The effect of isolated ultrafiltration on Doppler-derived indices of left ventricular diastolic function

Seppo Ojanen1, Vesa Virtanen1, Tiit Kööbi2, Jukka Mustonen1,3 and Amos Pasternack1,3

1 Department of Medicine and 2 Department of Clinical Physiology, Tampere University Hospital and 3 Medical School, University of Tampere, Tampere, Finland

Correspondence and offprint requests to: Seppo Ojanen, Department of Medicine, Tampere University Hospital, Box 2000, Teiskontie 35, FIN-33521 Tampere, Finland. Email: seppo.ojanen{at}kotiportti.fi



   Abstract
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. Haemodialysis (HD) is associated with acute changes simultaneously in fluid status (ultrafiltration) and in many biochemical parameters (dialysis). Reports on the effects of these changes on left ventricular (LV) diastolic function are scant. This study evaluated the effect of isolated ultrafiltration (UF) and subsequent HD with minimal fluid removal on Doppler-derived indices of LV diastolic function in patients who were asymptomatic and stable on HD.

Methods. In 11 HD cases, the 5 h treatment session was divided into a 2.5 h period of fluid removal without dialysis (UF phase) and 2.5 h of dialysis with minimal fluid removal (HD phase). We examined the following parameters of LV diastolic function echocardiographically: early rapid filling (Emax), atrial peak filling (Amax), Emax/Amax ratio, isovolumic relaxation time (IVRT) and deceleration time of the E-wave (DT).

Results. During the UF phase, Emax decreased from 0.82±0.2 to 0.62±0.2 m/s (P = 0.003), Amax decreased from 0.72±0.2 to 0.63±0.2 m/s (P = 0.042) and the ratio Emax/Amax did not change (P = NS). During the HD phase, Emax increased from 0.62±0.2 to 0.72±0.2 m/s (P = 0.018), Amax increased from 0.63±0.2 to 0.70±0.3 m/s (P = NS) and the Emax/Amax ratio remained unchanged (P = NS). IVRT was prolonged in 10 out of 11 patients at the start of the UF phase and it was further prolonged from 142±40 to 171±55 ms (P = 0.03) during the UF phase. IVRT did not alter during the HD phase (P = NS). During the UF phase, DT increased from 175±83 to 244±119 and it decreased from 244±119 to 209±98 in the HD phase, but both changes were statistically insignificant. No statistically significant correlations were observed between the changes in the Doppler indices of diastolic function and changes in biochemical parameters during the HD phase.

Conclusions. UF affects the parameters Emax, Amax and IVRT used to evaluate LV diastolic function. The changes in Emax and Amax during the HD phase are due to fluid refilling from tissues into the blood space, HD as such having no effect on Doppler indices. However, isolated UF or HD does not affect the Emax/Amax ratio. Emax and IVRT seem to be the most volume-sensitive parameters.

Keywords: haemodialysis; isolated ultrafiltration; left ventricular diastolic function



   Introduction
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
It has been accepted generally that the principal functional disorder in uraemic cardiomyopathy in patients on renal replacement therapy is left ventricular (LV) diastolic dysfunction. Its prevalence appears to be 30–60% [1,2]. It results from impaired LV diastolic relaxation and decreased LV compliance. Diastolic function is of considerable importance in the haemodynamic response to hypovolaemia, and dialysis patients with reduced LV compliance are particularly sensitive to haemodialysis (HD) hypotension [2–4]. The aim of this study was to explore the impact of ultrafiltration (UF) during dialysis on Doppler-derived indices of LV diastolic function in patients who are asymptomatic and stable on HD.

Diastolic LV function can be assessed non-invasively using pulsed Doppler analysis of flow across the mitral valve during diastole. Normally, as the mitral valve opens, ventricular relaxation occurs, with a rapid increase in flow leading to an early peak (Emax), followed by a later increase, to the atrial peak (Amax), which reflects atrial contraction. When the relaxation of the LV is reduced, Emax decreases. Thus, the second (atrial contraction) phase becomes compensatorily more important, resulting in a lowered Emax/Amax ratio.

