Skip to main content

Advertisement

SpringerLink
Log in

Retinal and choroidal vasculature changes associated with chronic kidney disease

  • Retinal Disorders
  • Published:
Graefe's Archive for Clinical and Experimental Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

Retinal and choroidal microvascular changes can be related to renal impairment in hypertension and chronic kidney disease (CKD). The study examines the association between retinochoroidal parameters and renal impairment in hypertensive, non-diabetic patients.

Methods

This is a cross-sectional study on Caucasian patients with systemic arterial hypertension with different levels of renal function. All subjects were studied by blood chemistry, urine examination, microalbuminuria and blood pressure. Complete eye examination was completed with swept source optical coherence tomography (SS-OCT) and optical coherence tomography angiography (OCTA) scans of macular region. Patients were divided in groups: LowGFR and HighGFR and CKD− and CKD+, according to the value of glomerular filtrate (GFR) and albuminuria. LowGFR and CKD+ groups included patients with clinical kidney impairment.

Results

One hundred and twenty eyes of 120 hypertensive patients were evaluated. The mean retinal thickness was thinner in CKD+ versus CKD− group (p < 0.009). LowGFR and CKD+ groups showed thinner choroidal values than HighGFR (p < 0.02) and CKD− (p < 0.001) groups. OCTA showed lower density in LowGFR than in HighGFR group (p < 0.001) and in CKD+ versus CKD− group (p < 0.001). Albuminuria was inversely related to choroidal and retinal thickness measures (p < 0.001) and to the indices of superficial parafoveal (p < 0.05) and foveal (p < 0.05) vascular densities.

Conclusions

CKD is associated with retinal thinning, eGFR and decreasing renal function with progressive reduction of choroidal and retinal vascular density. SS-OCT and OCTA documented close association between CKD and reduction of both choroidal thickness and paracentral retinal vascular density in hypertensive patients.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Jorgensen T, Capewell S, Prescott E et al (2013) Population-level changes to promote cardiovascular health. Eur J Prev Cardiol 20(3):409–421

    Article  PubMed  Google Scholar 

  2. Mendis S, Davis S, Norrving B (2015) Organizational update: the world health organization global status report on noncommunicable diseases 2014; one more landmark step in the combat against stroke and vascular disease. Stroke 46(5):e121–e122

    Article  PubMed  Google Scholar 

  3. Lewington S, Clarke R, Qizilbash N, Prospective Studies Collaboration et al (2002) Age-specific relevance of usual blood pressure to vascular mortality: a meta-analysis of individual data for one million adults in 61 prospective studies. Lancet 360(9349):1903–1913

    Article  Google Scholar 

  4. Mulè G, Castiglia A, Cusumano C et al (2017) Subclinical kidney damage in hypertensive patients: a renal window opened on the cardiovascular system. Focus on microalbuminuria. Adv Exp Med Biol 956:279–306

    Article  PubMed  Google Scholar 

  5. Wong CW, Wong TY, Cheng CY et al (2014) Kidney and eye diseases: common risk factors, etiological mechanisms, and pathways. Kidney Int 85(6):1290–1302

    Article  PubMed  Google Scholar 

  6. Wilkinson-Berka JL, Agrotis A et al (2012) The retinal renin-angiotensin system: roles of angiotensin II and aldosterone. Peptides 36:142–150

    Article  CAS  PubMed  Google Scholar 

  7. Benigni A, Cassis P, Remuzzi G (2010) Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol Med 2:247–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wong TY, Coresh J, Klein R et al (2004) Retinal microvascular abnormalities and renal dysfunction: the atherosclerosis risk in communities study. J Am Soc Nephrol 15(9):2469–2476

    Article  PubMed  Google Scholar 

  9. Grunwald JE, Alexander J, Maguire M, CRIC Study Group et al (2010) Prevalence of ocular fundus pathology in patients with chronic kidney disease. Clin J Am Soc Nephrol 5(5):867–873

    Article  PubMed  PubMed Central  Google Scholar 

  10. Ferrara D, Waheed NK, Duker JS (2016) Investigating the choriocapillaris and choroidal vasculature with new optical coherence tomography technologies. Prog Retin Eye Res 52:130–155

    Article  Google Scholar 

  11. ESH/ESC task Force for the Management of Arterial Hypertension (2013) 2013 Practice guidelines for the management of arterial hypertension of the European Society of Hypertension (ESH) and the European Society of Cardiology (ESC): ESH/ESC task force for the management of arterial hypertension. J Hypertens 31(10):1925–1938

    Article  CAS  Google Scholar 

  12. Downie LE, Hodgson LA, Dsylva C et al (2013) Hypertensive retinopathy: comparing the Keith-Wagener-Barker to a simplified classification. J Hypertens 31(5):960–965

    Article  CAS  PubMed  Google Scholar 

  13. Balmforth C, van Bragt JJ, Ruijs T et al (2016) Chorioretinal thinning in chronic kidney disease links to inflammation and endothelial dysfunction. JCI Insight 8(1):20 e89173

    Google Scholar 

  14. Mulè G, Vadalà M, Geraci G, Cottone S (2018) Retinal vascular imaging in cardiovascular medicine: new tools for an old examination. Atherosclerosis. 268:188–190. https://doi.org/10.1016/j.atherosclerosis.2017.11.001

