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VIEWS, VISIONS AND VISTAS IN DIALYSIS

Dietary Restrictions in Dialysis Patients: Is There Anything Left


to Eat?
Kamyar Kalantar-Zadeh,*†‡†† Amanda R. Tortorici,*† Joline L. T. Chen,*† Mohammad
Kamgar,§ Wei-Ling Lau,* Hamid Moradi,*† Connie M. Rhee,* Elani Streja,*† and
Csaba P. Kovesdy¶**
*Division of Nephrology and Hypertension, Harold Simmons Center for Kidney Disease Research and
Epidemiology, University of California Irvine, Orange, California, †Long Beach Veterans Affairs Healthcare
System, Long Beach, California, ‡Department of Epidemiology, UCLA Fielding School of Public Health,
University of California Los Angeles, Los Angeles, California, §Long Beach Memorial Medical Center, Long
Beach, California, ¶Renal Division, University of Tennessee Health Science Center, Memphis, Tennessee,
**Memphis Veterans Affairs Medical Center, Memphis, Tennessee, and ††Los Angeles Biomedical Research
Institute at Harbor-UCLA, Torrance, California

ABSTRACT

A significant number of dietary restrictions are imposed related to calcium, vitamins, and trace elements are scarce
traditionally and uniformly on maintenance dialysis and often contradictory. The restriction of eating during
patients, whereas there is very little data to support their hemodialysis treatment is likely another incorrect practice
benefits. Recent studies indicate that dietary restrictions that may worsen hemodialysis induced hypoglycemia and
of phosphorus may lead to worse survival and poorer nutritional derangements. We suggest careful relaxation
nutritional status. Restricting dietary potassium may of most dietary restrictions and adoption of a more bal-
deprive dialysis patients of heart-healthy diets and lead to anced and individualized approach, thereby easing some
intake of more atherogenic diets. There is little data about of these overzealous restrictions that have not been pro-
the survival benefits of dietary sodium restriction, and ven to offer major advantages to patients and their out-
limiting fluid intake may inherently lead to lower protein comes and which may in fact worsen patients’ quality of
and calorie consumption, when in fact dialysis patients life and satisfaction. This manuscript critically reviews the
often need higher protein intake to prevent and correct current paradigms and practices of recommended dietary
protein-energy wasting. Restricting dietary carbohydrates regimens in dialysis patients including those related to die-
in diabetic dialysis patients may not be beneficial in those tary protein, carbohydrate, fat, phosphorus, potassium,
with burnt-out diabetes. Dietary fat including omega-3 sodium, and calcium, and discusses the feasibility and
fatty acids may be important caloric sources and should implications of adherence to ardent dietary restrictions
not be restricted. Data to justify other dietary restrictions and future research.

Dietary counseling and nutritional interventions requirement for an outpatient dialysis clinic to have
are quintessential components in the management an on-site registered dietitian to provide dietary
of chronic kidney disease (CKD) patients, including monitoring and counseling to all dialysis patients
those who receive maintenance dialysis therapy. To (1). Both dietitians and nephrologists often impose
that end, in the United States, it is a regulatory a number of dietary restrictions on their patients
related to dietary phosphorus, potassium, sodium,
Address correspondence to: Kamyar Kalantar-Zadeh, MD,
fluid intake, and macronutrients including carbohy-
MPH, PhD, Division of Nephrology & Hypertension, Harold drate and fat. Dietitians also emphasize the impor-
Simmons Center for Kidney Disease Research and Epide- tance of high dietary protein intake in dialysis
miology, University of California Irvine Medical Center, 101 patients, while they may also recommend weight
The City Drive South, City Tower, Suite 400 - ZOT: 4088 loss efforts in patients with morbid obesity who are
Orange, California 92868-3217, Tel.: (714) 456-5142, Fax:
(714) 456-6034, or e-mail: kkz@uci.edu. not yet eligible for kidney transplant wait list (2).
Potential Conflicts of Interest: KKZ has received honoraria Eating or not eating during hemodialysis treatment
from Abbott, Abbvie, Fresenius, Keryx, Shire, Vifor, and is another controversy; in the United States, many
other manufacturers of phosphorus binders, nutritional dialysis centers prohibit food intake during dialysis
supplements, or medications and items related to dialysis
patients.
treatment, while in other countries meals are proac-
Seminars in Dialysis—2015
tively served to dialysis patients (3).
DOI: 10.1111/sdi.12348 Many of these dietary recommendations for dial-
© 2015 Wiley Periodicals, Inc. ysis patients are highly restrictive (see Table 1), and
1
2 Kalantar-Zadeh et al.
TABLE 1. Dietary recommendations and restriction in dialysis patients and their implications.

Recommended
range Evidence Observations

Dietary protein 1.2–1.4 g/kg/day Epidemiologic studies show greatest Most dialysis patients eat <1.0 g/kg/day.
recommendations survival with 1.2–1.4 g/kg/day.
Dietary phosphorus <800 mg/day Mostly based on epidemiologic Adhering to low-phosphorus diet may result
restrictions association between serum in adequate protein intake (and even
phosphorus and mortality. higher mortality?).
Dietary potassium (K) <3 g/day Very recent data suggest an Most K-rich foods are heart-healthy.
restrictions association between Higher dietary
K load and death.
Dietary salt and fluid <2.5 g/day Salt data are mostly opinion based. Less fluid intake may be difficult to adhere
restrictions There is more recent data on adverse to if patients are to eat larger amounts of
outcomes from fluid retention. protein and calorie.
Dietary carbohydrate and Mostly for Higher A1c >9% may be associated May aggravate burnt-out diabetes leading
glycemic restrictions diabetic with higher death risk. to poor outcomes, especially if A1c<6%.
dialysis patients
Dietary lipid restrictions e.g., DASH diet Recent data show benefit of Omega-3 Dietary fat restriction may aggravate
and unsaturated fatty acids. calorie malnutrition.
Dietary vitamins and Different data Mixed data regarding vitamin D and Some old data suggest certain vitamins such
trace elements inadequate data for most others. as A should be given with restriction.
Dietary calcium restrictions <1200 mg/day Data are mostly based on association Hypocalcemia may be aggravated, especially
between serum calcium and mortality. with calcimimetics.
Eating restrictions during Meals during Anecdotal case reports regarding Hemodialysis induced hypoglycemia.
hemodialysis treatment hemodialysis aspiration during hemodialysis
while eating.

