Introduction
Hyperoxaluria is a serious metabolic condition. Primary hyperoxaluria results from inherited endogenous oxalic acid overproduction. Secondary hyperoxaluria mainly occurs in digestive diseases leading to increased intestinal absorption (enteric hyperoxaluria) (1,2). All these conditions lead to accumulation of oxalate within the body. The kidney is the main target organ because oxalate is excreted in the urine and exerts a toxic effect on renal epithelial cells with direct tubular damage. Depending on urine and plasma concentration of oxalate, kidney involvement may consist of recurrent oxalate urolithiasis or tubulointerstitial oxalate deposits. Both conditions carry the risk of kidney failure. Acute oxalate nephropathy (AON) is a devastating entity characterized by massive oxalate deposits and acute kidney injury with dismal prognosis (3–6). AON is the most threatening complication in patients with primary hyperoxaluria (7). It may also result from ethylene glycol intoxication (8). Enteric conditions responsible for AON include chronic inflammatory bowel diseases, short-bowel syndrome, and bariatric surgery with jejuno-ileal bypass or Roux-en-Y gastric bypass (5,9). In addition, AON has been reported in 10 patients with chronic pancreatitis but only as case reports or in small series (3,4,10–14).
Chronic pancreatitis (CP) is a heterogeneous disorder characterized by intermittent or persistent abdominal pain and progressive tissue damage leading to pancreatic fibrosis with loss of exocrine and endocrine pancreatic function. The terminal stage of chronic pancreatitis is characterized by maldigestion and diabetes mellitus. AON is an uncommon complication of chronic pancreatitis. The pathophysiological mechanisms, risk factors, and the clinical course of AON in chronic pancreatitis are poorly known, precluding adequate management.
In this observational study, we extensively describe the clinical, biologic, and pathologic findings in 12 patients with both chronic pancreatitis and AON. In four cases, AON prompted recognition of chronic pancreatitis and exocrine pancreatic insufficiency, highlighting the need of accurate assessment of pancreatic exocrine function in all patients with acute interstitial nephritis and birefringent crystalline deposits suggestive of calcium oxalate deposits.
Materials and Methods
We retrospectively reviewed the clinical charts of all patients with a diagnosis of AON and chronic pancreatitis who came to attention between January 2004 and August 2010 in three renal units settled in southwest France (University Hospitals in Toulouse and Pont-de-Chaume Clinic in Montauban) and one in Paris (Georges Pompidou-European University hospital). This study was approved by our internal review board and fulfilled the criteria of the Declaration of Helsinki.
Clinical history was recorded through a standardized screening of the patient's hospital records. Age of the patients refers to the age at the admission for AON. If present, a past history of urinary stones was recorded. Hypertension was defined by a BP higher than 140/80 mmHg and/or the use of antihypertensive medications. Hematuria and leukocyturia were assessed by urinary dipstick analysis. Proteinuria was assessed by measurement of a 24-hour urine sample. Estimated GFR (eGFR) was calculated by the simplified Modification of Diet in Renal Disease (MDRD) formula. Renal failure was defined by eGFR <60 ml/min per 1.73 m2 and stages of chronic kidney disease were defined according to Kidney Disease Outcomes Quality Initiative (KDOQI) classification (15). In patients requiring hemodialysis, eGFR was arbitrarily set at 0. Hypocalcemia and hyperoxaluria were defined by serum calcium level <2.1 mmol/L and urinary oxalate excretion >500 ÎĽmol/d (or >45 mg/d), respectively. Kidney and pancreas imaging studies (ultrasonography or computed tomography) were reviewed. Diabetes mellitus was diagnosed on the basis of receiving either insulin or oral antidiabetic agents, or biochemical evidence of diabetes in accordance with World Health Organization guidelines. All medications were recorded.
Renal pathology consisted of light microscopy and immunostaining directed against IgG, IgA, IgM, kappa and lambda light chains, and fibrinogen. In the patient with kidney graft, C4d immunostaining was also performed. Polarization was routinely done when unexpected crystals were detected.
Diagnosis criteria for AON were as follows: (1) rapidly progressive renal failure (defined by a >75% increase of serum creatinine in <6 months); (2) tubulointerstitial nephritis with massive birefringent crystalline deposits within tubular lumen, tubular epithelial cells, and/or interstitial space on kidney biopsy; and (3) exclusion of other causes of acute kidney injury, i.e., obstructive nephropathy, acute rejection in patients with kidney graft, and toxic or drug-induced tubulopathy.
Criteria to diagnose chronic pancreatitis required at least one clinical feature (episodic or persistent pain, attacks of acute pancreatitits, diabetes mellitus, steatorrhea) and demonstration of pancreatic function loss by a direct pancreatic function test (daily fecal elastase excretion <200 ÎĽg/g of stools or massive steatorrhea >6 g/d) or well defined pancreas imaging abnormalities (i.e., ductal dilation or irregularity; or parenchymal changes including atrophy, cysts, or calcifications of the gland upon computed tomography scan) (16).
All data are shown as medians and ranges.
Results
From January 2004 to August 2010, we identified 12 individuals (three women and nine men, median age 67 years [41 to 90]) with AON and concomitant chronic pancreatitis. Before the onset of AON, median serum creatinine was 96 ÎĽmol/L (70 to 179). Median eGFR was 57 ml/min per 1.73 m2 (36 to 89). Seven of 12 patients had stage 3 chronic kidney disease (CKD). Eight patients were on treatment for hypertension. One patient had received kidney and pancreas grafts for type 1 diabetic nephropathy 8 and 3 years before AON, respectively. The pancreas graft was removed shortly after engraftment because of arterial thrombosis.
Clinical and biologic data at diagnosis and at the end of follow-up are presented in Tables 1, 2, and 3.
;)
Table 1: Clinical charts of 12 patients with chronic pancreatitis and acute oxalate nephropathy
Table 2: Clinical charts of 12 patients with chronic pancreatitis and acute oxalate nephropathy
Table 3: Renal features, treatment, and outcome in 12 patients with chronic pancreatitis–related acute oxalate nephropathy
Renal Presentation
At diagnosis of AON, renal function was severely impaired (median serum creatinine 587 ÎĽmol/L [294 to 849]). Three patients were oliguric. Seven had low-range proteinuria (<1 g/d), one had high-range proteinuria (>1 g/d), three had microscopic hematuria, and seven had leukocyturia without concomitant urinary tract infection. Urinalysis failed to identify cellular casts or crystalluria. Nine patients had hypocalcemia (75%). Among them, frank hypocalcemia (<1.5 mmol/L) was found in four patients. No patient had worsening of pre-existing hypertension.
Renal imaging showed bilateral kidney atrophy in three patients and normal-sized kidneys in nine. Nonobstructive nephrolithiasis was detected in three cases.
A kidney biopsy was performed in all of the patients. By light microscopy, the most prominent findings consisted of acute tubular injury (including tubular necrosis, cortical tubule dilation, diminishment or loss of the proximal tubule brush border, and flattened regenerating epithelium), interstitial inflammatory cell infiltrate, and interstitial edema. In all kidney specimens, light microscopic examination also showed large clear crystals within the tubule lumen (see Figure 1), interstitium, and tubular epithelium cells with adjacent tubular basal membrane damage. Birefringency of the crystalline deposits under polarized light (see Supplemental Figure 2) was suggestive of calcium oxalate deposits. In addition, glomerulosclerosis was identified in six patients and features of diabetic nephropathy in three. In the patient who had received a kidney transplant, renal C4d immunostaining was negative and no feature of acute rejection could be found.
Figure 1: Pancreas imaging (A, B and C) and renal pathology (Massons's trichrome staining) (D) in patients with acute oxalate nephropathy related to chronic pancreatitis. (A) Dilation of the Wirsung duct; (B) corporeal and (C) head calcifications of the pancreas; (D) calcium oxalate crystal (→) within a tubular lumen with flattened epithelium, interstitial edema, and inflammatory cells.
Pancreas Involvement
At referral, eight patients had a past history of chronic pancreatitis, including seven with established pancreatic exocrine insufficiency lasting from 2 to 17 years. Six of them received pancreatic enzyme replacement therapy whereas in one patient pancreatic enzyme replacement therapy was withdrawn 2 months before the onset of AON. In four patients, the diagnosis of chronic pancreatitis was established after recognition of AON. Fecal elastase was below the normal threshold in five tested patients. Nine patients had a history of diabetes mellitus (median duration 10 years [6 to 16]) and received oral antidiabetic agents or insulin (n = 2 and n = 8, respectively). Pancreas imaging (see Figure 1) showed pancreatic calcification (n = 10), pancreas atrophy (n = 4), Wirsung duct dilation (n = 2), or cysts (n = 1). Chronic pancreatitis was from alcoholic origin in two patients and idiopathic in the others.
Oxaluria and Oxalate Metabolism
At recognition of AON, daily urinary excretion of oxalate was >45 mg/d (52 to 92) in the 11 tested patients. None of the patients had a history of ethylene glycol poisoning or chronic digestive disease. However, in addition to pancreatic exocrine failure, one or more endogenous or exogenous factors that can acutely modify oxalate urinary concentration through volume depletion were identified in all of the patients, including diarrhea-induced hypovolemia (n = 5), diuretics use (n = 5), and antihypertensive therapy that reduces glomerular filtration fraction in CKD patients (i.e., angiotensin II receptor antagonists or angiotensin-converting enzyme inhibitors, n = 8). Four patients were recently given antibiotherapy active on Oxalobacter formigenes, which may represent a risk factor of hyperoxaluria (15). One patient received a high dose of ascorbic acid intravenously (4 g/d for 4 days), an oxalate precursor.
Treatment
Blood volume was restored in all patients with crystalloid infusion according to clinical requirement. Following AON recognition, all individuals received a low-fat and oxalate-free diet. Oral calcium supplementation was started in eight patients. Drugs with potential renal hemodynamic or oxalate metabolism-modifying effects were stopped. Pancreatic enzyme supplementation was pursued in six and started in six patients (with a median delay from referral of 22 days [7–35]). Early renal replacement therapy (RRT) (i.e., before day 10) was required in five patients. Four patients received intermittent hemodialysis because of metabolic acidosis or hyperkaliemia, whereas one patient received early continuous veno-venous hemodiafiltration (CVVHDF) in an attempt to remove disposable oxalate.
Renal Outcome
The median follow-up was 7 months (2 to 60). None of the patients died. Among the four patients who required hemodialysis at referral, three still received chronic hemodialysis at the end of the follow-up. After a 5-month follow-up, the patient treated with early CVVHDF had stage 3 chronic kidney disease (eGFR 55 ml/min per 1.73 m2). In the nine patients who did not require RRT at the end of the follow-up, last mean serum creatinine and eGFR available were 212 ÎĽmol/L (98 to 410) and 25 ml/min per 1.73 m2 (12 to 55), respectively. In one of these nine patients follow-up urinary data were available and showed a normalization of the urinary oxalate concentration.
Discussion
In this study, we aimed to better characterize the clinical course of AON in patients with chronic pancreatitis.
Acute oxalate nephropathy (AON) is acute tubulointerstitital nephritis characterized by abundant calcium oxalate deposits (5). By light microscopy, calcium oxalate crystals are gray-white and spiculated. Most importantly, they are birefringent under polarized light, whereas calcium phosphate crystals do not polarize (5,17,18). In this series, all patients had biopsy-proven AON. Most presented with a typical tubulointerstitial profile consisting of severe renal failure with persistent diuresis, no renal dilation by ultrasonography, low-grade proteinuria, and no or low-grade hematuria. Although eight of 12 patients had a definite history of type 2 diabetes mellitus (and one of type 1), it should be clearly stated that renal presentation of AON highly differs from diabetic glomerulopathy (high-range proteinuria with slowly progressive renal failure). On the basis of our experience, two unusual findings in acute kidney failure may suggest AON before kidney biopsy: (1) severe hypocalcemia (<1.5 mmol/L) as observed in one third of our patients and (2) urinary oxalate excretion above 45 mg/d. Because renal biopsy may be delayed in diabetic patients because of concomitant antiaggregant therapy (n = 3 in this study), oxaluria should be tested early during the course of acute renal failure with tubulointerstitial profile of unclear origin.
Scarce or isolated tubular deposits of oxalate crystals is not a rare finding in the normal or failing kidney at any stage, and even in the transplanted kidney. Isolated oxalate crystals do not imply renal damage, although oxalate deposits in kidney grafts have a negative effect on long-term renal function (18,19). In contrast, abundant tubular or interstitial deposits of calcium oxalate are highly suggestive of a hyperoxaluric condition in native or transplanted kidney.
Plasma oxalate in humans has two sources. The main site of oxalate synthesis is the liver peroxysome, where oxalate is an end product of a number of amino acids, sugars, and ascorbic acid. Oxalate is also present in the gut, mostly complexed to calcium and therefore not absorbed. Malabsorption of fat facilitates fatty acids to bind calcium, leaving oxalate uncomplexed and free to be absorbed. Oxalate plasma concentration is <5.5 μmol/L in adult individuals. In the rodent kidney, plasma oxalate is freely filtered within the glomerulus and then reabsorbed or secreted within various segments of proximal tubules in part because of SLC26A transporters (20). In patients with advanced renal failure, urinary excretion of oxalate decreases, leading to plasma and interstitial oxalate accumulation. Given its poor solubility, a serum oxalate concentration above 30 μmol/L carries the risk of crystallization ensuing in systemic oxalosis. Oxalate precursors incriminated in toxic or drug-induced AON include acute poisoning by ethylene glycol (8) and ascorbic acid (21), respectively. Enteric hyperoxaluria has been described in various malabsorptive intestinal diseases, like jejuno-ileal bypass (17,22), short bowel syndrome (23,24), and chronic inflammatory bowel disease (25–27). Recently, short series have emphasized the risk of AON after modern bariatric surgery with Roux-en-Y gastric bypass (5,9).
Chronic pancreatitis with exocrine pancreatic insufficiency may also be associated with hyperoxaluria and AON. In this series, eight of 12 patients had evidence of chronic pancreas disease at AON recognition, including six with pancreatic enzyme replacement therapy. Exocrine pancreas insufficiency was further proven in the four remaining patients for whom fecal elastase was extremely low. These findings, along with median age in this series and pancreatic calcifications in 10 of 12 patients, strongly argue for AON being a late complication of chronic pancreatitis.
In chronic pancreatitis, the pathogenesis of hyperoxaluria remains uncertain. It is admitted that fat malabsorption leads to an increase in intraluminal free fatty acid content that competitively inhibits the precipitation of dietary calcium with oxalate. Consistent with this hypothesis, urinary oxalate levels are significantly increased in patients receiving a gastrointestinal lipase inhibitor (28). As a result, a high amount of soluble uncomplexed oxalate remains available in the intestinal lumen. Because bile salts and free fatty acids induce colonic mucosa hyperpermeability, dietary oxalate absorption increases from 10% to 40%, leading to hyperoxalemia, hyperoxaluria, and subsequent urinary oxalate crystallization (29–32).
Except in the patient who had a massive ascorbic acid intake, the event triggering AON in patients with chronic pancreatitis is not yet clear. All changes that modify oxalate metabolism and abruptly increase the plasma oxalate concentration may lead to sudden kidney interstitial and urinary oxalate supersaturation. First, because one patient developed AON within 8 weeks after stopping enzyme supplementation, whether insufficient enzyme therapy was a trigger of AON in the remaining patients is open to question. Second, the role of intestinal colonization by Oxalobacter formigenes (OF) in oxalate gut absorption has been emphasized (33). OF degrades intraluminal soluble oxalate and decreases the colonic oxalate absorption (34). Oral or intravenous antibiotherapy is the main cause of OF absence (35) and could trigger AON in four of the patients. This finding remains speculative as a marked increase in urine oxalate after antibiotic use has not been shown. Third, recent dehydration (vomiting, diarrhea, and diuretics) or renin-angiotensin system (RAS) inhibitors intake are frequently reported in patients with AON (5,10,13). Increased intratubular concentration of oxalate, secondary to enhanced reabsorption of sodium and water in the proximal tubule, likely explains the propensity of AON to be triggered by extracellular depletion. In this series, all patients received at least one RAS inhibitor or diuretics.
Treatment of AON remains largely empirical. Because the ultimate goal is to decrease both plasma and urine oxalate concentration, the following management should be promptly achieved: (1) restore optimal GFR by stopping antihypertensive medication interfering with renal hemodynamics and ensuring high diuresis output with crystalloids infusion; and (2) decrease oxalate intestinal absorption by using a low-fat, low-oxalate diet, providing high oral calcium intake (>1.5 g/d), and starting adequate pancreatic enzymatic supplementation (36). Whether long-term use of high-dose calcium or probiotics containing OF is beneficial or detrimental remains unknown. In patients with hyperoxaluria, the use of OF probiotics failed to reduce daily urinary oxalate excretion (37).
In the very early phase of management of AON, it is tempting to hypothesize that intensive plasma oxalate removal by hemodialysis may promptly reduce the plasma oxalate level and hyperoxaluria until a more specific treatment is efficient. In line with this hypothesis, one patient received early CVVHDF. A similar approach has been recommended in patients with primary hyperoxaluria type 1, to eliminate the dramatic increase of serum oxalate concentration resulting from tissue deposits removal occurring after kidney transplantation (38,39). Given the small size of our cohort, we could not assess the efficiency of early CVVHDF. Whether early and intensive RRT may be useful in chronic pancreatitis–related AON and severe renal failure warrants better assessment.
Overall, prognosis of AON is poor. AON mostly occurs in patients with pre-existing CKD, mainly related to diabetic nephropathy (5,13). Consistent with data issued from patients with jejuno-ileal bypass (5), pre-existing CKD seems to be a prognosis factor of renal function worsening: in our series three of seven individuals with stage 3 CKD subsequently required RRT at the end of the follow-up and three reached stage 4 CKD. Among the 10 cases of chronic pancreatitis–related AON previously reported (3,4,10–14), six patients progressed to end-stage kidney disease at the end of the follow-up. Thus, the cumulative rate of patients with CP-related AON reaching end-stage renal disease in published series and in our cohort reaches 41% (9 of 22), a feature close to the outcome of gastric bypass–related AON (5). Overall, gastric bypass and CP-related AON share common features (i.e., risk factors, treatment, and prognosis) but the latter may benefit from an early intake of pancreatic enzyme allowing partial AON reversal.
Renal transplantation has been proposed in few patients with end stage-renal failure and enteric hyperoxaluria, but recurrent oxalate deposition leading to graft loss may occur (3,24,25,40). Serum oxalate should thus be reduced before transplantation by means of an oxalate-free diet, calcium supplementation, and maybe high-flux daily dialysis. After transplantation, pancreatic supplementation should be continued.
Renal units involved in this study have neither specific referral bias nor practice pattern that may account for aggregation of AON in their population. However, two main limits have to be considered. First, this is not an epidemiologic study and the prevalence of both hyperoxaluria and AON in patients with chronic pancreatitis cannot be addressed. Second, we retrospectively reviewed the cases of AON followed in nephrology units for acute renal failure. Accordingly, this series was biased and focused toward the most severe phenotype of AON. Mild to moderate AON may not come to the attention of nephrologists. Moreover, AON superimposed on diabetic glomerulonephritis could be missed. A prospective assessment of oxaluria in patients with newly diagnosed chronic pancreatitis may address this question.
In summary, we report 12 cases of acute oxalate nephropathy related to chronic pancreatitis and provide keys for early recognition (rapid progressive renal failure, tubulointerstitial profile, severe hypocalcemia, hyperoxaluria, and oxalate deposits on renal biopsy) and optimal management. Risk factors amenable to prevent this severe renal disease are well identified. We show here that AON was the presenting manifestation of chronic pancreatitis in four of 12 patients, highlighting the need of pancreas function assessment in patients with acute tubulointerstitial nephritis and oxalate deposits. Conversely, AON occurred in six patients with pancreatic enzyme supplementation, suggesting that a close monitoring of renal function and oxaluria should be performed in patients with chronic pancreatitis.
Disclosures
None.
Published online ahead of print. Publication date available at www.cjasn.org.
Supplemental information for this article is available online at www.cjasn.org.
References
1. Cochat P: Primary hyperoxaluria. In: Oxford Textbook of Nephrology, Vol. 1, Oxford, Oxford University Press, 2005
2. Hoppe B, Beck BB, Milliner DS: The primary hyperoxalurias. Kidney Int 75: 1264–1271, 2009
3. Cuvelier C, Goffin E, Cosyns JP, Wauthier M, de Strihou CY: Enteric hyperoxaluria: A hidden cause of early renal graft failure in two successive transplants: Spontaneous late graft recovery. Am J Kidney Dis 40: E3, 2002
4. Wharton R, D'Agati V, Magun AM, Whitlock R, Kunis CL, Appel GB: Acute deterioration of renal function associated with enteric hyperoxaluria. Clin Nephrol 34: 116–121, 1990
5. Nasr SH, D'Agati VD, Said SM, Stokes MB, Largoza MV, Radhakrishnan J, Markowitz GS: Oxalate nephropathy complicating Roux-en-Y Gastric Bypass: An underrecognized cause of irreversible renal failure. Clin J Am Soc Nephrol 3: 1676–1683, 2008
6. McDonald GB, Earnest DL, Admirand WH: Hyperoxaluria correlates with fat malabsorption in patients with sprue. Gut 18: 561–566, 1977
7. Cibrik DM, Kaplan B, Arndorfer JA, Meier-Kriesche HU: Renal allograft survival in patients with oxalosis. Transplantation 74: 707–710, 2002
8. Brent J: Fomepizole for ethylene glycol and methanol poisoning. N Engl J Med 360: 2216–2223, 2009
9. Nelson WK, Houghton SG, Milliner DS, Lieske JC, Sarr MG: Enteric hyperoxaluria, nephrolithiasis, and oxalate nephropathy: Potentially serious and unappreciated complications of Roux-en-Y gastric bypass. Surg Obes Relat Dis 1: 481–485, 2005
10. Fakhouri F, Chauveau D, Touam M, Noel LH, Grunfeld JP: Crystals from fat. Acute oxalate nephropathy. Nephrol Dial Transplant 17: 1348–1350, 2002
11. Mpofu S, Rhodes JM, Mpofu CM, Moots RJ: An unusual cause of acute renal failure in systemic sclerosis. Ann Rheum Dis 62: 1133–1134, 2003
12. Rankin AC, Walsh SB, Summers SA, Owen MP, Mansell MA: Acute oxalate nephropathy causing late renal transplant dysfunction due to enteric hyperoxaluria. Am J Transplant 8: 1755–1758, 2008
13. Hill P, Karim M, Davies DR, Roberts IS, Winearls CG: Rapidly progressive irreversible renal failure in patients with pancreatic insufficiency. Am J Kidney Dis 42: 842–845, 2003
14. Lefaucheur C, Hill GS, Amrein C, Haymann JP, Jacquot C, Glotz D, Nochy D: Acute oxalate nephropathy: A new etiology for acute renal failure following nonrenal solid organ transplantation. Am J Transplant 6: 2516–2521, 2006
15. Levey AS, Coresh J, Balk E, Kausz AT, Levin A, Steffes MW, Hogg RJ, Perrone RD, Lau J, Eknoyan G: National Kidney Foundation practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Ann Intern Med 139: 137–147, 2003
16. Witt H, Apte MV, Keim V, Wilson JS: Chronic pancreatitis: Challenges and advances in pathogenesis, genetics, diagnosis, and therapy. Gastroenterology 132: 1557–1573, 2007
17. Hicks K, Evans GB, Rogerson ME, Bass P: Jejuno-ileal bypass, enteric hyperoxaluria, and oxalate nephrosis: a role for polarised light in the renal biopsy. J Clin Pathol 51: 700–702, 1998
18. Bagnasco SM, Mohammed BS, Mani H, Gandolfo MT, Haas M, Racusen LC, Montgomery RA, Kraus E: Oxalate deposits in biopsies from native and transplanted kidneys, and impact on graft function. Nephrol Dial Transplant 24: 1319–1325, 2009
19. Pinheiro HS, Camara NO, Osaki KS, De Moura LA, Pacheco-Silva A: Early presence of calcium oxalate deposition in kidney graft biopsies is associated with poor long-term graft survival. Am J Transplant 5: 323–329, 2005
20. Knight TF, Sansom SC, Senekjian HO, Weinman EJ: Oxalate secretion in the rat proximal tubule. Am J Physiol 240: F295–F298, 1981
21. Friedman AL, Chesney RW, Gilbert EF, Gilchrist KW, Latorraca R, Segar WE: Secondary oxalosis as a complication of parenteral alimentation in acute renal failure. Am J Nephrol 3: 248–252, 1983
22. Stauffer JQ: Hyperoxaluria and calcium oxalate nephrolithiasis after jejunoileal bypass. Am J Clin Nutr 30: 64–71, 1977
23. Emmett M, Guirl MJ, Santa Ana CA, Porter JL, Neimark S, Hofmann AF, Fordtran JS: Conjugated bile acid replacement therapy reduces urinary oxalate excretion in short bowel syndrome. Am J Kidney Dis 41: 230–237, 2003
24. Kistler H, Peter J, Thiel G, Brunner FP: Seven-year survival of renal transplant for oxalate nephropathy due to short-bowel syndrome. Nephrol Dial Transplant 10: 1466–1469, 1995
25. Bernhardt WM, Schefold JC, Weichert W, Rudolph B, Frei U, Groneberg DA, Schindler R: Amelioration of anemia after kidney transplantation in severe secondary oxalosis. Clin Nephrol 65: 216–221, 2006
26. Hylander E, Jarnum S, Jensen HJ, Thale M: Enteric hyperoxaluria: Dependence on small intestinal resection, colectomy, and steatorrhoea in chronic inflammatory bowel disease. Scand J Gastroenterol 13: 577–588, 1978
27. Mandell I, Krauss E, Millan JC: Oxalate-induced acute renal failure in Crohn's disease. Am J Med 69: 628–632, 1980
28. Sarica K, Akarsu E, Erturhan S, Yagci F, Aktaran S, Altay B: Evaluation of urinary oxalate levels in patients receiving gastrointestinal lipase inhibitor. Obesity (Silver Spring) 16: 1579–1584, 2008
29. Earnest DL: Enteric hyperoxaluria. Adv Intern Med 24: 407–427, 1979
30. Harper J, Mansell MA: Treatment of enteric hyperoxaluria. Postgrad Med J 67: 219–222, 1991
31. Chadwick VS, Modha K, Dowling RH: Mechanism for hyperoxaluria in patients with ileal dysfunction. N Engl J Med 289: 172–176, 1973
32. Modigliani R, Labayle D, Aymes C, Denvil R: Evidence for excessive absorption of oxalate by the colon in enteric hyperoxaluria. Scand J Gastroenterol 13: 187–192, 1978
33. Campieri C, Campieri M, Bertuzzi V, Swennen E, Matteuzzi D, Stefoni S, Pirovano F, Centi C, Ulisse S, Famularo G, De Simone C: Reduction of oxaluria after an oral course of lactic acid bacteria at high concentration. Kidney Int 60: 1097–1105, 2001
34. Hatch M, Cornelius J, Allison M, Sidhu H, Peck A, Freel RW: Oxalobacter sp. reduces urinary oxalate excretion by promoting enteric oxalate secretion. Kidney Int 69: 691–698, 2006
35. Mittal RD, Kumar R, Bid HK, Mittal B: Effect of antibiotics on Oxalobacter formigenes colonization of human gastrointestinal tract. J Endourol 19: 102–106, 2005
36. Stauffer JQ: Hyperoxaluria and intestinal disease. The role of steatorrhea and dietary calcium in regulating intestinal oxalate absorption. Am J Dig Dis 22: 921–928, 1977
37. Lieske JC, Tremaine WJ, De Simone C, O'Connor HM, Li X, Bergstralh EJ, Goldfarb DS: Diet, but not oral probiotics, effectively reduces urinary oxalate excretion and calcium oxalate supersaturation. Kidney Int 78: 1178–1185, 2010
38. Diaz C, Catalinas FG, de Alvaro F, Torre A, Sanchez C, Costero O: Long daily hemodialysis sessions correct systemic complications of oxalosis prior to combined liver-kidney transplantation: Case report. Ther Apher Dial 8: 52–55, 2004
39. Yamauchi T, Quillard M, Takahashi S, Nguyen-Khoa M: Oxalate removal by daily dialysis in a patient with primary hyperoxaluria type 1. Nephrol Dial Transplant 16: 2407–2411, 2001
40. Rifkin SI: Transplantation for renal failure secondary to enteric hyperoxaluria: A case report. J Med Case Reports 1: 31, 2007
