Prevalence, Incidence, and Risk of Cancer in Patients With Psoriasis and Psoriatic Arthritis: A Systematic Review and Meta-analysis

Sofie Vaengebjerg; Lone Skov; Alexander Egeberg; Nikolai Dyrberg Loft

doi:10.1001/jamadermatol.2020.0024

. 2020 Feb 19;156(4):421–429. doi: 10.1001/jamadermatol.2020.0024

Prevalence, Incidence, and Risk of Cancer in Patients With Psoriasis and Psoriatic Arthritis

A Systematic Review and Meta-analysis

Sofie Vaengebjerg ^1,^✉, Lone Skov ¹, Alexander Egeberg ¹, Nikolai Dyrberg Loft ¹

¹Department of Dermatology and Allergy, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark

Accepted for Publication: January 3, 2020.

^✉

Corresponding Author: Sofie Vaengebjerg, MD, Department of Dermatology and Allergy, Herlev and Gentofte Hospital, University of Copenhagen, Gentofte Hospitalsvej 1, 2900 Hellerup, Denmark (sofie@vaengebjerg.dk).

Published Online: February 19, 2020. doi:10.1001/jamadermatol.2020.0024

Author Contributions: Dr Vaengebjerg had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Skov, Egeberg, Loft.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Vaengebjerg, Loft.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Egeberg.

Administrative, technical, or material support: All authors.

Supervision: Skov, Egeberg, Loft.

Conflict of Interest Disclosures: Dr Egeberg reported receiving grants, personal fees, and nonfinancial support from Eli Lilly, AbbVie, and Almirall; grants and personal fees from Pfizer and Janssen; personal fees from Novartis; and personal fees from Bristol-Myers Squibb, Samsung Bioepis, and UCB outside the submitted work. Dr Skov reported receiving personal fees from AbbVie, Janssen Cilag, Novartis, Eli Lilly, LEO Pharma, UCB, Almirall, and Sanofi; and has received grants from Pfizer, AbbVie, Novartis, Sanofi, Janssen Cilag, and LEO Pharma outside the submitted work; was a paid speaker for AbbVie, Eli Lilly, Novartis, and LEO Pharma; has been a paid consultant or has served on advisory boards of AbbVie, Janssen Cilag, Novartis, Eli Lilly, LEO Pharma, UCB, Almirall, and Sanofi; has served as an investigator for AbbVie, Janssen Cilag, Boehringer Ingelheim, AstraZeneca, Eli Lilly, Novartis, Regeneron, and LEO Pharma; and has received research and educational grants from Pfizer, AbbVie, Novartis, Sanofi, Janssen Cilag, and LEO Pharma. Dr Loft reported receiving personal fees from Eli Lilly outside the submitted work. No other disclosures were reported.

^✉

Corresponding author.

PMCID: PMC7042857 PMID: 32074260

Key Points

Question

Is psoriasis or psoriatic arthritis associated with an increased risk of cancer?

Findings

In a systematic review and meta-analysis of 112 studies including more than 2 million patients, the risk of cancer overall was slightly increased in patients with psoriasis, particularly the risks of keratinocyte cancer and lymphomas. No increase in cancer was seen among patients with psoriasis treated with biologic agents, and psoriatic arthritis was not associated with an increased risk of cancer.

Meaning

Patients with psoriasis appear to have a slightly increased risk of developing cancers.

Abstract

Importance

The association between psoriasis and risk of cancer remains debatable.

Objective

To evaluate the association and risk of cancer in patients with psoriasis or psoriatic arthritis, including risk of specific cancer subtypes.

Data Sources

Two databases (PubMed and Embase) were screened from inception to January 1, 2019, using the search string psoriasis or psoriatic and neoplasms or malignancy or cancer. The search was filtered to only include human participants and publications in English.

Study Selection

Observational cohort studies with a population of patients with psoriasis or psoriatic arthritis were included. Studies had to be original and report the incidence or prevalence of cancer within this population. Studies evaluating pediatric populations and cancer types not included in the protocol were excluded.

Data Extraction and Synthesis

This study was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines. The search string, objectives, and study protocol methods were defined before the study was initiated. A total of 365 studies were included for full-text assessment. Owing to the heterogeneity of the included studies, a random-effects model was used.

Main Outcomes and Measures

Main outcome was cancer (overall and specific subtypes) and measures were prevalence, incidence, and risk estimate for cancer in patients with psoriasis or psoriatic arthritis.

Results

Of the 365 studies assessed, 112 were included in the analysis (N = 2 053 932 patients). The overall prevalence of cancer in patients with psoriasis was 4.78% (95% CI, 4.02%-5.59%), with an incidence rate of 11.75 per 1000 person-years (95% CI, 8.66-15.31) and a risk ratio (RR) of 1.21 (95% CI, 1.11-1.33). There was an increased risk of several cancers, including keratinocyte cancer (RR, 2.28; 95% CI, 1.73-3.01), lymphomas (RR, 1.56; 95% CI, 1.37-1.78), lung cancer (RR, 1.26; 95% CI, 1.13-1.40), and bladder cancer (RR, 1.12; 95% CI, 1.04-1.19). No increased risk of cancer for patients with psoriasis treated with biologic agents was found (RR, 0.97; 95% CI, 0.85-1.10). Psoriatic arthritis was not associated with increased risk of cancer overall (RR, 1.02; 95% CI, 0.97-1.08).

