Skip to main content
SpringerLink
Log in

Association Between Inflammatory Skin Disease and Cardiovascular and Cerebrovascular Co-Morbidities in US Adults: Analysis of Nationwide Inpatient Sample Data

  • Original Research Article
  • Published:
American Journal of Clinical Dermatology Aims and scope Submit manuscript

Abstract

Background

Psoriasis, atopic dermatitis or eczema (AD-E), pemphigus, bullous pemphigoid (BP), and hidradenitis are chronic inflammatory skin disorders associated with systemic immune activation, considerable symptom burden, stigma, functional disturbances, and mental health symptoms. All of these might increase cardiovascular risk.

Objective

The objective of this study was to determine whether these inflammatory skin diseases are associated with increased cardiovascular/cerebrovascular risk and/or disease.

Methods

We analyzed data from the 2002–2012 National Inpatient Sample, including a representative 20% sample of all US hospitalizations (n = 72,108,077 adults).

Results

In multivariate logistic regression models with propensity score matching, patients hospitalized with versus without a diagnosis the inflammatory skin diseases examined had higher odds of obesity (odds ratio [95% confidence interval] for pemphigus: 1.16 [1.05–1.29]; BP 1.14 [1.06–1.23]; AD-E: 1.82 [1.79–1.86]; psoriasis: 2.36 [2.32–2.41]; hidradenitis: 2.79 [2.59–3.01]). Inflammatory skin disease was also associated with significantly higher odds of different cardiovascular risk factors, including hypertension (pemphigus: 1.39 [1.31–1.48]; BP 1.96 [1.88–2.05]; AD-E: 1.19 [1.17–1.21]; psoriasis: 1.61 [1.59–1.64]), and diabetes mellitus with complications (pemphigus: 1.34 [1.18–1.52]; BP: 2.06 [1.90–2.24]; AD-E: 1.13 [1.10–1.17]; psoriasis: 1.39 [1.35–1.44]), as well as vascular, cardiovascular, and cerebrovascular disease, including peripheral vascular disease (pemphigus: 1.14 [1.00–1.30]; BP: 1.83 [1.69–1.98]; AD-E: 1.18 [1.14–1.22]; psoriasis: 1.32 [1.28–1.35]), peripheral and visceral atherosclerosis (BP: 1.67 [1.53–1.81]; AD-E: 1.16 [1.12–1.20]; psoriasis: 1.27 [1.24–1.30]), pulmonary circulation disorders (pemphigus: 1.67 [1.39–2.01]; BP: 2.17 [1.92–2.45]; AD-E: 1.39 [1.33–1.45]; psoriasis: 1.37 [1.31–1.43]), congestive heart failure (pemphigus: 1.75 [1.60–1.90]; BP: 2.82 [2.68–2.98]; AD-E: 1.10 [1.07–1.13]; psoriasis: 1.05 [1.02–1.07]), history of transient ischemic attack (pemphigus: 1.36 [1.14–1.62]; BP: 2.03 [1.83–2.26]; AD-E: 1.19 [1.15–1.23]; psoriasis: 1.31 [1.26–1.36]), and cerebrovascular disease. In stratified analyses, multiple inflammatory skin diseases were associated with significantly higher rates of obesity, hypertension, and/or diabetes in patients aged <50 years and females.

Conclusions

Psoriasis, pemphigus, BP, AD-E, and hidradenitis were all associated with increased cardiovascular and cerebrovascular risk, especially at younger age.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Hsu DY, Gordon K, Silverberg JI. The inpatient burden of psoriasis in the United States. J Am Acad Dermatol. 2016;75(1):33–41.

    Article  PubMed  Google Scholar 

  2. Silverberg JI. Health care utilization, patient costs, and access to care in US adults with eczema: a population-based study. JAMA Dermatol. 2015;151(7):743–52.

    Article  PubMed  Google Scholar 

  3. Hsu D, Brieva J, Silverberg JI. Costs of care for hospitalization for pemphigus in the United States. JAMA Dermatol. 2016;152(6):645–54.

