Next Article in Journal
The Dose-Effects of Caffeine on Lower Body Maximal Strength, Muscular Endurance, and Rating of Perceived Exertion in Strength-Trained Females
Previous Article in Journal
Preference, Expected Burden, and Willingness to Use Digital and Traditional Methods to Assess Food and Alcohol Intake
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Nutrients
Volume 13
Issue 10
10.3390/nu13103341
nutrients-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Nutritional Adequacy of Animal-Based and Plant-Based Asian Diets for Chronic Kidney Disease Patients: A Modeling Study

by
Ban-Hock Khor
1,
Dina A. Tallman
2,3,
Tilakavati Karupaiah
4,
Pramod Khosla
2,
Maria Chan
5 and
Joel D. Kopple
6,7,*
1
Faculty of Food Science and Nutrition, Universiti Malaysia Sabah, Kota Kinabalu 56000, Sabah, Malaysia
2
Department of Nutrition and Food Science, Wayne State University, Detroit, MI 48202, USA
3
US Food and Drug Administration, Detroit, MI 48207, USA
4
School of Biosciences, Faculty of Health and Medical Sciences, Taylor’s University, Subang Jaya 47500, Selangor, Malaysia
5
Departments of Renal Medicine and Nutrition and Dietetics, The St. George Hospital, Kogarah, NSW 2217, Australia
6
Harbor-UCLA Medical Center, The Lundquist Institute, Torrance, CA 90502, USA
7
David Geffen School of Medicine at UCLA and UCLA Fielding School of Public Health, Los Angeles, CA 90095, USA
*
Author to whom correspondence should be addressed.
Nutrients 2021, 13(10), 3341; https://doi.org/10.3390/nu13103341
Submission received: 31 August 2021 / Revised: 21 September 2021 / Accepted: 21 September 2021 / Published: 24 September 2021
(This article belongs to the Section Nutrition and Public Health)
Browse Figures
Versions Notes

Abstract

:
Plant-based low protein diets (LPDs) have gained popularity for managing chronic kidney disease (CKD) patients. The nutritional adequacy of these and other LPDs prescribed for CKD patients have not been carefully examined. This study assessed the nutrient composition of such LPDs and moderately high protein diets (MHPDs) that might be prescribed for patients in the Asia Pacific region with CKD who are not dialyzed or undergoing maintenance dialysis. Conventional diets containing at least 50% animal-based proteins and plant-based diets were also planned with protein prescriptions of 0.5 to 0.8 g/kg/day and MHPDs with protein prescriptions of 1.0 to 1.2 g/kg/day. Plant-based, lacto-, ovo-, and lacto-ovo-vegetarian and vegan LPDs and MHPDs were planned by replacing some or all of the animal proteins from the conventional diet. With 0.5 g protein/kg/day, all diets were below the Recommended Dietary Allowances (RDA) for at least one essential amino acid (EAA). At a protein prescription of 0.6 g/kg/day, only the conventional LPD met the RDA for all EAAs. This deficiency with the plant-based LPDs persisted even with several plant food substitutions. With a protein prescription ≥0.7 g/kg/day, all the plant-based and vegetarian LPDs provided the RDA for all EAA. The plant-based and vegetarian diets also contained relatively greater potassium, phosphorus, and calcium content but lower long-chain n-3 polyunsaturated fatty acids and vitamin B-12 than the conventional diet. Other essential micronutrients were commonly below the RDA even at higher protein intakes. The low contents of some essential micronutrients were found in both animal-based and plant-based diets. Prescription of all LPDs for CKD patients, especially plant-based and vegetarian LPDs, requires careful planning to ensure the adequacy of all nutrients, particularly essential amino acids. Consideration should be given to supplementing all animal-based and plant-based LPDs and MHPDs with multivitamins and certain trace elements.

1. Introduction

Chronic kidney disease (CKD) is a global health concern. A recent systematic analysis estimates that 9.1% of the worldwide adult population is affected by CKD, and almost a third of people with CKD live in China and India [1]. A low protein diet (LPD) providing 0.6 to 0.8 g protein per kg body weight has been recommended for patients with non-dialysis dependent CKD stages 3 to 5 since protein restriction engenders a reduction of proteinuria and decreases the generation of protein-derived toxins, including acid, other metabolites and phosphate [2,3]. Contrarily, a greater amount of protein (1.0–1.2 g/kg) is recommended for CKD patients undergoing maintenance dialysis to compensate for the increase in protein catabolism as well as protein, peptide, and amino acid losses into the dialysate that occur during dialysis treatments [3,4].
Recently, vegetarian and plant-based diets have been proposed as part of healthier and more environmentally sustainable eating patterns. Although the terms “vegetarian diet” and “plant-based diet” are often used interchangeably, they represent two different eating patterns. Vegetarian diets eliminate flesh foods, including meat, poultry, wild game, and seafood, while their products, such as eggs and milk, may be excluded [5]. Contrarily, plant-based diets emphasize consuming foods mainly from plants, such as fruit, vegetables, nuts, healthy oils, whole grains, and legumes, with the inclusion of small quantities of animal-based food sources, including milk, eggs, meat, and fish [6]. A growing body of epidemiological evidence supports the recommendation of plant-based and vegetarian diets to prevent and treat certain nutrition-related chronic diseases such as obesity, type 2 diabetes, hypertension, cardiovascular diseases, and some cancers [5,7]. A number of reports suggest that plant-based foods may be associated with favorable effects on CKD patients with regard to blood pressure, phosphorus burden, acid load, uremic toxins, inflammation, and oxidative stress [8,9,10,11,12,13,14]. However, these purported benefits have largely not yet been confirmed in randomized prospective controlled clinical trials with clinical outcomes as the key outcome measures.
Since plant proteins are more likely to contain lower amounts of certain essential amino acids (EAAs), especially lysine and the sulfur-containing amino acids [15], as well as lesser quantities of some micronutrients [5], it has been questioned as to whether these plant-based LPDs may be deficient in some essential nutrients. A few interventional studies from Italy [16,17] and Israel [18] did not describe an increased prevalence of protein-energy wasting or malnutrition in non-dialyzed CKD patients prescribed vegetarian LPDs ranging from 0.7 to 0.75 g protein per kg body weight. However, the assessment of nutritional status performed in these studies only included body weight and various serum protein markers, whereas the patients’ amino acid, vitamin, mineral, and trace element status were not evaluated. These latter reports also did not carefully track the actual nutrient intake of the CKD patients that were studied. On the other hand, an observational study in Taiwan reported that lacto-ovo vegetarians with CKD had a lower dietary energy and protein intakes and lower body mass index than their omnivore counterparts [19]. The self-reported dietary protein intake of these latter patients ranged from 0.79 to 0.92 g per kg body weight. Thus, although diets providing as low as 0.6 g protein/kg/day are recommended, there is very little information concerning the adequacy of essential nutrients, including the EAAs, of vegetarian or plant-based LPDs providing 0.5 to 0.6 g protein per kg body weight.
Vegetarianism has a long tradition in Indian cultures due at least partly to religious interdictions against taking living creatures’ lives [20]. At present, about 40% of India’s population traditionally adheres to vegetarian diets, which primarily include fermented milk (i.e., curds), lentils, and fresh sprouting seeds such as green gram/mung bean as the protein source [20]. Similarly, vegetarianism in China is also encouraged by the practice of Buddhism and Daoism, and the Chinese vegetarian diet generally includes soybean products, such as soybean curd (tofu) and textured vegetable protein as protein sources [21]. The nature and nutritional adequacy of vegetarian or plant-based diets prescribed to CKD patients from these two cultural backgrounds have not been carefully examined, even though these two countries have, by far, the largest populations in the world. In addition, the literature on vegetarian and plant-based diets for CKD management is mainly proposed for Western societies, and little has been published about its applicability in Asian cultures. Therefore, the present study examined the nutritional adequacy of EAA and micronutrients of plant-based and vegetarian diets for Asian CKD patients, primarily of Chinese or Indian cultural backgrounds. Since there is also little published information concerning the essential nutrient content of animal-based LPDs prescribed for CKD patients, we analyzed the essential nutrients in the more conventional animal-based LPDs and moderately high protein diets (MHPDs) that might be prescribed to Asian CKD patients.

2. Materials and Methods

2.1. Planning of a Conventional Menu

As a comparator reference diet, we designed a conventional 3-day animal-based menu using 70 kg as the reference body weight for an adult (Table 1). The LPDs consisted of four protein prescriptions, providing 0.5, 0.6, 0.7, and 0.8 g protein per kg body weight. At least 50% of the protein was high biological value protein derived from animal-based food sources [22]. MHPDs providing 1.0, 1.1, and 1.2 g protein per kg body weight which are often prescribed for maintenance hemodialysis and peritoneal dialysis patients were also analyzed [2,3]. The energy prescription was set at 2100 kcal for all diets, based on 30 kcal per kg body weight. Total carbohydrates contributed 54 to 58% of energy (284–305 g) across all protein prescriptions, while the proportion of total fat in the diets ranged from 30 to 35% of energy (70–82 g).
We then determined the exchange or serving size for each food group based on the macronutrient distribution across protein prescriptions. All meal plans were fixed to provide three exchanges of fruit and four servings of non-starchy vegetables. For LPDs, there were eight exchanges of cereals or cereal products and 14 exchanges of fat. Variation for the number of protein food exchanges ranged from two to five exchanges with three to five exchanges of sugar. For MHPDs, there were 11 exchanges of cereals or cereal products. The protein foods varied in providing six to eight exchanges with 11 to 13 exchanges of fat.

