Hyperoxaluric nephrolithiasis is a complication of Roux-en-Y gastric bypass surgery
2007; Elsevier BV; Volume: 72; Issue: 1 Linguagem: Inglês
10.1038/sj.ki.5002194
ISSN1523-1755
AutoresManasi Sinha, Maria L. Collazo‐Clavell, Andrew D. Rule, Dawn S. Milliner, Wayne K. Nelson, Michael G. Sarr, Rajiv Kumar, John C. Lieske,
Tópico(s)Bariatric Surgery and Outcomes
ResumoRoux-en-Y bypass surgery is the most common bariatric procedure currently performed in the United States for medically complicated obesity. Although this leads to a marked and sustained weight loss, we have identified an increasing number of patients with episodes of nephrolithiasis afterwards. We describe a case series of 60 patients seen at Mayo Clinic-Rochester that developed nephrolithiasis after Roux-en-Y gastric bypass (RYGB), including a subset of 31 patients who had undergone metabolic evaluation in the Mayo Stone Clinic. The mean body mass index of the patients before procedure was 57 kg/m2 with a mean decrease of 20 kg/m2 at the time of the stone event, which averaged 2.2 years post-procedure. When analyzed, calcium oxalate stones were found in 19 and mixed calcium oxalate/uric acid stones in two patients. Hyperoxaluria was a prevalent factor even in patients without a prior history of nephrolithiasis, and usually presented more than 6 months after the procedure. Calcium oxalate supersaturation, however, was equally high in patients less than 6 months post-procedure due to lower urine volumes. In a small random sampling of patients undergoing this bypass procedure, hyperoxaluria was rare preoperatively but common 12 months after surgery. We conclude that hyperoxaluria is a potential complicating factor of RYGB surgery manifested as a risk for calcium oxalate stones. Roux-en-Y bypass surgery is the most common bariatric procedure currently performed in the United States for medically complicated obesity. Although this leads to a marked and sustained weight loss, we have identified an increasing number of patients with episodes of nephrolithiasis afterwards. We describe a case series of 60 patients seen at Mayo Clinic-Rochester that developed nephrolithiasis after Roux-en-Y gastric bypass (RYGB), including a subset of 31 patients who had undergone metabolic evaluation in the Mayo Stone Clinic. The mean body mass index of the patients before procedure was 57 kg/m2 with a mean decrease of 20 kg/m2 at the time of the stone event, which averaged 2.2 years post-procedure. When analyzed, calcium oxalate stones were found in 19 and mixed calcium oxalate/uric acid stones in two patients. Hyperoxaluria was a prevalent factor even in patients without a prior history of nephrolithiasis, and usually presented more than 6 months after the procedure. Calcium oxalate supersaturation, however, was equally high in patients less than 6 months post-procedure due to lower urine volumes. In a small random sampling of patients undergoing this bypass procedure, hyperoxaluria was rare preoperatively but common 12 months after surgery. We conclude that hyperoxaluria is a potential complicating factor of RYGB surgery manifested as a risk for calcium oxalate stones. Nearly 20% of the United States population can be currently described as obese (body mass index (BMI) >30 kg/m2), including 11.5 million who are morbidly obese (BMI>40 kg/m2).1Demaria E.J. Jamal M.K. Surgical options for obesity.Gastroenterol Clin North Am. 2005; 34: 127-142Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar No single dietary therapy or medication has been more than modestly effective for sustainable weight loss. Further, approximately 5 million Americans have what is deemed medically complicated obesity (e.g., weight-related comorbidities such as concurrent diabetes mellitus, hypertension, sleep apnea, and/or other weight-related medical comorbidities). As a consequence, increasing numbers of patients choose surgical interventions to treat their illness, including Roux-en-Y Gastric Bypass (RYGB) procedures, the most common bariatric operation in the United States.2Sarr M.G. Felty C.L. 