    Article  PubMed  Google Scholar 

  4. Ren Z, Hsu D, Brieva J, Silverberg N, Langan S, Silverberg J. Hospitalization, inpatient burden and comorbidities associated with bullous pemphigoid in the USA. Br J Dermatol. 2017;176(1):87–99.

    Article  CAS  PubMed  Google Scholar 

  5. Desai N, Shah P. High burden of hospital resource utilisation in patients with hidradenitis suppurativa in England: a retrospective cohort study using hospital episode statistics. Br J Dermatol. 2017;176(4):1048–55.

    Article  CAS  PubMed  Google Scholar 

  6. Miller IM, Ellervik C, Yazdanyar S, Jemec GB. Meta-analysis of psoriasis, cardiovascular disease, and associated risk factors. J Am Acad Dermatol. 2013;69(6):1014–24.

    Article  PubMed  Google Scholar 

  7. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of psoriasis. Nature. 2007;445(7130):866–73.

    Article  CAS  PubMed  Google Scholar 

  8. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352(16):1685–95.

    Article  CAS  PubMed  Google Scholar 

  9. Silverberg JI, Becker L, Kwasny M, Menter A, Cordoro KM, Paller AS. Central obesity and high blood pressure in pediatric patients with atopic dermatitis. JAMA Dermatol. 2015;151(2):144–52.

    Article  PubMed  Google Scholar 

  10. Silverberg JI, Greenland P. Eczema and cardiovascular risk factors in 2 US adult population studies. J Allergy Clin Immunol. 2015;135(3):721–8.e6.

  11. Silverberg JI. Association between adult atopic dermatitis, cardiovascular disease, and increased heart attacks in three population-based studies. Allergy. 2015;70(10):1300–8.

    Article  CAS  PubMed  Google Scholar 

  12. Zhang A, Silverberg JI. Association of atopic dermatitis with being overweight and obese: a systematic review and metaanalysis. J Am Acad Dermatol. 2015;72(4):606–16.e4.

  13. Ambiel MV, Roselino AM. Prevalence of metabolic syndrome and its components in a Brazilian sample of pemphigus patients. An Bras Dermatol. 2014;89(5):752–6.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Forsti AK, Jokelainen J, Timonen M, Tasanen K. Risk of death in bullous pemphigoid: a retrospective database study in Finland. Acta Derm Venereol. 2016;96(6):758–61.

    PubMed  Google Scholar 

  15. Kibsgaard L, Bay B, Deleuran M, Vestergaard C. A retrospective consecutive case-series study on the effect of systemic treatment, length of admission time, and co-morbidities in 98 bullous pemphigoid patients admitted to a tertiary centre. Acta Derm Venereol. 2015;95(3):307–11.

    Article  PubMed  Google Scholar 

  16. Cai SC, Allen JC, Lim YL, Chua SH, Tan SH, Tang MB. Mortality of bullous pemphigoid in Singapore: risk factors and causes of death in 359 patients seen at the National Skin Centre. Br J Dermatol. 2014;170(6):1319–26.

    Article  CAS  PubMed  Google Scholar 

  17. Tzellos T, Zouboulis CC, Gulliver W, Cohen AD, Wolkenstein P, Jemec GB. Cardiovascular disease risk factors in patients with hidradenitis suppurativa: a systematic review and meta-analysis of observational studies. Br J Dermatol. 2015;173(5):1142–55.

    Article  CAS  PubMed  Google Scholar 

  18. Kouris A, Platsidaki E, Christodoulou C, Armyra K, Korkoliakou P, Stefanaki C, et al. Quality of life, depression, anxiety and loneliness in patients with bullous pemphigoid. A case control study. An Bras Dermatol. 2016;91(5):601–3.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Blome C, Radtke MA, Eissing L, Augustin M. Quality of life in patients with atopic dermatitis: disease burden, measurement, and treatment benefit. Am J Clin Dermatol. 2016;17(2):163–9.