2.2. Reference Menus

The approach to menu construction was centered on typical dietary patterns of Indian and Southern Chinese ethnic groups by reference to the patient education materials and the menus designed for patients with CKD from North Indian (Indraprastha Apollo Hospital, New Delhi, India), South Indian (Apollo Hospital Chennai, Tamil Nadu, India), and southern China (Guangzhou Red Cross Hospital, Guangzhou, China) hospitals These menus were obtained via personal communications with the dietitians (Anita Jatana, Apollo Hospital, New Delhi, India and Daphnee DK, Apollo Hospital, Chennai, Tamil Nadu, India) and a nephrologist (Prof. Dr. Tan Rong Shao, Guangzhou Red Cross Hospital, Guangzhou, China) living and working in these areas.
The cereals and cereal products group consisted primarily of rice, which is the staple food for Asians. Other cereal products on the menu included dosa, biscuits, and rice noodles. We included fruits and vegetables common to the Asian region, such as papaya, banana, pear, apple, mango, orange, okra, cucumber, eggplant, cabbage, and spinach. For LPDs, the preparation method for fish and poultry dishes was mainly deep-frying. Beverages such as tea, typically consumed with sugar in India, although not China was featured in the menu to promote adequacy towards the energy prescription without exceeding the protein limit.

2.3. Protein Food Substitutions in Plant-Based and Vegetarian Diets

We planned a menu for a plant-based and four vegetarian diets by substituting the animal-based protein in the conventional menu with plant-based protein such as soy products (i.e., tofu and tempeh), lentils (dhal), or beans. Other food groups on the plant-based and vegetarian menu remained the same as the conventional menu. Constructed menus are provided as supplementary material (Table S1). Menu details for each plant-based and vegetarian diet are as below:
Model 1: The plant-based diet was planned according to the principles of the plant-dominant (PLADO) diet proposed by Kalantar-Zadeh et al. [13]. This diet consisted of about 70% plant-based protein. For instance, a menu with a total protein content of 49 g/day would comprise 35 g protein from plant-based food and 14 g protein from animal-based food. Therefore, any animal-based food such as chicken, fish, or pork from the conventional menu was substituted with a plant-based food so that the animal-based food provided only 30% of total protein.
Model 2: A vegan diet that excluded all food derived from animals, including egg and dairy products. All animal-based protein was substituted with such plant-based protein as tofu, soybean milk, lentils, and chickpeas.
Model 3: An ovo-vegetarian diet that excluded all food derived from animals except for eggs. All animal-based protein, except eggs, was substituted with plant-based protein, and at least one exchange of egg (i.e., one whole egg or the whites from two eggs) was included in the daily diet. The maximum number of eggs included in the menu was three exchanges per day.
Model 4: A lacto-vegetarian diet that excluded all food derived from animals except for dairy products (such as milk, paneer, and curd). All animal-based protein, except dairy products, was substituted with plant-based protein, and at least one exchange of dairy products (i.e., 8 ounces or 240 mL milk) was included in the daily diet. The maximum number of dairy products included in the menu was two exchanges per day.
Model 5: A lacto-ovo vegetarian diet that excluded all food derived from animals except egg and dairy products. All animal-based protein was substituted with plant-based protein, and at least one exchange of egg and dairy products was included in the daily diet. The maximum number of egg and dairy products included in the menu was three and two exchanges per day, respectively.

2.4. Nutrient Analyses

The nutrient profile of all menus was analyzed using the Nutritionist Pro Software (Axxya Systems LLC, Redmond, WA, USA), which refers to the FoodData Central Database of the United States Department of Agriculture [23]. We omitted salt and seasonings in the menu construction and nutrient analysis because the use of these condiments varied by individual preferences and cooking practices, which did not reflect the nutrient composition differences caused by the substitution of animal-based protein with plant-based protein. Therefore, the sodium content of all menus reflected the sodium naturally found in foods. Similarly, the potassium content reflected the natural presence of potassium in foods as a salt substitute such as potassium chloride was not included in the menu planning and nutrient analysis. We presented the exact value of the phosphorus content of all diets that was reported in the database without factoring in the bioavailability of phosphorus sources. The phosphorus content may be underestimated because phosphorus-containing food additives were not accounted for in the food composition database.
We also calculated the Potential Renal Acid Load (PRAL) based on the nutrient composition of all types of LPDs and MHPDs using the formula as described by Remer et al. [24]:
PRAL (mEq/d) = 0.49 × protein (g/d) + 0.037 × phosphorus (mg/d) − 0.021 × potassium (mg/d) − 0.026 × magnesium (mg/d) − 0.013 × calcium (mg/d)
A diet with a positive PRAL value indicates acid is produced while a diet with a negative PRAL value indicates base is produced.

2.5. Defining Nutritional Reference Values

We determined the adequacy of EAAs by referencing the Recommended Dietary Allowance (RDA) for adults (19 years and older) [25]. The recommendation for eicosapentaenoic acid (EPA) plus docosahexaenoic acid (DHA) was set at 250 mg/day [26]. The adequacy of dietary fiber was based on the Adequate Intake (AI) for total dietary fiber, which was 14 g/1000 kcal [25]. Since the energy prescription was 2100 kcal, the AI of the fiber was set at 29 g/day. We determined the adequacy of thiamine, riboflavin, niacin, folate, cobalamin, magnesium, copper, iron, and zinc according to their RDAs, while the AI for manganese was used as the reference value to determine adequacy [27,28,29]. CKD-specific recommendations were used as reference values for selected nutrients such as sodium, calcium, and pyridoxine [3,30]. There was no specific reference value for dietary phosphorus and potassium because the recommendation of the updated Kidney Disease Outcomes Quality Initiative Clinical Practice Guideline is to adjust the dietary intake of these two minerals to maintain serum phosphate and potassium within the normal range [3].

3. Results

The composition of macronutrients in the LPDs (0.5–0.8 g protein/kg/day) is presented in Table 2. The energy ranged from 2016–2229 kcal or 29–32 kcal/kg based on the reference body weight of 70 kg. The vegan LPDs had the greatest carbohydrate and fiber, whereas the lacto-ovo LPDs had the highest fat content. Only the conventional and PLADO LPDs met the WHO recommendations for EPA and DHA, while the EPA and DHA content in vegan and lacto-vegetarian LPDs was almost negligible.
At the dietary protein prescription of 0.5 g/kg/day, no diet met the RDA for threonine, leucine, lysine, and histidine. Furthermore, the PLADO, lacto-vegetarian, ovo-vegetarian, and vegan diets did not meet the RDA for methionine + cysteine. The percent adequacy for these EAAs according to their RDA is presented in Figure 1A.
At the dietary protein prescription of 0.6 g/kg/day, the conventional diet met the RDA for all EAAs. The PLADO, ovo-vegetarian, lacto-vegetarian, and lacto-ovo-vegetarian diets were below the RDA only for lysine, whereas the vegan diet did not meet the RDAs for lysine and methionine + cysteine. The percent of adequacy for these EAAs according to the RDAs is presented in Figure 1B. With diets at 0.7 g protein/kg/day and greater, all plant-based and vegetarian diets as well as the conventional diet met the RDA for all EAAs.
The composition of macronutrients in the MHPDs (1.0–1.2 g/kg/day) is presented in Table 3. The energy ranged from 2079–2410 kcal or 20–34 kcal/kg based on the reference body weight of 70 kg. The vegan MHPDs had the greatest amount of carbohydrate and dietary fiber, whereas the lacto-ovo MHPDs had the highest fat content. Only the conventional and PLADO MHPDs met the WHO recommendations for EPA and DHA, whereas the EPA and DHA content in the vegan and lacto-vegetarian LPDs were almost negligible. All MHPDs met the RDA for each EAA.
The macromineral, trace element, and vitamin content of LPDs and MHPDs are presented in Table 4 and Table 5, respectively. The plant-based and vegetarian diets contained a greater amount of potassium, phosphorus, and calcium than the conventional diet. On the other hand, the conventional diet contained a relatively greater amount of sodium compared to the plant-based and vegetarian diets, although the sodium content was still below the amount usually recommended for CKD patients [3]. The plant-based and vegetarian LPDs, but not the conventional LPD, met the RDA for copper, whereas all MHPDs met the RDA for copper. All LPDs and MHPDs also met the AI for manganese. No LPD met the RDA for zinc, whereas only vegan MHPDs (≥1.0 g/kg/day), lacto-ovo-vegetarian MHPDs (≥1.1 g/kg/day), lacto-vegetarian MHPDs (≥1.1 g/kg/day), and ovo-vegetarian MHPDs (≥1.2 g/kg/day) were adequate. Similarly, no LPD met the RDA for magnesium, but vegan MHPDs (≥1.0 g/kg/day), lacto-vegetarian MHPDs (≥1.1 g/kg /day), and ovo-vegetarian MHPDs (≥1.2 g/kg /day) met the RDA for magnesium. All LPDs and MHPDs met the RDA for iron for both men and women above 50 years old (8 mg/day), whereas vegan diets (≥0.6 g/kg/day), ovo-vegetarian diets (≥0.7 g/kg/day), ovo-vegetarian diets (≥0.8 g/kg/day), PLADO diets (≥0.8 g/kg/day) and lacto-ovo-vegetarian diets (≥1.0 g/kg/day), but not the conventional diet, met the iron RDA for only women 19–50 years old (18 mg/day) [29].
For the B vitamins, all LPDs and MHPDs met the RDA for thiamine and folate, whereas no LPD or MHPD met the CKD-specific recommendation for pyridoxine. No LPD met the RDA for riboflavin except the lacto-ovo vegetarian LPDs (≥0.6 g/kg/day). The ovo-vegetarian and lacto-vegetarian diets at a protein prescription ≥1.1 g/kg/day met the RDA for riboflavin. None of the ovo-vegetarian and lacto-ovo-vegetarian diets met the RDA for niacin, whereas conventional LPDs (≥0.6 g/kg/day), PLADO LPDs (≥0.7 g/kg/day), vegan MHPDs (≥1.1 g/kg/day), and lacto-vegetarian MHPDs (≥1.2 g/kg/day) met the RDA for niacin. With regard to the RDA for cobalamin, none of the ovo-vegetarian, lacto-vegetarian, and vegan LPDs or MHPDs met this RDA, whereas the conventional diets (≥0.6 g/kg/day), PLADO diets (≥0.6 g/kg/day), and lacto-ovo-vegetarian diets (≥0.7 g/kg/day) met the RDA for cobalamin.
Figure 2 shows the PRAL of all types of LPDs and MHPDs. All PLADO, lacto-vegetarian, and vegan diets had negative PRAL, though at a decreasing trend when the protein prescription increased. The ovo-vegetarian diets had negative PRAL values at protein prescriptions from 0.5 to 1.1 g/kg body weight/day, and the PRAL value became positive at protein prescription of 1.2 g/kg body weight/day. The conventional and lacto-ovo-vegetarian diets had negative PRAL values at protein prescription below 0.8 g/kg body weight/day, and the PRAL values became positive at 1.0 g protein/kg body weight/day and above.

