Nitric oxide synthesis capacity, ambulatory blood pressure and end organ damage in a black and white population: The SABPA study

Amino Acids

Volumn 48, Issue 3, 2016, Pages 801-810

  Mels, Catharina M C ^a   Loots, Ilisma ^a   Schwedhelm, Edzard ^b   Atzler, Dorothee ^b,c   Böger, Rainer H ^b   Schutte, Aletta E ^a  

^a NORTH WEST UNIVERSITY   (South Africa)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

ADMA; African; Carotid intima media thickness; Endothelial function; Estimated glomerular filtration rate; Ethnicity; Hypertension; l arginine; l citrulline; l homoarginine; Nighttime blood pressure; Renal function; SDMA; Urinary albumin to creatinine ratio

Indexed keywords

6 N,N' DIMETHYLARGININE; ALBUMIN; ARGININE; ARGININE DERIVATIVE; CITRULLINE; CREATININE; DIMETHYLARGININE; HOMOARGININE; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

ADULT; ALBUMIN TO CREATININE RATIO; AMBULATORY BLOOD PRESSURE; ARTERIAL WALL THICKNESS; ARTICLE; BLACK PERSON; BLOOD PRESSURE; CAUCASIAN; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DISEASE MARKER; END ORGAN DAMAGE; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; NIGHT; PRIORITY JOURNAL; RACE DIFFERENCE; RENAL SYSTEM PARAMETERS; SYSTOLIC BLOOD PRESSURE; TEACHER; TISSUE INJURY; AGED; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; BLOOD; CROSS-SECTIONAL STUDY; ETHNOLOGY; HYPERTENSION; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; SOUTH AMERICA;

ADULT; AFRICAN CONTINENTAL ANCESTRY GROUP; AGED; ARGININE; BIOMARKERS; BLOOD PRESSURE; CAROTID INTIMA-MEDIA THICKNESS; CITRULLINE; CROSS-SECTIONAL STUDIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; HOMOARGININE; HUMANS; HYPERTENSION; MALE; MIDDLE AGED; NITRIC OXIDE; SOUTH AMERICA;

EID: 84958153499     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-015-2128-5     Document Type: Article

References (58)

