Progressive Renal Disease: A Disorder of Adaptation
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1 Quarterly Journal of Medicine. New Series 70. No. 263, pp , March 1989 Editorial Progressive Renal Disease: A Disorder of Adaptation SHARON ANDERSON and BARRY M. BRENNER From the Renal Division and Department of Medicine, Brigham and Women's Hospital, and The Harvard Center for The Study of Kidney Diseases, Harvard Medical School, Boston, MA 02115, U.S.A Chronic renal insufficiency generally progresses to end-stage renal failure, suggesting that, after a certain point, reduction in functioning nephron number leads to failure of the remaining units. A well-recognized risk factor contributing to acceleration of renal disease is systemic hypertension, which may be both cause and consequence of chronic renal disease. However, clinical studies have not uniformly demonstrated slowing of progressive renal disease with antihypertensive therapy. Recent studies in animal models of hypertensive renal disease have provided insight into this apparent paradox by clarifying the complex and variable relationship between systemic and glomerular hypertension. Recognition that systemic and glomerular hypertension do not necessarily coexist, and that therapeutic interventions may affect systemic and glomerular capillary pressures independently, helps to explain the renal responses to systemic hypertension and to antihypertensive therapy in a number of different circumstances. In contrast to the classic notion that ischemia mediates hypertensive glomerular injury, recent studies suggest that it is in fact glomerular capillary hyperperfusion and hypertension which initiate glomerular structural injury [1, 2]. Afferent arteriolar resistance (R A ) determines the fraction of systemic pressure which is transmitted to the glomerular capillary network. Early studies in rats with mineralocorticoid-salt hypertension [3] and salt-sensitive hypertensive rats [4] suggested that failure of RA to increase in the face of systemic hypertension resulted in glomerular capillary hyperperfusion and hypertension, which were associated with the development of glomerular sclerosis. This concept has been further clarified in studies of the partially nephrectomized rat. Reduction of functioning nephron number leads to an increase in the single nephron glomerular filtration rate in the remaining nephrons [5, 6]. Vascular resistance is reduced in both afferent and efferent arterioles, allowing an increase in the glomerular capillary plasma flow rate, Q A. Because the decrease in R A is proportionately greater than that in efferent arteriolar resistance (RE), the hydraulic pressure in the glomerular capillary (PGC) increases. Extensive renal ablation leads to severe systemic hypertension, and a syndrome of progressive azotemia, proteinuria, and glomerular sclerosis [7-9]. These compensatory elevations of PGC and Q A appear in fact to be maladaptive, and to contribute to the development of proteinuria and glomerular injury in the remaining nephrons [1, 2]. Support for this concept comes from observations that dietary protein restriction, which limits the adaptive increases in single nephron glomerular filtration rate, Address correspondence to Barry M. Brenner, M. D., Renal Division, Department of Medicine, Brigham and Women's Hospital, 75 Francis Street, Boston, MA 02115, U.S.A. Telephone (617) Oxford University Press 1989
2 186 S. Anderson and B. M. Brenner QA and PGC, ameliorates the development of proteinuria and glomerular sclerosis in rats with progressive renal injury [7, 10, 11]. Of note, dietary protein restriction has no effect on systemic hypertension in most experimental models. Thus, benefit may be obtained from limitation of PGC and QA even in the face of continued systemic hypertension. Recent micropuncture studies have provided a hemodynamic explanation for the sometimes conflicting findings of the effects of antihypertensive therapy on the progression of experimental renal disease. In both salt-sensitive hypertensive nephrotoxic serum nephritis [12] and the uninephrectomized spontaneously hypertensive rats [13], antihypertensive therapy with reserpine, hydralazine and hydrochlorothiazide restored systemic and glomerular capillary pressures to normal levels, and protected against renal injury. In contrast, extensive glomerular sclerosis develops despite excellent control of systemic hypertension with this regimen in rats subjected to five-sixths nephrectomy [9] or mineralocorticoid-salt hypertension [14]. In these studies, systemic hypertension was prevented but glomerular hypertension was not alleviated, and failure to control PGC afforded no renal structural protection. Alternatively, antihypertensive therapy which normalizes PGC protects against progressive glomerular injury. In rats with five-sixths nephrectomy [8, 9, 15, 16] and in uninephrectomized spontaneously hypertensive rats [13], administration of angiotensin I converting enzyme inhibitors (CEI) controls systemic and glomerular hypertension, and markedly limits proteinuria and glomerular sclerosis. Reduction of PGC without using drugs limits glomerular injury as well, as has been demonstrated in studies of rats subjected