Increased cardiovascular risk in rats with primary renal dysfunction; Mediating role for vascular endothelial function

Basic Research in Cardiology

Volumn 107, Issue 2, 2012, Pages

  Szymanski, M K ^a   Buikema, J H ^a   Van Veldhuisen, D J ^a   Koster, J ^a   Van Der Velden, J ^b   Hamdani, N ^b   Hillege, J L ^a   Schoemaker, R G ^a,c,d  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d Center for Life Sciences   (Netherlands)

Author keywords

Cardiorenal; Congestive heart failure; Endothelial dysfunction

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIORENAL SYNDROME; CARDIOVASCULAR RISK; CONTROLLED STUDY; CORRELATION ANALYSIS; DIASTOLIC DYSFUNCTION; DISEASE MODEL; ENDOTHELIAL DYSFUNCTION; FOCAL GLOMERULOSCLEROSIS; HEART ATRIUM WEIGHT; HEART INFARCTION; HEART LEFT VENTRICLE OVERLOAD; HEART OUTPUT; HEART RIGHT VENTRICLE HYPERTROPHY; HEART WEIGHT; KIDNEY BLOOD FLOW; KIDNEY DYSFUNCTION; LUNG WEIGHT; MALE; NONHUMAN; PROTEINURIA; RAT; VASCULAR ENDOTHELIUM;

EID: 84855794185     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-011-0242-4     Document Type: Article

References (56)

