Evaluation of secondary malignancies in a large series of mycosis fungoides<sup/>

Atci, Tugba; Ak, Dilay Yerlioğlu; Baykal, Can

doi:10.1016/j.abd.2023.06.004

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Original Article • An. Bras. Dermatol. 99 (3) • 2024 • https://doi.org/10.1016/j.abd.2023.06.004 copy

Evaluation of secondary malignancies in a large series of mycosis fungoides^☆ ☆ Study conducted at the Istanbul Medical Faculty, Istanbul University, Istanbul, Turkey.

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Background

An increased risk of Secondary Malignancies (SMs) in Mycosis Fungoides (MF) has been suggested previously. However, the relationship between this risk and the features of MF is not well-known.

Objective

To investigate the rate and types of SMs in a large cohort of MF patients focusing on the associated features of these patients.

Methods

The demographic features, subtype, and stage of MF, as well as the temporal relationship between the diagnosis of MF and the development of SMs were determined. Major clinical features of MF in this group were compared with MF patients without association of SMs.

Results

Among 730 MF patients with a mean follow-up period of 67.9 ± 52.4 months, 56 SMs were identified in a total of 52 (7.1%) patients. While 28.8% of patients were previously diagnosed with other malignancies, then subsequently had a diagnosis of MF, it was vice versa in 53.8% of patients. Most of the SM-associated MF patients had early-stage (80.7%) and classical type of MF (86.5%) without a significant difference from MF patients without association of SMs; 85.5% and 72.5%, respectively. The most commonly identified SMs were hematologic malignancies (64.3%) including lymphomatoid papulosis (n = 22), Hodgkin’s lymphoma (n = 4), non-Hodgkin’s lymphoma (n = 5), polycythemia vera (n = 2). Other most commonly associated malignancies were breast cancer (n = 4), prostate cancer (n = 3), renal cell carcinoma (n = 2), melanoma (n = 2), and Kaposi’s sarcoma (n = 2).

Study limitations

A single tertiary dermatology center study with a retrospective design.

Conclusion

Apart from the well-known lymphomatoid papulosis association, systemic hematological malignancies were also quite common in the large cohort of MF patients.