Conclusions and Relevance

Patients with psoriasis appear to have a slightly increased risk of cancer, particularly keratinocyte cancer and lymphomas. Data on treatment with biologic agents did not show an increased risk of cancer. Data on cancer in patients with psoriatic arthritis remain scarce, and further research is warranted in this area.

This systematic review and meta-analysis evaluates the association between cancer and psoriasis or psoriatic arthritis.

Introduction

Psoriasis is a chronic T-cell–mediated inflammatory disease of the skin and joints. It has been suggested that patients with psoriasis are at an increased risk of cancer, and many cancer risk factors, including smoking and alcohol consumption, are associated with psoriasis.^1,2 Two large studies have found an increased risk of cancer overall, compared with either the general population or a reference population without psoriasis.^3,4 Lymphomas and keratinocyte cancer are more prevalent in patients with psoriasis than in control populations.^4,5,6,7,8 Approximately 1 in 4 patients with psoriasis develop psoriatic arthritis during their life course.⁹ Patients with psoriatic arthritis are considered to be more severely affected than those with psoriasis and often require systemic treatment. The risk of cancer in patients with psoriatic arthritis is also debated,¹⁰ but a collective assessment of the cancer risk in such patients is lacking.

A systematic review and meta-analysis from 2013 reported that patients with psoriasis were at an increased risk of some solid cancers, lymphoma, and keratinocyte cancer.¹¹ Since then, multiple, larger studies investigating the association between psoriasis and cancer have been conducted.^4,5,6,7,12 Moreover, the use of biologic agents has increased during recent years with novel drugs being introduced to the market.¹³ Serious adverse events of biologic agents include cancers, but whether biologic agents carry an independent risk of cancer is not known.

We conducted a systematic review and meta-analysis investigating the risk of overall cancer in psoriasis and psoriatic arthritis, as well as the risk of specific cancers. We also investigated the risk of cancer in patients with psoriasis treated with biologic agents compared with conventional therapy.

Methods

Prior to the study, a protocol describing the aims, search strategy, and analysis plan of this systematic review and meta-analysis was developed. The study was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines.¹⁴

Two of us (S.V. and N.D.L.) systematically searched PubMed and Embase from inception until January 1, 2019. The search terms were psoriasis or psoriatic and neoplasms or malignancy or cancer. The search was limited to human participants and publications in English. The reference lists of key articles and reviews were screened for additional studies.

Records were screened according to title and abstracts and duplicates were removed. Relevant articles were selected for full-text review, as well as studies in which eligibility could not be determined based on title or abstract. Disagreement between the reviewers was resolved through debate and the resulting decisions were unanimous.

Studies were eligible for inclusion if they were observational cohort studies with a full-text article or conference abstract available. The source population had to be patients with psoriasis and/or psoriatic arthritis, and the study had to report an incidence or prevalence of cancer within this population.

We limited the analysis to include (1) all cancer, (2) cancer excluding keratinocyte cancer, (3) keratinocyte cancer, (4) melanoma, (5) lymphoma overall, (6) non-Hodgkin lymphoma, (7) Hodgkin lymphoma, (8) breast cancer, (9) lung cancer, (10) colorectal cancer, (11) colon cancer, (12) rectal cancer, and (13) bladder cancer. Studies were excluded if they did not include at least 1 of these categories. Studies investigating only a pediatric population were excluded to minimize age-related bias.

The method of recruitment of study populations was reviewed to avoid including the same population more than once (eg, studies based on the same database in the same time period or follow-ups of older studies). In the case of population duplicates, the newest study or the one that reported on the outcome of interest was chosen for inclusion.

The following data were retrieved, if available: author information, publication year, country, age, sex, number of patients with psoriasis or psoriatic arthritis, assessment of psoriasis or psoriatic arthritis, number of person-years, number of patients with psoriasis or psoriatic arthritis and cancer, incidence rate of cancer, risk estimates including 95% CIs, assessment of cancer, type of cancers, and use of biologic agents. If a control population was available, we also extracted the number of controls, origin of controls (eg, general population, dermatology patients), number of person-years, and number of controls with cancer.

Statistical Analysis

A proportion meta-analysis was performed to obtain pooled prevalence and incidences with 95% CIs. Pooled estimates of patients with psoriasis or psoriatic arthritis compared with controls were conducted using an inverse variance approach. Heterogeneity of studies was assessed with the Cochran Q test, with a significance level of .05, and I² statistic, and forest plots were constructed. The Cochran Q test provides a binary outcome for whether there is significant heterogeneity among the reported effect sizes. The I² statistic provides a quantitative estimate of the variability across studies, where a high percentage suggests that variation is likely due to study heterogeneity and a percentage of 0 suggests that any variation is likely due to chance. In this analysis, which is based on a heterogenic pool of studies, we opted to use the random-effects model (Der Simonian and Laird¹⁵). Publication bias was assessed with funnel plots and Egger tests. Quality of studies was evaluated using the Newcastle-Ottawa scale.¹⁶ Scores of 7 or higher were considered good quality. The following sensitivity analyses were conducted to investigate sources of variability: period published (before 2000, 2000-2009, and 2010-present) and Newcastle-Ottawa scale score (good quality vs fair/poor quality). Data analysis was conducted using StatsDirect, version 3 (StatsDirect Ltd).

