Abstract
Cardiology, dermatology, and rheumatology form a fascinating triad. Many skin and joint disorders are associated with cardiovascular comorbidities because they share etiologic elements. Female predominance is often remarkable and likely related to autoimmune pathology. Although studies have shown that X-encoded genes may be involved in the differences in immunity between males and females, other studies have also shown that sex chromosomes are irrelevant and that estrogens and androgens are responsible for the differences. The elevated immune activity in females provides a beneficial position in coping with a pathogenic stimulus but may also enhance their susceptibility to autoimmunity. The complexity of the immune system and its role as a defensive force against infection requires an armamentarium to precisely identify and selectively control inflammatory processes or cells which promote atherosclerosis. On the other hand, the inflammation in skin diseases seems to be an active source of diverse proinflammatory cytokines and chemokines which can predispose to cardiovascular comorbidities. Also, it has been shown that comorbidity disproportionately accelerates risk in women.
The skin offers a readily available window to facilitate detection of risk factors or even to assist the diagnostic process regarding a variety of disorders, including those with cardiovascular involvement. Current imaging techniques provide exquisite capabilities for diagnosing and possibly even counteracting atherosclerotic plaque formation, before serious cardiovascular events occur. Combining imaging approaches (such as videocapillaroscopy, intravascular ultrasound, and FDG positron emission tomography) with insights based on immunology will likely accelerate advances in this area.
We review major dermatologic manifestations and rheumatologic disorders which are associated with cardiac and vascular abnormalities. In particular we discuss sex-specific aspects concerning incidence and severity of cardiovascular disease associated with systemic sclerosis, rheumatoid arthritis, systemic lupus erythematosus, psoriasis, atopic dermatitis, and hidradenitis suppurativa.
Keywords
- Cardio-dermatology
- Sex-specific risk factors
- Heart failure
- Stroke
- Psoriasis
- Atopic dermatitis
- Hidradenitis suppurativa
- Systemic sclerosis
- Systemic lupus erythematosus
- Rheumatoid arthritis
- Ankylosing spondylitis
- Inflammatory bowel disease
- Rosacea
- Immune-mediated inflammatory disease
- Ischemic heart disease
- Inflammasome
- Neutrophil extracellular trap
- Inflammation imaging
- Sex hormones
- Pulse wave velocity
- Carotid intima-media thickness
- Nailfold videocapillaroscopy
- PET scan
- Review
Primary Raynaud’s phenomenon and nailfold videocapillaroscopy. Example of irregular, apical, and venous branch dilations, as well as presence of microhemorrhages. Normal capillaries are also visible (magnification ×200). Reproduced from Pizzorni et al. Clin Rheumatol. 2017;36: 1637–1642, with permission.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Ahlehoff O, Skov L, Gislason G, Gniadecki R, Iversen L, Bryld LE, Lasthein S, Lindhardsen J, Kristensen SL, Torp-Pedersen C, Hansen PR. Cardiovascular outcomes and systemic anti-inflammatory drugs in patients with severe psoriasis: 5-year follow-up of a Danish nationwide cohort. J Eur Acad Dermatol Venereol. 2015;29(6):1128–34. https://doi.org/10.1111/jdv.12768.
Andersen LK, Davis MDP. Sex differences in the incidence of skin and skin-related diseases in Olmsted County, Minnesota, United States, and a comparison with other rates published worldwide. Int J Dermatol. 2016;55(9):939–55. https://doi.org/10.1111/ijd.13285.
Avena-Woods C. Overview of atopic dermatitis. Am J Manag Care. 2017;23(8 Suppl):S115–23.
Avolio AP, Kuznetsova T, Heyndrickx GR, Kerkhof PLM, Li JK-J. Arterial flow, pulse pressure and pulse wave velocity in men and women at various ages. In: Kerkhof PLM, Miller VM, editors. Sex-specific analysis of cardiovascular function. New York: Springer; 2018. https://doi.org/10.1007/978-3-319-77932-4_10.
Barbarot S, Auziere S, Gadkari A, Girolomoni G, Puig L, Simpson EL, Margolis DJ, de Bruin-Weller M, Eckert L. Epidemiology of atopic dermatitis in adults: results from an international survey. Allergy. 2018. doi: https://doi.org/10.1111/all.13401.
Bairey Merz CN, Shaw LJ, Reis SE, et al. Insights from the NHLBI-Sponsored Women’s Ischemia Syndrome Evaluation (WISE) Study: Part II: gender differences in presentation, diagnosis, and outcome with regard to gender-based pathophysiology of atherosclerosis and macrovascular and microvascular coronary disease. J Am Coll Cardiol. 2006;47(3 Suppl):S21–9.