1. Bongartz LG, Braam B, Verhaar MC, Cramer MJ, Goldschmeding R, Gaillard CA, Doevendans PA, Joles JA (2010) Transient nitric oxide reduction induces permanent cardiac systolic dysfunction and worsens kidney damage in rats with chronic kidney disease. Am J Physiol Regul Integr Comp Physiol 298:R815-R823. doi:10.1152/ajpregu.00727.2009
2. Borbely A, van der Velden J, Papp Z, Bronzwaer JG, Edes I, Stienen GJ, Paulus WJ (2005) Cardiomyocyte stiffness in diastolic heart failure. Circulation 111:774-781. doi:10.1161/ 01.CIR.0000155257.33485.6D (Pubitemid 40250638)
3. Choi JH, Kim KL, Huh W, Kim B, Byun J, Suh W, Sung J, Jeon ES, Oh HY, Kim DK (2004) Decreased number and impaired angiogenic function of endothelial progenitor cells in patients with chronic renal failure. Arterioscler Thromb Vasc Biol 24:1246-1252. doi:10.1161/01.ATV.0000133488.56221.4a (Pubitemid 38880016)
4. Correia-Pinto J, Henriques-Coelho T, Roncon-Albuquerque R Jr, Lourenco AP, Melo-Rocha G, Vasques-Novoa F, Gillebert TC, Leite-Moreira AF (2009) Time course and mechanisms of left ventricular systolic and diastolic dysfunction in monocrotalineinduced pulmonary hypertension. Basic Res Cardiol 104:535-545. doi:10.1007/s00395-009-0017-3
5. Damman K, Hillege HL, van Veldhuisen DJ (2009) Albuminuria in heart failure: a CHARMing new risk factor? Lancet 374:506-508. doi:10.1016/s0140- 6736(09)61469-0
6. Damman K, Navis G, Smilde TD, Voors AA, van der Bij W, van Veldhuisen DJ, Hillege HL (2007) Decreased cardiac output, venous congestion and the association with renal impairment in patients with cardiac dysfunction. Eur J Heart Fail 9:872-878. doi:10.1016/j.ejheart.2007.05.010 (Pubitemid 47332311)
7. Damman K, Voors AA, Hillege HL, Navis G, Lechat P, van Veldhuisen DJ, Dargie HJ (2010) Congestion in chronic systolic heart failure is related to renal dysfunction and increased mortality. Eur J Heart Fail 12:974-982. doi:10.1093/eurjhf/hfq118
8. de las Heras N, Aragoncillo P, Maeso R, Vazquez-Perez S, Navarro-Cid J, DeGasparo M, Mann J, Ruilope LM, Cachofeiro V, Lahera V (1999) AT(1) receptor antagonism reduces endothelial dysfunction and intimal thickening in atherosclerotic rabbits. Hypertension 34:969-975 (Pubitemid 29501332)
9. Dikow R (2009) Effect of insulin and glucose infusion on myocardial infarction size in uraemic rats. Basic Res Cardiol 104:571-579. doi:10.1007/s00395-009-0018-2
10. Dikow R, Schmidt U, Kihm LP, Schaier M, Schwenger V, Gross ML, Katus HA, Zeier M, Hardt SE (2010) Uremia aggravates left ventricular remodeling after myocardial infarction. Am J Nephrol 32:13-22. doi:10.1159/000313846
11. Falcao-Pires I, Palladini G, Goncalves N, van der Velden J, Moreira-Goncalves D, Miranda-Silva D, Salinaro F, Paulus WJ, Niessen HW, Perlini S, Leite-Moreira AF (2011) Distinct mechanisms for diastolic dysfunction in diabetes mellitus and chronic pressure-overload. Basic Res Cardiol 106:801-814. doi: 10.1007/s00395-011-0184-x
12. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY (2004) Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351:1296-1305. doi:10.1056/NEJMoa041031 (Pubitemid 39268908)
13. Gschwend S, Buikema H, Henning RH, Pinto YM, de Zeeuw D, van Gilst WH (2003) Endothelial dysfunction and infarct-size relate to impaired EDHF response in rat experimental chronic heart failure. Eur J Heart Fail 5:147-154. doi:10.1016/S1388- 9842(02)00248-9 (Pubitemid 36383621)
14. Gschwend S, Buikema H, Navis G, Henning RH, de Zeeuw D, van Dokkum RP (2002) Endothelial dilatory function predicts individual susceptibility to renal damage in the 5/6 nephrectomized rat. J Am Soc Nephrol 13:2909-2915. doi:10.1097/01.ASN. 0000036865.22253 (Pubitemid 35386910)
15. Gschwend S, Pinto-Sietsma SJ, Buikema H, Pinto YM, van Gilst WH, Schulz A, de Zeeuw D, Kreutz R (2002) Impaired coronaryendothelial function in a rat model of spontaneous albuminuria. Kidney Int 62:181-191. doi:10.1046/j.1523- 1755.2002.00431.x (Pubitemid 34754061)
16. Herbrig K, Pistrosch F, Foerster S, Gross P (2006) Endothelial progenitor cells in chronic renal insufficiency. Kidney Blood Press Res 29:24-31. doi:10.1159/000092484 (Pubitemid 43875169)
17. Herzog CA (2002) Dismal long-term survival of dialysis patients after acute myocardial infarction: can we alter the outcome? Nephrol Dial Transplant 17:7-10. doi:10.1093/ndt/17.1.7 (Pubitemid 34092999)
18. Heusch G (2009) Diastolic heart failure: a misNOmer. Basic Res Cardiol 104:465-467. doi:10.1007/s00395-009-0025-3
19. Heywood JT, Fonarow GC, Costanzo MR, Mathur VS, Wigneswaran JR, Wynne J (2007) High prevalence of renal dysfunction and its impact on outcome in 118,465 patients hospitalized with acute decompensated heart failure: a report from the ADHERE database. J Card Fail 13:422-430. doi: 10.1016/j.cardfail.2007.03.011 (Pubitemid 47179911)