the task of finding anything permissible to eat is a needs to be supplemented by either essential amino
major challenge for dialysis patients. Indeed, many acids or their keto-analog (5,7).
of these dietary restrictions such as a low-potassium Notwithstanding the ongoing discussion on the
diet contradict the current recommendations for a safety, adequacy, and effectiveness of the LPD or
heart-healthy diet (4). It is not an exaggeration to supplemented vLPD for NDD-CKD patients, for
say that the dialysis dietary regimen is among the those who transition to dialysis treatment, the
most restrictive diets, and these restrictions may guidelines are relatively consistent in that the rec-
render many patients frustrated and lead to subopti- ommended dietary protein intake range is to be
mal adherence and compliance. In this manuscript, 1.2–1.4 g/kg/day, which is two times higher than
some of these dietary recommendations and restric- the LPD and even higher than what the general
tions are critically reviewed and their impact on population eats. This poses a major challenge for
dialysis patient outcomes and recommendations for the successful transition from NDD-CKD to dialy-
future research are discussed. sis therapy, especially as many of these patients,
who were used to LPD, need to undergo significant
reeducation and acculturation. In reality, over half
Dietary Protein Recommendations of dialysis patients have inadequate dietary protein
[<1.0 g/kg/day as measured by the normalized pro-
Nondialysis-dependent (NDD) CKD patients are tein nitrogen appearance (nPNA) also known as
generally advised to eat lower amounts of protein. normalized protein catabolic rate (nPCR)] as shown
The so-called low-protein diet (LPD) that is often in a recent study by Shinaberger et al (8) (Fig. 1).
recommended for nondiabetic, NDD-CKD Stages The estimates of nPNA or nPCR are calculated by
3b, 4, and 5 (eGFR<45 ml/minute/1.73 m2 BSA) urea kinetic modeling (8–10). As to whether such a
targets a daily dietary protein intake of ~0.6 g/kg/ high-protein intake of 1.2–1.4 g/kg/day is useful or
day, i.e., 35–45 g of total daily protein for a not, observational studies including those by Kalan-
60–70 kg person (5). The LPD is significantly lower tar-Zadeh et al. (9), Shinaberger et al. (8), and
than what the nonvegetarian general population in Ravel et al. (10), have suggested superior hospital-
the United States and most Western countries eat, ization and survival outcomes, although there has
i.e., 0.9–1.1 g/kg/day. Furthermore, the Institute of never been any controlled trial to corroborate these
Medicine “Food and Nutrition Board” recommends dietary targets. According to Shinaberger et al. (8),
a daily dietary protein intake of 0.8 g/kg/day in the the best survival in 53,933 hemodialysis patients
general population, which is 0.2 g/kg/day above the was achieved when the nPCR was in the 1.2–1.4
minimum dietary protein requirement, offering a g/kg/day range (Fig. 2).
safety cushion against protein-energy malnutrition A high-protein intake of ~1.2 g/kg/day poses
(5,6). The so-called very low-protein diet (vLDP) additional challenges including a somewhat high
consists of only 0.3 g/kg/day and is also recom- dietary phosphorus and potassium load, higher risk
mended for very late-stage NDD-CKD; it invariably of metabolic acidosis, and higher probability of
DIETARY RESTRICTIONS 3

Fig. 1. Frequency of different ranges of protein intake estimated by nPCR (nPNA) in 53,933 hemodialysis patients (adapted from ref-
erence 8).

Incident & Prevalent MHD Patients (n= 53,933)

unadjusted
3
case-mix
All Cause Death Hazard Ratio

1.5 KDOQI
Recommended
range:
1.0-1.2 g/kg/day

0.6

<0
.6 .69 .79 .89 . 99 .09 . 19 . 29 .39 1.4
-0 -0 -0 -0 -1 -1 -1 -1 >=
0.6 0.7 0.8 0.9 1.0 1.1 1.2 1.3
nPNA (nPCR) (g/kg/day)
Fig. 2. Associations between dietary protein intake, estimated by nPCR (nPNA) and survival in 53,933 hemodialysis patients (adapted
from reference 8).

increased fluid intake by virtue of the need for lar- alysis treatment is a separate topic and beyond the
ger amounts of food (Fig. 3) (11). Nevertheless, as scope of this review article (3,6).
the advantages of higher dietary protein intake may
outweigh its potential challenges in thrice-weekly
hemodialysis patients, they should be consistently Dietary Phosphorus Restrictions
reminded and educated during rounds to increase
their dietary protein intake including consumption Counseling on dietary phosphorus and monitoring
of more meat, fish, eggs, and poultry as well as patients’ phosphorus intake are perhaps the most
fruits and vegetable high in protein such as legumes time-consuming tasks of dialysis clinic dietitians in
and tofu-based foods. If such interventions are the United States and many other countries (12,13).
inadequate, then meals during dialysis should be Nevertheless, recent data examining the impact of
provided with high-protein content (3), and high- dietary phosphorus counseling efforts on dialysis
protein oral nutritional supplements should be patient outcomes have questioned the wisdom of this
offered (6). Meals and supplements during hemodi- several decade-old paradigm, supported by the
4 Kalantar-Zadeh et al.

phosphorus = 11.8*protein + 78(R2 =0.83)

2000

1800

1600

Dietary P hosphorus (mg/day)


1400

1200

1000

800

600

400

200

0
0 20 40 60 80 100 120 140
Dietary Protein Intake (g/day)

Fig. 3. Correlation between dietary protein and phosphorus content; a recommended protein intake of 1.2 g/kg/day in a 70 kg chronic
dialysis patient is equivalent to 85 g/day of protein which exceeds the 800 mg/day phosphorus restriction as shown by the black arrows
(adapted from reference 11).

notion that restricting dietary protein intake via phosphorus restriction may not be associated with
traditional approaches can invariably lead to lower improved survival among hemodialysis patients if it
dietary protein intake and hence may increase the results in inadequate protein intake, and heightened
risk of protein-energy wasting and death (14). In a dietary phosphorus restrictions may be associated
recent study by Lynch et al. (15), the impact of pre- with greater mortality, such that the risk of control-
scribed dietary phosphorus restrictions on long-term ling serum phosphorus by restricting dietary protein
survival was examined in 1751 hemodialysis patients intake may outweigh the benefits and lead to
using marginal structural models to adjust for longi- greater mortality in dialysis patients (14,15).
tudinal confounding. The study found that more It is important to note, however, that in a study
restrictive prescribed dietary phosphorus was associ- using Food Frequency Questionnaires in a cohort of
ated with poorer indices of nutritional status and that 224 hemodialysis patients over 5 years, Noori et al.
there was an incrementally greater survival with more (19) showed that higher dietary phosphorus intake
liberal dietary phosphorus prescription; in particular, and higher dietary phosphorus-to-protein (P-to-P)
those who were prescribed >1000 mg/day dietary ratios were each associated with increased death risk
phosphorus or no dietary restriction had 27% and even after adjustments for serum phosphorus, phos-
29% greater survival, respectively (15). phorus binders and their classes, dietary protein,
In another study, Shinaberger et al. (14) reported energy, and potassium intake (Fig. 4). In this study,
on 30,075 prevalent hemodialysis patients in the dietary P-to-P ratios of 14 to <16, and ≥16 mg/g were
United States; in comparison to patients whose associated with 80% and 99% higher death risk,
serum phosphorus and dietary protein intake both respectively, compared to those who ate food with a
rose over 6 months, those whose serum phosphorus P-to-P ratio of <14 mg/g (19). Hence, the choice of
decreased but whose protein intake increased had type of protein that has lower P-to-P ratio such as
10% greater survival, whereas those whose phos- egg Whites may have a bearing on survival (13).
phorus increased but whose dietary protein Do such recent provocative studies suggest that
decreased or those whose phosphorus and dietary we should abandon any type of dietary phosphorus
protein intake concomitantly decreased had 11% restriction in dialysis patients? There is little doubt
and 6% worse mortality, respectively (14). that hyperphosphatemia is associated with poorer
Both old and new data have been relatively con- outcomes in CKD (20). The aforementioned studies
sistent in showing that a low serum phosphorus offer important opportunities to rechannel dietary
level, e.g., <3.5 mg/dl, is associated with higher counseling efforts into the correct direction with
mortality independent of age (16) and other con- greater focus on understanding and identifying the
founders (17). To that end, adherence to KDIGO’s sources of added phosphorus in processed foods
guidelines of “normalization” of serum phosphorus, (21) and better appreciating that natural (organic)
which may mean targeting levels even below phosphorus is not well absorbed, e.g., approxi-
3.5 mg/dl in dialysis patients, has become a chal- mately 40–60% of phosphorus from animal protein
lenging dilemma (18). Hence, prescribed dietary and <40% of plant-based protein is usually
DIETARY RESTRICTIONS 5
Adjusted for case mix, serum potassium and intakes of energy, protein and phosphorus

2
1
0
-1

879±161 1,342±109 1,852±217 3,440±969 mmol/d*


-2

0 20 40 60 80 100
dietary potassium percentile
Fig. 4. Association of dietary phosphorus-to-protein ratio and mortality in hemodialysis patients (adapted from reference 19).

absorbed through the GI tract, whereas the added the majority of patients transitioning to ESRD, par-
or inorganic phosphorus is almost 100% absorbable ticularly in hemodialysis patients. A recent cohort
(17,21,22). Hence, the incorrect practice of frighten- study over 3 years in 81,013 prevalent hemodialysis
ing dialysis patients to avoid natural sources of pro- patients suggested that the best prehemodialysis
tein that may also have high phosphorus content serum potassium range associated with the greatest
(such as meat, poultry, fish, eggs, natural dairy survival was 4.6 to 5.3 mEq/l, whereas potassium
products, and legumes) should be discouraged. levels <4.0 or ≥5.6 mEq/l were associated with
We believe that dietitians should spend more time increased mortality (27). Another clinically relevant
and efforts on educating dialysis patients on how finding in this study was that serum potassium
to: (1) identify added phosphorus in processed correlated closely with nutritional markers, in partic-
foods to avoid them (23), (2) choose natural sources ular nPCR (nPNA) suggesting that patients who eat
of proteins with the lowest P-to-P ratio such as egg more protein also tend to have higher serum potas-
Whites (24), and (3) take phosphorus binders cor- sium level (Fig. 5) (27). In a more recent cohort study
rectly and diligently, including avoidance of con- that examined the mortality of hyperkalemia in
suming binders on an empty stomach (e.g., before 111,651 hemodialysis and 10,468 peritoneal dialysis
meals), and adjustment of binder dose based on the patients, the latter group was 3.3 times more likely to
binder potency and in particular based on the esti- have lower serum potassium <4.0 mEq/l, and their
mated amount of phosphorus in each meal (12). To death risk was 51% and 52% higher with serum
give blind phosphorus binder prescriptions to dialy- potassium levels <3.5 mEq/l and ≥5.5 mEq/l (28).
sis patients with a fixed number of pills “per meal” Hence, both hypo- and hyperkalemia appear to be
without providing first such fundamental education harmful in dialysis patients irrespective of dialysis
about types of dietary phosphorus or without edu- modality. It is important to note that the variability
cating the proper use of phosphorus binders is in serum potassium in dialysis patients is not the
indeed an incorrect approach adopted by many exclusive function of dietary potassium load and that
professional caring for dialysis patients and should several other factors such as potassium concentration
be reexamined (12). Additional studies including in the dialysate bath or the dialysis treatment length
randomized controlled trials should examine and frequency play important roles.
whether nondietary control of phosphorus or A recent study by Noori et al. (29) examined the
restriction of nonprotein sources of phosphorus is association between dietary potassium intake via
safe and more effective, keeping in mind that hyper- Food Frequency Questionnaire (30) at the start of a
phosphatemia is not merely a reflection of dietary 5-year cohort of 224 hemodialysis patients in South-
phosphorus intake but of also many other factors ern California and found that patients with higher
including hyperparathyroidism (25,26). potassium intake had greater dietary energy, protein,
and phosphorus intake, and higher predialysis serum
potassium and phosphorus levels. Greater dietary
Dietary Potassium Restrictions potassium intake was associated with increased mor-
tality in survival models that were adjusted for nutri-
Dietary potassium restrictions are often imple- tional factors including serum potassium and
mented during earlier stages of CKD when patients phosphorus levels, in that death risk of the three
are still nondialysis-dependent, and are reinforced in higher quartiles of dietary potassium intake were 1.4,
6 Kalantar-Zadeh et al.
5.3

5.1

Serum Potassium (mEq/L)


4.9

4.7

4.5

4.3

4.1

3.9

3.7

3.5
9

9
0

40
.6

.7

.8

.9

.0

.1

.2

.3
.6

1.
-0

-0

-0

-0

-1

-1

-1

-1
<0

>=
60

70

80

90

00

10

20

30
0.

0.

0.

0.

1.

1.

1.

1.
Estimated Daily Protein Intake (nPNA) g/kg/day
Fig. 5. Correlation between higher dietary protein intake and higher serum potassium level in hemodialysis patients (adapted from ref-
erence 27).

