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. 2023 Sep 13;159(11):1248–1252. doi: 10.1001/jamadermatol.2023.2849

Risk of Multiple Primary Cancers in Patients With Merkel Cell Carcinoma

A SEER-Based Analysis

Edward Eid 1, Nolan J Maloney 2, Zhuo Ran Cai 1, Lisa C Zaba 2, Nour Kibbi 2, Esther M John 3,4,5, Eleni Linos 2,3,5,
PMCID: PMC10500424  PMID: 37703005

This cohort study examines whether patients with cutaneous Merkel cell carcinoma are at increased risk of developing subsequent other cancers.

Key Points

Question

Are patients with cutaneous Merkel cell carcinoma (MCC) at increased risk of developing other cancers?

Findings

In this cohort study of 6146 patients diagnosed with a first primary cutaneous MCC in the US between 2000 and 2018, there was an increased risk of developing subsequent primary cancers, including solid tumors such as papillary thyroid carcinoma and melanoma and hematologic cancers such as non-Hodgkin lymphoma.

Meaning

Findings of this study suggest that patients with MCC have an increased risk of developing subsequent cancers, and further studies exploring possible common etiological factors shared between MCC and other primary cancers are warranted.

Abstract

Importance

The risk of subsequent primary cancers after a diagnosis of cutaneous Merkel cell carcinoma (MCC) is not well established.

Objective

To evaluate the risk of subsequent primary cancers after the diagnosis of a first primary cutaneous MCC.

Design, Setting, and Participants

This cohort study analyzed data from 17 registries of the Surveillance, Epidemiology, and End Results (SEER) Program from January 1, 2000, to December 31, 2019. In all, 6146 patients diagnosed with a first primary cutaneous MCC were identified.

Main Outcomes and Measures

The primary outcome was the relative and absolute risks of subsequent primary cancers after the diagnosis of a first primary MCC, which were calculated using the standardized incidence ratio (SIR; ratio of observed to expected cases of subsequent cancer) and the excess risk (difference between observed and expected cases of subsequent cancer divided by the person-years at risk), respectively. Data were analyzed between January 1, 2000, and December 31, 2019.

Results

Of 6146 patients with a first primary MCC diagnosed at a median (IQR) age of 76 (66-83) years, 3713 (60.4%) were men, and the predominant race and ethnicity was non-Hispanic White (5491 individuals [89.3%]). Of these patients, 725 (11.8%) developed subsequent primary cancers, with an SIR of 1.28 (95% CI, 1.19-1.38) and excess risk of 57.25 per 10 000 person-years. For solid tumors after MCC, risk was elevated for cutaneous melanoma (SIR, 2.36 [95% CI, 1.85-2.97]; excess risk, 15.27 per 10 000 person-years) and papillary thyroid carcinoma (SIR, 5.26 [95% CI, 3.25-8.04]; excess risk, 6.16 per 10 000 person-years). For hematologic cancers after MCC, risk was increased for non-Hodgkin lymphoma (SIR, 2.62 [95% CI, 2.04-3.32]; excess risk, 15.48 per 10 000 person-years).

Conclusions and Relevance

This cohort study found that patients with MCC had an increased risk of subsequently developing solid and hematologic cancers. This increased risk may be associated with increased surveillance, treatment-related factors, or shared etiologies of the other cancers with MCC. Further studies exploring possible common etiological factors shared between MCC and other primary cancers are warranted.

Introduction

Merkel cell carcinoma (MCC) is believed to develop either from oncogenic sequence variations from Merkel cell polyomavirus (MCPyV) infection or from UV radiation (UVR)–mediated DNA damage.1 Merkel cell carcinoma is highly immunogenic, as evidenced by the high response rate to immune checkpoint inhibitors.2 While the incidence of most solid organ tumors peaks in the 7th decade of life, MCC incidence continues to rise exponentially with increasing age, suggesting that immunosenescence may play a role in MCC etiology.3 A better understanding of the development of subsequent primary cancers in patients with MCC may provide additional insights on the causes of this highly aggressive neuroendocrine tumor. The survival of patients with MCC has increased in recent years largely due to the advent of immunotherapy.2 Therefore, understanding the risk of subsequent primary tumors is important to inform screening and treatment recommendations for patients with MCC.

