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Rheumatology International

, Volume 39, Issue 1, pp 97–104 | Cite as

Are the 2016 EULAR/ACR/PRINTO classification criteria for macrophage activation syndrome applicable to patients with adult-onset Still’s disease?

  • Yoshifumi Tada
  • Satomi Inokuchi
  • Akihito Maruyama
  • Rie Suematsu
  • Mariko Sakai
  • Yuri Sadanaga
  • Nobuyuki Ono
  • Yojiro Arinobu
  • Syuichi Koarada
Classification Criteria
  • 222 Downloads

Abstract

The objectives of this study are to determine whether the 2016 European League Against Rheumatism/American College of Rheumatology/Paediatric Rheumatology International Trials Organization classification criteria for macrophage activation syndrome (MAS) complicating systemic juvenile idiopathic arthritis (SJIA) can be used to identify MAS in patients with adult-onset Still’s disease (AOSD). Using laboratory data from 76 AOSD patients with and without MAS, we analyzed the ability of the collective and individual constitutive elements of the 2016 MAS in SJIA criteria and additional laboratory measures to discriminate between AOSD patients with (n = 16) and without (n = 60) MAS. Cutoff values to determine the sensitivity, specificity, and predictive values were calculated from receiver operating characteristic curves, and modified classification criteria for MAS in AOSD were evaluated. The 2016 MAS in SJIA classification criteria had an overall sensitivity of 100%, specificity of 70.0%, positive predictive value of 47.1%, and negative predictive value of 100% to discriminate between AOSD patients with and without MAS based on laboratory data. Among the individual criteria, the sensitivity of triglycerides (46.7%) and the specificity of ferritin (15.0%) for MAS in AOSD were particularly low. The sensitivity and specificity for classifying MAS in AOSD patients were increased to 100 and 93%, respectively, by excluding triglycerides and changing the cutoff values for other criteria in the 2016 MAS in SJIA classification. The 2016 classification criteria for MAS in SJIA had higher sensitivity but lower specificity to identify MAS in AOSD patients compared with SJIA patients.

Keywords

Adult-onset Still’s disease Macrophage activation syndrome Classification criteria Ferritin Fibrinogen Platelet 

Notes

Acknowledgements

The authors thank Ms. Eguchi and Ms. Ibe for secretarial assistance and Atsushi Kawaguchi for statistical analysis. We thank Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

Author contributions

YT was responsible for the design of the study, acquisition, analysis and evaluation of the data, and manuscript preparation. SI, NO, and SK were responsible for acquisition and evaluation of the data, and discussion; AM, RS, MS, YS, and YM were responsible for the acquisition and interpretation of the data. All the authors have read, revised, and approved the content of the manuscript. All the authors agreed to be accountable for the accuracy or integrity of the work.

Compliance with ethical standards

Conflict of interest

Author Tada Y has received research grants and personal fees from Mitsubishi-Tanabe, Chugai, Astellas, Takeda, Teijin, and Eisai, personal fees from Novartis, Sanofi, Actelion, Daiichi Sankyo, Ayumi, Abbvie, Bristol-Myers Squibb, Janssen, Asahikasei, Nippon Kayaku, and Pfizer, outside the submitted work. Author Maruyama A has received a speaker honorarium from Janssen, Mitsubishi-Tanabe, Chugai, Astellas, and Bristol-Myers Squibb, outside the submitted work. Author Ono N has received personal fees from Mitsubishi-Tanabe, Chugai, Astellas, Takeda, Teijin, Abbvie, and Bristol-Myers Squibb, outside the submitted work. Author Arinobu Y has received personal fees from Mitsubishi-Tanabe, Chugai, Astellas, Takeda, Eisai, Actelion, Abbvie, Bristol-Myers Squibb, Daiichi-Sankyo, Ayumi, Asahikasei, and Nihon Shinyaku, outside the submitted work. Author Koarada S has received personal fees from Mitsubishi-Tanabe, Chugai, Astellas, Takeda, Eisai, Novartis, Abbvie, Bristol-Myers Squibb, Sanofi, Janssen, Pfizer, and Asahikasei, outside the submitted work. The authors Inokuchi S, Suematsu R, Sakai M, and Sadanaga Y declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. For this type of study formal consent is not required. This study was approved by the Saga University Hospital Ethics Committee (#2017-07-R-01) and the Kyushu University Hospital Ethics Committee (#29–521).

