Subclinical Cardiac Organ Damage in Patients with Moderate to Severe Psoriasis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Cardiovascular Risk Factor Assessment
2.3. Assessment of Quality of Life and Severity of Psoriasis
2.4. Echocardiography
2.5. Statistical Analysis
3. Results
3.1. Clinical Characteristics and CV Risk Factors
3.2. Prevalence and Covariables of Subclinical Cardiac Organ Damage
4. Discussion
Study Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Mehrmal, S.; Uppal, P.; Nedley, N.; Giesey, R.L.; Delost, G.R. The global, regional, and national burden of psoriasis in 195 countries and territories, 1990 to 2017: A systematic analysis from the Global Burden of Disease Study 2017. J. Am. Acad. Dermatol. 2021, 84, 46–52. [Google Scholar] [CrossRef] [PubMed]
- Georgescu, S.R.; Tampa, M.; Caruntu, C.; Sarbu, M.I.; Mitran, C.I.; Mitran, M.I.; Matei, C.; Constantin, C.; Neagu, M. Advances in understanding the immunological pathways in psoriasis. Int. J. Mol. Sci. 2019, 20, 739. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Danielsen, K.; Duvetorp, A.; Iversen, L.; Østergaard, M.; Seifert, O.; Tveit, K.S.; Skov, L. Prevalence of psoriasis and psoriatic arthritis and patient perceptions of severity in Sweden, Norway and Denmark: Results from the Nordic patient survey of psoriasis and psoriatic arthritis. Acta Derm. Venereol. 2019, 99, 18–25. [Google Scholar] [CrossRef] [Green Version]
- Nast, A.; Gisondi, P.; Ormerod, A.D.; Saiag, P.; Smith, C.; Spuls, P.I.; Arenberger, P.; Bachelez, H.; Barker, J.; Dauden, E.; et al. European S3-Guidelines on the systemic treatment of psoriasis vulgaris—Update 2015—Short version—EDF in cooperation with EADV and IPC. J. Eur. Acad. Dermatol. Venereol. 2015, 29, 2277–2294. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miller, I.M.; Ellervik, C.; Yazdanyar, S.; Jemec, G.B. Meta-analysis of psoriasis, cardiovascular disease, and associated risk factors. J. Am. Acad. Dermatol. 2013, 69, 1014–1024. [Google Scholar] [CrossRef] [PubMed]
- Nowowiejska, J.; Baran, A.; Lewoc, M.; Grabowska, P.; Kaminski, T.W.; Flisiak, I. The Assessment of risk and predictors of sleep disorders in patients with psoriasis-a questionnaire-based cross-sectional analysis. J. Clin. Med. 2021, 10, 664. [Google Scholar] [CrossRef]
- Iskandar, I.Y.; Ashcroft, D.M.; Warren, R.B.; Yiu, Z.Z.; McElhone, K.; Lunt, M.; Barker, J.N.; Burden, A.D.; Ormerod, A.D.; Reynolds, N.J.; et al. Demographics and disease characteristics of patients with psoriasis enrolled in the British Association of Dermatologists Biologic Interventions Register. Br. J. Dermatol. 2015, 173, 510–518. [Google Scholar] [CrossRef]
- Gelfand, J.M.; Neimann, A.L.; Shin, D.B.; Wang, X.; Margolis, D.J.; Troxel, A.B. Risk of myocardial infarction in patients with psoriasis. J. Am. Med. Assoc. 2006, 296, 1735–1741. [Google Scholar] [CrossRef] [Green Version]
- Ahlehoff, O.; Skov, L.; Gislason, G.; Lindhardsen, J.; Kristensen, S.L.; Iversen, L.; Lasthein, S.; Gniadecki, R.; Dam, T.N.; Torp-Pedersen, C.; et al. Cardiovascular disease event rates in patients with severe psoriasis treated with systemic anti-inflammatory drugs: A Danish real-world cohort study. J. Intern. Med. 2013, 273, 197–204. [Google Scholar] [CrossRef] [PubMed]
