Feeding during dialysis—risks and uncertainties

Feeding during dialysis—risks and uncertainties ABSTRACT Allowing dialysis patients to eat during the treatment is controversial. It is, therefore, no surprise that practices and policies with respect to intradialytic food consumption vary considerably from unit to unit and from country to country. Those who defend the position of feeding during dialysis reason that intradialytic meals offer a supervised and effective therapy for protein-energy wasting. Those who take the opposite view argue that intradialytic food intake should be avoided for the following three reasons. First, interventional studies show that eating during dialysis causes a clinically significant reduction in systemic blood pressure during the postprandial period and elevates the risk of symptomatic intradialytic hypotension; the latter is associated with increased mortality risk. Second, clinical studies have shown that eating during dialysis interferes with the adequacy of the delivered dialysis, whereas eating 2–3 h before the dialysis session has no impact on the efficiency of the subsequent dialysis treatment. And third, randomized studies show that eating during dialysis focus on the positive outcomes but do not adequately balance this potential benefit against the risk of intradialytic hemodynamic instability and poor quality of delivered dialysis. Even after half a century of providing long-term dialysis, definitive randomized trials that balance risks and benefits of eating during dialysis are missing. These knowledge gaps require randomized trials. Since there is a real possibility of harm with eating during dialysis, we caution that instead of encouraging the widespread use of intradialytic meals, practices and policies should focus on adequate nutrient intake during the interdialytic interval. blood pressure, dialysis adequacy, intradialytic hypotension, intradialytic meals INTRODUCTION Whether end-stage renal disease (ESRD) patients on chronic dialysis should be allowed to eat during the treatment or not remains a rather controversial issue [1, 2]. It is, therefore, not surprising that practices and policies on eating during dialysis differ from unit to unit and country to country. For example, dialysis units in North America, and particularly in the USA, are less likely than European and Asian units to permit eating during dialysis [3, 4]. In a recent survey of clinic practices and clinician opinions related to intradialytic feeding within a large dialysis care provider in the USA, it was shown that 28.6 and 22.6% of dialysis units restricted eating during treatment in 2011 and 2014, respectively [5]. This shift towards less restrictive in-center positions on eating during dialysis could be partially explained within the context of studies supporting the notion that oral food intake or intradialytic nutritional supplementation may improve protein-energy wasting [6–8] and health-related quality of life [9], and that these effects are possibly translated into a net clinical benefit [10, 11]. It has to be noted, however, that the abovementioned effect on nutritional status, if any, is counteracted by an unrecognized risk. Intradialytic feeding may unfavorably influence the postprandial blood pressure (BP) response and induce intradialytic hemodynamic instability. In this review, we discuss observational and interventional studies which show that eating during dialysis is accompanied by a more rapid postprandial reduction in BP as well as increased incidence of symptomatic hypotension and other adverse intradialytic symptoms [12–14]. We also discuss studies that provide evidence of alterations in systemic circulation in response to intradialytic food consumption that interfere with the adequacy of the delivered dialysis [15, 16]. The argument that these observations were evident predominantly in earlier studies conducted in patients receiving renal replacement therapy with acetate dialysate solutions and before the widespread use of more biocompatible membranes, volumetric ultrafiltration and low-temperature dialysis is opposed by the results of recent studies confirming the adverse hemodynamic effect of eating during dialysis even in the era of dialysis procedure optimization [17]. In this context, the 2007 European Best Practice Guidelines on intradialytic hemodynamic stability recommended the avoidance of food consumption during dialysis as a measure to prevent the occurrence of adverse intradialytic events, particularly in patients susceptible to intradialytic hypotension [18]. In this review, we discuss the existing evidence regarding eating during dialysis. We conclude that the scientific basis of the use of intradialytic meals or nutritional supplements as a tool to increase the caloric intake and improve nutritional status is weak and clearly counteracted by increased risk for intradialytic hemodynamic instability and reduced dialysis adequacy. INTRADIALYTIC HEMODYNAMIC STABILITY Intradialytic hypotension is the most commonly occurring dialysis-related complication, affecting approximately 20–30% of all dialysis treatments [19]. Apart from impairing patients' overall sense of well-being, the abrupt tissue hypoxia and hypoperfusion resulting from intradialytic hypotension is an important cause of morbidity among dialysis patients [19]. Prospective observational studies have associated intradialytic hypotension with a variety of clinical events such as excess risk of cardiac arrhythmias, myocardial and cerebral ischemia, vascular access thrombosis and more rapid deterioration of residual renal function [20–23]. Importantly, either symptomatic hypotension or large asymptomatic reductions in BP from pre- to post-dialysis are both strong and independent predictors of cardiovascular and all-cause mortality [24–26]. Among several other mechanistic pathways involved in the pathogenesis of intradialytic hypotension, observational and interventional studies suggest that oral food intake during dialysis exacerbates the incidence of this serious and potentially life-threatening dialysis-related complication. These studies are summarized in (Table 1) and discussed in detail below. Table 1 Interventional studies evaluating the effect of eating during dialysis on intradialytic hemodynamic stability Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min DialNa, dialysate sodium; IDH, intradialytic hypotension; N/A, not available. Table 1 Interventional studies evaluating the effect of eating during dialysis on intradialytic hemodynamic stability Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min DialNa, dialysate sodium; IDH, intradialytic hypotension; N/A, not available. Observational studies In a cross-sectional study, Strong et al. [29] evaluated the association between food and fluid intake during dialysis with the occurrence of symptomatic intradialytic hypotension requiring interventions in 23 randomly selected patients over 166 dialysis treatments. Intradialytic food consumption (i.e. >200 calories/session) was associated with 2-fold higher incidence of hypotension (P = 0.003); the likelihood of hypotension was three times higher if patients reported the consumption of any fluid during dialysis (P = 0.011). In addition, the use of mannitol as a therapeutic intervention to control symptomatic hypotension was also significantly higher when patients consumed meals or fluids during the intradialytic period [29]. The association of oral food intake with intradialytic hemodynamic instability was not confirmed in a subsequent retrospective analysis of 126 stable dialysis patients studied over three consecutive dialysis treatments [30]. However, the absence of association could be attributable to the