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NDT Advance Access published online on September 4, 2008
Nephrology Dialysis Transplantation, doi:10.1093/ndt/gfn501
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© The Author [2008]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org


Haemodialysis is associated with a pronounced fall in myocardial perfusion

Judith J. Dasselaar1,2, Riemer H. J. A. Slart3, Martine Knip2, Jan Pruim3, René A. Tio4, Christopher W. McIntyre5, Paul E. de Jong2 and Casper F. M. Franssen1,2

1 Dialysis Center Groningen 2 Division of Nephrology, Department of Internal Medicine 3 Department of Nuclear Medicine and Molecular Imaging 4 Department of Cardiology, University Medical Center Groningen, Groningen, The Netherlands 5 Department of Renal Medicine, Derby City General Hospital, Derby, UK

Correspondence and offprint requests to: Casper F. M. Franssen, Division of Nephrology, Department of Internal Medicine, University Medical Center Groningen, Hanzeplein 1, 9713 GZ, Groningen, The Netherlands. Tel: +31-50-3615497; Fax: +31-50-3615403; E-mail: c.f.m.franssen{at}int.umcg.nl



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. Whereas haemodialysis (HD) is lifesaving by replacement of renal function, there are data to suggest that the HD procedure itself may contribute to the high cardiac risk in dialysis patients. The HD procedure is associated with an increased risk of sudden death, and there is accumulating evidence that HD can elicit myocardial ischaemia. In this study, we evaluated the effect of HD on global and regional myocardial blood flow (MBF) and left ventricular (LV) function in non-diabetic, non-cardiac compromised patients.

Methods. 13N-NH3 positron emission tomography (PET) was used to quantify changes in MBF, LV wall motion, cardiac output (CO), LV end-diastolic volume (LVEDV) and end-systolic volume (LVESV) in seven non-diabetic patients with uneventful cardiac histories. PET scans were performed before and at 30 and 220 min of HD.

Results. In all patients global MBF fell during HD. At 30 min of HD without ultrafiltration (UF), global MBF had fallen 13.5 ± 11.5% (P < 0.05) while CO, LVEDV and LVESV were 4.6 ± 5.3% (NS), 5.6 ± 4.2% (P < 0.05) and 6.9 ± 7.2% (P < 0.05) lower, respectively. At 220 min of HD, after UF of 2.5 ± 0.9 l, global MBF had fallen 26.6 ± 13.9% (P < 0.05) from baseline while CO, LVEDV and LVESV were 21.0 ± 19.7%, 31.1 ± 12.7% and 36.4 ± 17.5% (all P < 0.05) lower, respectively. In two patients, new LV regional wall motion abnormalities (RWMA) developed at 220 min of HD. MBF was reduced to a greater extent in regions that developed LV RWMA compared to those that did not.

Conclusions. Haemodialysis induced a pronounced fall in MBF. Since MBF fell already early during HD not only hypovolaemia but also acute dialysis-associated factors seem to play a role. Haemodialysis-associated reductions in MBF may contribute to the high cardiac event rate of dialysis patients.

Keywords: 13N-NH3 positron emission tomography; haemodialysis; myocardial ischaemia; myocardial perfusion; left ventricular function



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 References
 
Haemodialysis (HD) patients have markedly elevated cardiac mortality rates [1]. Much research has been directed at the mechanisms behind this excess mortality, but little attention has been given to the HD procedure itself as a potential cause of cardiac complications. It is evident that HD is stressful for the cardiovascular system since haemodynamic instability is one of its most frequent complications [2]. The risk of sudden cardiac death is increased during and immediately after an HD session [3]. Previous studies using electrocardiography [4–7], cardiac troponin T levels [8–11], 99Tc-sestamibi single-photon emission computed tomography [12] and echocardiography [13,14] suggest that HD may elicit myocardial ischaemia in a proportion of patients. Recently, McIntyre et al. demonstrated that HD is indeed capable of inducing regional myocardial ischaemia [15]. Using intra-dialytic H215O positron emission tomography (PET) and echocardiography, they showed that HD treatment elicited reversible left ventricular (LV) regional wall motion abnormalities (RWMA) with matched reductions in myocardial blood flow (MBF).

The patient group in the study of McIntyre et al. consisted of four patients, three of whom had diabetes mellitus as the cause of renal failure [15]. Although these patients did not have significant coronary artery disease, their longstanding diabetes may have caused structural and functional microvascular alterations that render them susceptible for the development of myocardial ischaemia. We questioned whether and to what extent an uncomplicated HD procedure would affect MFB and LV function in non-diabetic non-cardiac compromised patients. We specifically studied whether HD affects global and/or regional MBF in these patients and, if so, whether reductions in MBF are associated with the development of LV RWMA. We used gated 13N-NH3 PET since this technique allows the simultaneous assessment of MBF, LV wall motion, cardiac output and LV volumes during rest [16,17] and stress [18,19]. In order to delineate the influence of the hypovolaemic component of HD on MBF from the diffusive component of HD, we performed PET scans at almost zero ultrafiltration (UF) within 30 min after the start of HD and during maximal ultrafiltration-induced hypovolaemia at the end of the HD session.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 References
 
Patients
To be eligible, patients had to fulfil the following criteria: (1) Adult (age ≥18 years old) non-diabetic patients on maintenance HD for at least 6 months. (2) No episodes of dialysis hypotension in the 6 weeks preceding the study. Dialysis hypotension was defined as a drop in systolic blood pressure of >40 mmHg from the pre-HD value and/or institution of a treatment intervention by the dialysis nurse (temporary stop of UF and/or infusion of intravenous fluids). (3) Uneventful cardiac history, i.e. no angina pectoris (Canadian Cardiovascular Society classification [20] class <1), no myocardial infarction, no cardiac arrhythmia’s, no heart failure (New York Heart Association [21] class < 1). (4) No hypokinetic or akinetic regions or significant cardiac valve abnormalities on echocardiography. In our centre, echocardiography is performed at the start of HD treatment and thereafter at yearly intervals according to a standardized protocol. Exclusion criteria were (1) absence of informed consent and (2) (suspicion of) pregnancy.

Study protocol
The study comprised a single HD session that was carried out in the PET centre of the Department of Nuclear Medicine and Molecular Imaging. The study protocol is shown schematically in Figure 1. All patients underwent three gated 13N-NH3 PET scans: before HD, shortly after the start of the HD and at the end of HD. Data collection for the second and third PET scan was complete at 30 min and 220 min of HD, respectively. For the sake of clarity, the second and third PET scans are referred to as the 30-min and the 220-min scans, respectively, although data collection took 20 min preceding these time points. The timing of the 30-min PET scan was chosen in order to assess MBF, LV wall motion and LV volumes at almost zero UF. The timing of the 220-min PET scan was chosen in order to assess these parameters during maximal hypovolaemia since UF-induced intra-vascular volume depletion is most prominent at the end of HD treatment.


Figure 1
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  		Fig. 1 Schematic representation of the study protocol. Haemodialysis was started at T = 0 and lasted 4 h. During the first 30 min of HD, the UF rate was set at the minimal value (200 ml/h). Immediately after completion of the second PET scan the UF rate was increased to the value necessary to reach dry weight at the end of the remaining 3.5 h of dialysis. *The PET scan data acquisition took 20 min for each PET scan with the last 10 min in gating mode. See the text for detailed description of the study protocol.

 
13N-NH3 was administered intravenously at a constant rate through an indwelling catheter in the non-dialysis access arm. The Formula of 13N-NH3 is 10 min.

Each HD session was evaluated for pre- and post-HD body weight, blood pressure, heart rate, UF volume and treatment interventions. Blood pressure and heart rate were measured at 30-min intervals and immediately before and after each PET scan using an automated oscillometric monitor. Pre- and post-PET scan blood pressure and heart rate were averaged to obtain pre-HD and 30- and 220-min HD values. The rate–pressure product was calculated as the multiplication of heart rate and systolic blood pressure.

Patients were asked to refrain from coffee, tea, alcohol and tobacco use from the night prior to the study until completion of the study.

The study was approved by the Medical Ethics Committee of the University Medical Center, Groningen. Written informed consent was obtained from all participating patients. The study was performed in accordance with the principles of the Declaration of Helsinki and guidelines for Good Clinical Practice.

Dialysis settings
Since we wanted to mimic a regular HD session as much as possible, dialysis settings were identical to the usual settings in our centre with only one exception that the UF-rate was set at the minimal value (200 ml/h) until completion of the second PET scan at 30 min HD for reasons explained above. Immediately after completion of the 30-min PET scan the UF rate was increased in order to reach dry weight in the remaining 3.5 h of HD. A constant UF rate was used. The total duration of the HD session was 4 h.

Dialysis was performed with an AK 200 (Gambro-Hospal, Lund, Sweden) dialysis apparatus using low-flux polysulphone hollow-fibre dialyzers (F8, Fresenius Medical Care, Bad Homburg, Germany). The extracorporeal circuit volume was 280 ml. During connection of the extracorporeal circuit, 100 ml of NaCl (0.9%) was intravenously administered to the patient. Thus, the net volume loss from the circulation due to connection of the extracorporeal circuit was 180 ml. Patients were dialyzed in supine position and were not allowed to eat during the study in order to avoid the influence of posture and food intake on blood volume [22]. Blood and dialysate flow rates were 250 ml/min and 500 ml/min, respectively. Dialysate composition was sodium 139 mmol/l, potassium 1.0 mmol/l, calcium 1.5 mmol/l (3.0 mEq/l), magnesium 0.5 mmol/l, chloride 108 mmol/l, bicarbonate 3.1 mS/cm, acetate 3 mmol/l and glucose 1.0 g/l. Dialysate temperature was 36.0°C.

13N-NH3 study, data acquisition
An ECAT EXACT HR+ PET scanner (Siemens/CTI, Knoxville, TN, USA) was used that acquires 63 planes over a total axial length of 155 mm. A transmission scan (using 68Ge/68Ga rod sources) was performed 30 min before HD and before the last PET scan, followed by an injection of 400 MBq of 13N-NH3 intravenously. Dynamic data of 13N-NH3 were acquired over 20 min, with the last 10 min acquired in gated mode with 16 frames per cardiac cycle. The length of each gate was based on the current RR-interval. The RR-interval was allowed to vary 10%. Data were corrected for attenuation using the transmission scan and reconstructed using filtered back-projection (Hann filter: 0.5 pixels/ cycle). Ten minutes after starting HD, a second injection of 400 MBq of 13N-NH3 was administered followed by data acquisition over 20 min, with the last 10 min acquired in gated mode with 16 frames per cardiac cycle. After the second scan, the patients were transferred to a normal bed (maintaining the supine position) since this was more comfortable for the patient. At 180 min of HD, the patients were again positioned in the camera while maintaining the supine position. At 195 min of HD, a transmission scan was repeated and followed by a third injection of 400 MBq of 13N-NH3 at 200 min and subsequent 20 min data collection. Data of the second and third 13N-NH3 scan were corrected for the remaining activity of the previous scan.

13N-NH3 study, data analysis
A fit-procedure using the three-compartment model described by Hutchins et al. [23] was performed and absolute MBF was calculated. MATLAB was used for reorientation of the data into 12 short-axis slices of the 13N-NH3 studies. Using a parametric polar map programme, polar maps were reconstructed for baseline, early dialysis and late dialysis 13N-NH3 MBF. Polar maps were divided into 17 segments [24]. Segmental values of 13N-NH3 MBF were expressed in ml/min/100 g. Results for global MBF are presented as the mean of these 17 segments.

Gating data from the 13N-NH3 studies were reorientated to short-axis, horizontal and vertical long-axis sections. Gating data of 13N-NH3 were analysed quantitatively using the automatic quantitative gated SPECT (QGS) program (version 3; Cedars-Sinai Medical Center, Los Angeles, CA, USA), a commercially (Siemens Medical Systems, Hoffman Estates, IL, USA) available cardiac software package [25,26]. This program automatically detects the contours of the endocardium of the LV. Left ventricular end-diastolic (LVEDV), LV end-systolic volume (LVESV) and LV ejection fraction (LVEF) are calculated with QGS. RWMA were visually scored per LV wall segment as follows: 0 = normal; 1 = hypokinesia, 2 = akinesia/ dyskinesia. Wall motion was assessed separately for each of the 17 LV segments.

Statistical analysis
All data were analysed using GraphPad Prism, version 4.00 for Windows (GraphPad Software, San Diego, CA, USA). Data are presented as mean ± standard deviation (SD) unless stated otherwise. Comparisons were made with a paired Student's t-test or an unpaired t-test when appropriate. Pearson's correlation was used to assess the correlation between continuous variables. P-values of <0.05 were considered significant.



   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 References
 
Patients
Seven HD patients (five men) participated in the study. The patient characteristics are shown in Table 1. The mean age was 45.0 ± 18.6 years (range 24–75 years). The mean time on dialysis was 4.0 ± 2.4 years (range 1–8 years). The average pre-dialysis haemoglobin level was 11.9 ± 0.9 g/dl (range 10.6–13.5 g/dl). Three patients used 50 mg metoprolol taken after HD for the indication hypertension. No other vasoactive medication was taken. All patients were dialyzed via a native arteriovenous fistula. Gating was not successful in patient NR 6 because of frequent premature ventricular contractions, and therefore, data on cardiac output and LV volumes are presented for six patients.


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  		Table 1 Patient characteristics

 
Weight, UF volume, blood pressure and heart rate
Pre- and post-HD weight was 77.8 ± 12.5 kg and 75.3 ± 11.7 kg, respectively. The individual total UF volumes are shown in Table 1. The average UF volume during the complete HD session was 2831 ± 960 ml (range 1300–3780 ml). The cumulative UF volume was 100 ml at 30 min of HD and 2543 ± 859 ml (range 1174–3392 ml) at 220 min of HD (Table 2).


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  		Table 2 Ultrafiltration volume, blood pressure and heart rate

 
All HD sessions were uneventful. No episodes of dialysis hypotension occurred and none of the patients had angina complaints during or after HD. Systolic and diastolic blood pressure did not change significantly from baseline to either 30 min or 220 min of HD (Table 2). At 220 min of HD, systolic blood pressure was slightly but significantly lower in comparison with 30 min of HD. The heart rate showed a non-significant increase from baseline to 220 min of HD; at 220 min of HD, the heart rate was significantly higher than that at 30 min of HD. The rate–pressure products at 30 and 220 min did not differ from baseline (Table 2).

LV volumes, cardiac output and LV ejection fraction
LVEDV and LVESV decreased during HD in all patients (Figure 1 and Table 3). At 30 min of HD, LVEDV and LVESV had declined slightly but significantly (–5.6 ± 4.2% and –6.9 ± 7.2%, respectively). At 220 min of HD, LVEDV and LVESV had decreased by 31.1 ± 12.7% and 36.4 ± 17.5% from baseline, respectively (both P < 0.05). The stroke volume showed a non-significant decrease of 4.7 ± 5.4% at 30 min of HD; at 220 min of HD stroke volume had fallen by 26.5 ± 20.8% (P < 0.05) in comparison with baseline (Table 3).


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  		Table 3 Left ventricular volumes, cardiac output, left ventricular ejection fraction and myocardial blood flow

 
The cardiac output showed a non-significant decrease of 4.6 ± 5.3% at 30 min of HD, whereas at 220 min of HD the cardiac output had decreased by 21.0 ± 19.7% (P < 0.05) from baseline (Figure 1 and Table 3). The LV ejection fraction (LVEF) showed a non-significant increase of 13.3 ± 26% from baseline to 220 min of HD (Table 3).

Myocardial perfusion and LV wall motion
MBF decreased during HD in all patients (Figure 2). Global MBF had already significantly fallen by 13.5 ± 11.5% at 30 min of HD. At 220 min of HD, the average global MBF had decreased by 26.6 ± 13.9% (P < 0.05) compared with baseline (Table 2). At 220 min of HD, the change in global MBF correlated significantly (r = 0.84, P = 0.03) with the change in the cardiac output (Figure 3). There was a trend towards a significant correlation between the cumulative UF volume at 220 min of HD and the change in global MBF from baseline to 220 min of HD (r = –0.66; P = 0.11).


Figure 2
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  		Fig. 2 Relative change from baseline of the left ventricular end-diastolic volume (LVEDV, A), left ventricular end-systolic volume (LVESV, B), cardiac output (C) and myocardial blood flow (D). Each line represents an individual patient. In each of these figures, the same symbols are used for individual patients. The patient numbers correspond with those used in Table 1.

 

Figure 3
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  		Fig. 3 Relationship between the relative change in myocardial blood flow and the relative change in cardiac output (both from baseline). The open squares represent the correlation at 30 min of HD (not significant). The closed squares represent the correlation at 220 min of HD (r = 0.84; P = 0.03).

 
At baseline and at 30 min of HD, no LV RWMA were observed. At 220 min of HD, LV RWMA were observed in two patients (patients NR 1 and 2 from Table 1). In patient NR 1, new LV RWMA developed in 3 of the 17 LV segments at 220 min. In this patient, the mean change in MBF was –26 ± 5% in segments that developed LV RWMA and –13 ± 9% in those that preserved normal function (P = 0.03). In patient NR 2, new LV RWMA developed in 8 of the 17 LV segments. Compared with baseline, the mean change in MBF for segments in which LV RWMA developed and those that preserved normal function was –47 ± 6% and –33 ± 13%, respectively (P = 0.004). These data demonstrate that the reduction in regional LV contractility was associated with relative perfusion defects in the corresponding regions in both patients. In the two patients that developed LV RWMA, the cardiac output had decreased by –39.4% and –32.3% at 220 min of HD, respectively, whereas the average fall in the cardiac output in the remaining patients was –13.6 ± 20.5% (non-significant).



   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
References
 
This study demonstrates that the HD procedure is associated with a significant fall in myocardial perfusion. This was observed in ‘relatively healthy’ dialysis patients that were selected for having a low cardiovascular risk, e.g. non-diabetic patients with stable HD sessions and uneventful cardiac histories. Two of the seven patients who were studied developed regional LV dysfunction in regions with the greatest fall in MBF. Notably, these cardiac derangements were clinically silent.

Our results confirm the recent data from McIntyre et al. [15] who reported similar intra-dialytic reductions in MBF. In their study, all four (three of whom had diabetes) patients developed segmental LV dysfunction with matched reductions in MBF [15]. These and our data, together with the observation of functional post-dialysis recovery [15], indicate that HD is capable of inducing myocardial ischaemia and myocardial stunning.