Prior studies have shown a higher risk of subsequent cancers, particularly cutaneous melanoma and keratinocyte carcinomas, after a diagnosis of MCC.4,5 In addition, the risk of MCC is increased after a first primary diagnosis of melanoma, chronic lymphocytic leukemia (CLL), or non-Hodgkin lymphoma.4,6,7 However, studies to date have had small sample sizes and conflicting results,4,6,7,8,9 and the latest Surveillance, Epidemiology, and End Results (SEER) analysis included MCC cases diagnosed from 1986 to 2002.6 We estimated site-specific risk of multiple subsequent primary cancers among patients with a first primary cutaneous MCC diagnosed from 2000 to 2018.

Methods

In accordance with the Common Rule, this cohort study was exempt from institutional board review and informed consent because publicly available deidentified data were used. Primary MCC cases diagnosed from January 1, 2000, to December 31, 2018, were identified in the SEER Program, which comprises 17 cancer registries. The Multiple Primary–Standardized Incidence Ratio session was used to identify patients with a first primary MCC and subsequent primary neoplasms. Subsequent primary cancer risk was measured by accumulation of person-years at risk (PYR) from the first primary diagnosis of MCC to death, loss to follow-up, or December 31, 2019, whichever occurred first. Primary cancers arising within 2 months of an initial diagnosis of MCC were considered synchronous tumors and were excluded. Second primary MCCs were also excluded to minimize bias due to potential recurrence misclassification. Keratinocyte carcinomas were also excluded as subsequent cancers.

The expected numbers of specific subsequent cancers were calculated by applying sex, age, race and ethnicity (including Hispanic individuals of any race and non-Hispanic American Indian or Alaska Native, non-Hispanic Asian or Pacific Islander, non-Hispanic Black, and non-Hispanic White individuals), and calendar year–adjusted SEER incidence rates of matching primary cancers to the accumulated person-years of observation. Data on race and ethnicity were examined for multiple reasons. Different racial and ethnic groups may have varying rates of subsequent primary cancers. Understanding these differences is essential for targeting interventions and for identifying potential genetic or environmental risk factors unique to specific groups. Moreover, examining data on race and ethnicity can help shed light on disparities in access to health care, which can impact cancer outcomes, including the risk of developing subsequent cancers. Identifying these disparities can guide policy decisions and interventions to address these inequities. The standardized incidence ratio (SIR), an estimate of relative risk, was calculated by dividing the observed number of subsequent cancers at each site (O) by the expected number of cancers (E). The excess risk, an estimate of absolute risk, was calculated per 10 000 person-years as ([O − E] / PYR) × 10 000, and represents the additional number of cancers expected per 10 000 person-years. In the secondary analysis, these calculations were also carried out for first primary cancers of any type or site to determine cancers associated with an increased risk of subsequent primary MCC. Data were analyzed between January 1, 2000, and December 31, 2019 using SEER*Stat, version 8.4.0 (National Cancer Institute). Two-sided P < .05 was considered statistically significant.

Results

The study included 6146 patients (median [IQR] age at diagnosis, 76 [66-83] years; 2433 females (39.6%) and 3713 males (60.4%) with a first primary MCC; 381 patients [6.2%] were Hispanic of any race; 163 [2.7%] were non-Hispanic Asian or Pacific Islander, 22 (0.4%) were non-Hispanic American Indian or Alaska Native, 89 patients (1.4%) were non-Hispanic Black, and 5491 (89.3%) were non-Hispanic White individuals) (Table 1). Of these patients, 725 (11.8%) developed a subsequent primary cancer by a mean follow-up of 4.49 years). The risk of developing a subsequent primary cancer after a first primary MCC was elevated (SIR, 1.28 [95% CI, 1.19-1.38]; excess risk, 57.25 per 10 000 person-years).

Table 1. Characteristics of Patients Diagnosed With a First Primary Cutaneous Merkel Cell Carcinoma (MCC) and Associated Standardized Incidence Ratios (SIRs) Stratified According to Demographic and Clinical Characteristics in the 17 SEER Registries From 2000 to 2018.