Supplementary material

296_2018_4114_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 14 KB)

References

  1. 1.
    Bywaters EG (1971) Still’s disease in the adult. Ann Rheum Dis 30:121CrossRefGoogle Scholar
  2. 2.
    Ohta A, Yamaguchi M, Kaneoka H, Nagayoshi T, Hiida M (1987) Adult Still’s disease: review of 228 cases from the literature. J Rheumatol 14:1139–1146Google Scholar
  3. 3.
    Jamilloux Y, Gerfaud-Valentin M, Martinon F, Belot A, Henry T, Sève P (2015) Pathogenesis of adult-onset Still’s disease: new insights from the juvenile counterpart. Immunol Res 61:53–62.  https://doi.org/10.1007/s12026-014-8561-9 CrossRefGoogle Scholar
  4. 4.
    Schulert GS, Grom AA (2014) Macrophage activation syndrome and cytokine-directed therapies. Best Pract Res Clin Rheumatol 28:277–292.  https://doi.org/10.1016/j.berh.2014.03.002 CrossRefGoogle Scholar
  5. 5.
    Kumakura S, Ishikura H, Kondo M, Murakawa Y, Masuda J, Kobayashi S (2004) Autoimmune-associated hemophagocytic syndrome. Mod Rheumatol 14:205–215.  https://doi.org/10.1007/s10165-004-0293-6 CrossRefGoogle Scholar
  6. 6.
    Asanuma YF, Mimura T, Tsuboi H, Noma H, Miyoshi F, Yamamoto K, Sumida T (2015) Nationwide epidemiological survey of 169 patients with adult Still’s disease in Japan. Mod Rheumatol 25:393–400.  https://doi.org/10.3109/14397595.2014.974881 CrossRefGoogle Scholar
  7. 7.
    Arlet JB, Le TH, Marinho A, Amoura Z, Wechsler B, Papo T, Piette JC (2006) Reactive haemophagocytic syndrome in adult-onset Still’s disease: a report of six patients and a review of the literature. Ann Rheum Dis 65:1596–1601.  https://doi.org/10.1136/ard.2005.046904 CrossRefGoogle Scholar
  8. 8.
    Gerfaud-Valentin M, Maucort-Boulch D, Hot A, Iwaz J, Ninet J, Durieu I, Broussolle C, Sève P (2014) Adult-onset still disease: manifestations, treatment, outcome, and prognostic factors in 57 patients. Medicine (Baltimore) 93:91–99.  https://doi.org/10.1097/MD.0000000000000021 CrossRefGoogle Scholar
  9. 9.
    Hot A, Toh ML, Coppèrè B, Perard L, Madoux MH, Mausservey C, Desmurs-Clavel H, Ffrench M, Ninet J (2010) Reactive hemophagocytic syndrome in adult-onset Still disease. Clinical features and long-term outcome: a case-control study of 8 patients. Medicine (Baltimore) 89:37–46.  https://doi.org/10.1097/MD.0b013e3181caf100 CrossRefGoogle Scholar
  10. 10.
    Ruscitti P, Rago C, Breda L, Cipriani P, Liakouli V, Berardicurti O, Carubbi F, Di Battista C, Verrotti A, Giacomelli R (2017) Macrophage activation syndrome in Still’s disease: analysis of clinical characteristics and survival in paediatric and adult patients. Clin Rheumatol 36:2839–2845.  https://doi.org/10.1007/s10067-017-3830-3 CrossRefGoogle Scholar
  11. 11.
    Kumakura S, Murakawa Y (2014) Clinical characteristics and treatment outcomes of autoimmune-associated hemophagocytic syndrome in adults. Arthritis Rheumatol 66:2297–2307.  https://doi.org/10.1002/art.38672 CrossRefGoogle Scholar
  12. 12.
    Efthimiou P, Kadavath S, Mehta B (2014) Life-threatening complications of adult-onset Still’s disease. Clin Rheumatol 33:305–314.  https://doi.org/10.1007/s10067-014-2487-4 CrossRefGoogle Scholar
  13. 13.
    Schulert GS, Grom AA (2015) Pathogenesis of macrophage activation syndrome and potential for cytokine-directed therapies. Annu Rev Med 66:145–159.  https://doi.org/10.1146/annurev-med-061813-012806 CrossRefGoogle Scholar
  14. 14.
    Ruscitti P, Cipriani P, Ciccia F, Masedu F, Liakouli V, Carubbi F, Berardicurti O, Guggino G et al (2017) 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. Autoimmun Rev 16:16–21.  https://doi.org/10.1016/j.autrev.2016.09.016 CrossRefGoogle Scholar
  15. 15.
    Aytaç S, Batu ED, Ünal Ş, Bilginer Y, Çetin M, Tuncer M, Gümrük F, Özen S (2016) Macrophage activation syndrome in children with systemic juvenile idiopathic arthritis and systemic lupus erythematosus. Rheumatol Int 36:1421–1429.  https://doi.org/10.1007/s00296-016-3545-9 CrossRefGoogle Scholar
  16. 16.
    Bae CB, Jung JY, Kim HA, Suh CH (2015) Reactive hemophagocytic syndrome in adult-onset Still Disease. Clinical features, predictive factors, and prognosis in 21 patients. Medicine (Baltimore) 94:e451.  https://doi.org/10.1097/MD.0000000000000451 CrossRefGoogle Scholar