Results

We identified 10 176 records through database searching (3643 in PubMed, 6533 in Embase); 8558 nonduplicate articles were screened by title and abstract. Of these, 363 studies were included for full-text assessment, as well as 2 additional records identified by screening references. In total, 112 studies were included for qualitative assessment and data extraction (eFigure 1 in the Supplement). The included studies comprise 2 053 932 patients with psoriasis or psoriatic arthritis (eTable 1 in the Supplement). Quality assessment for analyses of prevalence of all cancer types is presented in Table 1, incidence rates in Table 2, and risk estimates in Table 3. The Newcastle-Ottawa scale scores are presented in eTable 2 in the Supplement. In eTables 3-5 in the Supplement, we present the Egger tests, and in eFigures 2-16 in the Supplement, funnel plots are presented.

Table 1. Prevalence and Quality Assessment According to Different Cancer Types.

Group	Studies, No.	Patients, No.	Prevalence, % (95% CI) Random Effects	I² (95% CI), %	Cochran Q, df	P Value
Cancer overall	41	1 214 030	4.78 (4.02-5.59)	99.3 (99.3-99.3)	5760.99₄₀	<.001
Cancer excluding keratinocyte cancer	41	373 597	4.06 (3.31-4.87)	98.9 (98.8-98.9)	3555.86₄₀	<.001
Keratinocyte cancer	48	374 895	2.55 (2.05-3.11)	99.1 (99.0-99.1)	5111.00₄₇	<.001
Melanoma	31	519 267	0.31 (0.23-0.40)	94.4 (93.3-95.2)	534.44₃₀	<.001
Lymphoma overall	28	1 598 836	0.25 (0.19-0.32)	96.8 (96.3-97.2)	837.26₂₇	<.001
Non-Hodgkin lymphoma	13	395 213	0.30 (0.21-0.39)	92.5 (89.6-94.4)	161.01₁₂	<.001
Hodgkin lymphoma	8	376 984	0.04 (0.02-0.06)	71.3 (25.2-84.4)	24.40₇	.001
Breast cancer	26	613 429	1.63 (1.23-2.08)	98.5 (98.3-98.6)	1619.15₂₅	<.001
Lung cancer	29	825 435	0.87 (0.69-1.08)	97.6 (97.4-97.9)	1188.33₂₈	<.001
Colon cancer	19	362 314	0.59 (0.44-0.75)	94.5 (93.1-95.5)	325.96₁₈	<.001
Rectal cancer	8	135 220	0.27 (0.18-0.37)	84.1 (68.1-90.2)	44.00₇	<.001
Colorectal cancer	13	1 077 432	0.60 (0.47-0.76)	96.3 (95.3-97.0)	322.57₁₂	<.001
Bladder cancer	18	959 642	0.34 (0.20-0.51)	94.7 (93.3-95.7)	320.04₁₇	<.001
Psoriasis treated with biologic agents
Cancer overall	14	22 422	3.85 (2.69-5.20)	92.8 (90.2-94.5)	181.65₁₃	<.001
Cancer excluding keratinocyte cancer	13	32 558	2.28 (1.64-3.02)	90.6 (86.3-93.1)	128.12₁₂	<.001
Keratinocyte cancer	13	30 966	1.87 (1.30-2.54)	90.7 (86.5-93.2)	129.38₁₂	<.001
Lymphoma overall	8	21 701	0.17 (0.08-0.31)	59.8 (0-79.7)	17.42₇	.01
Psoriatic arthritis
Cancer overall	13	39 608	5.74 (3.64-8.28)	98.6 (98.3-98.7)	837.07₁₂	<.001
Cancer excluding keratinocyte cancer	7	13 507	3.59 (1.67-6.21)	96.9 (95.7-97.6)	192.08₆	<.001
Keratinocyte cancer	9	23 096	3.10 (1.24-5.76)	98.7 (98.5-98.9)	621.52₈	<.001
Melanoma	6	32 408	0.29 (0.17-0.44)	62.1 (0-82.4)	13.20₅	.02
Lymphoma overall	4	23 546	0.19 (0.09-0.31)	33.5 (0-77.5)	4.51₃	.21
Breast cancer	6	2546	1.63 (0.57-3.23)	76.9 (32.9-87.9)	21.68₅	<.001
Lung cancer	4	20 924	0.70 (0.18-1.54)	79.2 (9.9-90.3)	14.39₃	.002
Colorectal cancer	7	24 234	0.42 (0.21-0.69)	57.8 (0-79.8)	14.22₆	.03

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Table 2. Incidence and Quality Assessment According to Different Cancer Types.

