Non-mycosis fungoides cutaneous lymphomas in a referral center in Taiwan: A retrospective case series and literature review

Autoři: Kwei-Lan Liu aff001;  Wen-Chien Tsai aff002;  Chih-Hung Lee aff001
Působiště autorů: Department of Dermatology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan aff001;  Huang PH Dermatology and Aesthetics, Kaohsiung, Taiwan aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0228046



While mycosis fungoides (MF) and Sézary syndrome (SS) are the most common cutaneous lymphomas (CLs), there is limited data about non-MF/SS CLs.


We aimed to evaluate clinical characteristics of non-MF/SS CLs.


A retrospective analysis evaluated patients with non-MF/SS CLs covering a period of 17 years. The records of 59 patients with non-MF/SS CLs were reviewed for demographic profiles, clinical features, and survival outcomes.


Our series consisted of 38 non-MF/SS cutaneous T-cell lymphomas (CTCLs) and 21 cutaneous B-cell lymphomas (CBCLs). In the group of non-MF/SS CTCLs including 33 primary and five secondary cases, there were cases of anaplastic large cell lymphoma (15.3% of non-MF/SS CLs), extranodal natural killer/ T-cell lymphoma (13.5%), peripheral T-cell lymphoma, not otherwise specified (13,5%), adult T-cell leukemia/lymphoma (8.5%), subcutaneous panniculitis-like T-cell lymphoma (6.8%) and angioimmunoblastic T-cell lymphoma (6.8%). In the group of CBCLs including nine primary and 12 secondary cases, there were cases of diffuse large B-cell lymphoma (22.0%), mantle cell lymphoma (5.1%), extranodal marginal lymphoma of mucosa associated lymphoid tissue (3.4%), follicle center lymphoma (3.4%) and intravascular large B-cell lymphoma (1.7%). The overall survivals were 57 months for non-MF/SS CTCLs and 41.5 months for CBCLs. Elevated serum lactate dehydrogenase level, thrombocytopenia, multiple anatomical sites of skin involvement and lower albumin level may be associated with poor prognosis in non-MF/SS CTCLs, but the latter two were not in CBCLs.


With this series, we hope to provide indigenous data and outcome of non-MF/SS CLs. The overall survival of non-MF/SS CTCLs was better than CBCLs.

Klíčová slova:

Albumins – B cells – Lymphomas – Prognosis – Skin anatomy – T cells – Taiwan – Thrombocytopenia


1. Willemze R, Kerl H, Sterry W, Berti E, Cerroni L, Chimenti S, et al. EORTC classification for primary cutaneous lymphomas: a proposal from the Cutaneous Lymphoma Study Group of the European Organization for Research and Treatment of Cancer. Blood 1997;90:354–371. 9207472

2. Willemze R, Jaffe ES, Burg G, Cerroni L, Berti E, Swerdlow SH, et al. WHO-EORTC classification for cutaneous lymphomas. Blood 2005;105:3768–3785. doi: 10.1182/blood-2004-09-3502 15692063

3. Willemze R, Cerroni L, Kempf W, Berti E, Facchetti F, Swerdlow SH, et al. The 2018 update of the WHO-EORTC classification for primary cutaneous lymphomas. Blood 2019;133:1703–1714. doi: 10.1182/blood-2018-11-881268 30635287

4. Bradford PT, Devesa SS, Anderson WF, Toro JR. Cutaneous lymphoma incidence patterns in the United States: a population-based study of 3884 cases. Blood 2009;113:5064–5073. doi: 10.1182/blood-2008-10-184168 19279331

5. Willemze R, Meijer CJ. Classification of cutaneous T-cell lymphoma: from Alibert to WHO-EORTC. J Cutan Pathol 2006; 33 Suppl 1: 18–26.

6. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. 4th ed. vol. 2. Lyon: IARC Press; 2008.

7. Lee HS, Suh KS, Lee DY, Cho KH, Oh SH, Kim SC, et al. Cutaneous Lymphoma in Korea: A Nationwide Retrospective Study. Acta Derm Venereol 2016;96:535–539. doi: 10.2340/00015555-2283 26560051

8. Liao JB, Chuang SS, Chen HC, Tseng HH, Wang JS, Hsieh PP. Clinicopathologic analysis of cutaneous lymphoma in Taiwan: a high frequency of extranodal natural killer/T-cell lymphoma, nasal type, with an extremely poor prognosis. Arch Pathol Lab Med 2010;134:996–1002. doi: 10.1043/2009-0132-OA.1 20586627

9. Liu KL, Shen JL, Yang CS, Chen YJ. Mycosis fungoides in a referral center in central Taiwan: A retrospective case series and literature review. Dermatol Sin 2014;32:148–153.

10. Lee CN, Hsu CK, Chang KC, Wu CL, Chen TY, Lee JY. Cutaneous lymphomas in Taiwan: a review of 118 cases from a medical center in southern Taiwan. Dermatol Sin 2018;36:16–24.