Belli AA, Altun I, Altun I. Rosacea patients had significantly higher epicardial fat thickness and carotid intima-media thickness volumes than controls. An Bras Dermatol. 2017;92(6):820–5. https://doi.org/10.1590/abd1806-4841.20176832.
Benacka O, Benacka J, Blazicek P, Belansky M, Payer J, Killinger Z, Lietava J. Speckle tracking can detect subclinical myocardial dysfunction in rheumatoid arthritis patients. Bratisl Lek Listy. 2017;118(1):28–33. https://doi.org/10.4149/BLL_2017_006.
Beretta L, Caronni M, Origgi L, Ponti A, Santaniello A, Scorza R. Hormone replacement therapy may prevent the development of isolated pulmonary hypertension in patients with systemic sclerosis and limited cutaneous involvement. Scand J Rheumatol. 2006;35:468–71.
Bergman M, Lundholm A. Mitigation of disease- and treatment-related risks in patients with psoriatic arthritis. Arthritis Res Ther. 2017;19(1):63. https://doi.org/10.1186/s13075-017-1265-5.
Biesbroek PS, Heslinga SC, Konings TC, van der Horst-Bruinsma IE, Hofman MBM, van de Ven PM, Kamp O, van Halm VP, Peters MJL, Smulders YM, van Rossum AC, Nurmohamed MT, Nijveldt R. Insights into cardiac involvement in ankylosing spondylitis from cardiovascular magnetic resonance. Heart. 2017;103(10):745–52. https://doi.org/10.1136/heartjnl-2016-310667.
Biousse V, Bruce BB, Newman NJ. Ophthalmoscopy in the 21st century: the 2017 H. Houston Merritt Lecture. Neurology. 2018;90(4):167–75. https://doi.org/10.1212/WNL.0000000000004868.
Boehncke WH, Boehncke S, Tobin AM, Kirby B. The ‘psoriatic march’: a concept of how severe psoriasis may drive cardiovascular comorbidity. Exp Dermatol. 2011;20:303–7.
Brunner PM, Suárez-Fariñas M, He H, Malik K, et al. The atopic dermatitis blood signature is characterized by increases in inflammatory and cardiovascular risk proteins. Sci Rep. 2017;7(1):8707. https://doi.org/10.1038/s41598-017-09207-z.
Croca SC, Rahman A. Imaging assessment of cardiovascular disease in systemic lupus erythematosus. Clin Dev Immunol. 2012;2012:694143. https://doi.org/10.1155/2012/694143.
Croca S, Rahman A. Atherosclerosis in systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2017;31:364–72. https://doi.org/10.1016/j.berh.2017.09.012.
David Boothe W, Tarbox JA, Tarbox MB. Atopic dermatitis: pathophysiology. Adv Exp Med Biol. 2017;1027:21–37. https://doi.org/10.1007/978-3-319-64804-0_3.
Damen MSMA, Popa CD, Netea MG, Dinarello CA, Joosten LAB. Interleukin-32 in chronic inflammatory conditions is associated with a higher risk of cardiovascular diseases. Atherosclerosis. 2017;264:83–91. https://doi.org/10.1016/j.atherosclerosis.2017.07.005.
Davidovici BB, Sattar N, Prinz J, Puig L, Emery P, Barker JN, van de Kerkhof P, Ståhle M, Nestle FO, Girolomoni G, Krueger JG. Psoriasis and systemic inflammatory diseases: potential mechanistic links between skin disease and co-morbid conditions. J Invest Dermatol. 2010;130:1785–96.
Deckers IE, Benhadou F, Koldijk MJ, Del Marmol V, Horváth B, Boer J, van der Zee HH, Prens EP. Inflammatory bowel disease is associated with hidradenitis suppurativa: results from a multicenter cross-sectional study. J Am Acad Dermatol. 2017;76(1):49–53. https://doi.org/10.1016/j.jaad.2016.08.031.
Dregan A. Arterial stiffness association with chronic inflammatory disorders in the UK Biobank study. Heart. 2018. pii: heartjnl-2017-312610. doi:https://doi.org/10.1136/heartjnl-2017-312610.
Dzieża-Grudnik A, Sulicka J, Strach M, et al. Arterial stiffness is not increased in patients with short duration rheumatoid arthritis and ankylosing spondylitis. Blood Press. 2017;26:115–21.
