SHORT COMMUNICATION

Dermatological Comorbidities in Patients with Familiar Mediterranean Fever

Eli MAGEN1,2, David OZERI3, Eugene MERZON1,4, Shlomo VINKER1,5 and Ariel ISRAEL1,5

1Leumit Health Services, Tel Aviv-Yafo, 2Medicine A Department, Assuta Ashdod University Hospital Faculty of Health Sciences, Ben-Gurion University, 8410501 Beer-Sheba, 3Division of Rheumatology, Sheba Medical Center, Ramat Gan, 4Adelson School of Medicine, Ariel University, Ariel, and 5Department of Family Medicine, Faculty of Medicine, Tel-Aviv University, Tel Aviv-Yafo, Israel. E-mail: allergologycom@gmail.com

 

Citation: Acta Derm Venereol 2024; 104: adv39988. DOI: https://doi.org/10.2340/actadv.v104.39988.

Copyright: © 2024 The Author(s). Published by MJS Publishing, on behalf of the Society for Publication of Acta Dermato-Venereologica. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/).

Submitted: Jan 28, 2024; Accepted: Jul 4, 2024; Published: Aug 15, 2024

Competing interests and funding: The authors have no conflicts of interest to declare.

 

INTRODUCTION

Familial Mediterranean fever (FMF) is a well-defined autoinflammatory disease characterized by recurrent febrile episodes and serositis resulting from marenostrin-encoding fever (MEFV) gene mutations located on chromosome 16p13.3, leading to dysregulated inflammasome activity and systemic inflammation (1). While FMF is renowned for its systemic symptoms, its cutaneous manifestations, such as erythema elevatum diutinum (2), urticaria (3), Henoch-Schönlein purpura, polyarteritis nodosa, and episodic purpuric lesions (4), are less prominently recognized. These manifestations indicate a wider influence of FMF on the skin, an aspect that has received limited attention in medical research. This paper seeks to investigate additional dermatological comorbidities linked to FMF.

MATERIALS AND METHODS

This study utilized data from Leumit Health Services (LHS), a national healthcare provider in Israel. The study cohort was extracted from over 1,000,000 individuals insured by LHS from January 2001 until December 2023. The study employed International Classification of Diseases 9th revision (ICD-9) codes to identify cases of FMF. Specifically, the code 277.31 was utilized. The FMF group included patients with a documented FMF diagnosis by board-certified rheumatologists according to the Tel Hashomer criteria for a diagnosis of FMF (5). The control group comprised individuals without FMF randomized with a ratio of 1:4. Rigorous matching based on age, gender, socioeconomic status, and first year of LHS membership was performed to ensure comparability between the 2 groups. ICD-9 codes recorded in electronic health records were used to compare the lifelong prevalence of dermatological comorbidities. The Leumit Health Services Institutional Ethics Committee approved the study.

Statistical analysis

Differences in demographic and clinical characteristics between groups were analysed using independent sample t-tests for normally distributed continuous variables. For categorical variables, proportions were tested using Fisher’s exact test. Odds ratios and 95% confidence intervals (95% CIs) were calculated. All statistical analyses were conducted using R software version 4.0.4 (R Foundation for Statistical Computing, Vienna, Austria).

RESULTS

Our study compared the demographics of 3,324 patients with FMF and 13,296 controls. The age and gender distribution across both groups was similar, with an average age of 36.9 ± 20.1 years, and 51.1% females in both FMF patients and controls. The average BMI was slightly lower in the FMF group (22.3 ± 6.1) compared with the controls (22.7 ± 6.2) (p = 0.001).

Our analysis of the lifelong prevalence of dermatological comorbidities in patients with FMF compared with controls is presented in Table I. In the category of inflammatory skin diseases, FMF patients showed a higher prevalence of atopic dermatitis (14.6% vs 12.6%, OR 1.19 [CI 1.06 to 1.33]; p = 0.002), contact dermatitis (25.1% vs 22.8%, OR 1.13 [CI 1.04 to 1.24]; p = 0.006), seborrheic dermatitis (9.60% vs 8.45%, OR 1.15 [CI 1.01 to 1.31]; p = 0.039), and psoriasis (4.27% vs 3.52%, OR 1.22 [CI 1.00 to 1.49]; p = 0.044). Acne was also more common in FMF patients (22.6% vs 19.3%, OR 1.22 [CI 1.11 to 1.34]; p < 0.001), as were erythema nodosum (0.57% vs 0.18%, OR 3.18 [CI 1.64 to 5.06]; p < 0.001) and hidradenitis suppurativa (0.57% vs 0.15%, OR 3.82 [CI 1.92 to 7.54]; p < 0.001). Acute urticaria was another condition with a significantly higher prevalence in the FMF group (13.5% vs 10.4%, OR 1.13 [CI 1.20 to 1.51]; p < 0.001).