20. Hillege HL, Nitsch D, Pfeffer MA, Swedberg K, McMurray JJ, Yusuf S, Granger CB, Michelson EL, Ostergren J, Cornel JH, de Zeeuw D, Pocock S, van Veldhuisen DJ (2006) Renal function as a predictor of outcome in a broad spectrum of patients with heart failure. Circulation 113:671-678. doi:10.1161/CIRCULATIONA HA.105.580506
21. Ho-Yen DO, Saleem N, Fleming LW, Stewart WK, Goodall HB (1980) Bone marrow cellularity and iron stores in chronic renal failure. Acta Haematol 64:265-270 (Pubitemid 11243176)
22. Horina JH, Schmid CR, Roob JM, Winkler HM, Samitz MA, Hammer HF, Pogglitsch H, Krejs GJ (1991) Bone marrow changes following treatment of renal anemia with erythropoietin. Kidney Int 40:917-922
23. Jie KE, Verhaar MC, Cramer MJ, van der Putten K, Gaillard CA, Doevendans PA, Koomans HA, Joles JA, Braam B (2006) Erythropoietin and the cardiorenal syndrome: cellular mechanisms on the cardiorenal connectors. Am J Physiol Renal Physiol 291:F932-F944. doi:10.1152/ajprenal.00200.2006 (Pubitemid 44773680)
24. Joles JA, Bongartz LG, Gaillard CA, Braam B (2009) Renal venous congestion and renal function in congestive heart failure. J Am Coll Cardiol 54:1632-1633. doi:10.1016/j.jacc.2009.05.068
25. Kazory A, Ross EA (2009) Anemia: the point of convergence or divergence for kidney disease and heart failure? J Am Coll Cardiol 53:639-647. doi:10.1016/j.jacc.2008.10.046
26. Kjaergaard J, Akkan D, Iversen KK, Kjoller E, Kober L, Torp- Pedersen C, Hassager C (2007) Prognostic importance of pulmonary hypertension in patients with heart failure. Am J Cardiol 99:1146-1150. doi:10.1016/j.amjcard.2006.11.052 (Pubitemid 46578202)
27. Lamberts RR, Hamdani N, Soekhoe TW, Boontje NM, Zaremba R, Walker LA, de Tombe PP, van der Velden J, Stienen GJ (2007) Frequency-dependent myofilament Ca2? Desensitization in failing rat myocardium. J Physiol 582:695-709. doi: 10.1113/jphysiol.2007.134486 (Pubitemid 47040553)
28. Mann JF, Gerstein HC, Pogue J, Bosch J, Yusuf S (2001) Renal insufficiency as a predictor of cardiovascular outcomes and the impact of ramipril: the HOPE randomized trial. Ann Int Med 134:629-636 200104170-00007[pii] (Pubitemid 32322240)
29. Mesquita ET, Jorge AJ (2009) Heart failure with normal ejection fraction: new diagnostic criteria and pathophysiological advances. Arq Bras Cardiol 93:180-187. doi:10.1590/S0066-782X200 9000800018
30. Ochodnicky P, Henning RH, Buikema H, Kluppel AC, van Wattum M, de Zeeuw D, van Dokkum RP (2009) Renal endothelial function and blood flow predict the individual susceptibility to adriamycin-induced renal damage. Nephrol Dial Transplant 24:413-420. doi:10.1093/ndt/gfn483
31. Ochodnicky P, Vettoretti S, Henning RH, Buikema H, van Dokkum RP, de Zeeuw D (2006) Endothelial dysfunction in chronic kidney disease: determinant of susceptibility to end-organ damage and therapeutic response. J Nephrol 19:246-258 (Pubitemid 46785535)
32. Paulus WJ, Tschope C, Sanderson JE, Rusconi C, Flachskampf FA, Rademakers FE, Marino P, Smiseth OA, De KG, Leite- Moreira AF, Borbely A, Edes I, Handoko ML, Heymans S, Pezzali N, Pieske B, Dickstein K, Fraser AG, Brutsaert DL (2007) How to diagnose diastolic heart failure: a consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the Heart Failure and Echocardiography Associations of the European Society of Cardiology.Eur Heart J 28:2539-2550. doi:10.1093/eurheartj/ehm037 (Pubitemid 47614269)
33. Qian C, Schoemaker RG, van Gilst WH, Roks AJ (2009) The role of the renin-angiotensin-aldosterone system in cardiovascular progenitor cell function. Clin Sci (Lond) 116:301-314. doi: 10.1042/CS20080157
34. Rambausek M, Ritz E, Mall G, Mehls O, Katus H (1985) Myocardial hypertrophy in rats with renal insufficiency. Kidney Int 28:775-782 (Pubitemid 16156318)
35. Remuzzi A, Puntorieri S, Alfano M, Macconi D, Abbate M, Bertani T, Remuzzi G (1992) Pathophysiologic implications of proteinuria in a rat model of progressive glomerular injury. Lab Invest 67:572-579
36. Ronco C, Haapio M, House AA, Anavekar N, Bellomo R (2008) Cardiorenal syndrome. J Am Coll Cardiol 52:1527-1539. doi: 10.1016/j/jacc.2008.07.051
37. Schoemaker RG, Debets JJ, Struyker-Boudier HA, Smits JF (1991) Delayed but not immediate captopril therapy improves cardiac function in conscious rats, following myocardial infarction. J Mol Cell Cardiol 23:187-197. doi:10.1016/0022-2828(91) 90105-U
38. Schoemaker RG, Urquhart J, Debets JJ, Struyker Boudier HA, Smits JF (1990) Acute hemodynamic effects of coronary arteryligation in conscious rats. Basic Res Cardiol 85:9-20 (Pubitemid 20097098)
