Next Article in Journal
Short-Term Effects of a Ready-to-Drink Pre-Workout Beverage on Exercise Performance and Recovery
Previous Article in Journal
Effects of Popular Diets without Specific Calorie Targets on Weight Loss Outcomes: Systematic Review of Findings from Clinical Trials
Previous Article in Special Issue
Pregnancy, Proteinuria, Plant-Based Supplemented Diets and Focal Segmental Glomerulosclerosis: A Report on Three Cases and Critical Appraisal of the Literature
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Dietary Approaches in the Management of Diabetic Patients with Kidney Disease

by
Gang Jee Ko
1,2,
Kamyar Kalantar-Zadeh
1,3,4,
Jordi Goldstein-Fuchs
5,6 and
Connie M. Rhee
1,*
1
Harold Simmons Center for Kidney Disease Research and Epidemiology, Division of Nephrology and Hypertension, University of California Irvine, School of Medicine, Orange, CA 92868, USA
2
Department of Internal Medicine, Korea University, School of Medicine, Seoul 08308, Korea
3
Department of Medicine, Tibor Rubin Veteran Affairs Health System, Long Beach, CA 90822, USA
4
Los Angeles Biomedical Research Institute at Harbor-UCLA, Torrance, CA 90502, USA
5
Sierra Nevada Nephrology Consultants, Reno, NV 89511, USA
6
Department of Internal Medicine, University of Nevada Reno, School of Medicine, Reno, NV 89557, USA
*
Author to whom correspondence should be addressed.
Nutrients 2017, 9(8), 824; https://doi.org/10.3390/nu9080824
Submission received: 5 July 2017 / Revised: 22 July 2017 / Accepted: 25 July 2017 / Published: 31 July 2017
(This article belongs to the Special Issue Nutrition and Chronic Kidney Disease)

Abstract

:
Chronic kidney disease (CKD) is one of the most prevalent complications of diabetes, and patients with diabetic kidney disease (DKD) have a substantially higher risk of cardiovascular disease and death compared to their non-diabetic CKD counterparts. In addition to pharmacologic management strategies, nutritional and dietary interventions in DKD are an essential aspect of management with the potential for ameliorating kidney function decline and preventing the development of other end-organ complications. Among DKD patients with non-dialysis dependent CKD, expert panels recommend lower dietary protein intake of 0.8 g/kg of body weight/day, while higher dietary protein intake (>1.2 g/kg of body weight/day) is advised among diabetic end-stage renal disease patients receiving maintenance dialysis to counteract protein catabolism, dialysate amino acid and protein losses, and protein-energy wasting. Carbohydrates from sugars should be limited to less than 10% of energy intake, and it is also suggested that higher polyunsaturated and monounsaturated fat consumption in lieu of saturated fatty acids, trans-fat, and cholesterol are associated with more favorable outcomes. While guidelines recommend dietary sodium restriction to less than 1.5–2.3 g/day, excessively low sodium intake may be associated with hyponatremia as well as impaired glucose metabolism and insulin sensitivity. As patients with advanced DKD progressing to end-stage renal disease may be prone to the “burnt-out diabetes” phenomenon (i.e., spontaneous resolution of hypoglycemia and frequent hypoglycemic episodes), further studies in this population are particularly needed to determine the safety and efficacy of dietary restrictions in this population.

1. Introduction

Epidemiologic data show that the prevalence of diabetes is increasing worldwide, particularly in the United States (US) where 29.1 million people (9.3% of the population) are estimated to have diabetes [1]. While longitudinal data from the US show that the incidence of diabetic end-organ complications has declined over the past two decades [2], diabetes remains a major source of morbidity and mortality due to its staggering rise in prevalence [3]. Indeed, United States Renal Data System (USRDS) registry data show that diabetes accounts for nearly half of the end-stage renal disease (ESRD) population in the US [4]. Thus, two major goals in the management of diabetic kidney disease (DKD) are stabilization of kidney function and prevention of the development of other end-organ complications. Provision of balanced nutritional therapy, in conjunction with pharmacologic interventions that optimize glycemic status, lipid levels, and blood pressure, are cornerstones of the management of DKD patients [5]. In this review, we summarize current clinical practice guidelines and supporting evidence regarding the nutritional management of patients with DKD.

2. Clinical Practice Guidelines on the Nutritional Management of Diabetic Kidney Disease

While nutritional therapy is an essential aspect of the treatment of DKD, current clinical practice guidelines (Figure 1) do not wholly address all areas of dietary management due to existing controversies and gaps in knowledge about particular interventions (e.g., dietary protein restriction) in this population (Figure 2). Furthermore, recommendations may differ across the stages of DKD due to differential risk-to-benefit ratio profiles of certain management strategies across varying levels of kidney function. For example, among advanced chronic kidney disease (CKD) and ESRD patients who may be susceptible to hypoglycemia, intensive glycemic control may be associated with heightened risk of adverse outcomes [6,7]. In 2007, the National Kidney Foundation (NKF) Kidney Disease Outcome Quality Initiative (KDOQI) Clinical Practice Guidelines for the Nutritional Management of Diabetes and CKD was first introduced [8]. These seminal guidelines were primarily focused upon recommending dietary protein restriction among DKD patients, with a specific target dietary protein intake of 0.8 g/kg of body weight (BW)/day (approximately 10% of total caloric intake) among those with stages 1–4 CKD based on moderate to strong evidence. A similar management strategy for DKD patients with stage 5 CKD was also advised. However, in 2012, a Kidney Disease Improving Global Outcome (KDIGO) expert panel recommended comparatively liberal parameters with respect to dietary protein intake, advising that it should be maintained at 0.8 g/kg BW/day while avoiding levels above 1.3 g/kg BW/day [9]. KDIGO guidelines also highlighted that there was insufficient evidence demonstrating that long term restriction of dietary protein intake below 0.8 g/kg BW/day is beneficial in DKD patients. Other experts suggest a low protein intake of 0.6 to 0.8 g/kg/day including 25% to 50% of high biologic value protein as a more effective dietary strategy [10,11].
In 2014, a consensus conference for DKD convened by the American Diabetes Association (ADA) in collaboration with the American Society of Nephrology (ASN) and the National Kidney Foundation (NKF) summarized existing evidence and issued updated recommendations regarding the optimal intake of various macro-nutrients. With respect to dietary protein intake, the expert panel recommended a “usual level of dietary protein intake” among DKD patients of approximately 16−18% of total caloric intake [12]. The panel′s recommendations regarding optimal intake of other macro-nutrients are summarized in Table 1.

