A Review of Survival in Mycosis Fungoides
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1 A Review of Survival in Mycosis Fungoides Robin T. Vollmer, MD From the VA and Duke University Medical Centers, Durham, NC. Key Words: Mycosis fungoides; Survival; Hazard function; Cutaneous T-cell lymphoma Am J Clin Pathol May 2014;141: DOI: /AJCPH2PHXFCX3BOX ABSTRACT Objectives: The objectives of this study are to review prior publications of survival for patients with mycosis fungoides (MF), to perform some analyses on the consolidated data, and then to consider the implications of the results. Methods: The data for this study comprise 18 survival curves derived from seven prior publications of long-term survival in relatively large series of patients with MF. Altogether, the study uses results from over 5,000 patients. To examine fatality, the study uses hazard functions derived from the survival curves. Results: The analyses demonstrate significant variability in survival between different groups who have studied MF, and the results document that for most patients the diagnosis of MF has little impact on fatality. Conclusions: Although MF is considered a cutaneous lymphoma, that is, a malignancy, it may be time to reconsider low stages of MF as precursors to malignancy analogous to the precursors to malignancies of other types or organs. Mycosis fungoides (MF) is the most common primary lymphoma of the skin. Yet, MF is not common, and its histologic definition remains both elusive and controversial. 1-5 Many investigators have thoroughly studied the histologic features of MF, 3-16 finally achieving a consensus of sorts that emphasizes the importance of the following: MF cells cytology (modestly enlarged lymphocytes with dark convoluted nuclei and, for the most part, a high nuclear-to-cytoplasmic ratio), the presence of these cells in the epidermis (in basilar epidermal rows, scattered singly, or in Pautrier clusters), the clear halos that often surround these cells, their presence in the papillary dermis (where they are often appear interstitially among collagen fibers), and the limited changes typical for spongiotic or other dermatoses. 1,3-5,15,17-20 Despite this consensus, benign nonlymphomatous mimics of MF confound the diagnosis Controversy and uncertainty also mark outcomes of MF. For example, most patients with MF live for decades after the diagnosis and die of other causes, so deciding when they have died of complications of MF is not straightforward. In this setting, many investigators have studied and reported the most objective outcome of overall survival Herein I review prior reports of survival in MF, reanalyze the data, and then examine the implications of the results. Materials and Methods The data for this study comprise 18 survival curves derived from seven prior publications of survival in patients with MF The years of publication spanned from 1988 through If a single institution published several 706 Am J Clin Pathol 2014;141: DOI: /AJCPH2PHXFCX3BOX
2 times, then data from just the latest publication were used. The midpoints of the year of diagnosis ranged from 1978 through 1996 (mean, 1986), and follow-up times ranged from 6.7 to 38 years (median, 20 years). Data from curves with fewer than 40 patients were not used, and there were no additional exclusion criteria. Altogether, the survival curves involved a total of 5,953 patients. Seventeen of the survival curves gave overall survival, and one provided relative survival, defined as the ratio of overall survival to the expected survival for matched patients from the population free of MF. 29 Each survival curve was digitized to yield a list of survival probabilities at times from zero to the time of last follow-up, and the total number of such points was 328. Table 1 summarizes the studies and data used For ease of interpolation, further analysis, and plotting, hazard functions for these curves were derived as before. 30,31 Specifically, if the survival probability at any time t is symbolized as S(t), then the hazard function h relates to S(t) through the following equation: Equation 1 S(t) = exp( t 0 h dx) Because some of the results are given for specific T stages of MF, their definitions are summarized in Table Results Fit of Derived Hazard Functions to Observed Survival Curves Because most of the results rely on hazard functions derived from the survival curves and Equation 1, the first result shows how well these hazard functions provided survival probabilities that fit the original data. Figure 1 is a plot of the observed values of S(t) on the x-axis vs values of S(t) derived from the hazard functions and Equation 1 on the y-axis. The line shows where perfect fits should occur, and the fact that the points are consistently close to the line implies that the derived hazard functions accurately reflect the observed survival probabilities. Altogether, the mean difference between observed and fitted survival probabilities was (units of probability), with a median difference of 0 and a range of.04 to.05. for MF Figure 2 shows three survival plots for a total of 2,305 patients with MF of all stages and according to the three institutions that reported them: the Dutch group (Dutch Cutaneous Lymphoma Working Group registry), 23 the UK group (ICA- RIS cutaneous lymphoma database in London, England), 27 and the University group. 25 The Dutch group did not contain cases of Sézary syndrome (SS), whereas 12% and 7%, respectively, of the UK and group patients had SS, so the better survival of the Dutch patients could in part Table 1 Study Data Used a Institution Year T Stage No. of Patients NCI 1988 T2 61 NCI 1988 T4 42 Dutch 1997 All T T T T T T T T All 525 SEER 2011 All 1,815 UK 2012 All 1,502 MDA 2012 T1 522 MDA 2012 T2 395 MDA 2012 T3 136 MDA 2012 T4 188 Dutch, Dutch Cutaneous Lymphoma Working Group registry 23 ; MDA, MD Anderson medical center 27 ; NCI, National Cancer Institute 22 ; SEER, Surveillance, Epidemiology, and End Results program 28 ;, University 25 ;, University of California, San Francisco 24 ; UK, group of investigators associated with the ICARIS cutaneous lymphoma database in London, England. 26 a The listed year is the year of publication. Table 2 T Stages of Mycosis Fungoides a Stage T1 T2 T3 T4 Description Limited patches, papules, and/or plaques covering less than 10% of the skin surface Patches, papules, or plaques covering 10% or more of the skin surface One or more tumors 1 cm or larger in diameter Confluence of erythema covering 80% or more of the skin surface a From American Joint Committee on Cancer. 32 Calculated Survival Probability Observed Survival Probability Figure 1 A plot of observed values of S(t) on the x-axis vs values of S(t) derived from the hazard functions and Equation 1 on the y-axis. The line shows where perfect fits should occur. Am J Clin Pathol 2014;141: DOI: /AJCPH2PHXFCX3BOX 707
3 Vollmer / Survival in Mycosis Fungoides and MDA Dutch UK Figure 2 Overall survival plots for mycosis fungoides reported in three studies from the Dutch group, 23 the University group, 25 and the UK group. 27 In total, the number of patients used for these curves comprised 2,305. be due to the lack of patients with SS. Nevertheless, 10-year survival for the UK and groups was 63% and 53%, respectively, a difference that was significant by the equality of proportions test (P =.0001, c 2 = 16) but a difference not intuitively related to the percentage of patients with SS since the UK data included more, not fewer, patients with SS. for Stage T1 MF Figure 3 shows survival plots for a total of 855 patients with stage T1 MF according to the three institutions that reported them: the University of California, San Francisco () group 24 ; the University group 25 ; and the MD Anderson (MDA) group. 27 The 10-year survival among the three groups was the same at approximately 86% (P > 0.3, c 2 test). for Stage T2 MF Figure 4 shows survival plots for a total of 847 patients with stage T2 MF according to the four institutions that reported them: National Cancer Institute (NCI), 22 the group, 24 the University group, 25 and the MDA group. 27 Survival at 10 years was significantly different for the patients from these four groups (P ~ 0, c 2 test) and ranged from approximately 55% to 77% (weighted mean, 67%). for Stage T3 MF Figure 5 shows survival plots for a total of 279 patients with stage T3 MF according to the three institutions that reported them: the group, 24 the University group, 25 and the MDA group. 27 Survival at 10 years was significantly different for the patients from these three groups (P =.01, c 2 test) and ranged from approximately 28% to 42% (weighted mean, 34%). Figure 3 Overall survival plots for a total of 855 patients with stage T1 mycosis fungoides according to the three institutions that reported them: the University of California, San Francisco () group 24 ; the University group 25 ; and the MD Anderson (MDA) group. 27 for Stage T4 MF Figure 6 shows survival plots for a total of 377 patients with stage T4 MF according to the four institutions that reported them: the NCI, 22 the group, 24 the University group, 25 and the MDA group. 27 Survival at 10 years was significantly different between these groups (P =.0018, c 2 test) and ranged from approximately 0.1% to 29%. Because the NCI had both the lowest survival and the lowest number of patients (n = 42), its data may represent an outlier. Furthermore, there was no significant difference MDA NCI Figure 4 Overall survival plots for a total of 847 patients with stage T2 mycosis fungoides according to the four institutions that reported them: National Cancer Institute (NCI) 22 ; the University of California, San Francisco () group 24 ; the University group 25 ; and the MD Anderson (MDA) group Am J Clin Pathol 2014;141: DOI: /AJCPH2PHXFCX3BOX
4 MDA MDA Figure 5 Overall survival plots for a total of 279 patients with stage T3 mycosis fungoides according to the three institutions that reported them: the University of California, San Francisco () group 24 ; the University group 25 ; and the MD Anderson (MDA) group. 27 between the 10-year survival probabilities for patients in the remaining three groups with T4 stage (P >.7, c 2 test). The weighted 10-year survival for these last three groups was 27%. Consolidated values of overall survival at 10 years by T stage are summarized in Table 3. Relative Survival for MF in the Surveillance, Epidemiology, and End Results Database Unlike the above sets of data, the Surveillance, Epidemiology, and End Results (SEER) data provide relative survival probabilities, that is, overall survival probability divided by the expected survival probability for a matched group from the MF-free population. 29 Figure 7 shows the survival curve derived from the SEER survival data on 1,815 patients with MF of all stages, and Figure 8 shows the corresponding hazard function. The hazard function begins at 0, rises to a peak during the first 2 years after diagnosis, and then gradually declines to near 0 by 10 years. The fall in hazard at 10 years corresponds to a leveling of the survival curve after 10 years. Both curves indicate that after 10 years, the risk of death nearly equals that of the general population. In addition, the results suggest that approximately 19% of patients have a fatal form of MF and approximately 81% do not. Because academic centers have found that 15% of patients have the T4 stage and 28% have either the T3 or T4 stage, these results suggest that most with fatal MF have tumor stages higher than T1 or T2. Finally, the rise and fall in the hazard function implies that the timing of deaths in the few with fatal MF is skewed. For example, more than 50% of the observed deaths occur in the first 4 years after diagnosis, and an additional 40% occur over the next 6 years. NCI Figure 6 Overall survival plots for a total of 377 patients with stage T4 mycosis fungoides according to the four institutions that reported them: National Cancer Institute (NCI) 22 ; the University of California, San Francisco () group 24 ; the University group 25 ; and the MD Anderson (MDA) group. 27 Table 3 Consolidated Values for 10-Year by T Stage a T Stage Survival, % No. of Patients T T T T4 b a The reported survival probability was calculated as a weighted mean, that is, a mean across the studies with results weighted by the number of patients in each of the studies. b For patients with T4 stage mycosis fungoides, the National Cancer Institute (NCI) data were not included because of the small number of cases and because the low survival for NCI data appeared to be an outlier. Relative Survival Figure 7 A plot of relative survival probabilities vs time from diagnosis for 1,815 patients in the Surveillance, Epidemiology, and End Results data. Am J Clin Pathol 2014;141: DOI: /AJCPH2PHXFCX3BOX 709
5 Vollmer / Survival in Mycosis Fungoides Relative Hazard Discussion Figure 8 The derived hazard function for relative survival of 1,815 patients in the Surveillance, Epidemiology, and End Results data set. The hazard function begins at 0, rises to a peak during the first 2 years after diagnosis, and then falls to near 0 by 10 years. The variability found in the survival curves of Figures 2 to 6 and across several T stages for MF is likely due to uncontrolled factors, including referral patterns for the academic institutions involved as well as differences in prognostic factors such as patient age, patient sex, status of N and B stages, and status of patch vs plaque morphology in the primary lesions. Variability in the histopathologic diagnosis of MF must have added to these, because disagreements between pathologists about the diagnosis of MF are well documented. 3,7,8,14,33,34 How to improve diagnostic agreement is not, however, clear. The International Society for Cutaneous Lymphomas has proposed an algorithm that combines clinical, histologic, molecular, and immunohistochemical (IHC) components. 15 Yet, some have not found it helpful and even discovered that IHC stains offered limited help. 2-5 For example, McCalmont recently wrote that one cannot immunostain one s way to a diagnosis of mycosis fungoides. 35 Despite these issues, the collected data illustrated in Figures 2 to 6 and in Table 2 emphasize how overall survival relates closely to T stage, how patients with stage T1 do well, and how most of those with shortened survival have higher T stages. Thus, if we see a skin biopsy specimen with histologic features of early MF, perhaps we should, as LeBoit 2 suggests, question how much effort to put into diagnosing early MF and instead pursue further dialogue with dermatologists about the differential diagnosis as well as additional biopsies of persistent or plaque-like lesions. The survival results for patients in the SEER database are provocative for several reasons. The data comprise the largest number of patients and were collected over a relatively long and current period from 1988 through Because the SEER results use relative survival, the survival end point is most likely related to MF. Unlike the other data reported here, the SEER data reflect community practices broader than the academic centers for the other data. Regardless, the SEER survival data on MF suggest that most patients do not have a fatal disease. In summary, MF is classified as a lymphoma that is, as a cancer yet the survival results of more than 5,000 patients summarized here demonstrate that most with MF do not have a fatal disease. Perhaps a better way to think of early stages of MF is as precursors to, or markers of, cancer rather than cancer itself. In this regard, early MF may be similar to other precursors and markers such as dysplastic nevus, melanoma in situ, actinic keratoses, Bowen disease, dysplasias of the cervix, adenomas of the colon with high-grade dysplasia, and high-grade intraepithelial neoplasia of the prostate. For the most part, we embrace these diagnoses while recognizing that their pathologies do not imply a fatal form of cancer. Perhaps we should view early MF the same way. Address reprint requests to Dr Vollmer: Laboratory Medicine 113, VA Medical Center, 508 Fulton St, Durham, NC 27705; Robin. Vollmer@med.va.gov. References 1. Glusac EJ. Of cells and architecture: new approaches to old criteria in mycosis fungoides. J Cutan Pathol. 2001;28: LeBoit PE. Simulators of cutaneous lymphoma: where should our efforts go? Am J Clin Pathol. 2013;139: Florell SR, Cessna M, Lundell RB, et al. Usefulness (or lack thereof) of immunophenotyping in atypical cutaneous T-cell infiltrates. Am J Clin Pathol. 2006;125: Ferrara G, Di Blasi A, Zalaudek I, et al. Regarding the algorithm for the diagnosis of early mycosis fungoides proposed by the International Society for Cutaneous Lymphomas: suggestions from a routine histopathology practice. J Cutan Pathol. 2007;35: Furmanczyk PS, Wolgamot GM, Kussick SJ, et al. Diagnosis of mycosis fungoides with different algorithmic approaches. J Cutan Pathol. 2010;37: Sanchez JL, Ackerman AB. The patch stage of mycosis fungoides. Am J Dermatopathol. 1979;1: Lefeber WP, Robinson JK, Clendenning WE, et al. Attempts to enhance light microscopic diagnosis of cutaneous T-cell lymphoma (mycosis fungoides). Arch Dermatol. 1981;117: Nickoloff BJ. Light-microscopic assessment of 100 patients with patch/plaque-stage mycosis fungoides. Am J Dermatopathol. 1988;10: King-Ismael D, Ackerman AB. Guttate parapsoriasis/digitate dermatosis (small plaque parapsoriasis) is mycosis fungoides. Am J Dermatopathol. 1992;14: Shapiro PE, Pinto FJ. The histologic spectrum of mycosis fungoides/sézary syndrome (cutaneous T-cell lymphoma). Am J Surg Pathol. 1994;18: Am J Clin Pathol 2014;141: DOI: /AJCPH2PHXFCX3BOX
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