- Williams, B.; Mancia, G.; Spiering, W.; Agabiti Rosei, E.; Azizi, M.; Burnier, M.; Clement, D.; Coca, A.; De Simone, G.; Dominiczak, A.; et al. 2018 Practice Guidelines for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension. Blood Press 2018, 27, 314–340. [Google Scholar] [CrossRef]
- Cramariuc, D.; Gerdts, E. Epidemiology of left ventricular hypertrophy in hypertension: Implications for the clinic. Expert Rev. Cardiovasc. Ther. 2016, 14, 915–926. [Google Scholar] [CrossRef]
- Halland, H.; Lønnebakken, M.T.; Pristaj, N.; Saeed, S.; Midtbø, H.; Einarsen, E.; Gerdts, E. Sex differences in subclinical cardiac disease in overweight and obesity (the FATCOR study). Nutr. Metab. Cardiovasc. Dis. 2018, 28, 1054–1060. [Google Scholar] [CrossRef]
- Mrowietz, U.; Kragballe, K.; Reich, K.; Spuls, P.; Griffiths, C.E.; Nast, A.; Franke, J.; Antoniou, C.; Arenberger, P.; Balieva, F.; et al. Definition of treatment goals for moderate to severe psoriasis: A European consensus. Arch. Dermatol. Res. 2011, 303, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Fredriksson, T.; Pettersson, U. Severe psoriasis—Oral therapy with a new retinoid. Dermatologica 1978, 157, 238–244. [Google Scholar] [CrossRef]
- Gao, J.; Meyer, K.; Borucki, K.; Ueland, P.M. Multiplex immuno-MALDI-TOF MS for targeted quantification of protein biomarkers and their proteoforms related to inflammation and renal dysfunction. Anal. Chem. 2018, 90, 3366–3373. [Google Scholar] [CrossRef]
- Lang, R.M.; Badano, L.P.; Mor-Avi, V.; Afilalo, J.; Armstrong, A.; Ernande, L.; Flachskampf, F.A.; Foster, E.; Goldstein, S.A.; Kuznetsova, T.; et al. Recommendations for cardiac chamber quantification by echocardiography in adults: An update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur. Heart J. Cardiovasc. Imaging 2015, 16, 233–270. [Google Scholar] [CrossRef]
- Galderisi, M.; Henein, M.Y.; D’Hooge, J.; Sicari, R.; Badano, L.P.; Zamorano, J.L.; Roelandt, J.R. European Association of E. Recommendations of the European Association of Echocardiography: How to use echo-Doppler in clinical trials: Different modalities for different purposes. Eur. J. Echocardiogr. 2011, 12, 339–353. [Google Scholar] [CrossRef] [Green Version]
- Kuznetsova, T.; Haddad, F.; Tikhonoff, V.; Kloch-Badelek, M.; Ryabikov, A.; Knez, J.; Malyutina, S.; Stolarz-Skrzypek, K.; Thijs, L.; Schnittger, I.; et al. Impact and pitfalls of scaling of left ventricular and atrial structure in population-based studies. J. Hypertens. 2016, 34, 1186–1194. [Google Scholar] [CrossRef] [PubMed]
- Atas, H.; Kepez, A.; Bozbay, M.; Gencosmanoglu, D.S.; Cincin, A.; Sunbul, M.; Bozbay, A.Y.; Darvishova, R.; Ergun, T. Assessment of left atrial volume and function in patients with psoriasis by using real time three-dimensional echocardiography. Wien. Klin. Wochenschr. 2015, 127, 858–863. [Google Scholar] [CrossRef]
- Biyik, I.; Narin, A.; Bozok, M.A.; Ergene, O. Echocardiographic and clinical abnormalities in patients with psoriasis. J. Int. Med. Res. 2006, 34, 632–639. [Google Scholar] [CrossRef] [PubMed]