Group	Studies, No.	Patient-Years, No.	Incidence, per 1000 Person-Years (95% CI) Random Effects	I² (95% CI), %	Cochran Q, df	P Value
Cancer overall	17	4 637 131	11.75 (8.66-15.31)	99.3 (99.3-99.4)	2380.06₁₆	<.001
Cancer excluding keratinocyte cancer	17	277 062	7.61 (6.53-8.77)	96.7 (96.1-97.2)	489.16₁₆	<.001
Keratinocyte cancer	19	198 191	4.35 (3.18-5.7)	99.4 (99.4-99.5)	3129.47₁₈	<.001
Melanoma	18	2 819 678	0.37 (0.29-0.46)	87.6 (82.2-90.8)	136.78₁₇	<.001
Lymphoma overall	13	7 946 421	0.39 (0.29-0.51)	97.3 (96.7-97.7)	510.65₁₄	<.001
Non-Hodgkin lymphoma	7	2 096 160	0.35 (0.29-0.42)	73.0 (24.3-85.7)	22.20₆	.001
Hodgkin lymphoma	6	2 045 729	0.07 (0.04-0.10)	72.4 (9.7-86.1)	18.09₅	.003
Breast cancer	15	2 898 716	2.06 (1.32-2.95)	99.1 (98.9-99.2)	565.05₅	<.001
Lung cancer	13	6 650 880	0.95 (0.74-1.20)	97.6 (97.1-98.0)	496.34₁₂	<.001
Colon cancer	11	2 259 188	0.61 (0.48-0.76)	86.7 (77.9-91.0)	75.33₁₀	<.001
Rectal cancer	4	922 621	0.29 (0.24-0.36)	44.1 (0-80.3)	5.36₃	.15
Colorectal cancer	8	5 540 749	0.80 (0.65-0.96)	93.3 (89.7-95.2)	104.09₇	<.001
Bladder cancer	7	939 408	0.31 (0.19-0.45)	92.5 (87.7-94.9)	80.22₆	<.001
Psoriasis treated with biologic agents
Cancer overall	6	45 005	14.11 (10.08-18.80)	90.1 (81.1-93.8)	50.72₅	<.001
Cancer excluding keratinocyte cancer	4	20 863	8.09 (7.44-8.76)	0 (0-67.9)	1.64₃	.65
Keratinocyte cancer	6	70 904	8.30 (5.32-11.93)	94.5 (91.2-96.1)	90.39₅	<.001
Lymphoma overall	3	41 997	0.27 (0.07-0.62)	65.9 (0-88.1)	5.87₂	.053
Psoriatic arthritis
Cancer overall	9	23 630	6.44 (4.80-8.32)	93.9 (91.0-95.5)	130.23₈	<.001
Cancer excluding keratinocyte cancer	5	13 091	4.76 (3.25-6.55)	82.3 (48.5-90.7)	22.58₄	<.001
Keratinocyte cancer	6	22 620	6.12 (1.78-13.03)	99.3 (99.2-99.4)	697.24₅	<.001
Melanoma	4	31 482	0.46 (0.31-0.64)	39.7 (0-79.1)	4.98₃	.17
Lymphoma overall	3	23 329	0.32 (0.23-0.43)	0 (0-72.9)	0.60₂	.74
Breast cancer	4	2375	1.01 (0.31-2.10)	66.6 (0-86.4)	8.98₃	.03
Lung cancer	2	20 042	0.47 (0.35-0.60)	0	0.87₁	.35
Colorectal cancer	5	23 902	0.66 (0.49-0.87)	6.9 (0-66.5)	4.30₄	.35

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Table 3. Risk Estimates and Quality Assessment According to Different Cancer Types.

Group	No. of Studies	No. of Patients	RR (95% CI) Random Effects	I² (95% CI), %	Cochran Q, df	P Value
Cancer overall	14	1 147 009	1.21 (1.11-1.33)	96 (95.0-96.8)	328.48₁₃	<.001
Cancer excluding keratinocyte cancer	15	292 228	1.14 (1.04-1.25)	90.3 (86.1-92.7)	143.59₁₄	<.001
Keratinocyte cancer	17	387 173	2.28 (1.73-3.01)	100 (100-100)	303 133.91₁₆	<.001
Melanoma	16	456.924	1.13 (0.99-1.29)	52.1 (0-71.6)	31.29₁₅	.008
Lymphoma overall	15	1 512 417	1.56 (1.37-1.78)	71.2 (46.4-81.7)	48.59₁₄	<.001
Non-Hodgkin lymphoma	9	377 594	1.48 (1.30-1.69)	49.4 (0-74.7)	15.81₈	.045
Hodgkin lymphoma	6	375 475	1.87 (1.40-2.48)	43.8 (0-76.2)	8.90₅	.11
Breast cancer	13	582 645	1.07 (0.99-1.15)	54.9 (0-74.4)	26.62₁₂	.009
Lung cancer	14	789 630	1.26 (1.13-1.40)	76.8 (58.4-.9)	55.92₁₃	<.001
Colon cancer	13	341 673^a	1.20 (0.98-1.47)	86.1 (77.8-90.3)	86.31₁₂	<.001
Rectal cancer	8	135 163^a	1.04 (0.88-1.23)	40.6 (0-72.3)	11.78₇	.11
Colorectal cancer	10	1 060 351^a	1.16 (0.99-1.35)	89.0 (82.0-92.4)	81.59₉	.001
Bladder cancer	9	940 980	1.12 (1.04-1.19)	0 (0-54.4)	6.80₈	.002
Biologic agents
Cancer overall	3	12 163^b	0.97 (0.85-1.10)	17.3 (0-77.3)	2.42₂	.30
Cancer excluding keratinocyte cancer	6	25 430	0.86 (0.75-0.99)	5 (0-65)	5.60₅	.03
Keratinocyte cancer	4	20 345	0.91 (0.64-1.30)	86.8 (61.1-93.1)	22.80₃	<.001
Lymphoma overall	3	14 673	0.68 (0.42-1.09)	4.4 (0-74.1)	2.09₂	.35
Psoriatic arthritis
Cancer overall	6	32 979	1.02 (0.97-1.08)	0 (0-61)	3.39₅	.64
Cancer excluding keratinocyte cancer	3	11 680	1.06 (0.96-1.17)	0 (0-72.9)	1.27₂	.53
Keratinocyte cancer	6	20 786	1.22 (0.89-1.66)	75.2 (24.4-87.2)	20.15₅	.001
Melanoma	4	31 081	1.20 (0.94-1.54)	0 (0-67.9)	2.58₃	.46
Lymphoma overall	3	22 928	0.99 (0.70-1.39)	0 (0-72.9)	0.00₂	>.99
Breast cancer	3	1611	1.73 (1.15-2.59)	0 (0-72.9)	1.71₂	.43
Lung cancer	3	20 623	0.93 (0.71-1.22)	0 (0-72.9)	1.01₂	.60
Colorectal cancer	4	23 200	0.88 (0.69-1.11)	0 (0-67.9)	2.40₃	.49

