Kume, M., Hatano, Y., Komatsuda, A., Kawabata, Y., Yanagiya, N., Ichikawa, Y., Miura, A.B., Miura, I., A clinical analysis of 52 adult patients with hemophagocytic syndrome: the prognostic significance of the underlying diseases. Int J Hematol 74 (2001), 209–213.
29. [29] Cohen, L.A., Gutierrez, L., Weiss, A., Leichtmann-Bardoogo, Y., Zhang, D.L., Crooks, D.R., Sougrat, R., Morgenstern, A., Galy, B., Hentze, M.W., Lazaro, F.J., Rouault, T.A., Meyron-Holtz, E.G., Serum ferritin is derived primarily from macrophages through a nonclassical secretory pathway. Blood 116 (2010), 1574–1584.
30. [30] Torti, F.M., Torti, S.V., Regulation of ferritin genes and protein. Blood 99 (2002), 3505–3516.
31. [31] Chen, D.Y., Lan, J.L., Lin, F.J., Hsieh, T.Y., Proinflammatory cytokine profiles in sera and pathological tissues of patients with active untreated adult onset Still's disease. J Rheumatol 31 (2004), 2189–2198.
32. [32] Maruyama, J., Inokuma, S., Cytokine profiles of macrophage activation syndrome associated with rheumatic diseases. J Rheumatol 37 (2010), 967–973.
33. [33] Smirnov, I.M., Bailey, K., Flowers, C.H., Garrigues, N.W., Wesselius, L.J., Effects of TNF-alpha and IL-1beta on iron metabolism by A549 cells and influence on cytotoxicity. Am J Physiol 277 (1999), L257–L263.
34. [34] Wei, Y., Miller, S.C., Tsuji, Y., Torti, S.V., Torti, F.M., Interleukin 1 induces ferritin heavy chain in human muscle cells. Biochem Biophys Res Commun 169 (1990), 289–296.
35. [35] Piñero, D.J., Hu, J., Cook, B.M., Scaduto, R.C. Jr., Connor, J.R., Interleukin-1beta increases binding of the iron regulatory protein and the synthesis of ferritin by increasing the labile iron pool. Biochim Biophys Acta 1497 (2000), 279–288.
36. [36] Ruscitti, P., Cipriani, P., Di Benedetto, P., Ciccia, F., Liakouli, V., Carubbi, F., Berardicurti, O., Rizzo, A., Triolo, G., Giacomelli, R., Increased level of H-ferritin and its imbalance with L-ferritin, in bone marrow and liver of patients with adult onset Still's disease, developing macrophage activation syndrome, correlate with the severity of the disease. Autoimmun Rev 14 (2015), 429–437.
37. [37] Ruscitti, P., Ciccia, F., Cipriani, P., Guggino, G., Di Benedetto, P., Rizzo, A., Liakouli, V., Berardicurti, O., Carubbi, F., Triolo, G., Giacomelli, R., The CD68(+)/H-ferritin(+) cells colonize the lymph nodes of the patients with adult onset Still's disease and are associated with increased extracellular level of H-ferritin in the same tissue: correlation with disease severity and implication for pathogenesis. Clin Exp Immunol 183 (2016), 397–404.
38. [38] Ruscitti, P., Cipriani, P., Ciccia, F., Di Benedetto, P., Liakouli, V., Berardicurti, O., Carubbi, F., Guggino, G., Di Bartolomeo, S., Triolo, G., Giacomelli, R., H-ferritin and CD68 +/H-ferritin + monocytes/macrophages are increased in the skin of adult onset Still's disease patients and correlate with the multi-visceral involvement of the disease. Clin Exp Immunol, Jun 18 2016, 10.1111/cei.12826 [Epub ahead of print].
39. [39] Minoia, F., Davì, S., Horne, A., Bovis, F., Demirkaya, E., Akikusa, J., Ayaz, N.A., Al-Mayouf, S.M., Barone, P., Bica, B., Bolt, I., Breda, L., De Cunto, C., Enciso, S., Gallizzi, R., Griffin, T., Hennon, T., Horneff, G., Jeng, M., Kapovic, A.M., Lipton, J.M., Magni Manzoni, S., Rumba-Rozenfelde, I., Magalhaes, C.S., Sewairi, W.M., Stine, K.C., Vougiouka, O., Weaver, L.K., Davidsone, Z., De Inocencio, J., Ioseliani, M., Lattanzi, B., Tezer, H., Buoncompagni, A., Picco, P., Ruperto, N., Martini, A., Cron, R.Q., Ravelli, A., Pediatric Rheumatology International Trials Organization, Childhood Arthritis and Rheumatology Research Alliance, Pediatric Rheumatology Collaborative Study Group; Histiocyte Society. Dissecting the heterogeneity of macrophage activation syndrome complicating systemic juvenile idiopathic arthritis. J Rheumatol 42 (2015), 994–1001.