4. Discussion

The World Health Organization recommends that the safe level of protein intake for healthy adults is 0.83 g/kg body weight per day, for proteins with protein digestibility-corrected amino acid score value of 1.0 [31]. The LPDs (0.6–0.8 g/kg) prescribed to non-dialysis dependent CKD patients have been recommended to include at least 50% high biological value protein to ensure the adequacy of dietary needs [22]. Our LPD food pattern modeling concurred with this recommendation, since only the conventional LPD (0.6 g/kg/day) containing at least 50% of the animal-based protein met the RDA for all EAAs. However, the plant-based and vegetarian diets only met the RDA for all EAA with the protein prescription of >0.7 g/kg and above, and these EAAs are likely to be deficient when the protein intake is restricted to 0.6 g per kg body weight.
Plant proteins typically are less abundant than animal proteins in certain EAAs, especially methionine and lysine [15]. A cross-sectional study comparing the dietary intake and plasma concentration of amino acids among healthy men based on their habitual dietary intakes reported that vegans had the lowest dietary intake and plasma concentrations of lysine and methionine compared to meat-eaters, fish-eaters, and vegetarians [32]. Table 6 shows the content of selected EAA of proteins from different food sources in one exchange (7 g protein). For an LPD providing 0.6 g protein/kg/day or 42 g/day (using the reference body weight of 70 kg), three exchanges (21 g protein) of animal protein, such as fish or poultry, provide about 55–75% of the RDA for leucine, lysine, and methionine plus cysteine. However, when the animal proteins are substituted with plant protein such as tofu, lentils, or beans, the content of EAAs are expected to be lower, since three exchanges of these plant proteins provide only 50–55% of the RDA for leucine and lysine, and 30–40% of the RDA for methionine plus cysteine. As the protein prescription becomes higher (≥0.7 g/kg/day) and more plant proteins can be included in the diet, it is then possible for the diet to meet the RDAs for all EAAs.
Barsotti et al. [16] and Soraka et al. [18] demonstrated that a vegetarian LPD with a protein prescription of 0.70–0.75 g per kg body weight could meet their reported requirements for all EAAs. The authors noted that the patients prescribed with these diets did not experience a deterioration in nutritional status, even though the vegetarian LPD was proportionally lower in lysine, leucine, and methionine in comparison to both animal-based diets of lower protein content and the RDAs. There are several possible explanations for these observations. First, the RDA for a nutrient is determined if the dietary intake provides nutritionally sufficient amounts of that nutrient for about 97% of a normal population [25]. By this criterion, most people could ingest less than the RDA of a given nutrient and yet still receive a sufficient amount of that nutrient to be nutritionally adequate for them. Secondly, patients’ actual dietary protein intake might be more than what they were prescribed, at least some of the time [33]. Third, a limitation may arise from their nutritional assessment approach to determining patients’ protein-energy status which was not sufficiently sensitive as it relied only on body weight and serum proteins, whilst the patient’s vitamin, mineral, and trace element status were not evaluated by these studies.
To the best of our knowledge, the lowest protein content for a vegan diet for CKD patients that has been previously examined was 0.7 g/kg body weight/day, and the methods for assessing nutritional status in these patients were quite imprecise [16]. As shown in Table 6, plant proteins are inherently low in lysine and methionine. Therefore, achieving the RDA of these EAAs is very unlikely when the diet is low in protein (0.6 g/kg) and contains exclusively plant proteins at the same time. The PLADO low protein diet (0.6 g/kg) consisting of only 30% animal proteins was also deficient in lysine. In fact, our data indicate that the conventional low protein diet (0.6 g/kg) with 50% animal proteins also marginally met the RDA for lysine (108%). Nonetheless, many nitrogen balance studies indicate that a 0.60 g protein/kg/day diet providing about 50% of protein of high biological value (i.e., animal protein) will maintain neutral or positive nitrogen balance in advanced CKD patients who are not undergoing dialysis therapy [22,34].
Although the data from this food pattern modeling indicated that a well-planned plant-based or vegetarian LPD (≥0.7 g/kg/day) can meet the RDA for all EAAs, the RDA is not CKD-specific. It is possible that there are alterations in the dietary requirements for some EAAs in people with CKD, especially if such individuals have comorbid conditions [35,36,37,38]. Patients with advanced CKD have altered plasma and tissue amino acid profiles [39,40,41]. There is evidence for intracellular taurine depletion in nondialyzed CKD and maintenance hemodialysis patients [35,36,42], and plant foods are markedly deficient in taurine [43]. Therefore, a plant-based or a vegan diet may be unable to supply a sufficient amount of taurine or other sulfur containing amino acids to maintain normal cellular taurine levels [44], and CKD and chronic dialysis patients consuming vegan diets could be at risk for taurine deficiency. Future studies are indicated to confirm that these plant-based and especially vegan LPDs are nutritionally adequate for CKD patients. These considerations also suggest that CKD and chronic dialysis patients adhering to a vegan LPD should be monitored especially closely to assess their nutritional status and to prevent protein-energy wasting. This issue may be especially challenging in low- and middle-income Asian countries with limited dietitian accessibility [45] and where malnutrition risk may be particularly high, chronic infections such as tuberculosis are endemic [46], and populations have marginal protein intakes [47].
A recent review of observation studies by Picard et al. [48] reported that free-living CKD patients consuming vegetarian or plant-based diets had a significantly lower self-reported dietary protein intake. However, the effects of this lower protein intake on the patients’ protein-energy status were not carefully assessed; only serum albumin levels were reported, and serum albumin, which was not different in the patients consuming the animal-based vs. the plant-based diets, is rather a more sensitive indicator of inflammation than nutritional status [49]. Nevertheless, this review supports the contention that CKD patients prescribed LPDs, and especially plant-based or vegetarian LPDs, should be counselled by experienced dietitians, and their protein-energy status should be periodically monitored [48]. An epidemiological study of Chinese maintenance hemodialysis patients suggested that the proportion of plant-based proteins in their diet bore a U-curve relationship with adjusted all-cause mortality and cardiovascular mortality [49]. The lowest adjusted mortality rates were observed in the maintenance dialysis patients who ingested plant-based and animal-based proteins in approximately a 0.45 ratio. Hence, 55 percent of the food intake was animal-based for this data. This study was limited by the fact that the assessment of food intake was made for three separate 24 h periods at the beginning of the median follow-up period of 28 months [50].
The preceding discussion indicates that plant-based LPDs may place CKD patients at increased risk for nutritional deficiencies, especially if these diets provide less than 0.7 g protein/kg/day. However, plant-based diets might also increase the intake of other nutrients to unwanted levels. For CKD patients, this may be particularly the case for potassium and phosphorus, which could exacerbate electrolyte imbalances in patients with CKD [10]. Indeed, the vegetarian LPDs and MHPDs contained greater amounts of potassium and phosphorus than the conventional and plant-based diets, as shown in Table 4 and Table 5. This is especially true for the vegan diets. The sodium content of these diets reflected only the sodium found naturally in foods, and the amount was substantially lower than what a person would normally consume. As condiments and seasonings were not included in nutrient analysis, the potassium and phosphorus contents were also underestimated because certain condiments commonly used in Chinese cuisine such as soy sauce, oyster sauce, and fish sauce also contain significant amounts of potassium and phosphorus [51].
In this study, we did not include vegetarian meat substitutes that may contain substantial amounts of sodium, potassium, and phosphorus [52]. In addition, these plant-based meat alternatives are low in certain nutrients such as zinc, calcium, and vitamin B12 [53]. Therefore, natural or unprocessed plant-based proteins were chosen. Although the phosphorus of plant-based foods is generally believed to have lower bioavailability (10–30%) due to the phytates in these diets, a review of human intervention studies suggests that a much greater amount of phytate-phosphorus is absorbed (at least 50%). Commercial food processing also increases the amount of bioavailable phosphorus. Therefore, the phosphorus of plant proteins, particularly those that are highly processed, should not be assumed to be poorly absorbed [54]. Nevertheless, the phosphorus bioavailability of plant foods is still lower than animal foods. On the other hand, the dairy products included in the lacto- and lacto-ovo vegetarian diets are significant sources of dietary phosphorus and calcium. The high dietary calcium content might increase the risk of calcium deposition in tissues, which is a not an uncommon occurrence amongst advanced CKD patients [55].
Plant-based and vegetarian diets may also lack some other essential nutrients that are more prevalent in foods of animal origin, such as long-chain n-3 PUFAs and vitamin B-12 or cobalamin [56]. A cross-sectional study showed that fish-eaters had a greater dietary intake of long-chain n-3 PUFAs than vegetarians or vegans. However, the difference in plasma long-chain n-3 PUFAs status between fish-eaters and vegetarians or vegans was smaller than expected, possibly due to a greater estimated precursor-product ratio of dietary α-linolenic acid to long-chain n-3 PUFAs among vegetarians or vegans [57]. Therefore, patients adhering to a plant-based or vegetarian diet should be encouraged to consume foods high in α-linolenic acid to ensure optimal plasma n-3 PUFAs status. On the other hand, since vitamin B-12 is obtained exclusively from animal sources, CKD patients adhering to a vegetarian diet must consume vitamin B-12 fortified foods or dietary supplements to prevent deficiency [5].
On the other hand, it is worthwhile to highlight that the planned plant-based and vegetarian diets contained a relatively greater amount of dietary fiber than the conventional diet that was basically animal-based. Meta-analyses of experimental studies have demonstrated the benefits of dietary fiber supplements (dosage ranging from 7 to 50 g/day) in reducing serum urea, creatinine, and p-cresyl sulphate [58,59]. In our study, the fiber content of the plant-based or vegetarian LPDs (0.5–0.8 g/kg/day) was greater than the conventional LPDs by 8–20 g/day. In addition, plant proteins such as beans, legumes, and lentils have a lower PRAL than animal proteins such as meat, cheese, and eggs [60]. Both epidemiological studies [61,62] and clinical trials [63,64] have indicated that even mild acidosis can be associated with more rapid progression of CKD, and a diet that is low in its PRAL may slow such progression [65,66]. However, our study showed that the PRAL values of the conventional LPDs were not substantially higher than the plant-based or vegetarian diets when the protein content was low (0.5–0.6 g/kg body weight/day).
Plant proteins also do not contain cholesterol and have a lower saturated fat content than animal proteins. However, the evidence does not indicate that advanced CKD or chronic dialysis patients who ingest lower cholesterol diets or who are taking statins have less cardiovascular disease or reduced mortality [67]. Consumption of plant-based foods is proposed to confer planetary benefits as negative impacts of large-scale meat production on the environment in terms of the land use, water use, and the emission of greenhouse gases have been highlighted [68]. It should be considered though that for many Asian countries, animal proteins are often derived from seafood, poultry or pork, rather than from cattle [69]. With caution, plant proteins may be encouraged for individuals with CKD as long as the diet is carefully planned to ensure that the overall nutritional adequacy is met. As our study suggests, the 0.60 g protein/kg/day diet, it may be difficult to ensure sufficient amounts of all of the EAAs without including animal protein.
Our study had some limitations. Firstly, the LPD and MHPD modeling was based on an ideal menu planning that is theoretical in nature and therefore may not necessarily reflect habitual dietary intakes of any individual CKD patient. Secondly, the modeling study was based on food choices commonly consumed in Asian cuisine, mainly Chinese and Indian. Therefore, these findings may not be generalized to other Asian food cultures, but analysis of these Chinese and Indian hospital-based diets may provide useful insights to food choices across the Asian spectrum. In addition, we determined the amino acid content using a food composition database (FoodData Central) rather than by direct laboratory analytical procedures. In addition, variability in the composition of foods may exist between regions and between countries. However, this concern also raises the possibility that some foodstuffs might contain fewer essential nutrients than is reported in this database. Moreover, we did not include protein-free products (e.g., pasta, bread, and flour) in planning the LPDs, which, if included, would reduce the proportion of protein from cereals and allow the inclusion of a greater amount of protein food sources for the LPDs. However, such products are atypical to Asian societies and therefore have limited availability in food retail, whereas rice is the staple cereal of choice in the Asian region [70]. Lastly, the actual phosphorus content of the diets may be substantially higher than is indicated in the food composition database because the widely prevalent use of phosphorus-based additives was not taken into account and potentially available in ready-to-use spice powders, flavorings, and ultraprocessed foods available to Indian and Chinese societies. Moreover, the varying bioavailability of phosphorus in different food sources was not addressed in our calculations.