Characteristic MCC, No. (%) Subsequent primary cancer, No. SIR (95% CI)a
All patients 6146 725 1.28 (1.19-1.38) d
Sex
Female 2433 (39.6) 230 1.17 (1.02-1.33)d
Male 3713 (60.4) 495 1.34 (1.22-1.46)d
Age, y
<60 792 (12.9) 78 1.44 (1.14-1.80)d
60-74 2090 (34.0) 298 1.25 (1.11-1.40)d
≥75 3264 (53.1) 349 1.27 (1.14-1.41)d
Race and ethnicity
Hispanic (all races) 381 (6.2) 34 1.00 (0.69-1.40)
Non-Hispanic American Indian or Alaska Native 22 (0.4) 0 NA
Non-Hispanic Asian or Pacific Islander 163 (2.7) 14 1.26 (0.69-2.12)
Non-Hispanic Black 89 (1.4) 8 1.47 (0.63-2.89)
Non-Hispanic White 5491 (89.3) 669 1.30 (1.20-1.40)d
Year of diagnosis
2000-2009 2814 (45.8) 423 1.19 (1.08-1.31)d
2010-2018 3332 (54.2) 302 1.43 (1.27-1.60)d
Anatomic site
Head and neck 2595 (42.2) 307 1.30 (1.16-1.45)d
Trunk and limbs 3033 (49.3) 364 1.26 (1.13-1.39)d
Unknownb 518 (8.4) 54 1.34 (1.01-1.75)d
Surgical therapy
Surgery 5085 (82.7) 638 1.29 (1.19-1.39)d
Local destructive treatmentc 8 (0.1) 2 2.11 (0.26-7.61)
No surgery 1027 (16.7) 81 1.19 (0.95-1.48)
Unknown 26 (0.4) 4 1.88 (0.51-4.81)
Radiotherapy
Yes 3001 (48.8) 360 1.24 (1.12-1.38)d
None or unknown 3145 (51.2) 365 1.31 (1.18-1.46)d
Chemotherapy
Yes 788 (12.8) 96 1.51 (1.22-1.85)d
None or unknown 5358 (87.2) 629 1.25 (1.15-1.35)d
Duration of follow-up, y
<1 6146 (100) 154 1.59 (1.35-1.86)d
1 to <5 5064 (82.4) 341 1.28 (1.15-1.42)d
5 to <10 2117 (34.4) 171 1.19 (1.02-1.39)d
≥10 852 (13.9) 59 0.98 (0.75-1.27)

Abbreviations: NA, not applicable; SEER, Surveillance, Epidemiology, and End Results Program.

a

SIR indicates the ratio of the observed number to the expected number of subsequent primary cancer cases.

b

Includes unspecified overlapping sites of skin (International Statistical Classification of Diseases, Tenth Revision, Clinical Modification [ICD-10-CM] code C44.8) and skin, not otherwise specified (ICD-10-CM code C44.9).

c

Includes electrocautery, fulguration, and laser and local tumor destruction, not otherwise specified.

d

SEER*STAT does not provide exact P values but only indicates whether a value is significant P < .05.

Table 2 lists the types of cancers with significantly increased risk after MCC (eTable 1 in Supplement 1 lists the risk for all subsequent cancers). Risk of all solid tumors was elevated after MCC, including liver (SIR, 1.92 [95% CI, 1.09-3.11]; excess risk, 2.77 per 10 000 person-years), pancreas (SIR, 1.65 [95% CI, 1.13-2.32]; excess risk, 4.55 per 10 000 person-years), cutaneous melanoma (SIR, 2.36 [95% CI, 1.85-2.97]; excess risk, 15.27 per 10 000 person-years), and kidney (SIR, 1.64 [95% CI, 1.08-2.39]; excess risk, 3.83 per 10 000 person-years). Risk of papillary thyroid carcinoma (PTC) was also elevated (SIR, 5.26 [95% CI, 3.25-8.04]; excess risk, 6.16 per 10 000 person-years). Risk of hematological cancers after MCC was elevated, including non-Hodgkin lymphoma (SIR, 2.62 [95% CI, 2.04-3.32]; excess risk, 15.48 per 10 000 person-years) and myelodysplastic syndrome (SIR, 2.17 [95% CI, 1.18-3.64]; excess risk, 2.73 per 10 000 person-years). Stratification by follow-up intervals of 1, 5, and 10 years revealed a significant increase in risk of subsequent tumors as well as melanoma and non-Hodgkin lymphoma for up to 10 years and an increase in risk of PTC and kidney cancers for up to 5 years after a first primary diagnosis of MCC (eTable 2 in Supplement 1).