Many previous studies have evaluated the effect of HD on LV diastolic function [5–8]. Emax, Amax, the Emax/Amax ratio, deceleration time (DT) and isovolumic relaxation time (IVRT), Doppler-derived indices, have been used to estimate function. In clinical practice, the Emax/Amax ratio is the most commonly used parameter [9], but its assessment value is limited in dialysis patients, since the pattern of LV diastolic filling is significantly altered by changes in preload [10]. Earlier studies suggest the preload-dependence of rapid early diastolic filling, but no significant change in the maximum velocity of the A-wave [5–8]. A decrease in the Emax/Amax ratio during UF might, thus, be interpreted erroneously to indicate deterioration of LV diastolic function.

Although HD entails acute changes both in preload (ultrafiltration) and in many biochemical parameters, the separate effects of HD and UF on diastolic function have not been studied adequately. In one study two incomparable dialyses were performed on different days: HD with and without fluid removal [11]. In our study, UF without dialysis and dialysis with only minimal UF were carried out sequentially during one session and simultaneous changes in LV diastolic function parameters were examined echocardiographically.



   Subjects and methods
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The study cohort consisted of 11 patients [six females and five males, aged 32–76 years (mean age±SD: 55.9±13.8 years)] with end-stage renal disease who were on regular maintenance HD for 4–5 h thrice weekly, with a mean time on dialysis of 13±6 months. The clinical characteristics of the studied patients and the other patients in the unit are summarized in Table 1. Table 2 compares weight changes and UF rates between these two groups. All patients were in sinus rhythm, in a stable haemodynamic state and were allowed to continue their usual medications.


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Table 1. Clinical characteristics of the studied patients and other HD patients in the unit

 

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Table 2. Comparison of mean weight changes (kg) and mean UF (ml) between the studied patients and other HD patients in the unit

 
The machine used for HD was a Fresenius 4008E (Fresenius AG, Bad Homburg, Germany), which controls UF volumetrically and which was fitted with cellulose acetate membrane hollow-fibre dialysers (Ca 130/170 series; Baxter Healthcare, Round Lake, IL, USA). The dialysate consisted of Na 140 mmol/l, K 2 mmol/l, Ca 1.5 mmol/l, Mg 0.5 mmol/l, Cl 111 mmol/l, HCO3 33 mmol/l, used at 36.5°C. The blood flow rate was individually prescribed (range: 250–350 ml/min).

The study session took place 43–45 h after a standard dialysis. A 5 h treatment session was divided into two parts. During the first 2.5 h (UF phase) the dialysate flow was turned off and the UF volume (mean: 1819 ml; range: 1060–3500 ml) was determined individually to yield a patient's clinically defined dry weight. At the close of the UF phase, patients were allowed to eat and during the next 2.5 h (HD phase) only the fluid volume they gained during the meal was removed (mean: 254 ml; range: 0–300 ml). Dialysate flow was fixed at 500 ml/min during the HD phase.

M-mode, two-dimensional and Doppler echocardiographic examinations were performed before and after the UF and after the HD phases by a single experienced observer (V.V.) using a Wingmed ultrasound unit with a 2.5 MHz transducer. The following parameters were assessed: left atrial diameter (LAD), left ventricular end-diastolic diameter (LVEDD), left ventricular end-systolic diameter (LVESD), interventricular septum thickness (IVST) and left ventricular posterior wall thickness (LVPWT). Left ventricular mass (LVM) was calculated according to the formula of Devereux et al. [9]:

LVM was corrected for body surface area to give the LVM index (LVMI). Left ventricular hypertrophy (LVH) was defined as an LVMI >134 g/m2 for males and >110 g/m2 for females at the end of the UF phase [12]. Left ventricular fractional shortening (FS) was defined as:

Systolic dysfunction was defined as an FS <25%. Left atrial enlargement was defined as a left atrial diameter >40 mm, after UF [13].