Keywords
Hematologic neoplasms; Lymphomatoid papulosis; Mycosis fungoides

Sex (number)	Age (mean), (range)^a a Age at the time of MF diagnosis, years.	MF subtype	Stage of MF	Secondary malignancy diagnosis	The temporal relationship of secondary malignancy regarding MF diagnosis (years)
					Before	Contemporaneously	After
Systemic hematologic malignancies
M (n = 4)	43.5 ± 12.5 (27‒57)	Classic (n = 3)	IA (n = 2)	Hodgkin's lymphoma	n = 3 (1‒6)	n = 1	-
		Folliculotropic (n = 1)	IB (n = 1)
		Folliculotropic (n = 1)	IVA (n = 1)
M (n = 3)	58.6 ± 13.5 (40‒74)	Classic (n = 4)	IB (n = 2)	Non Hodgkin’s lymphoma (S-ALCL, n = 4)^c c Associated lymphomatoid papulosis diagnosis in two of them.	n = 1 (3)	-	n = 4 (1‒11)
F (n = 2)		Folliculotropic (n = 1)	IIB (n = 2)
F (n = 2)		Folliculotropic (n = 1)	IVA (n = 1)
M (n = 1)	69	Classic + syringotropic	IB	Chronic lymphocytic leukemia	n = 1 (7)	-	-
M (n = 2)	58.5 ± 30.4 (37‒80)	Classic (n = 2)	IB (n = 1)	Polycythemia vera	n = 1 (25)	n = 1	-
M (n = 2)	58.5 ± 30.4 (37‒80)	Classic (n = 2)	IVA (n = 1)	Polycythemia vera	n = 1 (25)	n = 1	-
M (n = 1)	40	Classic	IB	Hypereosinophilic syndrome	-	-	n = 1 (7)
M (n = 1)	68	Classic	IB	MGUS	n = 1 (5)	-	-
Primary cutaneous lymphomas
M (n = 10)	42.9 ± 15.1 (16‒73)	Classic (n = 19)	IB (n = 12)	Lymphomatoid papulosis	n = 5 (1‒10)	n = 2	n = 15 (1‒20)
F (n = 12)		Folliculotropic (n = 1)	IA (n = 7)
		Granulomatous (n = 1)	IIA (n = 2)
		Hyperpigmented (n = 1)	IVA (n = 1)
		Poikilodermic (n = 1)	IVA (n = 1)
Cutaneous malignancies ^b b Excluding cutaneous epithelial tumors.
M (n = 2)	76.5 ± 2.1 (75‒78)	Folliculotropic (n = 1)	IB (n = 1)	Kaposi’s sarcoma	-	-	n = 2 (1‒3)
M (n = 2)	76.5 ± 2.1 (75‒78)	Poikilodermic (n = 1)	IIB (n = 1)	Kaposi’s sarcoma	-	-	n = 2 (1‒3)
M (n = 1)	41	Classic	IA	Fibromyxoid sarcoma	-	+	-
M (n = 1)	40 ± 12.7 (31‒49)	Classic (n = 2)	IA (n = 1)	Cutaneous melanoma	n = 1 (12)	‒	n = 1 (9)
F (n = 1)	40 ± 12.7 (31‒49)	Classic (n = 2)	IIB (n = 1)	Cutaneous melanoma	n = 1 (12)	‒	n = 1 (9)
Solid malignancies
F (n = 4)	55.2 ± 16.8 (30‒64)	Classic (n = 4)	IA (n = 2)	Breast cancer	n = 1 (3)	n = 1	n = 2 (2‒7)
F (n = 4)	55.2 ± 16.8 (30‒64)	Classic (n = 4)	IB (n = 2)	Breast cancer	n = 1 (3)	n = 1	n = 2 (2‒7)
F (n = 1)	64	Classic	IA	Lung cancer	-	+	-
M (n = 1)	54 ± 8.5 (48‒60)	Classic (n = 2)	IA (n = 1)	Renal cell carcinoma	-	n = 1	n = 1 (1)
F (n = 1)	54 ± 8.5 (48‒60)	Classic (n = 2)	IIA (n = 1)	Renal cell carcinoma	-	n = 1	n = 1 (1)
M (n = 3)	67 ± 8.2 (58‒74)	Classic (n = 3)	IB (n = 1)	Prostate cancer	n = 1 (1)	-	n = 2 (8-10)
M (n = 3)	67 ± 8.2 (58‒74)	Classic (n = 3)	IIB (n = 2)	Prostate cancer	n = 1 (1)	-	n = 2 (8-10)
M (n = 1)	55	Classic	IA	Papillary thyroid cancer	-	n = 1	-
M (n = 1)	55	Classic	IA	Astrocytoma	-	n = 1	-
M (n = 1)	68	Classic	IB	Hepatocellular carcinoma	-	n = 1	-
F (n = 1)	58	Classic	IA	Endometrium cancer	n = 1 (3)	-	-
F (n = 1)	87	Classic	IB	Gastric adenocarcinoma	-	-	n = 1 (2)