2.2, and 2.4 times higher than the lowest dietary automatically continued on the same dietary restric-
potassium quartile (29). Hence, higher dietary potas- tions as non-CKD patients with diabetes (33). Even
sium load per se, independent of serum potassium, is though high glycemic burden is associated with
incrementally associated with higher mortality. poor outcomes in the dialysis population (34–36),
These and other data have been used to justify many diabetic dialysis patients develop a so-called
strict dietary potassium restrictions in CKD and dial- “burnt-out diabetes” phenomenon, such that their
ysis patients. However, it is important to appreciate insulin and oral hypoglycemic agents can be signifi-
that many potassium rich foods are considered cantly decreased and at times need to be discontin-
“heart healthy” including fresh fruits and vegetables, ued due to risk of hypoglycemia (37–39). Indeed,
fresh squeezed juices, legumes, and grains (29). hemodialysis-induced hypoglycemia is an under-rec-
Hence, a low-potassium diet falls outside of what is ognized and widespread event that may happen
generally recommended as a healthy diet and life even more frequently in diabetic dialysis patients
style, and such dietary restrictions may contribute to (40). Recent studies suggest that the best hemoglo-
the burden of cardiovascular disease in the CKD bin A1c target range for diabetic dialysis patients is
patient population according to several studies 7–9% and that a lower A1c, especially <6%, is
(4,31). We suggest educating patients regarding the associated with poor outcomes, which may be
different sources of potassium and empowering our related to poor nutritional status or other metabolic
patients to make choices which fall within the “heart derangements of uremia (34,37,41–43). Hence, gly-
healthy” category and avoid other sources of potas- cemic restrictions that are traditionally used in non-
sium so that they obtain the most benefit from a diet CKD diabetic patients may lead to harm in diabetic
with moderate amounts of potassium. Hence in this dialysis patients. We suggest that dietary glycemic
case, a relaxation of dietary potassium restrictions restrictions in dialysis patients with A1c <7% be
and a more balanced and realistic approach to such relaxed, and that among patients with higher A1c
overzealous restrictions would mean choosing the levels, careful and balanced dietary recommenda-
most beneficial sources of potassium which is only tions be considered to assure the provision of at
possible through a concerted education effort. The least 35 cal/kg/day (6).
use of potassium binding resins for hyperkalemia
control may also allow for more consumption of
heart-healthy diets with less risk of hyperkalemia, Dietary Salt and Fluid Restriction
although their intake can be limited by side effects
and more studies are needed (32). Newer resins, in Although there are important data suggesting
development, may facilitate this approach. that high interdialytic weight gain is associated with
higher death risk (44), there are no convincing data
to suggest that more dietary sodium restriction in
Dietary Glycemic Restrictions and dialysis patients has any bearing on outcomes.
Carbohydrate Load Indeed, recent studies in the general population sug-
gest that low salt intake is associated with poorer
In the United States, almost half of all new dialy- outcomes (45). With regard to fluid restriction, a
sis patients are diabetic, and many of them are cohort study by Kalantar-Zadeh et al. in 34,107
DIETARY RESTRICTIONS 7
hemodialysis patients showed that in unadjusted tive protein fell by 1.69 mg/l and there was no sig-
survival analyses, higher weight gain reflecting nificant changes in blood lipids. These investigators
higher fluid intake was associated with better nutri- concluded that dietary unsaturated fat have favor-
tional status including higher protein intake, serum able nutritional benefits (52). The anti-inflammatory
albumin, and body mass index, and tended to be benefits of higher dietary intake of certain fats has
linked to greater survival (44). The higher fluid-gain recently been shown in a 5-year cohort of hemodial-
increments were originally associated with better ysis patients, in whom lower dietary omega-6 to
survival but after multivariate adjustment (including omega-3 ratio was associated with reduced inflam-
for nutritional status), it was associated with higher mation over time and a trend toward lower death
(not lower) death risk. This suggests that the bene- risk (53). Hence, it is possible, although not yet pro-
fit of fluid restriction is achieved only if optimal ven, that dietary fat not only provides a good
nutritional status and food intake is not compro- source of the needed calories but if properly admin-
mised (44). While we do not recommend complete istered it could also have additional benefits includ-
relaxation of fluid and salt restrictions given the ing dietary modulation of inflammation (54).
problems associated with volume overload, we warn
against overzealous salt and fluid restrictions in
dialysis patients, especially in those with significant Dietary Recommendations for Trace Elements
residual renal function and urine output, if such and Vitamins
dietary restrictions would compromise the need
for adequate protein and energy intake in these In addition to protein-energy wasting, dialysis
patients. patients may also suffer from deficiencies of mi-
cronutrients, particularly trace elements and vita-
mins. Common vitamin deficiencies observed in
Dietary Fat Restrictions maintenance dialysis patients include vitamin C or
ascorbic acid, vitamin B6 or pyridoxine, folate, and
Although it would seem intuitive to extrapolate 1,25-dihydroxycholecalciferol or calcitriol, and trace
the low dietary fat recommendations of the general element deficiencies may include iron, zinc, and
population to dialysis patients, there are virtually selenium. In contrast, toxicities in dialysis patients
no convincing data to suggest that restricting die- may include aluminum and possibly copper (55).
tary fat has any advantage in this latter group. A Examining dietary recommendations for each of
surprising observation, is that total and LDL hyper- these vitamins and trace elements is beyond the
cholesterolemia, although very common in nondial- scope of this review article. However, it is impor-
ysis ambulatory outpatients, are substantially less tant to note that in dialysis patients, there is an
prevalent in the dialysis population, although the abnormally high prevalence of antioxidant defi-
prevalence of hypertriglyceridemia is nearly equiva- ciency which can be engendered or aggravated by
lent (46). In comparative analyses of randomly low intake of natural sources such as fresh fruits
selected hemodialysis patients in Southern Califor- and vegetable given the imposed dietary restriction
nia who were one-to-one randomly matched on gen- that may be associated with inadequate ingestion of
der, race/ethnicity, diabetes mellitus, and age antioxidant vitamins such as vitamins E, C, and
(5 years) to nondialyzed outpatients from the carotenoids (4,31,55).
same geographic area and whose lipid panels were
measured in the same laboratory center, total cho-
lesterol and LDL and HDL levels were 51, 39; Dietary Calcium Restrictions
10 mg/dl lower, respectively, in hemodialysis
patients than in control subjects even after adjust- With the emergence of calcium-free phosphorus
ment for body mass index and statin use (p < 0.001) binders and recent data on vascular calcification
(46). It is important to note that in most epidemio- (56–58), there has been a drastic change in the pre-
logic studies, higher lipoprotein levels (47) or higher vailing paradigm of maintaining positive calcium
body fat (48) are associated with greater survival in balance (59) and recommending low dietary calcium
dialysis patients, while associations with HDL are over the past 10–15 years (60). Even though virtu-
more complex (49–51); hence, achieving higher cir- ally all epidemiologic studies show higher death risk
culating levels of lipoproteins and their dietary associated with high serum calcium levels >10.5 mg/
modulation may have favorable impact in dialysis dl, low serum calcium levels <8.5 mg/dl are also
patients. associated with higher mortality (61). A high serum
In a randomized controlled study by Ewers et al. calcium level is not necessarily a result of a greater
(52), the effects of oral unsaturated fat supplements calcium load, but may be related to other hormonal
were examined in 40 Danish hemodialysis patients. derangements including hyperparathyroidism (62).
Fat supplementation resulted in increased total The surge in use of calcimimetics (63,64) may com-
energy intake of +380 cal/day, a 9% greater intake plicate the current recommendations pertaining to
of total energy attributed to dietary fat, and dietary calcium intake in dialysis patients; this is an
a + 0.5 kg increase in weight, while serum C-reac- area that begs future research.
8 Kalantar-Zadeh et al.
In-Center Restrictions for Eating during the nutritional status and patients’ health-related
Hemodialysis quality of life, which is per se related to nutritional
status (71). There is little doubt that both dietary-
In the United States and Canada, there are signif- nutritional and pharmacologic status of dialysis
icant restrictions for eating during hemodialysis patients have overarching and long-lasting impact
treatment in dialysis clinics. Among the reasons to on patient survival even after successful kidney
justify these restrictions are postprandial hypoten- transplantation (72). As stated above, a case–con-
sion, aspiration risk, infection control and hygiene, trol study comparing dietary patterns of hemodialy-
dialysis staff burden, diabetes and phosphorus con- sis patients versus the general population suggested
trol, and financial constraints (3). However, in other that dietary restriction in dialysis patients, including
countries such as Germany, Japan, and many other low potassium and phosphorus, leads to avoidance
European and Asian nations, meals and meal trays of most fresh fruits and vegetables and a more ath-
are regularly prepared and served during each he- erogenic diet with lower vitamin C, fiber, and carot-
modialysis treatment session (3). We believe that in enoid (31). In a recent cross-sectional study by
carefully selected and monitored patients, in-center Khoueiry et al. (4) using the “Dialysis Food
provision of high-protein meals and/or oral nutri- Frequency Questionnaire,” (31), 97% of hemodialy-
tional supplements during hemodialysis is a feasible, sis patients had lower than the recommended die-
inexpensive, and patient-friendly strategy (3). Given tary fiber intake of 25 g/day or more. The study
the fact that meals and supplements during hemodi- concluded that most dialysis patients did not meet
alysis would require only a small fraction of the the dietary guidelines for reducing the risk of car-
funds currently used for dialysis patients, this is also diovascular disease (4). Hence, reinforcing dietary
an economically feasible strategy (3). restrictions on dialysis patients may contribute to
atherosclerosis and increased cardiovascular mor-
bidity and mortality.
Racial Disparities and Diet Some nephrologists have noted that less compli-
ant dialysis patients appear to live longer than the
Several unique racial/ethnic disparities exist more compliant ones, an observation that may have
among hemodialysis patients, such that there is a some roots in the aforementioned dietary restric-
3.5- and 1.5-fold greater representation of African tions. Although we warn against over-interpretation
Americans and Hispanics, respectively, compared to of anecdotal observations, we cannot dismiss the
non-Hispanic Whites (65,66). For reasons that have plausible hypothesis that adhering to severe dietary
remained vastly unexplainable, minority dialysis restrictions may cause more harm than benefit, no
patients exhibit greater survival than non-Hispanic matter how provocative it may sound. Many dieti-
white dialysis patients (67). African American dialy- tians are under pressure by dialysis companies to
sis patients are 15–20% less likely to die of cardio- achieve lower averaged phosphorus and potassium
vascular (68) disease than Whites especially those values in their dialysis units, and this may lead to
who are older than 50 years (69). Recent data sug- the risky practice of hounding patients to eat less in
gest that significant differences exist between African an effort to improve arbitrary numbers. It is time to
American and non-Hispanic and Hispanic white he- revisit the role of dietitians and nephrologists in the
