doi: 10.1161/hy09t1.095205
(Hypertension. 2001;38:625.)
© 2001 American Heart Association, Inc.
Renal Factors |
Functional Assessment of the Circulation of the Single Kidney
From the Department of Internal Medicine, Divisions of Hypertension (L.O.L.) and Cardiovascular Diseases (M.R.-P.), Mayo Clinic, Rochester, Minn.
Correspondence to Lilach O. Lerman, MD, PhD, Division of Hypertension, Mayo Clinic, 200 First St SW, Rochester, MN 55905. E-Mail Lerman.Lilach{at}Mayo.edu
Abstract
Abstract—— Functional alterations in the renal circulation that can contribute to abnormal renal perfusion have been demonstrated in various models of renal injury. To detect impairments in renal vascular function, renal flow reserve can be determined by repeated measurements of renal blood flow (RBF) during pharmacological challenge with short-acting vasodilators that should increase RBF in kidneys that are not severely damaged structurally. Among the invasive techniques for such measurements, the most readily available is probably the intravascular Doppler, which can be employed during renal angiography for rapid evaluation of changes in RBF during intrarenal injections of vasoactive substances. High-resolution tomographic imaging techniques, like electron-beam x-ray computed tomography, further offer the potential for noninvasive measurements of renal parenchymal perfusion and function, in association with either intrarenal or systemic injections of vasoactive substances. Acetylcholine is a potent short-acting renal vasodilator that can be useful to assess the response of the renal microcirculation, define renal flow reserve, and examine the endothelium-dependent responses of RBF. Such assessments of the function of the renal circulation can assist in evaluation of patients with systemic or renal disease for early detection and monitoring of renovascular injury.
Key Words: renal circulation • renal blood flow • computed tomography • acetylcholine
Under normal conditions, basal renal vascular tone is well regulated by many vasoactive systems that keep renal blood flow (RBF) in equilibrium,1 including the endothelium-derived relaxing factor NO, prostaglandins, and the renin-angiotensin system.2 Therefore, at an early stage of renal disease, RBF may be normal, and impaired renal vascular tone may become evident only as an attenuated response during stimulus with vasoactive substances or physiological challenges. The mechanisms of the attenuated response have been postulated to include decreased release of vasodilators (eg, NO, prostaglandins) and co-existing vasoconstrictors (eg, thromboxane, angiotensin II), which may be released or rendered unopposed during challenge. The altered functional response may precede structural renal damage and can serve as a marker for abnormal handling of daily challenges by the kidney. Such impairment has been demonstrated in various models of renal injury, like hypertension, hypercholesterolemia, renal artery stenosis, ischemia and reperfusion, acute renal failure, diabetes mellitus, and aging. Hence, utilization of vasodilators to examine renal flow reserve (RFR) can serve to disclose subtle functional vascular alterations3 and may allow early detection and monitoring of renovascular injury. For example, residual responsiveness of the intrarenal circulation to challenge may also reflect renal viability and may conceivably predict success of subsequent therapy (eg, revascularization).
Evaluation of the reactivity of the single-kidney circulation entails rapid and successive measurements of single-kidney RBF, as well as availability of rapid-onset and short-acting renal vasodilators that could evoke a sufficient increase in RBF and/or distinguish normal from diseased kidneys. In the coronary or peripheral circulation, such assessment is often performed by measurement of vascular diameter, blood flow, or blood velocity under resting conditions and subsequently during pharmacological challenge with endothelium-dependent (eg, acetylcholine or bradykinin) or -independent (eg, nitroglycerin) vasodilators. Flow measurements in the forearm circulation are usually performed by strain-gauge plethysmography or intravascular Doppler, and in the coronary circulation, by the latter,4 both in conjunction with intra-arterial drug infusion. Although a similar approach could be useful to assess the renal circulation in patients with renal injury, it has been less commonly applied in the kidney. In this review we summarize techniques that have been previously used or are potentially useful to quantify RBF, that pharmacologically challenge the renal circulation, and that in combination measure single-kidney RFR in humans.