Table I. Lifelong prevalence of dermatological comorbidities in patients with familial Mediterranean fever (FMF)
Dermatological comorbidities FMF N = 3,324 n (%) Control N = 13,296 n (%) p-value OR [95% CI]
Inflammatory skin diseases
Atopic dermatitis 485 (14.6) 1,669 (12.6) 0.002 1.19 [1.06–1.33]
Contact dermatitis 835 (25.1) 3,038 (22.8) 0.006 1.13 [1.04–1.24]
Seborrheic dermatitis 319 (9.60) 1,124 (8.45) 0.039 1.15 [1.01–1.31]
Lichen planus 10 (0.30) 62 (0.47) 0.237 0.64 [0.29–1.27]
Psoriasis 142 (4.27) 468 (3.52) 0.044 1.22 [1.00–1.49]
Pityriasis rosea 69 (2.08) 228 (1.71) 0.164 1.21 [0.91–1.60]
Erythema multiforme 10 (0.30) 22 (0.17) 0.121 1.82 [0.77–4.01]
Acne 750 (22.6) 2,565 (19.3) <0.001 1.22 [1.11–1.34]
Rosacea 27 (0.81) 121 (0.91) 0.679 0.89 [0.56–1.36]
Erythema nodosum 19 (0.57) 24 (0.18) <0.001 3.18 [1.64–6.06]
Hidradenitis suppurativa 19 (0.57) 20 (0.15) <0.001 3.82 [1.92–7.54]
Acute urticaria 450 (13.5) 1,382 (10.4) <0.001 1.35 [1.20–1.51]
Infectious skin diseases
Impetigo 283 (8.51) 1,122 (8.44) 0.889 1.01 [0.88–1.16]
Cellulitis 1,118 (33.6) 3,104 (23.3) <0.001 1.66 [1.53–1.81]
Dermatophytosis (ringworm) 1,044 (31.4) 3,959 (29.8) 0.069 1.08 [0.99–1.17]
Onychomycosis 237 (7.13) 1021 (7.68) 0.285 0.92 [0.79–1.07]
Candidiasis 71 (2.14) 223 (1.68) 0.077 1.28 [0.96–1.68]
Herpes simplex 492 (14.8) 1,494 (11.2) <0.001 1.37 [1.23–1.53]
Herpes zoster 193 (5.81) 633 (4.76) 0.014 1.23 [1.04–1.46]
Molluscum contagiosum 206 (6.20) 808 (6.08) 0.807 1.02 [0.87–1.20]
Autoimmune diseases
Lupus erythematosus (systemic) 19 (0.57) 26 (0.20) 0.001 2.93 [1.53–5.52]
Lupus erythematosus (discoid) 0 2 (0.015) 0.885 0.80 [0.04–16.66]
Dermatomyositis 1 (0.03) 16 (0.12) 0.224 0.25 [0.01–1.61]
Scleroderma (systemic) 3 (0.09) 12 (0.09) 0.999 1.00 [0.18–3.71]
Scleroderma (localized) 0 3 (0.02) 0.711 0.57 [0.03–11.06]
Behcet disease 35 (1.053) 10 (0.075) <0.001 14.13 [6.84–32.04]
Pemphigus 1 (0.03) 2 (0.015) 0.488 2.00 [0.03–38.48]
Bullous pemphigoid 0 1 (0.01) 0.860 1.33 [0.05–32.73]
Dermatitis herpetiformis 2 (0.060) 11 (0.083) 0.999 0.73 [0.08–3.33]
Alopecia areata 108 (3.25) 232 (1.74) <0.001 1.89 [1.49–2.39]
Vitiligo 27 (0.81) 86 (0.65) 0.289 1.26 [0.78–1.96]
Chronic spontaneous urticaria 43 (1.29) 129 (0.97) 0.104 1.34 [0.95–1.89]
Neoplastic skin diseases
Mycosis fungoides 4 (0.12) 22 (0.17) 0.557 0.73 [0.25–2.11]
Melanoma 5 (0.15) 23 (0.17) 0.869 0.87 [0.26–2.34]
Basal cell carcinoma 19 (0.57) 84 (0.63) 0.805 0.90 [0.52–1.50]
Squamous cell carcinoma 10 (0.30) 28 (0.21) 0.314 1.43 [0.62–3.04]
Kaposi’s sarcoma 0 1 (0.01) 0.860 1.33 [0.05–32.73]