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Abbreviation: RR, risk ratio.

^{^a}

Includes a study by Hemminki et al¹⁷ that does not report number of patients with psoriasis.

^{^b}

Includes a study by Spehr et al¹⁸ that does not report number of patients with psoriasis.

The prevalence of cancer overall in patients with psoriasis was 4.78% (95% CI, 4.02%-5.59%), which decreased to 4.06% (95% CI, 3.31%-4.87%) when keratinocyte cancer was excluded (Table 1). The incidence rate (IR) per 1000 person-years for overall cancer was 11.75 (95% CI, 8.66-15.31) and 7.61 (95% CI, 6.53-8.77) when keratinocyte cancer was excluded (Table 2).

Fourteen studies reported risk estimates of cancer overall or had a reference group. Of these, 8 showed a significantly increased risk of cancer in patients with psoriasis,^{2,3,19,20,21,22,23,24} 2 found a protective effect of psoriasis,^12,25 and in 4 studies, the association was nonsignificant.^26,27,28,29 The overall risk ratio (RR) was 1.21 (95% CI, 1.11-1.33) and decreased to 1.14 (95% CI, 1.04-1.25) when keratinocyte cancer was excluded (Table 3). This finding was based on 15 studies, with 7 noting a significant association between psoriasis and cancer^{19,24,30,31,32,33,34} and 8 finding no association.^{12,26,29,35,36,37,38,39}

The overall prevalence of keratinocyte cancer in patients with psoriasis was 2.55% (95% CI, 2.05%-3.11%) (Figure 1). In the literature review, the prevalence ranged from 0.08%⁴⁰ to 34.93%.⁴¹ The IR was 4.35 (95% CI, 3.18-5.70) for keratinocyte cancer (Table 2). Risk estimates also presented large variants from 0.98, in a comparison of a psoriasis cohort with nonpsoriatic controls in a large UK-based database,¹² to 7.50, seen in a Taiwanese study comparing 7061 patients with psoriasis with a claims database cohort.⁴² The RR for keratinocyte cancer was based on 17 studies, of which 11 found a significant association with psoriasis^{5,6,7,19,20,21,23,24,26,42,43} and 6 found no association.^{12,28,29,38,44,45} Overall, the RR was significantly increased (2.28; 95% CI, 1.73-3.01) for keratinocyte cancer in psoriasis (Figure 2).

For melanoma, the prevalence was 0.31% (95% CI, 0.23%-0.40%) (Figure 1), with an IR of 0.37 (95% CI, 0.29-0.46). The RR for melanoma was 1.13 (95% CI, 0.99-1.29) (Figure 2), based on 16 studies. Three studies found a significant association to psoriasis,^6,39,42 while the remaining found no association.^{7,12,19,20,21,23,31,32,33,35,36,46,47}

The prevalence of lymphomas in patients with psoriasis was 0.25% (95% CI, 0.19%-0.32%). For non-Hodgkin lymphoma, the prevalence was 0.30% (95% CI, 0.21%-0.39%) vs the lower prevalence for Hodgkin lymphoma (0.04%; 95% CI, 0.02%-0.06%) (Table 1).

The IR of lymphomas was 0.39 (95% CI, 0.29-0.51). For non-Hodgkin lymphoma, the IR was 0.35 (95% CI, 0.29-0.42) and 0.07 (95% CI, 0.04-0.10) for Hodgkin lymphoma (Table 2).

Risk estimates were based on 15 studies. Nine found a significantly increased risk of lymphomas in patients with psoriasis,^{4,8,12,21,32,42,48,49,50,51} while the remaining 6 found no association.^{23,28,35,38,52,53} The risk of lymphoma was significantly increased (RR, 1.56; 95% CI, 1.37-1.78) (Figure 2). The risks of non-Hodgkin lymphoma (RR, 1.48; 95% CI, 1.30-1.69) and Hodgkin lymphoma (RR, 1.87; 95% CI, 1.40-2.48) were also significantly increased (Table 3).