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Belachew M. et al.Obesity surgery: evidence-based guidelines of the European Association for Endoscopic Surgery (EAES).Surg Endosc. 2005; 19: 200-221Crossref PubMed Scopus (297) Google Scholar, 7Olbers T. Fagevik-Olsen M. Maleckas A. Lonroth H. Randomized clinical trial of laparoscopic Roux-en-Y gastric bypass versus laparoscopic vertical banded gastroplasty for obesity.Br J Surg. 2005; 92: 557-562Crossref PubMed Scopus (70) Google Scholar RYGB procedures result in marked, sustained weight loss and an improvement in abnormal glucose homeostasis, insulin resistance, sleep apnea, hypertension, and cardiovascular risk factors.8Patriti A. Facchiano E. Sanna A. et al.The enteroinsular axis and the recovery from type 2 diabetes after bariatric surgery.Obes Surg. 2004; 14: 840-848Crossref PubMed Scopus (122) Google Scholar, 9Stubbs R.S. Wickremesekera S.K. Insulin resistance in the severely obese and links with metabolic co-morbidities.Obes Surg. 2002; 12: 343-348Crossref PubMed Scopus (29) Google Scholar, 10Reinhold R.B. Late results of gastric bypass surgery for morbid obesity.J Am Coll Nutr. 1994; 13: 326-331Crossref PubMed Scopus (48) Google Scholar, 11Klein S. Burke L.E. Bray G.A. et al.Clinical implications of obesity with specific focus on cardiovascular disease: a statement for professionals from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: endorsed by the American College of Cardiology Foundation.Circulation. 2004; 110: 2952-2967Crossref PubMed Scopus (690) Google Scholar, 12Gleysteen J.J. Results of surgery: long-term effects on hyperlipidemia.Am J Clin Nutr. 1992; 55: 591S-593SPubMed Google Scholar Although both short-term and long-term complications of the RYGB procedure have been recognized, including osteopenia, osteomalacia, and more rarely neurological disorders,13Benotti P.N. 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Metabolic bone disease after gastric bypass surgery for obesity.Am J Med Sci. 2005; 329: 57-61Abstract Full Text Full Text PDF PubMed Scopus (115) Google Scholar, 18Colazzo-Clavell M.L. Jiminez A. Hodgson S.F. Sarr M.G. Osteomalacia after Roux-en-Y gastric bypass.Endocr Pract. 2004; 10: 195-198Crossref PubMed Scopus (71) Google Scholar, 19Chaves L.C. Faintuch J. Kahwage S. Alencar Fde A. A cluster of polyneuropathy and Wernicke–Korsakoff syndrome in a bariatric unit.Obes Surg. 2002; 12: 328-334Crossref PubMed Scopus (140) Google Scholar the procedure has been deemed relatively safe and effective. In a consecutive cohort of 191 RYGB patients from our institution,20Balsiger B.M. Murr M.M. Poggio J.L. Sarr M.G. Bariatric surgery. Surgery for weight control in patients with morbid obesity.Med Clin North Am. 2000; 84: 477-489Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar hospital mortality was 0.5% (1/191), and postsurgical hospital morbidity occurred in 10.5% (20/191) of all patients. Good long-term weight loss was achieved, and patients adapted well to the required new eating habits. Overall, 72% of the patients achieved and maintained a weight loss of 50% or more of their preoperative excess body weight 3 years after the operation. Because RYGB is felt to be a safe, effective, and durable procedure for most patients with medically complicated obesity, in the United States it is considered the procedure of choice for patients receiving bariatric surgery to treat medically complicated obesity. Consequently, in the United States, the number of procedures has increased from an estimated 14 000 in 1998 to 108 000 in 2003.21Shinogle J.A. Owings M.F. Kozak L.J. Gastric bypass as treatment for obesity: trends, characteristics, and complications.Obes Res. 2005; 13: 2202-2209Crossref PubMed Scopus (38) Google Scholar Until very recently, an increased incidence of renal stones in patients after RYGB procedures had not been appreciated. Furthermore, extensive testing for abnormalities in urine analytes that would characterize those at risk for development of nephrolithiasis has not been carried out in patients after RYGB. A small series of 23 patients with hyperoxaluria after RYGB was reported recently from our institution.22Nelson W.K. Houghton S.G. Milliner D.S. et al.Enteric hyperoxlauria, nephrolithiasis, and oxalate nephropathy: potentially serious and unappreciated complications of Roux-en-Y gastric bypass.Surg Obes Relat Dis. 2005; 1: 481-485Abstract Full Text Full Text PDF PubMed Scopus (129) Google Scholar In this study, we collected detailed metabolic data from a larger cohort of RYGB patients with nephrolithiasis (n=60, including the previous 23 patients), in order to delineate the potential urinary lithogenic factors and response to treatment strategies. To further assess the prevalence and rapidity of onset of potentially lithogenic abnormalities in urine, we conducted a pilot cross-sectional study of urinary oxalate excretion among obese patients before and after RYGB. Our studies show that nephrolithiasis is more common than previously recognized in patients undergoing RYGB surgery, and that abnormalities in the lithogenic profile of urine can occur within 12 months of the procedure in a significant percentage of patients. Of the 60 patients identified who underwent RYGB and subsequently developed nephrolithiasis, 30 patients were women and 30 were men. Mean time to development of first stone post-RYGB was 2.9 years (range: 1 month–13 years). Twenty-four patients underwent standard RYGB and 36 patients underwent distal RYGB. Because the percentage of patients who undergo the distal procedure at Mayo Clinic is approximately 1/5th that of the standard RYGB (Table 1), the risk of nephrolithiasis may be greater after distal RYGB.Table 1Mayo Clinic, Rochester, nephrolithiasis cases identified after RYGBStandardDistalMayo RYGB patients 1985–20041178258Mayo RYGB patients with Mayo diagnosis codes of nephrolithiasis, oxalate nephropathy, enteric hyperoxaluria (1985–2004)149Mayo RYGB survey responders with nephrolithiasis events elsewhere (survey sent only to Mayo distal RYGB patients 1985–2004; 168 out of 258 responded)—27Additional Mayo and non-Mayo post-RYGB nephrolithiasis cases identified via stone clinic referrals (through May 2006)100Total known cases of nephrolithiasis after RYGB seen at Mayo (through May 2006)2436Total nephrolithiasis cases after RYGB with available metabolic data1516RYGB, Roux-en-Y gastric bypass. Open table in a new tab RYGB, Roux-en-Y gastric bypass. Of these 60 post-RYGB patients with nephrolithiasis, 31 patients had been seen in the Mayo Stone Clinic and therefore had detailed urinary data for further analysis (Table 2 and Figure 1). Among this group, the prevalence of pre-existing nephrolithiasis was relatively high (11/31; 32%). The first patient was seen in 1994, but the majority (17) was seen in the last 2 years. Mean age at time of RYGB was 48 years (range 30–61 years), preprocedure BMI was 57±12 kg/m2, time to stone event was 2.2±2.7 years, and decrease in BMI at the time of stone event 17.5±8.9 kg/m2. Stone type was analyzed in the Mayo Clinic Metals Lab for 21 patients revealing (CaOx) in 19 patients, and mixed CaOx and uric acid (UA) in two patients. Urinary CaOx supersaturation (SS) was increased to 2.23±0.50 delta Gibbs units (DG) (normal population reference mean 1.77 DG), whereas SS for UA was low (0.83±3.40 DG), and absent for calcium phosphate (-1.47±1.56 DG). Hyperoxaluria was a common contributing factor present in 17/31 patients (mean urinary oxalate 0.66±0.40 mM/24 h).Table 224 h urinary composition in patients presenting with nephrolithiasis after standard and distal RYGBRYGB – standard and distal (n=31)RYGB – standard (n=15)RYGB – distal (n=16)Reference rangeMean(s.d.)Mean(range)Mean(range)Male/female14/177/87/9Age(years)47.8(8.2)49.2(34–60)46.3(30–61)Time to first stone(years)2.2(2.7)2.1(0.2–11.0)1.9(2.3.2–7.0)BMI prekg/m257.0(12.4)51.8(41.7–83.8)62.2*(49.8–102.7)Mean BMI losskg/m217.5(8.9)15.3(6.2–43.5)9.9(19.6–40.3)no. with stones before9/31 (29%)6/15 (40%)3/16 (21%)Volume(ml)1612(687)1583(486–2939)1643(502–3573)PH5.6(0.6)5.7(5.0–6.8)5.6(4.8–7.0)Citrate>∼400 mg/24 h#394(361)518(0–1176)269(0–853)Oxalate0.11–0.46 mmol/24 h0.66(0.41)0.61(0.24–1.19)0.71(0.07–1.80)Calcium20–275 mg/24 h132(96)115(37–241)149(43–504)Uric Acid<750 mg/24 h456(207)479(213–708)435(153–1002)Magnesium75–150 mg/24 h98(47)100(31–227)96(40–149)Phosphorous<1100 mg/24 h893(450)717(38–1513)1069*(610–2059)Sodium40–217 mmol/24 h180(76)168(74–396)192(86–299)Potassium30–90 mmol/24 h43(18)38(24–56)46(21–90)Chloride10–250 mmol/24 h162(56)144(75–209)170(58–265)Sulfate<47 mmol/24 h12.1(5.2)12.6(6.0–24.0)12.1(4.0–24.0)CaOx SS<1.77 DGaDG is negative for undersaturated solutions, and positive for saturated solutions. Any value greater that the reference mean is considered at risk for the respective crystal type.2.23(0.52)2.02(1.14–2.84)2.34(1.72–2.92)BR SS<0.21 DGaDG is negative for undersaturated solutions, and positive for saturated solutions. Any value greater that the reference mean is considered at risk for the respective crystal type.-1.47(1.56)-1.41(-2.75–0.31)-1.49(-5.22–1.10)UA SS<1.04 DGaDG is negative for undersaturated solutions, and positive for saturated solutions. Any value greater that the reference mean is considered at risk for the respective crystal type.0.83(3.40)0.81(-4.73–4.51)0.85(-6.27–4.64)Creat Clearance(ml/min)89(25)99(75–145)83(49–124)BMI, body mass index; BR, brushite; CaOx, calcium oxalate; DG, delta Gibbs unit; RYGB, Roux-en-Y gastric bypass; SS, supersaturation; UA, uric acid.*P<0.05 standard vs distal.a DG is negative for undersaturated solutions, and positive for saturated solutions. Any value greater that the reference mean is considered at risk for the respective crystal type. Open table in a new tab BMI, body mass index; BR, brushite; CaOx, calcium oxalate; DG, delta Gibbs unit; RYGB, Roux-en-Y gastric bypass; SS, supersaturation; UA, uric acid. *P<0.05 standard vs distal. Because the distal RYGB is associated with a shorter absorptive surface and might lead to a greater risk of malabsorption, patients were divided into standard (n=15) and distal (n=16) RYGB groups (Table 2). The major difference between the two subgroups was a greater presurgical BMI in the distal RYGB patients (62 vs 52 kg/m2), which is not surprising because greater BMI has been a criterion for this more aggressive procedure. Twenty-four-hour citrate excretion was modestly less in the distal group (269±308 vs 519±388 mg; P=0.08), whereas phosphorous excretion was significantly higher; other parameters including oxalate excretion did not appear to differ. Mean creatinine clearance in the entire cohort was not decreased (89 ml/min) but was less than 60 ml/min in three individuals (Figure 1). Eleven patients had a history of stones before RYGB. When analyzed as a group, those with a prior history of stones (n=11) when compared with those without (n=20) demonstrated a possible trend toward higher excretions of calcium (153±28 vs 120±21 mg/24 h; P=0.18) and citrate (491±116 vs 378±84 mg; P=0.22), but lower excretion of oxalate (0.55±0.08 vs 0.73±0.12 mM/24 h; P=0.10). However, none of these trends reached statistical significance (Figure 2). Ten patients had follow-up visits to our stone clinic after being placed on treatments that varied but typically included low-fat, low-oxalate diets, and use of calcium binders with meals. Overall, urinary CaOx SS decreased from 2.69±0.25 to 2.12±0.37 DG (P 6 months; n=23). As expected, the early group had lost less weight (BMI change 10±3 vs 20±10 kg/m2). Urinary oxalate excretion was increased in a greater percentage of patients that presented with stones >6 months after RYGB, as compared with those <6 months after RYGB, with overall higher oxalate excretions (0.74±0.42 vs 0.44±0.24 mM/24 h; P<0.05). However, CaOx SS was equally high in both groups (2.28±0.19 vs 2.22±0.58 DG), largely owing to a lower 24 h urine volume (1223±413 vs 1747±812 ml; P<0.05) as well as a lower magnesium excretion among the patients in the earlier postoperative period. We could not determine, from these observations in a stone clinic population, how common hyperoxaluria might be before or after RYGB. Therefore, we performed a small cross-sectional study of patients seen at Mayo Clinic pre- and post-RYGB surgery. This included patients undergoing preoperative assessment (n=20) and follow-up visits after surgery at 6 months (n=8) or 12 months (n=13). Patients were recruited randomly over the course of several weeks in order to represent all three time periods. At baseline in this obese population (mean BMI 48±8 kg/m2), hyperoxaluria was present in only 2/20 patients (group mean 0.35 mM/24 h) and mean CaOx SS was below the reference mean (Table 3). Changes in the urinary composition were minimal at 6 months, but in the 12-month group significant decreases in urinary citrate and calcium were observed, as was an increase in urinary oxalate (mean urinary oxalate 0.74 mM/24 h; Table 3). At 12 months postoperatively, hyperoxaluria was present in 7/13 subjects and the resulting SS for CaOx was increased dramatically above the reference mean in 12 of 13 patients (mean CaOx SS of 2.38±0.49 DG at 12 months vs 1.51±0.78 DG at baseline; P=0.009 for comparison of the two groups; Figure 4). Therefore, the risk for CaOx stones appears markedly increased in the group 1 year after RYGB as compared with the preoperative group. Because obesity is a known risk factor for renal stones, it is not surprising that nephrolithiasis was commonly present preoperatively in this RYGB patient population (14 of the 41 patients were previous stone formers). However, even when these patients with preexisting nephrolithiasis were removed from the analysis, hyperoxaluria was present in five out of eight patients at 12 months after RYGB (mean urinary oxalate 0.83±0.46 mM/24 h).Table 324 h urinary composition of lithogenic substances in a cross-sectional sample of patients at baseline, 6 months, and 12 months after RYGB surgeryBaseline preoperative (n=20)6 months postoperative (n=8)12 months postoperative (n=13)Mean(s.d.)Mean(s.d.)Mean(s.d.)Volume1939(762)1409(894)1629(823)pH5.95(0.38)5.81(0.92)5.76(0.59)Citrate660(277)563(449)444(376)Oxalate0.35(0.18)0.32(0.15)*0.74(0.44)Calcium206(111)*111(86)*112(92)UA708(255)*426(108)*461(166)Magnesium113(55)92(58)156(126)Phosphorous1149(580)*716(227)900(266)Sodium199(98)*118(72)171(103)Potassium63(21)*35(11)53(34)Chloride188(102)*114(63)171(109)Sulfate24.7(10.5)*12(6.7)*15.9(8.6)CaOx SS1.51(0.78)1.49(1.31)*2.38(0.49)BR SS-0.31(1.18)-1.38(1.83)-0.92(1.54)UA SS1.43(2.81)1.82(4.06)1.26(3.63)Creatinine clearance117(44)110(26)99(40)BR, brushite; CaOx, calcium oxalate; SS, supersaturation; UA, uric acid.*P<0.05 vs baseline; see Table 2 for normal reference ranges. Open table in a new tab BR, brushite; CaOx, calcium oxalate; SS, supersaturation; UA, uric acid. *P<0.05 vs baseline; see Table 2 for normal reference ranges. In this paper, we report 60 patients that developed renal stones after RYGB surgery. These include 23 patients from our previous study.22Nelson W.K. Houghton S.G. Milliner D.S. et al.Enteric hyperoxlauria, nephrolithiasis, and oxalate nephropathy: potentially serious and unappreciated complications of Roux-en-Y gastric bypass.Surg Obes Relat Dis. 2005; 1: 481-485Abstract Full Text Full Text PDF PubMed Scopus (129) Google Scholar A subset of 31 patients was seen in the Mayo Stone Clinic and urinary data were available for detailed analysis. Hyperoxaluria was a common risk factor in these stone-forming patients, although low urinary volumes and reduced 24 h urinary excretions of citrate and magnesium appear to be important contributing factors as well. Even though the RYGB operation with a Roux limb 120 kg) men (0.37 vs 0.50 mM/24 h) and obese (>100 kg) women (0.28 vs 0.37 mM), whereas in a German report,25Siener R. Glatz S. Nicolay C. Hesse A. The role of overweight and obesity in calcium oxalate stone formation.Obes Res. 2004; 12: 106-113Crossref PubMed Scopus (202) Google Scholar oxalate levels were increased in obese (BMI >30 kg/m2) women (0.45 vs 0.32 mM) but not in obese (BMI >30 kg/m2) men (0.33 vs 0.36 mM). The increases in urinary oxalate we observed after RYGB were in general much higher (mean oxalate excretion 0.66 mM/ 24 h). Further, the mean oxalate excretion among a random cross-section of obese patients before RYGB surgery was only 0.35±0.18 mM/24 h (Table 3). Finally, obesity is associated with higher rather than lower excretions of calcium and citrate.24Powell C.R. Stoller M.L. Schwartz B.F. et al.Impact of body weight on urinary electrolytes in urinary stone formers.Urology. 2000; 55: 825-830Abstract Full Text Full Text PDF PubMed Scopus (165) Google Scholar, 25Siener R. Glatz S. Nicolay C. Hesse A. The role of overweight and obesity in calcium oxalate stone formation.Obes Res. 2004; 12: 106-113Crossref PubMed Scopus (202) Google Scholar The findings in patients after RYGB may or may not parallel observations in patients who had undergone previous ileal or jejuno-ileal bypass procedures for hypercholesterolemia or medically complicated obesity, respectively, in whom a markedly increased incidence of renal stones, nephrocalcinosis, and renal failure was observed.26Hassan I. Juncos L.A. Milliner D.S. et al.Chronic renal failure secondary to oxalate nephropathy: a preventable complication after jejunoileal bypass.Mayo Clin Proc. 2001; 76: 758-760Abstract Full Text Full Text PDF PubMed Scopus (40) Google Scholar, 27Ehlers S.M. Posalaky Z. Strate R.G. Quattlebaum F.W. Acute reversible renal failure following jejunoileal bypass for morbid obesity: a clinical and pathological (EM) study of a case.Surgery. 1977; 82: 629-634PubMed Google Scholar, 28Canos H.J. Hogg G.A. Jeffery J.R. Oxalate nephropathy due to gastrointestinal disorders.Can Med Assoc J. 1981; 124: 729-733PubMed Google Scholar, 29Scott Jr, H.W. Dean R.H. Shull H.J. Gluck F.W. Metabolic complications of jejunoileal bypass operations for morbid obesity.Annu Rev Med. 1976; 27: 397-405Crossref PubMed Scopus (10) Google Scholar, 30Bendezu R. Wieland R.G. Green S.G. et al.Certain metabolic consequences of jejunoileal bypass.Am J Clin Nutr. 1976; 29: 366-370PubMed Google Scholar, 31Telmos A.J. Long-term morbidity of jejunoileal bypass.Am Surg. 1977; 43: 389-391PubMed Google Scholar, 32Nordenvall B. Backman L. Larsson L. 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Results of jejunoileal bypass in two hundred patients with morbid obesity.Surg Gynecol Obstet. 1977; 145: 661-673PubMed Google Scholar, 34Griffin W.O. Young V.L. Severson C.C. A prospective comparison of gastric and jejunoileal bypass procedures for morbid obesity.Ann Surg. 1977; 186: 500-509Crossref PubMed Scopus (334) Google Scholar until recently it had not been recognized as a potential complication of RYGB.22Nelson W.K. Houghton S.G. Milliner D.S. et al.Enteric hyperoxlauria, nephrolithiasis, and oxalate nephropathy: potentially serious and unappreciated complications of Roux-en-Y gastric bypass.Surg Obes Relat Dis. 2005; 1: 481-485Abstract Full Text Full Text PDF PubMed Scopus (129) Google Scholar Our results suggest that hyperoxaluria is indeed a common underlying risk factor in those RYGB patients that do develop stones, whereas hypocitraturia and a decreased 24-hr urine volume is also a contributing factor. Enteric hyperoxaluria, observed often in association with fat malabsorption, is believed to develop when oxalates derived from the diet are delivered to the colon uncomplexed with calcium. This phenomenon is observed commonly when disorders such as Crohn's disease affect the ileum, or when the ileum has been resected, leading to bile acid and fat malabsorption. The mechanism by which RYGB patients develop hyperoxaluria has yet to be determined, but it seems likely that the length of the com
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