3. Dietary Protein Intake in Diabetic Kidney Disease: Non-Dialysis Dependent Chronic Kidney Disease

3.1. Quantity of Dietary Protein Intake

Dietary protein requirements among diabetic patients without kidney disease are considered to be equivalent to that of the general population. In the general population, National Health and Nutritional Examination Survey (NHANES) data demonstrated that the average dietary protein intake of US adults is 1.34 g/kg of ideal body weight (IBW)/day or 1.09 g/kg of actual body weight (ABW)/day, which substantially exceeds the requisite amount needed to avoid negative nitrogen balance for normal healthy adults (i.e., 0.8 g/kg ABW/day) [9,13]. When examined according to demographic characteristics, higher dietary protein intake was observed among men vs. women (1.36 vs. 1.25 g/kg IBW/day, respectively); Mexican-American and Latino participants vs. other racial/ethnic groups (1.43, 1.24, 1.30, and 1.35 g/kg IBW/day among Mexican-American/Latino, non-Hispanic Black, non-Hispanic White, and other racial/ethnic groups, respectively). Incrementally higher dietary protein intake was also observed in younger vs. older aged participants (1.40, 1.38, 1.32, 1.22, 1.16, and 1.08 g/kg IBW/day for participants 20–34, 35–44, 45–54, 55–64, 65–74, and ≥74 years of age, respectively). However, little is known about how dietary protein intake varies among diabetic vs. non-diabetic patients in the broader US population.
It should be noted that type 2 diabetic patients may be more frequently exposed to protein-rich food sources as a means (1) to promote weight loss, such as fad dietary regimens including the Atkins or Protein Power diets; or (2) to avoid postprandial hyperglycemia by replacing carbohydrate-rich foods with protein-rich foods [8,14]. However, receipt of these high protein diets may heighten diabetic patients′ risk of developing impaired renal function [15]. In contrast to fats and carbohydrates, high dietary protein intake increases glomerular filtration rates (GFRs) in order to excrete protein-derived nitrogen metabolites [16,17,18], as shown in a recent meta-analysis of 30 randomized controlled trials (RCTs) that included 2160 participants [19]. Renal hemodynamic changes induced by excess protein intake may also exert deleterious consequences over time. For example, a population-based study of patients with mild kidney dysfunction (estimated GFR (eGFR) 55–80 mL/min/1.73 m2) who had long-term consumption of a high protein diet (20% versus 10% of total daily calories) showed a significant decline in kidney function over an 11-year follow up period [20]. Although current nutritional guidelines for diabetic patients without kidney disease have not recommended dietary protein restriction [21], avoidance of excess dietary protein intake may be beneficial in preventing long-term renal complications.
Among patients with DKD, the potential benefits and risks of a low protein diet (LPD) have been widely debated. Many studies, including RCTs, have shown a beneficial impact of LPD upon trajectory of kidney function in this population [22,23,24,25,26]. More specifically, it has been suggested that a LPD, often used in conjunction with essential amino acids and ketoacids, may reduce proteinuria, uremic burden, metabolic derangements (e.g., metabolic acidosis), and oxidative stress leading to attenuation in the progression of CKD and delayed initiation of dialysis treatment [11,27,28]. Conversely, other studies have not confirmed that a LPD favorably impacts CKD trajectory [29,30,31]. A Cochrane review of 12 RCTs concluded that administration of LPDs showed a small but non-significant benefit upon slowing of eGFR decline [32]. It should be noted that the study populations’ sizes and stages of CKD, as well as durations of treatment intervention were highly variable across studies, and adherence to dietary recommendations were not systematically assessed (i.e., actual protein intake may have differed from prescribed intake). In a meta-analysis of 13 RCTs, LPD was associated with significant improvement in eGFR (5.82 (95% CI) (2.30 to 9.33) mL/min/1.73 m2) [33]. These beneficial effects were observed independent of the type of diabetes, stage of CKD, and duration of the intervention. However, in subgroup analyses that assessed dietary compliance using urinary urea excretion, improvement in eGFR was observed only among those in whom compliance was fair. Notably, another meta-analysis has shown a differential effect of dietary protein restriction upon CKD progression according to type of diabetes, such that restriction was beneficial in type 1 diabetic patients but not in those with type 2 diabetes [34]. However, it should be noted that the meta-analysis had proportionately fewer studies of type 2 diabetes patients. Another prospective study of type 2 diabetic patients has demonstrated that a LPD was beneficial upon kidney function and proteinuria trajectory over a three-year period [35].

3.2. Sources of Dietary Protein Intake

In addition to quantity, the quality and characteristics of dietary protein intake and their impact upon kidney function have also been a focus of investigation in the broader CKD population. In an RCT with follow up over four years, soy protein consumption as a replacement for animal sources of protein (35% animal, 35% soy-origin, and 30% vegetable proteins) was associated with significant improvement in proteinuria as compared with usual protein consumption (70% animal and 30% vegetable proteins) [36]. A recent prospective observational study of 63,257 participants in Singapore has also shown that incrementally higher red meat intake was strongly associated with increasingly higher risk of ESRD in a dose-dependent manner (HR (95% CI) for the highest vs. lowest quartiles of intake: 1.40 (1.15–1.71)) [37]. However, a secondary analysis of type 2 diabetic patients with proteinuria from the Ongoing-Telmisartan-Alone-and-in-combination-with-Ramipril-Global-Endpoint-Trial (ONTARGET) showed that higher animal protein intake was associated with a lower risk of CKD, albeit a non-significant difference. Furthermore, plant protein (defined as protein from tofu/soybean curd, legumes, and whole and refined grains) consumption was not found to be associated with CKD progression, although greater vegetable (leafy green, raw, and cooked vegetables) and fruit consumption was associated with lower risk of CKD progression [38].
Varying sources of dietary protein may also differentially impact CKD-related complications in DKD patients. For example, it has been suggested that higher consumption of vegetable protein sources among patients with advanced CKD may result in phosphate and potassium derangements. In a report of stage 3–4 CKD patients who were administered an omnivore diet containing 70% of protein from plant sources over a four-week period, lower phosphate, sodium, and titratable acid excretion in urine were observed; in contrast, there were no significant changes in serum phosphorus, parathyroid hormone, nor Fibroblast-Growth-Factor 23 level according to dietary protein source [39]. In addition, two episodes of mild hyperkalemia were reported which were corrected with food substitutions. Yet in a study of 14,866 participants from the NHANES III cohort, a higher proportion of dietary protein intake from plant sources (plant protein to total protein ratio) was associated with lower mortality in those with eGFR < 60 mL/min/1.73 m2, but not in those with eGFR ≥ 60 mL/min/1.73 m2 [40]. Future studies are needed to determine the effect of protein type upon kidney function and other relevant outcomes in the DKD population.

4. Dietary Protein Intake in Diabetic Kidney Disease Patients Receiving Dialysis

It should be highlighted that the aforementioned guidelines and studies do not apply to diabetic patients with ESRD receiving dialysis. Given that ESRD patients are predisposed to protein catabolism and losses of protein and amino acids in the dialysate [41], dietary protein restriction may lead to protein energy malnutrition (PEW), a potent predictor of mortality in this population [42]. Several observational studies have shown that low dietary protein intake ascertained by protein equivalent of nitrogen appearance normalized to body weight (nPNA) is associated with higher hospitalization and mortality risk in hemodialysis patients [43,44]. The National Kidney Foundation- Kidney Disease Outcomes Quality Initiative (NKF-KDOQI) Guidelines for Dialysis Patients indeed recommend higher dietary protein intake (>1.2 g/kg BW/day) as compared to non-dialysis dependent CKD patients [45]. While various markers of overnutrition, such as increased body mass index or high serum cholesterol levels, have shown deleterious effects upon cardiovascular disease and death in the general population, multiple observational studies have paradoxically shown survival benefit in dialysis patients [46,47]. Notably, in a Taiwanese study of 21 vegetarian dialysis patients and 42 age- and sex-matched non-vegetarian dialysis patients selected as controls, those who followed vegetarian diets demonstrated markers of subclinical protein malnutrition and vitamin D deficiency [48]. Indeed, monitored liberalization of protein intake is needed to ensure adequate dietary intake and prevention of PEW in diabetic ESRD patients receiving dialysis [49].