Only breast cancer in women was considered. The overall prevalence was 1.63% (95% CI, 1.23%-2.08%) (Figure 1). The IR was 2.06 (95% CI, 1.32-2.95) (Table 2). The risk of breast cancer in women with psoriasis was 1.07 (95% CI, 0.99-1.15) (Figure 2). This finding was based on 13 studies, 3 of which showed a significant association between psoriasis and breast cancer^30,34,53; 10 found no association.^{4,12,19,20,21,23,32,35,39,54}

The overall prevalence of lung cancer in patients with psoriasis was 0.87% (95% CI, 0.69%-1.08%) (Table 1). The IR was 0.95 (95% CI, 0.74-1.20) (Table 2). The risk of lung cancer was significantly increased, with an RR of 1.26 (95% CI, 1.13-1.40) (Figure 2). The result was based on 14 studies; 7 showed a significant association between psoriasis and lung cancer^{4,7,12,19,21,33,34} and 7 found no association.^{20,23,27,32,37,39,53}

The overall prevalence of colorectal cancer in patients with psoriasis was 0.60% (95% CI, 0.47%-0.76%) (Figure 1). The IR was 0.80 (95% CI, 0.65-0.96) (Table 2). The risk of colorectal cancer was not significantly increased (Table 3). This finding was based on 10 studies, 3 of which found a significant association between psoriasis and cancer,^3,17,55 1 found a protective effect of psoriasis,⁷ and 6 identified no association.^{4,19,32,33,35,39} Analyzing colon and rectal cancer separately did not change the association (Figure 2).

The prevalence of bladder cancer was 0.34% (95% CI, 0.20%-0.51%) in patients with psoriasis (Figure 1). The IR was 0.31 (95% CI, 0.19-0.45) (Table 2). The risk of bladder cancer was increased with a RR of 1.12 (95% CI, 1.04-1.19) (Figure 2). This finding was based on 9 studies; 1 found a significant association between psoriasis and bladder cancer⁵⁶ and the remaining 8 found no significant results.^{4,19,20,21,27,36,39,53}

The prevalence of overall cancer in patients with psoriasis receiving biologic agents was 3.85% (95% CI, 2.69%-5.20%) (Table 1). The IR was 14.11 (95% CI, 10.08-18.80) (Table 2). Three studies comprising more than 12 000 patients with psoriasis receiving biologic agents could be included in the risk analysis.^18,57,58 Compared with patients receiving conventional therapy, no increased risk of cancer was seen (RR, 0.97; 95% CI, 0.85-1.10) (Table 3, Figure 2). When excluding keratinocyte cancer, 6 studies (n = 25 430) could be included.^{38,57,58,59,60,61}

When comparing the risk of both keratinocyte cancer (4 studies, n = 25 993)^38,57,58,62 and lymphomas (3 studies, n = 14 673)^38,57,58 in patients receiving biologic agents vs patients receiving conventional therapy, no increased risk of cancer was noted in patients treated with biologic agents (Figure 2).

The prevalence of cancer overall in patients with psoriatic arthritis was 5.74% (95% CI, 3.64%-8.28%) (Figure 1) with an IR of 6.44 (95% CI, 4.80-8.32) (Table 2). The risk of cancer overall in patients with psoriatic arthritis, based on 6 studies (n = 32 979), was not increased (Table 3).^{10,63,64,65,66,67} Of the included studies, none found a significant association between psoriatic arthritis and cancer overall (RR, 1.02; 95% CI, 0.97-1.08). Psoriatic arthritis was significantly associated with an increased risk of breast cancer (3 studies).^63,64,67 The remaining cancer types either had too few studies for analysis or no association was seen.

In general, the same results were seen in sensitivity analyses for high- and low/fair-quality studies, except for cancer excluding keratinocyte cancer, in which the association between cancer and psoriasis was lost. The same outcomes were seen for studies published since 2010. For the high-quality studies, an association between psoriasis and colorectal cancer was seen. The results of the sensitivity analysis are presented in eTables 6-9 in the Supplement. Sensitivity analyses could not be conducted for the association between psoriatic arthritis and cancer and biologic agents and cancer.

Discussion

In this systematic review and meta-analysis, we found significant associations between psoriasis and risk of overall cancer, cancer excluding keratinocyte cancer, keratinocyte cancer, lymphomas, lung cancer, and bladder cancer. When comparing biologic agents with conventional treatment, we found a decreased risk of cancer when excluding keratinocyte cancer. We did not find an increased risk of cancer in patients with psoriatic arthritis. No publication bias was detected.

A meta-analysis from 2013 showed an association between psoriasis and cancer excluding keratinocyte cancer, keratinocyte cancer, and some solid cancers, including respiratory tract and urinary tract cancer.¹¹ In agreement, we found a significant association with cancer excluding keratinocyte cancer, keratinocyte cancer, lung cancer, and bladder cancer. Our study comprises more than twice the number of studies, including newer and larger investigations, than the 2013 meta-analysis. Given that our results align with those of the older analysis, the notion of an association is supported.