Table 2. Select Subsequent Primary Cancers With Increased Risk After First Primary Merkel Cell Carcinoma Diagnosis in the 17 SEER Registries From 2000 to 2018a.

Subsequent primary cancer Cases of subsequent primary cancer, No. SIR (95% CI)b Excess risk per 10 000 person-years
Observed Expected
All sites 725 567.06 1.28 (1.19-1.38) 57.25
All sites excluding keratinocyte carcinoma 721 564.89 1.28 (1.18-1.37) 56.58
All solid tumors 569 479.55 1.19 (1.09-1.29) 32.42
Oral cavity and pharynxc 27 13.05 2.07 (1.36-3.01) 5.06
Salivary gland 9 1.86 4.83 (2.21-9.16) 2.59
Floor of mouth, gum, and other mouth 7 2.73 2.57 (1.03-5.29) 1.55
Liver 16 8.35 1.92 (1.09-3.11) 2.77
Pancreas 32 19.44 1.65 (1.13-2.32) 4.55
Skin excluding keratinocyte carcinoma 77 33.04 2.33 (1.84-2.91) 15.93
Melanoma 73 30.88 2.36 (1.85-2.97) 15.27
Kidney and renal pelvis 31 18.14 1.71 (1.16-2.43) 4.66
Kidney 27 16.42 1.64 (1.08-2.39) 3.83
Endocrine systemd 23 5.57 4.13 (2.62-6.20) 6.32
Thyroid 23 5.11 4.50 (2.85-6.75) 6.48
Papillary thyroid carcinoma 21 3.99 5.26 (3.25-8.04) 6.16
All lymphatic and hematopoietic cancerse 121 61.91 1.95 (1.62-2.34) 21.42
Myelodysplastic syndrome 14 6.46 2.17 (1.18-3.64) 2.73
Lymphomaf 70 27.38 2.56 (1.99-3.23) 15.45
NHL 69 26.29 2.62 (2.04-3.32) 15.48
NHL, nodal 49 17.51 2.80 (2.07-3.70) 11.41
NHL, extranodal 20 8.78 2.28 (1.39-3.52) 4.07
Leukemiag 31 18.99 1.63 (1.11-2.32) 4.35
Nonlymphocytic leukemiah 18 9.66 1.86 (1.10-2.95) 3.02

Abbreviations: NHL, non-Hodgkin lymphoma; SEER, Surveillance, Epidemiology, and End Results Program; SIR, standardized incidence ratio.

a

Only cancers with a significantly elevated risk (P < .05) after Merkel cell carcinoma are presented in the table.

b

SIR indicates the ratio of the observed number to the expected number of subsequent primary cancer cases.

c

Includes tumors of the lip, tongue, tonsil, and other oral cavity and pharynx (other tumors were not defined).

d

Includes tumors of the thymus and adrenal gland as well as other endocrine tumors (other tumors were not defined).

e

Includes lymphomas, leukemias, myelodysplastic syndrome, and myeloma.

f

Includes Hodgkin lymphomas and NHLs.

g

Includes lymphocytic leukemias.

h

Includes acute nonlymphocytic leukemia and myeloid and monocytic leukemias.

