NDT Advance Access originally published online on July 19, 2006
Nephrology Dialysis Transplantation 2006 21(10):2859-2866; doi:10.1093/ndt/gfl307
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Arterial wave reflections and mortality in haemodialysis patients—only relevant in elderly, cardiovascularly compromised?
1Dialysis and Transplantation Center, ‘C. I. PARHON’ University Hospital, 2Cardiology Center, Iasi, Romania and 3Renal Unit, Guy's Hospital, London, UK
Correspondence and offprint requests to: Prof. Adrian Covic, MD, PhD, Director Dialysis and Transplantation Center, ‘C. I. PARHON’ University Hospital, 50 Carol 1st Blvd., Iasi, 700503, Romania. Email: acovic{at}xnet.ro
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Abstract |
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Background. Chronic kidney disease (CKD) patients have a 3–30-fold increased risk of death compared with the general population. This mortality difference is even more pronounced in younger subjects. Two markers of aortic stiffness––aortic pulse wave velocity (PWV) and augmentation index (AIx)––have been prospectively related to all-cause and cardiovascular (CV) mortality in end-stage renal disease (ESRD) populations. The aims of our study were first, to confirm the important deleterious effect of arterial stiffness in uraemia and second, to assess the impact on survival of increased AIx in a relatively young non-diabetic dialysis population, with minimal CV disease.
Methods. Ninety-two patients (mean age 42.6 ± 11.2 years) were included in the study and followed for a period of 61 ± 25 months. None of the patients had diabetes mellitus, and only 3.3% had prior history of CV disease. AIx was determined by applantation tonometry using a SphygmoCor® device (AtCorTM, PWV Inc., Westmead, Sydney, Australia).
Results. Mean AIx in our study population was 19.9 ± 13.7%; other significant haemodynamic parameters were: systolic blood pressure (SBP) 129 ± 24 mmHg, pulse pressure 35.3 ± 17.5 mmHg with 27.2% of the study population receiving angiotensin-converting enzyme inhibitors (ACE-I). On univariate analysis, in our group AIx correlated with: body weight (P < 0.001), radial SBP (P < 0.001) and haemoglobin levels (P < 0.05). There was no correlation between AIx and any of the echocardiographic parameters. In the stepwise multiple regression analysis, the only independent predictors for AIx were weight (P < 0.001), SBP (P < 0.001) and haemoglobin (P < 0.05) with the model explaining 33% of the AIx variability (adjusted R2 = 0.33).
During the follow-up period, 15 deaths were recorded. In the Cox analysis (P = 0.014; chi square 20.7 for the model) the only independent predictors for all-cause mortality were age (P = 0.001), left ventricular mass index (P = 0.032) and ACE-I therapy (P = 0.039) while AIx did not reach statistical significance. There was no difference in patients’ survival when divided by AIx tertiles, assessed by the log rank test (P = 0.78).
Conclusion. Our results fail to support the notion that an increased effect of wave reflections on central arteries is a strong and independent predictor of mortality in all ESRD patients on haemodialysis. The effect of arterial wave reflections might be in fact dependent on patient age and concurrent comorbidity status.
Keywords: arterial stiffness; augmentation index; haemodialysis; survival
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Introduction |
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Cardiovascular (CV) disease is the most important cause of mortality in chronic kidney disease (CKD). Compared with the general population, patients with CKD have a 3–30-fold risk of succumbing to CV disease; this difference is even more pronounced in young subjects [1,2]. Many potential explanations exist for this CV disease epidemic in renal patients. Whether these are equally relevant for all CKD patients (across all age categories) is not yet known. In the last decade, CV research in the general and renal population has increasingly focused on arteriosclerosis, the diffuse process of arterial stiffening, as opposed to the focal process of atherosclerosis. Reduced arterial compliance (a synonym for increased arterial stiffness) seems to have a pivotal role in the genesis of high systolic blood pressure (SBP), widened pulse pressure (PP), increased left ventricular (LV) workload and hypertrophy—and ultimately in CV mortality [3,4]. Underlying mechanisms for increased stiffness in uraemia are not well-defined, but may include: chronic fluid overload, arterial calcifications, microinflammation, sympathetic nervous system over-activity, activation of the renin–angiotensin system, increased lipid oxidation and abnormalities of the nitric oxide system [5].