The mitral inflow velocity was measured by pulsed-wave Doppler echocardiography in the apical four-chamber view. The following indices were measured or calculated: maximal early diastolic flow velocity (Emax); maximal late atrial flow velocity (Amax); the Emax/Amax ratio; isovolumic relaxation time (IVRT), measured as the time from the closure of the aortic valve to the onset of mitral valve opening; and the rate of decrease in velocity following the E-velocity, measured as the deceleration time (DT). The criteria for diagnosing diastolic heart failure were based on the working group report of the European Study Group on Diastolic Heart Failure [14]. The reproducibility of M-mode and Doppler echocardiography has been published earlier by our group [15].

A whole-body impedance cardiograph (CircMonTM B202 device; JR Medical Ltd, Tallinn, Estonia) was used to estimate changes in extracellular water (ECW) and haemodynamic responses, as described elsewhere [16,17]. The following haemodynamic parameters were measured: heart rate (HR), stroke volume (SV) and cardiac output (CO). Systolic (SBP) and diastolic blood pressure (DBP) (measured by a manual sphygmomanometer) and their values were entered into CircMonTM B202 database. Systemic vascular resistance (SVR) was calculated according to the formula SVR = 79.96 (MAP/CO). Five-minute impedance measurements were made before the start of the UF phase, at 30 min intervals during the UF and HD phases and at the end of the HD phase. Blood volume (BV) was monitored non-invasively and continuously during each session with the CRIT-LINETM instrument (In-Line Diagnostics, Riverdale, UT, USA). During the study, averaged BV data were collected every 20 s and ECW data every 30 min.

Blood samples were taken before and after the UF and HD phases for haematocrit (B-Hct), sodium (P-Na), potassium (P-K), ionized calcium (P-iCa), phosphate (P-Pi) and venous blood pH and bicarbonate ion (), quantification being done with standard automated techniques (Kodak Ektachem 700, Technicon H2, Hitachi 717, ABL 500, CIBA Corning 634).

To compare changes in different parameters during the study, we used the two-way paired samples t-test with a Bonferroni adjustment. Associations between laboratory, BV, ECW, haemodynamic and echocardiographic parameters were evaluated using linear regression. A P-value of <0.05 was considered statistically significant. Results are expressed as means±SD.

All patients gave informed consent to participate in the study, which had been approved by the Ethics Committee of Tampere University Hospital.



   Results
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Figure 1 illustrates changes in BV and ECW during the study. The mean amount of fluid removed during the UF phase was 1.82±0.75 l (range: 1.06–3.50 l; 667±356 ml/h; range: 432–1400 ml/h). The mean ECW decline at the same time was 7.9±2.4% (P<0.001) and the mean diminution of BV was 7.8±3.4% (P<0.001). The mean amount of fluid removed during the HD phase was 0.25±0.91 l (range: 0–0.30 l; 93±45 ml/h; range: 0–132 ml/h). During the HD phase, ECW declined by 0.6±1.8% (P = NS) and BV increased by 2.9±2.8% (P<0.001).



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Fig. 1. Percentages of changes in BV and ECW during UF and HD with minimal UF. The bold line is the mean of the changes.

 
The effects of isolated UF and HD with minimal UF on cardiac parameters are listed in Table 3. During the UF phase, Emax decreased from 0.82±0.2 to 0.62±0.2 m/s (P = 0.001) and Amax from 0.72±0.2 to 0.63±0.2 m/s (P = 0.014); the change in their ratio (Emax/Amax) from 1.18±0.4 to 1.07±0.4 was not statistically significant (P = NS). At the time of UF, other echocardiographic indicators of diastolic function, IVRT and DT, lengthened, but DT insignificantly. During the HD phase, an increase in Emax from 0.62±0.2 to 0.72±0.2 m/s (P = 0.018) was the only statistically significant change in the parameters of diastolic function. Amax increased from 0.63±0.2 to 0.70±0.3 m/s (P = NS), while Emax/Amax did not change significantly (from 1.07±0.4 to 1.12±0.4; P = NS). When pre- and post-study values were compared, the changes in Emax from 0.82±0.2 to 0.72±0.2, in Amax from 0.72±0.2 to 0.70±0.3 and in Emax/Amax from 1.18±0.4 to 1.12±0.4 were statistically insignificant. The changes in Emax, Amax and in the Emax/Amax ratio are illustrated in Figure 2 and the changes in IVRT and DT in Figure 3.