In infectious skin diseases, cellulitis (33.6% vs 23.3%, OR 1.66 [CI 1.53 to 1.81]; p < 0.001), herpes simplex (14.8% vs 11.2%, OR 1.37 [CI 1.23 to1.53]; p < 0.001), and herpes zoster (5.81% vs 4.76%, OR 1.23 [CI 1.04 to 1. 46]; p = 0.014) were more prevalent among FMF patients.

Regarding autoimmune diseases, lupus erythematosus (systemic) was notably more common in FMF patients (0.57% vs 0.20%, OR 2.93 [CI 1.53 tox 5.52]; p < 0.001), as was Behcet disease (1.053% vs 0.075% in controls, OR 14.13 [6.84 to 32.04], p < 0.001), and alopecia areata (3.25% vs 1.74%, OR 1.89 [CI 1.49 to 2.39]; p < 0.001). However, no significant differences were observed in the prevalence of discoid lupus erythematosus, dermatomyositis, systemic and localized scleroderma, pemphigus, bullous pemphigoid, dermatitis herpetiformis, vitiligo, and chronic spontaneous urticaria.

No significant differences were observed between the 2 groups in neoplastic skin diseases.

DISCUSSION

Our study presents novel insights into the dermatological comorbidities associated with FMF, expanding the understanding of this autoinflammatory disease beyond its classical systemic manifestations. The significant findings of higher prevalence rates of certain dermatological conditions in FMF patients compared with controls underscore the multifaceted nature of FMF and its broader impact on skin health.

One of the most notable findings is the increased prevalence of inflammatory skin diseases in FMF patients. Previous research on children with FMF did not show an increase in atopic dermatitis (AD) (6). At the same time, we observed higher lifelong prevalence rates of AD, contact dermatitis, and seborrheic dermatitis in FMF. Our study supports the previous observation that psoriasis (7), erythema nodosum (8), and hidradenitis suppurativa (9) are more common in FMF patients than in the normal population. Our observation suggests a possible link between the dysregulated inflammasome activity in FMF and the pathogenesis of these skin conditions (10). This correlation could be attributed to the systemic inflammation and altered immune response inherent in FMF, which may predispose patients to these dermatological conditions.

The study also revealed a higher prevalence of infectious skin diseases, such as cellulitis, herpes simplex, and herpes zoster, in the FMF cohort. This finding could indicate an altered skin barrier or immune dysregulation in FMF patients, making them more susceptible to skin infections (11). Nevertheless, while providing effective treatment for FMF, colchicine and anti-IL-1 drugs (anakinra, canakinumab, rilonacept) are associated with the reactivation of latent viral infections and exacerbation or new onset of psoriasis and other dermatological conditions by modulating the immune system and inflammatory pathways (12).

In skin autoimmune diseases, the significantly higher prevalence of systemic lupus erythematosus, Behcet disease, and alopecia areata in FMF patients is particularly intriguing. Several case series and small studies have reported associations between FMF and autoimmune disorders (13). Our findings may reflect a shared pathophysiological mechanism between FMF and autoimmune skin diseases, potentially involving MHC-I-opathies but not MHC-II-associated autoimmunity (14).

Although a previous study found a significantly lower incidence of cancer in FMF patients than in the general population of Israel (15), our study did not observe significant differences in the prevalence of neoplastic skin diseases between FMF patients and controls. This finding warrants further investigation.

It is essential to acknowledge the limitations of the current study. As a retrospective cohort study, it is subject to limitations inherent in data availability and potential confounding factors. In addition, using ICD-9 codes to identify dermatological comorbidities may introduce inaccuracies or misclassification. However, the large sample size and rigorous matching process enhance the reliability and generalizability of these findings. While previous studies’ results acknowledge dermatological issues as potential comorbidities in FMF, none present a dedicated, real-world study thoroughly characterizing and quantifying these skin conditions without relying on ICD coding.