Recently, two highly reproducible [6] markers of aortic stiffness—aortic pulse wave velocity (PWV) and augmentation index (AIx)—have been shown to be strong CV morbidity predictors for patients on haemodialysis (HD). Most importantly, PWV has been prospectively related to all-cause mortality in two different studies, with different end-stage renal disease (ESRD) populations [7,8]. Similarly, in studies using AIx to assess arterial stiffness, for each 10% increase in AIx the risk ratio was 1.51 [95% confidence interval (CI) = 1.23–1.86] for all-cause mortality [9]. Although impressive, it needs to be noted that these results have been obtained in a typical modern dialysis population: older patients with a high prevalence of diabetes and prior CV disease. It is also important to see whether these arterial stiffness alterations can confer the same negative mortality impact in populations that have yet to develop overt CV pathology.
Eastern European dialysis populations still have a large proportion of younger ESRD subjects, without significant overt cardiac comorbidities [10]. Therefore, these offer a unique experimental design opportunity, to better assess the effects of uraemia ‘per se’ as opposed to cumulative effects of numerous traditional and non-traditional CV risk factors and confounders.
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Methods |
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Study population
The enrolment period extended from January 1998 to December 2001. The ‘Dr C. I. Parhon’ University Hospital Dialysis Center opened in 1995, a period when an important development in dialysis facilities was also seen in Romania. Patients were selected if they have been on HD for at least 3 months and agreed to participate in the study, which was approved by the Hospital Ethics Committee. Based on the data from London et al. [9] we assumed a median survival time for the highest AIx tertile of 10 years, a median survival time for the lowest tertile of 4 years. We calculated that for a power of 80%, CI of 95% and an accrual period of 48 months (i.e. minimum 12 months of observation for the patients included at the end), we would require a total sample size of 80 patients. Since our population is relatively young compared with similar western populations and the rate of adverse events lower, a 10% increase in the final size of our group would be required. 118 of the entire 130 patient population of the ‘C. I. Parhon’ University Hospital Dialysis Center agreed to participate; a total of 10 patients were excluded due to a poor echocardiographic window, four patients due to recent stroke, 10 patients for severe chronic heart failure and two patients for severe chronic infections. Therefore, 92 patients were finally included in the analysis (i.e. 70.8% of the centre's dialysis population, 78% of the population considered and accepting to be studied)—inside the power calculation range. None of the patients had diabetes mellitus, and only 3.3% had prior history of CV disease.
During the follow-up period all patients were dialysed with similar technique in 5 h sessions, three sessions/week. Dialysis was performed on Fresenius 4008 dialysers with blood flow rate (QB) = 300, dialysate flow rate (QD) = 600, dialysate sodium concentration 135 mmol/l and dialysate calcium concentration 1.75 mmol/l. All patients were on erythropoietin therapy and on active vitamin D as recommended by national and European guidelines. At inclusion, 48.9% of our patients received anti-hypertensive medication: 27.2% were receiving angiotensin-converting enzyme inhibitors (ACE-I) therapy and 9.7% were receiving calcium channel blockers. None of the patients were on lipid-lowering therapy.
Data collection
Mortality data were obtained from patient charts. At inclusion, demographic data, blood pressure, blood chemistry, echocardiography and pulse wave analysis were performed.
Haemoglobin, total serum proteins and albumins, serum calcium and phosphate levels were recorded at inclusion and at monthly intervals after inclusion as a part of the centre protocol. Intact parathormone (iPTH) was determined at 6 month intervals and mean yearly value was retained in the study. Blood pressure was determined 10 min before the arterial stiffness measurements, with a mercury sphygmomanometer and cuff of appropriate size. All measurements were performed the day after the second HD session of the week.
CV disease was defined by the presence of stroke, myocardial infarction, chronic heart failure, coronary artery disease (CAD) and peripheral vascular disease.