5. Conclusions

Our food pattern modeling indicated that the Asian plant-based and vegetarian diets providing 0.7 g protein/kg/day or more could meet the RDA for all EAAs. However, at the protein prescription of 0.6 g/kg/day, only the conventional diet consisting of 50% high biological protein from animal-based foods is able to meet the RDA of all EAAs, while the vegetarian or plant-based LPDs are likely to be deficient in EAAs. Therefore, a higher protein level (at least 0.7 g protein/kg/day) should be considered for individuals who wish to adhere to vegetarian or plant-based diets, and these diets must be carefully planned because the protein prescription is still below the RDA. With regards to macrominerals, plant-based and vegetarian diets contained a considerable amount of potassium, phosphorus, and calcium as compared to the conventional diet. The conventional diet was low in essential nutrients such as zinc, copper, magnesium, riboflavin, and pyridoxine while plant-based and vegetarian diets were low in n-3 long-chain polyunsaturated fatty acids, magnesium, riboflavin, niacin, pyridoxine, and cobalamin. The use of a multivitamin and trace element supplement should be considered with these diets. The foregoing data indicate that prescription of all LPDs for CKD patients requires careful planning and continued monitoring.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/nu13103341/s1, Table S1: Three days sample menu.

Author Contributions

Conceptualization, B.-H.K., T.K., P.K. and J.D.K.; methodology, B.-H.K.; formal analysis, B.-H.K. and D.A.T.; investigation, B.-H.K., D.A.T., T.K. and M.C.; writing—original draft preparation, B.-H.K., T.K. and J.D.K. writing—review and editing, D.A.T., P.K. and M.C.; supervision, J.D.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created in this study. Data sharing is not applicable to this article.

Acknowledgments

We would like to thank the nephrologist and dietitians from India and China who shared their sample menus for CKD patients.

Conflicts of Interest

The authors declare no conflict of interest.

Disclaimer

This article solely reflects the view of the authors and does not represent any views or policies of the FDA.