Egeberg A, Gislason GH, Hansen PR. Risk of major adverse cardiovascular events and all-cause mortality in patients with hidradenitis suppurativa. JAMA Dermatol. 2016;152(4):429–34. https://doi.org/10.1001/jamadermatol.2015.6264.
Egeberg A, Skov L, Joshi AA, Mallbris L, Gislason GH, Wu JJ, Rodante J, Lerman JB, Ahlman MA, Gelfand JM, Mehta NN. The relationship between duration of psoriasis, vascular inflammation, and cardiovascular events. J Am Acad Dermatol. 2017;77:650–656.e3. https://doi.org/10.1016/j.jaad.2017.06.028.
Furue M, Kadono T. “Inflammatory skin march” in atopic dermatitis and psoriasis. Inflamm Res. 2017;66(10):833–42. https://doi.org/10.1007/s00011-017-1065-z.
Gabrielli A, Avvedimento EV, Krieg T. Mechanisms of disease: scleroderma. N Engl J Med. 2009;360:1989–2003. REVIEW
Garner R, Kumari R, Lanyon P, Doherty M, Zhang W. Prevalence, risk factors and associations of primary Raynaud’s phenomenon: systematic review and meta-analysis of observational studies. BMJ Open. 2015;5(3):e006389. https://doi.org/10.1136/bmjopen-2014-006389.
Gilbert EL, Ryan MJ. Estrogen in cardiovascular disease during systemic lupus erythematosus. Clin Ther. 2014;36:1901–12. https://doi.org/10.1016/j.clinthera.2014.07.021.
González-López MA, Lacalle M, Mata C, et al. Carotid ultrasound is useful for the cardiovascular risk stratification in patients with hidradenitis suppurativa. PLoS One. 2018;13(1):e0190568. https://doi.org/10.1371/journal.pone.0190568.
Gubbels Bupp MR. Sex, the aging immune system, and chronic disease. Cell Immunol. 2015;294:102–10.
Guttman-Yassky E, Krueger JG, Lebwohl MG. Systemic immune mechanisms in atopic dermatitis and psoriasis with implications for treatment. Exp Dermatol. 2017. doi:https://doi.org/10.1111/exd.13336.
Hägg D, Sundström A, Eriksson M, Schmitt-Egenolf M. Severity of psoriasis differs between men and women: a study of the clinical outcome measure Psoriasis Area and Severity Index (PASI) in 5438 Swedish Register patients. Am J Clin Dermatol. 2017;18(4):583–90. https://doi.org/10.1007/s40257-017-0274-0.
Harden JL, Lewis SM, Lish SR, Suárez-Fariñas M, Gareau D, Lentini T, Johnson-Huang LM, Krueger JG, Lowes MA. The tryptophan metabolism enzyme L-kynureninase is a novel inflammatory factor in psoriasis and other inflammatory diseases. J Allergy Clin Immunol. 2016;137:1830–40. https://doi.org/10.1016/j.jaci.2015.09.055.
Hendriks AG, Steenbergen W, Hondebrink E, van Hespen JC, van de Kerkhof PC, Seyger MM. Whole field laser Doppler imaging of the microcirculation in psoriasis and clinically unaffected skin. J Dermatolog Treat. 2014;25:18–21. https://doi.org/10.3109/09546634.2013.777382.
Hoffman LK, Ghias MH, Garg A, Hamzavi IH, Alavi A, Lowes MA. Major gaps in understanding and treatment of hidradenitis suppurativa. Semin Cutan Med Surg. 2017;36(2):86–92. https://doi.org/10.12788/j.sder.2017.024.
Hoffman LK, Ghias MH, Lowes MA. Pathophysiology of hidradenitis suppurativa. Semin Cutan Med Surg. 2017;36(2):47–54. https://doi.org/10.12788/j.sder.2017.017.
Honma M, Shibuya T, Iwasaki T, Iinuma S, Takahashi N, Kishibe M, Minami-Hori M, Ishida-Yamamoto A. Prevalence of coronary artery calcification in Japanese patients with psoriasis: a close correlation with bilateral diagonal earlobe creases. J Dermatol. 2017;44(10):1122–8. https://doi.org/10.1111/1346-8138.13895.
Ibáñez Vodnizza S, Visman IM, van Denderen C, Lems WF, Jaime F, Nurmohamed M, van der Horst-Bruinsma IE. Muscle wasting in male TNF-α blocker naïve ankylosing spondylitis patients: a comparison of gender differences in body composition. Rheumatology (Oxford). 2017;56(9):1566–72. https://doi.org/10.1093/rheumatology/kex187.
