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Choroidal thickness is associated with cardiovascular risk factors and cardiac health: the Gutenberg Health Study

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Abstract

Background

Choroidal thickness is associated with several cardiovascular parameters in case–control studies including patients with manifest disease. So far, it was unclear whether underlying cardiovascular risk factors or the continuum of heart failure may lead to alterations of the choroid. Therefore, our hypothesis was to test in a population-based study, whether choroidal thickness is associated with cardiovascular risk factors and heart disease.

Methods

A population-based cross-sectional study was carried out in Germany. A comprehensive medical examination including assessment of cardiovascular risk factors, echocardiography and ophthalmological examinations with spectral-domain optical coherence tomography of the choroid was performed. Subfoveal choroidal thickness as well as left ventricular ejection fraction (LVEF) and a surrogate marker for left ventricular end-diastolic pressure (E/e’) were measured. Linear regression analyses were carried out to determine the relationship between subfoveal choroidal thickness and age, sex, body mass index, systolic blood pressure, dyslipidemia, HbA1c level, hematocrit, estimated glomerular filtration rate (eGFR), LVEF, E/e’ and left ventricular mass index adjusted for ocular parameters.

Results

1.742 subjects (48% females) with a mean age 59.3 ± 10.6 years were included in this study. Mean subfoveal thickness was 252 ± 77 µm (right eyes) and 255 ± 77 µm (left eyes). Unadjusted linear regression analysis revealed that subfoveal choroidal thickness is associated with sex, age, systolic blood pressure, hematocrit, eGFR, left ventricular end-diastolic pressure, left ventricular mass index (all p < 0.001) and dyslipidemia (p = 0.009). Adjusted linear regression only revealed age as associated parameter (p < 0.001).

Conclusions

We did find evidence for an association between subfoveal choroidal thickness and cardiovascular risk factors which was mediated by aging.

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References

  1. Ahmad M, Kaszubski PA, Cobbs L, Reynolds H, Smith RT (2017) Choroidal thickness in patients with coronary artery disease. PLoS One 12(6):e0175691. https://doi.org/10.1371/journal.pone.0175691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ahn SJ, Woo SJ, Park KH (2014) Retinal and choroidal changes with severe hypertension and their association with visual outcome. Invest Ophthalmol Vis Sci 55(12):7775–7785. https://doi.org/10.1167/iovs.14-14915

    Article  PubMed  Google Scholar 

  3. Akay F, Gundogan FC, Yolcu U, Toyran S, Uzun S (2016) Choroidal thickness in systemic arterial hypertension. Eur J Ophthalmol 26(2):152–157. https://doi.org/10.5301/ejo.5000675

    Article  PubMed  Google Scholar 

  4. Akcay BI, Kardes E, Macin S, Unlu C, Ozgurhan EB, Macin A, Bozkurt TK, Ergin A, Surmeli R (2016) Evaluation of subfoveal choroidal thickness in internal carotid artery stenosis. J Ophthalmol 2016:5296048. https://doi.org/10.1155/2016/5296048

    Article  PubMed  PubMed Central  Google Scholar 

  5. Altinkaynak H, Kara N, Sayin N, Gunes H, Avsar S, Yazici AT (2014) Subfoveal choroidal thickness in patients with chronic heart failure analyzed by spectral-domain optical coherence tomography. Curr Eye Res 39(11):1123–1128. https://doi.org/10.3109/02713683.2014.898310

    Article  PubMed  Google Scholar 

  6. Pekel G, Dogu MH, Keskin A, Acer S, Yagci R, Kasikci A, Cetin EN (2015) Subfoveal choroidal thickness is associated with blood hematocrit level. Ophthalmologica 234(1):55–59. https://doi.org/10.1159/000433449

    Article  PubMed  Google Scholar 

  7. Tan KA, Gupta P, Agarwal A, Chhablani J, Cheng CY, Keane PA, Agrawal R (2016) State of science: choroidal thickness and systemic health. Surv Ophthalmol 61(5):566–581. https://doi.org/10.1016/j.survophthal.2016.02.007

    Article  PubMed  Google Scholar 

  8. Sansom LT, Suter CA, McKibbin M (2016) The association between systolic blood pressure, ocular perfusion pressure and subfoveal choroidal thickness in normal individuals. Acta Ophthalmol 94(2):e157–158. https://doi.org/10.1111/aos.12794

    Article  PubMed  Google Scholar 

  9. Wei WB, Xu L, Jonas JB, Shao L, Du KF, Wang S, Chen CX, Xu J, Wang YX, Zhou JQ, You QS (2013) Subfoveal choroidal thickness: the Beijing Eye Study. Ophthalmology 120(1):175–180. https://doi.org/10.1016/j.ophtha.2012.07.048