1. Achan V, Broadhead M, Malaki M, Whitley G, Leiper J, MacAllister R, Vallance P (2003) Asymmetric dimethylarginine causes hypertension and cardiac dysfunction in humans and is actively metabolized by dimethylarginine dimethylaminohydrolase. Arterioscler Thromb Vasc Biol 23(8):1455-1459. doi: 10.1161/01.ATV.0000081742.92006.59
2. Aldámiz-Echevarría L, Andrade F (2012) Asymmetric dimethylarginine, endothelial dysfunction and renal disease. Int J Mol Sci 13(9):11288-11311. doi: 10.3390/ijms130911288
3. American Diabetes Association (2014) Standards of medical care in diabetes-2014. Diabetes Care 37:S14. doi: 10.1161/ATVBAHA.114.304398
4. Atzler D, Mieth M, Maas R, Böger RH, Schwedhelm E (2011) Stable isotope dilution assay for liquid chromatography-tandem mass spectrometric determination of l-homoarginine in human plasma. J Chromatogr B 879(23):2294-2298. doi: 10.1016/j.jchromb.2011.06.016
5. Atzler D, Gore MO, Ayers CR, C-u Choe, Böger RH, de Lemos JA, McGuire DK, Schwedhelm E (2014) Homoarginine and cardiovascular outcome in the population-based dallas heart study. Arterioscler Thromb Vasc Biol 34(11):2501-2507. doi: 10.1161/ATVBAHA
6. Böger RH (2005) Asymmetric dimethylarginine (ADMA) and cardiovascular disease: insights from prospective clinical trials. Vasc Med 10(2 suppl):S19-S25. doi: 10.1191/1358863x05vm602oa
7. Busse R, Fleming I (1996) Endothelial dysfunction in atherosclerosis. J Vasc Res 33(3):181-194. doi: 10.1159/000159147
8. Butler CJ, Schutte R, Glyn MC, van der Westhuizen FH, Gona P, Schutte AE (2013) Exploring the link between serum peroxides and angiogenesis in a bi-ethnic population from South Africa: the SAfrEIC study. J Am Soc Hypertens 7(4):267-275. doi: 10.1016/j.jash.2013.04.005
9. Choe C-U, Atzler D, Wild PS, Carter AM, Böger RH, Ojeda F, Simova O, Stockebrand M, Lackner K, Nabuurs C (2013) Homoarginine levels are regulated by l-arginine: glycine amidinotransferase and affect stroke outcome results from human and murine studies. Circulation 128(13):1451-1461. doi: 10.1161/CIRCULATIONAHA.112.000580
10. Delanaye P, Schaeffner E, Ebert N, Cavalier E, Mariat C, Krzesinski J-M, Moranne O (2012) Normal reference values for glomerular filtration rate: what do we really know? Nephrol Dial Transplant 27(7):2664-2672. doi: 10.1093/ndt/gfs265
11. Dharmashankar K, Widlansky ME (2010) Vascular endothelial function and hypertension: insights and directions. Curr Hypertens Rep 12(6):448-455. doi: 10.1007/s11906-010-0150-2
12. Drechsler C, Kollerits B, Meinitzer A, März W, Ritz E, König P, Neyer U, Pilz S, Wanner C, Kronenberg F (2013) Homoarginine and progression of chronic kidney disease: results from the mild to moderate kidney disease study. PLoS One 8(5):e63560. doi: 10.1371/journal.pone.0063560
13. Duranton F, Lundin U, Gayrard N, Mischak H, Aparicio M, Mourad G, Daurès J-P, Weinberger KM, Argilés À (2013) Plasma and urinary amino acid metabolomic profiling in patients with different levels of kidney function. Clin J Am Soc Nephrol 9:37-45. doi: 10.2215/CJN.06000613
14. Fleck C, Janz A, Schweitzer F, Karge E, Schwertfeger M, Stein G (2001) Serum concentrations of asymmetric (ADMA) and symmetric (SDMA) dimethylarginine in renal failure patients. Kidney Int 59:S14-S18. doi: 10.1046/j.1523-1755.2001.59780014.x
15. Fliser D, Kronenberg F, Kielstein JT, Morath C, Bode-Böger SM, Haller H, Ritz E (2005) Asymmetric dimethylarginine and progression of chronic kidney disease: the mild to moderate kidney disease study. J Am Soc Nephrol 16(8):2456-2461. doi: 10.1681/ASN.2005020179
16. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18(6):499-502
17. Furuki K, Adachi H, Matsuoka H, Enomoto M, Satoh A, Hino A, Hirai Y, Imaizumi T (2007) Plasma levels of asymmetric dimethylarginine (ADMA) are related to intima-media thickness of the carotid artery: an epidemiological study. Atherosclerosis 191(1):206-210. doi: 10.1016/j.atherosclerosis.2006.03.022
18. Furuki K, Adachi H, Enomoto M, Otsuka M, Fukami A, S-i Kumagae, Matsuoka H, Nanjo Y, Kakuma T, Imaizumi T (2008) Plasma level of asymmetric dimethylarginine (ADMA) as a predictor of carotid intima-media thickness progression: six-year prospective study using carotid ultrasonography. Hypertens Res 31(6):1185-1189. doi: 10.1291/hypres.31.1185
19. Glyn M, Anderssohn M, Lüneburg N, Van Rooyen J, Schutte R, Huisman H, Fourie C, Smith W, Malan L, Malan N (2012) Ethnicity-specific differences in l-arginine status in South African men. J Hum Hypertens 26(12):737-743. doi: 10.1038/jhh.2011.103
20. Hanai K, Babazono T, Nyumura I, Toya K, Tanaka N, Tanaka M, Ishii A, Iwamoto Y (2009) Asymmetric dimethylarginine is closely associated with the development and progression of nephropathy in patients with type 2 diabetes. Nephrol Dial Transplant 24(6):1884-1888. doi: 10.1093/ndt/gfn716
21. Higashi Y, Nakagawa K, Kimura M, Noma K, Hara K, Sasaki S, Goto C, Oshima T, Chayama K, Yoshizumi M (2002) Circadian variation of blood pressure and endothelial function in patients with essential hypertension: a comparison of dippers and non-dippers. J Am Coll Cardiol 40(11):2039. doi: 10.1016/S0735-1097(02)02535-4
22. Ikeda H, Takajo Y, Murohara T, Ichiki K, Adachi H, Haramaki N, Katoh A, Imaizumi T (2000) Platelet-derived nitric oxide and coronary risk factors. Hypertension 35(4):904-907. doi: 10.1161/01.HYP.35.4.904
23. Kalinowski L, Dobrucki IT, Malinski T (2004) Race-specific differences in endothelial function predisposition of African Americans to vascular diseases. Circulation 109(21):2511-2517
24. Ikeda H, Takajo Y, Haramaki N, Murohara T, Shintani S, Kanaya S, Yokoyama S, Ueno T, Honma T (2002) Coexistence of impairment of endothelium-derived nitric oxide and platelet-derived nitric oxide in patients with coronary risk factors. Circ J 66(9):837-840. doi: 10.1253/circj.66.837
25. Kielstein JT, Bode-Böger SM, Frölich JC, Ritz E, Haller H, Fliser D (2003) Asymmetric dimethylarginine, blood pressure, and renal perfusion in elderly subjects. Circulation 107(14):1891-1895. doi: 10.1161/01.CIR.0000060496.23144.A7
26. Kielstein JT, Impraim B, Simmel S, Bode-Böger SM, Tsikas D, Frölich JC, Hoeper MM, Haller H, Fliser D (2004) Cardiovascular effects of systemic nitric oxide synthase inhibition with asymmetrical dimethylarginine in humans. Circulation 109(2):172-177. doi: 10.1161/01.CIR.0000105764.22626.B1
27. Kielstein JT, Salpeter SR, Bode-Boeger SM, Cooke JP, Fliser D (2006) Symmetric dimethylarginine (SDMA) as endogenous marker of renal function - a meta-analysis. Nephrol Dial Transplant 21(9):2446-2451. doi: 10.1093/ndt/gfl292
28. Kleber ME, Seppälä I, Pilz S, Hoffmann MM, Tomaschitz A, Oksala N, Raitoharju E, Lyytikäinen L-P, Mäkelä K-M, Laaksonen R (2013) Genome-wide association study identifies 3 genomic loci significantly associated with serum levels of homoarginine the atheroremo consortium. Circulation: Cardiovascular Genetics 6 (5):505-513. doi:10.1161/CIRCGENETICS.113.000108
29. Kohara K, Nishida W, Maguchi M, Hiwada K (1995) Autonomic nervous function in non-dipper essential hypertensive subjects evaluation by power spectral analysis of heart rate variability. Hypertension 26(5):808-814. doi: 10.1161/01.HYP.26.5.808