modialysis patients with regard to nutritional status, dialysis units and to reexamine current practices (1),
dietary intake, and inflammation, and that these so that their approach to dietary counseling of dial-
differences may contribute to racial survival dispari- ysis patients may be consistent with most recent
ties (68,70). In a 6-year cohort of 799 hemodialysis data such as those by Lynch et al. (15) and Shinab-
patients, the dietary intake of African Americans erger et al. (14), which suggest that mere dietary
was higher in energy (+293  119 cal/day) and fat restrictions may be detrimental.
(+18  5 g/day) compared to Whites (68,69). Given the significant knowledge gap discussed
Whether or not minorities are less compliant with above, there is a pressing need for high-impact
the dietary restrictions, with subsequent paradoxi- research with immediate clinical applicability in the
cally better outcomes is a highly provocative hypoth- nutritional management of dialysis patients. Several
esis that remains to be examined in future studies. relevant questions for future research in this area are
the following: What are the real impact of restricting
dietary potassium, phosphorus, calcium, and salt on
Consequences of Dietary Restriction and clinical outcomes? What is the best dietary protein
Future Research Directions range upon transition to dialysis therapy? Should the
recommended “low”-protein diet for advanced CKD
It is not clear whether imposing the traditionally prior to ESRD be continued for less frequent and
practiced dietary restrictions on dialysis patients incremental hemodialysis regimen including those
contribute to improved outcomes. While some die- who receive only once or twice weekly hemodialysis
tary restrictions appear to be justifiable, it is possi- therapy (73–77) as compared to thrice-weekly or
ble, although not yet proven, that overzealous and more frequent hemodialysis? What types of high
extensive restrictions may lead to poor outcomes biological value proteins including plants- versus
including worse survival by virtue of deteriorating animal-based foods can be recommended as better
DIETARY RESTRICTIONS 9
sources of low-phosphorous diet? Additional 17. Lukowsky LR, Molnar MZ, Zaritsky JJ, Sim JJ, Mucsi I, Kovesdy
CP, Kalantar-Zadeh K: Mineral and bone disorders and survival in
research on the potential of a more liberalized dietary hemodialysis patients with and without polycystic kidney disease.
approach on patient-centered outcomes would be Nephrol Dial Transplant 27:2899–2907, 2012
relevant as well. Overall, the benefits and harms of 18. Qunibi W, Kalantar-Zadeh K: Target levels for serum phosphorus
and parathyroid hormone. Semin Dial 24:29–33, 2011
the decade-long practiced dietary restrictions are 19. Noori N, Kalantar-Zadeh K, Kovesdy CP, Bross R, Benner D, Kop-
widely unknown and need urgent research. ple JD: Association of dietary phosphorus intake and phosphorus to
protein ratio with mortality in hemodialysis patients. Clin J Am Soc
Nephrol 5:683–692, 2010
20. Sim JJ, Bhandari SK, Smith N, Chung J, Liu IL, Jacobsen SJ, Kalan-
Acknowledgments tar-Zadeh K: Phosphorus and risk of renal failure in subjects with
normal renal function. Am J Med 126:311–318, 2013
21. Cupisti A, Kalantar-Zadeh K: Management of natural and added die-
This work was supported by KKZ’s research grants tary phosphorus burden in kidney disease. Semin Nephrol 33:180–190,
from the NIH/NIDDK (K24-DK091419 and R01- 2013
22. Cupisti A, Benini O, Ferretti V, Gianfaldoni D, Kalantar-Zadeh K:
DK078106) and philanthropic grants from Harold Sim- Novel differential measurement of natural and added phosphorus in
mons, Louis Chang, and AVEO. cooked ham with or without preservatives. J Ren Nutr 22:533–540, 2012
23. Benini O, Saba A, Ferretti V, Gianfaldoni D, Kalantar-Zadeh K,
Cupisti A: Development and analytical evaluation of a spectrophoto-
metric procedure for the quantification of different types of phospho-
References rus in meat products. J Agric Food Chem 62:1247–1253, 2014
24. Taylor LM, Kalantar-Zadeh K, Markewich T, Colman S, Benner D,
1. Ikizler TA, Franch HA, Kalantar-Zadeh K, ter Wee PM, Wanner C: Sim JJ, Kovesdy CP: Dietary egg Whites for phosphorus control in
Time to revisit the role of renal dietitian in the dialysis unit. J Ren maintenance haemodialysis patients: a pilot study. J Ren Care 37:
Nutr 24:58–60, 2014 16–24, 2011
2. Streja E, Molnar MZ, Kovesdy CP, Bunnapradist S, Jing J, Nissenson 25. Streja E, Wang HY, Lau WL, Molnar MZ, Kovesdy CP, Kalantar-
AR, Mucsi I, Danovitch GM, Kalantar-Zadeh K: Associations of pre- Zadeh K, Park J: Mortality of combined serum phosphorus and para-
transplant weight and muscle mass with mortality in renal transplant thyroid hormone concentrations and their changes over time in he-
recipients. Clin J Am Soc Nephrol 6:1463–1473, 2011 modialysis patients. Bone 61:201–207, 2014
3. Kalantar-Zadeh K, Ikizler TA: Let them eat during dialysis: an over- 26. Streja E, Lau WL, Goldstein L, Sim JJ, Molnar MZ, Nissenson AR,
looked opportunity to improve outcomes in maintenance hemodialysis Kovesdy CP, Kalantar-Zadeh K: Hyperphosphatemia is a combined
patients. J Ren Nutr 23:157–163, 2013 function of high serum PTH and high dietary protein intake in dialysis
4. Khoueiry G, Waked A, Goldman M, El-Charabaty E, Dunne E, patients. Kidney Int Suppl 3:462–468, 2013
Smith M, Kleiner M, Lafferty J, Kalantar-Zadeh K, El-Sayegh S: Die- 27. Kovesdy CP, Regidor DL, Mehrotra R, Jing J, McAllister CJ, Green-
tary intake in hemodialysis patients does not reflect a heart healthy land S, Kopple JD, Kalantar-Zadeh K: Serum and dialysate potas-
diet. J Ren Nutr 21:438–447, 2011 sium concentrations and survival in hemodialysis patients. Clin J Am
5. Kovesdy CP, Kopple JD, Kalantar-Zadeh K: Management of protein- Soc Nephrol 2:999–1007, 2007
energy wasting in non-dialysis-dependent chronic kidney disease: rec- 28. Torlen K, Kalantar-Zadeh K, Molnar MZ, Vashistha T, Mehrotra R:
onciling low protein intake with nutritional therapy. Am J Clin Nutr Serum potassium and cause-specific mortality in a large peritoneal
97:1163–1177, 2013 dialysis cohort. Clin J Am Soc Nephrol 7:1272–1284, 2012
6. Kalantar-Zadeh K, Cano NJ, Budde K, Chazot C, Kovesdy CP, Mak 29. Noori N, Kalantar-Zadeh K, Kovesdy CP, Murali SB, Bross R,
