Skip to main content
The Egyptian Journal of Internal Medicine
Download PDF

Functional and structural abnormalities of the skin microcirculation in hemodialysis patients

The Egyptian Journal of Internal Medicine volume 26, pages 116–123 (2014)Cite this article

Abstract

Background

The changes that occur at the level of the skin microvessels reflect changes at other microvessels including the cardiac microvessels. Several disease states seem to alter skin microvascular function and structure such as diabetes, hypertension, and hypercholesterolemia. Many of these disease states are frequently encountered in hemodialysis (Hdx) patients. The process of Hdx itself is also associated with vascular abnormalities. It was thus the aim of our study to examine the structure and function of skin microcirculation in Hdx patients.

Materials and methods

Sixty patients were examined: 20 patients on regular Hdx, younger than 60 years old, with no diabetes, hypertension, or hypercholesterolemia, 20 patients on regular hemodialysis with coexisting hypertension (Htn-Hdx), and 20 young healthy volunteers. The skin microcirculation was assessed using the laser Doppler fluxmetry and the capillaroscope.

Results

Results showed significant differences in the laser Doppler fluxmetry measurements between the Hdx group and the Htn-Hdx group compared with the control group, with no significant differences in the capillaroscope study.

Conclusion

The study of skin microcirculation in Hdx patients indicated the presence of functional abnormalities without significant structural changes.

References

  1. Debbabi H, Bonnin P, Dnluzeau PH, Leftheriotis G, Levy BI. Non invasive assessment of endothelial function in the skin microcirculation. Am J Hypertens 2010; 23:541–546.

    PubMed  Google Scholar 

  2. Khan F, Patterson D, Belch JJF, et al. Relationship between peripheral and coronary function using laser Doppler imaging and transthoracic echocardiography. Clin Sci 2008; 115:295–300.

    PubMed  Google Scholar 

  3. Vuilleumier P, Decosterd D, et al. Postischemic forearm skin reactive hyperemia is related to cardovascular risk factors in a healthy female population. J Hypertens 2002; 20:1753–1757.

    CAS  PubMed  Google Scholar 

  4. Ijzerman RG, De Jongh RT, MA Beijk, et al. Individuals at increased coronary heart disease risk are characterized by an impaired microvascular function in skin. Eur J Clin Invest 2003; 33:536–542.

    CAS  PubMed  Google Scholar 

  5. Rossi M, Carpi A, Galetta F. Skin vasomotion investigation: a useful tool for clinical evaluation of microvascular endothelial function?. Biomed Pharmacother 2008; 62:541–545.

    CAS  PubMed  Google Scholar 

  6. Angela CS. Capillaroscopy and the measurement of capillary pressure. Br J Clin Pharmacol 2000; 50:501–513.

    Google Scholar 

  7. Raman P, Thakur B, Mathew V. Ankle-brachial index as a predictor of atherosclerosis. J Assoc Physicians India 2001; 49:1074–1077.

    CAS  PubMed  Google Scholar 

  8. Bonetti PO, Pumper GM, Higano ST, et al. Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol 2004; 44:2137–2141.

    PubMed  Google Scholar 

  9. Bukhari M, Hollis S, Moore T, Jayson MIV, et al. Quantitation of microcirculatory abnormalities in patients with primary Raynaud’s phenomenon and systemic sclerosis by video capillaroscopy. Rheumatology 2000; 39:506–512.

    CAS  PubMed  Google Scholar 

  10. Cutolo M, Sulli A, Secchi ME, Paolino S, et al. Nailfold capillaroscopy is useful for the diagnosis and follow-up of autoimmune rheumatic diseases. A future tool for the analysis of microvascular heart involvement? Rheumatology 2006; 45:iv43–iv46.

    PubMed  Google Scholar 

  11. Rossi M, Ricco R, Carpi A. Spectral analysis of skin laser Doppler blood perfusion signal during cutaneous hyperemia in response to acetylcholine iontophoresis and ischemia in normal subjects. Clin Hemorheol Microcirc 2004; 31:303–310.

    CAS  PubMed  Google Scholar 

  12. Jung F, Mrowietz C, Labarrere C. Primary cutaneous micro-angiopathy in heart recipients. Microvasc Res 2001; 62:154–163.

    CAS  PubMed  Google Scholar 

  13. Arshed AQ, Riyaz SP. Endothelial dysfunction and hypertension. Cause or effect?. Hypertension 2010; 55:1092–1094.

    Google Scholar 

  14. Cheung AK, Sarnak MJ, Yan G. Cardiac diseases in maintenance hemodialysis patients: results of the HEMO Study. Kidney Int 2004; 65:2380–2389.

    Google Scholar 

  15. Ricks J, Molnar MZ, Kovesdy CP. Glycemic control and cardiovascular mortality in hemodialysis patients with diabetes: a 6-year cohort study. Diabetes 2012; 61:708–715.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Agarwal R. Blood pressure and mortality among hemodialysis patients. Hypertension 2010; 55:762–768.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Agarwal R. Volume overload in dialysis: the elephant in the room, no one can see. Am J Nephrol 2013; 38:75–77.

    PubMed  Google Scholar 

  18. Ariyamuthu VK, Balla S, Chaudhary K. Ischemic heart disease in patients undergoing dialysis. Hosp Pract (1995) 2012; 40:33–39.

    Google Scholar 

  19. Cupisti A, Rossi M, Placidi S, et al. Responses of the skin microcirculation to acetylcholine and to sodium nitroprusside in chronic uremic patients. Int J Clin Lab Res 2000; 30:157–162.

    CAS  PubMed  Google Scholar 

  20. Stewart J, Kohen A, Brouder D, Rahim F, Adler S, Garrick R, Goligorsky MS. Non-invasive interrogation of microvasculature for signs of endothelial dysfunction in patients with chronic renal failure. Am J Physiol Heart Circ Physiol 2004; 287; H2687–H2696.

    CAS  PubMed  Google Scholar 

  21. Ngo B, Rongey C, Hiscox B, Rendell M, Woodley D, Smogorzewski M. Skin blood flow in patients with stage 5 chronic kidney disease on hemodialysis. J Ren Nutr 2010; 20:S89–S94.

    PubMed  Google Scholar 

  22. Katalin F, János N, Endre K, et al. Impairment of skin micro-vascular reactivity in hypertension and uremia. Nephrol Dial Transplant 2005; 9:1821–1827.

    Google Scholar 

  23. Kocak H, Ceken K, Yavuz A, Yucel S, Gurkan A, Erdogan O, et al. Effect of renal transplantation on endothelial function in haemodialysis patients. Nephrol Dial Transplant 2006; 21:203–207.

    PubMed  Google Scholar 

  24. Passauer J, Pistrosch F, Lässig G, Herbrig K, Büssemaker E, Gross P, Fleming I. Nitric oxide- and EDHF-mediated arteriolar tone in uremia is unaffected by selective inhibition of vascular cytochrome P450 2C9. Kidney Int 2005; 67:1907–1912.

    CAS  PubMed  Google Scholar 

  25. Pannier B, Guerin AP, Marchais SJ, et al. Post-ischemic vasodilation, endothelial activation, and cardiovascular remodeling in end-stage renal disease. Kidney Int 2000; 57:1091–1099.

    CAS  PubMed  Google Scholar 

  26. Cross JM, Donald A, Vallance PJ, Deanfield JE, Woolfson RG, MacAllister RJ. Dialysis improves endothelial function in humans. Nephrol Dial Transplant 2001; 16:1823–1829.

    CAS  PubMed  Google Scholar 

  27. Hirschl M, Kundi M, Hirschl MM. Microcirculation of nailfold capillaries in chronic hemodialysis patients with and without diabetes mellitus. Clin Nephrol 1993; 40:179–184.

    CAS  PubMed  Google Scholar 

  28. Virdis A, Taddei S. How to evaluate microvascular organ damage in hypertension: assessment of endothelial function. High Blood Press Cardiovasc Prev 2011; 18:163–167.

    PubMed  Google Scholar 

  29. Zairova AR, Oshchepkova EV, Rogoza AN. Vasomotor endothelial dysfunction in young men with grade 1 arterial hypertension. Kardiologiia 2013; 53:24–30.

    CAS  PubMed  Google Scholar 

  30. Puddu P, Puddu GM, Zaca F, et al. Endothelial dysfunction in hypertension. Acta Cardiol 2000; 55:221–232.

    CAS  PubMed  Google Scholar 

  31. Ghiadoni L, Taddei S, Virdis A. Hypertension and endothelial dysfunction: therapeutic approach. Curr Vasc Pharmacol 2012; 10:42–60.

    CAS  PubMed  Google Scholar 

  32. Weinbacher M, Martina B, Gasser P, et al. Nail fold capillaroscopy and echocardiography in mild-to-moderate hypertension treated with cilazapril plus hydrochlorothiazide: first results. J Cardiovasc Pharmacol 1994; 24:S83–S85.

    CAS  PubMed  Google Scholar 

  33. Bonacci E, Santacroce N, D’Amico N, et al. Nail-fold capillaroscopy in the study of microcirculation in elderly hypertensive patients. Arch Gerontol Geriatr 1996; 22:79–83.

    PubMed  Google Scholar 

  34. Noon JP, Walker BR, Webb DJ, et al. Impaired microvascular dilatation and capillary rarefaction in young adults with a predisposition to high blood pressure. J Clin Invest 1997; 99:1873–1879.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Kanishcheva E, Fedorovich A, Loukianov M, et al. Capillary nail bed parameters in hypertensives and normotensives in age group of 60–80 years. J Hypertens 2010; 28:Pp. 11.438.

    Google Scholar 

  36. Van der Veldt AA, de Boer MP, Boven E, et al. Reduction in skin microvascular density and changes in vessel morphology in patients treated with sunitinib. Anticancer Drugs 2010; 21:439–446.

    PubMed  Google Scholar 

  37. Stam F, van Guldener C, Schalkwijk CG, ter Wee PM, Donker AJM, Stehouwer CDA. Impaired renal function is associated with markers of endothelial dysfunction and increased inflammatory activity. Nephrol Dial Transplant 2003; 18:892–898.

    PubMed  Google Scholar 

  38. Yelken B, Caliskan Y, Gorgulu N, Altun I, Yilmaz A, Yazici H, et al. Reduction of uric acid levels with allopurinol treatment improves endothelial function in patients with chronic kidney disease. Clin Nephrol 2012; 77:275–282.

    CAS  PubMed  Google Scholar 

  39. Wang Y, Bao X. Effects of uric acid on endothelial dysfunction in early chronic kidney disease and its mechanisms. Eur J Med Res 2013; 18:26.

    PubMed  PubMed Central  Google Scholar 

  40. Shuto E, Taketani Y, Tanaka R, Harada N, et al. Dietary phosphorus acutely impairs endothelial function. J Am Soc Nephrol 2009; 20:1504–1512.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Waheed AA, Pedraza F, Lenz O, Isakova T. Phosphate control in endstage renal disease: barriers and opportunities. Nephrol Dial Transplant 2013; 2961–2968.

  42. Jin X, Rong S, Mei C, Ye C, et al. Effects of in-center nocturnal versus conventional hemodialysis on endothelial dysfunction. Ther Apher Dial 2012; 16:334–340.

    CAS  PubMed  Google Scholar 

  43. Choi SR, Lim JH, Kim MY, Hong YA, et al. Cinacalcet improves endothelial dysfunction and cardiac hypertrophy in patients on hemodialysis with secondary hyperparathyroidism. Nephron Clin Pract 2012; 122:1–8.

    CAS  PubMed  Google Scholar 

  44. Bosworth C, Sachs MC, Duprez D, Hoofnagle AN, et al. Parathyroid hormone and arterial dysfunction in the multi-ethnic study of atherosclerosis. Clin Endocrinol (Oxf) 2013; 79:429–436.

    CAS  Google Scholar 

  45. Solak Y, Yilmaz MI, Saglam M, Caglar K, et al. Red cell distribution width is independently related to endothelial dysfunction in patients with chronic kidney disease. Am J Med Sci 2014; 347:118–124.

    PubMed  Google Scholar 

  46. Solak Y, Yilmaz MI, Saglam M, Demirbas S, et al. Mean corpuscular volume is associated with endothelial dysfunction and predicts composite cardiovascular events in patients with chronic kidney disease. Nephrology (Carlton) 2013; 18:728–735.

    CAS  Google Scholar 

  47. Huertas A, Das SR, Emin M, Sun L, et al. Erythrocytes induce pro-inflammatory endothelial activation in hypoxia. Am J Respir Cell Mol Biol 2013; 48:78–86.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Cortese-Krott MM, Rodriguez-Mateos A, Sansone R, Kuhnle GG, et al. Human red blood cells at work: identification and visualization of erythrocytic eNOS activity in health and disease. Blood 2012; 120:4229–4237.

    CAS  PubMed  Google Scholar 

  49. Taddei S, Fabio G, Virdio A, et al. Physical activity prevents age-related impairment in nitric oxide availability in elderly athletes. Circulation 2002; 101:2896–2901.

    Google Scholar 

  50. Carr A, Frei B. The role of natural antioxidants in preserving the biological activity of endothelium derived NO. Free Radic Biol Med 2000; 28:1806–1814.

    CAS  PubMed  Google Scholar 

  51. Andrew MK. Statins, platelets, and the elderly. J Geriatr Cardiol 2007; 4:218–219.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Cairo University, Cairo, Egypt

    Maggie S. El-Nahid MD & Ali M. El-Ashmaoui

Authors
  1. Maggie S. El-Nahid MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali M. El-Ashmaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maggie S. El-Nahid MD.

Rights and permissions

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

El-Nahid, M.S., El-Ashmaoui, A.M. Functional and structural abnormalities of the skin microcirculation in hemodialysis patients. Egypt J Intern Med 26, 116–123 (2014). https://doi.org/10.4103/1110-7782.145307

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.4103/1110-7782.145307

Keywords

  • capillaroscopy
  • endothelial dysfunction
  • hemodialysis
  • laser Doppler fluxmetry