30. Kuo H-C, Hsu C-N, Huang C-F, Lo M-H, Chien S-J, Tain Y-L (2012) Urinary arginine methylation index associated with ambulatory blood pressure abnormalities in children with chronic kidney disease. J Am Soc Hypertens 6(6):385-392. doi: 10.1016/j.jash.2012.09.003
31. Lau T, Owen W, Yu YM, Noviski N, Lyons J, Zurakowski D, Tsay R, Ajami A, Young VR, Castillo L (2000) Arginine, citrulline, and nitric oxide metabolism in end-stage renal disease patients. J Clin Invest 105(9):1217-1225. doi: 10.1172/JCI7199
32. Leone A, Moncada S, Vallance P, Calver A, Collier J (1992) Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 339(8793):572-575. doi: 10.1016/0140-6736(92)90865-Z
33. Lloyd-Sherlock P, Beard J, Minicuci N, Ebrahim S, Chatterji S (2014) Hypertension among older adults in low-and middle-income countries: prevalence, awareness and control. Int J Epidemiol 43(1):116-128. doi: 10.1093/ije/dyt215
34. Luescher TF, Barton M (1997) Biology of the endothelium. Clin Cardiol 3-10 20(11):3-10
35. Malan L, Hamer M, Frasure-Smith N, Steyn HS, Malan NT (2014) COHORT PROFILE: sympathetic activity and ambulatory blood pressure in Africans (SABPA) prospective cohort study. Int J Epidemiol. doi: 10.1093/ije/dyu199
36. Mancia G, Fagard R, Narkiewicz K, Redán J, Zanchetti A, Böhm M, Christiaens T, Cifkova R, De Backer G, Dominiczak A (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. doi: 10.1097/HJH.0b013e328364ca4c
37. Marfell-Jones MJ, Stewart A, de Ridder J (2012) International standards for anthropometric assessment. International Society for the Advancement of Kinanthropometry, Wellington
38. März W, Meinitzer A, Drechsler C, Pilz S, Krane V, Kleber ME, Fischer J, Winkelmann BR, Böhm BO, Ritz E (2010) Homoarginine, cardiovascular risk, and mortality. Circulation 122(10):967-975. doi: 10.1161/CIRCULATIONAHA.109.908988
39. Melikian N, Wheatcroft SB, Ogah OS, Murphy C, Chowienczyk PJ, Wierzbicki AS, Sanders TA, Jiang B, Duncan ER, Shah AM (2007) Asymmetric dimethylarginine and reduced nitric oxide bioavailability in young Black African men. Hypertension 49(4):873-877. doi: 10.1161/01.HYP.0000258405.25330.80
40. Mels C, Schutte A, Schutte R, Huisman H, Smith W, Fourie C, Kruger R, Van Rooyen J, Malan N, Malan L (2013) The link between vascular deterioration and branched chain amino acids in a population with high glycated haemoglobin: the SABPA study. Amino Acids 45(6):1405-1413. doi: 10.1007/s00726-013-1611-0
41. Mels CM, Schutte AE, Schutte R, Pretorius PJ, Smith W, Huisman HW, van der Westhuizen FH, Fourie CM, van Rooyen JM, Kruger R (2014) 8-Oxo-7, 8-dihydro-2′-deoxyguanosine, reactive oxygen species and ambulatory blood pressure in African and Caucasian men: the SABPA study. Free Radical Res 48(11):1291-1299. doi: 10.3109/10715762.2014.951840
42. Miyazaki H, Matsuoka H, Cooke JP, Usui M, Ueda S, Okuda S, Imaizumi T (1999) Endogenous nitric oxide synthase inhibitor a novel marker of atherosclerosis. Circulation 99(9):1141-1146. doi: 10.1161/01.CIR.99.9.1141
43. Morris SM (1992) Regulation of enzymes of urea and arginine synthesis. Annu Rev Nutr 12(1):81-101. doi: 10.1146/annurev.nu.12.070192.000501
44. Palm F, Onozato ML, Luo Z, Wilcox CS (2007) Dimethylarginine dimethylaminohydrolase (DDAH): expression, regulation, and function in the cardiovascular and renal systems. Am J Physiol Heart Circ Physiol 293(6):H3227-H3245. doi: 10.1152/ajpheart.00998.2007
45. Ravani P, Maas R, Malberti F, Pecchini P, Mieth M, Quinn R, Tripepi G, Mallamaci F, Zoccali C (2013) Homoarginine and mortality in pre-dialysis chronic kidney disease (CKD) patients. PLoS One. doi: 10.1371/journal.pone.0072694
46. Reimann M, Hamer M, Malan NT, Schlaich MP, Lambert GW, Ziemssen T, Boeger RH, Malan L (2013) Effects of acute and chronic stress on the l-arginine nitric oxide pathway in black and white South Africans: the sympathetic activity and ambulatory blood pressure in Africans study. Psychosom Med 75(8):751-758. doi: 10.1097/PSY.0b013e3182a3e465
47. Schutte AE, Schutte R, Huisman HW, van Rooyen JM, Fourie CM, Malan L, Malan NT, Schwedhelm E, Strimbeanu S, Anderssohn M (2010) Dimethylarginines: their vascular and metabolic roles in Africans and Caucasians. Eur J Endocrinol 162(3):525-533. doi: 10.1530/EJE-09-0865
48. Schwedhelm E, Maas R, Tan-Andresen J, Schulze F, Riederer U, Böger RH (2007) High-throughput liquid chromatographic-tandem mass spectrometric determination of arginine and dimethylated arginine derivatives in human and mouse plasma. J Chromatogr B 851(1):211-219. doi: 10.1016/j.jchromb.2006.11.052
49. Schwedhelm E, Xanthakis V, Maas R, Sullivan LM, Atzler D, Lüneburg N, Glazer NL, Riederer U, Vasan RS, Böger RH (2011) Plasma symmetric dimethylarginine reference limits from the Framingham offspring cohort. Clin Chem Lab Med 49(11):1907-1910. doi: 10.1515/cclm.2011.679
50. Siegerink B, Maas R, Vossen CY, Schwedhelm E, Koenig W, Böger R, Rothenbacher D, Brenner H, Breitling LP (2013) Asymmetric and symmetric dimethylarginine and risk of secondary cardiovascular disease events and mortality in patients with stable coronary heart disease: the KAROLA follow-up study. Clin Res Cardiol 102(3):193-202. doi: 10.1007/s00392-012-0515-4
51. Sliwa K, Wilkinson D, Hansen C, Ntyintyane L, Tibazarwa K, Becker A, Stewart S (2008) Spectrum of heart disease and risk factors in a black urban population in South Africa (the Heart of Soweto Study): a cohort study. Lancet 371(9616):915-922. doi: 10.1016/S0140-6736(08)60417-1
52. Tomaschitz A, Meinitzer A, Pilz S, Rus-Machan J, Genser B, Drechsler C, Grammer T, Krane V, Ritz E, Kleber ME (2014) Homoarginine, kidney function and cardiovascular mortality risk. Nephrol Dial Transplant 29(3):663-671. doi: 10.1093/ndt/gft512
53. Tousoulis D, Antoniades C, Tentolouris C, Goumas G, Stefanadis C, Toutouzas P (2002) l-Arginine in cardiovascular disease: dream or reality? Vasc Med 7(3):203-211. doi: 10.1191/1358863x02vm434ra
54. Tsioufis C, Dimitriadis K, Andrikou E, Thomopoulos C, Tsiachris D, Stefanadi E, Mihas C, Miliou A, Papademetriou V, Stefanadis C (2010) ADMA, C-reactive protein, and albuminuria in untreated essential hypertension: a cross-sectional study. Am J Kidney Dis 55(6):1050-1059. doi: 10.1053/j.ajkd.2009.11.024
55. Van der Zwan LP, Davids M, Scheffer PG, Dekker JM, Stehouwer CD, Teerlink T (2013) L-Homoarginine and l-arginine are antagonistically related to blood pressure in an elderly population: the Hoorn study. J Hypertens 31(6):1114-1123. doi: 10.1097/HJH.0b013e32836037fb
56. Van Rooyen J, Kruger H, Huisman H, Wissing M, Margetts B, Venter C, Vorster H (2000) An epidemiological study of hypertension and its determinants in a population in transition: the THUSA study. J Hum Hypertens 14(12):779-787. doi: 10.1038/sj.jhh.1001098
57. Widlansky ME, Gokce N, Keaney JF, Vita JA (2003) The clinical implications of endothelial dysfunction. J Am Coll Cardiol 42(7):1149-1160. doi: 10.1016/S0735-1097(03)00994-X
58. Wu G, Morris J (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1-17