RH, Mehrotra R, Raj DS, Sehgal AR, Stenvinkel P, Ikizler TA: Diets Nissenson AR, Kopple JD: Dietary potassium intake and mortality
and enteral supplements for improving outcomes in chronic kidney in long-term hemodialysis patients. Am J Kidney Dis 56:338–347,
disease. Nat Rev Nephrol 7:369–384, 2011 2010
7. Shah AP, Kalantar-Zadeh K, Kopple JD: The role of keto acid sup- 30. Kalantar-Zadeh K, Kovesdy CP, Bross R, Benner D, Noori N, Mu-
plements in the management of chronic kidney disease: a north ameri- rali SB, Block T, Norris J, Kopple JD, Block G: Design and develop-
can perspective. Am J Kidney Dis, 2015 in press ment of a dialysis food frequency questionnaire. J Ren Nutr 21:
8. Shinaberger CS, Kilpatrick RD, Regidor DL, McAllister CJ, Green- 257–262, 2011
land S, Kopple JD, Kalantar-Zadeh K: Longitudinal associations 31. Kalantar-Zadeh K, Kopple JD, Deepak S, Block D, Block G: Food
between dietary protein intake and survival in hemodialysis patients. intake characteristics of hemodialysis patients as obtained by food fre-
Am J Kidney Dis 48:37–49, 2006 quency questionnaire. J Ren Nutr 12:17–31, 2002
9. Kalantar-Zadeh K, Supasyndh O, Lehn RS, McAllister CJ, Kopple 32. Pitt B, Anker SD, Bushinsky DA, Kitzman DW, Zannad F, Huang
JD: Normalized protein nitrogen appearance is correlated with hospi- IZ, Investigators P-H: Evaluation of the efficacy and safety of
talization and mortality in hemodialysis patients with Kt/V greater RLY5016, a polymeric potassium binder, in a double-blind, placebo-
than 1.20. J Ren Nutr 13:15–25, 2003 controlled study in patients with chronic heart failure (the PEARL-
10. Ravel VA, Molnar MZ, Streja E, Kim JC, Victoroff A, Jing J, Benner HF) trial. Eur Heart J 32:820–828, 2011
D, Norris KC, Kovesdy CP, Kopple JD, Kalantar-Zadeh K: Low 33. Rhee CM, Leung AM, Kovesdy CP, Lynch KE, Brent GA, Kalantar-
protein nitrogen appearance as a surrogate of low dietary protein Zadeh K: Updates on the management of diabetes in dialysis patients.
intake is associated with higher all-cause mortality in maintenance he- Semin Dial 27:135–145, 2014
modialysis patients. J Nutr 143:1084–1092, 2013 34. Ricks J, Molnar MZ, Kovesdy CP, Shah A, Nissenson AR, Williams
11. Kalantar-Zadeh K, Gutekunst L, Mehrotra R, Kovesdy CP, Bross R, M, Kalantar-Zadeh K: Glycemic control and cardiovascular mortality
Shinaberger CS, Noori N, Hirschberg R, Benner D, Nissenson AR, in hemodialysis patients with diabetes: a 6-year cohort study. Diabetes
Kopple JD: Understanding sources of dietary phosphorus in the treat- 61:708–715, 2012
ment of patients with chronic kidney disease. Clin J Am Soc Nephrol 35. Molnar MZ, Huang E, Hoshino J, Krishnan M, Nissenson AR, Kov-
5:519–530, 2010 esdy CP, Kalantar-Zadeh K: Association of pretransplant glycemic
12. Kalantar-Zadeh K: Patient education for phosphorus management in control with posttransplant outcomes in diabetic kidney transplant
chronic kidney disease. Patient Prefer Adherence 7:379–390, 2013 recipients. Diabetes Care 34:2536–2541, 2011
13. Fouque D, Horne R, Cozzolino M, Kalantar-Zadeh K: Balancing 36. Hoshino J, Mehrotra R, Rhee CM, Yamagata K, Ubara Y, Takaichi
nutrition and serum phosphorus in maintenance dialysis. Am J Kidney K, Kovesdy CP, Molnar MZ, Kalantar-Zadeh K: Using hemoglobin
Dis 64:143–150, 2014 A1c to derive mean blood glucose in peritoneal dialysis patients. Am J
14. Shinaberger CS, Greenland S, Kopple JD, Van Wyck D, Mehrotra R, Nephrol 37:413–420, 2013
Kovesdy CP, Kalantar-Zadeh K: Is controlling phosphorus by 37. Park J, Lertdumrongluk P, Molnar MZ, Kovesdy CP, Kalantar-
decreasing dietary protein intake beneficial or harmful in persons with Zadeh K: Glycemic control in diabetic dialysis patients and the burnt-
chronic kidney disease? Am J Clin Nutr 88:1511–1518, 2008 out diabetes phenomenon. Curr Diab Rep 12:432–439, 2012
15. Lynch KE, Lynch R, Curhan GC, Brunelli SM: Prescribed dietary 38. Kovesdy CP, Park JC, Kalantar-Zadeh K: Glycemic control and
phosphate restriction and survival among hemodialysis patients. Clin J burnt-out diabetes in ESRD. Semin Dial 23:148–156, 2010
Am Soc Nephrol 6:620–629, 2011 39. Kalantar-Zadeh K, Derose SF, Nicholas S, Benner D, Sharma K,
16. Lertdumrongluk P, Rhee CM, Park J, Lau WL, Moradi H, Jing J, Kovesdy CP: Burnt-out diabetes: impact of chronic kidney disease
Molnar MZ, Brunelli SM, Nissenson AR, Kovesdy CP, Kalantar- progression on the natural course of diabetes mellitus. J Ren Nutr
Zadeh K: Association of serum phosphorus concentration with mor- 19:33–37, 2009
tality in elderly and nonelderly hemodialysis patients. J Ren Nutr 40. Abe M, Kalantar-Zadeh K: Hemodialysis associated hypoglycemia
23:411–421, 2013 and glyemic disarrays. Nat Rev Nephrol 2015 in press
10 Kalantar-Zadeh et al.
41. Kalantar-Zadeh K: A critical evaluation of glycated protein parame- 59. Winchester JF, Rotellar C, Goggins M, Robino D, Rakowski TA,
ters in advanced nephropathy: a matter of life or death: A1C remains Argy WP: Calcium and phosphate balance in dialysis patients. Kidney
the gold standard outcome predictor in diabetic dialysis patients. Int Suppl 41:S174–178, 1993
Counterpoint.. Diabetes Care 35:1625–1628, 2012 60. Moe S, Drueke T, Cunningham J, Goodman W, Martin K, Olgaard
42. Duong U, Mehrotra R, Molnar MZ, Noori N, Kovesdy CP, Nissen- K, Ott S, Sprague S, Lameire N, Eknoyan G: Definition, evaluation,
son AR, Kalantar-Zadeh K: Glycemic control and survival in perito- and classification of renal osteodystrophy: a position statement from
neal dialysis patients with diabetes mellitus. Clin J Am Soc Nephrol Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int
6:1041–1048, 2011 69:1945–1953, 2006
43. Kalantar-Zadeh K, Kopple JD, Regidor DL, Jing J, Shinaberger CS, 61. Miller JE, Kovesdy CP, Norris KC, Mehrotra R, Nissenson AR,
Aronovitz J, McAllister CJ, Whellan D, Sharma K: A1C and survival Kopple JD, Kalantar-Zadeh K: Association of cumulatively low or
in maintenance hemodialysis patients. Diabetes Care 30:1049–1055, high serum calcium levels with mortality in long-term hemodialysis
2007 patients. Am J Nephrol 32:403–413, 2010
44. Kalantar-Zadeh K, Regidor DL, Kovesdy CP, Van Wyck D, Bunna- 62. Li J, Molnar MZ, Zaritsky JJ, Sim JJ, Streja E, Kovesdy CP, Salusky
pradist S, Horwich TB, Fonarow GC: Fluid retention is associated I, Kalantar-Zadeh K: Correlates of parathyroid hormone concentra-
with cardiovascular mortality in patients undergoing long-term tion in hemodialysis patients. Nephrol Dial Transplant 28:1516–1525,