to mild anemia [17], as well as protein restriction. - Less is known of the intraglomerular hemodynamic consequences of other available antihypertensive agents. Conflicting evidence has been presented on calcium channel blockers. It has been reported that verapamil, given in doses which do not lower blood pressure, nonetheless reduces the glomerular transcapillary hydraulic pressure gradient [18] and glomerular injury [19] in rats with renal ablation. However, other investigators have found that blood pressure reduction with these agents is ineffective in retarding progressive renal disease in the rat [20-22]. Studies of the effects of these agents on PGC have also produced conflicting results [23-25]. Clearly, further studies are required to clarify their role as renal protective agents. Glomerular hypertension is also associated with renal injury in the absence of systemic hypertension. In the moderately hyperglycemic diabetic rat, systemic arterial pressure is near normal, but the metabolic derangements are accompanied by elevations of single nephron glomerular filtration rate, QA and PGC [26-28]. In this model as well, intraglomerular hyperperfusion and hypertension lead to glomerular sclerosis [27, 28]. Dietary protein restriction limits single nephron glomerular filtration rate, Q A, and PGC, and glomerular sclerosis, in diabetic rats in the absence of any changes in metabolic control [27]. The critical role of glomerular hypertension has been confirmed using CEI. A modest reduction in systemic pressure in these normotensive rats results in normalization of PGC, and protection against structural injury, without affecting supranormal single nephron glomerular filtration rate and Q A [28]. The pivotal role of glomerular hypertension in the initiation and progression of glomerular sclerosis is summarized schematically in Fig. 1. Renal ablation or primary parenchyma! disease lead to systemic hypertension, and to glomerular hypertension. Other factors, including normal ageing, diabetes, and dietary factors, also lead to glomerular hypertension, even in the absence of systemic hypertension. Once present, glomerular hypertension exerts deleterious effects on all glomerular cell constituents. In analogy with atherosclerosis, increased glomerular hydraulic pressure enhances endothelial cell release of
3 Editorial 187 Systemic Hypertension Primary Renal Disease Renal Ablation Aging Diabetes MeDitus Dietary Factors r GLOMERULAR HYPERTENSION \ r ENDOTHELIAL INJURY Release of vasoactive factors Vascular lipid deposition Intracapillary thrombosis \ i MESANGIAL INJURY Accumulation of macromolecules t matrix production t cell proliferation i EPITHELIAL INJURY Proteinuna I permeability to water 1 GLOMERULAR SCLEROSIS FIG. 1. Pivotol role of glomerular hypertension in the initiation and progression of structural injury. vasoactive substances (e.g. thromboxanes), lipid deposition, and intracapillary thrombosis. Injury to the mesangial region consists of increased accumulation of injurious macromolecules, which enhance both mesangial cell proliferation and mesangial matrix production. Epithelial cell injury augments glomerular basement membrane permeability, and proteinuria. Together injury to these cells results in glomerular sclerosis. Progressive nephron destruction in turn contributes to systemic and glomerular hypertension, thus perpetuating the cycle. These encouraging findings notwithstanding, a great deal remains to be learned about the mechanisms by which these hemodynamic maladaptations, and particularly glomerular hypertension, cause progressive renal injury. While long-term prospective clinical studies are needed, recent preliminary reports suggest that converting enzyme inhibitors may be effective, and perhaps superior to conventional combination antihypertensive therapy [29-31], in controlling systemic hypertension and stabilizing renal function in patients with renal insufficiency. Similarly, recent studies have provided encouraging preliminary evidence that administration of converting enzyme inhibitors alone or in conjunction with other antihypertensive drugs may slow the progression of albuminuria or decline in renal function in patients with diabetic renal disease [32-35]. It is hoped that further experimental and clinical studies relating nutritional and pharmacogical maneuvers to glomerular function will ultimately alter the otherwise inexorable natural progression of renal disease. REFERENCES 1. Brenner BM, Meyer TW, Hostetter TH. Dietary protein intake and the progressive nature of kidney disease. N Engl J Med 1982; 307:
