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Immune-mediated diseases and subsequent risk of alopecia areata in a prospective study of US women

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Abstract

Introduction

Alopecia areata (AA) is the most common form of immune-mediated hair loss. Studies have begun to establish the most frequent comorbid diseases of AA; however, results have been inconsistent with few prospective studies.

Methods

A total of 63,692 women in the Nurses’ Health Study, 53–80 years, were prospectively followed from 2002 to 2014 to determine whether history of immune-mediated disease was associated with AA risk. Hazard ratios (HRs) and 95% confidence intervals (CIs) for AA in relation to immune-mediated conditions were computed using Cox proportional hazard models, adjusted for AA risk factors.

Results

133 AA cases were identified during follow-up. Personal history of any immune-mediated disease was associated with increased AA risk (HR 1.72, 95% CI 1.24–2.37). History of systemic lupus erythematosus (HR 5.43, 95% CI 2.11–13.97), multiple sclerosis (HR 4.10, 95% CI 1.40–11.96), vitiligo (HR 3.13, 95% CI 1.08–9.10), psoriasis (HR 2.01, 95% CI 1.00–4.03), hypothyroidism (HR 1.88, 95% CI 1.30–2.71), and rheumatoid arthritis (HR 1.66, 95% CI 1.09–2.52) were associated with increased AA risk. History of inflammatory bowel disease or Graves’ disease/hyperthyroidism was not significantly associated with AA risk.

Conclusions

In this prospective study, personal history of immune-mediated diseases either individually or overall was associated with increased AA risk.

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Data availability

The data of this study are available upon reasonable request. Further information including the procedures to obtain and access data from the Nurses’ Health Studies is described at https://www.nurseshealthstudy.org/researchers (contact e-mail: nhsaccess@channing.harvard.edu).

Abbreviations

NHS:

Nurses’ Health Study

HR:

Hazard ratio

CI:

Confidence interval

AA:

Alopecia areata

RA:

Rheumatoid arthritis

IBD:

Inflammatory bowel disease

SLE:

Systemic lupus, vitiligo

MS:

Multiple sclerosis

References:

  1. Lee H, Jung SJ, Patel AB, Thompson JM, Qureshi A, Cho E (2020) Racial characteristics of alopecia areata in the United States. J Am Acad Dermatol 83:1064–1070

    Article  PubMed  Google Scholar 

  2. Fawzi MMT, Mahmoud SB, Ahmed SF, Shaker OG (2016) Assessment of vitamin D receptors in alopecia areata and androgenetic alopecia. J Cosmet Dermatol 15:318–323

    Article  PubMed  Google Scholar 

  3. Toussi A, Barton VR, Le ST, Agbai ON, Kiuru M (2021) Psychosocial and psychiatric comorbidities and health-related quality of life in alopecia areata: a systematic review. J Am Acad Dermatol 85:162–175

    Article  PubMed  Google Scholar 

  4. Strazzulla LC, Wang EHC, Avila L, Lo Sicco K, Brinster N, Christiano AM et al (2018) Alopecia areata: disease characteristics, clinical evaluation, and new perspectives on pathogenesis. J Am Acad Dermatol 78:1–12

    Article  PubMed  Google Scholar 

  5. Giordano CN, Sinha AA (2013) Cytokine pathways and interactions in alopecia areata. Eur J Dermatol 23:308–318

    Article  CAS  PubMed  Google Scholar 

  6. Waśkiel-Burnat A, Osińska M, Salińska A, Blicharz L, Goldust M, Olszewska M et al (2021) The role of serum Th1, Th2, and Th17 cytokines in patients with alopecia areata: clinical implications. Cells 10:3397

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lee S, Lee H, Lee CH, Lee WS (2019) Comorbidities in alopecia areata: a systematic review and meta-analysis. J Am Acad Dermatol 80(466–77):e16

    Google Scholar 

  8. Kennedy Crispin M, Ko JM, Craiglow BG, Li S, Shankar G, Urban JR et al (2016) Safety and efficacy of the JAK inhibitor tofacitinib citrate in patients with alopecia areata. JCI Insight 1:e89776

    Article  PubMed  PubMed Central  Google Scholar 

  9. Liu M, Murphy E, Amerson EH (2016) Rethinking screening for thyroid autoimmunity in vitiligo. J Am Acad Dermatol 75:1278–1280

    Article  PubMed  Google Scholar 

  10. Chu S-Y, Chen Y-J, Tseng W-C, Lin M-W, Chen T-J, Hwang C-Y et al (2011) Comorbidity profiles among patients with alopecia areata: the importance of onset age, a nationwide population-based study. J Am Acad Dermatol 65:949–956

    Article  PubMed  Google Scholar 

  11. Li WQ, Cho E, Weinstock MA, Mashfiq H, Qureshi AA (2016) Epidemiological assessments of skin outcomes in the nurses’ health studies. Am J Public Health 106:1677–1683