References

  1. GBD Chronic Kidney Disease Collaboration. Global, regional, and national burden of chronic kidney disease, 1990–2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet 2020, 395, 709–733. [Google Scholar] [CrossRef] [Green Version]
  2. Kalantar-Zadeh, K.; Fouque, D. Nutritional management of chronic kidney disease. N. Engl. J. Med. 2017, 377, 1765–1776. [Google Scholar] [CrossRef]
  3. Ikizler, T.A.; Burrowes, J.D.; Byham-Gray, L.D.; Campbell, K.L.; Carrero, J.J.; Chan, W.; Fouque, D.; Friedman, A.N.; Ghaddar, S.; Goldstein-Fuchs, D.J.; et al. KDOQI clinical practice guideline for nutrition in CKD: 2020 update. Am. J. Kidney Dis. 2020, 76, S1–S107. [Google Scholar] [CrossRef]
  4. Kopple, J.D. Pathophysiology of protein-energy wasting in chronic renal failure. J. Nutr. 1999, 129, 247S–251S. [Google Scholar] [CrossRef] [PubMed]
  5. Melina, V.; Craig, W.; Levin, S. Position of the Academy of Nutrition and Dietetics: Vegetarian diets. J. Acad. Nutr. Diet 2016, 116, 1970–1980. [Google Scholar] [CrossRef] [PubMed]
  6. Alcorta, A.; Porta, A.; Tárrega, A.; Alvarez, M.D.; Vaquero, M.P. Foods for Plant-Based Diets: Challenges and Innovations. Foods 2021, 10, 293. [Google Scholar] [CrossRef]
  7. Mullins, A.P.; Arjmandi, B.H. Health Benefits of Plant-Based Nutrition: Focus on Beans in Cardiometabolic Diseases. Nutrients 2021, 13, 519. [Google Scholar] [CrossRef]
  8. Adair, K.E.; Bowden, R.G. Ameliorating chronic kidney disease using a whole food plant-based diet. Nutrients 2020, 12, 1007. [Google Scholar] [CrossRef] [Green Version]
  9. Carrero, J.J.; González-Ortiz, A.; Avesani, C.M.; Bakker, S.J.; Bellizzi, V.; Chauveau, P.; Clase, C.M.; Cupisti, A.; Espinosa-Cuevas, A.; Molina, P.; et al. Plant-based diets to manage the risks and complications of chronic kidney disease. Nat. Rev. Nephrol. 2020, 16, 525–542. [Google Scholar] [CrossRef]
  10. Cases, A.; Cigarrán-Guldrís, S.; Mas, S.; Gonzalez-Parra, E. Vegetable-based diets for chronic kidney disease? It is time to reconsider. Nutrients 2019, 11, 1263. [Google Scholar] [CrossRef] [Green Version]
  11. Chauveau, P.; Koppe, L.; Combe, C.; Lasseur, C.; Trolonge, S.; Aparicio, M. Vegetarian diets and chronic kidney disease. Nephrol. Dial. Transplant. 2019, 34, 199–207. [Google Scholar] [CrossRef]
  12. Joshi, S.; McMacken, M.; Kalantar-Zadeh, K. Plant-based diets for kidney disease: A guide for clinicians. Am. J. Kidney Dis. 2020, 77, 287–296. [Google Scholar] [CrossRef] [PubMed]
  13. Kalantar-Zadeh, K.; Joshi, S.; Schlueter, R.; Cooke, J.; Brown-Tortorici, A.; Donnelly, M.; Schulman, S.; Lau, W.L.; Rhee, C.M.; Streja, E.; et al. Plant-dominant low-protein diet for conservative management of chronic kidney disease. Nutrients 2020, 12, 1931. [Google Scholar] [CrossRef]
  14. Verzola, D.; Picciotto, D.; Saio, M.; Aimasso, F.; Bruzzone, F.; Sukkar, S.G.; Massarino, F.; Esposito, P.; Viazzi, F.; Garibotto, G. Low Protein Diets and Plant-Based Low Protein Diets: Do They Meet Protein Requirements of Patients with Chronic Kidney Disease? Nutrients 2021, 13, 83. [Google Scholar] [CrossRef]
  15. Gorissen, S.H.; Crombag, J.J.; Senden, J.M.; Waterval, W.H.; Bierau, J.; Verdijk, L.B.; van Loon, L.J. Protein content and amino acid composition of commercially available plant-based protein isolates. Amino Acids 2018, 50, 1685–1695. [Google Scholar] [CrossRef] [Green Version]
  16. Barsotti, G.; Morelli, E.; Cupisti, A.; Meola, M.; Dani, L.; Giovannetti, S. A low-nitrogen low-phosphorus Vegan diet for patients with chronic renal failure. Nephron 1996, 74, 390–394. [Google Scholar] [CrossRef]
  17. Cupisti, A.; Morelli, E.; Meola, M.; Barsotti, M.; Barsotti, G. Vegetarian diet alternated with conventional low-protein diet for patients with chronic renal failure. J. Ren. Nutr. 2002, 12, 32–37. [Google Scholar] [CrossRef]
  18. Soroka, N.; Silverberg, D.S.; Greemland, M.; Birk, Y.; Blum, M.; Peer, G.; Iaina, A. Comparison of a vegetable-based (soya) and an animal-based low-protein diet in predialysis chronic renal failure patients. Nephron 1998, 79, 173–180. [Google Scholar] [CrossRef] [PubMed]
  19. Chang, C.Y.; Chang, H.R.; Lin, H.C.; Chang, H.H. Comparison of renal function and other predictors in lacto–Ovo vegetarians and omnivores with chronic kidney disease. J. Am. Coll. Nutr. 2018, 37, 466–471. [Google Scholar] [CrossRef]
  20. Singh, P.N.; Arthur, K.N.; Orlich, M.J.; James, W.; Purty, A.; Job, J.S.; Rajaram, S.; Sabaté, J. Global epidemiology of obesity, vegetarian dietary patterns, and noncommunicable disease in Asian Indians. Am. J. Clin. Nutr. 2014, 100, 359S–364S. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  21. Cao, D. Chinese Takeaways: Vegetarian Culture in Contemporary China. Camb. J. China Stud. 2018, 13, 1–23. [Google Scholar]
  22. Kopple, J.D.; Monteon, F.J.; Shaib, J.K. Effect of energy intake on nitrogen metabolism in nondialyzed patients with chronic renal failure. Kidney Int. 1986, 29, 734–742. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. U.S. Department of Agriculture. FoodData Central. Available online: https://fdc.nal.usda.gov (accessed on 23 July 2021).
  24. Remer, T.; Dimitriou, T.; Manz, F. Dietary potential renal acid load and renal net acid excretion in healthy, free-living children and adolescents. Am. J. Clin. Nutr. 2003, 77, 1255–1260. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Institute of Medicine. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids; The National Academies Press: Washington, DC, USA, 2005. [Google Scholar]
  26. Joint FAO/WHO Expert Consultation. Fats and Fatty Acids in Human Nutrition: Report of an EXPERT consultation. In Proceedings of the Joint FAO/WHO Expert Consultation, Rome, Italy, 25–29 January 2010. [Google Scholar]
  27. Institute of Medicine. Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride; The National Academies Press: Washington, DC, USA, 1997. [Google Scholar]
  28. Institute of Medicine. Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin and Choline; The National Academies Press: Washington, DC, USA, 1998. [Google Scholar]
  29. Institute of Medicine. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc; The National Academies Press: Washington, DC, USA, 2000. [Google Scholar]
  30. Kopple, J.D.; Mercurio, K.; Blumenkrantz, M.J.; Jones, M.R.; Tallos, J.; Roberts, C.; Card, B.; Saltzman, R.; Casciato, D.A.; Swendseid, M.E. Daily requirement for pyridoxine supplements in chronic renal failure. Kidney Int. 1981, 19, 694–704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. WHO/FAO/UNU. Protein and amino acid requirements in human nutrition: Report of a joint WHO/FAO/UNU expert consultation. World Health Organ Tech. Rep. Ser. 2007, 935, 1–265. [Google Scholar]
  32. Schmidt, J.A.; Rinaldi, S.; Scalbert, A.; Ferrari, P.; Achaintre, D.; Gunter, M.J.; Appleby, P.N.; Key, T.J.; Travis, R.C. Plasma concentrations and intakes of amino acids in male meat-eaters, fish-eaters, vegetarians and vegans: A cross-sectional analysis in the EPIC-Oxford cohort. Eur. J. Clin. Nutr. 2016, 70, 306–312. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Kopple, J.D.; Levey, A.S.; Greene, T.; Chumlea, W.C.; Gassman, J.J.; Hollinger, D.L.; Maroni, B.J.; Merrill, D.; Scherch, L.K.; Schulman, G.; et al. Effect of dietary protein restriction on nutritional status in the Modification of Diet in Renal Disease Study. Kidney Int. 1997, 52, 778–791. [Google Scholar] [CrossRef] [Green Version]
  34. Kopple, J.D.; Coburn, J.W. Metabolic studies of low protein diets in uremia. I. Nitrogen and potassium. Medicine 1973, 52, 583–595. [Google Scholar] [CrossRef]
  35. Bergstrom, J.; Alvestrand, A.; Furst, P.; Lindholm, B. Sulphur amino acids in plasma and muscle in patients with chronic renal failure: Evidence for taurine depletion. J. Intern. Med. 1989, 226, 189–194. [Google Scholar] [CrossRef]
  36. Suliman, M.E.; Anderstam, B.; Bergstrom, J. Evidence of taurine depletion and accumulation of cystenesulfinic acid in chronic dialysis patients. Kidney Int. 1996, 50, 1713–1717. [Google Scholar] [CrossRef] [Green Version]