  17. 17.
    Minoia F, Davì S, Horne A, Demirkaya E, Bovis F, Li C, Lehmberg K, Weitzman S et al (2014) Clinical features, treatment, and outcome of macrophage activation syndrome complicating systemic juvenile idiopathic arthritis: a multinational, multicenter study of 362 patients. Arthritis Rheumatol 66:3160–3169.  https://doi.org/10.1002/art.38802 CrossRefGoogle Scholar
  18. 18.
    Machaczka M, Klimkowska M (2015) Bone marrow assessment in the diagnosis of acquired hemophagocytic lymphohistiocytosis in adults. Am J Clin Pathol 143:308–309.  https://doi.org/10.1309/AJCPUK8TLI2MLYOQ CrossRefGoogle Scholar
  19. 19.
    Henter JI, Home A, Aricò M, Egeler RM, Filipovich AH, Imashuku S, Ladisch S, McClain K et al (2007) HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 48:124–131CrossRefGoogle Scholar
  20. 20.
    Ravelli A, Minoia F, Davì S, Horne A, Bovis F, Pistorio A, Aricò M, Avcin T et al (2016) 2016 Classification Criteria for Macrophage Activation Syndrome complicating Systemic Juvenile Idiopathic Arthritis. A European League Against Rheumatism/American College of Rheumatology/Paediatric Rheumatology International Trials Organisation collaborative initiative. Ann Rheum Dis 75:481–489.  https://doi.org/10.1136/annrheumdis-2015-208982 CrossRefGoogle Scholar
  21. 21.
    Yamaguchi M, Ohta A, Tsunematsu T, Kasukawa R, Mizushima Y, Kashiwagi H, Kashiwazaki S (1992) Preliminary criteria for classification of adult Still’s disease. J Rheumatol 19:424–430Google Scholar
  22. 22.
    Henter JI, Aricò M, Elinder G, Imashuku S, Janka G (1998) Familial hemophagocytic lymphohistiocytosis. Primary hemophagocytic lymphohistiocytosis. Hematol Oncol Clin North Am 12:417–433CrossRefGoogle Scholar
  23. 23.
    Janka G, Imashuku S, Elinder G, Schneider M, Henter JI (1998) Infection- and malignancy-associated hemophagocytic syndromes. Secondary hemophagocytic lymphohistiocytosis. Hematol Oncol Clin North Am 12:435–444CrossRefGoogle Scholar
  24. 24.
    Minoia F, Bovis F, Davì S, Insalaco A, Lehmberg K, Shenoi S, Weitzman S, Espada G et al (2017) Development and initial validation of the macrophage activation syndrome/primary hemophagocytic lymphohistiocytosis score, a diagnostic tool that differentiates primary hemophagocytic lymphohistiocytosis from macrophage activation syndrome. J Pediatr 189:72–78.  https://doi.org/10.1007/s10067-017-3830 CrossRefGoogle Scholar
  25. 25.
    Tsuda H, Shirono K (1996) Serum lipids in adult patients with hemophagocytic syndrome. Am J Hematol 53(199612):285.  https://doi.org/10.1002/(SICI)1096-8652 5 :AID-AJH21>3.0.CO;2-A ) : 53:4<28CrossRefGoogle Scholar
  26. 26.
    Tsuda H (1997) Hemophagocytic syndrome (HPS) in children and adults. Int J Hematol 65:215–226CrossRefGoogle Scholar
  27. 27.
    Lenert A, Yao Q (2016) Macrophage activation syndrome complicating adult onset Still’s disease: a single center case series and comparison with literature. Semin Arthritis Rheum 45:711–716.  https://doi.org/10.1016/j.semarthrit.2015.11.002 CrossRefGoogle Scholar
  28. 28.
    Imashuku S (1997) Differential diagnosis of hemophagocytic syndrome: underlying disorders and selection of the most effective treatment. Int J Hematol 66:135–151CrossRefGoogle Scholar
  29. 29.
    Mizuta M, Shimizu M, Inoue N, Kasai K, Nakagishi Y, Takahara T, Hamahira K, Yachie A (2016) Serum ferritin levels as a useful diagnostic marker for the distinction of systemic juvenile idiopathic arthritis and Kawasaki disease. Mod Rheumatol 26:929–932.  https://doi.org/10.3109/14397595.2016.1159120 CrossRefGoogle Scholar
  30. 30.
    Ahn SS, Yoo BW, Jung SM, Lee SW, Park YB, Song JJ (2017) Application of the 2016 EULAR/ACR/PRINTO classification criteria for macrophage activation syndrome in patients with adult-onset Still disease. J Rheumatol 44:996–1003.  https://doi.org/10.1016/j.jpeds.2017.06.005 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Rheumatology, Faculty of MedicineSaga UniversitySagaJapan
  2. 2.Department of Medicine and Biosystemic Science, Graduate School of Medical SciencesKyusyu UniversityFukuokaJapan

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