4 Anderson and B. M. Brenner 2. Brenner BM. Nephron adaptation to renal injury or ablation. Am J Physio! 1985; 249: F Hill GS, Heptinstall RH. Steroid-induced hypertension in the rat. Am J Pathol 1968; 52: Azar S, Johnson MA, Hertel B, Tobian L. Single-nephron pressures, flows and resistances in hypersensitive kidneys with nephrosclerosis. Kidney Int 1977; 12: Deen WM, Maddox DA, Robertson CR, Brenner BM. Dynamics of glomerular ultrafiltration in the rat. VII. Response to reduced renal mass. Am J Physiol 1974; 227: Hostetter TH, Olson JL, Rennke HG, Venkatachalam MA, Brenner BM. Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation. Am J Physiol 1981; 241: F Olson JL, Hostetter TH, Rennke HG, Brenner BM, Venkatachalam MA. Altered glomerular permselectivity and progressive sclerosis following extreme ablation of renal mass. Kidney Int 1982; 22: Anderson S, Meyer TW, Rennke HG, Brenner BM. Control of glomerular hypertension limits glomerular injury in rats with reduced renal mass. J Clin Invest 1985; 76: Anderson S, Rennke HG, Brenner BM. Therapeutic advantage of converting enzyme inhibitors in arresting progressive renal disease associated with systemic hypertension in the rat. J Clin Invest 1986; 77: Hostetter TH, Meyer TW, Rennke HG, Brenner BM. Chronic effects of dietary protein on renal structure and function in the rat with intact and reduced renal mass. Kidney Int 1986; 30: DworkinLD, Hostetter TH, Rennke HG, Brenner BM. Hemodynamic basis for glomerular injury in rats with desoxycorticosterone-salt hypertension. J Clin Invest 1984; 73: Neugarten J, Kaminetsky B, Feiner H, Schacht RG, Liu DT, Baldwin DS. Nephrotoxic serum nephritis with hypertension: amelioration by antihypertensive therapy. Kidney Int 1985; 28: Dworkin LD, Grosser M, Feiner H, Ullian M, Randazzo J, Parker M. Both converting enzyme inhibitors and vasodilators reduce glomerular capillary pressure and injury in uninephrectomized spontaneously hypertensive rats. Kidney Int 1987; 31: 383 (abstr). 14. Dworkin LD, Feiner HD, Randazzo J. Glomerular hypertension and injury in desoxycorticosterone-salt rats on antihypertensive therapy. Kidney Int 1987; 31: Meyer TW, Anderson S, Rennke HG, Brenner BM. Reversing glomerular hypertension stabilizes established glomerular injury. Kidney Int 1987; 31: Garcia DL, Rennke HG, Brenner BM, Anderson S. Chronic glucocorticoid therapy amplifies glomerular injury in rats with renal ablation. J Clin Invest 1987; 80: Garcia DL, Anderson S, Rennke HG, Brenner BM. Anemia lessens and its prevention with recombinant human erythropoietin worsens glomerular injury and hypertension in rats with reduced renal mass. Proc Natl Acad Sci (USA) 1988; 85: Pelayo JC, Harris DCH, Shanley PF, Miller GF, Schrier RW. Glomerular hemodynamic adaptations in remnant nephrons: effects of verapamil. Am J Physiol 1988; 254: F Harris DCH, Hammond WS, Burke TJ, Schrier RW. Verapamil protects against progression of experimental chronic renal failure. Kidney Int 1987; 31: Jackson B, Debrevi L, Cubela R, Whitty M, Johnston CI. Preservation of renal function in the rat remnant kidney model of chronic renal failure by blood pressure reduction. Clin Exp Pharm Physiol 1986; 13: Jackson B, Debrevi L, Whitty M, Johnston CI. Progression of renal disease: effects of different classes of antihypertensive therapy. J Hypertension 1986; 4 (Suppl 5): S Brunner FP, Thiel G, Hermle M, Mihatsch M. Longterm enalapril and verapamil in rats with reduced renal mass. Kidney Int 1987; 31: 380 (abstr). 23. Frei U, Schindler R, Graf S, Koch KM. Glomerular hemodynamics of the clipped kidney: effects of calcium-antagonist and converting enzyme inhibition. Proc Xth Int Cong Nephrol 1987; 277 (abstr). 24. Anderson S, Clarey LE, Rjley SL, Troy JL. Acute infusion of calcium channel blockers reduces glomerular capillary pressure in rats with reduced renal mass. Kidney Int 1988; 33: 370 (abstr). 25. Dworkin LD, Benstein J, Feiner HD, Parker M. Nifedipine prevents glomerular injury without reducing glomerular pressure in rats with desoxycorticosterone-salt hypertension. Kidney Int 1988; 33: 374 (abstr). 26. Hostetter TH, Troy JL, Brenner BM. Glomerular hemodynamics in experimental diabetes mellitus. Kidney Int 1981; 19: Zatz R, Meyer TW, Rennke HG, Brenner BM. Predominance of hemodynamic rather than
5 Editorial 189 metabolic factors in the pathogenesis of diabetic glomerulopathy. Proc Natl Acad Sci (USA) 1985; 82: Zatz R, Dunn BR, Meyer TW, Anderson S, Rennke HG, Brenner BM. Prevention of diabetic glomemlopathy by pharmacological amelioration of glomerular capillary hypertension. J Clin Invest 1986; 77: Mann J, Ritz E. Preservation of kidney function by use of converting enzyme inhibitors for control of hypertension. Lancet 1987; 2: Heeg JE, de Jong PE, van der Hem GK, de Zeeuw D. Reduction of proteinuria by angiotensin converting enzyme inhibition. Kidney Int 1987; 32: Ruilope LM, Miranda B, Morales JM, Rodicio JL, Romero JC, Raij L. Control of hypertension with a converting enzyme inhibitor slows progression of renal insufficiency in human chronic renal failure. Kidney Int 1987; 31: 215 (abstr) 32. Taguma Y, Kitamoto Y, Futaki G, el al. Effect of captopril on heavy proteinuria in azotemic diabetics. N Engl J Med 1985; 313: Bjorck S, Nyberg G, Mulec H, Granerus G, Herlitz H, Aurell M. Beneficial effects of angiotensin converting enzyme inhibition on renal function in patients with diabetic nephropathy. Br Med J 1986; 293: Hommel E, Parving H-H, Mathiesen E, Edsberg B, Nielsen MD, Giese J. Effect of captopril on kidney function in insulin-dependent diabetic patients with nephropathy. Br Med J 1986; 293: Marre M, Leblanc H, Suarez L, Guyenne T, Menard J, Passa P. Converting enzyme inhibition and kidney function in normotensive diabetic patients with persistant microalbuminuria. Br Med J 1987; 294:
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