40. [40] Minoia, F., Davì, S., Horne, A., Demirkaya, E., Bovis, F., Li, C., Lehmberg, K., Weitzman, S., Insalaco, A., Wouters, C., Shenoi, S., Espada, G., Ozen, S., Anton, J., Khubchandani, R., Russo, R., Pal, P., Kasapcopur, O., Miettunen, P., Maritsi, D., Merino, R., Shakoory, B., Alessio, M., Chasnyk, V., Sanner, H., Gao, Y.J., Huasong, Z., Kitoh, T., Avcin, T., Fischbach, M., Frosch, M., Grom, A., Huber, A., Jelusic, M., Sawhney, S., Uziel, Y., Ruperto, N., Martini, A., Cron, R.Q., Ravelli, A., Pediatric Rheumatology International Trials Organization, Childhood Arthritis and Rheumatology Research Alliance Pediatric Rheumatology Collaborative Study Group, Histiocyte Society, Clinical features, treatment, and outcome of macrophage activation syndrome complicating systemic juvenile idiopathic arthritis: a multinational, multicenter study of 362 patients. Arthritis Rheumatol 66 (2014), 3160–3169.
41. [41] Wang, Y., Huang, W., Hu, L., Cen, X., Li, L., Wang, J., Shen, J., Wei, N., Wang, Z., Multicenter study of combination DEP regimen as a salvage therapy for adult refractory hemophagocytic lymphohistiocytosis. Blood 126 (2015), 2186–2192.
42. [42] Kumakura, S., Murakawa, Y., Clinical characteristics and treatment outcomes of autoimmune-associated hemophagocytic syndrome in adults. Arthritis Rheumatol 66 (2014), 2297–2307.
43. [43] Buyse, S., Teixeira, L., Galicier, L., Mariotte, E., Lemiale, V., Seguin, A., Bertheau, P., Canet, E., de Labarthe, A., Darmon, M., Rybojad, M., Schlemmer, B., Azoulay, E., Critical care management of patients with hemophagocytic lymphohistiocytosis. Intensive Care Med 36 (2010), 1695–1702.
44. [44] Escalante, A., del Rincon, I., How much disability in rheumatoid arthritis is explained by rheumatoid arthritis?. Arthritis Rheum 42 (1999), 1712–1721.
45. [45] Radner, H., Smolen, J.S., Aletaha, D., Impact of comorbidity on physical function in patients with rheumatoid arthritis. Ann Rheum Dis 69 (2010), 536–541.
46. [46] Janka, G.E., Schneider, E.M., Modern management of children with haemophagocytic lymphohistiocytosis. Br J Haematol 124 (2004), 4–14.
47. [47] Wong, K.F., Hui, P.K., Chan, J.K., Chan, Y.W., Ha, S.Y., The acute lupus hemophagocytic syndrome. Ann Intern Med 114 (1991), 387–390.
48. [48] Bürgi, U., Mendez, A., Hasler, P., Hüllstrung, H.D., Hemophagocytic syndrome in adult-onset Still's disease (AOSD): a must for biologics?—Case report and brief review of the literature. Rheumatol Int 32 (2012), 3269–3272.
49. [49] Fujii, K., Kitamura, Y., Osugi, Y., Koyama, Y., Ota, T., A case of adult-onset Still's disease complicated by hemophagocytic syndrome and interstitial pneumonia with pneumomediastinum/recurrent pneumothorax. Int J Rheum Dis 15 (2012), e60–e62.
50. [50] Emmenegger, U., Frey, U., Reimers, A., Fux, C., Semela, D., Cottagnoud, P., Spaeth, P.J., Neftel, K.A., Hyperferritinemia as indicator for intravenous immunoglobulin treatment in reactive macrophage activation syndromes. Am J Hematol 68 (2001), 4–10.
51. [51] Takahashi, N., Naniwa, T., Banno, S., Successful use of etanercept in the treatment of acute lupus hemophagocytic syndrome. Mod Rheumatol 18 (2008), 72–75.
52. [52] Henzan, T., Nagafuji, K., Tsukamoto, H., Miyamoto, T., Gondo, H., Imashuku, S., Harada, M., Success with infliximab in treating refractory hemophagocytic lymphohistiocytosis. Am J Hematol 81 (2006), 59–61.
53. [53] Bosman, G., Langemeijer, S.M., Hebeda, K.M., Raemaekers, J.M., Pickkers, P., van der Velden, W.J., The role of rituximab in a case of EBV-related lymphoproliferative disease presenting with haemophagocytosis. Neth J Med 67 (2009), 364–365.
54. [54] Balamuth, N.J., Nichols, K.E., Paessler, M., Teachey, D.T., Use of rituximab in conjunction with immunosuppressive chemotherapy as a novel therapy for Epstein Barr virus-associated hemophagocytic lymphohistiocytosis. J Pediatr Hematol Oncol 29 (2007), 569–573.
55. [55] Kelly, A., Ramanan, A.V., A case of macrophage activation syndrome successfully treated with anakinra. Nat Clin Pract Rheumatol 4 (2008), 615–620.
56. [56] Miettunen, P.M., Narendran, A., Jayanthan, A., Behrens, E.M., Cron, R.Q., Successful treatment of severe paediatric rheumatic disease-associated macrophage activation syndrome with interleukin-1 inhibition following conventional immunosuppressive therapy: case series with 12 patients. Rheumatology (Oxford) 50 (2011), 417–419.
57. [57] Landewé, R., van der Heijde, D., Follow up studies in rheumatoid arthritis. Ann Rheum Dis 61 (2002), 479–481.
58. [58] Salas, M., Hofman, A., Stricker, B.H., Confounding by indication: an example of variation in the use of epidemiologic terminology. Am J Epidemiol 149 (1999), 981–983.