Skip to main content
Top
Published in: Urolithiasis 3/2016

01-06-2016 | Original Paper

The mechanistic basis of hyperoxaluria following gastric bypass in obese rats

Authors: Marguerite Hatch, Benjamin K. Canales

Published in: Urolithiasis | Issue 3/2016

Login to get access

Abstract

Roux-en-Y gastric bypass (RYGB) surgery is a popular and extremely effective procedure for sustained weight loss in the morbidly obese. However, hyperoxaluria and oxalate kidney stones frequently develop after RYGB and steatorrhea has been speculated to play a role. We examined the effects of RYGB and the role of dietary fat in an obese rat model by measuring fecal fat content and transmural oxalate fluxes across the distal colon compared to sham-operated controls (SHAM). Direct measurements of fecal fat content confirmed that RYGB on a 10 % fat diet excreted 40-fold more fecal fat than SHAM and, on a 40 % fat diet, RYGB excreted sevenfold more fecal fat than SHAM fed similarly. Results from the transport studies revealed a clear effect of high dietary fat (40 %) on colonic oxalate permeability and tissue conductance (G T) with comparable oxalate fluxes in RYGB and in SHAM. Administering a diet containing 10 % fat to both groups distinguished differences between RYGB and SHAM, revealing a 40 % increase in G T in RYGB and a reversal in the direction of net oxalate flux from absorption in SHAM to secretion in RYGB. These changes in colonic oxalate permeability were associated with a fourfold increase in urinary oxalate excretion in RYGB compared to SHAM. Therefore, oxalate solubility and permeability in the RYGB model are promoted by steatorrhea and result in enhanced passive oxalate absorption and hyperoxaluria. To our knowledge, these are the first measurements of intestinal oxalate transport in rats with RYGB.
Literature
1.
go back to reference Ammon HV, Phillips SF (1973) Inhibition of colonic water and electrolyte absorption by fatty acids in man. Gastroenterology 65:744–749PubMed Ammon HV, Phillips SF (1973) Inhibition of colonic water and electrolyte absorption by fatty acids in man. Gastroenterology 65:744–749PubMed
2.
go back to reference Ammon HV, Phillips SF (1974) Inhibition of ileal water absorption by intraluminal fatty acids. Influence of chain length, hydroxylation, and conjugation of fatty acids. J Clin Investig 53:205–210CrossRefPubMedPubMedCentral Ammon HV, Phillips SF (1974) Inhibition of ileal water absorption by intraluminal fatty acids. Influence of chain length, hydroxylation, and conjugation of fatty acids. J Clin Investig 53:205–210CrossRefPubMedPubMedCentral
3.
go back to reference Ammon HV, Thomas PJ, Phillips SF (1974) Effects of oleic and ricinoleic acids on net jejunal water and electrolyte movement. Perfusion studies in man. J Clin Investig 53:374–379CrossRefPubMedPubMedCentral Ammon HV, Thomas PJ, Phillips SF (1974) Effects of oleic and ricinoleic acids on net jejunal water and electrolyte movement. Perfusion studies in man. J Clin Investig 53:374–379CrossRefPubMedPubMedCentral
5.
go back to reference Bright-Asare P, Binder HJ (1973) Stimulation of colonic secretion of water and electrolytes by hydroxy fatty acids. Gastroenterology 64:81–88PubMed Bright-Asare P, Binder HJ (1973) Stimulation of colonic secretion of water and electrolytes by hydroxy fatty acids. Gastroenterology 64:81–88PubMed
6.
go back to reference Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K (2004) Bariatric surgery: a systematic review and meta-analysis. JAMA 292:1724–1737CrossRefPubMed Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K (2004) Bariatric surgery: a systematic review and meta-analysis. JAMA 292:1724–1737CrossRefPubMed