11. Kim YH, Willemze R, Pimpinelli N, Whittaker S, Olsen EA, Ranki A, et al. TNM classification system for primary cutaneous lymphomas other than mycosis fungoides and Sézary syndrome: a proposal of the International Society for Cutaneous Lymphomas (ISCL) and the Cutaneous Lymphoma Task Force of the European Organization of Research and Treatment of Cancer (EORTC). Blood 2007;110:479–484. doi: 10.1182/blood-2006-10-054601 17339420

12. Assaf C, Gellrich S, Steinhoff M, Nashan D, Weisse F, Dippel E, et al. Cutaneous lymphomas in Germany: an analysis of the Central Cutaneous Lymphoma Registry of the German Society of Dermatology (DDG). J Dtsch Dermatol Ges. 2007;5:662–668. doi: 10.1111/j.1610-0387.2007.06337.x 17659039

13. Chang KC, Huang GC, Jones D, Tsao CJ, Lee JY, Su IJ. Distribution and prognosis of WHO lymphoma subtypes in Taiwan reveals a low incidence of germinal-center derived tumors. Leuk Lymphoma 2004;45:1375–1384. doi: 10.1080/10428194042000198849 15359636

14. Fujita A, Hamada T, Iwatsuki K. Retrospective analysis of 133 patients with cutaneous lymphomas from a single Japanese medical center between 1995 and 2008. J Dermatol 2001;38:524–530.

15. Hamada T, Iwatsuki K. Cutaneous lymphoma in Japan: a nationwide study of 1733 patients. J Dermatol 2014;41:3–10. doi: 10.1111/1346-8138.12299 24438138

16. Lee WJ, Lee SH, Moon IJ, Won CH, Chang SE, Choi JH, et al. Relative frequency, clinical features, and survival outcomes of 395 patients with cutaneous lymphoma in Korea: a subgroup analysis per 10-year period. Acta Derm Venereol 2016;96:888–893. doi: 10.2340/00015555-2404 26975334

17. Amador C, Greiner TC, Heavican TB, Smith LM, Galvis KT, Lone WG, et al. Reproducing the molecular subclassification of peripheral T-cell lymphoma-NOS by immunohistochemistry. Blood 2019 Sep 27. pii: blood.2019000779. doi: 10.1182/blood.2019000779 [Epub ahead of print] 31562134

18. Kim YM, Jeong SH, Kim JW, Lee SH, Hwang JH, Park YS, et al. Chronic hepatitis B, non-Hodgkin's lymphoma, and effect of prophylactic antiviral therapy. J Clin Virol 2011;51:241–245. doi: 10.1016/j.jcv.2011.05.004 21628103

19. Lim ST, Fei G, Quek R, Lim LC, Lee LH, Yap SP, et al. The relationship of hepatitis B virus infection and non-Hodgkin's lymphoma and its impact on clinical characteristics and prognosis. Eur J Haematol. 2007;79:132–137. doi: 10.1111/j.1600-0609.2007.00878.x 17635237

20. Chuang SS, Liao YL, Chang ST, Hsieh YC, Kuo SY, Lu CL, et al. Hepatitis C virus infection is significantly associated with malignant lymphoma in Taiwan, particularly with nodal and splenic marginal zone lymphomas. J Clin Pathol 2010;63:595–598. doi: 10.1136/jcp.2010.076810 20530156

21. Turner NC, Dusheiko G, Jones A. Hepatitis C and B-cell lymphoma. Ann Oncol 2003;14:1341–1345. doi: 10.1093/annonc/mdg363 12954572

22. Landau DA, Saadoun D, Calabrese LH, Cacoub P. The pathophysiology of HCV induced B-cell clonal disorders. Autoimmun Rev 2007;6:581–587. doi: 10.1016/j.autrev.2007.03.010 17854753

23. Yang JF, Lin CI, Huang JF, Dai CY, Lin WY, Ho CK, et al. Viral hepatitis infections in southern Taiwan: a multicenter community-based study. Kaohsiung J Med Sci. 2010;26:461–469. doi: 10.1016/S1607-551X(10)70073-5 20837342

24. Chen CH, Yang PM, Huang GT, Lee HS, Sung JL, Sheu JC. Estimation of seroprevalence of hepatitis B virus and hepatitis C virus in Taiwan from a large-scale survey of free hepatitis screening participants. J Formos Med Assoc 2007;106:148–155. doi: 10.1016/S0929-6646(09)60231-X 17339159

25. Park JH, Shin HT, Lee DY, Lee JH, Yang JM, Jang KT, et al. World Health Organization–European Organization for Research and Treatment of Cancer classification of cutaneous lymphoma in Korea: A retrospective study at a single tertiary institution. J Am Acad Dermatol 2012;67:1200–1209. doi: 10.1016/j.jaad.2012.02.033 22521781

26. Yasukawa K, Kato N, Kodama K, Hamasaka A, Hata H. The spectrum of cutaneous lymphomas in Japan: a study of 62 cases based on the World Health Organization Classification. J Cutan Pathol 2006;33:487–491. doi: 10.1111/j.1600-0560.2006.00460.x 16872471