Study/Year/Country	Included cutaneous lymphoma types, patient number (n=)	Patients with secondary malignancies, n (%) (non-melanoma skin cancer excluded)	Most common malignancy, n (non-melanoma skin cancer excluded)	Other malignancies (n) (non-melanoma skin cancer excluded)	Ratio of hematologic malignancy among patients with secondary malignancies (%) (non-melanoma skin cancer excluded)
Olsen et al., 1984, USA³3 Olsen EA, Delzell E, Jegasothy BV. Second malignancies in cutaneous T cell lymphoma. J Am Acad Dermatol. 1984;10:197-204.	CTCL (n = 63)	10 (15.9)	Colon cancer (n = 2)	Bladder cancer (n = 1), prostate cancer (n = 1), pyriform sinus carcinoma (n = 1), thymus germinoma (n = 1), bronchus carcinoma (n = 1), kidney cancer (n = 1), uterus cancer (n = 1), breast cancer (n = 1)	Absent
Kantor et al., 1989, USA⁴4 Kantor AF, Curtis RE, Vonderheid EC, van Scott EJ, Fraumeni JF Jr. Risk of second malignancy after cutaneous T-cell lymphoma. Cancer. 1989;63:1612-5.	CTCL (n = 544)	35 (6)	Colon cancer (n = 7)	Digestive system cancer (n = 11), respiratory system cancer (n = 11), breast cancer (n = 3), hematologic malignancies (n = 6), others (n = 4)	17.1
Scarisbrick et al., 1999, England⁵5 Scarisbrick JJ, Child FJ, Evans AV, Fraser-Andrews EA, Spittle M, Russell-Jones R. Secondary malignant neoplasms in 71 patients with Sézary syndrome. Arch Dermatol. 1999;135:1381-	SS (n = 71)	9 (12.7)	Lung cancer (n = 2)	Endometrium cancer (n = 1), ovarian cancer (n = 1), pancreatic cancer (n = 1), HL (n = 1), prostate cancer (n = 1), bladder cancer (n = 1), unknown metastatic (n = 1)	11.1
Väkevä et al., 2000, Finland⁶6 Väkevä L, Pukkala E, Ranki A. Increased risk of secondary cancers in patients with primary cutaneous T cell lymphoma. J Invest Dermatol. 2000;115:62-5.	CTCL (n = 319)	33 (10)	Lung cancer (n = 12)	Digestive system cancer (n = 5), breast cancer (n = 4), HL (n = 2), NHL (n = 2), genitourinary cancer (n = 2), leukemia (n = 2)	18.2
Evans et al., 2004, United Kingdom⁷7 Evans AV, Scarisbrick JJ, Child FJ, Acland KM, Whittaker SJ, Russell-Jones R. Cutaneous malignant melanoma in association with mycosis fungoides. J Am Acad Dermatol. 2004;50:701-5.	MF (n = 285)	6 (2.1)	Melanoma (n = 6)	Not-included	NA
Huang et al., 2007, USA⁸8 Huang KP, Weinstock MA, Clarke CA, McMillan A, Hoppe RT, Kim YH. Second lymphomas and other malignant neoplasms in patients with mycosis fungoides and Sezary syndrome: evidence from population-based and clinical cohorts. Arch Dermatol. 2007;143:45-50.	MF & SS (n = 429)	37 (8.62)	HL and NHL (n = 7)	Colon cancer (n = 5), lung cancer (n = 5), biliary system cancer (n = 2), melanoma (n = 1)	18.9
Brownell et al., 2008, USA⁹9 Brownell I, Etzel CJ, Yang DJ, Taylor SH, Duvic M. Increased malignancy risk in the cutaneous T-cell lymphoma patient population. Clin Lymphoma Myeloma. 2008;8:100-5.	CTCL (n = 672)	37 (5.5)	NHL (n = 7)	Digestive system cancer (n = 3), respiratory system cancer (n = 4), melanoma (n = 2), HL (n = 2), AML (n = 3), CML (n = 1), multiple myeloma (n = 1), breast cancer (n = 1), prostate cancer (n = 5), female genital cancer (n = 4), urinary system cancer (n = 2), thyroid cancer (n = 1)	37.8
Herro et al., 2009, USA¹⁰10 Herro E, DiCaudo DJ, Davis MDP, Weaver AL, Swanson DL. Review of contemporaneous mycosis fungoides and B-cell malignancy at Mayo Clinic. J Am Acad Dermatol. 2009;61:271-5.	MF & SS (n = 533)	23 (4.16)	Systemic B-cell lymphomas (n = 23)	Not-included	NA