    Article  CAS  PubMed  Google Scholar 

  15. Nickla DL, Wallman J (2010) The multifunctional choroid. Prog Retin Eye Res 29:144–168

    Article  Google Scholar 

  16. Linsenmeier RA, Padnick-Silver L (2000) Metabolic dependence of photoreceptors on the choroid in the normal and detached retina. Invest Ophthalmol Vis Sci 41:3117–3123

    CAS  Google Scholar 

  17. Spraul CW, Lang GE, Lang GK et al (2002) Morphometric changes of the choriocapillaris and the choroidal vasculature in eyes with advanced glaucomatous changes. Vis Res 42:923–932

    Article  PubMed  Google Scholar 

  18. Brown JS, Flitcroft DI, Ying G et al (2009) In vivo human choroidal thickness measurements: evidence for diurnal fluctuations. Invest Ophthalmol Vis Sci 50:5–12

    Article  PubMed  Google Scholar 

  19. Gao SS, Jia Y, Zhang M et al (2016) Optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57(9):OCT27–OCT36

    Article  PubMed  PubMed Central  Google Scholar 

  20. Cerasola G, Cottone S, Mule G (2010) The progressive pathway of microalbuminuria: from early marker of renal damage to strong cardiovascular risk predictor. J Hypertens 28(12):2357–2369

    CAS  PubMed  Google Scholar 

  21. Chen YH, Chen HS, Tarng DC (2012) More impact of microalbuminuria on retinopathy than moderately reduced GFR among type 2 diabetic patients. Diabetes Care 35(4):803–808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Schlaich MP, Socratous F, Hennebry S et al (2009) Sympathetic activation in chronic renal failure. J Am Soc Nephrol 20(5):933–939

    Article  PubMed  Google Scholar 

  23. Wallman J, Wildsoet C, Xu A et al (1995) Moving the retina: choroidal modulation of refractive state. Vis Res 35(1):37–50

    Article  CAS  Google Scholar 

  24. Copete S, Flores-Moreno I, Montero JA et al (2014) Direct comparison of spectral-domain and swept-source OCT in the measurement of choroidal thickness in normal eyes. Br J Ophthalmol 98(3):334–338

    Article  Google Scholar 

  25. Bahrami B, Ewe SYP, Hong T et al (2017) Influence of retinal pathology on the reliability of macular thickness measurement: a comparison between optical coherence tomography devices. Ophthalmic Surg Lasers Imaging Retina 48(4):319–325

    Article  PubMed  Google Scholar 

  26. Ulaş F, Doğan Ü, Keleş A et al (2013) Evaluation of choroidal and retinal thickness measurements using optical coherence tomography in non-diabetic haemodialysis patients. Int Ophthalmol 33(5):533–539

    Article  PubMed  Google Scholar 

  27. Jung JW, Chin HS, Lee DH et al (2014) Changes in subfoveal choroidal thickness and choroidal extravascular density by spectral domain optical coherence tomography after haemodialysis: a pilot study. Br J Ophthalmol 98(2):207–212

    Article  PubMed  Google Scholar 

  28. Ruiz-Medrano J, Flores-Moreno I, Peña-García P et al (2014) Macular choroidal thickness profile in a healthy population measured by swept-source optical coherence tomography. Invest Ophthalmol Vis Sci 55(6):3532–3542

    Article  PubMed  Google Scholar 

  29. Masis M, Hernandez E, Wu L (2011) Choroidal thickness in patients with systemic hypertension. ARVO Meeting Abstract Invest Ophthalmol Vis Sci (52):5296

  30. Akay F, Gundogan FC, Yolcu U et al (2016) Choroidal thickness in systemic arterial hypertension. Eur J Ophthalmol 26(2):152–157

    Article  Google Scholar 

  31. Liao MT, Sung CC, Hung KC et al (2012) Insulin resistance in patients with chronic kidney disease. J Biomed Biotechnol 2012:691369

    PubMed  PubMed Central  Google Scholar 

  32. Chen J, Muntner P, Hamm LL et al (2003) Insulin resistance and risk of chronic kidney disease in nondiabetic US adults. J Am Soc Nephrol 14:469–477

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Thanks are due to Sergio Milletarì, University of Palermo, for the clinical and technical support.

Author information

Authors and Affiliations

  1. Dipartimento di Biomedicina Sperimentale e Neuroscienze cliniche, Sezione di Oftalmologia, University of Palermo, Via Liborio Giuffrè 13, 90127, Palermo, Italy

    Maria Vadalà, Massimo Castellucci, Giulia Guarrasi & Micol Terrasi

  2. Dipartimento Biomedico di Medicina Interna e Specialistica, Università di Palermo, Palermo, Italy

    Tiziana La Blasca & Giuseppe Mulè

Authors
  1. Maria Vadalà
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Massimo Castellucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giulia Guarrasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Micol Terrasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tiziana La Blasca
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Giuseppe Mulè
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Vadalà.

Ethics declarations

Conflict of interest

No author has a proprietary interest in this study.

Maria Vadalà is consultant for Allergan plc Italia, Bayer SpA, Novartis Co.

Massimo Castellucci, Giulia Guarrasi, Micol Terrasi, Tiziana La Blasca and Giuseppe Mulè have no financial disclosures.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vadalà, M., Castellucci, M., Guarrasi, G. et al. Retinal and choroidal vasculature changes associated with chronic kidney disease. Graefes Arch Clin Exp Ophthalmol 257, 1687–1698 (2019). https://doi.org/10.1007/s00417-019-04358-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00417-019-04358-3

Keywords

Search

Navigation