fact that the incidence of symptomatic intradialytic hypotension was not directly assessed in this analysis, possibly due to the retrospective study design; in contrast, intradialytic hypotension was defined as the occurrence of systolic BP <100 mmHg at any time-point of the dialysis sessions under study [30]. Since the observational evidence cannot prove causality, we subsequently discuss the evidence from interventional studies in order to clarify the association of food intake with intradialytic hemodynamic instability. Interventional studies In the first study to investigate the effect of food intake on intradialytic BP response, Sherman et al. [13] enrolled nine nondiabetic dialysis patients who had no evidence of autonomic neuropathy or orthostatic hypotension. A standard meal was administered 1.5 h after the initiation of dialysis in 62 out of 125 dialysis treatments in a prospective, non-randomized study design. Compared with control dialysis, administration of intradialytic meals was associated with a more rapid postprandial reduction in mean arterial pressure (MAP) (−14.4 mmHg/h versus −2.2 mmHg/h; P = 0.03) and in diastolic BP (−9.9 mmHg/h versus −2.8 mmHg/h; P = 0.01) [13]. Symptomatic hypotension occurred more frequently during the postprandial intradialytic periods than during the corresponding fasting periods (13 versus 2 episodes; P < 0.05) [13]. In a randomized crossover study, Zoccali et al. [14] compared the postprandial BP alterations induced by a standard snack (≈450 kcal energy) given 1 h after the initiation of dialysis with the BP changes occurring during the corresponding fasting period in 13 stable dialysis patients. Although BP was reduced during both snack-dialysis and control-dialysis, oral food intake was associated with a higher rate of postprandial BP reduction (−0.29 versus −0.08 mmHg/min; P < 0.001 for systolic BP and −0.15 versus −0.03 mmHg/min; P < 0.001 for diastolic BP) [14]. Once again, the incidence of symptomatic intradialytic hypotension requiring saline infusion was significantly higher during the snack-dialysis than during the control-dialysis (23 events in 10 patients versus 12 events in 6 patients; P = 0.025) [14]. In a subsequent double-blind, randomized, cross-over study [12] 10 dialysis patients were studied on three different occasions (placebo/no meal versus placebo/meal versus caffeine/meal). The ultrafiltration rate in the first 2 h of dialysis was maximized to accentuate hemodynamic stress. Compared with control dialysis, the rate and the magnitude of reduction in MAP were significantly higher during the placebo/meal and caffeine/meal dialysis. This postprandial reduction in MAP was shown to be mediated through a parallel decrease in systematic vascular resistance; notably, there was no compensatory increase in cardiac output. The administration of caffeine was unable to mitigate the impact of intradialytic meal ingestion on MAP levels [12]. The mechanistic background of the hemodynamic response to intradialytic food consumption was explored in two subsequent studies investigating potential alterations in intravascular volume with the use of relative blood volume (RBV) monitoring during dialysis. In the first, Shibagaki et al. [27] showed a significant increase in RBV between the pre-prandial and postprandial periods (3.24 ± 0.57 versus 13.99 ± 0.91%/h) in 16 dialysis patients who digested a standard meal in the supine position. The rate of change in RBV was modified simultaneously with meal ingestion and this effect disappeared within 43 ± 3 min after food ingestion. Postprandial alteration in RBV was more prominent when the meal was digested in the sitting position (ΔRBV: 28.21 ± 2.14%/h) and was accompanied by a parallel reduction in BP levels (152/85 versus 143/79 mmHg from pre- to postprandial periods) [27]. In the second study, Sivalingam et al. [28] evaluated the hemodynamic effect of intradialytic food intake in 20 nondiabetic dialysis patients. A standard meal was administered 45 min after the initiation of dialysis and several hemodynamic parameters (i.e. BP, cardiac output, peripheral vascular resistance and RBV) were continuously monitored over a regular mid-week dialysis session. In line with the results of the aforementioned study of Shibagaki et al. [27] a significant increase in the rate of reduction in RBV was noted between the pre- and postprandial periods (0.08 ± 0.07 versus 0.24 ± 0.10%/min; P < 0.005). The maximal reduction in RBV occurred at a mean time of 16 min (range: 8–26 min) and the effect disappeared at a mean time of 30 min (range: 10–40 min) after food ingestion. A parallel reduction in MAP levels was noted between the start and 30 min after meal ingestion (P = 0.04) [28]. In contrast, intradialytic food intake had no impact on cardiac output, peripheral vascular resistance and heart rate. These findings directly support the notion that redistribution in blood volume between the systemic and splanchnic circulations is involved in the causal pathway of the BP-lowering effect of food consumption during dialysis. To investigate the potential effect of timing of food intake on the intradialytic hemodynamic response, Borzou et al. [17] evaluated 48 dialysis patients in two dialysis sessions. In the first session, patients were given a standard meal 1 h after the initiation of dialysis and in the second session, the same meal was given 2 h after the initiation of dialysis. Significant reductions in BP levels were noted between the pre-meal and post-meal periods in both dialysis sessions under study (first session: −7.7/−4.4 mmHg; P < 0.001; second session: −4.6/–3.0 mmHg; P < 0.001, respectively) [17]. However, the magnitude of BP reduction during the postprandial period was unaffected by the timing of meal intake. Similarly, changes in the timing of meal intake during the dialysis session did not modify the intensity of nausea, vomiting or other adverse intradialytic symptoms [17]. Ingestion of a large amount of food during dialysis may lead to errors in the estimation of ultrafiltration volume when calculated by the difference in weight from pre-dialysis to post-dialysis. Accordingly, in some dialysis units, the quantity of fluid ingested during dialysis is added to the ultrafiltration goal for the day. This may further exacerbate the risk for intradialytic hypotension. Such a practice is also without an evidence base. DIALYSIS ADEQUACY The hemodynamic alterations evoked by intradialytic meal intake (i.e. postprandial reduction in BP and peripheral vascular resistance) and redistribution of circulating blood volume due to excessive blood pooling in the splanchnic circulation are proposed as the mechanistic substrate for a negative impact of intradialytic food intake on the adequacy of delivered dialysis [2]. This notion is supported by a number of interventional studies summarized (Table 2) and discussed in detail below. Table 2 Interventional studies evaluating of intradialytic food consumption on dialysis adequacy Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min DialNa, dialysate sodium; N/A, not available. aOnline monitored Kt/V during the dialysis session. Table 2 Interventional studies evaluating of intradialytic food consumption on dialysis adequacy Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min DialNa, dialysate sodium; N/A, not available. aOnline monitored Kt/V during the dialysis session. In a prospective controlled study, 14 dialysis patients were evaluated during two mid-week dialysis sessions with a 1-week interval between them. In the first session, patients were allowed to eat during dialysis and in the second session, intradialytic meal consumption was prohibited [16]. Dialysis adequacy assessed in terms of urea reduction