39. Silverberg DS, Wexler D, Iaina A, Steinbruch S, Wollman Y, Schwartz D (2006) Anemia, chronic renal disease and congestive heart failure-the cardio renal anemia syndrome: the need for cooperation between cardiologists and nephrologists. Int Urol Nephrol 38:295-310. doi:10.1007/s11255-006-0064-8 (Pubitemid 44138158)
40. Surdacki A, Legutko J, Turek P, Dudek D, Zmudka K, Dubiel JS (1996) Determinants of depressed left ventricular ejection fraction in pure mitral stenosis with preserved sinus rhythm. J Heart Valve Dis 5:1-9 (Pubitemid 26058349)
41. Szymanski MK, de Boer RA, Navis GJ, van Gilst WH, Hillege HL (2011) Animal models of cardiorenal syndrome: a review. Heart Fail Rev doi. doi:10.1007/s10741-011-9279-6
42. Teng R, Calvert JW, Sibmooh N, Piknova B, Suzuki N, Sun J, Martinez K, Yamamoto M, Schechter AN, Lefer DJ, Noguchi CT (2011) Acute erythropoietin cardioprotection is mediated by endothelial response. Basic Res Cardiol 106:343-354. doi: 10.1007/s00395-011-0158-z
43. Tyralla K, Amann K (2003) Morphology of the heart and arteries in renal failure. Kidney Int Suppl S80-S83 (Pubitemid 36513382)
44. Ulu N, Schoemaker RG, Henning RH, Buikema H, Teerlink T, Zijlstra FJ, Bakker SJ, van Gilst WH, Navis G (2009) Proteinuriaassociated endothelial dysfunction is strain dependent. Am J Nephrol 30:209-217. doi:10.1159/000218062
45. van Albada ME, Schoemaker RG, Kemna MS, Cromme-Dijkhuis AH, van Veghel R, Berger RM (2005) The role of increased pulmonary blood flow in pulmonary arterial hypertension. Eur Respir J 26:487-493. doi:10.1183/09031936.05.00015405 (Pubitemid 41264214)
46. van der Putten K, Braam B, Jie KE, Gaillard CA (2008) Mechanisms of disease: erythropoietin resistance in patients with both heart and kidney failure. Nat Clin Pract Nephrol 4:47-57. doi: 10.1038/ncpneph0655 (Pubitemid 350308210)
47. van der Zee S, Baber U, Elmariah S, Winston J, Fuster V (2009) Cardiovascular risk factors in patients with chronic kidney disease. Nat Rev Cardiol 6:580-589. doi:10.1038/nrcardio.2009.121
48. van Dokkum RP, Eijkelkamp WB, Kluppel AC, Henning RH, van Gilst H, Citgez M, Windt WA, van Veldhuisen DJ, de Graeff PA, de Zeeuw D (2004) Myocardial infarction enhances progressive renal damage in an experimental model for cardio-renal interaction. J Am SocNephrol 15:3103-3110. doi:10.1097/01. ASN.0000145895.62896 (Pubitemid 39578842)
49. van Kerckhoven R, van Veghel R, Saxena PR, Schoemaker RG (2004) Pharmacological therapy can increase capillary density inpost-infarction remodeled rat hearts. Cardiovasc Res 61:620-629. doi:10.1016/j.cardiores.2003. 09.026 (Pubitemid 38210167)
50. van der Velden J, Klein LJ, van der Bijl M, Huybregts MA, Stooker W, Witkop J, Eijsman L, Visser CA, Visser FC, Stienen GJ (1999) Isometric tension development and its calcium sensitivity in skinned myocyte-sized preparations from different regions of the human heart. Cardiovasc Res 42:706-719. doi: 10.1016/S0008-6363(98)00337-X (Pubitemid 29298140)
51. Victor BM, Barron JT (2010) Diastolic heart failure versus diastolic dysfunction: difference in renal function. Clin Cardiol 33:770-774. doi:10.1002/clc.20824
52. Westenbrink BD, Lipsic E, van der Meer P, van der Harst P, Oeseburg H, Du Marchie Sarvaas GJ, Koster J, Voors AA, van Veldhuisen DJ, van Gilst WH, Schoemaker RG (2007) Erythropoietin improves cardiac function through endothelial progenitor cell and vascular endothelial growth factor mediated neovascularization. Eur Heart J 28:2018-2027. doi:10.1093/eurheartj/ehm177 (Pubitemid 47579534)
53. Westendorp B, Schoemaker RG, van Gilst WH, Buikema H (2005) Improvement of EDHF by chronic ACE inhibition declines rapidly after withdrawal in rats with myocardial infarction. J Cardiovasc Pharmacol 46:766-772. doi:00005344-20051 2000-00008 (Pubitemid 44378248)
54. Westermann D, Riad A, Richter U, Jager S, Savvatis K, Schuchardt M, Bergmann N, Tolle M, Nagorsen D, Gotthardt M, Schultheiss HP, Tschope C (2009) Enhancement of the endothelial NO synthase attenuates experimental diastolic heart failure. Basic Res Cardiol 104:499-509. doi:10.1007/s00395- 009-0014-6
55. Windt WA, Henning RH, Kluppel AC, Xu Y, de Zeeuw D, van Dokkum RP (2008) Myocardial infarction does not further impair renal damage in 5/6 nephrectomized rats. Nephrol Dial Transplant 23:3103-3110. doi:10.1093/ndt/gfn233
56. Windt WA, van Dokkum RP, Kluppel CA, Jeronimus-Stratingh CM, Hut F, de Zeeuw D, Henning RH (2008) Therapeutic resistance to angiotensin converting enzyme (ACE) inhibition is related to pharmacodynamic and -kinetic factors in 5/6 nephrectomized rats. Eur J Pharmacol 580:231-240. doi:10.1016/ j.ejphar.2007.10.060