The risk of developing keratinocyte cancer is associated with exposure to sunlight. Studies investigating risk of keratinocyte cancer in patients receiving psoralen–UV-A (PUVA) therapy show a highly elevated risk,³¹ particularly of squamous cell carcinomas.⁴¹ A previous study investigated the risk of melanoma and keratinocyte cancer in patients with psoriasis compared with the general population of Denmark.⁶ When adjusting for confounders, including PUVA, the study found a small but significantly increased risk of keratinocyte cancer, indicating that factors other than PUVA treatment may be important. Patients with psoriasis see dermatologists more frequently than the general population and, therefore, more keratinocyte cancers may be detected. Furthermore, patients with keratinocyte cancer often spend more time in the sunand have been treated with UV-B irradiation and tar, which are known to increase the risk of keratinocyte cancer.^68,69,70

In the sensitivity analysis, studies of high quality showed no association between psoriasis and overall cancer when excluding keratinocyte cancer. This finding further highlights the risk of keratinocyte cancer in patients with psoriasis.

We found that patients with psoriasis are at an increased risk of developing both Hodgkin and non-Hodgkin lymphoma. This elevation might in part be explained by an increased risk of cutaneous T-cell lymphoma (CTCL) in patients with psoriasis. Four of the included studies did separate analysis on CTCL and non-Hodgkin lymphoma excluding CTCL.^8,12,19,49 All found the risk of CTCL to be highly increased in patients with severe psoriasis. The association may in part be due to misclassification leading to an overestimation of the risk of lymphoma in patients with psoriasis. However, in a study of patients with coexisting diagnoses of CTCL and psoriasis, both diagnoses could be histologically verified in a high proportion of patients.⁷¹ Although misclassification occurs, the increased risk of lymphomas in psoriasis might also be explained by persistent immune activation leading to the development of a dominant clone.

Lifestyle factors, such as smoking and alcohol consumption, are associated with psoriasis,^1,2 and the increased risk of cancer in patients with psoriasis might be explained by this.⁷² Chiesa Fuxench et al¹² found a small increased risk of all cancers excluding keratinocyte cancer when adjusting for confounders. Likewise, they found an increased risk of lung cancer when adjusting for smoking. Brauchli et al³² found an increased risk of cancer excluding keratinocyte cancer when adjusting for body mass index, smoking, and benign tumors. Lee et al⁴ found an increased risk of overall cancer when adjusting for several confounders. Given that the effect sizes diminish when adjusting for certain lifestyle factors, it is evident that these lifestyle factors are associated with the increased risk of cancer observed in patients with psoriasis. However, because the risk is still increased after accounting for these lifestyle factors, the factors cannot explain the associations alone.

In our analysis, we included observational studies investigating the safety of biologic agents, as well as information on biologic agents in all included material. The results revealed no increased risk of cancers associated with biologic agent treatment. However, patients receiving biologic agents are selected and the results might be reliant on selection bias, and studies investigating long-term safety of these drugs are still limited. We did not find an increased risk of cancer in patients with psoriatic arthritis, except for breast cancer, which was based on only 3 studies.

Strengths and Limitations

Strengths of this investigation include the number of studies and patients included, the real-world setting of the studies, the inclusion of biologic agents, and analysis of patients with psoriatic arthritis. To our knowledge, this is the first meta-analysis to investigate cancer risk in psoriatic arthritis. Our risk estimates present narrow 95% CIs, which suggests a high accuracy of the estimates. The inclusion of cohort studies secures a high external validity. Moreover, we present both the prevalence and incidence of different cancers in patients with psoriasis.

However, some limitations should be addressed when interpreting the results of our study. The included studies were heterogeneous, which makes comparisons difficult. Inconsistencies between studies include risk estimates presented, assessment of psoriasis and cancer, origin of reference populations, and length of follow-up. Moreover, studies made different adjustments to their results and some did not collect information on risk factors. Few studies were available to provide data on biologic agents and psoriatic arthritis.

Conclusion

Patients with psoriasis appear to have an increased risk of cancer, particularly keratinocyte cancer, lymphomas, lung cancer, and bladder cancer. Clinicians treating patients with psoriasis should be aware of this increased risk, especially for lymphomas, as immunogenic treatment might be associated with exacerbations. The current literature does not suggest an increased risk of cancer associated with biologic agents; however, more research is needed. Evidence on the risk of cancer in psoriatic arthritis is limited, and further studies should be conducted.

Supplement.

eFigure 1. PRISMA Flowchart

eFigure 2. Funnel Plots for Prevalence of Cancer and Skin Cancer

eFigure 3. Funnel Plots for Prevalence of Lymphomas

eFigure 4. Funnel Plots for Prevalence of Solid Cancers

eFigure 5. Funnel Plots for Prevalence of Cancers in Patients Receiving Biological Treatment for Psoriasis

eFigure 6. Funnel Plots for Prevalence of Cancers in Patients With Psoriatic Arthritis

eFigure 7. Funnel Plots for Incidence of Cancer and Skin Cancer

eFigure 8. Funnel Plots for Incidence of Lymphomas

eFigure 9. Funnel Plots for Incidence of Solid Cancers

eFigure 10. Funnel Plots for Incidence of Cancers in Patients Receiving Biological Treatment for Psoriasis

eFigure 11. Funnel Plots for Incidence of Cancers in Patients With Psoriatic Arthritis

eFigure 12. Funnel Plots for Risk Ratio of Cancer and Skin Cancer

eFigure 13. Funnel Plots for Risk Ratio of Lymphomas

eFigure 14. Funnel Plots for Risk Ratio of Solid Cancers

eFigure 15. Funnel Plots for Risk Ratio of Cancer in Patients Receiving Biological Treatment

eFigure 16. Funnel Plots for Risk Ratio of Cancer in Patients With Psoriatic Arthritis

eTable 1. Overview of All Included Studies

eReferences.