Ishimori ML, Martin R, Berman DS, Goykhman P, Shaw LJ, Shufelt C, et al. Myocardial ischemia in the absence of obstructive coronary artery disease in systemic lupus erythematosus. JACC Cardiovasc Imaging. 2011;4(1):27–33.
Ivanovic BA, Tadic MV, Zlatanovic MM, Damjanov NN, Ostojić PM, Bonaci-Nikolic BN. Which factors impact myocardial function in systemic sclerosis? Echocardiography. 2012;29:307–17. https://doi.org/10.1111/j.1540-8175.2011.01560.x.
Karp I, Abrahamowicz M, Fortin PR, Pilote L, Neville C, Pineau CA, Esdaile JM. Longitudinal evolution of risk of coronary heart disease in systemic lupus erythematosus. J Rheumatol. 2012;39(5):968–73. https://doi.org/10.3899/jrheum.111127.
Katta R. Cutaneous sarcoidosis: a dermatologic masquerader. Am Fam Physician. 2002;65(8):1581–4.
Kim CH, Al-Kindi SG, Jandali B, Askari AD, Zacharias M, Oliveira GH. Incidence and risk of heart failure in systemic lupus erythematosus. Heart. 2017;103:227–33. https://doi.org/10.1136/heartjnl-2016-309561.
Klingenberg R, Lüscher TF. Rheumatoid arthritis and coronary atherosclerosis: two cousins engaging in a dangerous liaison. Eur Heart J. 2015;36(48):3423–5.
Kul S, Kutlu GA, Guvenc TS, Kavas M, Demircioglu K, Yilmaz Y, Yakar HI, Kanbay A, Boga S, Caliskan M. Coronary flow reserve is reduced in sarcoidosis. Atherosclerosis. 2017;264:115–21. https://doi.org/10.1016/j.atherosclerosis.2017.05.005.
Kwa L, Kwa MC, Silverberg JI. Cardiovascular comorbidities of pediatric psoriasis among hospitalized children in the United States. J Am Acad Dermatol. 2017;77(6):1023–9. https://doi.org/10.1016/j.jaad.2017.08.034.
Lebwohl M. Does treatment of psoriasis reduce cardiovascular comorbidities? J Invest Dermatol. 2017;137(8):1612–3. https://doi.org/10.1016/j.jid.2017.06.001.
Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868–74.
Libert C, Dejager L, Pinheiro I. The X chromosome in immune functions: when a chromosome makes the difference. Nat Rev Immunol. 2010;10:594–604. https://doi.org/10.1038/nri2815.
Lockwood MM, O’Malley PG. Admitting what we do not know in rheumatologic disease: The first step toward learning more. JAMA Intern Med. 2018. doi:https://doi.org/10.1001/jamainternmed.2017.8557.
Lowes MA, Suárez-Fariñas M, Krueger JG. Immunology of psoriasis. Annu Rev Immunol 2014;32:227–55. doi: https://doi.org/10.1146/annurev-immunol-032713-120225. Review. PMID: 24655295.
Magder LS, Petri M. Incidence of and risk factors for adverse cardiovascular events among patients with systemic lupus erythematosus. Am J Epidemiol. 2012;176:708–19.
Mavrogeni S, Markousis-Mavrogenis G, Koutsogeorgopoulou L, Kolovou G. Cardiovascular magnetic resonance imaging: clinical implications in the evaluation of connective tissue diseases. J Inflamm Res. 2017;10:55–61. https://doi.org/10.2147/JIR.S115508. eCollection 2017
Nestle FO, Kaplan DH, Barker J. Psoriasis. N Engl J Med. 2009;361:496–509. https://doi.org/10.1056/NEJMra0804595.
Nijsten T. Atopic dermatitis and comorbidities: added value of comprehensive dermatoepidemiology. J Invest Dermatol. 2017;137(5):1009–11. https://doi.org/10.1016/j.jid.2017.02.003.
Nurmohamed MT, Heslinga M, Kitas GD. Cardiovascular comorbidity in rheumatic diseases. Nat Rev Rheumatol. 2015;11:693–704. https://doi.org/10.1038/nrrheum.2015.112.
Nussinovitch, editor. The heart in rheumatic, autoimmune and inflammatory diseases. London: Academic Press; 2017.
O’Callaghan KM. Solutions for disparities for women with heart disease. J Cardiovasc Transl Res. 2009;2(4):518–25. https://doi.org/10.1007/s12265-009-9125-6.
Osto E, Piaserico S, Maddalozzo A, Forchetti G, Montisci R, Famoso G, Giovagnoni A, Peserico A, Iliceto S, Tona F. Impaired coronary flow reserve in young patients affected by severe psoriasis. Atherosclerosis. 2012;221(1):113–7. https://doi.org/10.1016/j.atherosclerosis.2011.12.015.
Phinikaridou A, Andia ME, Passacquale G, Ferro A, Botnar RM. Noninvasive MRI monitoring of the effect of interventions on endothelial permeability in murine atherosclerosis using an albumin-binding contrast agent. J Am Heart Assoc. 2013;2(5):e000402. https://doi.org/10.1161/JAHA.113.000402.
Pizzorni C, Sulli A, Smith V, Ruaro B, Trombetta AC, Cutolo M, Paolino S. Primary Raynaud’s phenomenon and nailfold videocapillaroscopy: age-related changes in capillary morphology. Clin Rheumatol. 2017;36(7):1637–42. https://doi.org/10.1007/s10067-016-3442-3.
Prens E, Deckers I. Pathophysiology of hidradenitis suppurativa: an update. J Am Acad Dermatol 2015;73(5 Suppl 1):S8–11. doi: https://doi.org/10.1016/j.jaad.2015.07.045. Review. PMID: 26470623.
Ritchlin CT, Colbert RA, Gladman DD. Psoriatic arthritis. N Engl J Med. 2017;376(21):2095–6. https://doi.org/10.1056/NEJMc1704342.
Robson JC, Kiran A, Maskell J, Hutchings A, Arden N, Dasgupta B, Hamilton W, Emin A, Culliford D, Luqmani R. Which patients with giant cell arteritis will develop cardiovascular or cerebrovascular disease? A Clinical Practice Research Datalink Study. J Rheumatol. 2016;43(6):1085–92. https://doi.org/10.3899/jrheum.151024.
Roshdy HS, Soliman MH, El-Dosouky II, Ghonemy S. Skin aging parameters: a window to heart block. Clin Cardiol. 2017. doi:https://doi.org/10.1002/clc.22848.
Ruaro B, Sulli A, Smith V, Pizzorni C, Paolino S, Alessandri E, Cutolo M. Microvascular damage evaluation in systemic sclerosis: the role of nailfold videocapillaroscopy and laser techniques. Reumatismo. 2017;69(4):147–55. https://doi.org/10.4081/reumatismo.2017.959.
Ryan C, Kirby B. Psoriasis is a systemic disease with multiple cardiovascular and metabolic comorbidities. Dermatol Clin. 2015;33(1):41–55. https://doi.org/10.1016/j.det.2014.09.004.
Scorza R, Caronni M, Bazzi S, Nador F, Beretta L, Antonioli R, Origgi L, Ponti A, Marchini M, Vanoli M. Post-menopause is the main risk factor for developing isolated pulmonary hypertension in systemic sclerosis. Ann N Y Acad Sci. 2002;966:238–46.
Shaw LJ, Bugiardini R, Merz CN. Women and ischemic heart disease: evolving knowledge. J Am Coll Cardiol. 2009;54(17):1561–75. https://doi.org/10.1016/j.jacc.2009.04.098.
Singh S, Michelena HI, Warrington KJ. The nails give it away. J Am Coll Cardiol. 2011;57:996. https://doi.org/10.1016/j.jacc.2010.03.111.
Sobchak C, Eder L. Cardiometabolic disorders in psoriatic disease. Curr Rheumatol Rep. 2017;19(10):63. https://doi.org/10.1007/s11926-017-0692-2.
Somers EC, Marder W, Cagnoli P, et al. Population-based incidence and prevalence of systemic lupus erythematosus: the Michigan Lupus Epidemiology and Surveillance program. Arthritis Rheumatol. 2014;66:369–78. https://doi.org/10.1002/art.38238.
Soto-Gomez N, Peters JI, Nambiar AM. Diagnosis and management of sarcoidosis. Am Fam Physician. 2016;93(10):840–8.
Sperry BW, Tamarappoo BK, Oldan JD, Javed O, Culver DA, Brunken R, Cerqueira MD, Hachamovitch R. Prognostic Impact of Extent, Severity, and Heterogeneity of Abnormalities on 18F-FDG PET Scans for Suspected Cardiac Sarcoidosis. JACC Cardiovasc Imaging. 2017. pii: S1936-878X(17)30612-5.