hemodialysis. Circulation 119:671–679, 2009 2013
45. Stolarz-Skrzypek K, Kuznetsova T, Thijs L, Tikhonoff V, Seidlerova 63. Kalantar-Zadeh K, Kovesdy CP: Is it worth correcting hyperparathy-
J, Richart T, Jin Y, Olszanecka A, Malyutina S, Casiglia E, Filipov- roidism if hyperphosphatemia and hypocalcemia worsen? A cinacalcet
sky J, Kawecka-Jaszcz K, Nikitin Y, Staessen JA, European Project story. Am J Kidney Dis 53:183–188, 2009
on Genes in Hypertension I: Fatal and nonfatal outcomes, incidence 64. Belozeroff V, Goodman WG, Ren L, Kalantar-Zadeh K: Cinacalcet
of hypertension, and blood pressure changes in relation to urinary lowers serum alkaline phosphatase in maintenance hemodialysis
sodium excretion. JAMA 305:1777–1785, 2011 patients. Clin J Am Soc Nephrol 4:673–679, 2009
46. Kalantar-Zadeh K, Kilpatrick RD, Kopple JD, Stringer WW: A 65. United States Renal Data System (USRDS): USRDS 2010 Annual
matched comparison of serum lipids between hemodialysis patients Data Report. Atlas of Chronic Kidney Disease and End-Stage Renal
and nondialysis morbid controls. Hemodial Int 9:314–324, 2005 Disease in the United States. Bethesda, MD: National Institutes of
47. Kilpatrick RD, McAllister CJ, Kovesdy CP, Derose SF, Kopple JD, Health, National Institute of Diabetes and Digestive and Kidney Dis-
Kalantar-Zadeh K: Association between serum lipids and survival in eases, 2010, www.usrds.org
hemodialysis patients and impact of race. J Am Soc Nephrol 18: 66. Kalantar-Zadeh K, Kovesdy CP, Derose SF, Horwich TB, Fonarow
293–303, 2007 GC: Racial and survival paradoxes in chronic kidney disease. Nat Clin
48. Noori N, Kovesdy CP, Dukkipati R, Kim Y, Duong U, Bross R, Ore- Pract Nephrol 3:493–506, 2007
opoulos A, Luna A, Benner D, Kopple JD, Kalantar-Zadeh K: Sur- 67. Nicholas SB, Kalantar-Zadeh K, Norris KC: Racial disparities in kid-
vival predictability of lean and fat mass in men and women ney disease outcomes. Semin Nephrol 33:409–415, 2013
undergoing maintenance hemodialysis. Am J Clin Nutr 92:1060–1070, 68. Noori N, Kovesdy CP, Dukkipati R, Feroze U, Molnar MZ, Bross
2010 R, Nissenson AR, Kopple JD, Norris KC, Kalantar-Zadeh K: Racial
49. Moradi H, Vaziri ND, Kashyap ML, Said HM, Kalantar-Zadeh K: and ethnic differences in mortality of hemodialysis patients: role of
Role of HDL dysfunction in end-stage renal disease: a double-edged dietary and nutritional status and inflammation. Am J Nephrol
sword. J Ren Nutr 23:203–206, 2013 33:157–167, 2011
50. Moradi H, Streja E, Kashyap ML, Vaziri ND, Fonarow GC, Kalan- 69. Kalantar-Zadeh K, Kovesdy CP, Norris KC: Racial survival paradox
tar-Zadeh K: Elevated high-density lipoprotein cholesterol and cardio- of dialysis patients: robust and resilient. Am J Kidney Dis 60:182–185,
vascular mortality in maintenance hemodialysis patients. Nephrol Dial 2012
Transplant 29:1554–1562, 2014 70. Lertdumrongluk P, Kovesdy CP, Norris KC, Kalantar-Zadeh K:
51. Khoueiry G, Abdallah M, Saiful F, Abi Rafeh N, Raza M, Bhat T, Nutritional and inflammatory axis of racial survival disparities. Semin
El-Sayegh S, Kalantar-Zadeh K, Lafferty J: High-density lipoprotein Dial 26:36–39, 2013
in uremic patients: metabolism, impairment, and therapy. Int Urol 71. Feroze U, Noori N, Kovesdy CP, Molnar MZ, Martin DJ, Reina-Pat-
Nephrol 46:27–39, 2014 ton A, Benner D, Bross R, Norris KC, Kopple JD, Kalantar-Zadeh
52. Ewers B, Riserus U, Marckmann P: Effects of unsaturated fat dietary K: Quality-of-life and mortality in hemodialysis patients: roles of race
supplements on blood lipids, and on markers of malnutrition and and nutritional status. Clin J Am Soc Nephrol 6:1100–1111, 2011
inflammation in hemodialysis patients. J Ren Nutr 19:401–411, 2009 72. Molnar MZ, Bunnapradist S, Huang E, Krishnan M, Nissenson AR,
53. Noori N, Dukkipati R, Kovesdy CP, Sim JJ, Feroze U, Murali SB, Bross Kovesdy CP, Kalantar-Zadeh K: Association of pre-transplant eryth-
R, Benner D, Kopple JD, Kalantar-Zadeh K: Dietary omega-3 fatty acid, ropoiesis-stimulating agent responsiveness with post-transplant out-
ratio of omega-6 to omega-3 intake, inflammation, and survival in long- comes. Nephrol Dial Transplant 27:3345–3351, 2012
term hemodialysis patients. Am J Kidney Dis 58:248–256, 2011 73. Kalantar-Zadeh K, Unruh M, Zager PG, Kovesdy CP, Bargman JM,
54. Kalantar-Zadeh K, Stenvinkel P, Bross R, Khawar OS, Rammohan Chen J, Sankarasubbaiyan S, Shah G, Golper T, Sherman RA, Gold-
M, Colman S, Benner D: Kidney insufficiency and nutrient-based farb DS: Twice-weekly and incremental hemodialysis treatment for ini-
modulation of inflammation. Curr Opin Clin Nutr Metab Care 8: tiation of kidney replacement therapy. Am J Kidney Dis 64:181–186,
388–396, 2005 2014
55. Kalantar-Zadeh K, Kopple JD: Trace elements and vitamins in main- 74. Rhee CM, Unruh M, Chen J, Kovesdy CP, Zager P, Kalantar-Zadeh
tenance dialysis patients. Adv Ren Replace Ther 10:170–182, 2003 K: Infrequent dialysis: a new paradigm for hemodialysis initiation. Se-
56. Shantouf RS, Budoff MJ, Ahmadi N, Ghaffari A, Flores F, Gopal A, min Dial 26:720–727, 2013
Noori N, Jing J, Kovesdy CP, Kalantar-Zadeh K: Total and individ- 75. Kalantar-Zadeh K, Casino FG: Let us give twice-weekly hemodialysis
ual coronary artery calcium scores as independent predictors of mor- a chance: revisiting the taboo. Nephrol Dial Transplant 29:1618–1620,
tality in hemodialysis patients. Am J Nephrol 31:419–425, 2010 2014
57. Shantouf R, Ahmadi N, Flores F, Tiano J, Gopal A, Kalantar-Zadeh 76. Zhang M, Wang M, Li H, Yu P, Yuan L, Hao C, Chen J, Kalantar-
K, Budoff MJ: Impact of phosphate binder type on coronary artery Zadeh K: Association of initial twice-weekly hemodialysis treatment
calcification in hemodialysis patients. Clin Nephrol 74:12–18, 2010 with preservation of residual kidney function in ESRD patients. Am J
58. Zeb I, Ahmadi N, Molnar MZ, Li D, Shantouf R, Hatamizadeh P, Nephrol 40:140–150, 2014
Choi T, Kalantar-Zadeh K, Budoff MJ: Association of coronary 77. Caria S, Cupisti A, Sau G, Bolasco P: The incremental treatment of
artery calcium score and vascular dysfunction in long-term hemodialy- ESRD: a low-protein diet combined with weekly hemodialysis may be
sis patients. Hemodial Int 17:216–222, 2013 beneficial for selected patients. BMC Nephrol 15:172, 2014

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