Overall, our study highlights the importance of dermatological evaluation in patients with FMF and suggests that dermatologists should be aware of the increased risk of certain skin conditions in this patient population. Further studies are needed to elucidate the exact pathophysiological links and to explore potential therapeutic implications for managing these comorbidities in FMF patients.

REFERENCES

  1. Hesker PR, Nguyen M, Kovarova M, Ting JP, Koller BH. Genetic loss of murine pyrin, the familial Mediterranean fever protein, increases interleukin-1β levels. PLoS One 2012; 7: e51105. https://doi.org/10.1371/journal.pone.0051105
  2. Lidar M, Doron A, Barzilai A, Shinar Y, Zaks N, Langevitz P, et al. Erysipelas-like erythema as the presenting feature of familial Mediterranean fever. J Eur Acad Dermatol Venereol 2013; 27: 912-915. https://doi.org/10.1111/j.1468-3083.2011.04442.x
  3. Baumal A, Kantor I. Urticaria and dermographism with Mediterranean fever: report of a case. Arch Dermatol 1961; 84: 630-632. https://doi.org/10.1001/archderm.1961.01580160094016
  4. Azizi E, Fisher BK. Cutaneous manifestations of familial Mediterranean fever. Arch Dermatol 1976; 112: 364-366. https://doi.org/10.1001/archderm.1976.01630270040009
  5. Livneh A, Langevitz P, Zemer D, Zaks N, Kees S, Lidar T, et al. Criteria for the diagnosis of familial Mediterranean fever. Arthritis Rheum 1997; 40: 1879-1885. https://doi.org/10.1002/art.1780401023
  6. Aydoğmuş Ç, Ayaz NA, Çakan M, Karadağ ŞG, Baş VN, Demir F, et al. Is there any difference regarding atopy between children with familial Mediterranean fever and healthy controls? Allergol Immunopathol 2017; 45: 549-552. https://doi.org/10.1016/j.aller.2016.12.006
  7. Erden A, Batu ED, Seyhoğlu E, Karakaş NM, Sağ E, Aktar F, et al. Increased psoriasis frequency in patients with familial Mediterranean fever. Ups J Med Sci 2018; 123: 57-61. https://doi.org/10.1080/03009734.2017.1423425
  8. Kavukcu S, Türkmen M, Soylu A, Kasap B, Tatli Güneş B. Skin and muscle involvement as presenting symptoms in four children with familial Mediterranean fever. Clin Rheumatol 2009; 28: 857-860. https://doi.org/10.1007/s10067-009-1138-7
  9. Vural S, Gündoğdu M, Gökpınar İli E, Yücelten AD, Aksu K, Özen S. Association of pyrin mutations and autoinflammation with complex phenotype hidradenitis suppurativa: a case-control study. Br J Dermatol 2019; 180: 1459-1467. https://doi.org/10.1111/bjd.17466
  10. Wouters F, Bogie J, Wullaert A, van der Hilst J. Recent insights in pyrin inflammasome activation: identifying potential novel therapeutic approaches in pyrin-associated autoinflammatory syndromes. J Clin Immunol 2023; 44: 8. https://doi.org/10.1007/s10875-023-01621-5
  11. Schnappauf O, Chae JJ, Kastner DL, Aksentijevich I. The pyrin inflammasome in health and disease. Front Immunol 2019; 10: 1745. https://doi.org/10.3389/fimmu.2019.01745
  12. Labrosse R, Haddad E. Immunodeficiency secondary to biologics. J Allergy Clin Immunol 2023; 151: 686-690. https://doi.org/10.1016/j.jaci.2023.01.012
  13. Salehzadeh F, Enteshari Moghaddam A. Coexisting diseases in patients with familial Mediterranean fever. Open Access Rheumatol 2020; 12: 65-71. https://doi.org/10.2147/OARRR.S252071
  14. Watad A, Bragazzi NL, Adawi M, Shoenfeld Y, Comaneshter D, Cohen AD, et al. FMF is associated with a wide spectrum of MHC class I- and allied SpA disorders but not with classical MHC class II-associated autoimmune disease: insights from a large cohort study. Front Immunol 2019; 10: 2733. https://doi.org/10.3389/fimmu.2019.02733
  15. Brenner R, Ben-Zvi I, Shinar Y, Padeh S, Lidar M, Feld O, et al. Familial Mediterranean fever and incidence of cancer: an analysis of 8,534 Israeli patients with 258,803 person-years. Arthritis Rheumatol 2018; 70: 127-133. https://doi.org/10.1002/art.40344