    Article  PubMed  Google Scholar 

  20. Gooderham M, Papp K. The psychosocial impact of hidradenitis suppurativa. J Am Acad Dermatol. 2015;73(5 Suppl 1):S19–22.

    Article  PubMed  Google Scholar 

  21. Rencz F, Gulacsi L, Tamasi B, Karpati S, Pentek M, Baji P, et al. Health-related quality of life and its determinants in pemphigus: a systematic review and meta-analysis. Br J Dermatol. 2015;173(4):1076–80.

    Article  CAS  PubMed  Google Scholar 

  22. de Korte J, Sprangers MA, Mombers FM, Bos JD. Quality of life in patients with psoriasis: a systematic literature review. J Investig Dermatol Symp Proc. 2004;9(2):140–7.

    Article  PubMed  Google Scholar 

  23. Kramer U, Schafer T, Behrendt H, Ring J. The influence of cultural and educational factors on the validity of symptom and diagnosis questions for atopic eczema. Br J Dermatol. 1998;139(6):1040–6.

    Article  CAS  PubMed  Google Scholar 

  24. ICD-9-CM coding and reporting official guidelines. American Hospital Association, American Medical Record Association, Health Care Financing Administration, National Center for Health Statistics. J Am Med Rec Assoc. 1990;61(10):suppl 1–17.

  25. Hsu D, Brieva J, Nardone B, Silverberg JI. Validation of database search strategies for the epidemiological study of pemphigus and pemphigoid. Br J Dermatol. 2016;174(3):645–8.

    Article  CAS  PubMed  Google Scholar 

  26. Hsu DY, Dalal P, Sable KA, Voruganti N, Nardone B, West D, et al. Validation of international classification of disease ninth revision codes for atopic dermatitis. Allergy. Epub 20 Dec 2016. doi:10.1111/all.13113.

  27. Icen M, Crowson CS, McEvoy MT, Gabriel SE, Kremers HM. Potential misclassification of patients with psoriasis in electronic databases. J Am Acad Dermatol. 2008;59(6):981–5.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Asgari MM, Wu JJ, Gelfand JM, Salman C, Curtis JR, Harrold LR, et al. Validity of diagnostic codes and prevalence of psoriasis and psoriatic arthritis in a managed care population, 1996–2009. Pharmacoepidemiol Drug Saf. 2013;22(8):842–9.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kim G, Shlyankevich J, Kimball A. The validity of the diagnostic code for hidradenitis suppurativa in an electronic database. Br J Dermatol. 2014;171(2):338–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Vena GA, Vestita M, Cassano N. Psoriasis and cardiovascular disease. Dermatol Ther. 2010;23(2):144–51.

    Article  PubMed  Google Scholar 

  31. Kupetsky EA, Mathers AR, Ferris LK. Anti-cytokine therapy in the treatment of psoriasis. Cytokine. 2013;61(3):704–12.

    Article  CAS  PubMed  Google Scholar 

  32. Koga C, Kabashima K, Shiraishi N, Kobayashi M, Tokura Y. Possible pathogenic role of Th17 cells for atopic dermatitis. J Invest Dermatol. 2008;128(11):2625–30.

    Article  CAS  PubMed  Google Scholar 

  33. Suarez-Farinas M, Dhingra N, Gittler J, Shemer A, Cardinale I, de Guzman Strong C, et al. Intrinsic atopic dermatitis shows similar TH2 and higher TH17 immune activation compared with extrinsic atopic dermatitis. J Allergy Clin Immunol. 2013;132(2):361–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Xue J, Su W, Chen Z, Ke Y, Du X, Zhou Q. Overexpression of interleukin-23 and interleukin-17 in the lesion of pemphigus vulgaris: a preliminary study. Mediators Inflamm. 2014;2014:463928.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Zebrowska A, Wagrowska-Danilewicz M, Danilewicz M, Stasikowska-Kanicka O, Cynkier A, Sysa-Jedrzejowska A, et al. IL-17 expression in dermatitis herpetiformis and bullous pemphigoid. Mediators Inflamm. 2013;2013:967987.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Martin-Ezquerra G, Masferrer E, Pujol RM. Use of biological treatments in patients with hidradenitis suppurativa. G Ital Dermatol Venereol. Epub 16 Dec 2016.

  37. Dowlatshahi EA, van der Voort EA, Arends LR, Nijsten T. Markers of systemic inflammation in psoriasis: a systematic review and meta-analysis. Br J Dermatol. 2013;169(2):266–82.

    Article  CAS  PubMed  Google Scholar 

  38. van der Zee HH, de Ruiter L, van den Broecke DG, Dik WA, Laman JD, Prens EP. Elevated levels of tumour necrosis factor (TNF)-alpha, interleukin (IL)-1beta and IL-10 in hidradenitis suppurativa skin: a rationale for targeting TNF-alpha and IL-1beta. Br J Dermatol. 2011;164(6):1292–8.

    Article  PubMed  Google Scholar 

  39. Khozeimeh F, Savabi O, Esnaashari M. Evaluation of interleukin-1alpha, interleukin-10, tumor necrosis factor-alpha and transforming growth factor-beta in the serum of patients with pemphigus vulgaris. J Contemp Dent Pract. 2014;15(6):746–9.

    Article  PubMed  Google Scholar 

  40. Alecu M, Alecu S, Coman G, Galatescu E, Ursaciuc C. ICAM-1, ELAM-1, TNF-alpha and IL-6 in serum and blister liquid of pemphigus vulgaris patients. Roum Arch Microbiol Immunol. 1999;58(2):121–30.

    CAS  PubMed  Google Scholar 

  41. Ameglio F, D’Auria L, Cordiali-Fei P, Mussi A, Valenzano L, D’Agosto G, et al. Bullous pemphigoid and pemphigus vulgaris: correlated behaviour of serum VEGF, sE-selectin and TNF-alpha levels. J Biol Regul Homeost Agents. 1997;11(4):148–53.

    CAS  PubMed  Google Scholar 

  42. Guttman-Yassky E, Nograles KE, Krueger JG. Contrasting pathogenesis of atopic dermatitis and psoriasis–part II: immune cell subsets and therapeutic concepts. J Allergy Clin Immunol. 2011;127(6):1420–32.

    Article  CAS  PubMed  Google Scholar 

  43. Sampogna F, Picardi A, Chren M-M, Melchi CF, Pasquini P, Masini C, et al. Association between poorer quality of life and psychiatric morbidity in patients with different dermatological conditions. Psychosom Med. 2004;66(4):620–4.

    Article  PubMed  Google Scholar 

  44. Armstrong AW, Harskamp CT, Dhillon JS, Armstrong EJ. Psoriasis and smoking: a systematic review and meta-analysis. Br J Dermatol. 2014;170(2):304–14.

    Article  CAS  PubMed  Google Scholar 

  45. Kantor R, Kim A, Thyssen JP, Silverberg JI. Association of atopic dermatitis with smoking: a systematic review and meta-analysis. J Am Acad Dermatol. 2016;75(6):1119–25 e1.

  46. Miller IM, McAndrew RJ, Hamzavi I. Prevalence, risk factors, and comorbidities of hidradenitis suppurativa. Dermatol Clin. 2016;34(1):7–16.

    Article  CAS  PubMed  Google Scholar 

  47. Bakhshi M, Manifar S, Azizi N, Asayesh H, Mansouri P, Nasiri S, et al. Risk factors in patients with oral pemphigus vulgaris: a case–control study. Gen Dent. 2016;64(3):e10–3.

    PubMed  Google Scholar 

  48. Wohl Y, Mashiah J, Kutz A, Hadj-Rabia S, Cohen AD. Pemphigus and depression comorbidity: a case control study. Eur J Dermatol. 2015;25(6):602–5.

    CAS  PubMed  Google Scholar 

  49. Wohl Y, Mashiah J, Kutz A, Hadj-Rabia S, Cohen AD. Pemphigus and depression comorbidity: a case control study. Eur J Dermatol. 2015;25(6):602–5.

    CAS  PubMed  Google Scholar 

  50. Do YK, Lakhani N, Malhotra R, Halstater B, Theng C, Østbye T. Association between psoriasis and leisure-time physical activity: findings from the National Health and Nutrition Examination Survey. J Dermatol. 2015;42(2):148–53.

    Article  PubMed  Google Scholar 

  51. Torres T, Alexandre JM, Mendonça D, Vasconcelos C, Silva BM, Selores M. Levels of physical activity in patients with severe psoriasis: a cross-sectional questionnaire study. Am J Clin Dermatol. 2014;15(2):129–35.

    Article  PubMed  Google Scholar 

  52. Wilson P, Bohjanen K, Ingraham S, Leon A. Psoriasis and physical activity: a review. J Eur Acad Dermatol Venereol. 2012;26(11):1345–53.

    Article  CAS  PubMed  Google Scholar 

  53. Strom MA, Silverberg JI. Associations of physical activity and sedentary behavior with atopic disease in United States children. J Pediatr. 2016;174(247–53):e3.

    Google Scholar 

  54. Silverberg JI, Song J, Pinto D, Sherry HY, Gilbert AL, Dunlop DD, et al. Atopic dermatitis is associated with less physical activity in US adults. J Invest Dermatol. 2016;136(8):1714–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Kim A, Silverberg JI. A systematic review of vigorous physical activity in eczema. Br J Dermatol. 2016;174(3):660–2.

    Article  CAS  PubMed  Google Scholar 

  56. Hsu DY, Gordon K, Silverberg JI. The inpatient burden of psoriasis in the United States. J Am Acad Dermatol. 2016;75(1):33–41.

    Article  PubMed  Google Scholar 

  57. Narla S, Hsu DY, Thyssen JP, Silverberg JI. Inpatient financial burden of atopic dermatitis in the United States. J Invest Dermatol. Epub 1 Mar 2017. doi:10.1016/j.jid.2017.02.975.

Download references

Author information

Authors and Affiliations

  1. Department of Dermatology, Northwestern University Feinberg School of Medicine, Suite 1600, 676 N. St. Clair St., Chicago, IL, 60611, USA

    Michael C. Kwa & Jonathan I. Silverberg

  2. Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL, 60611, USA

    Jonathan I. Silverberg

  3. Department of Medical Social Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL, 60611, USA

    Jonathan I. Silverberg

  4. Northwestern Medicine Multidisciplinary Eczema Center, Chicago, IL, 60611, USA

    Jonathan I. Silverberg

Authors
  1. Michael C. Kwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan I. Silverberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.I. Silverberg had full access to all the data in the study and takes responsibility for the integrity of the data and accuracy of the data analysis. J.I. Silverberg was involved in the study concept and design; and obtained the funding. J.I. Silverberg and M. Kwa were responsible for the acquisition of data; analysis and interpretation of data; drafting of the manuscript; critical revision of the manuscript for important intellectual content; and statistical analysis.

Corresponding author

Correspondence to Jonathan I. Silverberg.

Ethics declarations

Funding support

This publication was made possible with support from the Agency for Healthcare Research and Quality (AHRQ), Grant Number K12 HS023011, and the Dermatology Foundation. The AHRQ was not involved in the design and conduct of the study; collection, management, analysis, and interpretation of data; preparation, review, or approval of the manuscript; or the decision to submit the manuscript for publication.

Conflict of interest

J.I. Silverberg and M. Kwa have no relevant conflicts of interest to declare.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kwa, M.C., Silverberg, J.I. Association Between Inflammatory Skin Disease and Cardiovascular and Cerebrovascular Co-Morbidities in US Adults: Analysis of Nationwide Inpatient Sample Data. Am J Clin Dermatol 18, 813–823 (2017). https://doi.org/10.1007/s40257-017-0293-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40257-017-0293-x

Search

Navigation