5. Energy and Carbohydrate Intake in Diabetic Kidney Disease

In the broader CKD population, including those who are non-dialysis and dialysis dependent, the NKF-KDOQI guidelines and the International Society of Renal Nutrition and Metabolism recommend a total energy intake of 30–35 kcal/kg BW/day which should be tailored to physical activity levels [45,50]. In elderly patients who are sedentary, energy intake of 30 kcal/kg BW/day may be sufficient. These recommendations apply to all non-dialysis and dialysis dependent CKD patients irrespective of their etiology of kidney disease (i.e., diabetic and non-diabetic kidney disease).
Avoidance of obesity is also an important strategy in preventing the development and progression of CKD. For example, observational studies have shown that obesity is associated with a higher incidence of CKD, and moderate weight reduction (5–10% of body weight) has been recommended in obese CKD patients to prevent kidney disease progression [51]. In addition to increased physical activity, reduction of caloric intake by 500–750 kcal/day or an intake of 1200–1500 kcal/day in women and 1500–1800 kcal/day in men is recommended in patients with type 2 diabetes of overweight or obese status [6,52]. However, a low carbohydrate diet that is replaced by high dietary protein sources should be avoided in DKD patients [53] given the harmful effects of a high protein diet on CKD trajectory, as described above. Experimental animal models have shown that, while low-carbohydrate, high-protein diets led to leaner body habitus in mice, those that received high-carbohydrate, low-protein diets experienced less illness, lower blood pressure, better glucose tolerance, lower cholesterol levels, and longer life span [54]. Observational data from NHANES has also demonstrated that diabetic participants with high protein intake (≥20% of total caloric intake) as assessed by dietary interview had higher risk of mortality compared to those with ≤10% of caloric intake from protein. These associations were attenuated if the source of proteins were plant-based [55]. However, another study demonstrated that high carbohydrate intake was associated with higher risk of CKD [38]. In conclusion, there remain substantial knowledge gaps with respect to the impact of carbohydrate intake upon outcomes in DKD patients [56], and future studies in this area are warranted. Given that ~45–60% of energy intake is obtained from carbohydrate sources [6], careful consideration should be made with respect to the source of dietary carbohydrates. For example, carbohydrates from sugars should be restricted to less than 10% of energy intake, and higher glycemic index foods should be substituted with low glycemic index foods such as whole grains, fiber, fresh fruit, and vegetables [7,8,12]. However, these types of food are often restricted in advanced stages of DKD given their high potassium and phosphorus content. Thus, consumption of fruits and vegetables with low potassium content, appropriate prescription of phosphorus binders, avoidance of processed convenience foods with high phosphorus content, and cooking procedures that reduce potassium and phosphorus levels in food are recommended [5].

6. Fat Intake in Diabetic Kidney Disease

There are multiple areas of uncertainty surrounding ideal dietary fat intake in DKD. [12] Although treatment of dyslipidemia is a critical aspect of the management of DKD patients given their high risk of cardiovascular disease and death [57,58], the optimal amount of dietary fat intake has not yet been defined. There is a general consensus across guidelines that a reduction of saturated fatty acids (SFA) and trans-fat intake contributes to a reduction in risk of cardiovascular disease in patients with diabetes [7,59]. Thus, it is typically recommended that saturated fats be limited to <7% of total daily calories [7,21,60]. Existing literature indicate that the type of fat consumed has a greater bearing upon metabolic status than total fat intake per se. Omega-3 and 6 polyunsaturated fatty acids (PUFAs) and monounsaturated fatty acids (MUFAs) were found to have beneficial impact upon DKD outcomes through the attenuation of inflammation and endothelial dysfunction and improved control of hypertension and dyslipidemia [61]. In a multicenter prospective study of 192 patients with type 1 and 2 diabetes and albuminuria, those who experienced a rise in albuminuria over time had higher SFA to PUFA ratios of dietary fat consumption after a seven-year follow up period [62]. Another secondary analysis of patients with type 1 diabetes from the Diabetes Control and Complication Trial (DCCT) showed that the absolute level of albuminuria was lower among those with greater long chain omega-3 PUFA consumption [63]. However, PUFA consumption did not impact the incidence of new onset albuminuria. A recent case-control study also observed a marginally significant inverse trend between higher dietary PUFA intake and lower incidence of ESRD [64]. These observations corroborate data from studies in the general population which have generally shown a protective effect of omega-3 upon cardiovascular outcomes [61]. However, it should be noted that the Outcome-Reduction-with-an-Initial-Glargine-Intervention (ORIGIN) trial of 12,537 patients with impaired fasting glucose, impaired glucose tolerance, or type 2 diabetes showed a negative effect of omega-3 PUFA upon cardiovascular disease and mortality [65].

7. Sodium Intake in Diabetic Kidney Disease

Prior data has shown that low dietary sodium intake is associated with reductions in blood pressure and proteinuria in CKD patients, which may be extrapolated to DKD patients [5,66]. Current nutritional guidelines for DKD patients uniformly recommend restriction of dietary sodium intake to less than 1.5–2.3 g/day (5 g of sodium chloride) [8,9,12]. However, some studies have reported that excessively low sodium intake adversely affects glucose metabolism and decreases insulin sensitivity. In addition, the activation of the renin–angiotensin–aldosterone system and sympathetic nervous system following low dietary sodium intake may further reduce insulin sensitivity [67]. At this time, sodium restriction should be individualized, and further research examining sodium intake thresholds and outcomes across various populations is needed.

8. Comparison of Prescribed Diets

An alternative approach in the management of chronic disease populations, such as those with diabetes, hypertension, and CKD, is to prescribe a comprehensive diet, such as the Dietary Approaches to Stop Hypertension (DASH) and Mediterranean diets, as opposed to focusing on individual nutrients. For example, both of the aforementioned diets emphasize a greater intake of vegetables, whole grains (i.e., complex and unrefined carbohydrates), and fruit and plant proteins (e.g., nuts, seeds, and beans). Compared to Western diets, they also have a lower proportion of animal protein and whole-fat dairy products. Studies of the DASH diet have suggested that it has a favorable impact upon blood pressure and the incidence of diabetes, although it is unknown as to whether this is due to its protein content or other components (e.g., potassium or isoflavones) [60,68,69]. In a study of 14,882 patients with an eGFR ≥ 60 mL/min/1.73 m2 from the Atherosclerosis-Risk-In-Communities (ARIC) cohort, the DASH diet was associated with lower risk of kidney disease after a median follow up of 23 years, independent of socio-demographics and baseline kidney function [70]. Most recently, a study of 1630 participants without underlying CKD from the Tehran Lipid and Glucose Study conducted food frequency questionnaire assessment with assignment of DASH-style diet scores based on these data [71,72]. After a mean follow up of six years, it was found that participants in the highest quintile of the DASH-style diet had a lower incidence of CKD compared to those in the lowest quintile. However, given that the DASH diet prescribes a higher level of dietary protein intake (~<1.4 g/kg BW/day), application of this diet to DKD patients with non-dialysis dependent CKD should be modified. An RCT of the DASH diet (containing 18% energy from protein) versus control diet administered over eight weeks did not show improvement in albuminuria, while reductions were seen in those who received a fruit and vegetable diet [73]. The high potassium (4.5 g/day) and phosphorus (1.7 g/day) content of the DASH diet may also limit its broad implementation in advanced CKD. Given that the DASH trial only enrolled participants with preserved renal function (eGFR ≥ 60 mL/min/1.73 m2 and serum creatinine <1.2 mg/dL), its safety and efficacy in those with moderate to advanced stages of CKD are unknown [60].
Compared to the DASH diet, characteristics of the Mediterranean diet include a high monounsaturated versus saturated fat ratio by using olive oil, as well as moderate red wine consumption. In spite of unrestricted fat consumption, many studies demonstrated that it resulted in a lower incidence of major cardiovascular events and type 2 diabetes [7,74,75]. However, there were no differences in all-cause mortality between the DASH versus control diets [76]. The Mediterranean diet has also been associated with lower risk of metabolic syndrome after kidney transplantation [77]. With respect to kidney disease outcomes, a 15-year observational study demonstrated that adherence to the Mediterranean diet was associated with lower risk of rapid decline in eGFR [78]. An RCT has also shown that the Mediterranean diet led to significant improvement in eGFR after two years. However, similar reno-protective effects were observed in those who received low carbohydrate and fat diets [79]. Further studies of the impact of the DASH and Mediterranean diets upon DKD outcomes are needed.