ratio (URR) and Kt/V measured by the Daugirdas formula was significantly lower in the dialysis session with meal as compared with control dialysis session (URR: 71.5 ± 5.9 versus 73.5 ± 6.6; P < 0.05; Kt/V: 1.54 versus 1.65, P < 0.05) [16]. This reduction in URR and Kt/V in response to intradialytic food intake was confirmed in a subsequent study of 25 stable dialysis patients. Each patient was evaluated during two regular mid-week dialysis sessions performed at identical ultrafiltration rates (meal-dialysis versus control-dialysis) over two consecutive weeks [32]. The URR and Kt/V were significantly lower during the dialysis session with food intake than during the session without food intake (URR: 67.8 ± 6.1 versus 72.1 ± 6.0%; P < 0.001; Kt/V: 1.4 ± 0.2 versus 1.6 ± 0.2; P < 0.001) [32]. The effect of intradialytic food intake on dialysis adequacy was evaluated in 40 dialysis patients who underwent continuous online Kt/V monitoring during a regular mid-week dialysis session with the use of UV absorbance system [15]. A standard meal was given around 2 h after the initiation of dialysis to investigate whether meal-related hemodynamic alterations and/or redistribution in circulating blood volume may influence the slope of Kt/V curves. This study showed that intradialytic meal consumption had a direct impact on online Kt/V as measured by the UV absorbance system. While the mean Kt/V change over time was 0.33 ± 0.02/h before food intake, it dropped within minutes after meal ingestion to −0.01 ± 0.04/h. Intradialytic meal intake was responsible for a relative decrease of 101.5 ± 50.4% in continuously monitored Kt/V (P < 0.001). Shortly after the end of the meal, the rate of change in Kt/V increased and progressively reached the pre-meal levels (0.32 ± 0.01/h) [15]. This meal-related effect on dialysis adequacy was not reproducible when Kt/V was monitored using an ionic dialysance-based system. The explanation provided by the authors for the discrepancy between the two methods was that short-term postprandial variations in online Kt/V measured by UV absorbance may not reflect a true decrease in Kt/V, but these meal-related changes could be attributed to an intermittent increase in UV-absorbing dialyzed solutes [15]. In contrast, oral food intake some hours before the initiation of the treatment is less likely to affect the adequacy of the subsequently delivered dialysis. This hypothesis was tested in a study comparing the efficiency of a single dialysis session undertaken after a 3-h fasting with that of a meal 2 h before the initiation of dialysis in 42 stable dialysis patients [31]. This study showed that the levels of URR and Kt/V were identical regardless of the presence or absence of a meal ingested before the start of dialysis (URR: 72.4 ± 5.2 versus 72.8 ± 4.7%; P = 0.35; Kt/V: 1.56 ± 0.2 versus 1.58 ± 0.2; P = 0.42 for fed versus fasting dialysis, respectively) [32]. This effect was shown to be consistent in subgroup analyses performed according the gender and diabetic status of study participants [31]. These data suggest that instead of imposing the risk of a less efficient dialysis by allowing intradialytic food intake, we could cover their caloric requirements by encouraging the patients to eat 2–3 h before their dialysis treatment. An argument can be made that reduction in Kt/V with eating during dialysis is simply an artefact of measurement. If protein-induced increase in urea generation leads to an appearance of a reduced dialysis efficiency then this would not truly be a reduction in the efficiency of dialysis. However, the data of Muller-Deile et al. [15], where dialysis efficiency fell within minutes of food intake, suggest that hemodynamic mechanisms may be operative. Nonetheless, better quality data are needed to confirm or refute whether dialysis efficiency is truly reduced by eating during dialysis. NUTRITIONAL STATUS One may argue that dialysis patients should be allowed to eat during the treatment since intradialytic meals may benefit protein-energy wasting and nutritional status [3, 4]. This position is based mainly on the results of small interventional studies showing that oral nutritional supplementation during dialysis (and not administration of intradialytic meals) increases the caloric intake during the dialysis-on day and improves some markers reflecting malnutrition (a slight elevation in serum albumin levels) [6–9]. In addition, those opposing the restrictive in-center nutritional policies base their opinion on the results of a few observational studies associating intradialytic nutritional supplementation with reduced mortality risk [10, 11], arguing that restriction of intradialytic food consumption is a ‘lost opportunity’ to improve the clinical outcomes in the high-risk dialysis population. In 2016, Rhee et al. published the results of the Fosrenol (lanthanum carbonate) for Enhancing Dietary Protein Intake in Hypoalbuminemic Dialysis Patients (FrEDI) trial [33]. In this trial, 110 dialysis patients with serum albumin <4 g/dL were randomly assigned to receive high-protein (50–55 g) meals during dialysis combined with lanthanum carbonate or low-protein (<1 g) meals during dialysis for 8 weeks. Background therapy with non-lanthanum-based phosphate-binders remained constant throughout the course of the trial. This trial showed that administration of high-protein meals during dialysis improved the composite primary trial endpoint of a rise in serum albumin of ≥0.2 g/dL while maintaining phosphorus between 3.5 up to <5.5 mg/dL; 27 patients in the high-protein arm versus 12 patients in the low-protein arm reached the primary outcome (P = 0.045) [33]. The authors concluded that among hypoalbuminemic dialysis patients, intradialytic intake of high-protein meals in conjunction with lanthanum carbonate corrects serum albumin without aggravating the risk of hyperphosphatemia. Despite the theoretically positive results of the FrEDI trial [33], our position that dialysis patients should not be allowed to eat during the intradialytic period still relies on a strong scientific basis for several reasons: (i) the FrEDI trial did not assess the impact of intradialytic food intake on intradialytic hemodynamic stability and dialysis adequacy; these outcomes were not assessed even as secondary safety endpoints [33]. Accordingly, the FrEDI trial cannot answer the question of whether the slight benefit on serum albumin levels is counteracted by excess risk of intradialytic hypotension (symptomatic or asymptomatic) or less efficient dialysis. (ii) The prevention of the risk of hyperphosphatemia achieved through the supervised administration of phosphate binders during the intradialytic meal within the course of a randomized trial is possibly non-generalizable to the less motivated general dialysis population. Given the low adherence rates of dialysis patients to phosphate-binding therapies commonly seen in daily clinical practice [34, 35], we suspect that the widespread administration of intradialytic meals would make phosphate control even more difficult. (iii) Most importantly, a careful overview of the baseline characteristics of patients participating in the FrEDI trial suggests that a very low percentage of study participants were truly undernourished (baseline serum albumin: 3.7 g/dL; baseline body mass index: 27.7 kg/m2) [33]. In this regard, we should also mention that several lines of evidence suggest that serum albumin level is a very poor predictor of protein-waste malnutrition among patients on dialysis [36, 37]. (iv) The increment in serum albumin the FrEDI trial was not matched by changes in BUN or pre-albumin, making the data internally inconsistent. (v) Finally, the improvement observed in serum