The association of skin autofluorescence with cardiovascular events and all-cause mortality in persons with chronic kidney disease stage 3: A prospective cohort study
Autoři:
Adam Shardlow aff001; Natasha J. McIntyre aff001; Nitin V. Kolhe aff002; Laura B. Nellums aff003; Richard J. Fluck aff002; Christopher W. McIntyre aff004; Maarten W. Taal aff001
Působiště autorů:
Centre for Kidney Research and Innovation, Division of Medical Sciences and Graduate Entry Medicine, School of Medicine, University of Nottingham, Derby, United Kingdom
aff001; Renal Unit, Royal Derby Hospital, Derby, United Kingdom
aff002; Division of Epidemiology and Public Health, School of Medicine, University of Nottingham, Nottingham, United Kingdom
aff003; Division of Nephrology, Schulich School of Medicine and Dentistry, University of Western Ontario, London, Ontario, Canada
aff004; Department of Nephrology, The Victoria Hospital, London Health Sciences Centre, London, Ontario, Canada
aff005
Vyšlo v časopise:
The association of skin autofluorescence with cardiovascular events and all-cause mortality in persons with chronic kidney disease stage 3: A prospective cohort study. PLoS Med 17(7): e32767. doi:10.1371/journal.pmed.1003163
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pmed.1003163
Souhrn
Background
Tissue advanced glycation end product (AGE) accumulation has been proposed as a marker of cumulative metabolic stress that can be assessed noninvasively by measurement of skin autofluorescence (SAF). In persons on haemodialysis, SAF is an independent risk factor for cardiovascular events (CVEs) and all-cause mortality (ACM), but data at earlier stages of chronic kidney disease (CKD) are inconclusive. We investigated SAF as a risk factor for CVEs and ACM in a prospective study of persons with CKD stage 3.
Methods and findings
Participants with estimated glomerular filtration rate (eGFR) 59 to 30 mL/min/1.73 m2 on two consecutive previous blood tests were recruited from 32 primary care practices across Derbyshire, United Kingdom between 2008 and 2010. SAF was measured in participants with CKD stage 3 at baseline, 1, and 5 years using an AGE reader (DiagnOptics). Data on hospital admissions with CVEs (based on international classification of diseases [ICD]-10 coding) and deaths were obtained from NHS Digital. Cox proportional hazards models were used to investigate baseline variables associated with CVEs and ACM. A total of 1,707 of 1,741 participants with SAF readings at baseline were included in this analysis: The mean (± SD) age was 72.9 ± 9.0 years; 1,036 (60.7%) were female, 1,681 (98.5%) were of white ethnicity, and mean (±SD) eGFR was 53.5 ± 11.9 mL/min/1.73 m2. We observed 319 deaths and 590 CVEs during a mean of 6.0 ± 1.5 and 5.1 ± 2.2 years of observation, respectively. Higher baseline SAF was an independent risk factor for CVEs (hazard ratio [HR] 1.12 per SD, 95% CI 1.03–1.22, p = 0.01) and ACM (HR 1.16, 95% CI 1.03–1.30, p = 0.01). Additionally, increase in SAF over 1 year was independently associated with subsequent CVEs (HR 1.11 per SD, 95% CI 1.00–1.22; p = 0.04) and ACM (HR 1.24, 95% CI 1.09–1.41, p = 0.001). We relied on ICD-10 codes to identify hospital admissions with CVEs, and there may therefore have been some misclassification.
Conclusions
We have identified SAF as an independent risk factor for CVE and ACM in persons with early CKD. These findings suggest that interventions to reduce AGE accumulation, such as dietary AGE restriction, may reduce cardiovascular risk in CKD, but this requires testing in prospective randomised trials. Our findings may not be applicable to more ethnically diverse or younger populations.
Klíčová slova:
Albumins – Blood pressure – Cardiovascular diseases – Creatinine – diabetes mellitus – Chronic kidney disease – Medical risk factors – Urine
Zdroje
1. Arsov S, Graaff R, van Oeveren W, Stegmayr B, Sikole A, Rakhorst G, et al. Advanced glycation end-products and skin autofluorescence in end-stage renal disease: a review. Clin Chem Lab Med. 2014;52(1): 11–20. doi: 10.1515/cclm-2012-0832 23612551
2. Horner DV, Taal MW. Skin autofluorescence: an emerging biomarker in persons with kidney disease. Curr Opin Nephrol Hypertens. 2019;28(6): 507–12. doi: 10.1097/MNH.0000000000000549 31589190
3. Uribarri J, Woodruff S, Goodman S, Cai W, Chen X, Pyzik R, et al. Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Diet Assoc. 2010;110(6): 911–16 e12. doi: 10.1016/j.jada.2010.03.018 20497781
4. Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, et al. Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci U S A. 1997;94(25): 13915–20. doi: 10.1073/pnas.94.25.13915 9391127
5. Koschinsky T, He CJ, Mitsuhashi T, Bucala R, Liu C, Buenting C, et al. Orally absorbed reactive glycation products (glycotoxins): an environmental risk factor in diabetic nephropathy. Proc Natl Acad Sci U S A. 1997;94(12): 6474–9. doi: 10.1073/pnas.94.12.6474 9177242
6. Meerwaldt R, Hartog JW, Graaff R, Huisman RJ, Links TP, den Hollander NC, et al. Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients. J Am Soc Nephrol. 2005;16(12): 3687–93. doi: 10.1681/ASN.2005020144 16280473
7. Weiner DE, Tighiouart H, Elsayed EF, Griffith JL, Salem DN, Levey AS, et al. The Framingham predictive instrument in chronic kidney disease. J Am Coll Cardiol. 2007;50(3): 217–24. doi: 10.1016/j.jacc.2007.03.037 17631213
8. McIntyre NJ, Fluck RJ, McIntyre CW, Taal MW. Skin autofluorescence and the association with renal and cardiovascular risk factors in chronic kidney disease stage 3. Clin J Am Soc Nephrol. 2011;6(10): 2356–63. doi: 10.2215/CJN.02420311 21885790
9. Fraser SD, Roderick PJ, McIntyre NJ, Harris S, McIntyre CW, Fluck RJ, et al. Skin Autofluorescence and All-Cause Mortality in Stage 3 CKD. Clin J Am Soc Nephrol. 2014.
10. Shardlow A, McIntyre NJ, Fluck RJ, McIntyre CW, Taal MW. Chronic Kidney Disease in Primary Care: Outcomes after Five Years in a Prospective Cohort Study. PLoS Med. 2016;13(9): e1002128. doi: 10.1371/journal.pmed.1002128 27648564
11. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med. 1999;130(6): 461–70. doi: 10.7326/0003-4819-130-6-199903160-00002 10075613
12. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150(9): 604–12. doi: 10.7326/0003-4819-150-9-200905050-00006 19414839
13. Cavero-Redondo I, Soriano-Cano A, Alvarez-Bueno C, Cunha PG, Martinez-Hortelano JA, Garrido-Miguel M, et al. Skin Autofluorescence-Indicated Advanced Glycation End Products as Predictors of Cardiovascular and All-Cause Mortality in High-Risk Subjects: A Systematic Review and Meta-analysis. J Am Heart Assoc. 2018;7(18): e009833. doi: 10.1161/JAHA.118.009833 30371199
14. Arsov S, Trajceska L, van Oeveren W, Smit AJ, Dzekova P, Stegmayr B, et al. Increase in skin autofluorescence and release of heart-type fatty acid binding protein in plasma predicts mortality of hemodialysis patients. Artif Organs. 2013;37(7): E114–22. doi: 10.1111/aor.12078 23635017
15. Macsai E, Benke A, Kiss I. Skin Autofluorescence and Mortality in Patients on Peritoneal Dialysis. Medicine. 2015;94(45): e1933. doi: 10.1097/MD.0000000000001933 26559261
16. Siriopol D, Hogas S, Veisa G, Mititiuc I, Volovat C, Apetrii M, et al. Tissue advanced glycation end products (AGEs), measured by skin autofluorescence, predict mortality in peritoneal dialysis. Int Urol Nephrol. 2015;47(3): 563–9. doi: 10.1007/s11255-014-0870-3 25425437
17. Mukai H, Svedberg O, Lindholm B, Dai L, Heimburger O, Barany P, et al. Skin autofluorescence, arterial stiffness and Framingham risk score as predictors of clinical outcome in chronic kidney disease patients: a cohort study. Nephrol Dial Transplant. 2019;34(3): 442–8. doi: 10.1093/ndt/gfx371 29378035
18. Wang AY, Wong CK, Yau YY, Wong S, Chan IH, Lam CW. Skin autofluorescence associates with vascular calcification in chronic kidney disease. Arteriosclerosis, thrombosis, and vascular biology. 2014;34(8): 1784–90. doi: 10.1161/ATVBAHA.114.303378 24876353
19. Sanchez E, Betriu A, Arroyo D, Lopez C, Hernandez M, Rius F, et al. Skin Autofluorescence and Subclinical Atherosclerosis in Mild to Moderate Chronic Kidney Disease: A Case-Control Study. PLoS ONE. 2017;12(1): e0170778. doi: 10.1371/journal.pone.0170778 28141808
20. van Waateringe RP, Fokkens BT, Slagter SN, van der Klauw MM, van Vliet-Ostaptchouk JV, Graaff R, et al. Skin autofluorescence predicts incident type 2 diabetes, cardiovascular disease and mortality in the general population. Diabetologia. 2019;62(2): 269–80. doi: 10.1007/s00125-018-4769-x 30460578
21. Linden E, Cai W, He JC, Xue C, Li Z, Winston J, et al. Endothelial dysfunction in patients with chronic kidney disease results from advanced glycation end products (AGE)-mediated inhibition of endothelial nitric oxide synthase through RAGE activation. Clin J Am Soc Nephrol. 2008;3(3): 691–8. doi: 10.2215/CJN.04291007 18256374
22. Lindsey JB, Cipollone F, Abdullah SM, McGuire DK. Receptor for advanced glycation end-products (RAGE) and soluble RAGE (sRAGE): cardiovascular implications. Diab Vasc Dis Res. 2009;6(1): 7–14. doi: 10.3132/dvdr.2009.002 19156622
23. Wendt T, Harja E, Bucciarelli L, Qu W, Lu Y, Rong LL, et al. RAGE modulates vascular inflammation and atherosclerosis in a murine model of type 2 diabetes. Atherosclerosis. 2006;185(1): 70–7. doi: 10.1016/j.atherosclerosis.2005.06.013 16076470
24. Crowley LE, Johnson CP, McIntyre N, Fluck RJ, McIntyre CW, Taal MW, et al. Tissue advanced glycation end product deposition after kidney transplantation. Nephron Clin Pract. 2013;124(1–2): 54–9. doi: 10.1159/000355692 24135496
25. Nongnuch A, Davenport A. The effect of vegetarian diet on skin autofluorescence measurements in haemodialysis patients. Br J Nutr. 2015;113(7): 1040–3. doi: 10.1017/S0007114515000379 25761438
26. Peppa M, Uribarri J, Cai W, Lu M, Vlassara H. Glycoxidation and inflammation in renal failure patients. Am J Kidney Dis. 2004;43(4): 690–5. doi: 10.1053/j.ajkd.2003.11.022 15042546
27. Yacoub R, Nugent M, Cai W, Nadkarni GN, Chaves LD, Abyad S, et al. Advanced glycation end products dietary restriction effects on bacterial gut microbiota in peritoneal dialysis patients; a randomized open label controlled trial. PLoS ONE. 2017;12(9): e0184789. doi: 10.1371/journal.pone.0184789 28931089
28. de Lusignan S, Tomson C, Harris K, van Vlymen J, Gallagher H. Creatinine fluctuation has a greater effect than the formula to estimate glomerular filtration rate on the prevalence of chronic kidney disease. Nephron Clin Pract. 2011;117(3): c213–24. doi: 10.1159/000320341 20805694
29. Li X, Meng X, He Y, Spiliopoulou A, Timofeeva M, Wei WQ, et al. Genetically determined serum urate levels and cardiovascular and other diseases in UK Biobank cohort: A phenome-wide mendelian randomization study. PLoS Med. 2019;16(10): e1002937. doi: 10.1371/journal.pmed.1002937 31626644
Článek vyšel v časopise
PLOS Medicine
2020 Číslo 7
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- „Jednohubky“ z klinického výzkumu – 2024/44
- Je libo čepici místo mozkového implantátu?
Nejčtenější v tomto čísle
- Obesity, clinical, and genetic predictors for glycemic progression in Chinese patients with type 2 diabetes: A cohort study using the Hong Kong Diabetes Register and Hong Kong Diabetes Biobank
- Participation in adherence clubs and on-time drug pickup among HIV-infected adults in Zambia: A matched-pair cluster randomized trial
- Estimation of SARS-CoV-2 mortality during the early stages of an epidemic: A modeling study in Hubei, China, and six regions in Europe
- Neonatal outcome in 29 pregnant women with COVID-19: A retrospective study in Wuhan, China