Table 3 describes the risk of MCC after other first primary cancers (eTable 3 in Supplement 1 describes the risk for all primary cancers). Risk of MCC was increased after any primary cancer (SIR 1.43 [95% CI, 1.36-1.51]; excess risk, 0.13 per 10 000 person-years) and particularly after a first primary diagnosis of CLL (SIR, 6.51 [95% CI, 5.32-7.9]; excess risk, 2.35 per 10 000 person-years), chronic myeloid leukemia (SIR, 4.25 [95% CI, 2.04-7.82]; excess risk, 0.65 per 10 000 person-years), and lip cancer (SIR, 4.12 [95% CI, 2.13-7.2]; excess risk, 1.42 per 10 000 person-years).

Table 3. Risk of Subsequent Primary Merkel Cell Carcinoma (MCC) After Select First Primary Cancers in the 17 SEER Registries From 2000 to 2018a.

First primary cancer Cases of first primary cancer, No. Cases of subsequent MCC, No. SIR (95% CI)b Excess risk per 10 000 person-years
Observed Expected
All sites 5 441 134 1393 970.78 1.43 (1.36-1.51) 0.13
All sites excluding keratinocyte carcinoma 5 426 328 1378 967.22 1.42 (1.35-1.50) 0.13
All solid tumors 4 791 358 1090 875.31 1.25 (1.17-1.32) 0.07
Oral cavity and pharynxc 135 738 42 18.90 2.22 (1.60-3.00) 0.31
Lip 8797 12 2.91 4.12 (2.13-7.20) 1.42
Tongue 40 166 15 5.45 2.75 (1.54-4.54) 0.45
Salivary gland 14 921 7 2.48 2.82 (1.13-5.81) 0.49
Ascending colon 64 543 25 15.22 1.64 (1.06-2.42) 0.27
Anus, anal canal, and anorectum 21 402 8 2.45 3.27 (1.41-6.44) 0.46
Respiratory systemd 612 317 66 48.75 1.35 (1.05-1.72) 0.11
Lung, bronchus, trachea, mediastinum, and other respiratory organs 563 666 55 39.98 1.38 (1.04-1.79) 0.12
Lung and bronchus 561 598 55 39.90 1.38 (1.04-1.79) 0.12
Skin excluding keratinocyte carcinoma 259 657 175 57.86 3.02 (2.59-3.51) 0.59
Melanoma 244 851 160 54.30 2.95 (2.51-3.44) 0.56
Other nonepithelial skin 14 806 15 3.57 4.20 (2.35-6.93) 1.02
Kidney and renal pelvis 176 610 51 29.12 1.75 (1.30-2.30) 0.21
Kidney 167 965 51 27.46 1.86 (1.38-2.44) 0.23
All lymphatic and hematopoietic diseasese 511 149 251 76.17 3.30 (2.90-3.73) 0.60
Lymphomaf 261 085 113 41.02 2.75 (2.27-3.31) 0.43
NHL 224 953 109 39.10 2.79 (2.29-3.36) 0.51
NHL, nodal 149 578 74 25.57 2.89 (2.27-3.63) 0.53
NHL, extranodal 75 375 35 13.53 2.59 (1.80-3.60) 0.45
Leukemia 147 569 123 21.41 5.74 (4.77-6.85) 1.23
Lymphocytic leukemiag 85 969 108 17.11 6.31 (5.18-7.62) 1.62
Chronic lymphocytic leukemia 58 274 103 15.82 6.51 (5.32-7.90) 2.35
Other lymphocytic leukemia 5023 5 1.08 4.65 (1.51-10.84) 1.05
Nonlymphocytic leukemiah 61 600 15 4.30 3.49 (1.95-5.75) 0.41
Myeloid and monocytic leukemiai 55 735 13 3.72 3.50 (1.86-5.98) 0.39
Chronic myeloid leukemia 20 812 10 2.35 4.25 (2.04-7.82) 0.65

Abbreviations: NHL, Non-Hodgkin lymphoma; SEER, Surveillance, Epidemiology, and End Results Program; SIR, standardized incidence ratio.

a

Only sites that had significantly elevated (P < .05) risk of subsequent Merkel cell carcinoma are presented in the table.

b

SIR indicates the ratio of the observed number to the expected number of subsequent primary cancer cases.

c

Includes tumors of the floor of mouth, gum and other mouth, tonsil, and other oral cavity and pharynx (other tumors were not defined).