eTable 2. Newcastle Ottawa Scale

eTable 3. Egger Bias of Prevalence According to Different Cancer Types

eTable 4. Egger Bias of Incidence According to Different Cancer Types

eTable 5. Egger Bias of Risk Estimates According to Different Cancer Types

eTable 6. Prevalence and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—Year of Publication

eTable 7. Incidence and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—Year of Publication

eTable 8. Risk Estimates and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—Year of Publication

eTable 9. Risk Estimates and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—High Quality

Click here for additional data file.^{(1.3MB, pdf)}

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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.

eFigure 1. PRISMA Flowchart

eFigure 2. Funnel Plots for Prevalence of Cancer and Skin Cancer

eFigure 3. Funnel Plots for Prevalence of Lymphomas

eFigure 4. Funnel Plots for Prevalence of Solid Cancers

eFigure 5. Funnel Plots for Prevalence of Cancers in Patients Receiving Biological Treatment for Psoriasis

eFigure 6. Funnel Plots for Prevalence of Cancers in Patients With Psoriatic Arthritis

eFigure 7. Funnel Plots for Incidence of Cancer and Skin Cancer

eFigure 8. Funnel Plots for Incidence of Lymphomas

eFigure 9. Funnel Plots for Incidence of Solid Cancers

eFigure 10. Funnel Plots for Incidence of Cancers in Patients Receiving Biological Treatment for Psoriasis

eFigure 11. Funnel Plots for Incidence of Cancers in Patients With Psoriatic Arthritis

eFigure 12. Funnel Plots for Risk Ratio of Cancer and Skin Cancer

eFigure 13. Funnel Plots for Risk Ratio of Lymphomas

eFigure 14. Funnel Plots for Risk Ratio of Solid Cancers

eFigure 15. Funnel Plots for Risk Ratio of Cancer in Patients Receiving Biological Treatment

eFigure 16. Funnel Plots for Risk Ratio of Cancer in Patients With Psoriatic Arthritis

eTable 1. Overview of All Included Studies

eReferences.

eTable 2. Newcastle Ottawa Scale

eTable 3. Egger Bias of Prevalence According to Different Cancer Types

eTable 4. Egger Bias of Incidence According to Different Cancer Types

eTable 5. Egger Bias of Risk Estimates According to Different Cancer Types

eTable 6. Prevalence and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—Year of Publication

eTable 7. Incidence and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—Year of Publication

eTable 8. Risk Estimates and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—Year of Publication

eTable 9. Risk Estimates and Quality Assessment According to Different Cancer Types—Sensitivity Analysis—High Quality

Click here for additional data file.^{(1.3MB, pdf)}

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PERMALINK

Prevalence, Incidence, and Risk of Cancer in Patients With Psoriasis and Psoriatic Arthritis

Sofie Vaengebjerg, MD

Lone Skov, MD, PhD, DMSC

Alexander Egeberg, MD, PhD

Nikolai Dyrberg Loft, MD

Key Points

Question

Findings

Meaning

Abstract

Importance

Objective

Data Sources

Study Selection

Data Extraction and Synthesis

Main Outcomes and Measures

Results

Conclusions and Relevance

Introduction

Methods

Statistical Analysis

Results

Table 1. Prevalence and Quality Assessment According to Different Cancer Types.

Table 2. Incidence and Quality Assessment According to Different Cancer Types.

Table 3. Risk Estimates and Quality Assessment According to Different Cancer Types.

Figure 1. Prevalence of Cancers.

Figure 2. Risk Ratios (RRs) for Cancers.

Discussion

Strengths and Limitations

Conclusion

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

Cite

Add to Collections

PERMALINK

Prevalence, Incidence, and Risk of Cancer in Patients With Psoriasis and Psoriatic Arthritis

Sofie Vaengebjerg, MD

Lone Skov, MD, PhD, DMSC

Alexander Egeberg, MD, PhD

Nikolai Dyrberg Loft, MD

Key Points

Question

Findings

Meaning

Abstract

Importance

Objective

Data Sources

Study Selection

Data Extraction and Synthesis

Main Outcomes and Measures

Results

Conclusions and Relevance

Introduction

Methods

Statistical Analysis

Results

Table 1. Prevalence and Quality Assessment According to Different Cancer Types.

Table 2. Incidence and Quality Assessment According to Different Cancer Types.

Table 3. Risk Estimates and Quality Assessment According to Different Cancer Types.

Figure 1. Prevalence of Cancers.

Figure 2. Risk Ratios (RRs) for Cancers.

Discussion

Strengths and Limitations

Conclusion

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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