    Article  PubMed  PubMed Central  Google Scholar 

  12. Firth D (1993) Bias reduction of maximum likelihood estimates. Biometrika 80:27–38

    Article  Google Scholar 

  13. Adhikary AC, Shafiqur RM (2021) Firth’s penalized method in Cox proportional hazard framework for developing predictive models for sparse or heavily censored survival data. J Stat Comput Simul 91:445–463

    Article  Google Scholar 

  14. McElwee KJ, Gilhar A, Tobin DJ, Ramot Y, Sundberg JP, Nakamura M et al (2013) What causes alopecia areata? Exp Dermatol 22:609–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kridin K, Shalom G, Comaneshter D, Cohen AD (2020) Is there an association between alopecia areata and systemic lupus erythematosus? A population-based study. Immunol Res 68:1–6

    Article  CAS  PubMed  Google Scholar 

  16. Dahir AM, Thomsen SF (2018) Comorbidities in vitiligo: comprehensive review. Int J Dermatol 57:1157–1164

    Article  PubMed  Google Scholar 

  17. Lee H, Lee M-H, Lee DY, Kang HY, Kim KH, Choi GS et al (2015) Prevalence of vitiligo and associated comorbidities in Korea. Yonsei Med J 56:719–725

    Article  PubMed  PubMed Central  Google Scholar 

  18. Chen YT, Chen YJ, Hwang CY, Lin MW, Chen TJ, Chen CC et al (2015) Comorbidity profiles in association with vitiligo: a nationwide population-based study in Taiwan. J Eur Acad Dermatol Venereol 29:1362–1369

    Article  CAS  PubMed  Google Scholar 

  19. Liu JB, Li M, Yang S, Gui JP, Wang HY, Du WH et al (2005) Clinical profiles of vitiligo in China: an analysis of 3742 patients. Clin Exp Dermatol 30:327–331

    Article  PubMed  Google Scholar 

  20. Narita T, Oiso N, Fukai K, Kabashima K, Kawada A, Suzuki T (2011) Generalized vitiligo and associated autoimmune diseases in Japanese patients and their families. Allergol Int 60:505–508

    Article  PubMed  Google Scholar 

  21. Akay BN, Bozkir M, Anadolu Y, Gullu S (2010) Epidemiology of vitiligo, associated autoimmune diseases and audiological abnormalities: Ankara study of 80 patients in Turkey. J Eur Acad Dermatol Venereol 24:1144–1150

    Article  CAS  PubMed  Google Scholar 

  22. Egeberg A, Anderson S, Edson-Heredia E, Burge R (2021) Comorbidities of alopecia areata: a population-based cohort study. Clin Exp Dermatol 46:651–656

    Article  CAS  PubMed  Google Scholar 

  23. Gade VKV, Mony A, Munisamy M, Chandrashekar L, Rajappa M (2018) An investigation of vitamin D status in alopecia areata. Clin Exp Med 18:577–584

    Article  CAS  PubMed  Google Scholar 

  24. Rossi A, Muscianese M, Federico A, Magri F, Caro G, Fortuna MC et al (2020) Associations between alopecia areata and multiple sclerosis: a report of two cases and review of the literature. Int J Dermatol 59:490–493

    Article  PubMed  Google Scholar 

  25. Alviggi C, Carrieri PB, Pivonello R, Scarano V, Pezzella M, De Placido G et al (2006) Association of pelvic endometriosis with alopecia universalis, autoimmune thyroiditis and multiple sclerosis. J Endocrinol Invest 29:182–189

    Article  CAS  PubMed  Google Scholar 

  26. Tada Y, Hamaguchi T, Ikeda Y, Kazuya T, Yamada M (2017) Multiple sclerosis and alopecia areata. J Neurol Sci 381:1064

    Article  Google Scholar 

  27. Zimmermann J, Buhl T, Müller M (2017) Alopecia universalis following alemtuzumab treatment in multiple sclerosis: a barely recognized manifestation of secondary autoimmunity-report of a case and review of the literature. Front Neurol 8:569

    Article  PubMed  PubMed Central  Google Scholar 

  28. Alcalá C, Pzére-Miralles F, Gascón F, Evole M, Estutia M, Gil-Perotín S et al (2019) Recurrent and universal alopecia areata following alemtuzumab treatment in multiple sclerosis: a secondary autoimmune disease. Mult Scler Relat Disord 27:406–408

    Article  PubMed  Google Scholar 

  29. Rolfes L, Pfeuffer S, Hackert J, Pawlitzki M, Ruck T, Sondermann W et al (2021) Skin reactions in patients with multiple sclerosis receiving cladribine treatment. Neurol Neuroimmunol Neuroinflamm 8:e990

    Article  PubMed  PubMed Central  Google Scholar 

  30. Chin LD, AbuHilal M (2020) Ocrelizumab-induced alopecia areata-A series of five patients from Ontario, Canada: a case report. SAGE Open Med Case Rep. 8:2050313x20919614