  37. Furst, P.; Stehle, P. What are the essential elements needed for the determination of amino acid requirements in humans? J. Nutr. 2004, 134, 1558S–1565S. [Google Scholar] [CrossRef]
  38. Kopple, J.D. Phenylalanine and tyrosine metabolism in chronic kidney failure. J. Nutr. 2007, 137 (Suppl. S1), 1586S–1590S. [Google Scholar] [CrossRef] [PubMed]
  39. Flugel-Link, R.M.; Jones, M.R.; Kopple, J.D. Red cell and plasma amino acid concentrations in renal failure. J. Parenter. Enter. Nutr. 1983, 7, 450–456. [Google Scholar] [CrossRef]
  40. Laidlaw, S.A.; Berg, R.L.; Kopple, J.D.; Naito, H.; Walker, W.G.; Walser, M.; Modification of Diet in Renal Disease Study Group. Patterns of fasting plasma amino acid levels in chronic renal insufficiency: Results from the feasibility phase of the Modification of Diet in Renal Disease Study. Am. J. Kidney Dis. 1994, 23, 504–513. [Google Scholar] [CrossRef]
  41. Duranton, F.; Lundin, U.; Gayrard, N.; Mischak, H.; Aparicio, M.; Mourad, G.; Daurès, J.P.; Weinberger, K.M.; Argilés, À. Plasma and urinary amino acid metabolomic profiling in patients with different levels of kidney function. Clin. J. Am. Soc. Nephrol. 2014, 9, 37–45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Jung, B.C.; Laidlaw, S.A.; Kopple, J.D. Taurine levels in plasma and blood cells in patients undergoing routine maintenance hemodialysis. Am. J. Kidney Dis. 1991, 1, 74–79. [Google Scholar] [CrossRef]
  43. Laidlaw, S.A.; Grosvernor, M.; Kopple, J.D. The taurine content of common foodstuffs. J. Parenter. Enteral Nutr. 1990, 14, 183–188. [Google Scholar] [CrossRef]
  44. Laidlaw, S.A.; Shultz, T.D.; Cecchino, J.T.; Kopple, J.D. Plasma and taurine levels in vegans. Am. J. Kidney Dis. 1988, 47, 660–663. [Google Scholar]
  45. Riaz, P.; Fergus, C.; Mclsaac, M.; Davids, R.; Htay, H.; Jha, V.; Jindal, K.; Jun, M.; Khan, M.; Levin, A.; et al. Workforce capacity for the care of patients with kidney failure across world countries and regions. BMJ Glob. Health 2021, 6, e004014. [Google Scholar] [CrossRef]
  46. Basnyat, B.; Caws, M.; Udwadia, Z. Tuberculosis in South Asia: A tide in the affairs of men. Multidiscip. Respir. Med. 2018, 13, 10. [Google Scholar] [CrossRef] [Green Version]
  47. Swaminathan, S.; Vaz, M.; Kurpad, A.V. Protein intakes in India. Br. J. Nutr. 2012, 108, S50–S58. [Google Scholar] [CrossRef] [Green Version]
  48. Picard, K.; Mager, D.R.; Richard, C. The Impact of Protein Type on Phosphorus Intake, Serum Phosphate Concentrations, and Nutrition Status in Adults with Chronic Kidney Disease: A Critical Review. Adv. Nutr. 2021, nmab062. [Google Scholar] [CrossRef]
  49. Friedman, A.; Fadem, S.Z. Reassessment of albumin as a nutritional marker in kidney disease. J. Am. Soc. Nephrol. 2010, 21, 223–230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. He, Y.; Lu, Y.; Yang, S.; Li, Y.; Yang, Y.; Chen, J.; Huang, Y.; Lin, Z.; Li, Y.; Kong, Y.; et al. Dietary Plant Protein and Mortality Among Patients Receiving Maintenance Hemodialysis: A Cohort Study. Am. J. Kidney Dis. 2021. [Google Scholar] [CrossRef] [PubMed]
  51. Tan, W.L.; Azlan, A.; Noh, M.F.M. Sodium and potassium contents in selected salts and sauces. Int. Food Res. J. 2016, 23, 2181–2186. [Google Scholar]
  52. Banman, C. Vegetarian Meat Substitutes. J. Ren. Nutr. 2008, 18, e9–e11. [Google Scholar] [CrossRef]
  53. Tso, R.; Forde, C.G. Unintended consequences: Nutritional impact and potential pitfalls of switching from animal- to plant-based foods. Nutrients 2021, 13, 2527. [Google Scholar] [CrossRef] [PubMed]
  54. Calvo, M.S.; Uribarri, J. Perspective: Plant-based Whole-Grain Foods for Chronic Kidney Disease: The Phytate-Phosphorus Conundrum. Adv. Nutr. 2021, nmab066. [Google Scholar] [CrossRef]
  55. Wang, A.Y.M.; Akizawa, T.; Bavanandan, S.; Hamano, T.; Liew, A.; Lu, K.C.; Lumlertgul, D.; Oh, K.H.; Zhao, M.H.; Fung, S.K.S.; et al. 2017 Kidney Disease: Improving Global Outcomes (KDIGO) Chronic Kidney Disease–Mineral and Bone Disorder (CKD-MBD) Guideline Update Implementation: Asia Summit Conference Report. Kidney Int. Rep. 2019, 4, 1523–1537. [Google Scholar] [CrossRef] [Green Version]
  56. Chauveau, P.; Combe, C.; Fouque, D.; Aparicio, M. Vegetarianism: Advantages and drawbacks in patients with chronic kidney diseases. J. Ren. Nutr. 2013, 23, 399–405. [Google Scholar] [CrossRef]
  57. Welch, A.A.; Shakya-Shrestha, S.; Lentjes, M.A.; Wareham, N.J.; Khaw, K.T. Dietary intake and status of n–3 polyunsaturated fatty acids in a population of fish-eating and non-fish-eating meat-eaters, vegetarians, and vegans and the precursor-product ratio of α-linolenic acid to long-chain n–3 polyunsaturated fatty acids: Results from the EPIC-Norfolk cohort. Am. J. Clin. Nutr. 2010, 92, 1040–1051. [Google Scholar]
  58. Chiavaroli, L.; Mirrahimi, A.; Sievenpiper, J.L.; Jenkins, D.J.A.; Darling, P.B. Dietary fiber effects in chronic kidney disease: A systematic review and meta-analysis of controlled feeding trials. Eur. J. Clin. Nutr. 2015, 69, 761–768. [Google Scholar] [CrossRef] [Green Version]
  59. Wu, M.; Cai, X.; Lin, J.; Zhang, X.; Scott, E.M.; Li, X. Association between fibre intake and idoxyl sulphate/p-cresyl sulphate in patients with chronic kidney disease: Meta-analysis and systematic review of experimental studies. Clin. Nutr. 2019, 38, 2016–2022. [Google Scholar] [CrossRef]
  60. Scialla, J.J.; Anderson, C.A.M. Dietary acid load: A novel nutritional target in chronic kidney disease? Adv. Chronic Kidney Dis. 2013, 20, 141–149. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Dobre, M.; Yang, W.; Chen, J.; Drawz, P.; Hamm, L.L.; Hortwitz, E.; Hostetter, T.; Jaar, B.; Lora, C.M.; Nessel, L.; et al. Association of serum bicarbonate with risk of renal and cardiovascular outcomes in CKD: A report from the Chronic Renal Insufficiency Cohort (CRIC) study. Am. J. Kidney Dis. 2013, 62, 670–678. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Shah, S.N.; Abramowitz, M.; Hostetter, T.H.; Melamed, M.L. Serum bicarbonate levels and the progression of kidney disease: A cohort study. Am. J. Kidney Dis. 2009, 54, 270–277. [Google Scholar] [CrossRef] [Green Version]
  63. De Brito-Ashurst, I.; Varagunam, M.; Raftery, M.J.; Yaqoob, M.M. Bicarbonate supplementation slows progression of CKD and improves nutritional status. J. Am. Soc. Nephrol. 2009, 20, 2075–2084. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Iorio, B.R.D.; Bellasi, A.; Rapheal, K.L.; Santoro, D.; Aucella, F.; Garofano, L.; Caccarelli, M.; Lullo, L.D.; Capolongo, G.; Iorio, M.D.; et al. Treatment of metabolic acidosis with sodium bicarbonate delays progression of chronic kidney disease: The UBI Study. J. Nephrol. 2019, 32, 898–1001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Banerjee, T.; Tucker, K.; Griswold, M.; Sharon, B.W.; Harman, J.; Young, B.; Taylor, H.; Powe, N.R. Dietary potential renal acid load and risk of albuminuria and reduced kidney function in the Jackson Heart Study. J. Ren. Nutr. 2019, 28, 251–258. [Google Scholar] [CrossRef]
  66. Rebholz, C.M.; Coresh, J.; Grams, M.E.; Steffen, L.M.; Anderson, C.A.M.; Appel, L.J.; Crews, D.C. Dietary acid load and incident chronic kidney disease: Results from the ARIC study. Am. J. Nephrol. 2015, 42, 427–435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Wanner, C.; Krane, V.; Marz, W.; Olschewski, M.; Mann, J.F.E.; Ruf, G.; Ritz, E.; German Diabetes and Dialysis Study Investigators. Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N. Engl. J. Med. 2005, 353, 238–248. [Google Scholar] [CrossRef] [PubMed]
  68. Godfray, H.C.J.; Aveyard, P.; Garnett, T.; Hall, J.W.; Key, T.J.; Lorimer, J.; Pierrehumbert, R.T.; Scarborough, P.; Springmann, M.; Jebb, S.A. Meat consumption, health, and the environment. Science 2018, 361, eaam5324. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  69. Food and Agriculture Organization of the United Nations (FAOSTAT). Calculated from Food Balance Sheets. 2021. Available online: http://www.fao.org/faostat/en/#data/FBS (accessed on 19 September 2021).