Measurements of Single-Kidney RBF
Diverse techniques have also been used for measurement of RBF, but some were either incapable of single-kidney measurements without ureteral catheterization (eg, p-aminohippuric acid), did not provide quantitative (eg, scintigraphy, duplex) or accurate information across a wide range of physiological conditions (eg, inert diffusible indicators), or were too invasive to apply in humans. Nevertheless, several methods successfully used to measure RFR have shed important light on the short-term behavioral attributes of the renal circulation. Moreover, promising novel approaches have also enabled specific quantification of cortical and medullary perfusion, thereby providing insight into regulation of regional renal hemodynamics.
Xenon Washout
The xenon 133 (133Xe) washout technique is based on evaluation of the excretion profile of an externally administered indicator. This method has been very useful for assessment of RBF and its response to a wide spectrum of vasodilators. Using this technique, Hollenberg et al5 observed a blunted increase in RBF in response to graded doses of acetylcholine and dopamine in patients with parenchymal disease but observed a potentiated response in patients with increased basal renal vascular resistance (RVR) or mild essential hypertension and no structural damage. They later observed that patients with essential hypertension showed a significant reduction in renal vasomotion in response to a calcium channel blocker, and their first-degree relatives showed an exaggerated renal vasodilator response3 to this drug, which was attributed to abnormal flux of calcium into renal arterioles.6 More recently, intrarenal infusion of adenosine in essential hypertension or renal artery stenosis was shown to induced a dose-dependent vasodilatation, which was more prolonged in patients with renal artery stenosis, suggesting a potentiated mechanism for adenosine-induced vasodilatation.7
However, this methodology is invasive because it involves injection of the 133Xe directly into the renal artery and external counting with a scintillation probe.8,9 In addition, its washout curves cannot be reliably used for compartmental flow measurements.
Intravascular Doppler
This invasive technique provides percutaneous single-kidney measurements of blood velocity using an intrarenal Doppler wire, and synchronous documentation of renal arterial diameter enables calculation of RBF.10 This provides accurate velocity measurements of in small straight tubes <4.76 mm in diameter.11 However, in larger or more tortuous tubes and for flow rates >200 mL/min (which are common in the renal artery), it may underestimate blood flow, probably because of suboptimal positioning and wire instability or because of deformed flow profiles.11 Flow in collateral and accessory renal arteries may also be missed by Doppler measurements obtained within the main renal artery.
Despite its potential limitations, this technique is useful for rapid and sequential quantification of RBF. Important studies using the intravascular Doppler technique in humans have shown that intrarenal acetylcholine resulted in a significant vasodilatory effect on both conductance and resistance renal blood vessels and led to a marked reduction in RVR and enhancement of RBF.12 Nitroglycerin, an exogenous NO donor, caused a small and selective vasodilatory effect on renal conductance vessels and failed to decrease RVR and thus to increase RBF.12 In patients with chronic congestive heart failure, intrarenal adenosine induced marked reduction in RBF, mainly via a vasoconstrictor effect on intrarenal resistance vessels.10 Similarly, in patients with cardiovascular risk factors, adenosine decreased—whereas acetylcholine, papaverine, and nitroglycerin increased—Doppler-derived RBF, with acetylcholine showing the greatest efficacy for renal vasodilation.13 In hypertensive patients, isosorbide dinitrate increased RBF velocity and disclosed heterogeneous responses between the 2 kidneys,14 and the renal microcirculation response to papaverine showed variability among patients.15 Studies in pigs have shown that intrarenal isosorbide dinitrate and papaverine significantly increase RBF, but the response was greater with papaverine, probably because papaverine dilates small resistance vessels whereas isosorbide dinitrate dilates conductance vessels. Both drugs induced a significant decrease in mean arterial pressure (MAP).16 These studies also reinforced the observation that RFR is less marked than the coronary circulation.16 While coronary flow reserve (hyperemic-to-basal blood flow ratio) is up to 4 or 5, RFR of >2.5 is difficult to achieve, possibly because of the lower basal RVR compared with the coronary vascular resistance.
Although intrarenal injections of vasodilators have been very useful to examine renovascular reactivity, this invasive approach is no longer mandated. Development of fast, high-resolution imaging techniques now allows repetitive measurements of RBF17 and detection of small changes induced by intravenously injected vasoactive agents. Furthermore, these methods hold a potential to measure concomitant renal function and regional perfusion, and thereby assess the coupling of renal hemodynamics and function.
Computed Tomography Techniques
Tomographic imaging techniques using intravenously injected indicators may potentially have useful clinical applications, because their cross-sectional capability allows assessment of the circulation of the single kidneys noninvasively, bilaterally, and simultaneously. High spatial resolution coupled with dynamic imaging of indicators (iodinated or radioactive) allows evaluation of regional renal function and/or RBF,18 and measurements of parenchymal flow circumvent the potentially confounding presence of collateral and accessory renal arteries. Techniques applied to the kidneys include positron emission tomography (PET),19 magnetic resonance imaging (MRI),20 and x-ray computed tomography.17,21,22
Positron Emission Tomography
PET involves exposure to radioactivity, its tracers are difficult to produce, and its relatively low spatial resolution limits measurements of medullary perfusion. However, it is one of the few techniques capable of quantification of RBF and cortical blood flow in vivo.23 Using this technique, Middlekauff et al have shown that cortical RBF decreases and RVR increases in response to static handgrip exercise and that exogenous adenosine produces reflex renal vasoconstriction,19,24 which were exaggerated in heart failure.25 Juillard et al26 have also shown that PET provided reliable measurement of RBF in pigs using 15O-labeled water, a short-life tracer that allows repeated measurements. These investigators further demonstrated that during infusion of dopamine and angiotensin II, PET could detect the increase or decrease in RBF, respectively,26 suggesting that this method could be used to assess the reactivity of the renal circulation.
Magnetic Resonance Imaging
MRI has been used to measure flow through both the main renal artery and the renal parenchyma.27–29 Recording dynamic changes in signal intensity or disappearance rate after administration of gadopentetate dimeglumine has also been used to assess renal function,30,31 although nonlinearity of the paramagnetic contrast material concentration with tissue density limits quantitative measurements. MRI measurements have been obtained under various clinical conditions,32 but few of them examined RFR. MRI successfully demonstrated that dipyridamole decreased medullary more than cortical perfusion,33 and aminophylline attenuated a decrease in cortical flow following extracorporeal shockwave lithotripsy.34
Electron-Beam Computed Tomography
Electron-beam computed tomography (EBCT) has been extensively used to study renal perfusion and function by intravenous injection of nonionic contrast. The high spatial and temporal resolution of EBCT enables accurate, reproducible, and noninvasive quantification of single-kidney volume and cortical, medullary, and papillary perfusion in humans35,36 and in animal models.37–40 Furthermore, single-kidney tubular dynamics and glomerular filtration rate can be synchronously obtained to allow comprehensive evaluation of the kidney.41 The main limitations of this technique are related to exposure to radiation and x-ray contrast agents.
Measurements of RBF in normal animals during infusion of vasoactive substances showed a prompt increase in response to intrarenal bradykinin and secretin42 and to systemic furosemide,43 acetylcholine, and sodium nitroprusside.37,40 The response to both latter drugs was attenuated in pigs with hypercholesterolemia and hypertension37,40 (Figure), suggesting that early renal injury also impairs endothelium-independent vasodilation or that subtle impairments are detectable using smaller doses or systemic administration of the drugs.
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Choice of Vasoactive Substance
Compared with other vascular beds, the renal vasculature shows unique responses to vasoactive substances. For example, adenosine is a potent and short-acting vasodilator of coronary microvessels and is commonly used to define coronary flow reserve. In the kidney, on the other hand, the A1- and A2-adenosine receptors tend to have opposite effects on afferent arteriolar resistance and renin secretion, and exogenous adenosine can dose dependently either constrict or dilate the normal renal vasculature.44 In normal subjects, intrarenal adenosine reduced RBF,45 and in chronic congestive heart failure, increased RVR and decreased RBF.10 However, in both essential and renovascular hypertensive patients, intrarenal adenosine induced a dose-dependent increase in RBF.7 Hence, exogenous adenosine has differential renovascular effects and, unlike in the coronary vessels, does not constitute a reliable vasodilatory challenge.
In contrast, various endothelium-dependent and -independent (NO donors and smooth muscle relaxants) induce a substantial increase in RBF. Endothelium-independent vasodilators like papaverine,15 nitroglycerin,13 isosorbide dinitrate,14 or sodium nitroprusside46 induce an effective increase in RBF, but even intrarenal injections are often limited by profound systemic effects that restrict interpretation of RBF or achieving maximal RFR. Among these, papaverine dilates the renal microcirculation and is more likely to achieve a substantial decrease in RVR and RFR than conduit vessel dilators. However, acetylcholine,3,5,6,12,13,47–49 the prototypical endothelium-dependent vasodilator of the microcirculation, appears to be associated with greater RFR attended by a smaller and more transient decrease in MAP.
Indeed, using EBCT, we have observed that systemic administration of acetylcholine effectively increased RBF (Figure, part a) accompanied by only a transient decrease in MAP, whereas the dose of sodium nitroprusside required to increase RBF was accompanied by a small but sustained decrease in MAP.37,40 Intrarenal bolus injections of acetylcholine also dose dependently increased RBF (measured using intravascular Doppler) more effectively than papaverine, in association with smaller decrements in MAP (Figure, part b), suggesting that acetylcholine may be a suitable challenge for RFR.
In summary, assessment of renal circulatory function can assist in evaluation of patients with systemic or renal disease. Tomographic imaging techniques, like EBCT, offer the advantage of noninvasive measurements of renal regional perfusion and function. Determination of RFR can be achieved by repeated measurements of RBF during pharmacological challenge with short-acting vasoactive substances like acetylcholine, which can also be used to assess endothelium-dependent RBF and has few systemic hemodynamic effects.
Acknowledgments
This work was supported by grant numbers HL-03621 and HL-63282 from the National Institutes of Health and by the Mayo Foundation.
Received March 28, 2001; first decision May 30, 2001; accepted June 19, 2001.
References
1.
Salom MG, Lahera V, Romero JC. Role of prostaglandins and endothelium-derived relaxing factor on the renal response to acetylcholine. Am J Physiol. . 1991; 260: F145–F149.
2. Stein JH. Regulation of the renal circulation. Kidney Int. . 1990; 38: 571–576.[Medline] [Order article via Infotrieve]
3.
Blackshear JL, Garnic D, Williams GH, Harrington DP, Hollenberg NK. Exaggerated renal vasodilator response to calcium entry blockade in first-degree relatives of essential hypertensive subjects. Hypertension. . 1987; 9: 384–389.
4.
Hasdai D, Gibbons RJ, Holmes DJr, Higano ST, Lerman A. Coronary endothelial dysfunction in humans is associated with myocardial perfusion defects. Circulation. . 1997; 96: 3390–3395.
5. Hollenberg NK, Adams DF, Solomon H, Chenitz WR, Burger BM, Abrams HL, Merrill JP. Renal vascular tone in essential and secondary hypertension: hemodynamic and angiographic responses to vasodilators. Medicine (Baltimore). . 1975; 54: 29–44.[Medline] [Order article via Infotrieve]
6.
Hollenberg NK, Sandor T, Holtzman E, Meyerovitz MF, Harrington DP. Renal vasomotion in essential hypertension: influence of vasodilators. Hypertension. . 1989; 14: 9–13.
7. Wierema TK, Postma CT, Houben AJ, Kroon AA, Thien T, Smits P, de Leeuw PW. Adenosine-induced renal vasodilatation is prolonged in renal artery stenosis. J Hypertens. . 1998; 16: 2109–2112.[Medline] [Order article via Infotrieve]
8. Aukland K. Methods for measuring renal blood flow: total flow and regional distribution. Ann Rev Physiol. . 1980; 42: 543–555.[Medline] [Order article via Infotrieve]
9.
Porter LE, Hollenberg NK. Obesity, salt intake, and renal perfusion in healthy humans. Hypertension. . 1998; 32: 144–148.
10.
Elkayam U, Mehra A, Cohen G, Tummala PP, Karaalp IS, Wani OR, Canetti M. Renal circulatory effects of adenosine in patients with chronic heart failure. J Am Coll Cardiol. . 1998; 32: 211–215.
11.
Doucette JW, Corl PD, Payne HM, Flynn AE, Goto M, Nassi M, Segal J. Validation of a Doppler guide wire for intravascular measurement of coronary artery flow velocity. Circulation. . 1992; 85: 1899–1911.
12. Elkayam U, Cohen G, Gogia H, Mehra A, Johnson JV, Chandraratna PA. Renal vasodilatory effect of endothelial stimulation in patients with chronic congestive heart failure. J Am Coll Cardiol. . 1996; 28: 176–182.[Abstract]
13. Houghton JL, Cerda J, Smith VE. Basal and reserve renal artery blood flow: effect of endothelium-dependent and -independent vasoactive agonists and radiographic contrast medium in two patients. J Invasive Cardiol. . 2000; 12: 211–215.[Medline] [Order article via Infotrieve]
14. Beregi JP, Mounier-Vehier C, Willoteaux S, Gautier C, Lions C, Gaxotte V. Intravascular Doppler for the evaluation of renal blood flow: validation and demonstration of vessel reactivity. J Mal Vasc. . 2000; 25: 336–342.[Medline] [Order article via Infotrieve]
15. Beregi JP, Mounier-Vehier C, Devos P, Gautier C, Libersa C, McFadden EP, Carre A. Doppler flow wire evaluation of renal blood flow reserve in hypertensive patients with normal renal arteries. Cardiovasc Intervent Radiol. . 2000; 23: 340–346.[Medline] [Order article via Infotrieve]
16. Beregi JP, Lahoche A, Willoteaux S, McFadden E, Bordet R, Gautier C, Etchrivi T. Renal artery vasomotion: in vivo assessment in the pig with intravascular Doppler. Fundam Clin Pharmacol. . 1998; 12: 613–618.[Medline] [Order article via Infotrieve]
17. Lerman LO, Rodriguez Porcel M, Romero JC. The development of x-ray imaging to study renal function. Kidney Int. . 1999; 55: 400–416.[Medline] [Order article via Infotrieve]
18. Lorenz CH, Powers TA, Partain CL. Quantitative imaging of renal blood flow and function. Invest Radiol. . 1992; 27: S109–S114.
19.
Middlekauff HR, Nitzsche EU, Nguyen AH, Hoh CK, Gibbs GG. Modulation of renal cortical blood flow during static exercise in humans. Circ Res. . 1997; 80: 62–68.
20. Bennett HF, Li D. MR imaging of renal function. Magn Reson Imag Clin N Am. . 1997; 5: 107–126.
21. Romero JC, Lerman LO. Novel noninvasive techniques for studying renal function in man. Semin Nephrol. . 2000; 20: 456–462.[Medline] [Order article via Infotrieve]
22. Romero JC, Pelaez LI, Feldstein A, Lerman LO. New ways to investigate intrarenal distribution of blood flow and tubular flow dynamics. Curr Opin Nephrol Hypertens. . 1999; 8: 157–166.
23. Nitzsche EU, Choi Y, Killion D, C. K. H, Hawkins RA, Rosenthal JT, Buxton DB, Huang SC, Phelps ME, Schelbert HR. Quantification and parametric imaging of renal cortical blood flow in vivo based on Patlak graphical analysis. Kidney Int. . 1993; 44: 985–996.[Medline] [Order article via Infotrieve]
24.
Middlekauff HR, Nitzsche EU, Hamilton MA, Schelbert HR, Fonarow GC, Moriguchi JD, Hage A, Saleh S, Gibbs GG. Evidence for preserved cardiopulmonary baroreflex control of renal cortical blood flow in humans with advanced heart failure: a positron emission tomography study. Circulation. . 1995; 92: 395–401.
25.
Middlekauff HR, Nitzsche EU, Hoh CK, Hamilton MA, Fonarow GC, Hage A, Moriguchi JD. Exaggerated renal vasoconstriction during exercise in heart failure patients. Circulation. . 2000; 101: 784–789.
26. Juillard L, Janier MF, Fouque D, Lionnet M, Le Bars D, Cinotti L, Barthez P, Gharib C, Laville M. Renal blood flow measurement by positron emission tomography using 15O-labeled water. Kidney Int. . 2000; 57: 2511–2518.[Medline] [Order article via Infotrieve]
27. Wolf GL, Hoop B, Cannillo JA, Rogowska JA, Halpern EF. Measurement of renal transit of gadopentetate dimeglumine with echo-planar MR imaging. J Magn Reson Imaging. . 1994; 4: 365–372.[Medline] [Order article via Infotrieve]
28.
Roberts DA, Detre JA, Bolinger L, Insko EK, Lenkinski RE, Pentecost MJ, Leigh JS, Jr. Renal perfusion in humans: MR imaging with spin tagging of arterial water. Radiology. . 1995; 196: 281–286.
29. Binkert CA, Hoffman U, Leung DA, Matter HG, Schmidt M, Debatin JF. Characterization of renal artery stenoses based on magnetic resonance renal flow and volume measurements. Kidney Int. . 1999; 56: 1846–1854.[Medline] [Order article via Infotrieve]
30.
Ros PR, Gauger J, Stoupis C, Burton SS, Mao J, Wilcox C, Rosenberg EB, Briggs RW. Diagnosis of renal artery stenosis: feasibility of combining MR angiography, MR renography, and gadopentetate-based measurements of glomerular filtration rate. Am J Roentgenol. . 1995; 165: 1447–1451.
31.
Niendorf ER, Grist TM, Lee FT, Jr, Brazy PC, Santyr GE. Rapid in vivo measurement of single-kidney extraction fraction and glomerular filtration rate with MR imaging. Radiology. . 1998; 206: 791–798.
32. Vallee JP, Lazeyras F, Khan HG, Terrier F. Absolute renal blood flow quantification by dynamic MRI and Gd-DTPA. Eur Radiol. . 2000; 10: 1245–1252.[Medline] [Order article via Infotrieve]
33. Tello R, Hartnell GG, Hill T, Volpe J, Finn JP, Cohen M. MR perfusion imaging of the kidney pre- and post-dipyridamole stress. J Magn Reson Imaging. . 1996; 6: 460–464.[Medline] [Order article via Infotrieve]
34. Chan AJ, Prasad PV, Priatna A, Mostafavai MR, Sunduram C, Saltzman B. Protective effect of aminophylline on renal perfusion changes induced by high-energy shockwaves identified by Gd-DTPA-enhanced first-pass perfusion MRI. J Endourol. . 2000; 14: 117–121.[Medline] [Order article via Infotrieve]
35. Lerman LO, Flickinger AL, Sheedy PF, Turner ST. Reproducibility of human kidney perfusion and volume determinations with electron beam computed tomography. Invest Radiol. . 1996; 31: 204–210.[Medline] [Order article via Infotrieve]
36. Lerman LO, Taler SJ, Textor S, Sheedy PF, Stanson AW, Romero JC. CT-derived intra-renal blood flow in renovascular and essential hypertension. Kidney Int. . 1996; 49: 846–854.[Medline] [Order article via Infotrieve]
37.
Feldstein A, Krier JD, Hershman Sarafov M, Lerman A, Best PJM, Wilson SH, Lerman LO. Renal perfusion and function in hypercholesterolemic pigs in vivo. Hypertension. . 1999; 34: 859–864.
38.
Lerman LO, Nath KA, Rodriguez-Porcel M, Krier JD, Schwartz RS, Napoli C, Romero JC. Increased oxidative stress in experimental renovascular hypertension. Hypertension. . 2001; 37: 541–546.
39.
Lerman LO, Schwartz RS, Grande JP, Sheedy PF, Romero JC. Noninvasive evaluation of a novel swine model of renal artery stenosis. J Am Soc Nephrol. . 1999; 10: 1455–1465.
40.
Rodriguez-Porcel M, Krier JD, Lerman A, Sheedy PF, II, Romero JC, Napoli C, Lerman LO. Combination of hypercholesterolemia and hypertension augments renal function abnormalities. Hypertension. . 2001; 37: 774–780.
41. Krier JD, Ritman EL, Bajzer Z, Romero JC, Lerman A, Lerman LO. Noninvasive measurement of concurrent, single-kidney perfusion, glomerular filtration, and tubular function. Am J Physiol. . 2001: 281. (In press).
42. Lerman LO, Bell MR, Lahera V, Rumberger JA, Sheedy PF, Sanchez Fueyo A, Romero JC. Quantification of global and regional renal blood flow with electron beam computed tomography. Am J Hypertens. . 1994; 7: 829–837.[Medline] [Order article via Infotrieve]
43. Lerman LO, Rodriguez-Porcel M, Sheedy PFI, Romero JC. Renal tubular dynamics in the intact canine kidney. Kidney Int. . 1996; 50: 1358–1362.[Medline] [Order article via Infotrieve]
44.
Murray RD, Churchill PC. Concentration dependency of the renal vascular and renin secretory responses to adenosine receptor agonists. J Pharmacol Exp Ther. . 1985; 232: 189–193.
45. Marraccini P, Fedele S, Orsini E, Gliozheni E, Djukic G, Mazzarisi A, Serasini L, Marzilli M, L’Abbate A. Adenosine and angiotensin system interact in the regulation of renal microcirculation in humans. J Cardiovasc Pharmacol. . 2000; 35: 758–762.[Medline] [Order article via Infotrieve]
46. Maseda J, Hilberman M, Derby GC, Spencer RJ, Stinson EB, Myers BD. The renal effects of sodium nitroprusside in postoperative cardiac surgical patients. Anesthesiology. . 1981; 54: 284–288.[Medline] [Order article via Infotrieve]
47. Ladeforged J. Increase in renal blood flow in acute renal failure following intra- arterial infusion of acetylcholine. Scand J Clin Lab Invest. . 1977; 37: 709–716.[Medline] [Order article via Infotrieve]
48. Mattei P, Virdis A, Ghiadoni L, Taddei S, Salvetti A. Endothelial function in hypertension. J Nephrol. . 1997; 10: 192–197.[Medline] [Order article via Infotrieve]
49. Wierema TK, Houben AJ, de Leeuw PW. Acetylcholine-induced vasodilatation in the human hypertensive kidney: inhibition by muscarinic receptor antagonism. J Hypertens. . 1997; 15: 1649–1651.[Medline] [Order article via Infotrieve]
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