Tadic M, Zlatanovic M, Cuspidi C, Ivanovic B, Stevanovic A, Damjanov N, Kocijancic V, Celic V. The relationship between left ventricular deformation and heart rate variability in patients with systemic sclerosis: Two- and three-dimensional strain analysis. Int J Cardiol. 2017;236:145–50. https://doi.org/10.1016/j.ijcard.2017.02.043.
Tadic M, Cuspidi C, Vasic D, Kerkhof PLM. Cardiovascular implications of diabetes, metabolic syndrome, thyroid disease and cardio-oncology in women. In: Kerkhof PLM, Miller VM, editors. Sex-specific analysis of cardiovascular function. New York: Springer; 2018. https://doi.org/10.1007/978-3-319-77932-4_29.
Talsania M, Scofield RH. Menopause and rheumatic disease. Rheum Dis Clin N Am. 2017;43:287–302. https://doi.org/10.1016/j.rdc.2016.12.011.
Teague HL, Ahlman MA, Alavi A, et al. Unraveling vascular inflammation: from immunology to imaging. J Am Coll Cardiol. 2017;70:1403–12.
Ten Haaf ME, Rijndertse M, Cheng JM, et al. Sex differences in plaque characteristics by intravascular imaging in patients with coronary artery disease. EuroIntervention. 2017;13(3):320–8. https://doi.org/10.4244/EIJ-D-16-00361.
Thyssen JP, Halling-Overgaard AS, Andersen YMF, Gislason G, Skov L, Egeberg A. The association between cardiovascular disease and type 2 diabetes in adults with atopic dermatitis: a systematic review and meta-analysis. Br J Dermatol. 2017. https://doi.org/10.1111/bjd.16215.
Turk SA, Heslinga SC, Dekker J, Britsemmer L, van der Lugt V, Lems WF, van Schaardenburg D, Nurmohamed MT. The relationship between cardiac conduction times, cardiovascular risk factors, and inflammation in patients with early arthritis. J Rheumatol. 2017;44:580–6.
Verweij SL, Duivenvoorden R, Stiekema LCA, Nurmohamed NS, van der Valk FM, Versloot M, Verberne HJ, Stroes ESG, Nahrendorf M, Bekkering S, Bernelot Moens SJ. CCR2 expression on circulating monocytes is associated with arterial wall inflammation assessed by 18F-FDG PET/CT in patients at risk for cardiovascular disease. Cardiovasc Res. 2018;114:468–75. https://doi.org/10.1093/cvr/cvx224.
Vinkel C, Thomsen SF. Risk factors for cardiovascular disease in patients with hidradenitis suppurativa. J Eur Acad Dermatol Venereol. 2017;31(9):e411–3. https://doi.org/10.1111/jdv.14225.
Wernig G, Chen SY, Cui L, et al. Unifying mechanism for different fibrotic diseases. Proc Natl Acad Sci U S A. 2017;114:4757–62.
Wigley FM, Flavahan NA. Raynaud’s phenomenon. N Engl J Med. 2016;375:556–65.
Wu GC, Liu HR, Leng RX, et al. Subclinical atherosclerosis in patients with systemic lupus erythematosus: a systemic review and meta-analysis. Autoimmun Rev. 2016;15:22–37.
Wu GC, Leng RX, Lu Q, et al. Subclinical atherosclerosis in patients with inflammatory bowel diseases: a systematic review and meta-analysis. Angiology. 2017;68:447–61.
Yang CA, Chiang BL. Inflammasomes and human autoimmunity: a comprehensive review. J Autoimmun. 2015;61:1–8. https://doi.org/10.1016/j.jaut.2015.05.001.
Zanoli L, Boutouyrie P, Fatuzzo P, et al. Inflammation and aortic stiffness: an individual participant data meta-analysis in patients with inflammatory bowel disease. J Am Heart Assoc. 2017;6:e007003.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Kerkhof, P.L.M., Khamaganova, I. (2018). Sex-Specific Cardiovascular Comorbidities with Associations in Dermatologic and Rheumatic Disorders. In: Kerkhof, P., Miller, V. (eds) Sex-Specific Analysis of Cardiovascular Function. Advances in Experimental Medicine and Biology, vol 1065. Springer, Cham. https://doi.org/10.1007/978-3-319-77932-4_30
Download citation
DOI: https://doi.org/10.1007/978-3-319-77932-4_30
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-77931-7
Online ISBN: 978-3-319-77932-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)