- Daïen, C.I.; Fesler, P.; du Cailar, G.; Daïen, V.; Mura, T.; Dupuy, A.M.; Cristol, J.P.; Ribstein, J.; Combe, B.; Morel, J. Etanercept normalises left ventricular mass in patients with rheumatoid arthritis. Ann. Rheum. Dis. 2013, 72, 881–887. [Google Scholar] [CrossRef]
- Kotyla, P.J.; Owczarek, A.; Rakoczy, J.; Lewicki, M.; Kucharz, E.J.; Emery, P. Infliximab treatment increases left ventricular ejection fraction in patients with rheumatoid arthritis: Assessment of heart function by echocardiography, endothelin 1, interleukin 6, and NT-pro brain natriuretic peptide. J. Rheumatol. 2012, 39, 701–706. [Google Scholar] [CrossRef]
- Baniaamam, M.; Handoko, M.L.; Agca, R.; Heslinga, S.C.; Konings, T.C.; van Halm, V.P.; Nurmohamed, M.T. The effect of anti-tnf therapy on cardiac function in rheumatoid arthritis: An observational study. J. Clin. Med. 2020, 9, 3145. [Google Scholar] [CrossRef]
- Gerdts, E.; Cramariuc, D.; de Simone, G.; Wachtell, K.; Dahlöf, B.; Devereux, R.B. Impact of left ventricular geometry on prognosis in hypertensive patients with left ventricular hypertrophy (the LIFE study). Eur. J. Echocardiogr. 2008, 9, 809–815. [Google Scholar] [CrossRef] [Green Version]
- Myasoedova, E.; Davis, J.M., 3rd; Crowson, C.S.; Roger, V.L.; Karon, B.L.; Borgeson, D.D.; Therneau, T.M.; Matteson, E.L.; Rodeheffer, R.J.; Gabriel, S.E. Brief report: Rheumatoid arthritis is associated with left ventricular concentric remodeling: Results of a population-based cross-sectional study. Arthritis Rheum. 2013, 65, 1713–1718. [Google Scholar] [CrossRef] [Green Version]
- Midtbø, H.; Gerdts, E.; Kvien, T.K.; Olsen, I.C.; Hirth, A.; Davidsen, E.S.; Semb, A.G. Disease activity and left ventricular structure in patients with rheumatoid arthritis. Rheumatology 2015, 54, 511–519. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masiha, S.; Sundström, J.; Lind, L. Inflammatory markers are associated with left ventricular hypertrophy and diastolic dysfunction in a population-based sample of elderly men and women. J. Hum. Hypertens. 2013, 27, 13–17. [Google Scholar] [CrossRef]
- Wu, S.; Han, J.; Li, W.Q.; Qureshi, A.A. Hypertension, antihypertensive medication use, and risk of psoriasis. J. Am. Med. Assoc. Dermatol. 2014, 150, 957–963. [Google Scholar] [CrossRef] [PubMed]
- Midtbø, H.; Gerdts, E.; Kvien, T.K.; Olsen, I.C.; Lønnebakken, M.T.; Davidsen, E.S.; Rollefstad, S.; Semb, A.G. The association of hypertension with asymptomatic cardiovascular organ damage in rheumatoid arthritis. Blood Press 2016, 25, 298–304. [Google Scholar] [CrossRef]
- Cioffi, G.; Ognibeni, F.; Dalbeni, A.; Giollo, A.; Orsolini, G.; Gatti, D.; Rossini, M.; Viapiana, O. High prevalence of occult heart disease in normotensive patients with rheumatoid arthritis. Clin. Cardiol. 2018, 41, 736–743. [Google Scholar] [CrossRef] [PubMed]
- Gerdts, E.; Wachtell, K.; Omvik, P.; Otterstad, J.E.; Oikarinen, L.; Boman, K.; Dahlof, B.; Devereux, R.B. Left atrial size and risk of major cardiovascular events during antihypertensive treatment: Losartan intervention for endpoint reduction in hypertension trial. Hypertension 2007, 49, 311–316. [Google Scholar] [CrossRef]