Echocardiography
Echocardiographic studies were performed according to the guidelines of the American Society of Echocardiography, using a Kretz SA 9900 machine (Kretztechnik AG, Zipf, Austria), with a multi-frequency curved array transducer (2–4 MHz) allowing M-mode and two-dimensional measurements. The LV end diastolic diameter (EDD), interventricular septum thickness during diastole (IVST) and posterior wall thickness during diastole (PWT) were measured by M-mode. From these measurements, the LV mass (LVM) was calculated according to the Devereux formulae [11]. LVM index (LVMI) was calculated as the ratio between LVM and body surface area (BSA) (normal values 110 g/m2 for women and 130 g/m2 for men) [11].
Augmentation index (AIx)
AIx was determined from contour analysis of arterial waveforms recorded by applantation tonometry (AtCor®, PWV Inc., Westmead, Sydney, Australia) using a highly reproducible technique previously described elsewhere [12]. All measurements were taken in duplicate and averaged. AIx was calculated as the difference between the second and the first systolic peak measured on the aortic pressure waveform divided by the pulse wave height and multiplied with 100 (similar to [6]). All augmentation indices were corrected for a standard heart rate of 75 bpm. AIx and echocardiographic measurements were performed on a non-dialysis day, after the mid-week HD session, in order to minimize potential influences of the inter-dialytic weight gain. All measurements were performed between 11.00 and 13.00 h, exactly at 5 h after the ACE-I ingestion (as per design). After the baseline measurements, the patients were maintained on ACE-I therapy, if present at inclusion, for the entire duration of the follow-up, and was avoided in the rest of the patients without initial ACE-I therapy. The intra-observer error for AIx was first determined in 10 young healthy volunteers and in 10 ESRD patients: all results were under 1.4% with the same experienced investigator. Furthermore, in 10% of the patients AIx was measured for three consecutive HD sessions, by the same observer. The inter-session reproducibility was 94.7%.
Statistical analyses
All values are expressed as mean ± SD unless stated otherwise in the text. Data were analysed using the SSPS 12.0 for Windows software (SPSS Inc., Chicago, IL, USA). The outcome event was all-cause mortality. All potential (physiologically meaningful) determinants of AIx were investigated in a univariate screening procedure, using the Pearson's coefficient of correlation test. Significant determinants identified from these analyses were studied in a stepwise multiple regression model using the F-statistic. All variables associated with AIx with a level of significance <0.1 were included. Variables were forced in the model using a stepwise procedure. A P < 0.05 for the final model has been considered statistically significant.
Survival curves were estimated by the Kaplan–Meier product-limit method and compared by the Mantel (log rank) test. Prognostic factors of survival were identified by the use of logistic regression and the Cox proportional hazards regression model. Variables were considered to be prognostic when they were found to be statistically significant (P < 0.05) in the logistic regression or the Cox proportional hazards regression model of overall survival. The adjusted relative risk of experiencing an outcome event during follow-up was estimated as the hazards ratio (HR). Adjusted HR was calculated as the anti-logarithm of the ß-coefficient of the logistic regression of the outcome event with all prognostic variables considered as continuous variables in the model.
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Results |
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Patient characteristics
Baseline demographic, biochemical, vascular stiffness and echocardiography characteristics for the entire cohort at the time of inclusion are presented in Table 1. The age at inclusion was 42.6 years (range 20–60 years), and patients were on HD for 44.8 months (range 3–178 months). Comparative data from the only existing study in ESRD patients [9], and from non-renal patients with CAD [13], are also presented in Table 1. Our patients were significantly younger by 1–2 decades with better blood pressure control (significantly lower SBP and PP) and lower AIx.
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On univariate analysis, AIx was significantly correlated with: body weight (P < 0.001), radial SBP (P < 0.001) and haemoglobin (P < 0.05) (Table 2). There was no correlation between AIx and any of the echocardiographic parameters.
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All parameters correlating with AIx in the univariate analysis with a P < 0.1 were introduced in a stepwise multiple regression analysis model including also gender, height, time on dialysis, ACE-I use: again, AIx correlated only with weight (P < 0.001), SBP (P < 0.001) and haemoglobin (P < 0.05). Thirty-three percent of the AIx variability could be explained by these parameters (adjusted R2 = 0.33) (Table 3).