  70. Se, C.H.; Khor, B.H.; Karupaiah, T. Prospects in development of quality rice for human nutrition. Malays. Appl. Biol. 2015, 44, 1–31. [Google Scholar]
Nutrients 13 03341 g001 550
Figure 1. Percent of Recommended Dietary Allowance of selected essential amino acids for conventional, plant-based, and vegetarian diets at the protein prescription of (A) 0.5 g/kg/day and (B) 0.6 g/kg/day. Abbreviation: PLADO, plant-dominant. Amino acid abbreviations: Cys, cysteine; His, histidine; Leu, leucine; Lys, lysine; Met, methionine; Thr, threonine. Other essential amino acids such as tryptophan, isoleucine, phenylalanine, tyrosine, and valine are not included because all low protein diets meet the Recommended Dietary Allowance.
Figure 1. Percent of Recommended Dietary Allowance of selected essential amino acids for conventional, plant-based, and vegetarian diets at the protein prescription of (A) 0.5 g/kg/day and (B) 0.6 g/kg/day. Abbreviation: PLADO, plant-dominant. Amino acid abbreviations: Cys, cysteine; His, histidine; Leu, leucine; Lys, lysine; Met, methionine; Thr, threonine. Other essential amino acids such as tryptophan, isoleucine, phenylalanine, tyrosine, and valine are not included because all low protein diets meet the Recommended Dietary Allowance.
Nutrients 13 03341 g001
Nutrients 13 03341 g002 550
Figure 2. Potential renal acid load of all types of diets at different levels of protein prescription.
Figure 2. Potential renal acid load of all types of diets at different levels of protein prescription.
Nutrients 13 03341 g002
Table
Table 1. Macronutrient distribution and food groups of a conventional diet.
Table 1. Macronutrient distribution and food groups of a conventional diet.
LPD (g/kg BW)MHPD (g/kg BW)
0.50.60.70.81.01.11.2
Nutrients *
Energy (kcal)2100210021002100210021002100
Protein (% EN)78911131516
Protein (g)35424956707784
Carbohydrate (% EN)58575654545454
Carbohydrate (g)305299294284284284284
Fat (% EN)35353535333130
Fat (g)82828282777270
Food groups †
Cereals (exchange)8888131313
Fruits (exchange)3333333
Non-starchy vegetables (serving)4444444
Poultry/fish (exchange)2344566
Egg (exchange)0001112
Sugar (exchange)5443000
Fat (exchange)14141414131211
Abbreviations: BW, body weight; EN, energy; LPD, low protein diet; MHPD, moderately high protein diet. * Based on a body weight of 70 kg. † One exchange of cereal contains 15 g carbohydrate, 2 g protein, 0.5 g fat; one exchange of fruit or sugar contains 15 g carbohydrate; one exchange of poultry, fish, or egg contains 7 g protein; one exchange of fat contains 5 g fat; the portion size of one serving of cooked non-starchy vegetable is ½ cup.
Table
Table 2. Macronutrients, essential amino acid, and long-chain n-3 polyunsaturated fatty acid content of conventional, plant-based, and vegetarian low protein diets.
Table 2. Macronutrients, essential amino acid, and long-chain n-3 polyunsaturated fatty acid content of conventional, plant-based, and vegetarian low protein diets.
NutrientsReference †0.5 g/kg/Day or 35 g/Day *0.6 g/kg/Day or 42 g/Day *
ConventionalLacto-ovoPLADOOvoLactoVeganConventionalLacto-ovoPLADOOvoLactoVegan
Energy (kcal) 201620712047207820902098205921452088210021402138
Carbohydrate (g) 300301308311312324300302315298306325
Dietary fiber (g)29 a191921232327191923232432
Total protein (g) 363636363636434242424342
Animal protein (g) 15131168022191213110
Plant protein (g) 212325302836212330293242
Essential AA
Tryptophan (mg)350 a409441409417442408487524488500540470
Threonine (mg)1400 a137713531359132613231293168116311611160416101520
Isoleucine (mg)1330 a160816531586157916131531192719891879191519481802
Leucine (mg)2940 a267828662663266728072589324034103136321133963035
Lysine (mg)2660 a222620562147193420061906286125132601239125442326
Methionine +
Cysteine (mg)		1330 a133313841279125712131095161217101462158314111243
Phenylalanine +
Tyrosine (mg)		2310 a271530222738286729532779321836123234345735613258
Valine (mg)1680 a189520751872196219791833225125052171239123462121
Histidine (mg)980 a930875908857895881113410291089101111081054
Total fat (g) 778377808078788877858679
EPA+DHA (mg)250 b263212602100537422794200
NutrientsReference †0.7 g/kg/Day or 49 g/Day *0.8 g/kg/Day or 56 g/Day *
ConventionalLacto-ovoPLADOOvoLactoVeganConventionalLacto-ovoPLADOOvoLactoVegan
Energy (kcal) 207721702180214621852181208321952143218922292227
Carbohydrate (g) 295294318299309325282287299300311327
Dietary fiber (g)29 a192027282836192530323140
Total protein (g) 505050495049565657555555
Animal protein (g) 2925151314035251713140
Plant protein (g) 212535363649213140424155
Essential AA
Tryptophan (mg)350 a567623572574606545641689638649671619
Threonine (mg)1400 a197019191923186318461765224321602164210820562024
Isoleucine (mg)1330 a228823742250222322762090258226592526251125242399
Leucine (mg)2940 a375341193718371539703501423945904182418143684005
Lysine (mg)2660 a344331123180286230362756398935503652329133993226
Methionine +
Cysteine (mg)		1330 a188920081714175316641407213221661894191618061576
Phenylalanine +
Tyrosine (mg)		2310 a372143153849399941433761417548214311450245744302
Valine (mg)1680 a259029482530271827192421291332522839301829722748
Histidine (mg)980 a134612451318120612881233156714251493138514411428
Total fat (g) 799182878781839383898983
EPA+DHA (mg)250 b543422824200603424004200
Abbreviations: AA, amino acid, DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; PLADO, plant-dominant. Note: Table cells with grey shading indicate values below the reference value. * Represents dietary nutrient content for a 70 kg person. † The Reference values refer to Adequate Intake for dietary fiber [25], Recommended Daily Allowances for essential amino acids [25], and the recommended dietary requirement by FAO/WHO for n-3 polyunsaturated fatty acids [26]. a Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (2005) [25]. b Joint FAO/WHO Expert Consultation on Fats and fatty acids in Human Nutrition (2008) [26].
Table
Table 3. Macronutrients, essential amino acids, and long-chain n-3 polyunsaturated fatty acids of conventional, plant-based, and vegetarian moderately high protein diets.
Table 3. Macronutrients, essential amino acids, and long-chain n-3 polyunsaturated fatty acids of conventional, plant-based, and vegetarian moderately high protein diets.
NutrientsReference †1.0 g/kg/Day or 70 g/Day *1.1 g/kg/Day or 77 g/Day *1.2 g/kg/Day or 84 g/Day *
ConventionalLacto-ovoPLADOOvoLactoVeganConventionalLacto-ovoPLADOOvoLactoVeganConventionalLacto-ovoPLADOOvoLactoVegan
Energy (kcal) 214022202096227322242295209722652142224723062353207922902201229823402410
Carbohydrate (g) 286292289302315335286300297308331349286313310324345366
Dietary fiber (g)29 a233234404148253438424554253842464958
Total protein (g) 707170696970777879767778848586838584
Animal protein (g) 442523131305025251514058252815140
Plant protein (g) 264647565670275354616378266058687184
Essential AA
Tryptophan (mg)350 a80186579280081879087497689689192586995910489639621012936
Threonine (mg)1400 a282326872660259925472562309530013020288628642837341732323279312831403067
Isoleucine (mg)1330 a322833143113307331373011358837143529344335123333396039833818372638393609
Leucine (mg)2940 a532557115085512754495024586463395776570560415551644767866267616665656002
Lysine (mg)2660 a506245204461405343854043563650235140454948914538630254335644497453704962
Methionine +1330 a262625602244220421661905293328492497247623742085323730052698264525572228
Cysteine (mg)
Phenylalanine +2310 a527959835268555256725441579666715969618263166006634071546463668768826483
Tyrosine (mg)
Valine (mg)1680 a363139433468364836453408402244003930406540403753440046844241434643794061
Histidine (mg)980 a199918381833173118501801218820462095193020652004241522202280210822672179
Total fat (g) 818977928181738775838078678273797574
EPA+DHA (mg)250 b743424064200805425234200906425614200