    Article  PubMed  Google Scholar 

  10. Gupta P, Jing T, Marziliano P, Cheung CY, Baskaran M, Lamoureux EL, Wong TY, Cheung CM, Cheng CY (2015) Distribution and determinants of choroidal thickness and volume using automated segmentation software in a population-based study. Am J Ophthalmol 159(2):293–301.e293. https://doi.org/10.1016/j.ajo.2014.10.034

    Article  PubMed  Google Scholar 

  11. Hohn R, Kottler U, Peto T, Blettner M, Munzel T, Blankenberg S, Lackner KJ, Beutel M, Wild PS, Pfeiffer N (2015) The ophthalmic branch of the Gutenberg Health Study: study design, cohort profile and self-reported diseases. PLoS One 10(3):e0120476. https://doi.org/10.1371/journal.pone.0120476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Shao L, Xu L, Chen CX, Yang LH, Du KF, Wang S, Zhou JQ, Wang YX, You QS, Jonas JB, Wei WB (2013) Reproducibility of subfoveal choroidal thickness measurements with enhanced depth imaging by spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci 54(1):230–233. https://doi.org/10.1167/iovs.12-10351

    Article  PubMed  Google Scholar 

  13. Rahman W, Chen FK, Yeoh J, Patel P, Tufail A, Da Cruz L (2011) Repeatability of manual subfoveal choroidal thickness measurements in healthy subjects using the technique of enhanced depth imaging optical coherence tomography. Invest Ophthalmol Vis Sci 52(5):2267–2271. https://doi.org/10.1167/iovs.10-6024

    Article  PubMed  Google Scholar 

  14. Spaide RF, Koizumi H, Pozzoni MC (2008) Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 146(4):496–500. https://doi.org/10.1016/j.ajo.2008.05.032

    Article  PubMed  Google Scholar 

  15. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Rietzschel ER, Rudski L, Spencer KT, Tsang W, Voigt JU (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 28(1):1–39.e14. https://doi.org/10.1016/j.echo.2014.10.003

    Article  PubMed  Google Scholar 

  17. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF 3rd, Dokainish H, Edvardsen T, Flachskampf FA, Gillebert TC, Klein AL, Lancellotti P, Marino P, Oh JK, Popescu BA, Waggoner AD (2016) Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 29(4):277–314. https://doi.org/10.1016/j.echo.2016.01.011

    Article  PubMed  Google Scholar 

  18. Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JG, Coats AJ, Falk V, Gonzalez-Juanatey JR, Harjola VP, Jankowska EA, Jessup M, Linde C, Nihoyannopoulos P, Parissis JT, Pieske B, Riley JP, Rosano GM, Ruilope LM, Ruschitzka F, Rutten FH, van der Meer P (2016) 2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatment of acute and chronic heart failure of the european society of cardiology (ESC). Developed with the special contribution of the heart failure association (HFA) of the ESC. Eur J Heart Fail 18(8):891–975. https://doi.org/10.1002/ejhf.592

    Article  PubMed  Google Scholar 

  19. Bursi F, Weston SA, Redfield MM, Jacobsen SJ, Pakhomov S, Nkomo VT, Meverden RA, Roger VL (2006) Systolic and diastolic heart failure in the community. JAMA 296(18):2209–2216. https://doi.org/10.1001/jama.296.18.2209

    Article  CAS  PubMed  Google Scholar 

  20. Lam CSP, Gamble GD, Ling LH, Sim D, Leong KTG, Yeo PSD, Ong HY, Jaufeerally F, Ng TP, Cameron VA, Poppe K, Lund M, Devlin G, Troughton R, Richards AM, Doughty RN (2018) Mortality associated with heart failure with preserved vs. reduced ejection fraction in a prospective international multi-ethnic cohort study. Eur Heart J. https://doi.org/10.1093/eurheartj/ehy005

    Article  PubMed  PubMed Central  Google Scholar 

  21. de Boer RA, Nayor M, deFilippi CR, Enserro D, Bhambhani V, Kizer JR, Blaha MJ, Brouwers FP, Cushman M, Lima JAC, Bahrami H, van der Harst P, Wang TJ, Gansevoort RT, Fox CS, Gaggin HK, Kop WJ, Liu K, Vasan RS, Psaty BM, Lee DS, Hillege HL, Bartz TM, Benjamin EJ, Chan C, Allison M, Gardin JM, Januzzi JL Jr, Shah SJ, Levy D, Herrington DM, Larson MG, van Gilst WH, Gottdiener JS, Bertoni AG, Ho JE (2018) Association of cardiovascular biomarkers with incident heart failure with preserved and reduced ejection fraction. JAMA Cardiol. https://doi.org/10.1001/jamacardio.2017.4987

    Article  PubMed  PubMed Central  Google Scholar 

  22. Desai A, Fang JC (2008) Heart failure with preserved ejection fraction: hypertension, diabetes, obesity/sleep apnea, and hypertrophic and infiltrative cardiomyopathy. Heart Fail Clin 4(1):87–97. https://doi.org/10.1016/j.hfc.2007.11.001

    Article  PubMed  Google Scholar 

  23. Park JY, Kim BG, Hwang JH, Kim JS (2017) Choroidal thickness in and outside of vascular arcade in healthy eyes using spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci 58(13):5827–5837. https://doi.org/10.1167/iovs.17-22581

    Article  PubMed  Google Scholar 

  24. Gupta T, Saini N, Arora J, Sahni D (2017) Age-related changes in the chorioretinal junction: an immunohistochemical study. J Histochem Cytochem 65(10):567–577. https://doi.org/10.1369/0022155417726507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Gottdiener JS, Bednarz J, Devereux R, Gardin J, Klein A, Manning WJ, Morehead A, Kitzman D, Oh J, Quinones M, Schiller NB, Stein JH, Weissman NJ (2004) American society of echocardiography recommendations for use of echocardiography in clinical trials. J Am Soc Echocardiogr 17(10):1086–1119. https://doi.org/10.1016/j.echo.2004.07.013

    Article  PubMed  Google Scholar 

  26. Xu J, Xu L, Du KF, Shao L, Chen CX, Zhou JQ, Wang YX, You QS, Jonas JB, Wei WB (2013) Subfoveal choroidal thickness in diabetes and diabetic retinopathy. Ophthalmology 120(10):2023–2028. https://doi.org/10.1016/j.ophtha.2013.03.009

    Article  PubMed  Google Scholar 

  27. Gupta P, Thakku SG, Sabanayagam C, Tan G, Agrawal R, Cheung CMG, Lamoureux EL, Wong TY, Cheng CY (2017) Characterisation of choroidal morphological and vascular features in diabetes and diabetic retinopathy. Br J Ophthalmol 101(8):1038–1044. https://doi.org/10.1136/bjophthalmol-2016-309366

    Article  PubMed  Google Scholar 

  28. Schuster AK, Steinmetz P, Forster TM, Schlichtenbrede FC, Harder BC, Jonas JB (2014) Choroidal thickness in nonarteritic anterior ischemic optic neuropathy. Am J Ophthalmol 158(6):1342–1347.e1341. https://doi.org/10.1016/j.ajo.2014.09.008

    Article  PubMed  Google Scholar 

  29. Ikuno Y, Kawaguchi K, Nouchi T, Yasuno Y (2010) Choroidal thickness in healthy Japanese subjects. Invest Ophthalmol Vis Sci 51(4):2173–2176. https://doi.org/10.1167/iovs.09-4383

    Article  PubMed  Google Scholar 

  30. Eggebrecht L, Prochaska JH, Trobs SO, Schwuchow-Thonke S, Gobel S, Diestelmeier S, Schulz A, Arnold N, Panova-Noeva M, Koeck T, Rapp S, Gori T, Lackner KJ, Ten Cate H, Munzel T, Wild PS (2019) Direct oral anticoagulants and vitamin K antagonists are linked to differential profiles of cardiac function and lipid metabolism. Clin Res Cardiol. https://doi.org/10.1007/s00392-018-1408-y

    Article  PubMed  Google Scholar 

  31. Hirschberg K, Reinhart M, Mereles D, Uhlmann L, Andre F, Riffel J, Ochs M, Katus HA (2019) Echocardiographic calcification score in patients with low/intermediate cardiovascular risk. Clin Res Cardiol 108(2):194–202. https://doi.org/10.1007/s00392-018-1343-y

    Article  CAS  PubMed  Google Scholar 

  32. Fu M, Ahrenmark U, Berglund S, Lindholm CJ, Lehto A, Broberg AM, Tasevska-Dinevska G, Wikstrom G, Agard A, Andersson B (2017) Adherence to optimal heart rate control in heart failure with reduced ejection fraction: insight from a survey of heart rate in heart failure in Sweden (HR-HF study). Clin Res Cardiol 106(12):960–973. https://doi.org/10.1007/s00392-017-1146-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Usui S, Ikuno Y, Akiba M, Maruko I, Sekiryu T, Nishida K, Iida T (2012) Circadian changes in subfoveal choroidal thickness and the relationship with circulatory factors in healthy subjects. Invest Ophthalmol Vis Sci 53(4):2300–2307. https://doi.org/10.1167/iovs.11-8383

    Article  PubMed  Google Scholar 

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Acknowledgements

The Gutenberg Health Study is funded through the government of Rhineland-Palatinate („Stiftung Rheinland-Pfalz für Innovation“, contract AZ 961-386261/733), the research programs “Wissen schafft Zukunft” and “Center for Translational Vascular Biology (CTVB)” of the Johannes Gutenberg-University of Mainz, and its contract with Boehringer Ingelheim and PHILIPS Medical Systems, including an unrestricted grant for the Gutenberg Health Study. Philipp S. Wild is funded by the Federal Ministry of Education and Research (BMBF 01EO1503) and he is PI of the German Center for Cardiovascular Research (DZHK). Pfeiffer N receives financial support by Novartis, Ivantis, Santen, Thea, Boehringer Ingelheim Deutschland GmbH & Co. KG, Alcon, Sanoculis. Schuster AK holds the professorship for ophthalmic healthcare research donated by „Stiftung Auge“and financed by „Deutsche Ophthalmologische Gesellschaft“and „Berufsverband der Augenärzte Deutschlands e.V.“ All other authors: none. We thank all study participants for their willingness to provide data for this research project and we are indebted to all coworkers for their enthusiastic commitment.

Funding

Schuster AK received research funding from Bayer Vital, Novartis and Heidelberg Engineering; Pfeiffer N: receives financial support and grants by Novartis, Ivantis, Santen, Thea, Boehringer Ingelheim Deutschland GmbH & Co. KG, Alcon, Sanoculis; Nickels S received reimbursement of travel expenses from Novartis Pharma GmbH; Wild PS: received research grants from Boehringer Ingelheim Deutschland GmbH & Co. KG, Daiichi Sankyo Deutschland GmbH, Bayer HealthCare-Bayer-Vital GmbH, Portavita BV, Sanofi-Aventis Deutschland GmbH, the German Ministry of Research and the Ministry of Health of Rhineland-Palatinate; Münzel T: received speakers honorary from Boehringer Ingelheim Deutschland GmbH & Co. KG, Servier Deutschland GmbH, Actavis Deutschland GmbH, Berlin Chemie Deutschland and currently research grants from the German Ministry of Research and the government of Rhineland-Palatinate; all other authors: none.

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Authors and Affiliations

  1. Department of Ophthalmology, University Medical Center, Johannes Gutenberg-University Mainz, Langenbeckstr. 1, 55131, Mainz, Germany

    Alexander K. Schuster, Constantin Feretos, Philipp Blumenstein, Stefan Nickels & Norbert Pfeiffer

  2. Preventive Cardiology and Preventive Medicine, Center for Cardiology, University Medical Center, Johannes Gutenberg-University Mainz, Mainz, Germany

    Anja Leuschner, Sven-Oliver Troebs, Sören Schwuchow, Andreas Schulz & Philipp S. Wild

  3. Dardenne Eye Clinic, Bonn-Bad Godesberg, Germany

    Constantin Feretos, Philipp Blumenstein & Alireza Mirshahi

  4. Department of Biomedical Statistics, University Medical Center, Johannes Gutenberg-University Mainz, Mainz, Germany

    Maria Blettner

  5. Department of Psychosomatic Medicine and Psychotherapy, University Medical Center, Johannes Gutenberg-University Mainz, Mainz, Germany

    Manfred E. Beutel

  6. Institute for Clinical Chemistry and Laboratory Medicine, University Medical Center, Johannes Gutenberg-University Mainz, Mainz, Germany

    Karl J. Lackner

  7. Center for Cardiology, University Medical Center, Johannes Gutenberg-University Mainz, Mainz, Germany

    Sven-Oliver Troebs & Thomas Münzel

  8. Center for Thrombosis and Hemostasis, University Medical Center, Johannes Gutenberg-University Mainz, Mainz, Germany

    Thomas Münzel & Philipp S. Wild

  9. DZHK (German Center for Cardiovascular Research), Partner Site Rhine-Main, Mainz, Germany

    Sven-Oliver Troebs & Philipp S. Wild

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  1. Alexander K. Schuster
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  2. Anja Leuschner
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  3. Constantin Feretos
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  4. Philipp Blumenstein
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Corresponding author

Correspondence to Alexander K. Schuster.

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Conflict of interest

The authors have no conflicts of interest to declare.

Ethical statement

The study was approved by the ethics committee (Ethics Commission of the State Chamber of Physicians of Rhineland-Palatinate).

Informed consent

According to the tenets of the Declaration of Helsinki, written informed consent was obtained from all participants prior to entering the study.

Additional information

Pfeiffer N. and Wild P.S. are senior authors.

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Schuster, A.K., Leuschner, A., Feretos, C. et al. Choroidal thickness is associated with cardiovascular risk factors and cardiac health: the Gutenberg Health Study. Clin Res Cardiol 109, 172–182 (2020). https://doi.org/10.1007/s00392-019-01498-8

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  • DOI: https://doi.org/10.1007/s00392-019-01498-8

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