9. Practical Implementation of Nutritional Management

While adherence to nutritional guidelines may be challenging among DKD patients who bear multiple concurrent comorbidities resulting in complex medication regimens and recommendations from multiple providers, several strategies may be implemented that enhance its successful implementation. For example, data has shown that self-monitoring of food intake and feedback by clinicians can substantially improve adherence [80]. Frequent and clear communication with DKD patients about the importance of diet in their overall chronic disease management may further encourage adherence [81]. Using simplified diet approaches and instructions, as well as periodic monitoring of dietary intake with questionnaires administered by clinicians, particularly renal dietitians, may also augment compliance [82,83]. In an RCT of stage 3 CKD patients, a renal nutrition education program that included individual classes and hands-on sessions about food types and recipes improved adherence to dietary recommendations [84]. Obtaining patients’ feedback upon preferred food types and tolerability is also an indispensable aspect of successful nutritional management [85].

10. Future Areas for Research

There are multiple areas of uncertainty with respect to the nutritional management of DKD patients, including (1) the optimal amount of dietary protein intake among non-dialysis dependent CKD patients with diabetes, as well as (2) the comparative effects of animal vs. plant-based protein sources upon CKD and cardiovascular outcomes; (3) the preferred types and amounts of dietary fats in the DKD diet; (4) the role of complex carbohydrate foods upon DKD outcomes; (5) the ideal proportion of food types in DKD diets; and (6) the impact of “healthy diets” such as the DASH and Mediterranean diets upon outcomes in moderate to advanced CKD patients. It should also be noted that patients with advanced DKD progressing to end-stage renal disease may experience spontaneous resolution of hypoglycemia, normalization of glycated hemoglobin levels, and frequent hypoglycemic episodes necessitating discontinuation of anti-diabetic medications, known as the “burnt-out diabetes” phenomenon [86], and further studies in this population are particularly needed to determine the safety and efficacy of dietary restrictions in this population [49]. Given the exceedingly high morbidity and mortality of DKD patients, as well as compelling evidence demonstrating the critical importance of nutritional status in the broader CKD population, future studies that define the optimal nutritional management of this population may have a major impact upon improving the health and survival of this population.

Acknowledgments

The authors are supported by the research grants from the NIH/NIDDK, including K23-DK102903 (CMR), K24-DK091419 (KKZ), and philanthropist grants from Harold Simmons, Louis Chang, and Joseph Lee.

Author Contributions

Study concept and design: G.J.K., C.M.R., K.K.-Z., J.G.-F.; Drafting of the manuscript: G.J.K.; Critical revision of the manuscript for important intellectual content: G.J.K., C.M.R., K.K.-Z., J.G.-F.; Manuscript supervision: C.M.R.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Centers for Disease Control and Prevention. National Diabetes Statistics Report: Estimates of Diabetes and Its Burden in the United States; US Department of Health and Human Services: Atlanta, GA, USA, 2014.
  2. Gregg, E.W.; Li, Y.; Wang, J.; Burrows, N.R.; Ali, M.K.; Rolka, D.; Williams, D.E.; Geiss, L. Changes in diabetes-related complications in the united states, 1990–2010. N. Engl. J. Med. 2014, 370, 1514–1523. [Google Scholar] [CrossRef] [PubMed]
  3. Satirapoj, B.; Adler, S.G. Prevalence and management of diabetic nephropathy in western countries. Kidney Dis. 2015, 1, 61–70. [Google Scholar] [CrossRef] [PubMed]
  4. Collins, A.J.; Foley, R.N.; Chavers, B.; Gilbertson, D.; Herzog, C.; Ishani, A.; Johansen, K.; Kasiske, B.L.; Kutner, N.; Liu, J.; et al. US Renal Data System 2013 Annual Data Report. Am. J. Kidney Dis. 2014, 63, A7. [Google Scholar] [CrossRef] [PubMed]
  5. Goldstein-Fuchs, J.; Kalantar-Zadeh, K. Nutrition intervention for advanced stages of diabetic kidney disease. Diabetes Spectr. 2015, 28, 181–186. [Google Scholar] [CrossRef] [PubMed]
  6. Whitham, D. Nutrition for the prevention and treatment of chronic kidney disease in diabetes. Can. J. Diabetes 2014, 38, 344–348. [Google Scholar] [CrossRef] [PubMed]
  7. Ley, S.H.; Hamdy, O.; Mohan, V.; Hu, F.B. Prevention and management of type 2 diabetes: Dietary components and nutritional strategies. Lancet 2014, 383, 1999–2007. [Google Scholar] [CrossRef]
  8. KDOQI. KDOQI clinical practice guidelines and clinical practice recommendations for diabetes and chronic kidney disease. Am. J. Kidney 2007, 49, S12–154. [Google Scholar]
  9. Kovesdy, C.P.; Kopple, J.D.; Kalantar-Zadeh, K. Management of protein-energy wasting in non-dialysis-dependent chronic kidney disease: Reconciling low protein intake with nutritional therapy. Am. J. Clin. Nutr. 2013, 97, 1163–1177. [Google Scholar] [CrossRef] [PubMed]
  10. Kalantar-Zadeh, K.; Moore, L.W.; Tortorici, A.R.; Chou, J.A.; St-Jules, D.E.; Aoun, A.; Rojas-Bautista, V.; Tschida, A.K.; Rhee, C.M.; Shah, A.A.; et al. North american experience with low protein diet for non-dialysis-dependent chronic kidney disease. BMC Nephrol. 2016, 17, 90. [Google Scholar] [CrossRef] [PubMed]
  11. Ko, G.J.; Obi, Y.; Tortorici, A.R.; Kalantar-Zadeh, K. Dietary protein intake and chronic kidney disease. Curr. Opin. Clin. Nutr. Metab. Care 2017, 20, 77–85. [Google Scholar] [CrossRef] [PubMed]
  12. Tuttle, K.R.; Bakris, G.L.; Bilous, R.W.; Chiang, J.L.; de Boer, I.H.; Goldstein-Fuchs, J.; Hirsch, I.B.; Kalantar-Zadeh, K.; Narva, A.S.; Navaneethan, S.D.; et al. Diabetic kidney disease: A report from an ada consensus conference. Am. J. Kidney Dis. 2014, 64, 510–533. [Google Scholar] [CrossRef] [PubMed]
  13. Moore, L.W.; Byham-Gray, L.D.; Scott Parrott, J.; Rigassio-Radler, D.; Mandayam, S.; Jones, S.L.; Mitch, W.E.; Osama Gaber, A. The mean dietary protein intake at different stages of chronic kidney disease is higher than current guidelines. Kidney Int. 2013, 83, 724–732. [Google Scholar] [CrossRef] [PubMed]
  14. Campbell, A.P.; Rains, T.M. Dietary protein is important in the practical management of prediabetes and type 2 diabetes. J. Nutr. 2015, 145, 164S–169S. [Google Scholar] [CrossRef] [PubMed]
  15. Friedman, A.N. High-protein diets: Potential effects on the kidney in renal health and disease. Am. J. Kidney Dis. 2004, 44, 950–962. [Google Scholar] [CrossRef] [PubMed]
  16. Hammond, K.A.; Janes, D.N. The effects of increased protein intake on kidney size and function. J. Exp. Biol. 1998, 201, 2081–2090. [Google Scholar] [PubMed]
  17. Alavi, F.K.; Zawada, E.T.; Simmons, J.L. Renal hemodynamic and histological consequences of diets high in unsaturated fat, protein or sucrose in obese zucker rats. Clin. Nephrol. 1995, 43, 122–130. [Google Scholar] [PubMed]
  18. Graf, H.; Stummvoll, H.K.; Luger, A.; Prager, R. Effect of amino acid infusion on glomerular filtration rate. N. Engl. J. Med. 1983, 308, 159–160. [Google Scholar] [PubMed]
  19. Schwingshackl, L.; Hoffmann, G. Comparison of high vs. normal/low protein diets on renal function in subjects without chronic kidney disease: A systematic review and meta-analysis. PLoS ONE 2014, 9, e97656. [Google Scholar] [CrossRef] [PubMed]
  20. Knight, E.L.; Stampfer, M.J.; Hankinson, S.E.; Spiegelman, D.; Curhan, G.C. The impact of protein intake on renal function decline in women with normal renal function or mild renal insufficiency. Ann. Intern. Med. 2003, 138, 460–467. [Google Scholar] [CrossRef] [PubMed]
  21. Evert, A.B.; Boucher, J.L.; Cypress, M.; Dunbar, S.A.; Franz, M.J.; Mayer-Davis, E.J.; Neumiller, J.J.; Nwankwo, R.; Verdi, C.L.; Urbanski, P.; et al. Nutrition therapy recommendations for the management of adults with diabetes. Diabetes Care 2013, 36, 3821–3842. [Google Scholar] [CrossRef] [PubMed]
  22. Walker, J.D.; Bending, J.J.; Dodds, R.A.; Mattock, M.B.; Murrells, T.J.; Keen, H.; Viberti, G.C. Restriction of dietary protein and progression of renal failure in diabetic nephropathy. Lancet 1989, 2, 1411–1415. [Google Scholar] [CrossRef]
  23. Zeller, K.; Whittaker, E.; Sullivan, L.; Raskin, P.; Jacobson, H.R. Effect of restricting dietary protein on the progression of renal failure in patients with insulin-dependent diabetes mellitus. N. Engl. J. Med. 1991, 324, 78–84. [Google Scholar] [CrossRef] [PubMed]
  24. Dullaart, R.P.; Beusekamp, B.J.; Meijer, S.; van Doormaal, J.J.; Sluiter, W.J. Long-term effects of protein-restricted diet on albuminuria and renal function in IDDM patients without clinical nephropathy and hypertension. Diabetes Care 1993, 16, 483–492. [Google Scholar] [CrossRef] [PubMed]
  25. Raal, F.J.; Kalk, W.J.; Lawson, M.; Esser, J.D.; Buys, R.; Fourie, L.; Panz, V.R. Effect of moderate dietary protein restriction on the progression of overt diabetic nephropathy: A 6-mo prospective study. Am. J. Clin. Nutr. 1994, 60, 579–585. [Google Scholar] [PubMed]
  26. Hansen, H.P.; Tauber-Lassen, E.; Jensen, B.R.; Parving, H.H. Effect of dietary protein restriction on prognosis in patients with diabetic nephropathy. Kidney Int. 2002, 62, 220–228. [Google Scholar] [CrossRef] [PubMed]
  27. Klahr, S.; Levey, A.S.; Beck, G.J.; Caggiula, A.W.; Hunsicker, L.; Kusek, J.W.; Striker, G. The effects of dietary protein restriction and blood-pressure control on the progression of chronic renal disease. Modification of diet in renal disease study group. N. Engl. J. Med. 1994, 330, 877–884. [Google Scholar] [CrossRef] [PubMed]
  28. Shah, A.P.; Kalantar-Zadeh, K.; Kopple, J.D. Is there a role for ketoacid supplements in the management of CKD? Am. J. Kidney Dis. 2015, 65, 659–673. [Google Scholar] [CrossRef] [PubMed]
  29. Pijls, L.T.; de Vries, H.; van Eijk, J.T.; Donker, A.J. Protein restriction, glomerular filtration rate and albuminuria in patients with type 2 diabetes mellitus: A randomized trial. Eur. J. Clin. Nutr. 2002, 56, 1200–1207. [Google Scholar] [CrossRef] [PubMed]
  30. Meloni, C.; Morosetti, M.; Suraci, C.; Pennafina, M.G.; Tozzo, C.; Taccone-Gallucci, M.; Casciani, C.U. Severe dietary protein restriction in overt diabetic nephropathy: Benefits or risks? J. Ren. Nutr. 2002, 12, 96–101. [Google Scholar] [CrossRef] [PubMed]
  31. Dussol, B.; Iovanna, C.; Raccah, D.; Darmon, P.; Morange, S.; Vague, P.; Vialettes, B.; Oliver, C.; Loundoun, A.; Berland, Y. A randomized trial of low-protein diet in type 1 and in type 2 diabetes mellitus patients with incipient and overt nephropathy. J. Ren. Nutr. 2005, 15, 398–406. [Google Scholar] [CrossRef] [PubMed]
  32. Robertson, L.; Waugh, N.; Robertson, A. Protein restriction for diabetic renal disease. Cochrane Database Syst. Rev. 2007. [Google Scholar] [CrossRef]
  33. Nezu, U.; Kamiyama, H.; Kondo, Y.; Sakuma, M.; Morimoto, T.; Ueda, S. Effect of low-protein diet on kidney function in diabetic nephropathy: Meta-analysis of randomised controlled trials. BMJ. Open 2013, 3, e002934. [Google Scholar] [CrossRef] [PubMed]
  34. Rughooputh, M.S.; Zeng, R.; Yao, Y. Protein diet restriction slows chronic kidney disease progression in non-diabetic and in type 1 diabetic patients, but not in type 2 diabetic patients: A meta-analysis of randomized controlled trials using glomerular filtration rate as a surrogate. PLoS ONE 2015, 10, e0145505. [Google Scholar] [CrossRef] [PubMed]
  35. Giordano, M.; Ciarambino, T.; Castellino, P.; Cataliotti, A.; Malatino, L.; Ferrara, N.; Politi, C.; Paolisso, G. Long-term effects of moderate protein diet on renal function and low-grade inflammation in older adults with type 2 diabetes and chronic kidney disease. Nutrition 2014, 30, 1045–1049. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Azadbakht, L.; Atabak, S.; Esmaillzadeh, A. Soy protein intake, cardiorenal indices, and c-reactive protein in type 2 diabetes with nephropathy: A longitudinal randomized clinical trial. Diabetes Care 2008, 31, 648–654. [Google Scholar] [CrossRef] [PubMed]
  37. Lew, Q.J.; Jafar, T.H.; Koh, H.W.; Jin, A.; Chow, K.Y.; Yuan, J.M.; Koh, W.P. Red meat intake and risk of esrd. J. Am. Soc. Nephrol. 2016, 28, 304–312. [Google Scholar] [CrossRef] [PubMed]
  38. Dunkler, D.; Dehghan, M.; Teo, K.K.; Heinze, G.; Gao, P.; Kohl, M.; Clase, C.M.; Mann, J.F.; Yusuf, S.; Oberbauer, R.; et al. Diet and kidney disease in high-risk individuals with type 2 diabetes mellitus. JAMA Intern. Med. 2013, 173, 1682–1692. [Google Scholar] [CrossRef] [PubMed]
  39. Moorthi, R.N.; Armstrong, C.L.; Janda, K.; Ponsler-Sipes, K.; Asplin, J.R.; Moe, S.M. The effect of a diet containing 70% protein from plants on mineral metabolism and musculoskeletal health in chronic kidney disease. Am. J. Nephrol. 2014, 40, 582–591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Chen, X.; Wei, G.; Jalili, T.; Metos, J.; Giri, A.; Cho, M.E.; Boucher, R.; Greene, T.; Beddhu, S. The associations of plant protein intake with all-cause mortality in CKD. Am. J. Kidney Dis. 2016, 67, 423–430. [Google Scholar] [CrossRef] [PubMed]
  41. Ikizler, T.A. Protein and energy: Recommended intake and nutrient supplementation in chronic dialysis patients. Semin. Dial. 2004, 17, 471–478. [Google Scholar] [CrossRef] [PubMed]
  42. Obi, Y.; Qader, H.; Kovesdy, C.P.; Kalantar-Zadeh, K. Latest consensus and update on protein-energy wasting in chronic kidney disease. Curr. Opin. Clin. Nutr. Metab. Care 2015, 18, 254–262. [Google Scholar] [CrossRef] [PubMed]
  43. Kalantar-Zadeh, K.; Supasyndh, O.; Lehn, R.S.; McAllister, C.J.; Kopple, J.D. Normalized protein nitrogen appearance is correlated with hospitalization and mortality in hemodialysis patients with Kt/V greater than 1.20. J. Ren. Nutr. 2003, 13, 15–25. [Google Scholar] [CrossRef] [PubMed]
  44. Ravel, V.A.; Molnar, M.Z.; Streja, E.; Kim, J.C.; Victoroff, A.; Jing, J.; Benner, D.; Norris, K.C.; Kovesdy, C.P.; Kopple, J.D.; et al. Low protein nitrogen appearance as a surrogate of low dietary protein intake is associated with higher all-cause mortality in maintenance hemodialysis patients. J. Nutr. 2013, 143, 1084–1092. [Google Scholar] [CrossRef] [PubMed]
  45. Kopple, J.D. National kidney foundation K/DOQI clinical practice guidelines for nutrition in chronic renal failure. Am. J. Kidney Dis. 2001, 37, S66–S70. [Google Scholar] [CrossRef] [PubMed]
  46. Kalantar-Zadeh, K.; Fouque, D.; Kopple, J.D. Outcome research, nutrition, and reverse epidemiology in maintenance dialysis patients. J. Ren. Nutr. 2004, 14, 64–71. [Google Scholar] [CrossRef] [PubMed]
  47. Rhee, C.M.; Ahmadi, S.F.; Kalantar-Zadeh, K. The dual roles of obesity in chronic kidney disease: A review of the current literature. Curr. Opin. Nephrol. Hypertens. 2016, 25, 208–216. [Google Scholar] [CrossRef] [PubMed]
  48. Ou, S.H.; Chen, M.Y.; Huang, C.W.; Chen, N.C.; Wu, C.H.; Hsu, C.Y.; Chou, K.J.; Lee, P.T.; Fang, H.C.; Chen, C.L. Potential role of vegetarianism on nutritional and cardiovascular status in Taiwanese dialysis patients: A case-control study. PLoS ONE 2016, 11, e0156297. [Google Scholar] [CrossRef] [PubMed]
  49. Kalantar-Zadeh, K.; Tortorici, A.R.; Chen, J.L.; Kamgar, M.; Lau, W.L.; Moradi, H.; Rhee, C.M.; Streja, E.; Kovesdy, C.P. Dietary restrictions in dialysis patients: Is there anything left to eat? Semin. Dial. 2015, 28, 159–168. [Google Scholar] [CrossRef] [PubMed]
  50. Ikizler, T.A.; Cano, N.J.; Franch, H.; Fouque, D.; Himmelfarb, J.; Kalantar-Zadeh, K.; Kuhlmann, M.K.; Stenvinkel, P.; TerWee, P.; Teta, D.; et al. Prevention and treatment of protein energy wasting in chronic kidney disease patients: A consensus statement by the international society of renal nutrition and metabolism. Kidney Int. 2013, 84, 1096–1107. [Google Scholar] [CrossRef] [PubMed]
  51. Wang, Y.; Chen, X.; Song, Y.; Caballero, B.; Cheskin, L.J. Association between obesity and kidney disease: A systematic review and meta-analysis. Kidney Int. 2008, 73, 19–33. [Google Scholar] [CrossRef] [PubMed]
  52. American Diabetes Association. 4. Lifestyle management. Diabetes Care 2017, 40, S33–S43. [Google Scholar]
  53. Otoda, T.; Kanasaki, K.; Koya, D. Low-protein diet for diabetic nephropathy. Curr. Diabetes Rep. 2014, 14, 523. [Google Scholar] [CrossRef] [PubMed]
  54. Solon-Biet, S.M.; McMahon, A.C.; Ballard, J.W.; Ruohonen, K.; Wu, L.E.; Cogger, V.C.; Warren, A.; Huang, X.; Pichaud, N.; Melvin, R.G.; et al. The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab. 2014, 19, 418–430. [Google Scholar] [CrossRef] [PubMed]
  55. Levine, M.E.; Suarez, J.A.; Brandhorst, S.; Balasubramanian, P.; Cheng, C.W.; Madia, F.; Fontana, L.; Mirisola, M.G.; Guevara-Aguirre, J.; Wan, J.; et al. Low protein intake is associated with a major reduction in igf-1, cancer, and overall mortality in the 65 and younger but not older population. Cell Metab. 2014, 19, 407–417. [Google Scholar] [CrossRef] [PubMed]
  56. Evert, A.B.; Boucher, J.L. New diabetes nutrition therapy recommendations: What you need to know. Diabetes Spectr. 2014, 27, 121–130. [Google Scholar] [CrossRef] [PubMed]
  57. Michas, G.; Micha, R.; Zampelas, A. Dietary fats and cardiovascular disease: Putting together the pieces of a complicated puzzle. Atherosclerosis 2014, 234, 320–328. [Google Scholar] [CrossRef] [PubMed]
  58. Anderson, T.J.; Gregoire, J.; Hegele, R.A.; Couture, P.; Mancini, G.B.; McPherson, R.; Francis, G.A.; Poirier, P.; Lau, D.C.; Grover, S.; et al. 2012 Update of the Canadian cardiovascular society guidelines for the diagnosis and treatment of dyslipidemia for the prevention of cardiovascular disease in the adult. Can. J. Cardiol. 2013, 29, 151–167. [Google Scholar] [CrossRef] [PubMed]
  59. Canadian Diabetes Association Clinical Practice Guidelines Expert Committee; Dworatzek, P.D.; Arcudi, K.; Gougeon, R.; Husein, N.; Sievenpiper, J.L.; Williams, S.L. Nutrition therapy. Can. J. Diabetes 2013, 37 (Suppl. 1), S45–S55. [Google Scholar] [CrossRef] [PubMed]
  60. Tyson, C.C.; Nwankwo, C.; Lin, P.H.; Svetkey, L.P. The dietary approaches to stop hypertension (DASH) eating pattern in special populations. Curr. Hypertens. Rep. 2012, 14, 388–396. [Google Scholar] [CrossRef] [PubMed]
  61. Shapiro, H.; Theilla, M.; Attal-Singer, J.; Singer, P. Effects of polyunsaturated fatty acid consumption in diabetic nephropathy. Nat. Rev. Nephrol. 2011, 7, 110–121. [Google Scholar] [CrossRef] [PubMed]
  62. Cardenas, C.; Bordiu, E.; Bagazgoitia, J.; Calle-Pascual, A.L.; Diabetes and Nutrition Study Group, Spanish Diabetes Association. Polyunsaturated fatty acid consumption may play a role in the onset and regression of microalbuminuria in well-controlled type 1 and type 2 diabetic people: A 7-year, prospective, population-based, observational multicenter study. Diabetes Care 2004, 27, 1454–1457. [Google Scholar] [PubMed]
  63. Lee, C.C.; Sharp, S.J.; Wexler, D.J.; Adler, A.I. Dietary intake of eicosapentaenoic and docosahexaenoic acid and diabetic nephropathy: Cohort analysis of the diabetes control and complications trial. Diabetes Care 2010, 33, 1454–1456. [Google Scholar] [CrossRef] [PubMed]
  64. Malhotra, R.; Cavanaugh, K.L.; Blot, W.J.; Ikizler, T.A.; Lipworth, L.; Kabagambe, E.K. Dietary polyunsaturated fatty acids and incidence of end-stage renal disease in the Southern Community Cohort Study. BMC Nephrol. 2016, 17, 152. [Google Scholar] [CrossRef] [PubMed]
  65. ORIGIN Trial Investigators. Cardiovascular and other outcomes postintervention with insulin glargine and omega-3 fatty acids (originale). Diabetes Care 2016, 39, 709–716. [Google Scholar]
  66. Wright, J.A.; Cavanaugh, K.L. Dietary sodium in chronic kidney disease: A comprehensive approach. Semin. Dial. 2010, 23, 415–421. [Google Scholar] [CrossRef] [PubMed]
  67. Kong, Y.W.; Baqar, S.; Jerums, G.; Ekinci, E.I. Sodium and its role in cardiovascular disease—The debate continues. Front. Endocrinol. 2016, 7, 164. [Google Scholar] [CrossRef] [PubMed]
  68. Cutler, J.A.; Obarzanek, E. Nutrition and blood pressure: Is protein one link? Toward a strategy of hypertension prevention. Ann. Intern. Med. 2005, 143, 74–75. [Google Scholar] [CrossRef] [PubMed]
  69. Liese, A.D.; Nichols, M.; Sun, X.; D′Agostino, R.B., Jr.; Haffner, S.M. Adherence to the dash diet is inversely associated with incidence of type 2 diabetes: The insulin resistance atherosclerosis study. Diabetes Care 2009, 32, 1434–1436. [Google Scholar] [CrossRef] [PubMed]
  70. Rebholz, C.M.; Crews, D.C.; Grams, M.E.; Steffen, L.M.; Levey, A.S.; Miller, E.R., III; Appel, L.J.; Coresh, J. Dash (dietary approaches to stop hypertension) diet and risk of subsequent kidney disease. Am. J. Kidney Dis. 2016, 68, 853–861. [Google Scholar] [CrossRef] [PubMed]
  71. Asghari, G.; Yuzbashian, E.; Mirmiran, P.; Azizi, F. The association between dietary approaches to stop hypertension and incidence of chronic kidney disease in adults: The Tehran lipid and glucose study. Nephrol. Dial. Transplant. 2017, 32 (Suppl. 2), ii224–ii230. [Google Scholar] [CrossRef] [PubMed]
  72. Kovesdy, C.P.; Kalantar-Zadeh, K. Dash-ing toward improved renal outcomes: When healthy nutrition prevents incident chronic kidney disease. Nephrol. Dial. Transplant. 2017, 32 (Suppl. 2), ii231–ii233. [Google Scholar] [CrossRef] [PubMed]
  73. Jacobs, D.R., Jr.; Gross, M.D.; Steffen, L.; Steffes, M.W.; Yu, X.; Svetkey, L.P.; Appel, L.J.; Vollmer, W.M.; Bray, G.A.; Moore, T.; et al. The effects of dietary patterns on urinary albumin excretion: Results of the dietary approaches to stop hypertension (DASH) trial. Am. J. Kidney Dis. 2009, 53, 638–646. [Google Scholar] [CrossRef] [PubMed]
  74. Estruch, R.; Ros, E.; Salas-Salvado, J.; Covas, M.I.; Corella, D.; Aros, F.; Gomez-Gracia, E.; Ruiz-Gutierrez, V.; Fiol, M.; Lapetra, J.; et al. Primary prevention of cardiovascular disease with a Mediterranean diet. N. Engl. J. Med. 2013, 368, 1279–1290. [Google Scholar] [CrossRef] [PubMed]
  75. Salas-Salvado, J.; Bullo, M.; Babio, N.; Martinez-Gonzalez, M.A.; Ibarrola-Jurado, N.; Basora, J.; Estruch, R.; Covas, M.I.; Corella, D.; Aros, F.; et al. Reduction in the incidence of type 2 diabetes with the Mediterranean diet: Results of the predimed-reus nutrition intervention randomized trial. Diabetes Care 2011, 34, 14–19. [Google Scholar] [CrossRef] [PubMed]
  76. Tuttle, K.R.; Shuler, L.A.; Packard, D.P.; Milton, J.E.; Daratha, K.B.; Bibus, D.M.; Short, R.A. Comparison of low-fat versus mediterranean-style dietary intervention after first myocardial infarction (from the heart institute of spokane diet intervention and evaluation trial). Am. J. Cardiol. 2008, 101, 1523–1530. [Google Scholar] [CrossRef] [PubMed]