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Table 3. Effects of UF and HD on Doppler and M-mode echocardiography indices and the statistical significance of the changes (P-values)

 


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Fig. 2. Percentages of changes in Emax, Amax and the Emax/Amax ratio during UF and HD with minimal UF. The bold line is the mean of the changes.

 


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Fig. 3. Percentages of changes in IVRT and DT during UF and HD with minimal UF. The bold line is the mean of the changes.

 
During the UF phase, left atrial diameter decreased from 44.8±5.51 to 41.2±6.9 (P = NS) and during the HD phase from 41.2±6.9 to 40.4±6.19 (P = NS). In this study population, LVH was detected in every patient and left atrial enlargement in five out of 11. The systolic function of the heart was impaired in four patients and remained abnormal during the study in all of them.

The changes in systemic haemodynamic variables and laboratory values are presented in Tables 4 and 5, respectively.


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Table 4. Effects of UF and HD on systemic haemodynamic parameters and the statistical significance of changes (P-values)

 

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Table 5. Effects of UF and HD on biochemical parameters and the statistical significance of changes (P-values)

 
No statistically significant correlations were observed between the changes in Emax or Amax and the changes in haemodynamic parameters during the UF and HD phases. Furthermore, the changes in the dimensions of the heart did not correlate with those of Emax and Amax. However, if we analyse the whole group, there were close and logical Pearson correlations between the changes in the means of Emax, Amax, SV and HR during both the UF (R = 0.99, P<0.001) and HD (R = 0.99, P<0.001) phases.

During the UF phase, the change in Emax showed some correlation with the amount of UF (R = 0.45, P = 0.17) and the change in BV (R = 0.44, P = 0.17).

There was an inverse correlation between the changes in plasma iCa and the changes in Emax during the UF phase (R = –0.64, P = 0.04). Also, the changes in HCO3 correlated negatively with changes in Emax during the UF phase (R = –0.71, P = 0.01). There was no significant relationship between other biochemical parameters and pulsed Doppler indices during the study.

The Emax/Amax ratio was abnormal in only one patient at the start of the study. This ratio changed during the study in two cases from normal to abnormal and in one from abnormal to normal. At the start of the study DT was abnormal in two patients. DT changed from normal to abnormal in three patients during the UF phase but normalized in two of them during the HD phase. IVRT was abnormal in 10 out of 11 patients throughout the study and the IVRT of that one normal patient also changed to abnormal during the HD phase.



   Discussion
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The only essential external factor that changed during the UF phase was fluid balance, which in turn is closely associated with changes in preload. Our study thus indicates that a change in preload has an effect on Emax, Amax, IVRT and DT, but not on the Emax/Amax ratio. The constancy we observed in the Emax/Amax ratio is at odds with earlier reports showing that fluid removal during standard dialysis with UF reduces mainly Emax velocity and, thus, the Emax/Amax ratio [5–8,11,18]. It is necessary, however, to point out that in some of those studies Amax velocity diminished also, albeit clearly less than Emax [6,18].

The already-known dependency of Emax on preload was confirmed in our study, but the marked diminution of Amax during UF was a new finding. The maximal velocity of the A-wave depends on, among other factors, heart rate and the contractility of the left atrium [10]. A decrease in heart rate, even within the physiological range, reduces atrial velocities. Our patients evinced significant decreases in heart rates during the UF phase and increases during the HD phase, but no correlation was observed between changes in heart rate and Amax. Myocardial contractility does not usually decrease during normal HD and may even increase [19]. The situation is different in isolated UF, during which cardiac output decreases according to the Frank–Starling mechanism, i.e. stroke volume decreases concomitantly with a decrease in preload [19]. It is thus possible that the concomitant decreases in the contractility of the left atrium and of the heart rate during isolated UF explain the considerable diminution of the A-velocity. An increase seen in A-velocity during the UF phase in two patients may be due to the somewhat lower fluid removal they underwent. The increases in Emax and Amax during the HD phase were obviously due to fluid refilling from the extracellular space into the blood space.