d

Includes tumors of the nose, nasal cavity, middle ear, larynx, and pleura.

e

Includes myelodysplastic syndrome and myeloma.

f

Includes Hodgkin lymphomass.

g

Includes acute lymphocytic leukemia, chronic lymphocytic leukemia, and other lymphocytic leukemias (other lymphocytic leukemias were not defined).

h

Includes acute non-lymphocytic leukemia and myeloid and monocytic leukemias, and other leukemias (other leukemias were not defined).

i

Includes acute myeloid leukemia, acute monocytic leukemia, chronic myeloid leukemia, and other myeloid and monocytic leukemias (other myeloid and monocytic leukemias were not defined).

Discussion

In this study of more than 6000 patients with MCC, the risk of subsequent primary cancer after a first primary diagnosis of MCC was significantly elevated. This could be due to enhanced surveillance after diagnosis of MCC that resulted in increased detection rates, possible lead time bias, or a true biological association between MCC and these subsequent primary cancers.

To our knowledge, this is the largest study of subsequent primary cancers in patients with MCC and extends an earlier SEER analysis.6 We identified previously unreported increased risks of developing liver, pancreatic, thyroid, and kidney cancers after an MCC diagnosis. Merkel Cell Polyomavirus DNA has been detected in liver, thyroid, and renal cancer tissue samples, and MCPyV large T-antigen (LT) DNA and RNA have even been detected in PTC biopsy samples; however, conclusions about MCPyV oncogenicity in any of these cancers could not be established because the protein expression of the LT antigen was not tested.10,11

The present study confirmed the known increased risk of melanoma among patients with MCC, which may be associated with the fact that UVR-mediated etiology accounts for most MCPyV-negative MCCs. Like MCC, melanoma contains a high number of UVR-signature sequence variations.12 Notably, the risk of PTC is also elevated in patients with melanoma.13 While the present study confirmed prior reports that CLL was a risk factor for the development of MCC, the opposite was not true, underscoring the importance of a competent immune system for MCC surveillance. The LT antigen is also reportedly expressed in some CLL tumors.14

Limitations

Study limitations include the potential for surveillance bias, as many patients with MCC undergo regular screening with computed tomography or positron emission tomography, which may also identify other cancers. In addition, some patients with MCC have immunosuppresion either due to solid organ transplant or hematological cancer, which is an independent risk factor for developing a subsequent cancer and may have affected the results. Additionally, small sample sizes may limit power for some rarer subsequent cancers.

Conclusions

In this cohort study, we found that patients with MCC had an increased risk of developing multiple types of solid and hematologic cancers. This increased risk may be due to increased surveillance, treatment-related factors, or shared etiologies with MCC. This study strengthens previously reported associations with MCC and the subsequent development of other cancers, and it sheds light on potentially novel associations that could contribute to a better understanding of the etiology of this aggressive tumor.

Supplement 1.

eTable 1. Risk of Subsequent Primary Cancers After a First Primary Diagnosis of Merkel Cell Carcinoma in the 17 SEER Registries from 2000 to 2018

eTable 2. Risk of Selected Subsequent Primary Cancers After a First Primary Diagnosis of Merkel Cell Carcinoma in the 17 SEER Registries from 2000 to 2018, Stratified by Follow-up Interval

eTable 3. Risk of Subsequent Primary Merkel Cell Carcinoma After Other First Primary Cancers in the 17 SEER Registries from 2000 to 2018

Supplement 2.

Data Sharing Statement

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplement 1.

eTable 1. Risk of Subsequent Primary Cancers After a First Primary Diagnosis of Merkel Cell Carcinoma in the 17 SEER Registries from 2000 to 2018

eTable 2. Risk of Selected Subsequent Primary Cancers After a First Primary Diagnosis of Merkel Cell Carcinoma in the 17 SEER Registries from 2000 to 2018, Stratified by Follow-up Interval

eTable 3. Risk of Subsequent Primary Merkel Cell Carcinoma After Other First Primary Cancers in the 17 SEER Registries from 2000 to 2018

Supplement 2.

Data Sharing Statement


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