27. Royal V, Quint P, Leblanc M et al. IgD heavy-chain deposition disease: de- 31.

31. Berden AE, Ferrario F, Hagen EC et al. Histopathologic classification of

tection by laser microdissection and mass spectrometry. J Am Soc Nephrol ANCA-associated glomerulonephritis. J Am Soc Nephrol 2010; 21: 1628–1636
2015; 26: 784–790 32. Sethi S, D’Agati VD, Nast CC et al. A proposal for standardized grading of
28. Sethi S, Vrana JA, Theis JD et al. Mass spectrometry based proteomics in chronic changes in native kidney biopsy specimens. Kidney Int 2017; 91:
the diagnosis of kidney disease. Curr Opin Nephrol Hypertens 2013; 22: 787–789
273–280 33. Bomback AS, Santoriello D, Avasare RS et al. C3 glomerulonephritis
29. Roberts IS, Cook H, Troyanov S et al. The Oxford classification of IgA ne- and dense deposit disease share a similar disease course in a large United
phropathy: pathology definitions, correlations, and reproducibility. Kidney States cohort of patients with C3 glomerulopathy. Kidney Int 2018; 93:
Int 2009; 76: 546–556 977–985.
30. Bajema IM, Wilhelmus S, Alper CE. Revision of the International Society of 34. Glassock RJ, Bleyer AJ, Bargman JM et al. The 2010 nephrology quiz and
Nephrology/Renal Pathology Society classification for lupus nephritis: clari- questionnaire: part 2. Clin J Am Soc Nephrol 2011; 6: 2534–2547
fication of definitions, and modified National Institutes of Health activity
and chronicity indices. Kidney Int 2018; 93: 789–796 Received: 7.4.2018; Editorial decision: 7.6.2018

REVIEW
Nephrol Dial Transplant (2019) 34: 199–207

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

doi: 10.1093/ndt/gfy164
Advance Access publication 5 July 2018

Vegetarian diets and chronic kidney disease

Philippe Chauveau1,2, Laetitia Koppe3,4, Christian Combe1,2,5, Catherine Lasseur1,2, Stanislas Trolonge1 and
Michel Aparicio2
1
Aurad-Aquitaine, Service Hémodialyse, Gradignan, France, 2Service de Néphrologie Transplantation Dialyse, Centre Hospitalier Universitaire
de Bordeaux, Hôpital Pellegrin, Bordeaux, France, 3Department of Nephrology, Hospices Civils de Lyon, Centre Hospitalier Lyon-Sud, Pierre-
Benite, France, 4University of Lyon, CarMeN lab, INSERM U1060, INRA U1397, INSA de Lyon, Université Claude Bernard Lyon 1,
Villeurbanne, France and 5Unité INSERM 1026, Université de Bordeaux, Bordeaux, France

Correspondence and offprint requests to: Philippe Chauveau; E-mail: ph.chauveau@gmail.com

ABSTRACT Keywords: kidney disease, nutrition, vegetarianism

While dietary restriction of protein intake has long been pro-
posed as a possible kidney-protective treatment, the effects of
changes in the quality of ingested proteins on the prevalence INTRODUCTION
and risk of progression of chronic kidney disease (CKD) have For more than a century, the quantitative reduction of dietary
been scarcely studied; these two aspects are reviewed in the pre- protein intake has been recognized as a therapeutic measure
sent article. The prevalence of hypertension, type 2 diabetes in chronic kidney disease (CKD). In contrast, the relationship
and metabolic syndrome, which are the main causes of CKD between dietary protein sources and the risk of incident CKD
in Western countries, is lower in vegetarian populations. and its progression has long been neglected. The purpose of
Moreover, there is a negative relationship between several com- the present article is to successively provide information on
ponents of plant-based diets and numerous factors related to these two topics through recent data from the medical
CKD progression such as uraemic toxins, inflammation, oxida- literature.
tive stress, metabolic acidosis, phosphate load and insulin resis- First, to date, there seems to be a lack of reports on the prev-
tance. In fact, results from different studies seem to confirm a alence of renal disease in the vegetarian population, whereas
kidney-protective effect of plant-based diets in the primary pre- numerous studies have shown a decrease in the risk of hyper-
vention of CKD and the secondary prevention of CKD progres- tension [1], type 2 diabetes [2] and metabolic syndrome (MetS)
sion. Various studies have determined the nutritional safety of [3, 4], which are the main causes of CKD in Western countries,
plant-based diets in CKD patients, despite the combination of a in vegetarian populations. Given these findings, it would seem
more or less severe dietary protein restriction. As observed in reasonable to assume that the renal consequences of these dis-
the healthy population, this dietary pattern is associated with a eases should also be less prevalent among vegetarians.
reduced risk of all-cause mortality in CKD patients. We propose Second, numerous studies have shown that plant-based diets
that plant-based diets should be included as part of the clinical are associated with a decrease in many risk factors associated
recommendations for both the prevention and management with CKD progression, such as hypertension [5], uraemic tox-
of CKD. ins [6], inflammation [7] and oxidative stress [8], preventing

C The Author(s) 2018. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved.
V 199
the development of some metabolic disorders [9]. Thus one The dietary components capable of lowering BP include the
could be led to speculate on the potential benefits of plant- following.
based diets on renal outcomes in CKD patients. As a matter of
fact, these benefits have already been confirmed in most studies Salt intake. A reduced salt intake is one of the main dietary
[10, 11]. approaches to prevent and treat hypertension. But surprisingly,
As Mariotti did in his book [12], in this review we used the it was shown almost 30 years ago that while Seventh-day
term ‘vegetarian’ to include all forms of vegetarian diet, from Adventist vegetarians had lower BP than non-vegetarian control
lacto-ovo-vegetarian to strict vegan. In cases where a study re- subjects, their urinary sodium levels were similar [13].
ferred to a particular diet, we mention the diet in question.
Potassium intake. As shown in numerous observational
and epidemiological studies, a high potassium intake, related to
PREVALENCE OF THE MAIN CAUSES OF CKD high consumption of fruits and vegetables, is associated with
(HYPERTENSION, TYPE 2 DIABETES AND lower BP in both non-hypertensive and hypertensive individu-
METS) IN VEGETARIANS als. In the Dietary Approaches to Stop Hypertension (DASH)
Study, 8 weeks on a diet rich in fruits, vegetables and low-fat
Vegetarianism and blood pressure

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

dairy products resulted in a mean reduction in systolic and dia-
Numerous cross-sectional studies have found that, in indus- stolic BP of 5.6 and 3.0 mmHg, respectively [20, 21]. These find-
trialized countries, after adjustments for age, sex and body ings should be related to the diuretic and natriuretic effects of
weight, blood pressure (BP) was lower among vegetarians than potassium.
non-vegetarians. In observational studies, vegetarians also expe- Whether a cause or consequence, hypertension is commonly
rience a blunted increase in BP with age [13]. In black as well as associated with CKD, and because of a potential increased risk
white subjects of the Adventist Health Study-2, two different of hyperkalaemia in CKD patients, their diet is restricted in
analyses showed that the vegetarian Adventists had lower sys- terms of fruit and vegetable intake. At first glance, the risk of
tolic and diastolic BP than their omnivore counterparts [1, 14]. hyperkalaemia seems all the more real since it is potentiated by
A recent meta-analysis, including seven controlled trials (311 the frequent use of drugs, such as angiotensin-converting
participants) and 32 observational studies (21 604 participants), enzyme (ACE) inhibitors, angiotensin receptor blockers and
found that when omnivores are switched to a vegetarian diet, non-steroidal anti-inflammatory agents, that can substantially
the mean systolic BP is reduced by 4.8 mmHg and the mean di- impair urinary potassium excretion. However, in non-dialysed
astolic BP by 2.2 mmHg in the controlled trials, and the mean CKD patients, serum potassium concentration appears to be
systolic BP is reduced by 6.9 mmHg and the mean diastolic BP weakly associated with dietary potassium intake, and the alka-
by 4.7 mmHg in observational studies [15]. line load, linked to the increased intake of fruits and vegetables,
Furthermore, vegetarian diets have beneficial effects on favours the shift of potassium from extracellular to intracellular
weight reduction, and low rates of overweight and obesity in veg- fluids [22]. Lastly, fibres associated with high-potassium plant
etarians have been confirmed in different series. In a study in- foods correct the frequent constipation observed in these
cluding >90 000 Seventh-day Adventists, the body mass index patients. As a result, the shorter the intestinal transit time, the
(BMI) was 2.5 kg/m2 lower in vegetarians compared with non- less dietary potassium will be absorbed.
vegetarians [16]. In an analysis of three prospective cohort stud- Therefore it seems reasonable and safe, in CKD Stage 4 and
ies including >120 000 men and women, investigating the rela- 5 patients with retained urine flow, to set the potassium intake
tionship between lifestyle factors and weight changes at 4-year at 4.7 g/day (120 mmol/day), which corresponds to the potas-
intervals, consumption of plant-based foods was inversely asso- sium content of the DASH diet.
ciated with weight gain [17]. In a more recent meta-analysis, in-
cluding 15 intervention trials, prescription of a vegetarian diet of Dietary fibre intake. Results of the International Study on
>4-weeks duration, without energy intake limitations, was asso- Macro/micronutrients and Blood Pressure study have shown
ciated with a mean weight change of 3.4 kg (P < 0.001) [18]. that a higher intake of fibre, especially insoluble ones, may con-
These results may account for the lower BP in vegetarians, tribute to lower BP [23]. Results from this study have confirmed
since numerous observational studies and clinical trials have previous meta-analyses of randomized controlled trials indicat-
shown that BP is directly associated with weight. Dietary data ing that an increased intake of dietary fibre might contribute to
from different studies have shown that the calorie intake of veg- the prevention of hypertension or to the reduction of BP in hy-
etarians is typically lower than that of non-vegetarians, with a pertensive patients [24]. Enhanced insulin sensitivity, improved
mean difference of 400 calories/day, as observed, for example, vascular endothelial function and improved magnesium intesti-
in the National Health and Nutrition Examination Survey nal absorption have been proposed to explain the BP-lowering
(NHANES) 1999–2004 study [19]. This energy deficit can con- effect of dietary fibres [25].
tribute to a reduction in BP as a result of weight loss; however, a It was noticed that when the intake of fibre is increased, in
lower BP effect through a vegetarian diet has also been observed isolation from other dietary changes, no effects on BP were ob-
in individuals with normal body weight [1]. The effects of the served [26].
diet on BP cannot be explained by weight loss alone, and the
different dietary components of vegetarian diets each individu- Fat intake. Vegetarians eat less total fat and also more poly-
ally contribute to lowering BP. unsaturated fatty acids, resulting in an elevation in the dietary

200 P. Chauveau et al.

polyunsaturated:saturated (P:S) ratio (1.0 versus 0.3), but in non-vegetarians, while the prevalence was intermediate in
most studies do not support the view that these changes have a participants consuming lacto-ovo-, pesco- and semi-vegetarian
direct BP-lowering effect [27]. However, in a cross-sectional diets [2].
study comparing age- and sex-matched vegetarians and non- A systematic review and meta-analysis including 255 type 2
vegetarians, a higher resting energy expenditure (REE) was diabetic patients (17 lacto-ovo-vegetarians and 238 vegans)
found in vegetarians than in non-vegetarians, contributing to showed that consumption of a vegetarian diet, combined with
their lower BMI values, independent of exercise. This increase exercise, was associated with a dramatic reduction in the use
in REE was positively correlated with a specific component of of glucose-lowering medications and in haemoglobin A1c, as
the vegetarians’ diet—vegetable fats [28]. well as a non-significant reduction in fasting blood glucose con-
centration [34].
Carbohydrate intake. The OmniHeart Study has shown Lastly, vegetable proteins have a lower impact on renal hae-
that, under isocaloric conditions, partial substitution of carbo- modynamics than animal proteins. Replacing animal proteins
hydrates with either protein, particularly from plant sources, or with vegetable proteins may decrease renal hyperfiltration, pro-
monounsaturated fat can reduce BP, improve lipid levels and teinuria and, theoretically, in the long-term, the risk of develop-
reduce cardiovascular risks [25]. It remains uncertain whether ing renal failure [35].

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

these effects result from a reduction in carbohydrate or from a
compensatory increase in other macronutrients [29]. Vegetarianism and MetS
MetS is defined as the presence of at least three of the follow-
Protein intake. Data from several clinical trials suggest a ing criteria: abdominal obesity, low high-density lipoprotein,
small, but significant, inverse relationship between total dietary hypertriglyceridaemia, elevated fasting glucose and hyperten-
protein intake and BP, which was observed with protein intake sion. The prevalence of MetS, which occurs in 20% of the
from plant sources rather than with animal protein intake. This population of the USA, is increasing in developing and devel-
effect appears to be independent of changes in body weight and oped countries [36]. Various dietary patterns have been pro-
may be more apparent in populations with elevated BP and posed for preventing MetS, among which is a vegetarian diet.
older populations. Several cross-sectional and case–control studies have confirmed
The exact mechanisms linking plant proteins to BP have not an association between consumption of a vegetarian diet and an
yet been clarified and different explanations have been put for- estimated 2-fold reduction in the prevalence or risk
ward. Dietary protein has been related to the synthesis of cellu- of developing MetS (except for low-density lipoprotein) [4, 36].
lar ion channels inducing natriuresis, thus leading to lower BP The proposed recommendation of a vegetarian diet was well
[30]. Dietary protein may result in a higher concentration of illustrated in the prospective Atherosclerosis Risk in
several amino acids that have BP-lowering effects [31]. Communities (ARIC) Study, which included >10 000 middle-
Arginine, which serves as a substrate for nitric oxide (NO), is a aged adults, free of diabetes and cardiovascular disease, with an
potent vasodilator; its production improves endothelial func- estimated glomerular filtration rate (eGFR) >60 mL/min/
tion and contributes to BP lowering. Tryptophan may also re- 1.73 m2. Twenty-one per cent of the participants met the crite-
duce BP by augmenting NO production and by reducing ria for MetS at their initial visit, with prevalences of zero, one,
adrenaline and noradrenaline. Higher protein intake may result two, three, four or five traits of MetS of 26, 30, 23, 15, 5 and 1%,
in a higher concentration of histidine, which triggers a vasodila- respectively. After a 9-year follow-up, 7% of the participants de-
tory response [32]. veloped CKD, and the risk of incident CKD increased signifi-
To close this section concerning the relationship between cantly with the baseline number of traits of MetS. These data
vegetarianism and BP, we must mention that several non-die- confirm that, in addition to hypertension and diabetes, MetS is
tary aspects of a vegetarian lifestyle (low to moderate alcohol in- also independently associated with an increased risk for inci-
take, minimal cigarette smoking and regular physical activity) dent CKD [37].
might also contribute to lower BP and more generally have a
beneficial effect on the outcomes of patients [5].
VEGETARIANISM AND EFFECTS ON THE
Vegetarianism and type 2 diabetes FACTORS OF CKD PROGRESSION
Comparison of ovo-lacto-vegetarians with omnivores In addition to their likely impact on the prevalence of the main
showed that the former group were more insulin sensitive than causes of CKD, vegetarian diets should also be potentially bene-
their omnivore counterparts and that the degree of insulin sen- ficial to CKD patients because they inhibit the production of
sitivity was correlated with years on a vegetarian diet [33]. some of the deleterious factors proven responsible for adverse
Whole-grain products and vegetables generally have low gly- outcomes in CKD.
caemic index values, and individuals following vegetarian diets
are less than half as likely to develop diabetes compared with Uraemic toxins
non-vegetarians; these figures were confirmed by the Some protein-bound solutes are produced in the colon by
Adventists Health Study-2 that included >60 000 individuals the action of gut microbiota on food proteins and endogenous
who participated in the study conducted in 2002–06. After ad- proteins that have escaped digestion in the small intestine.
justment for age and different components of lifestyle, the prev- Indoxyl sulphate and p-cresyl sulphate, which result from bac-
alence of type 2 diabetes increased from 2.9% in vegans to 7.6% terial metabolism of the amino acid substrates tryptophan and

Vegetarianism and CKD 201

tyrosine, respectively, are some of the main protein-bound sol- vegetables, vitamins and antioxidants have a lower dietary in-
utes. In CKD patients, prolonged colonic transit times, thera- flammatory score and have been associated with reduced levels
peutic interventions, changes in dietary habits and changes to of interleukin-6 (IL-6) and C-reactive protein (CRP) [46]. The
the gut microbiota result in several changes in bacterial fermen- anti-inflammatory effects of these diets in CKD patients are
tation. These modifications lead to pathogen overgrowth, which linked to the correction of the gut microbiota dysbiosis.
affects the proteolytic bacterial species and results in an in- Consumption of plant-based diets is associated with an en-
creased generation of toxic proteins [38]. These proteins, which hanced richness and diversity of the gut microbiota, resulting in
are normally cleared by the kidneys, accumulate in the plasma a better state of health and metabolic profile. The consequent
of CKD patients, thus contributing to the syndrome of uraemia. decrease in pathobionts and the greater abundance of anti-
They are involved in the progression of CKD and increased car- inflammatory bacteria are also favoured by the increased bowel
diovascular risk, contribute to inflammation and oxidative transit. Moreover, some of the bacteria, which participate in the
stress [39] and insulin resistance (IR) [40] and are indepen- fermentation of carbohydrates that have escaped digestion in
dently associated with overall mortality. the small intestine, promote the generation of short-chain fatty
It has been convincingly demonstrated that the production acids that, besides their anti-inflammatory action, contribute to
of these solutes could be influenced by dietary modifications. In maintain colorectal tissue integrity [47].

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

individuals with normal renal function, a vegetarian diet rich in Besides their already mentioned beneficial effect on BP, die-
non-digestible fibre might reduce, by 60%, the urinary excre- tary fibre has a regulatory role in the inflammatory response, as
tion of p-cresyl sulphate and indoxyl sulphate, which reflects confirmed by NHANES 1999–2000 that included 3920 partici-
their production [6]. Increasing dietary fibre for 6 weeks in hae- pants >20 years of age and showed that dietary fibre intake was
modialysis (HD) patients significantly reduces the plasma free inversely associated with the concentration of serum CRP, with
level of indoxyl sulphate and p-cresyl sulphate by 27% and 24%, the association persisting after adjusting for multiple variables
respectively [41]. In a prospective randomized controlled study [48]. A recent epidemiological study showed that in a cohort of
of 32 CKD patients not yet on dialysis, indoxyl sulphate levels nearly 1 000 000 non-CKD individuals, higher dietary fibre in-
were reduced after only 1 week on a supplemented very-low- take was associated with a reduced risk of all-cause mortality
protein diet of plant-based origin (0.3 g/kg body weight/day), [49]. It can be concluded from these different studies performed
even when preceded by a conventional low-protein diet (0.6 g on healthy people that dietary habits, such as vegetarian diets,
of mixed origins/kg body weight/day) [42]. thus represent one of the potential therapeutic interventions to
Identical findings have been reported with trimethylamine counteract systemic low-grade inflammation of digestive origin.
(TMA) released through the action of gut microbiota from die- On the other hand, different cross-sectional studies have shown
tary compounds mainly found in animal proteins (lecithin, cho- that higher saturated fat intake of animal origin is directly asso-
line, L-carnitine). TMA is secondarily oxidized in the liver to ciated with an increased intestinal permeability, with negative
trimethylamine-N-oxide (TMAO), which is normally cleared consequences on microalbuminuria and inflammation [50].
by the kidney. The accumulation of TMAO in patients with im- In the CKD population, dietary fibre intake is usually low,
paired renal function is associated with an advanced cardiome- particularly in patients on maintenance HD, mainly because of
tabolic risk profile and an increased risk for all-cause mortality dietary recommendations. In a pool of 102 HD patients, dietary
[43]. Vegetarian diets that have a lower lecithin, choline and fibre intake was lower than in control subjects (12.4 6 5.8 g/day
L-carnitine content result in less TMAO production. versus 17.9 6 10.6 g/day; P <0.02), far below the 30 g/day usu-
ally recommended for the general population. Data from
NHANES III that included 14 543 participants confirmed that
Inflammation the CKD group of the cohort had a higher prevalence of high
Systemic low-grade inflammation, which is a common fea- serum CRP levels (>3 mg/L) compared with the non-CKD
ture of CKD, favours the progression of renal dysfunction and group (44.5% versus 24.5%; P <0.001). In CKD and non-CKD
is a major contributor to complications of CKD such as groups, intake of fibre was negatively associated with serum
protein-energy wasting (PEW) and accelerated vascular ageing. CRP levels. Moreover, during the 8.4 years of follow-up, fibre
A key role in the pathogenesis of chronic inflammation in intake was negatively associated with the risk of death, but only
CKD patients has been attributed to the gut microbiome. in the CKD group [51].
Profound changes in the composition of the gut microbiome re-
lated to metabolic alterations of uraemia favour pathogen over-
growth. This intestinal dysbiosis, associated with an increased Oxidative stress
intestinal permeability, which is linked to a decreased expres- Oxidative stress results from an imbalance between the ex-
sion of tight junction proteins, contributes greatly to systemic cessive production of reactive oxygen species during metabolic
inflammation and oxidative stress in CKD patients through the processes and the more or less reduced antioxidant defence sys-
translocation of living bacteria and bacterial components into tem of cells and tissues.
the systemic circulation [44, 45]. Compared with healthy age-matched omnivores, long-term
Nutrients also play a central role in the regulation of inflam- vegetarians have a better antioxidant status and coronary heart
mation, and there is a significant relationship between the type disease profile [52]. The age-dependent increase in the products
of diet, which shapes the gut microbiota, and chronic low-grade of oxidative damage to cellular DNA, lipids and proteins and
inflammation. Diets high in non-digestible fibres, fruits and the age-dependent decrease in antioxidant vitamins are not

202 P. Chauveau et al.

observed in long-term vegetarians [53]. These results were con- of normal, results in several adverse consequences of which
firmed by a study comparing 45 long-term (>15 years) vegeta- muscle wasting, bone loss, impaired insulin sensitivity, chronic
rians with 30 age- and sex-matched omnivores that showed the inflammation and progression of renal failure are the most im-
level of oxidative stress was lower in long-term vegetarians than portant, which may be corrected by oral alkali supplementation
in omnivores. The lack of a significant difference in endogenous [62].
antioxidant activities between the two groups suggests that the The daily acid load is partly dependent on the type of food
observed difference in oxidative stress level was related to the ingested. For a quantitatively identical protein intake, the acid
different dietary patterns. Unlike Western-type diets that lead load linked to animal proteins is higher than that linked to plant
to increased oxidative stress, plant-based diets have a low satu- proteins. Western-type diets are usually characterized by a high
rated fatty acid content and provide twice the antioxidant vita- consumption of animal proteins, which increases the net en-
mins, such as vitamins A and C, than do Western-type diets. dogenous acid production and tends to worsen metabolic aci-
Moreover, fruits and vegetables contain various phytochemi- dosis in CKD patients. In adults with normal renal function
cals, such as polyphenols and flavonoids, which are powerful who are on a Western-type diet, the acid–base equilibrium is
antioxidants and effectively prevent free radical generation [8]. maintained, but mild metabolic acidosis with deleterious effects
The high prevalence of oxidative stress observed in CKD may develop in older men and women as a consequence of the

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

patients is linked to an imbalance between the increased pro- normal decline in renal function with increasing age.
duction of reactive oxygen species favoured by age, hyperten- While a usual Western-type diet induces an acid excess of
sion, diabetes and inflammation and the low antioxidant status 50–100 mEq/day and a urinary pH close to 5.5, an increased
related to a reduced activity of the glutathione system and a low consumption of fruits and vegetables results in a renal acid ex-
intake of antioxidants from the usual diet. Oxidative stress is cretion of <10 mEq/day and urinary pH values of 6.6–6.8; in
present from the early stages of CKD and increases as CKD pro- vegans, the acid load is close to neutrality [63]. Fruits and vege-
gresses [54, 55]. Damage resulting from oxidative stress may in- tables are base-inducing foods, and increasing their daily intake,
fluence the progression of renal injury and plays a prominent as achieved with vegetarian diets, might lower the dietary acid
role in the cardiovascular complications of uraemia, constitut- load and induce results similar to those achieved with alkali
ing one of the major causes of morbidity and mortality [56]. therapy. It has been shown that, in patients with CKD Stage 2,
To date, study findings on the effects of antioxidant therapy adding 2–4 cups of fruits and vegetables to their daily diet was
on cardiovascular disease and mortality in CKD patients have comparable to the administration of 0.5 mEq/kg/day of sodium
remained inconclusive. Antioxidant therapy was found to delay bicarbonate [64].
CKD progression to end-stage renal disease (ESRD), but these On the other hand, a high dietary acid load is associated
results were derived from a very small number of cases with with an increased incidence of CKD. During a mean follow-up
short-term follow-up, so larger clinical trials are needed to con- of 21 years, incident CKD developed in 15.6% of the partici-
firm the possible effectiveness of antioxidant therapy [57]. pants in the prospective ARIC study. After adjusting for estab-
lished risk factors, a higher dietary acid load, estimated by using
Metabolic disorders the potential renal acid load method, was associated with a
higher risk of incident CKD [65], which may be due to activa-
IR. IR is present at all stages of CKD. As in the general popu- tion of the renin–angiotensin system or an increase in endothe-
lation, IR is an independent predictor of cardiovascular events, lin-1 levels [66].
related with impaired vascular endothelial function [58], and is Dietary acid load is also correlated with progression of renal
also strongly associated with increased muscle protein break- failure. In a recent study on 1486 adults with CKD enrolled in
down, contributing to protein energy wasting (PEW) and mal- NHANES III, with a median of 14.2 years of follow-up, 20.9%
nutrition commonly observed in CKD patients [59]. Lastly, of the participants developed ESRD. The risk of ESRD was asso-
there is a possible link between IR and progression of renal fail- ciated with the dietary acid load tertile, particularly in patients
ure [60]. Alterations in post-insulin receptor signalling path- with albuminuria; in contrast, a diet rich in fruits and vegetables
ways responsible for IR are mediated by the retention of was inversely associated with albuminuria, indirectly suggesting
nitrogenous waste products, oxidative stress, high angiotensin a dampening effect on the progression to ESRD [67].
II levels, metabolic acidosis, vitamin D deficiency and systemic The results of these various studies suggest that fruits and
inflammation. vegetables could represent an effective intervention to correct
Few studies have been performed on the effect of vegetarian metabolic acidosis and the consequences of CKD.
diets on IR in non-diabetic CKD patients, which confirmed an
improved insulin sensitivity by vegetarian diets. After 3 months Hyperphosphataemia. Changes in calcium phosphate me-
on a diet affording 0.3 g/kg/day of plant-based protein associ- tabolism, which are partly linked to a positive phosphorus bal-
ated with a mixture of essential amino acids and ketoanalogues, ance, start early in the course of CKD, favoured by the typical
fasting serum glucose levels, blood glucose levels and endoge- Western-type diet usually rich in dairy products and protein of
nous glucose production were reduced in six patients with CKD animal sources and often worsened by food additives [68]. The
Stages 4–5 [61]. resulting hyperphosphataemia and the linked compensatory
secondary hyperparathyroidism and increase in fibroblast
Metabolic acidosis. Metabolic acidosis, which is observed in growth factor 23 (FGF-23) are associated with progression of
the majority of CKD patients when the GFR decreases to <30% renal disease, vascular calcification and mortality.

Vegetarianism and CKD 203

 Uraemic
Fibres

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

FIGURE 1: Hypothesized effects of a vegetarian diet and its components on CKD. AGEs, advanced glycation end-products; FGF23, fibroblast
growth factor 23; IS, indoxyl sulphate; LPS, lipopolysaccharide; PCS, p-cresyl sulphate; P/S ratio FA, polyunsaturated/saturated ratio of fatty acids;
TMAO, triméthylamine-N-oxyde.

Dietary control of phosphate intake should not be limited to unprocessed foods, since it is almost completely absorbed in the
the phosphate content in foods, but the source of phosphorus intestinal tract.
should also be considered. While phosphates derived from ani-
mal sources are easily hydrolyzed and absorbed, phosphate bio- Effect of vegetarian diets on nutritional status, renal
availability from plants is relatively low in humans, because function and risk of all-cause mortality in patients with
phosphorus from plant-derived proteins is bound in larger mol- CKD
ecules, such as phytates, which cannot be broken down in the An often raised problem concerns nutritional tolerance of
digestive tract due to the absence of human phytase activity. vegetarian diets in CKD patients, especially since plant-based
The intestinal absorption of dietary phosphorus, which is close diets are normally associated with lower energy and protein in-
to 70% in meat eaters, does not exceed 30–40% in vegetarians take than omnivorous diets. In fact, several studies have con-
[69]. Moe et al. [70] reported that in CKD patients not yet on firmed that, similar to vegetarians with normal renal function,
dialysis treatment, despite equivalent energy, protein and phos- CKD patients on a vegetarian diet maintained a good nutri-
phorus intake, a vegetarian diet, compared with a meat diet, tional status at any stage of CKD [74], including patients on
was associated with a significant reduction in serum phospho- maintenance HD treatment [75]. A favourable consensus seems
rus and FGF-23 levels and a decrease in 24-h urinary phospho- to emerge from various studies on the nutritional tolerance of
rus excretion. Similar results have been reported in CKD plant-based diets in CKD patients, provided these diets supply
patients on a very-low-protein diet supplemented with ketoana- adequate energy in the normal to high range (30–35 kcal/kg/
logues, which is in fact a vegetarian diet [71]. Lastly, even if not day). Even without being on a strict vegetarian diet, the inclu-
strictly vegetarian, consumption of a greater percentage of sion of a greater amount of protein from plant-based sources
plant-based proteins is associated with lower FGF-23 levels [72]. (60–70%) in a conventional low-protein diet (0.6 g/kg/day)
Food additives represent another source of phosphorus that brings many benefits to CKD patients—such a diet results in
must also be taken into consideration in the estimation of die- higher energy intake because its greater palatability allows to
tary phosphorus. Phosphorus intake is also reduced in vegeta- add more calories to foods derived from plants, provides a
rians because their diet is almost free of phosphorus-containing more positive nitrogen balance, higher serum bicarbonate levels
food additives that are currently added to a large number of and more stable renal function and improves compliance, appe-
processed foods, particularly meat and poultry. The ‘enhance- tite and well-being [76].
ment’ of fresh meat and poultry products with phosphorus- Plant-based diets have a kidney-protective effect, and several
containing food additives increases the phosphorus content of observational studies have confirmed that healthy dietary pat-
these samples by 7–100% [73]. Lastly, phosphorus in food addi- terns usually rich in fruits, vegetables, legumes and whole grains
tives has a higher availability than phosphorus contained in and low in red meat, saturated fat, refined sugars and processed

204 P. Chauveau et al.

foods are more protective than usual diets in the primary pre- in agreement with a recent meta-analysis of seven cohort stud-
vention of CKD. ies including 15 285 adults with CKD. Healthy dietary patterns
These points are well summarized in the ARIC Study, which (i.e. higher content of fruits and vegetables, fish, legumes, cere-
is a large longitudinal observational study including almost als, whole grains and fibre and lower content of red meat, salt
12 000 adults with normal renal function at baseline. The pri- and refined sugars) were associated with a reduced risk of all-
mary endpoint was incident CKD Stage 3 (defined as an eGFR cause mortality [77].
<60 mL/min/1.73 m2, accompanied by a decrease in eGFR
>25% from baseline) occurring during a median follow-up of CONCLUSION
23 years. To assess the association between dietary protein sour- To confirm these interesting but scattered data, additional stud-
ces and the incidence of CKD Stage 3, patients were divided ies are needed, first to assess the prevalence of CKD in vegetar-
into quintiles of dietary food and protein intake. A total of 2 632 ian populations, second to evaluate, through large-scale
cases of incident CKD Stage 3 were observed during follow-up. randomized controlled trials, the benefits of plant-based diets
There was no significant association between total protein con- for their potential inclusion in clinical recommendations for the
sumption and incident CKD Stage 3; however, there was a sig- prevention and management of CKD.
nificantly higher risk of incident CKD in individuals

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

consuming more proteins from red and processed meat [hazard
ratio (HR) 1.23; P <0.01]. On the other hand, proteins from CONFLICT OF INTEREST STATEMENT
vegetable and dairy sources were found to be protective and None declared. This paper has not been published previously or
participants consuming the highest quintile of vegetable protein submitted to another journal.
had a reduced risk of incident CKD compared with individuals
with the lowest intake (HR 0.76; P <0.002). Lastly, substituting
one serving per day of red and processed meat for one serving REFERENCES
of low-fat dairy products, nuts or legumes was associated with a 1. Pettersen BJ, Anousheh R, Fan J et al. Vegetarian diets and blood pressure
lower risk of incident CKD. The authors concluded that there among white subjects: results from the Adventist Health Study-2 (AHS-2).
Public Health Nutr 2012; 15: 1909–1916
was an association between the development of CKD and the 2. Tonstad S, Butler T, Yan R et al. Type of vegetarian diet, body weight, and
type of dietary protein sources rather than the total protein in- prevalence of type 2 diabetes. Diabetes Care 2009; 32: 791–796
take [10]. 3. Orlich MJ, Fraser GE. Vegetarian diets in the Adventist Health Study 2: a re-
With regard to the effect of plant-based diets on the risk of view of initial published findings. Am J Clin Nutr 2014; 100: 353S–358S
incident ESRD, results available to date are not unanimous. 4. Sabaté J, Wien M. A perspective on vegetarian dietary patterns and risk of
metabolic syndrome. Br J Nutr 2015; 113: S136–S143
While some studies have reported such diets to be protective 5. Beilin LJ, Rouse IL, Armstrong BK et al. Vegetarian diet and blood pressure
against the risk of incident ESRD [11], this effect has not been levels: incidental or causal association? Am J Clin Nutr 1988; 48: 806–810
found in two recent studies [77, 78]. 6. Patel KP, Luo FJG, Plummer NS et al. The production of p-cresol sulfate
Regarding the mortality rate, it is widely recognized that in and indoxyl sulfate in vegetarians versus omnivores. Clin J Am Soc Nephrol
the general population, adherence to plant-based diets is associ- 2012; 7: 982–988
7. Haghighatdoost F, Bellissimo N, Totosy de Zepetnek JO, Rouhani MH.
ated with significantly increased longevity. This point is well il- Association of vegetarian diet with inflammatory biomarkers: a systematic
lustrated in a multi-adjusted analysis including 73 308 Seventh- review and meta-analysis of observational studies. Public Health Nutr 2017;
day Adventists recruited between 2002 and 2007 and compris- 20: 2713–2721
ing 48.2% of non-vegetarians and 51.8% of those on different 8. Kim MK, Cho SW, Park YK. Long-term vegetarians have low oxidative
vegetarian dietary patterns. During a mean follow-up period of stress, body fat, and cholesterol levels. Nutr Res Pract 2012; 6: 155–161
9. Chiu Y-F, Hsu C-C, Chiu THT et al. Cross-sectional and longitudinal com-
almost 6.0 years, there were 2570 deaths, with an overall mortal- parisons of metabolic profiles between vegetarian and non-vegetarian sub-
ity rate of 6.05 per 1000 person-years. Vegetarians had 0.88 jects: a matched cohort study. Br J Nutr 2015; 114: 1313–1320
times the risk of all-cause mortality and 0.48 times the risk of 10. Haring B, Selvin E, Liang M et al. Dietary protein sources and risk for inci-
renal mortality compared with non-vegetarians [79]. dent chronic kidney disease: results from the Atherosclerosis Risk in
Similar findings were reported in several other studies that Communities (ARIC) Study. J Ren Nutr 2017; 27: 233–242
11. Kelly JT, Carrero JJ. Dietary sources of protein and chronic kidney disease
focused on the effect of plant-based diets on the risk of all-cause progression: the proof may be in the pattern. J Ren Nutr 2017; 27: 221–224
mortality in CKD patients. In the recent NHANES III study 12. Mariotti FPD. Vegetarian and Plant-Based Diets in Health and Disease
comprising a cohort of 14 866 participants stratified by eGFRs Prevention. London: Academic Press, 2017, pp. 4–6
<60 or >60 mL/min/1.73 m2, the mean total protein intake and 13. Sacks FM, Kass EH. Low blood pressure in vegetarians: effects of specific
plant protein:total protein ratio estimated from 24-h dietary foods and nutrients. Am J Clin Nutr 1988; 48: 795–800
14. Fraser G, Katuli S, Anousheh R et al. Vegetarian diets and cardiovascular
recalls were 24.6 6 13.2 g/day and 33.0 6 14%, respectively. risk factors in black members of the Adventist Health Study-2. Public
During an average follow-up of 8.4 years, there were 2163 Health Nutr 2015; 18: 537–545
deaths (14.6%). In the subgroup of patients with eGFR 15. Yokoyama Y, Nishimura K, Barnard ND et al. Vegetarian diets and blood
<60 mL/min/1.73 m2, each 33% increase in the plant protein:- pressure: a meta-analysis. JAMA Intern Med 2014; 174: 577–587
total protein ratio was associated with a lower mortality risk 16. Fraser GE. Vegetarian diets: what do we know of their effects on common
chronic diseases? Am J Clin Nutr 2009; 89: 1607S–1612S
(HR 0.77). These data suggest that in CKD patients, at a given 17. Mozaffarian D, Hao T, Rimm EB et al. Changes in diet and lifestyle and
total protein intake, a diet with a higher proportion of vegetal long-term weight gain in women and men. N Engl J Med 2011; 364:
protein is associated with lower mortality [80]. These results are 2392–2404

Vegetarianism and CKD 205

18. Barnard ND, Levin SM, Yokoyama Y. A systematic review and meta- renal insufficiency and mortality risk in chronic kidney disease. Circ Res
analysis of changes in body weight in clinical trials of vegetarian diets. 2015; 116: 448–455
J Acad Nutr Diet 2015; 115: 954–969 44. Mafra D, Fouque D. Gut microbiota and inflammation in chronic kidney
19. Farmer B. Nutritional adequacy of plant-based diets for weight manage- disease patients. Clin Kidney J 2015; 8: 332–334
ment: observations from the NHANES. Am J Clin Nutr 2014; 100: 45. Ramezani A, Raj DS. The gut microbiome, kidney disease, and targeted
365S–368S interventions. J Am Soc Nephrol 2014; 25: 657–670
20. Mak RH. 1,25-dihydroxyvitamin D3 corrects insulin and lipid abnormalities 46. Cavicchia PP, Steck SE, Hurley TG et al. A new dietary inflammatory index
in uremia. Kidney Int 1998; 53: 1353–1357 predicts interval changes in serum high-sensitivity C-reactive protein.
21. Appel LJ, Moore TJ, Obarzanek E et al. A clinical trial of the effects of die- J Nutr 2009; 139: 2365–2372
tary patterns on blood pressure. N Engl J Med 1997; 336: 1117–1124 47. Donohoe DR, Garge N, Zhang X et al. The microbiome and butyrate regu-
22. St-Jules DE, Goldfarb DS, Sevick MA. Nutrient non-equivalence: does late energy metabolism and autophagy in the mammalian colon. Cell Metab
restricting high-potassium plant foods help to prevent hyperkalemia in he- 2011; 13: 517–526
modialysis patients? J Ren Nutr 2016; 26: 282–287 48. Ajani UA, Ford ES, Mokdad AH. Dietary fiber and C-reactive protein: find-
23. Aljuraiban GS, Griep LMO, Chan Q et al. Total, insoluble and soluble die- ings from national health and nutrition examination survey data. J Nutr
tary fibre intake in relation to blood pressure: the INTERMAP Study – 2004; 134: 1181–1185
CORRIGENDUM. Br J Nutr 2015; 114: 1480 49. Yang Y, Zhao L-G, Wu Q-J et al. Association between dietary fiber and
24. Whelton SP, Hyre AD, Pedersen B et al. Effect of dietary fiber intake on lower risk of all-cause mortality: a meta-analysis of cohort studies. Am J
blood pressure: a meta-analysis of randomized, controlled clinical trials. Epidemiol 2015; 181: 83–91

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

J Hypertens 2005; 23: 475–481 50. Barbier de La Serre C, Ellis CL, Lee J et al. Propensity to high-fat diet-in-
25. Wang YF, Yancy WS, Yu D et al. The relationship between dietary protein duced obesity in rats is associated with changes in the gut microbiota and
intake and blood pressure: results from the PREMIER study. J Hum gut inflammation. Am J Physiol Gastrointest Liver Physiol 2010; 299:
Hypertens 2008; 22: 745–754 G440–G448
26. He J, Streiffer RH, Muntner P, Krousel-Wood MA, Whelton PK. Effect of 51. Krishnamurthy VMR, Wei G, Baird BC et al. High dietary fiber intake is as-
dietary fiber intake on blood pressure: a randomized, double-blind, placebo- sociated with decreased inflammation and all-cause mortality in patients
controlled trial. J Hypertens 2004; 22: 73–80 with chronic kidney disease. Kidney Int 2012; 81: 300–306
27. Craig WJ. Nutrition concerns and health effects of vegetarian diets. Nutr 52. Szeto YT, Kwok TCY, Benzie IFF. Effects of a long-term vegetarian diet on
Clin Pract 2010; 25: 613–620 biomarkers of antioxidant status and cardiovascular disease risk. Nutrition
28. Montalcini T, De Bonis D, Ferro Y et al. High vegetable fats intake is associ- 2004; 20: 863–866
ated with high resting energy expenditure in vegetarians. Nutrients 2015; 7: 53. Krajcovicová-Kudlácková M, Valachovicová M, Pauková V, Dusinská M.
5933–5947 Effects of diet and age on oxidative damage products in healthy subjects.
29. Appel LJ, Brands MW, Daniels SR et al. Dietary approaches to prevent and Physiol Res 2008; 57: 647–651
treat hypertension: a scientific statement from the American Heart 54. Del Vecchio L, Locatelli F, Carini M. What we know about oxidative stress
Association. Hypertension 2006; 47: 296–308 in patients with chronic kidney disease on dialysis-clinical effects, potential
30. Altorf-van der Kuil W, Engberink MF, Brink EJ et al. Dietary protein and treatment, and prevention. Semin Dial 2011; 24: 56–64
blood pressure: a systematic review. PLoS One 2010; 5: e12102 55. Dounousi E, Papavasiliou E, Makedou A et al. Oxidative stress is progres-
31. Rebholz CM, Friedman EE, Powers LJ et al. Dietary protein intake and sively enhanced with advancing stages of CKD. Am J Kidney Dis 2006; 48:
blood pressure: a meta-analysis of randomized controlled trials. Am J 752–760
Epidemiol 2012; 176: S27–S43 56. Massy ZA, Stenvinkel P, Drüeke TB. The role of oxidative stress in chronic
32. Teunissen-Beekman KFM, van Baak MA. The role of dietary protein in kidney disease. Semin Dial 2009; 22: 405–408
blood pressure regulation. Curr Opin Lipidol 2013; 24: 65–70 57. Jun M, Venkataraman V, Razavian M et al. Antioxidants for chronic kidney
33. Kuo C-S, Lai N-S, Ho L-T et al. Insulin sensitivity in Chinese ovo- disease. Cochrane Database Syst Rev 2012; 10: CD008176
lactovegetarians compared with omnivores. Eur J Clin Nutr 2004; 58: 58. Shinohara K, Shoji T, Emoto M et al. Insulin resistance as an independent
312–316 predictor of cardiovascular mortality in patients with end-stage renal dis-
34. Yokoyama Y, Barnard ND, Levin SM et al. Vegetarian diets and glycemic ease. J Am Soc Nephrol 2002; 13: 1894–1900
control in diabetes: a systematic review and meta-analysis. Cardiovasc 59. Siew ED, Pupim LB, Majchrzak KM et al. Insulin resistance is associated
Diagn Ther 2014; 4: 373–382 with skeletal muscle protein breakdown in non-diabetic chronic hemodialy-
35. Kontessis PA, Bossinakou I, Sarika L et al. Renal, metabolic, and hormonal sis patients. Kidney Int 2007; 71: 146–152
responses to proteins of different origin in normotensive, nonproteinuric 60. Kaartinen K, Syrjänen J, Pörsti I et al. Insulin resistance and the progression
type I diabetic patients. Diabetes Care 1995; 18: 1233 of IgA glomerulonephritis. Nephrol Dial Transplant 2007; 22: 778–783
36. Kahleova H, Levin S, Barnard N. Cardio-metabolic benefits of plant-based 61. Rigalleau V, Combe C, Blanchetier V et al. Low protein diet in uremia:
diets. Nutrients 2017; 9: 848 effects on glucose metabolism and energy production rate. Kidney Int 1997;
37. Kurella M, Lo JC, Chertow GM. Metabolic syndrome and the risk for 51: 1222–1227
chronic kidney disease among nondiabetic adults. J Am Soc Nephrol 2005; 62. De Brito-Ashurst I, Varagunam M, Raftery MJ et al. Bicarbonate supple-
16: 2134–2140 mentation slows progression of CKD and improves nutritional status. J Am
38. Evenepoel P, Meijers BKI, Bammens BRM et al. Uremic toxins originating Soc Nephrol 2009; 20: 2075–2084
from colonic microbial metabolism. Kidney Int Suppl 2009; 76: S12–S19 63. Ausman LM, Oliver LM, Goldin BR et al. Estimated net acid excretion in-
39. Chao C-T, Chiang C-K. Uremic toxins, oxidative stress, and renal fibrosis: versely correlates with urine pH in vegans, lacto-ovo vegetarians, and omni-
an interwined complex. J Ren Nutr 2015; 25: 155–159 vores. J Ren Nutr 2008; 18: 456–465
40. Koppe L, Pillon NJ, Vella RE et al. p-Cresyl sulfate promotes insulin resis- 64. Goraya N, Simoni J, Jo C, Wesson DE. Dietary acid reduction with fruits
tance associated with CKD. J Am Soc Nephrol 2013; 24: 88–99 and vegetables or bicarbonate attenuates kidney injury in patients with a
41. Sirich TL, Plummer NS, Gardner CD et al. Effect of increasing dietary fiber moderately reduced glomerular filtration rate due to hypertensive nephrop-
on plasma levels of colon-derived solutes in hemodialysis patients. Clin J athy. Kidney Int 2012; 81: 86–93
Am Soc Nephrol 2014; 9: 1603–1610 65. Rebholz CM, Coresh J, Grams ME et al. Dietary acid load and incident
42. Marzocco S, Dal Piaz F, Di Micco L et al. Very low protein diet reduces chronic kidney disease: results from the ARIC study. Am J Nephrol 2015;
indoxyl sulfate levels in chronic kidney disease. Blood Purif 2013; 35: 42: 427–435
196–201 66. Wesson DE, Simoni J. Acid retention during kidney failure induces endo-
43. Tang WHW, Wang Z, Kennedy DJ et al. Gut microbiota-dependent trime- thelin and aldosterone production which lead to progressive GFR decline, a
thylamine N-oxide (TMAO) pathway contributes to both development of situation ameliorated by alkali diet. Kidney Int 2010; 78: 1128–1135

206 P. Chauveau et al.

67. Banerjee T, Crews DC, Wesson DE et al. High dietary acid load predicts 74. Chauveau P, Combe C, Fouque D, Aparicio M. Vegetarianism: advantages
ESRD among adults with CKD. J Am Soc Nephrol 2015; 26: 1693–1700 and drawbacks in patients with chronic kidney diseases. J Ren Nutr 2013;
68. Gutiérrez OM, Luzuriaga-McPherson A, Lin Y et al. Impact of phosphorus- 23: 399–405
based food additives on bone and mineral metabolism. J Clin Endocrinol 75. Wu T-T, Chang C-Y, Hsu W-M et al. Nutritional status of vegetarians on
Metab 2015; 100: 4264–4271 maintenance haemodialysis. Nephrology 2011; 16: 582–587
69. Kalantar-Zadeh K, Gutekunst L, Mehrotra R et al. Understanding sources 76. Passey C. Reducing the dietary acid load: how a more alkaline diet benefits
of dietary phosphorus in the treatment of patients with chronic kidney dis- patients with chronic kidney disease. J Ren Nutr 2017; 27: 151–160
ease. Clin J Am Soc Nephrol 2010; 5: 519–530 77. Kelly JT, Palmer SC, Wai SN et al. Healthy dietary patterns and risk of mor-
70. Moe SM, Zidehsarai MP, Chambers MA et al. Vegetarian compared with tality and ESRD in CKD: a meta-analysis of cohort studies. Clin J Am Soc
meat dietary protein source and phosphorus homeostasis in chronic kidney Nephrol 2017; 12: 272–279
disease. Clin J Am Soc Nephrol 2011; 6: 257–264 78. Gutiérrez OM, Muntner P, Rizk DV et al. Dietary patterns and risk of death
71. Di Iorio B, Di Micco L, Torraca S et al. Acute effects of very-low-protein diet and progression to ESRD in individuals with CKD: a cohort study. Am J
on FGF23 levels: a randomized study. Clin J Am Soc Nephrol 2012; 7: 581–587 Kidney Dis 2014; 64: 204–213
72. Scialla JJ, Appel LJ, Wolf M et al. Plant protein intake is associated with fi- 79. Orlich MJ, Singh PN, Sabaté J et al. Vegetarian dietary patterns and mortal-
broblast growth factor 23 and serum bicarbonate levels in patients with ity in Adventist Health Study 2. JAMA Intern Med 2013; 173: 1230
chronic kidney disease: the Chronic Renal Insufficiency Cohort study. J Ren 80. Chen X, Wei G, Jalili T et al. The associations of plant protein intake with
Nutr 2012; 22: 379e1–388e1 all-cause mortality in CKD. Am J Kidney Dis 2016; 67: 423–430
73. Sherman RA, Mehta O. Phosphorus and potassium content of enhanced

Downloaded from https://academic.oup.com/ndt/article/34/2/199/5049714 by guest on 21 June 2023

meat and poultry products: implications for patients who receive dialysis. Received: 5.11.2017; Editorial decision: 26.4.2018
Clin J Am Soc Nephrol 2009; 4: 1370–1373

Vegetarianism and CKD 207