Our study confirmed the observation of Chakko and colleagues [11], that HD without fluid removal has no effect on LV diastolic filling parameters. To eliminate the effect of refilling during the HD phase would have required a study design in which isovolaemic dialysis is followed by UF alone. We did not want to do that, because during isovolaemic dialysis the rapid rate of solute removal results in an abrupt fall in plasma osmolality that contributes to the development of hypotension during the quite short UF phase. It is also worthy of remark that the main focus of our study was on the UF phase and only the Emax of Doppler-derived indices of diastolic function changed significantly during the HD phase.

We observed a very mild but statistically significant rise in the plasma concentration of ionized calcium during the UF phase, correlating with the decrease in Emax. This rise may be due to UF and the Donnan effect [20], wherein a change in the concentration of negatively charged albumin causes a small parallel change in the concentration of positively charged calcium.

A long IVRT reflects a reduction in LV relaxation and usually it is associated with myocardial ischaemia or LV hypertrophy, of which the latter was present in all of our patients [21]. In spite of the fact that a high preload shortens IVRT [10], it was prolonged in 10 out of 11 of our patients at the start of the UF phase. IVRT further lengthened during this phase, for a decrease in left atrial pressure leads to delayed mitral valve opening. It is also known that myocardial ischaemia prolongs IVRT [21]. Ischaemia is an unlikely explanation here, since in a previous study we concluded that isolated UF does not cause myocardial ischaemia [22]. The behaviour of DT during that study was similar to that of IVRT. Earlier studies have yielded conflicting results regarding the behaviour of IVRT and DT during dialysis [7,11,23]. In the current study, the prolongation of IVRT and DT during the UF phase obviously did not reflect deterioration in relaxation, but rather a return to the patient's normal state. Changes in preload due to refilling during the HD phase were obviously too slight to affect IVRT or DT.

The changes in preload during the UF phase led to notable haemodynamic responses: HR, SV and CO decreased, reflecting the recovery of the patients from the hyperdynamic cardiovascular state at the start of the UF phase. Refilling from the tissues during the HD phase increased BV and the changes in HR, SV and CO were the opposite of those observed in the UF phase. It is apparent, however, that the increase in cardiac output during the HD phase is also dependent on an increase in heart rate and a decrease in SVR. It is also very logical that haemodynamic parameters Emax and Amax changed in parallel, although not statistically significantly, when their changes were analysed in separate patients.

As to the interpretation of these results, it is noteworthy, first, that for this study we recruited only patients in a stable haemodynamic state. Therefore, the cohort included fewer patients with diabetes and more patients with glomerulonephritis and adult dominant polycystic disease compared with the HD population in the unit (Table 1). However, it is important to point out that there were no differences in weight changes and UF volumes between these groups (Table 2). Secondly, although this study design allowed us to evaluate the effects of pure UF on Doppler-derived indices of diastolic function, due to refilling the HD phase was not completely isovolaemic. Thirdly, the cohort was rather small, since we were unable to recruit more patients from our unit into this exploratory study, which was quite demanding of them. Thus, some of the correlations and results may simply be due to the small sample size; however, they should not be dismissed as unimportant. Also, due to the small number of patients, we used the Bonferroni correction in statistical comparisons; therefore, we want to highlight the information that can be acquired directly from Figures 1–3GoGo, which clearly show the main trends of the findings.

In summary, the results of this study demonstrate that the LV diastolic filling parameters Emax, Amax and IVRT are significantly affected by UF and preload but not by HD. Emax and Amax were so consistently dependent on preload that their ratio was not affected by isolated UF or HD with minimal UF. We further conclude that the changes during UF in the parameters of diastolic function obviously do not reflect deterioration in diastolic function but rather recovery from the hyperdynamic cardiovascular state caused by fluid retention. Unlike the Emax/Amax ratio, IVRT seems to be volume-sensitive and fluid removal during UF probably reveals the real values of IVRT. The clinical implication of our findings is that the individual's state of hydration must be taken into consideration when interpreting Doppler-derived indices of LV diastolic function in HD patients.



   Acknowledgments
 
This study was supported by the Medical Research Fund of Tampere University Hospital.

Conflict of interest statement. None declared.



   References
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received for publication: 17. 6.03
Accepted in revised form: 21. 7.04





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