  77. Nafar, M.; Noori, N.; Jalali-Farahani, S.; Hosseinpanah, F.; Poorrezagholi, F.; Ahmadpoor, P.; Samadian, F.; Firouzan, A.; Einollahi, B. Mediterranean diets are associated with a lower incidence of metabolic syndrome one year following renal transplantation. Kidney Int. 2009, 76, 1199–1206. [Google Scholar] [CrossRef] [PubMed]
  78. Khatri, M.; Moon, Y.P.; Scarmeas, N.; Gu, Y.; Gardener, H.; Cheung, K.; Wright, C.B.; Sacco, R.L.; Nickolas, T.L.; Elkind, M.S. The Association between a Mediterranean-Style Diet and Kidney Function in the Northern Manhattan Study Cohort. Clin. J. Am. Soc. Nephrol. 2014, 9, 1868–1875. [Google Scholar] [CrossRef] [PubMed]
  79. Tirosh, A.; Golan, R.; Harman-Boehm, I.; Henkin, Y.; Schwarzfuchs, D.; Rudich, A.; Kovsan, J.; Fiedler, G.M.; Bluher, M.; Stumvoll, M.; et al. Renal function following three distinct weight loss dietary strategies during 2 years of a randomized controlled trial. Diabetes Care 2013, 36, 2225–2232. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  80. Milas, N.C.; Nowalk, M.P.; Akpele, L.; Castaldo, L.; Coyne, T.; Doroshenko, L.; Kigawa, L.; Korzec-Ramirez, D.; Scherch, L.K.; Snetselaar, L. Factors associated with adherence to the dietary protein intervention in the modification of diet in renal disease study. J. Am. Diet. Assoc. 1995, 95, 1295–1300. [Google Scholar] [CrossRef]
  81. Fouque, D.; Horne, R.; Cozzolino, M.; Kalantar-Zadeh, K. Balancing nutrition and serum phosphorus in maintenance dialysis. Am. J. Kidney Dis. 2014, 64, 143–150. [Google Scholar] [CrossRef] [PubMed]
  82. Pisani, A.; Riccio, E.; Bellizzi, V.; Caputo, D.L.; Mozzillo, G.; Amato, M.; Andreucci, M.; Cianciaruso, B.; Sabbatini, M. 6-tips diet: A simplified dietary approach in patients with chronic renal disease. A clinical randomized trial. Clin. Exp. Nephrol. 2016, 20, 433–442. [Google Scholar] [CrossRef] [PubMed]
  83. Kalantar-Zadeh, K.; Kovesdy, C.P.; Bross, R.; Benner, D.; Noori, N.; Murali, S.B.; Block, T.; Norris, J.; Kopple, J.D.; Block, G. Design and development of a dialysis food frequency questionnaire. J. Ren. Nutr. 2011, 21, 257–262. [Google Scholar] [CrossRef] [PubMed]
  84. Paes-Barreto, J.G.; Silva, M.I.; Qureshi, A.R.; Bregman, R.; Cervante, V.F.; Carrero, J.J.; Avesani, C.M. Can renal nutrition education improve adherence to a low-protein diet in patients with stages 3 to 5 chronic kidney disease? J. Ren. Nutr. 2013, 23, 164–171. [Google Scholar] [CrossRef] [PubMed]
  85. D′Alessandro, C.; Rossi, A.; Innocenti, M.; Ricchiuti, G.; Bozzoli, L.; Sbragia, G.; Meola, M.; Cupisti, A. Dietary protein restriction for renal patients: Don′t forget protein-free foods. J. Ren. Nutr. 2013, 23, 367–371. [Google Scholar] [CrossRef] [PubMed]
  86. Rhee, C.M.; Leung, A.M.; Kovesdy, C.P.; Lynch, K.E.; Brent, G.A.; Kalantar-Zadeh, K. Updates on the management of diabetes in dialysis patients. Semin. Dial. 2014, 27, 135–145. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Diabetic Kidney Disease Food Pyramid. Abbreviations: PUFA, polyunsaturated fatty acids; MUFA, monounsaturated fatty acids; FA, fatty acid.
Figure 1. Diabetic Kidney Disease Food Pyramid. Abbreviations: PUFA, polyunsaturated fatty acids; MUFA, monounsaturated fatty acids; FA, fatty acid.
Nutrients 09 00824 g001
Figure 2. Summary of existing evidence and gaps in knowledge in the dietary management of diabetic kidney disease. Abbreviations: LPD, low protein diet; GFR, glomerular filtration rate; CKD, chronic kidney disease; DKD, diabetic kidney disease; ESRD, end-stage renal disease; CV, cardiovascular; PUFA, polyunsaturated fatty acids; SFA, saturated fatty acids.
Figure 2. Summary of existing evidence and gaps in knowledge in the dietary management of diabetic kidney disease. Abbreviations: LPD, low protein diet; GFR, glomerular filtration rate; CKD, chronic kidney disease; DKD, diabetic kidney disease; ESRD, end-stage renal disease; CV, cardiovascular; PUFA, polyunsaturated fatty acids; SFA, saturated fatty acids.
Nutrients 09 00824 g002
Table 1. Summary of dietary management of patients with diabetic kidney disease based on National Kidney Foundation Kidney Disease Outcomes and Quality Initiative and American Diabetes Association/National Kidney Foundation/American Society of Nephrology guidelines [8,12].
Table 1. Summary of dietary management of patients with diabetic kidney disease based on National Kidney Foundation Kidney Disease Outcomes and Quality Initiative and American Diabetes Association/National Kidney Foundation/American Society of Nephrology guidelines [8,12].
NutrientGuidance for QuantityGuidance for QualitySpecial Considerations
Protein<15% of total calories, or RDA of 0.8 g/kg BW/day for patients with DKD.Emphasize vegan protein sources, and non-fat or low-fat dairy products are recommended.Modified to >1.2 g/kg BW/day in patients with ESRD treated with dialysis.
CarbohydrateSpecific recommendation was not provided.Choice of high fiber fruits and vegetables. No more than 10% of daily calories as simple sugars.Monitor potassium and phosphatelevels.
FatSpecific recommendation was not provided.Recommend omega-3 and omega-9 polyunsaturated fatty acid consumption.Within meal plan for calories and palatability.
Sodium1.5–2.3 g of sodium/day.Use non-processed fresh food, and utilize sodium-free herbs and spices.Sodium restrictions should be individualized.
Abbreviations: RDA, recommended dietary intake; BW, body weight; DKD, diabetic kidney disease; ESRD, end stage renal disease.

Share and Cite

MDPI and ACS Style

Ko, G.J.; Kalantar-Zadeh, K.; Goldstein-Fuchs, J.; Rhee, C.M. Dietary Approaches in the Management of Diabetic Patients with Kidney Disease. Nutrients 2017, 9, 824. https://doi.org/10.3390/nu9080824

AMA Style

Ko GJ, Kalantar-Zadeh K, Goldstein-Fuchs J, Rhee CM. Dietary Approaches in the Management of Diabetic Patients with Kidney Disease. Nutrients. 2017; 9(8):824. https://doi.org/10.3390/nu9080824

Chicago/Turabian Style

Ko, Gang Jee, Kamyar Kalantar-Zadeh, Jordi Goldstein-Fuchs, and Connie M. Rhee. 2017. "Dietary Approaches in the Management of Diabetic Patients with Kidney Disease" Nutrients 9, no. 8: 824. https://doi.org/10.3390/nu9080824

APA Style

Ko, G. J., Kalantar-Zadeh, K., Goldstein-Fuchs, J., & Rhee, C. M. (2017). Dietary Approaches in the Management of Diabetic Patients with Kidney Disease. Nutrients, 9(8), 824. https://doi.org/10.3390/nu9080824

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