Abbreviations: AA, amino acid, DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; PLADO, plant-dominant. Note: Table cells with grey shading indicate values below the reference value. * Represents dietary nutrient content for a 70 kg person. † The Reference values refer to Adequate Intake for dietary fiber [25], Recommended Daily Allowances for essential amino acids [25], and the recommended dietary requirement by FAO/WHO for n-3 polyunsaturated fatty acids [26]. a Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (2005) [25]. b Joint FAO/WHO Expert Consultation on Fats and fatty acids in Human Nutrition (2008) [26].
Table
Table 4. Macromineral, trace element, and vitamin content of conventional, plant-based, and vegetarian low protein diets.
Table 4. Macromineral, trace element, and vitamin content of conventional, plant-based, and vegetarian low protein diets.
NutrientsReference ‡0.5 g/kg/Day or 35 g/Day †0.6 g/kg/Day or 42 g/Day †
MaleFemaleConven-tionalLacto-ovoPLADOOvoLactoVeganConven-tionalLacto-ovoPLADOOvoLactoVegan
Sodium * (mg)<2300 a108857310826116925481120643758681728551
Potassium (mg) 193619522003199221142149209320192135200922122311
Phosphorus (mg) 525670563632705646606766651725818759
P/Prot ratio 14.518.615.517.719.418.014.118.115.417.219.018.0
Calcium (mg)800–1000 a264557341457634551270584486484812604
Magnesium (mg)420 b320 b222230237243248269233236260247266294
Copper (μg)900 c8389309651101101612568549811122113311001434
Manganese (mg)2.3 c1.8 c6.16.16.56.76.47.36.16.16.96.26.27.2
Iron (mg)8 c18 c,d111313151417111415161620
Zinc (mg)11 c8 c565666566677
Thiamine (mg)1.2 e1.1 e1.21.21.21.21.31.31.21.21.21.31.31.4
Riboflavin (mg)1.3 e1.1 e0.71.10.70.91.00.70.81.30.81.11.10.7
Niacin (mg)16 e14 e151114111112171115111112
Pyridoxine (mg)5.0 f1.31.11.31.21.11.21.41.21.31.31.21.3
Folate (μg)400 e483529532613584674484552584624604770
Cobalamin (μg)2.4 e2.31.32.20.60.80.05.31.93.11.31.10.0
NutrientsReference ‡0.7 g/kg/Day or 49 g/Day†0.8 g/kg/Day or 56 g/Day†
MaleFemaleConven-tionalLacto-ovoPLADOOvoLactoVeganConven-tionalLacto-ovoPLADOOvoLactoVegan
Sodium * (mg)<2300 a1135626110668549255811519001114692497561
Potassium (mg) 212121632282218324582486215723082406235725852660
Phosphorus (mg) 64493676584698186669410548619541069988
P/Prot ratio 12.918.815.217.319.617.912.418.715.217.219.317.8
Calcium (mg)800–1000 a2737965175698917242778515616891006809
Magnesium (mg)420 b320 b238252290275292324242279305304316352
Copper (μg)900 c8571012131313291241162185011881395151614041817
Manganese (mg)2.3 c1.8 c5.95.57.06.36.07.35.45.26.26.36.17.3
Iron (mg)8 c18 c,d121417191723121719222026
Zinc (mg)11 c8 c577788687899
Thiamine (mg)1.2 e1.1 e1.21.31.31.41.41.51.31.41.41.51.51.6
Riboflavin (mg)1.3 e1.1 e0.81.50.81.11.20.70.81.50.81.11.20.8
Niacin (mg)16 e14 e191116121213201117121213
Pyridoxine (mg)5.0 f1.51.21.51.41.31.41.61.31.61.51.41.5
Folate (μg)400 e481566668722700843470655708795759941
Cobalamin (μg)2.4 e5.32.53.11.31.40.05.82.53.81.31.40.0
Abbreviations: P/Prot, phosphorus/protein; PLADO, plant-dominant. Note: Table cells with grey shading indicate values below or exceeding the reference value. * Only sodium naturally found in food without condiments added during cooking, table salt, or sauces. † Represents dietary nutrient content for a 70 kg person. ‡ The reference value refers to the CKD-specific recommendation for dietary sodium, calcium [3], and pyridoxine [30]; Recommended Dietary Allowance for magnesium, copper, iron, zinc, thiamine, riboflavin, niacin, folate, and cobalamin [27,28,29] and Adequate Intake for manganese [29]. a KDOQI Clinical Practice Guideline for Nutrition in CKD: 2020 Update [3]. b Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride (1997) [27]. c Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc (2000) [29]. d RDA for women 19–50 years old only. The RDA for women >50 years old is 8 mg/day [29]. e Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin, and Choline (1998) [28]. f Kopple et al. 1981 [30].
Table
Table 5. Macromineral, trace element, and vitamin content of standard, plant-based, and vegetarian moderately high protein diets.
Table 5. Macromineral, trace element, and vitamin content of standard, plant-based, and vegetarian moderately high protein diets.
NutrientsReference ‡1.0 g/kg/Day or 70 g/Day †1.1 g/kg/Day or 77 g/Day †1.2 g/kg/Day or 84 g/Day †
MaleFemaleConven-tionalLacto-ovoPLADOOvoLactoVeganConven-tionalLacto-ovoPLADOOvoLactoVeganConventionalLacto-ovoPLADOOvoLactoVegan
Sodium * (mg)<2300 a10596918827865596581107749894828583667969755918834590672
Potassium (mg) 247126702701274529883045260229093003293733173351269830873245311935523623
Phosphorus (mg) 85412589811160128111998991363112912371434133696114671242134715541452
P/Prot ratio 12.217.814.116.818.517.111.717.414.316.218.517.211.417.414.516.318.317.3
Calcium (mg)800–1000 a3201173682830124110233261328796971141311183301442821106415671198
Magnesium (mg)420 b320 b283346350373385428289372384397423467296401411429458496
Copper (μg)900 c997155115361867176922249881670172820001988246099418671882222922122640
Manganese (mg)2.3 c1.8 c5.35.55.66.16.17.55.15.85.96.56.78.05.16.36.27.17.38.5
Iron (mg)8 c18 c,d142322272631142525292934142827323337
Zinc (mg)11 c8 c7108101011711910111271110111213
Thiamine (mg)1.2 e1.1 e1.61.61.61.81.81.91.61.71.81.81.92.01.61.81.91.92.02.1
Riboflavin (mg)1.3 e1.1 e1.01.60.91.21.20.81.11.80.91.31.40.91.21.91.01.41.41.0
Niacin (mg)16 e14 e241320141415241421151516271423151617
Pyridoxine (mg)5.0 f1.81.51.81.71.61.81.91.62.01.81.82.02.01.72.21.91.92.1
Folate (μg)400 e537797746925915106555483884096510281178554897922106211141279
Cobalamin (μg)2.4 e7.32.54.82.31.21.07.72.75.42.31.41.09.82.77.12.31.41.0
Abbreviations: P/Prot, phosphorus/protein; PLADO, plant-dominant. Note: Table cells with grey shading indicate values below or exceeding the reference value. * Only sodium naturally found in food without condiments added during cooking, table salt, or sauces. † Represents dietary nutrient content for a 70 kg person. ‡ The reference value refers to the CKD-specific recommendation for dietary sodium, calcium [3], and pyridoxine [30]; Recommended Dietary Allowance for magnesium, copper, iron, zinc, thiamine, riboflavin, niacin, folate, and cobalamin [27,28,29] and Adequate Intake for manganese [29]. a KDOQI Clinical Practice Guideline for Nutrition in CKD: 2020 Update [3]. b Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride (1997) [27]. c Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc (2000) [29]. d RDA for women 19–50 years old only. The RDA for women >50 years old is 8 mg/day [28]. e Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin, and Choline (1998) [28]. f Kopple et al. 1981 [30].
Table
Table 6. Selected essential amino acids of protein food sources (7 g protein).
Table 6. Selected essential amino acids of protein food sources (7 g protein).
Fish (King Mackerel)ChickenEggWhole MilkTofuLentilsChickpeas
Weight (g)353056220877880
Protein (g)7777777
Leucine (mg)577520609583534510505
Leucine RDA * (%)20182120181717
Lysine (mg)652589512308463491474
Lysine RDA * (%)25221912171818
Methionine (mg)210192213165906093
Cysteine (mg)768915237979295
Methionine + cysteine RDA * (%)22212715141114
Source: FoodData Central Database of the United States Department of Agriculture [23]. * The RDAs for Leucine, Lysine, and Methionine + Cysteine were 2940 mg, 2660 mg, and 1330 mg (based on the reference body weight of 70 kg).
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Khor, B.-H.; Tallman, D.A.; Karupaiah, T.; Khosla, P.; Chan, M.; Kopple, J.D. Nutritional Adequacy of Animal-Based and Plant-Based Asian Diets for Chronic Kidney Disease Patients: A Modeling Study. Nutrients 2021, 13, 3341. https://doi.org/10.3390/nu13103341

AMA Style

Khor B-H, Tallman DA, Karupaiah T, Khosla P, Chan M, Kopple JD. Nutritional Adequacy of Animal-Based and Plant-Based Asian Diets for Chronic Kidney Disease Patients: A Modeling Study. Nutrients. 2021; 13(10):3341. https://doi.org/10.3390/nu13103341

Chicago/Turabian Style

Khor, Ban-Hock, Dina A. Tallman, Tilakavati Karupaiah, Pramod Khosla, Maria Chan, and Joel D. Kopple. 2021. "Nutritional Adequacy of Animal-Based and Plant-Based Asian Diets for Chronic Kidney Disease Patients: A Modeling Study" Nutrients 13, no. 10: 3341. https://doi.org/10.3390/nu13103341

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop