Nutritional Management for Chronic Kidney Disease Patients who Undergo Bariatric Surgery: A Narrative Review

ABSTRACT

Bariatric surgery (BS) may be effective for chronic kidney disease (CKD) patients by reducing microalbuminuria and proteinuria, and by facilitating their meeting inclusion criteria for kidney transplantation. However, nutritional management for this population is complex and specific guidelines are scarce. A literature search was performed to create dietetic practice for these patients based on the most recent evidence. For the purposes of nutritional recommendations, we divided the patients into 2 subgroups: 1) patients with CKD and dialysis, and 2) patients after kidney transplantation. Before surgery, nutritional care includes nutritional status evaluation and adjusting doses of supplements to treat deficiencies and daily nutrient intake according to the dietary restrictions derived from kidney disease, including quantities of fluids, protein, phosphorus, potassium, and vitamins. After BS, these patients are at major risk for lean body mass loss, malnutrition and dehydration because of fluid restriction and diuretics. Postoperative nutritional recommendations should be carefully tailored according to CKD nutritional limitations and include specific considerations regarding protein, fluids, and supplementation, in particular calcium, vitamin A, and vitamin D. Nutritional management of CKD and kidney transplant patients undergoing BS is challenging and future studies are required to establish uniform high-level evidence-based guidelines.

Introduction

Bariatric surgery (BS) is an effective treatment for morbid obesity and its related morbidities (1, 2). The main surgical procedures include adjustable gastric banding, sleeve gastrectomy (SG), Roux-en-Y gastric bypass (RYGB), biliopancreatic diversion (BPD) with or without duodenal switch (3), and single anastomosis gastric bypass (4). In patients with chronic kidney disease (CKD), weight loss after surgical intervention can reduce comorbidities that enhance the progression of kidney disease (5, 6), such as diabetes, hypertension, dyslipidemia, microalbuminuria, and proteinuria (5–8). For end stage kidney disease (ESKD) patients, BS may facilitate achievement of the desired BMI criteria for kidney transplantation (6, 9). In obese transplant patients, BS may reduce obesity risk factors including graft dysfunction (6, 8, 10, 11). However, side effects of BS include nutritional deficiencies and their related metabolic complications such as bone loss (12, 13). This negative effect on nutritional status could be particularly relevant in advanced CKD patients. Highly restrictive diets after BS may lead to dietary intakes of potassium, phosphorus, and protein that are well below their recommendations (7). Furthermore, BS can lead to significant lean body mass (LBM) loss (14, 15), and greater survival advantage has been shown in transplant recipients whose muscle mass has been preserved (7, 16). Several studies have also shown an increased risk for calcium oxalate stones formation after the RYGB procedure (17). The mechanisms of nutritional deterioration postoperatively in kidney patients include rapid weight reduction, LBM loss, extremely restricted nutrient intake, and inadequate oral fluid intake (6, 7). Because of specific nutrient limitations (protein, fluids, potassium, sodium, phosphorous) (18), post-BS nutritional management for CKD patients is complex and challenging (6, 7). Clinical nutrition practice guidelines for BS patients address preoperative and postoperative management, and aim to prevent metabolic and nutritional complications (3, 19–26). However, no nutritional guidelines specifically address CKD and kidney transplant patients undergoing BS, evidently because of the lack of relevant studies in this specific population of patients. We summarized the published literature on the nutritional strategies tailored for 2 patient subgroups: 1) patients post BS with CKD stages 3–5, with or without hemodialysis [glomerular filtration rate (GFR) <60 mL/(min·1.73 m²)] (27), and 2) patients post BS after kidney transplantation with functioning allograft. Nutritional recommendations are focused on SG and RYGB, which are currently the most performed primary surgical bariatric procedures worldwide (28).

Current Status of Knowledge

Literature search

A literature search was performed as appropriate for narrative reviews, including electronic databases of PubMed, Cochrane Library, and Google Scholar. We aimed to summarize the published literature on the nutritional management of CKD and kidney transplant patients undergoing BS. A combination of the terms “obesity,” “BS,” “CKD,” “kidney transplantation,” “nutritional deficiencies,” “dietary supplements,” “nutritional status,” and “nutritional care” was used. Articles published in the medical literature relevant to the queries were selected and evaluated for relevance to each of the domains selected for review. Exclusion criteria were case reports, editorials, and papers for which full texts were not available in English. The last of these searches was carried out on October 16, 2018.

BS in CKD and kidney transplanted patients

Obesity is associated with the development of CKD and its progression (5, 7, 8, 27) and is also a main risk factor for complications after kidney transplantation (9, 10). Conventional weight loss in obese patients with pre-existing CKD has been shown to reduce proteinuria, microalbuminuria, systolic blood pressure, total cholesterol, and fasting blood glucose (5). Further, weight loss attained through surgical intervention has resulted in normalization of GFR (5), although whether this normalization in hyperfiltration post BS translates into long-term renal benefits remains unclear (2, 5, 29).

In a cohort study with up to 9 y follow-up, BS (96.5% RYGB) ameliorated the risk for 30% GFR reduction by 58% and the risk for increased serum creatinine by 57% (30). In a retrospective study of 254 morbidly obese individuals, BS significantly improved estimated GFR (eGFR) in patients with CKD stage 1–2, but not in those with CKD stage 3 (31). Yet, several studies have demonstrated improvement in renal function as evident by improved eGFR in individuals with established CKD stages 3 and 4 (32–35). In addition, improvement in the albumin to creatinine ratio was observed in CKD patients at stages 2–3 who underwent BS (36). Altogether, these data support a benefit of BS in obese patients with overt CKD. It is worth noting that different methods of assessing eGFR can lead to different interpretations of kidney function (37). Such a confounding factor could be the exclusion of body weight in the eGFR formula, because these patients lose significant amounts of weight and hence plasma creatinine is influenced by the loss of muscle mass or even reduced intake post BS (2, 33, 37). In obese patients with ESKD (with or without hemodialysis), BS interventions outperformed the standard medical care (2, 9). Four of 5 hemodialysis patients became eligible for kidney transplantation after substantial reduction in body weight after SG procedures (38). Moreover, the obese Swedish population study, comprising 4047 patients, demonstrated that BS decreased the incidence of ESKD (39). In particular, the incidence of ESKD and CKD4/ESKD increased by almost 2-fold in the control compared to the BS group (39). Thus, BS intervention in advanced kidney disease may increase the possibility of kidney transplantation and delay the progression of ESKD. Among 188 patients who were stratified according to the time they underwent BS, in relation to kidney transplantation (BS pre-list, BS while on the waiting list, and BS post kidney-transplantation) (40), all patients demonstrated a significant reduction in body mass (30–60% of their initial weight), and 20 of 29 on the waiting list were able to proceed to kidney transplantation. Nevertheless, 3.5% of patients on the waiting list and a similar proportion died post transplantation (40). This high mortality rate could be attributed to most BS being open surgeries. Overall, more data are needed to rigorously evaluate the efficacy of BS in kidney transplant patients.

Preoperative nutritional care

Nutritional status evaluation

Nutritional evaluation before BS entails a clinical interview to assess bariatric knowledge, surgery expectations, eating behaviors, weight management history, dietary recommendations, guidance for the presurgery and postsurgery periods, and psychosocial assessment (19). A supervised weight-management program, including a low-calorie diet, and identification and correction of preoperative nutritional deficiencies should begin before BS (3, 19, 25). In CKD patients, presurgery recommendations should address the particular nutrient limitations of kidney disease (18), and a comprehensive nutritional status evaluation is needed (6, 7, 41). The main methods for nutritional assessment of CKD patients who are candidates for BS are presented in Table 1 (41–43).

TABLE 1.

Methods of assessing the nutritional status of CKD patients who are candidates for bariatric surgery¹

Category	Measurements
Biochemical measurements	Serum albumin, pre-albumin, total protein, cholesterol, creatinine (hemodialysis patients), PCR, CRP, nPNA, BUN, iron, transferrin, ferritin, TIBC, CBC, folate, vitamin B-12, 25(OH)D, PTH, serum calcium, serum phosphorous, serum potassium, 24-h urine protein measurement
Anthropometric measurements	Body weight, adjusted edema-free body weight, BMI, MAC, MAMC, SFT, waist–hip ratio
Weight loss over time	Percentage of UBW calculated by: [actual weight/UBW] × 100
Body composition	DEXA, BIA
Muscle strength and extrapolation to muscle mass	Hand-grip strength test
Medical background	CKD stage, number of years on dialysis, medications, comorbidities (e.g., diabetes mellitus, tumors, infections), gastrointestinal symptoms, psychological problems, functional impairment
Evaluation of dietary intake	Dietary patterns (e.g. vegetarian), dietary records for the calculation of energy, macro and micronutrients intake, by 24-h recall or 3- and 7-d diet diaries
Screening methodologies	Scoring methods with a subjective component commonly used: SGA, MIS, MNA-SF, NRS, GNRI

¹BIA, bioelectrical impedance analysis; BS, bariatric surgery; BUN, blood urea nitrogen; CBC, complete blood count; CKD, chronic kidney disease; CRP, C-reactive protein; DEXA, dual X-ray energy absorptiometry; GNRI, geriatric nutritional risk index; MAC, mid-arm circumference; MAMC, mid-arm muscle circumference; MIS, malnutrition-inflammation score; MNA-SF, mini nutritional assessment short form; nPNA, normalized protein nitrogen; NRS, nutritional risk score; PCR, protein catabolic rate; PTH, parathyroid hormone; RBC, red blood cells; SFT, skin-fold thickness; SGA, subjective global assessment; TIBC, total iron binding capacity; UBW, usual body weight; 25(OH)D, 25-hydroxyvitamin D.

Biochemical measurements include normalized protein nitrogen appearance, which provides an independent assessment of dietary protein intake (42, 43); serum albumin and serum prealbumin, as predictors of future mortality and poor nutritional status (42–44); and serum cholesterol, which if low can serve as a marker for chronic protein–energy deficits or inflammation, and therefore should be investigated for malnutrition (43, 45). Anthropometric measurements assess fat and LBM, which may detect a potential risk for protein and energy wasting, including BMI, mid-arm circumference, mid-arm muscle circumference, and 4-site skin-fold thickness (42, 43). The body weight to be used for assessing protein and energy intake is the adjusted edema-free body weight for patients who have an edema-free body weight <95% or >115% of the median standard weight; whereas for all others, the actual edema-free body weight may be used (43). Changes in weight can have clinical significance, especially in the case of unplanned weight loss over a short period of time (42). Body composition can be evaluated by several technical tools such as bioelectrical impedance analysis and whole body dual energy X-ray absorptiometry (42, 43, 46, 47). In addition, the hand-grip strength functional test can be used to determine muscle strength and extrapolation to muscle mass (41, 48). The presence of comorbid conditions associated with chronic inflammation, which can cause protein energy wasting (PEW), should be considered (41, 49, 50). Dietary intake should be recorded by a 24-h recall or 3–7-d diet diaries (42), and the daily nutritional requirements should be calculated. Adjusted body weight is usually used for determining caloric and protein requirements (51). There is no single strategy to assess the risk for malnutrition (41, 42), but the subjective global assessment and the malnutrition-inflammation score are the most comprehensive evaluations for such in CKD and hemodialysis patients (41, 42, 52).

Postoperative nutritional therapy: adjustment of nutritional recommendations to patients with kidney disease who undergo BS

Metabolic and nutritional deterioration present in 20–50% of patients with advanced CKD (41, 53–57). PEW can increase mortality risk and hospitalization rate (41, 58, 59). Highly restrictive diets after BS may lead to dietary intakes of potassium, phosphorus, and protein that are well below the recommendations for ESKD patients. Therefore, the risk for malnutrition is greater than the risk for excessive intake in this population, and food considered high in potassium or phosphorus may be suitable because of the serving size restrictions post BS (7). The daily dietary requirements and recommendations for the first postoperative year and routine supplementation to prevent postoperative nutritional deficiencies in adult CKD and kidney transplant patients undergoing SG or RYGB procedures are detailed in Table 2. Table 3 summarizes the recommendations for treatment of common nutritional deficiencies post BS, as appropriate and adjusted to CKD patients (3, 6, 19, 22, 23, 26, 60–65).

TABLE 2.

Daily dietary requirements and routine supplementation to prevent postoperative nutritional deficiencies in adult stage 3 CKD patients and kidney transplant patients who are post BS¹

Nutrient	CKD/hemodialysis patients post BS2	Kidney transplant patients post BS2
Fluids	Determined by nephrologists, adapting diuretics	≥1500 mL with functioning allograft
Protein3	0.8–1 g/kg IBW Hemodialysis ≥1.2 g/kg IBW	≥1.1 g/kg IBW with functioning allograft
Sodium4	≤3000 mg Hemodialysis 1800–2300 mg	1800–2300 mg5
Phosphorous	≤800 mg	Adjusted to serum phosphorous levels
Potassium6	≤3000 mg from stage 4 adjusted to hyperkalemia≤4700 mg for stage 3 without hyperkalemia	≤4700 mg
Calcium7	CKD 800–1000 mg from foodHemodialysis <800 mg from food	1200–1500 mg from food and supplements
Iron	45–60 mg8	45–60 mg
Magnesium9	Men ≤420 mgWomen ≤320 mg	Men ≤420 mgWomen ≤320 mg
Copper	SG 1 mgRYGB 1–2 mg	SG 1 mgRYGB 1–2 mg
Zinc	SG 8–11 mgRYGB 8–22 mg	SG 8–11 mgRYGB 8–22 mg
Vitamin D10	3000 IU cholecalciferol for maintaining target levels	3000 IU cholecalciferol for maintaining target levels
Folic acid11	400–800 µgHemodialysis 1000 µg	400–800 µg
Vitamin B-12	350–500 µg sublinguistic	350–500 µg sublinguistic
Vitamin C	Men ≤90 mgWomen ≤75 mg	Men ≤90 mgWomen ≤75 mg
Thiamine (B-1)	≥12 mg	≥12 mg
Vitamin A	Men <3000 IUWomen <2330 IU	Men <3000 IUWomen <2330 IU
Vitamin E	<15 mg	<15 mg
Vitamin K	Men <120 µgWomen <90 µg	Men <120 µgWomen <90 µg

¹BS, bariatric surgery; CKD, chronic kidney disease; eGFR, estimated glomerular filtration rate; GFR, glomerular filtration rate; IBW, ideal body weight; IU, International Units; RYGB, Roux-Y-gastric bypass; SG, sleeve gastrectomy; 25(OH)D, 25-hydroxyvitamin D. Conversion factors: 25(OH)D in ng/mL to mmol/L × 2.496.

²Recommendations for routine supplementation post SG or RYGB procedures.

³Depending on renal function. Hyperfiltration because of excess protein intake has not been proven among transplanted kidney patients, therefore 1.5 g/kg IBW can be considered if necessary.

⁴In the presence of hypertension or heart failure, the amount of sodium should be further restricted. In hypotensive patients sodium requirements should follow the nephrologist's recommendations.

⁵According to renal function.

⁶Serum potassium, history of hyperkalemia, and renal function should be taken into account.

⁷Calcium supplements should be prescribed by nephrologists only.

⁸Routine iron supplementation after BS to prevent iron deficiency can be administered to CKD patients in accordance with post-BS protocols; however, such supplementation is not expected to be sufficient to prevent anemia and hence, in many cases i.v. iron will probably be prescribed by a nephrologist.

⁹Serum magnesium concentrations tend to fluctuate depending on eGFR and intake of medications. Several medications including laxatives and antacid medicines can elevate magnesium concentration, whereas diuretics can significantly reduce its concentration. In CKD patients [GFR <30 mL/(min·1.73 m²)] magnesium concentration changes constantly and tends to rise above normal. Among hemodialysis patients, dialysate concentration can affect magnesium concentration. As for kidney transplanted patients, magnesium stores can be highly affected by immunosuppressive drugs, therefore, magnesium should be adjusted to serum magnesium concentration according to nephrologist recommendations.

¹⁰Target levels are defined as serum 25(OH)D 30 ng/mL. Supplementation should be accompanied by monitoring serum calcium and phosphorous. If serum parathyroid hormone (PTH) is increased despite normal serum 25(OH)D, further therapeutic decisions should be made by the patient's nephrologist according to CKD stage.

¹¹Fertility age 800–1000 µg.

TABLE 3.

Treatment of common nutritional deficiencies post BS in patients with kidney disease¹

Nutrient	Treatment for depletion
Iron2	CKD non-dialysis iron deficiency can be treated orally by 200 mg/d elemental iron for 1–3 mo. If the goals for correction are not achieved, i.v. supplementation should be considered. Hemodialysis patients should be treated with i.v. supplementation at the beginning of treatment for iron deficiency. Iron supplementation may be discontinued when TSAT >30% and serum ferritin >500 ng/mL
Vitamin B-12	1000–2000 µg/d sublinguistic or 1000 µg/wk i.m. to achieve normal levels and then resume dosages recommended to maintain normal levels
Folate	Oral dose of 1000 µg folic acid/d for a short period of 3 mo to achieve normal levels and then resume recommended dosage to maintain normal levels, check B-12 before supplementation. It is not recommended to consume more than 1 mg/d to prevent masking of B-12 deficiency
Thiamine	Treat post-BS patients with suspected thiamine deficiency before or in the absence of laboratory confirmation of deficiency and monitor and evaluate resolution of signs and symptoms. Repletion dose for thiamine deficiency varies based on the route of administration and the severity of symptoms, as follows: oral therapy 100 mg 2–3 times per d until symptoms resolve; i.v. therapy 200 mg 3 times per d to 500 mg once or twice per d for 3–5 d, followed by 250 mg/d for 3–5 d or until symptoms resolve, then consider treatment with 100 mg/d orally, usually indefinitely or until risk factors have been resolved; i.m. therapy 250 mg once per d for 3–5 d or 100–250 mg monthly
Vitamin D	Cholecalciferol ≥3000–6000 IU/d, or 50,000 IU vitamin D-2 1–3 times/wk, followed by maintenance therapy. Vitamin D loading should be given over a limited time frame period, together with serum calcium, 25(OH)D, PTH, and phosphorous monitoring and under medical supervision. Supplementation should be decided on a personal basis and in some conditions active oral vitamin D should be considered by the nephrologist3
Magnesium	In case of deficiency after BS, oral magnesium citrate 300 mg/d should be prescribed

¹Cholecalciferol, vitamin D-3; CKD, chronic kidney disease; D-2, ergocalciferol; i.m., intramuscularly; i.v., intravenously; IU, International Units; PTH, parathyroid hormone; TSAT, transferrin saturation; 25(OH)D, 25-hydroxyvitamin D.

²Because of the combined risk factors for iron deficiency and anemia among kidney patients undergoing BS, it is recommended that the patient's nephrologist should determine the appropriate treatment of iron deficiency.

³If serum 25(OH)D >30 ng/mL (75 nmol/L) and PTH is above the target range, active oral vitamin D may be indicated by the patient's nephrologist.

Protein

Protein intake requirement after BS is 60–80 g/d or 1.1–1.5 g/kg of ideal body weight (IBW) (i.e., BMI = 25 kg/m²) and increases to 90–120 g/d after malabsorptive procedures (biliopancreatic diversion/biliopancreatic diversion with duodenal switch ) (3, 19, 23, 66), to preserve LBM postoperatively (14, 67). In clinically stable patients with stage 3–5 CKD who are not on dialysis [eGFR <45 mL/(min·1.73 m²)] (18, 68), dietary protein of 0.6–0.8 g/kg IBW per d (6, 18, 68, 69) is recommended, but this should be adjusted when hypermetabolic conditions such as acute illness and hospitalizations occur or if there is a risk for malnutrition (18, 68). In ESKD patients on hemodialysis, the minimum protein requirements are 1.2 g/kg IBW per d (18, 68, 69). After kidney transplantation, protein intake is less restricted and is dependent on kidney function (6, 18). Experimental evidence suggests that long-term dietary protein intake >1.5 g/kg IBW per d may cause glomerular hyperfiltration and proinflammatory gene expression, which are known risk factors for kidney disease (18), but these amounts of protein per day may be required in hypercatabolic states (18). Considering that for most adults who are at increased risk for malnutrition, protein intake closer to 0.8 g/kg per d may be necessary to prevent or correct PEW (18), and that BS subjects this population of patients to a risk of nutritional deterioration (6, 7), the preferred range of protein daily intake after BS may be 0.8–1 g/kg IBW for patients with stage 3–5 CKD who are not on dialysis, ≥1.2 g/kg IBW for hemodialysis patients, and ≥1.1 g/kg IBW for patients after kidney transplantation post BS, contingent on kidney function and the standard recommendations after BS (Table 2). About 50% of the protein intake should be of high biological value (18, 68, 69) and protein supplements should be considered postoperatively, to meet the daily minimum requirements (6, 68).

Fluids

Daily fluid intake to maintain adequate hydration after BS should be ≥1.5 L/d (3, 19). The main causes of dehydration in the early stages after surgery include a mechanical liquid intake limitation and reduced fluid intake because of taste changes and vomiting (19, 24, 25, 70). Vomiting is very common during the postoperative period (30–60%) (19, 71), mainly during the first month (19), and can lead to kidney injury (27, 72). The use of loop diuretics can lead to dehydration (73). Fluid is often restricted in advanced stage CKD patients (6, 42), but because of the risk of dehydration after BS (19, 71) and its implication on kidney function (72), inadequate oral fluid intake may be of greater concern than excess intake, especially in the case of vomiting and when loop diuretics are prescribed (7, 18).

Patients with CKD stages 1–3 rarely need fluid restrictions. Therefore, nutritional management of the post-BS patient with mildly impaired kidney function should follow existing postoperative protocols (7). However, because patients with ESKD have increased sodium and water retention, the intake of sodium and fluid volume should be tightly controlled, and fluid intake should match urine output or volume removed during dialysis (6, 42). Guidelines for daily fluid intake vary from 500 to 1000 mL in addition to daily urine output, to achieve an interdialytic weight gain of 2–2.5 kg or 4–4.5% dry body weight (42). After kidney transplantation with functioning allograft, restrictions on fluid intake are not necessary, and fluid is encouraged, to optimize hydration as is consistent with recommendations after BS (6).

Fat-soluble vitamins (A, E, K)

According to the latest nutritional guidelines of the American Society for Metabolic and Bariatric Surgery, the daily recommendations for postoperative vitamin doses are 5000–10,000 international units (IU) of vitamin A depending on the type of surgery, 15 mg vitamin E, and 90–120 µg vitamin K (22). In CKD patients, administration of excess amounts of vitamin A should be avoided to prevent any potential toxic effects (74–76). Concentrations of serum vitamin A and its metabolites were found to be increased among non-dialyzed patients with CKD, ESKD patients, and kidney transplant recipients (77–80), and a negative correlation was found between plasma retinol and eGFR (42, 77, 81). To prevent vitamin A toxicity, supplements containing amounts >700–900 µg/d (2333–3000 IU/d) should not be given to maintenance hemodialysis patients (42). Supplemental vitamin A is currently not recommended for CKD patients, unless the intake is less than that of the DRI (82). In such cases, supplemental vitamin A up to the DRI dose can be given (3000 IU/900 µg for men and 2330 IU/700 µg for women as retinol activity equivalents) (77, 82–84).

Plasma levels of vitamin E do not decrease in long-term maintenance hemodialysis patients (42), and plasma levels in patients with CKD do not appear to differ from those of healthy controls (77). Furthermore, clinical trials show inconclusive results regarding the effectiveness of vitamin E for prevention of cardiovascular disease in CKD patients (77, 85). Thus, the normal DRI for vitamin E (α-tocopherol) (15 mg for men and women) is recommended (77, 86). Vitamin K is often deficient in patients with advanced kidney disease (18, 77, 87) and experimental models of CKD suggest that vitamin K supplementation may blunt the development of vascular calcification (18). However, to date, there is little evidence that the reference intake for CKD patients differs from the DRI for healthy individuals; thus, a daily intake of DRI is recommended (120 µg for men and 90 µg for women) (42, 77, 82).

Vitamin D and calcium

Bariatric patients are at risk of fractures and osteoporosis caused by rapid weight loss and absorption changes that occur postoperatively (19). The nutritional supplementation post BS (SG and RYGB), according to the procedure, should include 1200–1500 mg calcium/d from food and supplements and 3000 IU vitamin D3 (cholecalciferol)/d (titrated to therapeutic levels) (19, 22). In CKD patients, the risk of skeletal fracture is up to 5 times higher in individuals with an eGFR <15 versus >60 mL/(min·1.73 m²), and the incidence of fractures was shown to be significantly higher in hemodialysis patients compared to the general population (88). Decreased production and conversion of vitamin D to its active form (1,25-dihydroxyvitamin D) in kidney disease results in reduced calcium absorption in the gastrointestinal tract (6, 18). Treatment of chronic kidney disease-mineral and bone disorder focuses on lowering high serum phosphate and maintaining serum calcium (89). Elevated parathyroid hormone (PTH) necessitates additional tests for hyperphosphatemia, hypocalcemia, and vitamin D deficiency (89). Calcium and vitamin D supplementation in CKD patients may be necessary to preserve bone mineral density, but the recommended dose of supplementation remains controversial (6, 88). Excess exposure to calcium through diet, medication, or dialysate may be harmful across all eGFR categories of CKD, leading to positive calcium balance, vascular calcifications, and episodes of hypercalcemia (18, 42, 89). In patients with moderate-to-advanced CKD, 800–1000mg elemental calcium/d from all sources has been suggested to suffice (18, 90, 91). Achievement of target serum levels of 25-hydroxyvitamin D (25(OH)D) is recommended for CKD patients, to reduce high PTH, which is associated with skeletal fractures (88). However, the evidence is insufficient to correlate correction of serum vitamin D concentration with improved patient outcomes, including fracture risk (88). Generally, in patients with serum concentration of 25(OH)D >30 ng/mL (75 nmol/l) who have PTH above the target range, an active oral vitamin D is indicated (6, 18). Special attention should be given to bone metabolism among kidney transplant patients because of post-transplant steroid-based immunosuppression in addition to a history of CKD (6).

Phosphate

Hyperphosphatemia and hypophosphatemia have been shown to increase the risk of mortality among CKD stage 3–5 and kidney transplant patients (63). In hyperphosphatemia, urinary phosphate excretion is accelerated, causing secondary hyperparathyroidism and elevated fibroblast growth factor 23, which can lead to bone disease (18, 63, 92). Restricting dietary phosphate intake to <800 mg/d (26 mmol/d) is recommended for patients with moderate-to-advanced kidney disease; whereas in hemodialysis patients or CKD who are at increased risk for PEW, excessive restriction of protein intake to control hyperphosphatemia may be associated with poor outcomes (18, 63, 92). The quality of evidence regarding phosphate restriction is considered relatively low (63). Furthermore, foods that contain organic phosphate should be preferred over those containing inorganic phosphate; the latter is almost completely absorbed in the gastrointestinal tract (18, 63). Therefore, nutritional education should focus on the reduction of processed food, which is rich in food additives that contain inorganic phosphate (18, 63). For transplanted kidney patients, there are no specific standards (93), although hypophosphatemia is common (10, 94). Therefore, each patient should be treated according to clinical characteristics and the presence of abnormal phosphate levels. Treatment for decreasing phosphate amounts (binders/diet/dialysis) should be adjusted to control chronic kidney disease-mineral and bone disorder (89).

Sodium

For all kidney disease patients, daily sodium restriction is recommended to reduce the risk of cardiovascular morbidity; however, long-term clinical trials are needed to establish this recommendation (18, 95). The daily recommendations for sodium intake in non-dialysis CKD patients without overt cardiovascular disease or hypertension should be <3 g/d (18). In the presence of hypertension, sodium intake should be <2 g/d (95). However, for hemodialysis patients and kidney-transplanted recipients, sodium consumption, regardless of hypertension, should be 1.8–2.3 g/d (10, 42). This rigid sodium intake recommendation is important in hemodialysis patients to suppress thirst and interdialytic weight gain (42), but should take into account concurrent conditions such as hyponatremia, in which sodium restriction should be not <1.5 g/d (18).

Potassium

The recommendation for potassium intake for the majority of the general population (eGFR >30 mL/(min · 1.73 m²) and proteinuria <0.3 g/d) is 4700 mg/d (18). Chronic hyperkalemia can be caused by several factors including decreased renal excretion, high potassium intake, certain medications (e.g., angiotensin pathway modulators), and metabolic acidosis (96–98). Dietary potassium should be adjusted to match serum potassium and restricted in advanced CKD patients who are susceptible to hyperkalemia (18, 98, 99). The daily recommendation for a low potassium diet is <3000 mg (18, 97, 100, 101). For kidney transplanted patients, potassium should be limited according to kidney function (18) and the occurrence of hyperkalemia from development of renal tubular acidosis or the effect of calcineurin inhibitors (96). Importantly, constipation is a common side effect after most BS, and (19, 102) in CKD patients, constipation can also result from excessive dietary restriction, mainly of potassium and water, and may actually result in lower gut potassium excretion (18, 100). Thus, potassium restriction is recommended mostly in patients with hyperkalemia, especially those with advanced stages of CKD (18, 97).

Folic acid and vitamin B-12

Folate deficiency after BS may occur because of noncompliance with supplement administration, drug interactions, malabsorption, and poor dietary intake, and is often related to vitamin B-12 deficiency (19). After BS, a routine daily intake of 400–800 µg folic acid/d is recommended, and 800–1000 µg/d for women of childbearing age (22). Low folic acid intake can be an important contributor to folate deficiency in patients with CKD (77) because the primary source of dietary folic acid is fresh green vegetables, which, because of their high potassium content, are often restricted (77). In hemodialysis patients, folate may be reduced in serum and red blood cells and this can induce megaloblastic anemia. Thus 1 mg folic acid/d has been prescribed to prevent deficiency (42, 103). Most hemodialysis patients present with plasma cobalamin in the normal range, regardless of whether or not they take vitamin B-12 supplements. Administration of vitamin B-12 has been shown to improve or correct nerve conduction velocity in hemodialysis patients with low vitamin B-12 in plasma (42, 103). Although vitamin B-12 deficiency is unusual in dialysis patients, because of the high frequency of low food intake, B-12 supplementation equivalent to the DRI may be recommended (103, 104). Administration of vitamin B-12 and folic acid should be similar to recommendations for the BS patient without CKD, and 1 mg folic acid/d to prevent deficiency in hemodialysis patients (Table 2) (6, 42, 103).

Iron

Patients who undergo BS are predisposed for iron deficiency (22, 105) for several reasons, including presurgery deficiency (19, 105), a persistent inflammatory response that attenuates iron absorption (105), low consumption of iron-rich foods post BS (19, 105), impaired iron absorption from reduced hydrochloric acid secretion (19, 105), use of antacid medication (19), and a shortage in gut absorption area (19, 105). Iron deficiency is a major risk factor for anemia (60), and anemia is related to cardiovascular morbidity and mortality among CKD patients (61). Because iron is a key component of red blood cells, iron deficiency can accelerate development of anemia in CKD patients by attenuating erythropoiesis (60, 61). Kidney transplanted patients are at high risk for anemia, particularly because of impaired function of the renal allograft and use of immunosuppressant drugs (106). Iron status is determined by serum transferrin saturation and by serum ferritin (22, 105). Particular attention should be taken when acute phase inflammation or infection is present, which can elevate serum ferritin (22, 60, 61), reduce transferrin (61), and mask the need for iron supplements (61, 105). When iron supplementation is necessary, several parameters should be considered, including the history and outcomes of such supplements, the current iron status (60), the usage and current doses of erythropoiesis-stimulating agents (61) and hemoglobin target (60). Iron supplements are usually taken until serum transferrin saturation is >20% and serum ferritin is >100 ng/mL for CKD non-dialysis patients or 200 ng/mL among dialysis patients (6). Routine iron supplementation after BS to prevent iron deficiency [45–60 mg of elemental iron/d (3, 6, 19, 22)] can be given to CKD patients in accordance with post-BS protocols; however, such supplementation is not expected to be sufficient to prevent anemia and hence, in many cases, intravenous iron will probably be prescribed by a nephrologist.

Multivitamin and mineral supplements

Daily nutritional supplementation post BS includes routine multivitamin-plus-mineral supplements, containing iron, folic acid, zinc, copper, selenium, vitamin C, thiamine, and fat-soluble vitamins (3, 19, 22, 25). However, in CKD patients, risks of accumulation of several micronutrients are increased, such as fat-soluble vitamins (6, 42, 77–79, 89, 103). Therefore, monitoring such nutrients routinely and often after surgery is recommended, as well as extra care in choosing the appropriate daily multivitamin supplement. Importantly, the metabolism of ascorbic acid leads to oxalic acid generation, which can be considered a uremic toxin (107). Thus, the recommended dose of vitamin C for CKD and dialysis patients is not more than the DRI for this vitamin (75 mg for females and 90 mg for males) (77, 86, 103). Special attention should be given to patients at high risk for hyperoxaluria post RYGB because ascorbic acid is metabolized to oxalate and may further increase the risk for calcium oxalate stone formation (17, 108).

Postoperative long-term nutritional follow-up

Multidisciplinary team postoperative follow-up

Previous studies have demonstrated that nutritional deficiencies are common before BS and that obesity itself is associated with a high prevalence of nutritional deficits such as iron and vitamin D deficiencies (109, 110), that may worsen during the first postoperative year (109, 111, 112). Thus, it is recommended to begin to correct nutritional deficiencies before BS (19). The question of whether routine postoperative standard supplementation regimen is sufficient to prevent nutritional deficiencies and for how long such supplementation must be maintained, especially after restrictive procedures, has not been fully answered (109, 113). However, as recent findings demonstrated high prevalence of nutritional deficiencies coupled with low adherence to supplementation recommendations during the long-term period after BS (109), lifetime supplement intake post surgery becomes necessary (19). Nevertheless, in CKD patients, caution must be taken with nutrient supplementation because of the risk of accumulation of several micronutrients such as fat-soluble vitamins (6, 42, 77–79, 89, 103). Thus, monitoring of the aforementioned nutrients routinely and often after surgery in this subset of patients is recommended, as well as extra care in choosing the appropriate supplements. To date, there is no clear statement on the appropriate frequency and duration of nutritional assessments in CKD patients post BS (7). Generally, in a morbidly obese patient after BS, follow-up is made by a multidisciplinary team including a surgeon, dietitian, endocrinologist, and a social worker or psychologist (19). In an attempt to prevent malnutrition in CKD-BS patients, it is reasonable to assume that this type of population would need some extra care during the first year after surgery. These patients, in particular those with more advanced kidney disease, should be defined as patients at risk of low nutritional status until stabilized. This conservative approach should be implemented to ascertain that every patient is assessed on a monthly basis to carefully monitor their nutritional balance (114). According to the Kidney Disease Outcomes Quality Initiative (K/DOQI) clinical practice guidelines, any nutritional management program should be re-evaluated frequently and in some particular cases of severe malnutrition, should be re-evaluated more often, such as on a weekly basis (43, 69). The European Best Practice Guidelines recommendation is to preform nutritional evaluation in pathologic cases, such as the need for a feeding tube or intradialytic parenteral nutrition (42). In these cases, nutritional assessment should be done very rapidly (e.g., in 2–3 d) followed by constant nutritional monitoring on a weekly basis (42). A reasonable approach is to distinguish between subpopulations of patients such as those with CKD and kidney transplanted patients and those with advanced kidney failure, such as hemodialysis patients.

Conclusions

Despite the benefits, BS is accompanied by adverse metabolic outcomes such as nutritional deficiencies, reduction in LBM, and bone loss, all of which are highly relevant in the population of CKD patients. In this review, we present strategies for integrated nutritional care for CKD-BS and kidney transplanted patients, aimed at preventing long-term nutritional deterioration and related metabolic complications. Nutritional care for BS patients should be adjusted individually, to meet CKD limitations in accordance with disease stage. Long-term monitoring after BS should focus on reducing the risks for malnutrition, nutritional deficiencies, and CKD progression. Postoperative nutritional guidance should focus on a personal course according to digestion ability and abnormal nutritional values. Although to date there is no clear statement regarding the frequency and duration of assessment of post-BS CKD patients to prevent malnutrition, it is reasonable that postoperative follow-up by a multidisciplinary team should be implemented frequently in the first month and then monthly until stabilization of medication and nutritional deficit adjustments. Several issues remain unclear and require future investigation to create uniform, evidence-based guidelines. Such issues include determining a reliable method to estimate GFR post BS, establishing the long-term effects of BS on CKD patients, clarifying the type of BS which is more preferable for this population, and understanding the impact of BS on nutritional status and its related long-term complications. Delineation of these unresolved questions by further long-term follow-up studies would make it possible to establish future evidence-based recommendations for this unique population of patients.

Notes

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author disclosures: TB-P, AW-S, AR, SS-D, CS, IMY-L, DW, OA, NS, RH, and RE, no conflicts of interest.

TB-P and AW-S are co-first authors.

Abbreviations used: BS, bariatric surgery; CKD, chronic kidney disease; ESKD, end-stage kidney disease; IU, International Units; GFR, glomerular filtration rate; LBM, lean body mass; PEW, protein energy wasting; PTH, parathyroid hormone; RYGB, Roux-en-Y Gastric Bypass; SG, sleeve gastrectomy; 25(OH)D, 25-hydroxyvitamin D.