Hodak et al., 2013, Israel¹¹11 Hodak E, Lessin S, Friedland R, Freud T, David M, Pavlovsky L, et al. New insights into associated co-morbidities in patients with cutaneous T-cell lymphoma (mycosis fungoides). Acta Derm Venereol. 2013;93:451-5.	MF^a a Institution-based cohort. (n = 343)	51 (15)^a a Institution-based cohort.	Breast cancer (n = 9)^a a Institution-based cohort. colon and rectal cancer (n = 23)^b b Population-based cohort.	Hematologic malignancy (n = 16^a a Institution-based cohort. +10^b b Population-based cohort. ), breast cancer (n = 12^a a Institution-based cohort. +9^b b Population-based cohort. ), colon and rectal cancer (n = 23^a a Institution-based cohort. +4^b b Population-based cohort. ), prostate cancer (n = 17^a a Institution-based cohort. +9^b b Population-based cohort. ), lung cancer (n = 6^a a Institution-based cohort. +4^b b Population-based cohort. ), melanoma (n = 7^a a Institution-based cohort. +7^b b Population-based cohort. ), others (n = 7^a a Institution-based cohort. +8^b b Population-based cohort. )	18.2
	MF^b b Population-based cohort. (n = 683)	88 (13)^b b Population-based cohort.			18.2
Lindahl et al., 2014, Denmark¹²12 Lindahl LM, Fenger-Grøn M, Iversen L. Subsequent cancers, mortality, and causes of death in patients with mycosis fungoides and parapsoriasis: a Danish nationwide, population-based cohort study. J Am Acad Dermatol. 2014;71:529-35.	MF (n = 386)	65 (15)	Urinary tract and genitalia (n = 11)	NHL (n = 8), other hematologic malignancies (n = 2), digestive (n = 10), colorectal cancer (n = 5), respiratory cancer (n = 10), melanoma (n = 1), breast cancer (n = 6)	15.4
Amber et al., 2016, USA¹³13 Amber KT, Bloom R, Nouri K. Second primary malignancies in CTCL patients from 1992 to 2011: a SEER-based, population-based study evaluating time from CTCL diagnosis, age, sex, stage, and CD30+ subtype. Am J Clin Dermatol. 2016;17:71-7.	CTCL (n = 2923)	183 (6)	NHL (n = NA)	HL, lung cancer and penile cancer (n = NA)	NA
Cengiz et al., 2017, Turkey¹⁴14 Cengiz FP, Emiroglu N, Onsun N. Frequency and risk factors for secondary malignancies in patients with mycosis fungoides. Turk J Hematol. 2017;34:378-9.	MF (n = 143)	13 (9.1)	HL (n = 3)	NHL (n = 2), adult T-cell leukemia (n = 2), lung cancer (n = 2), renal cell cancer (n = 1), bladder cancer (n = 1), melanoma (n = 1)	53.9
Kommalapati et al., 2018, USA¹⁵15 Kommalapati A, Tella SH, Go RS, Bennani NN, Goyal G. A population‐based analysis of second primary malignancies in T‐cell neoplasms. Br J Haematol. 2019;185:338-42.	MF & SS (n = 4774)	472 (10)	NHL and HL (n = NA)	AML, thyroid cancer, prostate cancer, brain cancer, breast cancer, lung cancer (n = NA)	NA
Almukhtar et al., 2019, USA¹⁶16 Almukhtar R, Gill F, Soine R, McBurney E. Gender differences in the risk of secondary malignancies in patients with mycosis fungoides and Sézary syndrome. J Am Acad Dermatol. 2020;83:647-8.	MF & SS (n = 4229)	550 (13)	NHL (n = 98)	Lung cancer (n = 82), CLL (n = 14), HL (n = 13), melanoma (n = 23)	22.7
Goyal et al., 2020, USA¹⁷17 Goyal A, O'Leary D, Goyal K, Rubin N, Bohjanen K, Hordinsky M, et al. Increased risk of second primary malignancies in patients with mycosis fungoides: a single-center cohort study. J Am Acad Dermatol. 2020;82:736-8.	MF (n = 172)	24 (14)	Melanoma (n = 4)	Anaplastic large cell lymphoma (n = 1), bladder cancer (n = 2), breast cancer (n = 2), CLL (n=1), cholangiocarcinoma (n=1), colon cancer (n = 1) endometrial cancer (1), HL (n = 1), NHL (n = 1) pancreatic cancer (n = 1), prostate cancer (n = 3), renal cancer (n = 3), tongue cancer (n = 1), uterine cancer (n = 1)	12.5