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In a next step, the study group was divided in three subgroups, based on tertiles of baseline AIx. Differences between the three groups are presented in Table 4. There was a significant trend for a lower weight, higher SBP and PP (P < 0.05 for trend) in patients with higher AIx. Also, patients in the first tertile of AIx had a significantly lower LVMI compared with the values recorded in patients in the other two tertiles.
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Furthermore, based on echocardiographic parameters at baseline, patients were divided into three groups: concentric LVH, eccentric LVH and concentric remodelling plus normal patients (similar to Koren et al. [14]). AIx was lower (17.3%) in the concentric remodelling plus normal patients group (compared with 20.4% in the concentric LVH group and 20.9% in the eccentric LVH group), but this difference did not reach statistical significance.
Outcome and prognostic impact of AIx
The follow-up period was 61 ± 25 months (range 3–108 months). During the follow-up period 15 deaths were recorded. In the Kaplan–Meier analysis, there was no difference in patients’ survival when divided by AIx tertiles, assessed by the log rank test (P = 0.78, Figure 1).
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According to the Cox analysis using a model including gender, age, time on dialysis, SBP, PP, LVMI, Aix and ACE-I therapy, the only independent predictors for all-cause mortality were age (P = 0.001), LVMI (P = 0.032) and ACE-I therapy (P = 0.039). The model significance was P = 0.014, with chi square 20.7 (Table 5). In our population, AIx was not an independent predictor for all-cause mortality. No other demographic, biochemical or echocardiography parameters were significant.
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Since LVMI was an independent predictor for survival, a second analysis was performed dividing the group in LVMI tertiles. Survival was not different in the three groups, as shown by the Kaplan–Meier analysis (log rank test, P = 0.173, Figure 2).
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Discussion |
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Structural changes in large arteries are characterized by dilatation, wall thickening and calcifications. Such changes are extremely frequent in ESRD patients [15,16]. Consequently, increased stiffness has been reported as being almost ubiquitously present in typical current dialysis populations. Most importantly, direct measures of arterial stiffness—such as pulse wave velocity (PWV) or incremental elastic modulus (Einc)—are major prognostic markers for CV and general mortality and morbidity [7]. Although frequently (and simplistically) considered to be another direct marker of increased arterial stiffness, augmentation index (AIx) depends in reality on many factors, including age, PWV, travelling distance of pressure waves (body height) and reflective properties of the arterial system. Until now, only one single study has prospectively described a significant negative prognostic impact on survival for AIx, in ESRD patients [9]. The main result of the present prospective study is that arterial wave reflections did not emerge as a significant independent predictor of mortality in a relatively young dialysis population without diabetes and overt CV disease. We did not measure changes in AIx to further refine the pathogenetic impact of the arterial wave reflections on cardiovascular outcomes—although this has been shown to be an equally important predictor [17], but our approach is similar to that of London et al. [9] and Weber et al. [13] (see below).
There are some major differences between the two longitudinal trials assessing the impact of AIx in renal patients (Table 1), mainly a large difference (12 years) in mean age and prior history of CV disease (3 vs 34%). Furthermore, in the study by London et al. [9] there were no data concerning the potential influence of an important confounder, LVM. In a very recent analysis of the prognostic power of 24 h ambulatory blood pressure monitoring for all-cause and CV mortality in a non-diabetic ESRD population, it was shown that when LVH is forced as a variable into the Cox model, the night/day systolic ratio loses its predictive power [18]. All these are extremely relevant, since according to the Cox analysis using a model including gender, age, time on dialysis, SBP, PP, LVMI, AIx, ACE-I therapy (see ‘Results’ section), the only independent predictors for all-cause mortality in our population were age, LVMI and ACE-I therapy. The increased effect of wave reflections on the aorta and central arteries causes increased SBP and decreased diastolic blood pressure (DBP) and/or diastolic tension-time index [19,20], greatly increasing LV oxygen requirements. It is therefore possible that the deleterious effect of a high(er) AIx may be apparent only in older patients with a drastically diminished cardiac reserve.
In non-renal subjects, an increased AIx has been shown to be predictive for CAD undergoing coronary angiography [13,21]: after controlling for classical risk factors, the highest quartile of AIx was associated with an increased risk of 6.91 (95% CI = 1.41–33.7) [13]. Similarly, in a recent study in CKD patients with various degrees of glomerular filtration rate (GFR) impairment [22], patients with normal angiograms had a significantly lower AIx (17.9 ± 5.6%) compared with subjects with evidence of obstructive coronary disease at angiography (23.4 ± 5.4%, P < 0.05). Moreover, as more coronary vessels were affected, AIx increased proportionally. There was a statistically significant linear relationship between the atherosclerosis burden and AIx (r = 0.46, P = 0.003). Based on receiver operating characteristics (ROC) analysis, mean AIx levels showed an optimal cut-off point at 17% (sensitivity = 0.87; specificity = 0.70)—very close to the mean AIx from our cohort. Independent predictors for AIx in this CKD population with a median age of 59 years were age and mean arterial pressure (MAP).
The present results support previous findings that prolonged survival is associated with ACE-I use, although, similar to [9], our study was not designed to compare the effect of different anti-hypertensive drugs on survival. Nevertheless, several trials have suggested a beneficial influence of ACE-I on arterial stiffness [23]. Other relevant therapies that might influence both survival and stiffness, such as statins [24] or sevelamer [25] were not used in our population. It is probably time now to formally test, in a randomized prospective trial, the impact of all these options (ACE-I, statins, new binding phosphates) on surrogate CVD endpoints (stiffness, LVM) and/or mortality, in dialysis populations.
Our study has several limitations. First, although the augmentation index (AIx) has been proposed and largely used as an index of arterial stiffness [26], this parameter—in addition to PWV—depends on the pattern of ventricular ejection and on arterial properties determining the amount and site of wave reflection. Particularly, these latter factors may be influenced by the vascular tone of the small, muscular arteries or arterioles, rather than by the elastic properties of the aorta. PWV was not measured concomitantly in our population to further dissect the exact role of increased arterial stiffness in this dialysis population. Second, the number of fatal events was significantly less compared with typical modern dialysis populations, most probably due to lower patient age and to a rather modest dialysis vintage (centre opened in 1995). Additionally, treatment was not standardized during the follow-up period, but this is practically impossible in such complex patients followed for long periods of time. A further potential bias might be related to the exclusion of patients with severe congestive heart failure (n = 10) and stroke (n = 4), usually associated with an abysmal outcome; however AIx is significantly influenced by these conditions (cardiac output, arm paralysis). Moreover, in our experience (data not shown) reproducibility is also significantly influenced (>5%) by such pathology, so we decided to avoid a technical-related bias.
In conclusion, the results presented fail to support the notion that an increased effect of wave reflections on central arteries is a strong and independent predictor of mortality in all ESRD patients on HD. The effect of wave reflections might be clearly dependent on patient age and concurrent comorbidity status. Further research is required to elucidate the independent impact of arterial stiffness in uraemia.
Conflict of interest statement. None declared.
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References |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
- Foley RN, Parfrey PS, Sarnak MJ. (1998) Clinical epidemiology of CV disease in chronic renal disease. Am J Kidney Dis 32 [Suppl 3]:S112–S119.
- Go AS, Chertow GM, Fan D, et al. (2004) Chronic kidney disease and the risks of death, CV events, and hospitalization. N Engl J Med 351:1296–1305.
[Abstract/Free Full Text] - Laurent S, Boutouyrie P, Asmar R, et al. (2001) Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37:1236–1241.
[Abstract/Free Full Text] - London GM, Guerin AP, Marchais SJ, et al. (1996) Cardiac and arterial interactions in end-stage renal disease. Kidney Int 50:600–608.[Web of Science][Medline]
- Covic A, Gusbeth-Tatomir P, Goldsmith DAJ. (2005) Arterial stiffness in renal patients: an update. Am J Kidney Dis 45:965–977.[CrossRef][Web of Science][Medline]
- Wilkinson IB, Fuchs SA, Jansen IM, et al. (1998) Reproducibility of pulse wave velocity and augmentation index measured by pulse wave analysis. J Hypertens 16:2079–2084.[CrossRef][Web of Science][Medline]
- Blacher J, Guérin AP, Pannier B, et al. (1999) Impact of aortic stiffness on survival in end-stage renal disease. Circulation 99:2434–2439.
[Abstract/Free Full Text] - Shoji T, Emoto M, Shinohara K, et al. (2001) Diabetes mellitus, aortic stiffness, and cardiovascular mortality in end-stage renal disease. J Am Soc Nephrol 12:2117–2124.
[Abstract/Free Full Text] - London GM, Blacher J, Pannier B, et al. (2001) Arterial wave reflections and survival in end-stage renal failure. Hypertension 38:434–438.
[Abstract/Free Full Text] - Mircescu G, Capsa D, Covic M, et al. (2004) Nephrology and renal replacement therapy in Romania-transition still continues (Cinderella story revisited). Nephrol Dial Transplant 19:2971–2980.
[Abstract/Free Full Text] - Devereux RB, Alonso DR, Lutas EM, et al. (1986) Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 57:450–458.[CrossRef][Web of Science][Medline]
- Covic A, Goldsmith DJ, Panaghiu L, et al. (2000) Analysis of the effect of haemodialysis on peripheral and central arterial pressure waveforms. Kidney Int 57:2634–2643.[CrossRef][Web of Science][Medline]
- Weber T, Auer J, O'Rourke MF, et al. (2004) Arterial stiffness, wave reflections, and the risk of coronary artery disease. Circulation 109:184–189.
[Abstract/Free Full Text] - Koren MJ, Devereux RB, Casale PN, et al. (1991) Relation of left ventricular mass and geometry to morbidity and mortality in uncomplicated essential hypertension. Ann Intern Med 114:345–352.
[Abstract/Free Full Text] - London GM, Guérin AP, Marchais SJ, et al. (1996) Cardiac and arterial interactions in end-stage renal disease. Kidney Int 50:600–608.[Web of Science][Medline]
- Savage T, Clarke AL, Giles M, et al. (1998) Calcified plaque is common in the carotid and femoral arteries of dialysis patients without clinical vascular disease. Nephrol Dial Transplant 13:2004–2012.
[Abstract/Free Full Text] - Takenaka T, Mimura T, Kanno Y, Suzuki H. (2005) Qualification of arterial stiffness as a risk factor to the progression of chronic kidney diseases. Am J Nephrol 25:417–424.[CrossRef][Web of Science][Medline]
- Tripepi G, Fagugli RM, Dattolo P, et al. (2005) Prognostic value of 24-hour ambulatory blood pressure monitoring and of night/day ratio in nondiabetic, cardiovascular events-free haemodialysis patients. Kidney Int 68:1294–1302.[CrossRef][Web of Science][Medline]
- Laurent S, Boutouyrie P, Asmar R, et al. (2001) Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37:1236–1241.
[Abstract/Free Full Text] - London GM. (2003) Cardiovascular calcifications in uremic patients: clinical impact on cardiovascular function. J Am Soc Nephrol 14 [Suppl 4]:S305–S309.
- Hayashi T, Nakayama Y, Tsumara K, et al. (2002) Reflection in the arterial system and the risk of coronary disease. Am J Hypertension 15:405–409.[CrossRef][Web of Science][Medline]
- Covic A, Haydar AA, Bhamra-Ariza P, et al. (2005) Aortic pulse wave velocity and arterial wave reflections predict the extent and severity of coronary artery disease in chronic kidney disease patients. J Nephrol 18:388–396.[Web of Science][Medline]
- London GM, Marchais SJ, Guerin AP, et al. (2003) Inflammation, arteriosclerosis, and cardiovascular therapy in haemodialysis patients. Kidney Int 83 [Suppl]:S88–S93.
- Ichihara A, Hayashi M, Ryuzaki M, et al. (2002) Fluvastatin prevents development of arterial stiffness in haemodialysis patients with type 2 diabetes mellitus. Nephrol Dial Transplant 17:1513–1517.
[Abstract/Free Full Text] - Takenaka T and Suzuki H. (2005) New strategy to attenuate pulse wave velocity in haemodialysis patients. Nephrol Dial Transplant 20:811–816.
[Abstract/Free Full Text] - Nichols WW and O'Rourke MF. (1998) McDonald's Blood Flow in Arteries: Theoretical, Experimental and Clinical Principles(Arnold, London, UK).
Accepted in revised form: 2. 5.06
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