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Plant-based diets to manage the risks and complications of chronic kidney disease
Carrero, Juan J.; Gonzalez-Ortiz, Ailema; Avesani, Carla M.; Bakker, Stephan J. L.; Bellizzi,
Vincenzo; Chauveau, Philippe; Clase, Catherine M.; Cupisti, Adamasco; Espinosa-Cuevas,
Angeles; Molina, Pablo
Published in:
Nature Reviews Nephrology
DOI:
10.1038/s41581-020-0297-2
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2020
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Citation for published version (APA):
Carrero, J. J., Gonzalez-Ortiz, A., Avesani, C. M., Bakker, S. J. L., Bellizzi, V., Chauveau, P., Clase, C. M.,
Cupisti, A., Espinosa-Cuevas, A., Molina, P., Moreau, K., Piccoli, G. B., Post, A., Sezer, S., & Fouque, D.
(2020). Plant-based diets to manage the risks and complications of chronic kidney disease. Nature
Reviews Nephrology, 16(9), 525-542. https://doi.org/10.1038/s41581-020-0297-2
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Reviews
Plant-based diets to manage the
risks and complications of chronic
kidney disease
1 1,2 3 4
Juan J. Carrero ✉, Ailema González-Ortiz , Carla M. Avesani , Stephan J. L. Bakker ,
5 6 7 8
Vincenzo Bellizzi , Philippe Chauveau , Catherine M. Clase , Adamasco Cupisti ,
2 9 10 11,12
Angeles Espinosa-Cuevas , Pablo Molina , Karine Moreau , Giorgina B. Piccoli ,
4 13 14
Adrian Post , Siren Sezer and Denis Fouque
|
Abstract Traditional dietary recommendations for patients with chronic kidney disease (CKD)
focus on the quantity of nutrients consumed. Without appropriate dietary counselling, these
restrictions can result in a low intake of fruits and vegetables and a lack of diversity in the diet.
Plant nutrients and plantbased diets could have beneficial effects in patients with CKD:
increased fibre intake shifts the gut microbiota towards reduced production of uraemic toxins;
plant fats, particularly olive oil, have antiatherogenic effects; plant anions might mitigate
metabolic acidosis and slow CKD progression; and as plant phosphorus has a lower bioavailability
than animal phosphorus, plantbased diets might enable better control of hyperphosphataemia.
Current evidence suggests that promoting the adoption of plantbased diets has few risks but
potential benefits for the primary prevention of CKD, as well as for delaying progression in
patients with CKD G3–5. These diets might also help to manage and prevent some of the
symptoms and metabolic complications of CKD. We suggest that restriction of plant foods as
a strategy to prevent hyperkalaemia or undernutrition should be individualized to avoid
depriving patients with CKD of these potential beneficial effects of plantbased diets. However,
research is needed to address knowledge gaps, particularly regarding the relevance and extent
of dietinduced hyperkalaemia in patients undergoing dialysis.
The kidneys have a key role in nutritional homeostasis. Dietitians and nephrologists recommend that these
In healthy individuals, sodium, potassium and phosphate patients restrict their intake of phosphorus, potassium,
body content and serum levels are tightly regulated by sodium and fluid, either pre-emptively or in response to
1,2
processes involving the kidneys . The kidneys also reg- clinical or laboratory findings. In addition, they empha-
ulate the amino acid pool via the synthesis, degradation, size the importance of tailoring protein intake according
filtration and reabsorption of dietary amino acids; they to CKD stage and type of kidney replacement therapy
3,4 10–12
are the sole means of excretion of nitrogenous waste ; (KRT), while still ensuring sufficient energy intake .
they metabolize glucose and release glucose via glu- Adherence to these recommendations seems prudent
4,5; and together with the lungs, they reg-
coneogenesis and may be necessary. However, without appropriate
ulate acid–base status6. In addition, the kidneys clear dietary counselling, such restrictions can result in frus-
low-molecular-weight proteins, which constitute a small tration and lack of autonomy. In combination with soci-
fraction of total proteins, but have important roles in etal secular trends (that is, high consumption of meat,
physiology, nutrient homeostasis and muscle growth. For processed foods and fast food), dietary restrictions for
example, immunoglobulin light chains and peptide hor- patients with CKD may result in a diet that lacks variety
13–17
mones, including insulin, growth hormone and leptin, and has a low intake of fruits and vegetables .