interleukin 6 concentration appear to recapitulate the phenomenon of regression to the mean. The intervention group had a baseline interleukin 6 concentration that was higher, and it came down over time. On the other hand, the control group had a lower concentration, and it increased over time. In the absence of solid evidence from randomized trials to prove that in-center nutritional supplementation improves clinical outcomes and mortality, we would avoid intradialytic feeding of patients who are not undernourished [36] and who could cover their caloric requirements from meals provided during the out-of-dialysis period. CONCLUSION In conclusion, ESRD patients on chronic dialysis should not be allowed to eat during the dialysis treatment for the following reasons: (i) a solid body of evidence from interventional studies show that oral food intake during dialysis induces a clinically significant postprandial reduction in BP levels and exacerbates the risk of symptomatic intradialytic hypotension. (ii) The hemodynamic alterations in response to meal ingestion (i.e. decrease in resistance of peripheral vascular beds) and the consequent redistribution of blood volume towards the splanchnic circulation interferes with the adequacy of the delivered dialysis, according to the results of relevant interventional studies comparing the efficiency of dialysis treatments performed with versus without intradialytic food consumption. (iii) The evidence that intradialytic food consumption improves nutritional status was not adequately balanced against the risk of intradialytic hemodynamic instability and less efficient dialysis. In addition, evidence from randomized trials to prove that in-center nutritional supplementation improves mortality or clinical outcomes is currently missing. In this context, we suggest that instead of feeding obese dialysis patients within the dialysis treatment, practices and policies should focus on the encouragement of adequate food and caloric intake during the out-of-dialysis period. FUNDING R.A. is supported by NIH 1 R01 HL126903-02 and a grant from VA Merit Review 5I01CX000829-04. CONFLICT OF INTEREST STATEMENT None declared. REFERENCES 1 Franch H. Peanuts or pretzels? Changing attitudes about eating on hemodialysis . Clin J Am Soc Nephrol 2016 ; 11 : 747 – 749 Google Scholar CrossRef Search ADS PubMed 2 Kistler BM , Fitschen PJ , Ikizler TA et al. . Rethinking the restriction on nutrition during hemodialysis treatment . J Ren Nutr 2015 ; 25 : 81 – 87 Google Scholar CrossRef Search ADS PubMed 3 Kalantar-Zadeh K , Ikizler TA. Let them eat during dialysis: an overlooked opportunity to improve outcomes in maintenance hemodialysis patients . J Ren Nutr 2013 ; 23 : 157 – 163 Google Scholar CrossRef Search ADS PubMed 4 Kalantar-Zadeh K , Tortorici AR , Chen JL et al. . Dietary restrictions in dialysis patients: is there anything left to eat? Semin Dial 2015 ; 28 : 159 – 168 Google Scholar CrossRef Search ADS PubMed 5 Benner D , Burgess M , Stasios M et al. . In-center nutrition practices of clinics within a large hemodialysis provider in the United States . Clin J Am Soc Nephrol 2016 ; 11 : 770 – 775 Google Scholar CrossRef Search ADS PubMed 6 Caglar K , Fedje L , Dimmitt R et al. . Therapeutic effects of oral nutritional supplementation during hemodialysis . Kidney Int 2002 ; 62 : 1054 – 1059 Google Scholar CrossRef Search ADS PubMed 7 Kalantar-Zadeh K , Braglia A , Chow J et al. . An anti-inflammatory and antioxidant nutritional supplement for hypoalbuminemic hemodialysis patients: a pilot/feasibility study . J Ren Nutr 2005 ; 15 : 318 – 331 Google Scholar CrossRef Search ADS PubMed 8 Pupim LB , Majchrzak KM , Flakoll PJ et al. . Intradialytic oral nutrition improves protein homeostasis in chronic hemodialysis patients with deranged nutritional status . J Am Soc Nephrol 2006 ; 17 : 3149 – 3157 Google Scholar CrossRef Search ADS PubMed 9 Scott MK , Shah NA , Vilay AM et al. . Effects of peridialytic oral supplements on nutritional status and quality of life in chronic hemodialysis patients . J Ren Nutr 2009 ; 19 : 145 – 152 Google Scholar CrossRef Search ADS PubMed 10 Lacson E Jr , Wang W , Zebrowski B et al. . Outcomes associated with intradialytic oral nutritional supplements in patients undergoing maintenance hemodialysis: a quality improvement report . Am J Kidney Dis 2012 ; 60 : 591 – 600 Google Scholar CrossRef Search ADS PubMed 11 Weiner DE , Tighiouart H , Ladik V et al. . Oral intradialytic nutritional supplement use and mortality in hemodialysis patients . Am J Kidney Dis 2014 ; 63 : 276 – 285 Google Scholar CrossRef Search ADS PubMed 12 Barakat MM , Nawab ZM , Yu AW et al. . Hemodynamic effects of intradialytic food ingestion and the effects of caffeine . J Am Soc Nephrol 1993 ; 3 : 1813 – 1818 Google Scholar PubMed 13 Sherman RA , Torres F , Cody RP. Postprandial blood pressure changes during hemodialysis . Am J Kidney Dis 1988 ; 12 : 37 – 39 Google Scholar CrossRef Search ADS PubMed 14 Zoccali C , Mallamaci F , Ciccarelli M et al. . Postprandial alterations in arterial pressure control during hemodialysis in uremic patients . Clin Nephrol 1989 ; 31 : 323 – 326 Google Scholar PubMed 15 Muller-Deile J , Lichtinghagen R , Haller H et al. . Online Kt/V monitoring in haemodialysis by UV absorbance: variations during intra-dialytic meals . Blood Purif 2014 ; 37 : 113 – 118 Google Scholar CrossRef Search ADS PubMed 16 San Juan MM , Pilar SM , Santos de Pablos MR. Reduction of Kt/V by food intake during haemodialysis . EDTNA ERCA J 2001 ; 27 : 150 – 152 Google Scholar CrossRef Search ADS PubMed 17 Borzou SR , Mahdipour F , Oshvandi K et al. . Effect of mealtime during hemodialysis on patients' complications . J Caring Sci 2016 ; 5 : 277 – 286 Google Scholar CrossRef Search ADS PubMed 18 Kooman J , Basci A , Pizzarelli F et al. . EBPG guideline on haemodynamic instability . Nephrol Dial Transplant 2007 ; 22 (Suppl 2) : ii22 – ii44 Google Scholar PubMed 19 Agarwal R. How can we prevent intradialytic hypotension? Curr Opin Nephrol Hypertens 2012 ; 21 : 593 – 599 Google Scholar CrossRef Search ADS PubMed 20 Assimon MM , Flythe JE. Intradialytic blood pressure abnormalities: the highs, the lows and all that lies between . Am J Nephrol 2015 ; 42 : 337 – 350 Google Scholar CrossRef Search ADS PubMed 21 Chang TI , Paik J , Greene T et al. . Intradialytic hypotension and vascular access thrombosis . J Am Soc Nephrol 2011 ; 22 : 1526 – 1533 Google Scholar CrossRef Search ADS PubMed 22 Flythe JE , Inrig JK , Shafi T et al. . Association of intradialytic blood pressure variability with increased all-cause and cardiovascular mortality in patients treated with long-term hemodialysis . Am J Kidney Dis 2013 ; 61 : 966 – 974 Google Scholar CrossRef Search ADS PubMed 23 Stefansson BV , Brunelli SM , Cabrera C et al. . Intradialytic hypotension and risk of cardiovascular disease . Clin J Am Soc Nephrol 2014 ; 9 : 2124 – 2132 Google Scholar CrossRef Search ADS PubMed 24 Lertdumrongluk P , Streja E , Rhee CM et al. . Changes in pulse pressure during hemodialysis treatment and survival in maintenance dialysis patients . Clin J Am Soc Nephrol 2015 ; 10 : 1179 – 1191 Google Scholar CrossRef Search ADS PubMed 25 Park J , Rhee CM , Sim JJ et al. . A comparative effectiveness research study of the change in blood pressure during hemodialysis treatment and survival . Kidney Int 2013 ; 84 : 795 – 802 Google Scholar CrossRef Search ADS PubMed 26 Shoji T , Tsubakihara Y , Fujii M et al. . Hemodialysis-associated hypotension as an independent risk factor for two-year mortality in hemodialysis patients . Kidney Int 2004 ; 66 : 1212 – 1220 Google Scholar CrossRef Search ADS PubMed 27 Shibagaki Y , Takaichi K. Significant reduction of the