    PubMed  PubMed Central  Google Scholar 

  31. Béné J, Moulis G, Auffret M, Lefevre G, Coquerelle P, Coupe P et al (2014) Alopecia induced by tumour necrosis factor-alpha antagonists: description of 52 cases and disproportionality analysis in a nationwide pharmacovigilance database. Rheumatology 53:1465–1469

    Article  PubMed  Google Scholar 

  32. Lee HH, Gwillim E, Patel KR, Hua T, Rastogi S, Ibler E et al (2019) Epidemiology of alopecia areata, ophiasis, totalis and universalis: a systematic review and meta-analysis. J Am Acad Dermatol 82:675–682

    Article  PubMed  Google Scholar 

  33. Han TY, Lee JH, Noh TK, Choi MW, Yun J-S, Lee KH et al (2018) Alopecia areata and overt thyroid diseases: a nationwide population-based study. J Dermatol 45:1411–1417

    Article  PubMed  Google Scholar 

  34. Dai Y-X, Tai Y-H, Chang Y-T, Chen T-J, Chen M-H (2021) Bidirectional association between alopecia areata and thyroid diseases: a nationwide population-based cohort study. Arch Dermatol Res 313:339–346

    Article  PubMed  Google Scholar 

  35. Senna M, Ko J, Tosti A, Edson-Heredia E, Fenske DC, Ellinwood AK et al (2021) Alopecia Areata treatment patterns, healthcare resource utilization, and comorbidities in the US population using insurance claims. Adv Ther 38:4646–4658

    Article  PubMed  PubMed Central  Google Scholar 

  36. Maghfour J, Olson J, Conic RR, Mesinkovska NA (2021) The association between alopecia and inflammatory bowel disease: a systematic review and meta-analysis. Dermatology 237:658–672

    Article  PubMed  Google Scholar 

  37. Kim M, Choi KH, Hwang SW, Lee YB, Park HJ, Bae JM (2017) Inflammatory bowel disease is associated with an increased risk of inflammatory skin diseases: a population-based cross-sectional study. J Am Acad Dermatol 76:40–48

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the contribution to this study from central cancer registries supported through the Centers for Disease Control and Prevention’s National Program of Cancer Registries (NPCR) and/or the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) Program. Central registries may also be supported by state agencies, universities, and cancer centers. Participating central cancer registries include the following: Alabama, Alaska, Arizona, Arkansas, California, Colorado, Connecticut, Delaware, Florida, Georgia, Hawaii, Idaho, Indiana, Iowa, Kentucky, Louisiana, Massachusetts, Maine, Maryland, Michigan, Mississippi, Montana, Nebraska, Nevada, New Hampshire, New Jersey, New Mexico, New York, North Carolina, North Dakota, Ohio, Oklahoma, Oregon, Pennsylvania, Puerto Rico, Rhode Island, Seattle SEER Registry, South Carolina, Tennessee, Texas, Utah, Virginia, West Virginia, Wyoming.

Funding

This work was funded by National Institutes of Health (NIH) Grant UM1 CA186107 and Pfizer Investigator Sponsored Research (ISR) grant.

Author information

Authors and Affiliations

  1. The Warren Alpert Medical School of Brown University, Providence, RI, USA

    Isabelle H. Moseley, Elisabeth A. George & Sara D. Ragi

  2. Department of Dermatology, The Warren Alpert Medical School, Brown University, The Warren Alpert Medical School of Brown University, 339 Eddy Street, Providence, RI, 02903, USA

    Jordan M. Thompson, Anthony M. Reginato, Abrar Qureshi & Eunyoung Cho

  3. Channing Division of Network Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Jae H. Kang & Eunyoung Cho

  4. Division of Rheumatology, The Warren Alpert Medical School of Brown University, Providence, RI, USA

    Anthony M. Reginato

  5. Department of Epidemiology, School of Public Health, Brown University, Providence, RI, USA

    Abrar Qureshi & Eunyoung Cho

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  1. Isabelle H. Moseley
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  8. Eunyoung Cho
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Contributions

Conceptualization: EC, EAG, JMT; formal analysis: EC, JHK; writing—original draft: IHM, EAG, JMT, SDR; writing—editing: IHM; JMT; EAG; SDR; JHK; AMR; AQ; EC.

Corresponding author

Correspondence to Eunyoung Cho.

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Conflict of interest

The authors declare that there are no conflicts of interest to report.

IRB approval status

The study protocol was approved by the institutional review boards of the Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health, and those of participating registries as required.

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Moseley, I.H., Thompson, J.M., George, E.A. et al. Immune-mediated diseases and subsequent risk of alopecia areata in a prospective study of US women. Arch Dermatol Res 315, 807–813 (2023). https://doi.org/10.1007/s00403-022-02444-x

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  • DOI: https://doi.org/10.1007/s00403-022-02444-x

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