7,8. The kidneys also activate Emerging evidence suggests that a focus on the qual-
are cleared by the kidneys
9
✉ vitamin D3 by hydroxylation of calcidiol to calcitriol . ity and diversity of the diet, particularly with liberal
e-mail: juan.jesus.carrero@ As loss of kidney function leads to disruption of consumption of plant foods, may be relevant for the
ki.se nutrient homeostasis, patients with chronic kidney prevention and management of CKD. Here, we evaluate
https://doi.org/10.1038/ disease (CKD) are often advised to change their diet.
s41581-020-0297-2 the strength and consistency of this evidence and discuss
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NA ture revIewS NePHROlOGy volume 16 September 2020 525
Reviews
Mediterranean diet, the Okinawan diet and the
Key points diet, the
healthy-eating diet. We do not discuss weight-control
• the idea that animal protein has ‘high biological value’ is not relevant in the context diets, crash diets, detox diets or belief-based diets,
of a mixed diet and is not an a priori reason to consider plant protein inferior to animal although some of these diets may contain predominantly
protein for people with or without chronic kidney disease (CKD). plant-based foods. As no definition of a plant-based diet
• plants are the only dietary source of fibre, which shifts the gut microbiota profile 18
towards increased production of antiinflammatory compounds and reduced is widely accepted , it is not currently possible to accu-
production of uraemic toxins. rately define how much plant and how little meat a diet
• plant fats, particularly olive oil, are antiinflammatory and antiatherogenic. must contain in order to be plant-based. This lack of a
standard definition limits the practical implementation
• plantbased diets have low net endogenous acid load, which could mitigate metabolic of plant-based diets (discussed further below).
acidosis in patients with CKD and potentially slow the progression of kidney disease. As animal foods have no fibre, high-fibre diets must
• plant phosphorus is bound to phytate and is less bioavailable than animal phosphorus; contain plant foods, but some plants are higher in fibre
consequently, many plantbased foods have a favourable protein to phosphorus ratio. than others. It is therefore possible to achieve a high-fibre
• restriction of plant foods as a strategy to prevent hyperkalaemia deprives patients diet that does not meet our criteria of a plant-based diet,
with CKD of the potential beneficial effects of these foods; plants with low potassium and some plant-based diets might not be high-fibre, par-
content provide choice for those who need to restrict their potassium intake. ticularly if they are rich in highly processed foods. In the
nephrology literature, a low-protein diet is widely under-
Vegan diet the possible benefits and risks of plant-based diets in stood to supply a protein intake of 0.6–0.8 g/kg per day,
A diet that excludes meat, patients with CKD, as well as implementation strategies which is achievable in the context of any of the diets
fish, seafood, eggs and dairy. and knowledge gaps. Whenever possible, we differen- mentioned above.
Vegetarian diets tiate evidence regarding the use of plant-based diets in We consider a good- or high-quality diet to be varied,
Diets that exclude meat, fish primary CKD prevention (public health initiatives) from relatively low in processed foods and rich in fruit and
and seafood, but not eggs evidence in patients with CKD who are not on dialysis vegetables. These criteria are also achievable in the con-
or dairy. and in patients on dialysis. Evidence for potential risks and text of all of the diets discussed above, including omniv-
benefits of plant-based diets in patients with function- orous diets. However, not all plant-based diets are of
Dietary Approaches to Stop ing kidney transplants is indirect; for the most part, we good or high quality; a higher intake of less healthy plant
Hypertension suggest applying information from studies in patients foods, such as potatoes and added sugars, has been asso-
(DASH). A diet that was 19,20
designed to help treat or with CKD who do not require dialysis. We consider ciated with a higher risk of cardiometabolic disease .
prevent hypertension. This diet animal welfare issues and the environmental impact of The concept of a high-quality diet must be distinguished
encourages reduced sodium plant-based diets to be beyond the scope of this review. from the concept of protein quality, which is discussed
consumption and increased further below.
intake of potassium, calcium Definition of a plantbased diet
and magnesium through the In this Review, we define plant-based diets as those Plant proteins
high consumption of fruit,
vegetables, legumes and nuts that emphasize the consumption of plant foods Some guideline recommendations for patients with CKD
and low consumption of meat, (fruit, vegetables, nuts, seeds, oils, whole grains, leg- suggest that at least half of their daily protein intake
fish, seafood, eggs and dairy. umes and beans) and may or may not include small should come from animal sources given their ‘high bio-
or moderate amounts of meat, fish, seafood, eggs logical value’10–12. The aim of these statements may be to
vegan diet is plant-based, as are many essential amino acids are not limiting if dietary
and dairy. A ensure that
vegetarian diets. Other examples of dietary patterns protein levels are reduced. However, the biological value
that align with the concept of plant-based diets are of a protein source is an outdated parameter that quanti-
the Dietary Approaches to Stop Hypertension (DASH) fies the proportion of the nitrogen that, after digestion, is
21
absorbed and retained in the body . Biological value
Author addresses is typically measured in rats on a single-food diet, some-
times after starvation21; however, essential amino acids
1
medical epidemiology and biostatistics, Karolinska Institutet, Stockholm, Sweden. are species-specific and differ between humans and rats.
2
Nephrology and mineral metabolism Department, Instituto Nacional de Ciencias In humans, the biological value of a protein source has
médicas y Nutrición Salvador, Zubirán, mexico. been shown to correlate with the completeness of essen-
3
Clinical Science, Intervention and technology, Karolinska Institutet, Stockholm, Sweden. tial amino acids in the protein source22, leading to con-
4
Department of Internal medicine, university medical Center Groningen, university of flation of the two concepts. The term ‘protein quality’
Groningen, Groningen, the Netherlands.
5 appears to be variably applied to both biological value and
Nephrology unit, university Hospital “San Giovanni di Dio e ruggi d’Aragona”,
Salerno, Italy. completeness of essential amino acids. The idea of scoring
6
Service de Néphrologie transplantation Dialyse, Centre Hospitalier universitaire a protein source on either its ability to be integrated into
de bordeaux et AuradAquitaine, bordeaux, France. other proteins, or its amino acid composition, is irrele-
7
Departments of medicine and Health evidence and Impact, mcmaster university, vant to most human diets in which mixtures of foods are
Hamilton, ontario, Canada. eaten, usually at each meal. The requirement for essential
8
Department of Clinical and experimental medicine, university of pisa, pisa, Italy. amino acids decreases with increasing overall nitrogen
9
Department of Nephrology, Hospital Universitari Dr Peset, Universitat de València, 23
València, Spain. intake , which further diminishes the usefulness of the
10 concept of the ‘completeness’ of the essential amino acid
renal transplant unit, pellegrin Hospital, bordeaux, France. profile of a particular dietary source. Different foods are
11
Department of Clinical and biological Sciences, university of torino, torino, Italy.
12 better or worse sources of individual essential amino
Nephrologie, Centre Hospitalier le mans, le mans, France.
13 acids, but because of complementarity, few natural diets
Department of Nephrology, baskent university School of medicine, Ankara, turkey.
14
Department of Nephrology, université de lyon, Carmen, Hospital lyonSud, lyon, France. provide insufficient amounts of essential amino acids,
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526 September 2020 volume 16 www.nature.com/nrneph
Reviews
23
Mediterranean diet except in infants and pre-school children . Although 14 trials of controlled feeding found that fibre supple-
A traditional diet from plant and animal proteins differ in their amino acid pro- mentation consistently reduced serum urea and cre-
countries surrounding the 24 44
files, digestibility and availability , these differences do atinine levels . In observational studies of the general
Mediterranean sea that not seem to be clinically relevant for the general popu- population, higher consumption of fibre was associated
emphasizes large numbers 25–28
of servings of fruit, vegetables, lation in the context of a varied and sufficient diet . with higher estimated glomerular filtration rate (eGFR)
45–48
legumes, nuts, olive oil and We were unable to identify any outcome-based studies and a lower risk of developing CKD .
fish, and low numbers of in patients with CKD to support recommendations for In patients with CKD, high fibre intake has been asso-
servings of meat, seafood, the inclusion of ‘high biological value’ foods in the diet. ciated with a lower risk of inflammation and mortality,
eggs, dairy and processed food Various observational studies have evaluated sources with an effect size that may be greater than that in people
(including bread and pastries). 46,49
of dietary protein and the risk of developing CKD. without CKD . In patients undergoing dialysis, low
Okinawan diet A higher intake of vegetable protein was associated fibre intake was associated with higher concentrations of
A traditional diet from the 50–52, myocardial hypertrophy
with a lower prevalence of CKD in patients with type 2 inflammatory biomarkers
island of Okinawa in Japan, diabetes mellitus29 and a lower risk of developing CKD and arterial stiffness51,52, and a higher risk of cardiovas-
which has a population with 30. In the latter study, the risk 52,53. Among kidney transplant
exceptional longevity. This in the general population cular events and death
diet is low in calories and fat associations with protein intake differed according to recipients, those with the highest tertile of fibre intake
and high in carbohydrates. food group; those who consumed more protein from red had the lowest incidence of metabolic syndrome in the
it emphasizes vegetables 54
and processed meats were at an increased risk of devel- first year after kidney transplantation .
and soy products alongside oping CKD, whereas CKD risk was lower among those A number of interventional studies have explored the
occasional, and small, amounts who had a higher consumption of nuts and legumes. potential benefits of fibre consumption in people with
of noodles, rice, pork and fish. Substituting one serving of red meat in the diet with CKD. In a small randomized controlled trial (RCT) in
Healthy eating diet one serving of legumes was estimated to reduce the risk patients on haemodialysis, increased dietary fibre intake
A diet that exemplifies of incident CKD by 31% (HR 0.69; 95% CI 0.57–0.83)30. for 6 weeks resulted in a significant reduction in the
the US recommended dietary Furthermore, among National Health and Nutrition plasma level of the uraemic toxin indoxyl sulfate and a
targets 2015–2020. This diet Examination Survey participants with CKD who were non-significant reduction in the level of another urae-
emphasizes fruits, vegetables,
55
whole grains and fat-free or not on dialysis, diets with a higher proportion of protein mic toxin, p-cresol sulfate . Another study in patients
low-fat milk and milk products. from plant sources were associated with lower mortal- on haemodialysis showed that compared with placebo,
it includes lean meats, poultry, ity31. It is plausible that plant protein offers advantages 6 weeks of dietary fermentable fibre supplementation
fish, beans, eggs and nuts. it is 32
low in saturated fats, trans fats, over animal protein in patients with CKD , but this improved lipid profile and oxidative status and decreased
56
cholesterol, salt (sodium) and hypothesis has not been extensively investigated. Studies systemic inflammation . Fibre supplementation studies
added sugars, and stays within 57
(ref. ) have reported similar
in obese rats showed that consumption of soya protein in patients with CKD G3–5
daily calorie needs. can reduce the expression of renin–angiotensin-system- reductions in plasma p-cresol concentration, as well as
57,58
Essential amino acids and angiogenesis-related genes, resulting in lower lev- improved stool frequency .
Amino acids that cannot be els of angiotensin I and II in adipose tissue33. Whether The gut microbiota may mediate some of the sal-
synthesized by an organism similar effects are observed in the kidney is not known. utary effects of a diet rich in fibre (fig. 1). As some
from other nitrogen sources. However, animal studies have found that higher con- microbial species are only able to utilize specific sub-
sumption of plant protein retards the development and strates derived from either dietary protein or fibre to
34
progression of CKD . Early mechanistic studies sug- expand their populations, the ratio of protein to fibre
gested that differences in amino acid intake, particu- intake modulates the fermentation processes medi-
larly of glycine and alanine, which are both abundant ated by the gut microbiota. Saccharolytic bacteria (also
in plant proteins, have different effects on kidney hae- called symbiotic bacteria) ferment dietary fibre, which
35–38
modynamics , suggesting a potential mechanism for releases short-chain fatty acids (e.g. acetate, butyrate or
these beneficial effects. In a seminal study in which ten propionate) that enhance gut barrier integrity and have
healthy volunteers consumed equivalent amounts of ani- anti-inflammatory and immunomodulatory effects46,49.
mal or plant protein for 3 weeks, consumption of plant By contrast, proteolytic bacteria ferment dietary pro-
protein resulted in reduced renal plasma flow, increased tein, which leads to the production of several uraemic
renal vascular resistance and lower fractional clearance toxins (e.g. indoxyl sulfate, indole-3 acetic acid, p-cresyl
37
of albumin or IgG . sulfate and trimethylamine N-oxide) that are absorbed
into the bloodstream and removed by the kidneys in
Plant carbohydrates 59–61,
people with normal glomerular filtration rate (GFR)
Plant-based diets are rich in carbohydrates, both mono- but accumulate in people with low GFR and have been
saccharides (glucose, fructose) and polysaccharides shown to exert toxic effects in experimental systems62.
39
(starch and fibre) . Starch is an important source of A large number of putative uraemic toxins exist, but
energy in modern diets, whereas dietary fibre is com- how their known specific toxicities translate into the
posed of non-digestible and non-absorbable carbohy- fatigue, anorexia, nausea, itching, myopathy, neurop-
drate polymers that influence the diversity of the gut athy, serositis and encephalopathy that are collectively
40
microbiota and the synthesis of metabolites . In the recognized clinically as the uremic syndrome is not well
general population, increased fibre consumption has understood. Furthermore, some uraemic toxins may
been consistently associated with lower levels of blood cause more rapid progression of CKD. For example,
lipids, particularly total cholesterol, and body weight indoxyl sulfate increases the expression of fibrogenic
41,42
reduction (TAble 1). genes, such as transforming growth factor beta, that
Dietary fibre increases faecal bacterial mass and increase fibrogenesis, a key pathway in the progressive
43 63
nitrogen excretion in humans . A meta-analysis of loss of GFR .
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