large-vessel blood volume by food intake during hemodialysis . Clin Nephrol 1998 ; 49 : 49 – 54 Google Scholar PubMed 28 Sivalingam M , Banerjee A , Nevett G. Haemodynamic effects of food intake during haemodialysis . Blood Purif 2008 ; 26 : 157 – 162 Google Scholar CrossRef Search ADS PubMed 29 Strong J , Burgett M , Buss ML et al. . Effects of calorie and fluid intake on adverse events during hemodialysis . J Ren Nutr 2001 ; 11 : 97 – 100 Google Scholar CrossRef Search ADS PubMed 30 Benaroia M , Iliescu EA. Oral intake during hemodialysis: is there an association with intradialytic hypotension? Hemodial Int 2008 ; 12 : 62 – 65 Google Scholar CrossRef Search ADS PubMed 31 Singri N , Johnstone D , Paparello J et al. . Effect of predialysis eating on measurement of urea reduction ratio and Kt/V . Adv Chronic Kidney Dis 2004 ; 11 : 398 – 403 Google Scholar CrossRef Search ADS PubMed 32 Kara B , Acikel CH. The effect of intradialytic food intake on the urea reduction ratio and single-pool Kt/V values in patients followed-up at a hemodialysis center . Turk J Med Sci 2010 ; 40 : 91 – 97 33 Rhee CM , You AS , Parsons TK et al. . Effect of high-protein meals during hemodialysis combined with lanthanum carbonate in hypoalbuminemic dialysis patients: findings from the FrEDI randomized controlled trial . Nephrol Dial Transplant 2017 ; 32 : 1233 – 1243 Google Scholar CrossRef Search ADS PubMed 34 Sherman RA. Hyperphosphatemia in dialysis patients: beyond nonadherence to diet and binders . Am J Kidney Dis 2016 ; 67 : 182 – 186 Google Scholar CrossRef Search ADS PubMed 35 Van Camp YP , Vrijens B , Abraham I et al. . Adherence to phosphate binders in hemodialysis patients: prevalence and determinants . J Nephrol 2014 ; 27 : 673 – 679 Google Scholar CrossRef Search ADS PubMed 36 Friedman AN , Fadem SZ. Reassessment of albumin as a nutritional marker in kidney disease . J Am Soc Nephrol 2010 ; 21 : 223 – 230 Google Scholar CrossRef Search ADS PubMed 37 Gama-Axelsson T , Heimburger O , Stenvinkel P et al. . Serum albumin as predictor of nutritional status in patients with ESRD . Clin J Am Soc Nephrol 2012 ; 7 : 1446 – 1453 Google Scholar CrossRef Search ADS PubMed Published by Oxford University Press on behalf of ERA-EDTA 2017. This work is written by US Government employees and is in the public domain in the US. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Nephrology Dialysis Transplantation Oxford University Press

Feeding during dialysis—risks and uncertainties

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Abstract

ABSTRACT Allowing dialysis patients to eat during the treatment is controversial. It is, therefore, no surprise that practices and policies with respect to intradialytic food consumption vary considerably from unit to unit and from country to country. Those who defend the position of feeding during dialysis reason that intradialytic meals offer a supervised and effective therapy for protein-energy wasting. Those who take the opposite view argue that intradialytic food intake should be avoided for the following three reasons. First, interventional studies show that eating during dialysis causes a clinically significant reduction in systemic blood pressure during the postprandial period and elevates the risk of symptomatic intradialytic hypotension; the latter is associated with increased mortality risk. Second, clinical studies have shown that eating during dialysis interferes with the adequacy of the delivered dialysis, whereas eating 2–3 h before the dialysis session has no impact on the efficiency of the subsequent dialysis treatment. And third, randomized studies show that eating during dialysis focus on the positive outcomes but do not adequately balance this potential benefit against the risk of intradialytic hemodynamic instability and poor quality of delivered dialysis. Even after half a century of providing long-term dialysis, definitive randomized trials that balance risks and benefits of eating during dialysis are missing. These knowledge gaps require randomized trials. Since there is a real possibility of harm with eating during dialysis, we caution that instead of encouraging the widespread use of intradialytic meals, practices and policies should focus on adequate nutrient intake during the interdialytic interval. blood pressure, dialysis adequacy, intradialytic hypotension, intradialytic meals INTRODUCTION Whether end-stage renal disease (ESRD) patients on chronic dialysis should be allowed to eat during the treatment or not remains a rather controversial issue [1, 2]. It is, therefore, not surprising that practices and policies on eating during dialysis differ from unit to unit and country to country. For example, dialysis units in North America, and particularly in the USA, are less likely than European and Asian units to permit eating during dialysis [3, 4]. In a recent survey of clinic practices and clinician opinions related to intradialytic feeding within a large dialysis care provider in the USA, it was shown that 28.6 and 22.6% of dialysis units restricted eating during treatment in 2011 and 2014, respectively [5]. This shift towards less restrictive in-center positions on eating during dialysis could be partially explained within the context of studies supporting the notion that oral food intake or intradialytic nutritional supplementation may improve protein-energy wasting [6–8] and health-related quality of life [9], and that these effects are possibly translated into a net clinical benefit [10, 11]. It has to be noted, however, that the abovementioned effect on nutritional status, if any, is counteracted by an unrecognized risk. Intradialytic feeding may unfavorably influence the postprandial blood pressure (BP) response and induce intradialytic hemodynamic instability. In this review, we discuss observational and interventional studies which show that eating during dialysis is accompanied by a more rapid postprandial reduction in BP as well as increased incidence of symptomatic hypotension and other adverse intradialytic symptoms [12–14]. We also discuss studies that provide evidence of alterations in systemic circulation in response to intradialytic food consumption that interfere with the adequacy of the delivered dialysis [15, 16]. The argument that these observations were evident predominantly in earlier studies conducted in patients receiving renal replacement therapy with acetate dialysate solutions and before the widespread use of more biocompatible membranes, volumetric ultrafiltration and low-temperature dialysis is opposed by the results of recent studies confirming the adverse hemodynamic effect of eating during dialysis even in the era of dialysis procedure optimization [17]. In this context, the 2007 European Best Practice Guidelines on intradialytic hemodynamic stability recommended the avoidance of food consumption during dialysis as a measure to prevent the occurrence of adverse intradialytic events, particularly in patients susceptible to intradialytic hypotension [18]. In this review, we discuss the existing evidence regarding eating during dialysis. We conclude that the scientific basis of the use of intradialytic meals or nutritional supplements as a tool to increase the caloric intake and improve nutritional status is weak and clearly counteracted by increased risk for intradialytic hemodynamic instability and reduced dialysis adequacy. INTRADIALYTIC HEMODYNAMIC STABILITY Intradialytic hypotension is the most commonly occurring dialysis-related complication, affecting approximately 20–30% of all dialysis treatments [19]. Apart from impairing patients' overall sense of well-being, the abrupt tissue hypoxia and hypoperfusion resulting from intradialytic hypotension is an