Various factors render HD patients sensitive for the development of cardiac ischaemia. Uraemic patients have a high prevalence of coronary atherosclerotic lesions [27,28] and structural and functional alterations in the microcirculation [29,30] as well as abnormalities in myocardial metabolism [31]. Specifically, a reduction in capillary density (‘myocyte-capillary mismatch’) has been described [29,30] which is, in part, explained by left ventricular hypertrophy (LVH). Myocardial perfusion reserve has been found to be decreased in patients with chronic renal failure [32], in diabetic HD patients [33] and in young adults after renal transplantation [34] in the absence of coronary artery disease. This indicates that reduced renal function is associated with attenuated coronary vasodilator capacity even in patients without obstructive coronary disease [32]. Additional factors also play a role. LVH renders the ventricle more sensitive to acute changes in filling pressure during UF-induced hypovolaemia [35]. Increased peripheral artery stiffness also has an adverse effect on MBF and reduces the threshold for myocardial ischaemia in patients with coronary artery disease [36]. LVH together with increased vascular stiffness predispose to reduce subendocardial blood flow [37].

Repetitive HD-induced myocardial ischaemia may contribute to the high cardiac event rate of HD patients [15,38]. Cardiac ischaemia may act as a trigger for arrhythmias and may lead to sudden death [3,39]. Repetitive cardiac ischaemia can lead to cumulative stunning and potentially has a role in the development of heart failure [40–42], a condition that is highly prevalent in HD patients [43]. Stunning has been shown to be a powerful predictor of a dismal prognosis in patients with coronary artery disease [44]. Presently, the prognostic impact of HD-associated stunning on the outcome in HD patients is unknown.

Contrary to our expectations, we observed a significant reduction in MBF already shortly after the start of HD. At this time hypovolaemia was not prominent since only 100 ml of fluid had been filtered during the first 30 min of HD although filling of the extracorporal circuit led to some additional blood loss from the circulation. Notably, at 30 min of HD the diastolic (the main determinant of coronary blood flow) and systolic blood pressure as well as the cardiac output were identical in comparison with baseline. All in all, hypovolaemia seems an unlikely explanation for the decrease in MBF this early during HD. We can only speculate on possible explanations. Acute dialysis-related factors may play a role, e.g. electrolyte shifts, acid–base shifts or HD-induced temperature effects. In particular, (changes in) the plasma calcium level and core body temperature may influence vascular tone and may thus potentially have an effect on myocardial blood flow. The effect of these and other factors, like the use of cardiotropic medication and (modifications of) the UF rate, on myocardial perfusion should be investigated in future studies. Notably, in the present study we used dialysis settings that favour haemodynamic stability, e.g. a relatively low dialysate temperature of 36°C and a dialysate calcium concentration of 1.5 mmol/l (3.0 mEq/l).

This study has some potential weaknesses. First, patient numbers are small and, thus, our results need to be replicated in a larger number of patients. Second, we did not perform coronary angiography in our patients, and therefore, we cannot rule out that some patients had significant coronary artery disease. However, none of the patients had angina pectoris before or during the 6 months’ follow-up after completion of this study. Third, we cannot prove that the observed fall in MBF and the LV RWMA reversed after termination of the HD session since we did not perform post-HD measurements. However, it is unlikely that these patients experienced cumulative reductions in MBF and cumulative LV RWMA since these patients exhibited no signs of myocardial ischaemia or heart failure, neither at the time of the study nor during the 6 months’ post-study follow-up. Notably, studies using echocardiography have shown that most of the regions that displayed HD-associated LV RWMA had regained normal contractile function at 30 min post-HD [13,14].

In conclusion, the HD procedure induced a pronounced fall in myocardial perfusion. This was observed in non-diabetic non-cardiac compromised patients. As myocardial perfusion fell already early during HD without significant fluid removal, not only UF-induced hypovolaemia but also acute dialysis-associated factors seem to play a role. HD-associated reductions in MBF may contribute to the high cardiac event rate of dialysis patients. The identification of the factors that are responsible for the HD-induced fall in MBF will probably yield strategies to better preserve myocardial perfusion during HD and may potentially benefit patients that experience HD-related adverse cardiac events.



   Acknowledgments
 
This study was supported by an unrestricted grant from Amgen BV.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received for publication: 18. 5.08
Accepted in revised form: 11. 8.08


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