27. Tan SH, Sim CS, Ong BH. Cutaneous lymphomas other than mycosis fungoides in Singapore: a clinicopathological analysis using recent classification systems. Br J Dermatol 2003;149:542–553. doi: 10.1046/j.1365-2133.2003.05476.x 14510987

28. Wang H, Li H, Xing X, Zhao C, Luo B. Genotypic analysis and latent membrane protein 1 expression of Epstein-Barr virus in extranodal NK/T-cell lymphoma from Northern Chinese patients. Arch Virol 2015;160:2071–2074. doi: 10.1007/s00705-015-2451-x 26008210

29. Khan G, Hashim MJ. Global burden of deaths from Epstein-Barr virus attributable malignancies 1990–2010. Infect Agent Cancer 2014;9:38. doi: 10.1186/1750-9378-9-38 25473414

30. Su WH, Hildesheim A, Chang YS. Human leukocyte antigens and Epstein-Barr virus-associated nasopharyngeal carcinoma: old associations offer new clues into the role of immunity in infection-associated cancers. Front Oncol 2013;3:299. doi: 10.3389/fonc.2013.00299 24367763

31. Gessain A, Cassar O. Epidemiological aspects and world distribution of HTLV-1 infection. Front Microbiol 2012;3:388. doi: 10.3389/fmicb.2012.00388 23162541

32. Ruggieri M, Berini C, Ducasa N, Malkovsky M, Fisch P, Biglione M. Molecular detection of human T-lymphotropic virus type 1 infection among oncology patients in Germany: A retrospective view. PLoS One 2019 May 28;14(5):e0217560. doi: 10.1371/journal.pone.0217560 eCollection 2019. 31136642

33. Shah UA, Shah N, Qiao B, Acuna-Villaorduna A, Pradhan K, Adrianzen Herrera D, et al. Epidemiology and survival trend of adult T-cell leukemia/lymphoma in the United States. Cancer 2019 Nov 26. doi: 10.1002/cncr.32556 [Epub ahead of print] 31769871

34. Grange F, Hedelin G, Joly P, Beylot-Barry M, D'Incan M, Delaunay M, et al. Prognostic factors in primary cutaneous lymphomas other than mycosis fungoides and the Sézary syndrome. The French Study Group on Cutaneous Lymphomas. Blood 1999;93:3637–3642. 10339469

35. Tomita N, Taguri M, Hashimoto C, Takasaki H, Fujimaki K, Motomura S, et al. Evaluation of soluble interleukin-2 receptor and serum lactate dehydrogenase in malignant lymphoma. Ann Hematol 2015;94:1935–1937. doi: 10.1007/s00277-015-2448-2 26208667

36. Duvic M, Apisarnthanarax N, Cohen DS, Smith TL, Ha CS, Kurzrock R. Analysis of long-term outcomes of combined modality therapy for cutaneous T-cell lymphoma. J Am Acad Dermatol 2003;49:35–49. 12833006

37. Park JH, Yoon DH, Kim DY, Kim S, Seo S, Jeong Y, et al. The highest prognostic impact of LDH among International Prognostic Indices (IPIs): an explorative study of five IPI factors among patients with DLBCL in the era of rituximab. Ann Hematol 2014;93:1755–1764. doi: 10.1007/s00277-014-2115-z 25027115

38. Hauswirth AW, Skrabs C, Schützinger C, Raderer M, Chott A, Valent P, et al. Autoimmune thrombocytopenia in non-Hodgkin's lymphomas. Haematologica 2008;93:447–450. doi: 10.3324/haematol.11934 18287133

39. Bhasin TS, Sharma S, Manjari M, Mannan R, Kansal V, Chandey M, et al. Changes in megakaryocytes in cases of thrombocytopenia: bone marrow aspiration and biopsy analysis. J Clin Diagn Res 2013;7:473–479. doi: 10.7860/JCDR/2013/5085.2801 23634399

40. Lee WJ, Won KH, Won CH, Chang SE, Choi JH, Moon KC, et al. Secondary cutaneous lymphoma: comparative clinical features and survival outcome analysis of 106 cases according to lymphoma cell lineage. Br J Dermatol 2015;173:134–145. doi: 10.1111/bjd.13582 25556641

41. Dalia S, Chavez JC, Bello CM, Chervenick PA, Little BJ, Al Ali NH, et al. A new prognostic index in diffuse large B-cell lymphoma using serum albumin: a pilot study evaluating the albumin adjusted-international prognostic index (A-IPI). Blood 2013;122:4267.

42. Bi XW, Wang L, Zhang WW, Yan SM, Sun P, Xia Y, et al. The pretreatment albumin to globulin ratio predicts survival in patients with natural killer/T-cell lymphoma. PeerJ 2016;4:e1742. doi: 10.7717/peerj.1742 26966671

Článek vyšel v časopise


2020 Číslo 1