Goyal et al., 2020, USA¹⁸18 Goyal A, O'Leary D, Goyal K, Rubin N, Bohjanen K, Hordinsky M, et al. Increased risk of second primary hematologic and solid malignancies in patients with mycosis fungoides: a Surveillance, Epidemiology, and End Results analysis. J Am Acad Dermatol. 2020;83:404-411.	MF (n = 6742)	511 (7.5)	NHL (n = 50)	HL (n = 3), leukemia (n = 7), multiple myeloma (n = 2), prostate cancer (n = 19), lung cancer (n = 12), colon cancer (n = 8)	12.1
Goyal et al., 2021, USA¹⁹19 Goyal A, O’Leary D, Goyal K, Rubin N, Janakiram M. Screening for second malignancies in mycosis fungoides: non‐Hodgkin lymphoma, Hodgkin lymphoma, lung cancer, bladder cancer and melanoma. J Eur Acad Dermatol Venereol. 2021;35:1821-9.	MF (n = 7984)	742 (9.29)	NHL (n = 99)	Melanoma (n = 25), HL (n = 14), lung cancer (n = 69), bladder cancer (n = 20)	15.2
Liu et al., 2021, Canada²⁰20 Liu YA, Finn AJ, Subtil A. Primary cutaneous lymphomas in patients with chronic lymphocytic leukemia/small lymphocytic lymphoma (CLL/SLL): a series of 12 cases. J Cutan Pathol. 2021;48:617-24.	MF & SS (n = 5)	5 (NA)	CLL/SLL (n = 5)	Not-included	NA
Scheu et al., 2021, Germany²¹21 Scheu A, Schnabl SM, Steiner DP, Fend F, Berneburg M, Yazdi AS. Importance of diagnostics and risk of secondary malignancies in primary cutaneous lymphomas. J Dtsch Dermatol Ges. 2021;19:373-81.	MF (n = 72)	8 (11)	Hematologic (n = 2)	Solid tumors (n = 5), melanoma (n = 1)	12.5
Błażewicz et al., 2021, Poland²²22 Błażewicz I, Olszewska B, Stawczyk-Macieja M, Jaśkiewicz M, Nowicki RJ, Sokołowska-Wojdyło M. The incidences of other primary cancers in patients with mycosis fungoides and Sézary syndrome. Postepy Dermatol Alergol. 2021;38:289-294.	MF & SS (n = 177)	29 (16.4)	Hematologic (n = 12)	Lung cancer (n = 4), breast cancer (n = 2), bladder cancer (n = 2), kidney cancer (n = 2), melanoma (n = 2), others (n = 5)	41.4
Pileri et al., 2021, Italy²³23 Pileri A, Guglielmo A, Fuligni F, Lastrucci I, Patrizi A, Pimpinelli N, et al. Second neoplasm in cutaneous T-cell lymphoma patients: a marker of worse prognosis? Ital J Dermatol Venerol. 2021;156:484-488.	MF (n = NA)	13 (NA)	Lung cancer (n = 4)	Prostate cancer (n = 2), pancreatic cancer (n = 2), others (n = 5)	7.7
Present study, 2023, Turkey	MF (n = 730)	56 (7.1)	Hematologic (n = 36)	Breast cancer (n = 4), prostate cancer (n = 3), Kaposi’s sarcoma (n = 2), melanoma (n = 2), renal cell cancer (n = 2), thyroid cancer (n = 1), astrocytoma (n = 1), hepatocellular cancer (n = 1), endometrium cancer (n = 1), fibromyxoid sarcoma (n = 1), lung cancer (n = 1), gastric adenocarcinoma (n = 1)	64.3

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[1] * Corresponding author. E-mail:tugba.ertan@istanbul.edu.tr dr.tugbaertan@hotmail.com (T. Atci)

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Evaluation of secondary malignancies in a large series of mycosis fungoides☆ ☆ Study conducted at the Istanbul Medical Faculty, Istanbul University, Istanbul, Turkey.

Abstract

Background

Objective

Methods

Results

Study limitations

Conclusion

Evaluation of secondary malignancies in a large series of mycosis fungoides^☆ ☆ Study conducted at the Istanbul Medical Faculty, Istanbul University, Istanbul, Turkey.