important cause of morbidity among dialysis patients [19]. Prospective observational studies have associated intradialytic hypotension with a variety of clinical events such as excess risk of cardiac arrhythmias, myocardial and cerebral ischemia, vascular access thrombosis and more rapid deterioration of residual renal function [20–23]. Importantly, either symptomatic hypotension or large asymptomatic reductions in BP from pre- to post-dialysis are both strong and independent predictors of cardiovascular and all-cause mortality [24–26]. Among several other mechanistic pathways involved in the pathogenesis of intradialytic hypotension, observational and interventional studies suggest that oral food intake during dialysis exacerbates the incidence of this serious and potentially life-threatening dialysis-related complication. These studies are summarized in (Table 1) and discussed in detail below. Table 1 Interventional studies evaluating the effect of eating during dialysis on intradialytic hemodynamic stability Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min DialNa, dialysate sodium; IDH, intradialytic hypotension; N/A, not available. Table 1 Interventional studies evaluating the effect of eating during dialysis on intradialytic hemodynamic stability Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of food digestion Postprandial BP response Incidence of IDH References Stable, nondiabetic dialysis patients 1988 9 51 Bicarbonate/acetrate White bread, turkey, mayonnaise, pound cake, cranberry juice 2 h on dialysis ↓ ↑ Sherman et al. [13] DialNa: 138–140 mEq Blood flow: 250–400 mL/min Stable dialysis patients without history of heart failure 1989 13 52 Acetrate White bread, sirloin steak (100 g), water/fruit juice 1 h on dialysis ↓ ↑ Zoccali et al. [14] DialNa: 138 mEq Blood flow: 250–400 mL/min Stable dialysis patients non-prone to IDH 1993 10 58 Bicarbonate Toast, two boiled eggs, marmalade, butter and fruit juice 1 h on dialysis ↓ ↑ Barakat et al. [12] DialNa: 135 mEq Blood flow: 250–350mL/min Stable dialysis patients 1998 21 55 Bicarbonate/acetrate Standard meal (450–600 kcal) 1 h on dialysis ↓ N/A Shibagaki and Takaichi [27] DialNa: 140 mEq Stable nondiabetic dialysis patients 2008 20 65.6 Bicarbonate Chicken sandwich, two digestive biscuits and 150 mL of lemonade 45 min on dialysis ↓ N/A Sivalingam et al. [28] Blood flow: 200–500 mL/min Dialysate flow: 800 mL/min Temperature 36°C Stable dialysis patients 2016 48 N/A Bicarbonate Standard meal (350 kcal) 1 h versus 2 h on dialysis ↓ N/A Borzou et al. [17] Blood flow: 250–350 mL/min DialNa, dialysate sodium; IDH, intradialytic hypotension; N/A, not available. Observational studies In a cross-sectional study, Strong et al. [29] evaluated the association between food and fluid intake during dialysis with the occurrence of symptomatic intradialytic hypotension requiring interventions in 23 randomly selected patients over 166 dialysis treatments. Intradialytic food consumption (i.e. >200 calories/session) was associated with 2-fold higher incidence of hypotension (P = 0.003); the likelihood of hypotension was three times higher if patients reported the consumption of any fluid during dialysis (P = 0.011). In addition, the use of mannitol as a therapeutic intervention to control symptomatic hypotension was also significantly higher when patients consumed meals or fluids during the intradialytic period [29]. The association of oral food intake with intradialytic hemodynamic instability was not confirmed in a subsequent retrospective analysis of 126 stable dialysis patients studied over three consecutive dialysis treatments [30]. However, the absence of association could be attributable to the fact that the incidence of symptomatic intradialytic hypotension was not directly assessed in this analysis, possibly due to the retrospective study design; in contrast, intradialytic hypotension was defined as the occurrence of systolic BP <100 mmHg at any time-point of the dialysis sessions under study [30]. Since the observational evidence cannot prove causality, we subsequently discuss the evidence from interventional studies in order to clarify the association of food intake with intradialytic hemodynamic instability. Interventional studies In the first study to investigate the effect of food intake on intradialytic BP response, Sherman et al. [13] enrolled nine nondiabetic dialysis patients who had no evidence of autonomic neuropathy or orthostatic hypotension. A standard meal was administered 1.5 h after the initiation of dialysis in 62 out of 125 dialysis treatments in a prospective, non-randomized study design. Compared with control dialysis, administration of intradialytic meals was associated with a more rapid postprandial reduction in mean arterial pressure (MAP) (−14.4 mmHg/h versus −2.2 mmHg/h; P = 0.03) and in diastolic BP (−9.9 mmHg/h versus −2.8 mmHg/h; P = 0.01) [13]. Symptomatic hypotension occurred more frequently during the postprandial intradialytic periods than during the corresponding fasting periods (13 versus 2 episodes; P < 0.05) [13]. In a randomized crossover study, Zoccali et al. [14] compared the postprandial BP alterations induced by a standard snack (≈450 kcal energy) given 1 h after the initiation of dialysis with the BP changes occurring during the corresponding fasting period in 13 stable dialysis patients. Although BP was reduced during both snack-dialysis and control-dialysis, oral food intake was associated with a higher rate of postprandial BP reduction (−0.29 versus −0.08 mmHg/min; P < 0.001 for systolic BP and −0.15 versus −0.03 mmHg/min; P < 0.001 for diastolic BP) [14]. Once again, the incidence of symptomatic intradialytic hypotension requiring saline infusion was significantly higher during the snack-dialysis than during the control-dialysis (23 events in 10 patients versus 12 events in 6 patients; P = 0.025) [14]. In a subsequent double-blind, randomized, cross-over study [12] 10 dialysis patients were studied on three different occasions (placebo/no meal versus placebo/meal versus caffeine/meal). The ultrafiltration rate in the first 2 h of dialysis was maximized to accentuate hemodynamic stress. Compared with control dialysis, the rate and the magnitude of reduction in MAP were significantly higher during the placebo/meal and caffeine/meal dialysis. This postprandial reduction in MAP was shown to be mediated through a parallel decrease in systematic vascular resistance; notably, there was no compensatory increase in cardiac output. The administration of caffeine was unable to mitigate the impact of intradialytic meal ingestion on MAP levels [12]. The mechanistic background of the hemodynamic response to intradialytic food consumption was explored in two subsequent studies investigating potential alterations in intravascular volume with the use of relative blood volume (RBV) monitoring during dialysis. In the first, Shibagaki et al. [27] showed a significant increase in RBV between the pre-prandial and postprandial periods (3.24 ± 0.57 versus 13.99 ± 0.91%/h) in 16 dialysis patients who digested a standard meal in the supine position. The rate of change in RBV was modified simultaneously with meal ingestion and this effect disappeared within 43 ± 3 min after food ingestion. Postprandial alteration in RBV was more prominent when the meal was digested in the sitting position (ΔRBV: 28.21 ± 2.14%/h) and was accompanied by a parallel reduction in BP levels (152/85 versus 143/79 mmHg from pre- to postprandial periods) [27]. In the second study, Sivalingam et al. [28] evaluated the hemodynamic effect of intradialytic food intake in 20 nondiabetic dialysis patients. A standard meal was administered 45 min after the initiation of dialysis and several hemodynamic parameters (i.e. BP, cardiac output, peripheral vascular resistance and RBV) were continuously monitored over a regular mid-week dialysis session. In line with the results of the aforementioned study of Shibagaki et al. [27] a significant increase in the rate of reduction in RBV was noted between the pre- and postprandial periods (0.08 ± 0.07 versus 0.24 ± 0.10%/min; P < 0.005). The maximal reduction in RBV occurred at a mean time of 16 min (range: 8–26 min) and the effect disappeared at a mean time of 30 min (range: 10–40 min) after food ingestion. A parallel reduction in MAP levels was noted between the start and 30 min after meal ingestion (P = 0.04) [28]. In contrast, intradialytic food intake had no impact on cardiac output, peripheral vascular resistance and heart rate. These findings directly support the notion that redistribution in blood volume between the systemic and splanchnic circulations is involved in the causal pathway of the BP-lowering effect of food consumption during dialysis. To investigate the potential effect of timing of food intake on the intradialytic hemodynamic response, Borzou et al. [17] evaluated 48 dialysis patients in two dialysis sessions. In the first session, patients were given a standard meal 1 h after the initiation of dialysis and in the second session, the same meal was given 2 h after the initiation of dialysis. Significant reductions in BP levels were noted between the pre-meal and post-meal periods in both dialysis sessions under study (first session: −7.7/−4.4 mmHg; P < 0.001; second session: −4.6/–3.0 mmHg; P < 0.001, respectively) [17]. However, the magnitude of BP reduction during the postprandial period was unaffected by the timing of meal intake. Similarly, changes in the timing of meal intake during the dialysis session did not modify the intensity of nausea, vomiting or other adverse intradialytic symptoms [17]. Ingestion of a large amount of food during dialysis may lead to errors in the estimation of ultrafiltration volume when calculated by the difference in weight from pre-dialysis to post-dialysis. Accordingly, in some dialysis units, the quantity of fluid ingested during dialysis is added to the ultrafiltration goal for the day. This may further exacerbate the risk for intradialytic hypotension. Such a practice is also without an evidence base. DIALYSIS ADEQUACY The hemodynamic alterations evoked by intradialytic meal intake (i.e. postprandial reduction in BP and peripheral vascular resistance) and redistribution of circulating blood volume due to excessive blood pooling in the splanchnic circulation are proposed as the mechanistic substrate for a negative impact of intradialytic food intake on the adequacy of delivered dialysis [2]. This notion is supported by a number of interventional studies summarized (Table 2) and discussed in detail below. Table 2 Interventional studies evaluating of intradialytic food consumption on dialysis adequacy Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min DialNa, dialysate sodium; N/A, not available. aOnline monitored Kt/V during the dialysis session. Table 2 Interventional studies evaluating of intradialytic food consumption on dialysis adequacy Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min Patient characteristics Year n Age (years) Dialysis parameters Meal Timing of meal digestion Change in URR Change in Kt/V References Stable dialysis patients 2001 14 60.0 Bicarbonate Free oral intake N/A ↓ ↓ San Juan et al. [16] Blood flow: 350–400 mL/min Dialysate flow: 500 mL/min Stable dialysis patients 2004 42 55.4 Bicarbonate Variable meals containing 0.4 g/kg protein 2 h before dialysis Unchanged Unchanged Singri et al. [31] Dialyzer: high-flux Stable nondiabetic dialysis patients without evidence of autonomic neuropathy 2010 25 56.5 Bicarbonate White bread, white cheese, tea 1 h on dialysis ↓ ↓ Kara and Acikel [32] DialNa: 140 mEq Blood flow: 200–450 mL/min Dialysate flow: 500 mL/min Temperature: 36°C Stable dialysis patients without overt cardiovascular disease 2014 40 71.0 Bicarbonate 2–3 slices white bread, cheese/marmalade, beverage 2 h on dialysis N/A ↓a Muller-Deile et al. [15] Blood flow: 300 mL/min Dialysate flow: 500 mL/min DialNa, dialysate sodium; N/A, not available. aOnline monitored Kt/V during the dialysis session. In a prospective controlled study, 14 dialysis patients were evaluated during two mid-week dialysis sessions with a 1-week interval between them. In the first session, patients were allowed to eat during dialysis and in the second session, intradialytic meal consumption was prohibited [16]. Dialysis adequacy assessed in terms of urea reduction ratio (URR) and Kt/V measured by the Daugirdas formula was significantly lower in the dialysis session with meal as compared with control dialysis session (URR: 71.5 ± 5.9 versus 73.5 ± 6.6; P < 0.05; Kt/V: 1.54 versus 1.65, P < 0.05) [16]. This reduction in URR and Kt/V in response to intradialytic food intake was confirmed in a subsequent study of 25 stable dialysis patients. Each patient was evaluated during two regular mid-week dialysis sessions performed at identical ultrafiltration rates (meal-dialysis versus control-dialysis) over two consecutive weeks [32]. The URR and Kt/V were significantly lower during the dialysis session with food intake than during the session without food intake (URR: 67.8 ± 6.1 versus 72.1 ± 6.0%; P < 0.001; Kt/V: 1.4 ± 0.2 versus 1.6 ± 0.2; P < 0.001) [32]. The effect of intradialytic food intake on dialysis adequacy was evaluated in 40 dialysis patients who underwent continuous online Kt/V monitoring during a regular mid-week dialysis session with the use of UV absorbance system [15]. A standard meal was given around 2 h after the initiation of dialysis to investigate whether meal-related hemodynamic alterations and/or redistribution in circulating blood volume may influence the slope of Kt/V curves. This study showed that intradialytic meal consumption had a direct impact on online Kt/V as measured by the UV absorbance system. While the mean Kt/V change over time was 0.33 ± 0.02/h before food intake, it dropped within minutes after meal ingestion to −0.01 ± 0.04/h. Intradialytic meal intake was responsible for a relative decrease of 101.5 ± 50.4% in continuously monitored Kt/V (P < 0.001). Shortly after the end of the meal, the rate of change in Kt/V increased and progressively reached the pre-meal levels (0.32 ± 0.01/h) [15]. This meal-related effect on dialysis adequacy was not reproducible when Kt/V was monitored using an ionic dialysance-based system. The explanation provided by the authors for the discrepancy between the two methods was that short-term postprandial variations in online Kt/V measured by UV absorbance may not reflect a true decrease in Kt/V, but these meal-related changes could be attributed to an intermittent increase in UV-absorbing dialyzed solutes [15]. In contrast, oral food intake some hours before the initiation of the treatment is less likely to affect the adequacy of the subsequently delivered dialysis. This hypothesis was tested in a study comparing the efficiency of a single dialysis session undertaken after a 3-h fasting with that of a meal 2 h before the initiation of dialysis in 42 stable dialysis patients [31]. This study showed that the levels of URR and Kt/V were identical regardless of the presence or absence of a meal ingested before the start of dialysis (URR: 72.4 ± 5.2 versus 72.8 ± 4.7%; P = 0.35; Kt/V: 1.56 ± 0.2 versus 1.58 ± 0.2; P = 0.42 for fed versus fasting dialysis, respectively) [32]. This effect was shown to be consistent in subgroup analyses performed according the gender and diabetic status of study participants [31]. These data suggest that instead of imposing the risk of a less efficient dialysis by allowing intradialytic food intake, we could cover their caloric requirements by encouraging the patients to eat 2–3 h before their dialysis treatment. An argument can be made that reduction in Kt/V with eating during dialysis is simply an artefact of measurement. If protein-induced increase in urea generation leads to an appearance of a reduced dialysis efficiency then this would not truly be a reduction in the efficiency of dialysis. However, the data of Muller-Deile et al. [15], where dialysis efficiency fell within minutes of food intake, suggest that hemodynamic mechanisms may be operative. Nonetheless, better quality data are needed to confirm or refute whether dialysis efficiency is truly reduced by eating during dialysis. NUTRITIONAL STATUS One may argue that dialysis patients should be allowed to eat during the treatment since intradialytic meals may benefit protein-energy wasting and nutritional status [3, 4]. This position is based mainly on the results of small interventional studies showing that oral nutritional supplementation during dialysis (and not administration of intradialytic meals) increases the caloric intake during the dialysis-on day and improves some markers reflecting malnutrition (a slight elevation in serum albumin levels) [6–9]. In addition, those opposing the restrictive in-center nutritional policies base their opinion on the results of a few observational studies associating intradialytic nutritional supplementation with reduced mortality risk [10, 11], arguing that restriction of intradialytic food consumption is a ‘lost opportunity’ to improve the clinical outcomes in the high-risk dialysis population. In 2016, Rhee et al. published the results of the Fosrenol (lanthanum carbonate) for Enhancing Dietary Protein Intake in Hypoalbuminemic Dialysis Patients (FrEDI) trial [33]. In this trial, 110 dialysis patients with serum albumin <4 g/dL were randomly assigned to receive high-protein (50–55 g) meals during dialysis combined with lanthanum carbonate or low-protein (<1 g) meals during dialysis for 8 weeks. Background therapy with non-lanthanum-based phosphate-binders remained constant throughout the course of the trial. This trial showed that administration of high-protein meals during dialysis improved the composite primary trial endpoint of a rise in serum albumin of ≥0.2 g/dL while maintaining phosphorus between 3.5 up to <5.5 mg/dL; 27 patients in the high-protein arm versus 12 patients in the low-protein arm reached the primary outcome (P = 0.045) [33]. The authors concluded that among hypoalbuminemic dialysis patients, intradialytic intake of high-protein meals in conjunction with lanthanum carbonate corrects serum albumin without aggravating the risk of hyperphosphatemia. Despite the theoretically positive results of the FrEDI trial [33], our position that dialysis patients should not be allowed to eat during the intradialytic period still relies on a strong scientific basis for several reasons: (i) the FrEDI trial did not assess the impact of intradialytic food intake on intradialytic hemodynamic stability and dialysis adequacy; these outcomes were not assessed even as secondary safety endpoints [33]. Accordingly, the FrEDI trial cannot answer the question of whether the slight benefit on serum albumin levels is counteracted by excess risk of intradialytic hypotension (symptomatic or asymptomatic) or less efficient dialysis. (ii) The prevention of the risk of hyperphosphatemia achieved through the supervised administration of phosphate binders during the intradialytic meal within the course of a randomized trial is possibly non-generalizable to the less motivated general dialysis population. Given the low adherence rates of dialysis patients to phosphate-binding therapies commonly seen in daily clinical practice [34, 35], we suspect that the widespread administration of intradialytic meals would make phosphate control even more difficult. (iii) Most importantly, a careful overview of the baseline characteristics of patients participating in the FrEDI trial suggests that a very low percentage of study participants were truly undernourished (baseline serum albumin: 3.7 g/dL; baseline body mass index: 27.7 kg/m2) [33]. In this regard, we should also mention that several lines of evidence suggest that serum albumin level is a very poor predictor of protein-waste malnutrition among patients on dialysis [36, 37]. (iv) The increment in serum albumin the FrEDI trial was not matched by changes in BUN or pre-albumin, making the data internally inconsistent. (v) Finally, the improvement observed in serum interleukin 6 concentration appear to recapitulate the phenomenon of regression to the mean. The intervention group had a baseline interleukin 6 concentration that was higher, and it came down over time. On the other hand, the control group had a lower concentration, and it increased over time. In the absence of solid evidence from randomized trials to prove that in-center nutritional supplementation improves clinical outcomes and mortality, we would avoid intradialytic feeding of patients who are not undernourished [36] and who could cover their caloric requirements from meals provided during the out-of-dialysis period. CONCLUSION In conclusion, ESRD patients on chronic dialysis should not be allowed to eat during the dialysis treatment for the following reasons: (i) a solid body of evidence from interventional studies show that oral food intake during dialysis induces a clinically significant postprandial reduction in BP levels and exacerbates the risk of symptomatic intradialytic hypotension. (ii) The hemodynamic alterations in response to meal ingestion (i.e. decrease in resistance of peripheral vascular beds) and the consequent redistribution of blood volume towards the splanchnic circulation interferes with the adequacy of the delivered dialysis, according to the results of relevant interventional studies comparing the efficiency of dialysis treatments performed with versus without intradialytic food consumption. (iii) The evidence that intradialytic food consumption improves nutritional status was not adequately balanced against the risk of intradialytic hemodynamic instability and less efficient dialysis. In addition, evidence from randomized trials to prove that in-center nutritional supplementation improves mortality or clinical outcomes is currently missing. In this context, we suggest that instead of feeding obese dialysis patients within the dialysis treatment, practices and policies should focus on the encouragement of adequate food and caloric intake during the out-of-dialysis period. FUNDING R.A. is supported by NIH 1 R01 HL126903-02 and a grant from VA Merit Review 5I01CX000829-04. CONFLICT OF INTEREST STATEMENT None declared. REFERENCES 1 Franch H. Peanuts or pretzels? Changing attitudes about eating on hemodialysis . Clin J Am Soc Nephrol 2016 ; 11 : 747 – 749 Google Scholar CrossRef Search ADS PubMed 2 Kistler BM , Fitschen PJ , Ikizler TA et al. . 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J Am Soc Nephrol 2010 ; 21 : 223 – 230 Google Scholar CrossRef Search ADS PubMed 37 Gama-Axelsson T , Heimburger O , Stenvinkel P et al. . Serum albumin as predictor of nutritional status in patients with ESRD . Clin J Am Soc Nephrol 2012 ; 7 : 1446 – 1453 Google Scholar CrossRef Search ADS PubMed Published by Oxford University Press on behalf of ERA-EDTA 2017. This work is written by US Government employees and is in the public domain in the US.

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Nephrology Dialysis TransplantationOxford University Press

Published: Jun 19, 2017

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