- Gerdts, E.; Izzo, R.; Mancusi, C.; Losi, M.A.; Manzi, M.V.; Canciello, G.; De Luca, N.; Trimarco, B.; de Simone, G. Left ventricular hypertrophy offsets the sex difference in cardiovascular risk (the Campania Salute Network). Int. J. Cardiol. 2018, 258, 257–261. [Google Scholar] [CrossRef] [PubMed]
- van der Schoot, L.S.; van den Reek, J.; Groenewoud, J.M.M.; Otero, M.E.; Njoo, M.D.; Ossenkoppele, P.M.; Mommers, J.M.; Koetsier, M.I.A.; Berends, M.A.M.; Arnold, W.P.; et al. Female patients are less satisfied with biological treatment for psoriasis and experience more side-effects than male patients: Results from the prospective BioCAPTURE registry. J. Eur. Acad. Dermatol. Venereol. 2019, 33, 1913–1920. [Google Scholar] [CrossRef]
- Hotard, R.S.; Feldman, S.R.; Fleischer, A.B., Jr. Sex-specific differences in the treatment of severe psoriasis. J. Am. Acad. Dermatol. 2000, 42, 620–623. [Google Scholar] [CrossRef]
- Hägg, D.; Eriksson, M.; Sundström, A.; Schmitt-Egenolf, M. The higher proportion of men with psoriasis treated with biologics may be explained by more severe disease in men. PLoS ONE 2013, 8, e63619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Psoriasis (n = 53) | Controls (n = 99) | p-Value | |
---|---|---|---|
Demographics | |||
Age, years | 47 (15) | 47 (11) | 0.94 |
Women, n (%) | 16 (30) | 28 (28) | 0.81 |
Body mass index, kg/m² | 29.2 (5.5) | 29.9 (3.9) | 0.42 |
Physical activity, hour/week | 4.6 (3.7) | 4.1 (3.4) | 0.44 |
High-sensitive CRP, µg/mL, median (IQR) | 1.0 (0.2–3.0) | 1.1 (0.6–3.2) | 0.33 |
Serum creatinine, µmol/L | 75 (14) | 77 (12) | 0.54 |
Disease duration, years | 24 (13) | - | |
PASI at initiation of infliximab treatment | 16.1 (11.5) | - | |
PASI current | 0.8 (0.8) | - | |
DLQI at initiation of infliximab treatment | 17.5 (6.0) | - | |
DLQI current | 0.7 (1.3) | - | |
Psoriasis arthritis, n (%) | 19 (36) | - | |
Cardiovascular risk factors | |||
Current smoking, n (%) | 19 (37) | 15 (17) | 0.005 |
Office systolic BP, mmHg | 137 (17) | 132 (17) | 0.11 |
Office diastolic BP, mmHg | 87 (8) | 82 (9) | 0.003 |
Ambulatory systolic BP, mmHg | 123 (12) | 122 (12) | 0.75 |
Ambulatory diastolic BP, mmHg | 80 (8) | 79 (7) | 0.60 |
Hypertension, n (%) | 31 (66) | 57 (61) | 0.54 |
Obesity, n (%) | 18 (34) | 33 (33) | 0.94 |
Diabetes, n (%) | 3 (6) | 5 (7) | 0.87 |
LDL cholesterol, mmol/L | 3.4 (0.9) | 3.6 (0.9) | 0.16 |
Statin, n (%) | 6 (11) | 11 (11) | 1.00 |
Medication | |||
Treated hypertension, n (%) | 15 (48) | 20 (35) | 0.22 |
Methotrexate, n (%) | 45 (85) | - | |
Infliximab, n (%) | 53 (100) | - | |
Duration of infliximab treatment, years | 4.9 (3.8) | - |
Psoriasis (n = 53) | Controls (n = 99) | p-Value | |
---|---|---|---|
Interventricular septum thickness at end diastole, cm | 1.0 (0.2) | 1.1 (0.3) | 0.007 |
LV diameter at end diastole, cm | 4.8 (0.6) | 5.1 (0.5) | 0.005 |
LV posterior wall thickness at end diastole, cm | 0.9 (0.2) | 0.8 (0.2) | 0.41 |
LV mass index, g/m2.7 | 36.1 (9.6) | 40.3 (9.8) | 0.01 |
LV hypertrophy, n (%) | 5 (9) | 14 (14) | 0.40 |
LV relative wall thickness, ratio | 0.38 (0.9) | 0.34 (0.7) | 0.001 |
Concentric geometry, n (%) | 13 (25) | 12 (12) | 0.05 |
Ejection fraction, % | 65 (6) | 62 (5) | <0.001 |
Left atrial volume, mL/m2 | 15.9 (4.6) | 19.3 (5.1) | <0.001 |
Dilated left atrium, n (%) | 17 (32) | 63 (64) | <0.001 |
Any cardiac organ damage, n (%) | 27 (51) | 72 (73) | 0.007 |
Univariable Analyses | Multivariable Analyses | |||
---|---|---|---|---|
OR (95% CI) | p | OR (95% CI) | p | |
Psoriasis | 0.39 (0.19–0.78) | 0.008 | 0.32 (0.13–0.77) | 0.01 |
Age, years | 1.04 (1.01–1.08) | 0.005 | 1.04 (1.00–1.07) | 0.05 |
Female sex | 2.67 (1.17–6.11) | 0.02 | 5.15 (1.72–14.40) | 0.003 |
Current smoking | 0.33 (0.15–0.74) | 0.006 | 0.51 (0.20–1.33) | 0.17 |
Hypertension | 2.21 (1.08–4.52) | 0.03 | 1.81 (0.75–4.37) | 0.19 |
Body mass index, kg/m2 | 1.07 (0.99–1.16) | 0.10 | 1.06 (0.96–1.17) | 0.22 |
Obesity | 1.67 (0.80–3.46) | 0.18 | ||
Diabetes | 4.29 (0.51–36.03) | 0.18 | ||
Anti-hypertensive treatment | 2.57 (1.04–6.38) | 0.04 | ||
LDL cholesterol, mmol/L | 1.28 (0.88–1.86) | 0.20 | ||
Statin, n (%) | 1.99 (0.35–2.88) | 1.00 |
Univariable Analyses | Multivariable Analyses | |||
---|---|---|---|---|
OR (95% CI) | p | OR (95% CI) | p | |
Age, years | 1.05 (1.01–1.10) | 0.02 | 1.05 (0.99–1.11) | 0.12 |
Female sex | 1.96 (0.59–6.52) | 0.27 | 3.24 (0.66–15.86) | 0.15 |
Hypertension | 9.10 (2.11–39.34) | 0.003 | 6.88 (1.32–35.98) | 0.02 |
Body mass index, kg/m2 | 1.12 (1.00–1.25) | 0.06 | 1.07 (0.93–1–24) | 0.36 |
Current smoking | 0.32 (0.10–1.05) | 0.06 | ||
Obesity | 1.87 (0.59–5.94) | 0.29 | ||
Diabetes | 2.08 (0.18–24.51) | 0.56 | ||
LDL cholesterol, mmol/L | 1.81 (0.96–3.42) | 0.07 | ||
Statin, n (%) | 2.01 (0.35–12.51) | 0.42 | ||
Anti-hypertensive treatment | 5.87 (1.41–24.40) | 0.02 | ||
Methotrexate | 1.01 (0.23–4.71) | 0.95 | ||
Disease duration, months | 1.04 (0.99–1.08) | 0.11 | ||
PASI at treatment start | 1.03 (0.97–1.08) | 0.34 | ||
Current PASI | 1.75 (0.81–3.75) | 0.15 | ||
DLQI at treatment start | 0.96 (0.86–1.06) | 0.38 | ||
Current DLQI | 1.02 (0.68–1.54) | 0.92 | ||
Psoriasis arthritis | 2.03 (0.79–5.27) | 0.14 |
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Linde, A.; Gerdts, E.; Tveit, K.S.; Kringeland, E.; Midtbø, H. Subclinical Cardiac Organ Damage in Patients with Moderate to Severe Psoriasis. J. Clin. Med. 2021, 10, 2440. https://doi.org/10.3390/jcm10112440
Linde A, Gerdts E, Tveit KS, Kringeland E, Midtbø H. Subclinical Cardiac Organ Damage in Patients with Moderate to Severe Psoriasis. Journal of Clinical Medicine. 2021; 10(11):2440. https://doi.org/10.3390/jcm10112440
Chicago/Turabian StyleLinde, Anja, Eva Gerdts, Kåre Steinar Tveit, Ester Kringeland, and Helga Midtbø. 2021. "Subclinical Cardiac Organ Damage in Patients with Moderate to Severe Psoriasis" Journal of Clinical Medicine 10, no. 11: 2440. https://doi.org/10.3390/jcm10112440
APA StyleLinde, A., Gerdts, E., Tveit, K. S., Kringeland, E., & Midtbø, H. (2021). Subclinical Cardiac Organ Damage in Patients with Moderate to Severe Psoriasis. Journal of Clinical Medicine, 10(11), 2440. https://doi.org/10.3390/jcm10112440