7.
go back to reference Canales BK, Ellen J, Khan SR, Hatch M (2013) Steatorrhea and hyperoxaluria occur after gastric bypass surgery in obese rats regardless of dietary fat or oxalate. J Urol 190:1102–1109CrossRefPubMedPubMedCentral Canales BK, Ellen J, Khan SR, Hatch M (2013) Steatorrhea and hyperoxaluria occur after gastric bypass surgery in obese rats regardless of dietary fat or oxalate. J Urol 190:1102–1109CrossRefPubMedPubMedCentral
8.
go back to reference Canales BK, Hatch M (2014) Kidney stone incidence and metabolic urinary changes after modern bariatric surgery: review of clinical studies, experimental models, and prevention strategies. Surg Obes Related Diseases 10:734–742CrossRef Canales BK, Hatch M (2014) Kidney stone incidence and metabolic urinary changes after modern bariatric surgery: review of clinical studies, experimental models, and prevention strategies. Surg Obes Related Diseases 10:734–742CrossRef
9.
go back to reference Canales BK, Reyes L, Reinhard MK, Khan SR, Goncalves CG, Meguid MM (2012) Renal glomerular and tubular injury after gastric bypass in obese rats. Nutrition 28:76–80CrossRefPubMedPubMedCentral Canales BK, Reyes L, Reinhard MK, Khan SR, Goncalves CG, Meguid MM (2012) Renal glomerular and tubular injury after gastric bypass in obese rats. Nutrition 28:76–80CrossRefPubMedPubMedCentral
10.
go back to reference Carlsson LM, Peltonen M, Ahlin S, Anveden A, Bouchard C, Carlsson B, Jacobson P, Lonroth H, Maglio C, Naslund I, Pirazzi C, Romeo S, Sjoholm K, Sjostrom E, Wedel H, Svensson PA, Sjostrom L (2012) Bariatric surgery and prevention of type 2 diabetes in Swedish obese subjects. N Engl J Med 367:695–704CrossRefPubMed Carlsson LM, Peltonen M, Ahlin S, Anveden A, Bouchard C, Carlsson B, Jacobson P, Lonroth H, Maglio C, Naslund I, Pirazzi C, Romeo S, Sjoholm K, Sjostrom E, Wedel H, Svensson PA, Sjostrom L (2012) Bariatric surgery and prevention of type 2 diabetes in Swedish obese subjects. N Engl J Med 367:695–704CrossRefPubMed
11.
go back to reference Cryer PE, Garber AJ, Hoffsten P, Lucas B, Wise L (1975) Renal failure after small intestinal bypass for obesity. Arch Intern Med 135:1610–1612CrossRefPubMed Cryer PE, Garber AJ, Hoffsten P, Lucas B, Wise L (1975) Renal failure after small intestinal bypass for obesity. Arch Intern Med 135:1610–1612CrossRefPubMed
12.
go back to reference Dobbins JW, Binder HJ (1976) Effect of bile salts and fatty acids on the colonic absorption of oxalate. Gastroenterology 70:1096–1100PubMed Dobbins JW, Binder HJ (1976) Effect of bile salts and fatty acids on the colonic absorption of oxalate. Gastroenterology 70:1096–1100PubMed
13.
go back to reference Dobbins JW, Binder HJ (1977) Importance of the colon in enteric hyperoxaluria. N Engl J Med 296:298–301CrossRefPubMed Dobbins JW, Binder HJ (1977) Importance of the colon in enteric hyperoxaluria. N Engl J Med 296:298–301CrossRefPubMed
14.
go back to reference Duffey BG, Alanee S, Pedro RN, Hinck B, Kriedberg C, Ikramuddin S, Kellogg T, Stressman M, Moeding A, Monga M (2010) Hyperoxaluria is a long-term consequence of Roux-en-Y gastric bypass: a 2-year prospective longitudinal study. J Am Coll Surg 211:8–15CrossRefPubMed Duffey BG, Alanee S, Pedro RN, Hinck B, Kriedberg C, Ikramuddin S, Kellogg T, Stressman M, Moeding A, Monga M (2010) Hyperoxaluria is a long-term consequence of Roux-en-Y gastric bypass: a 2-year prospective longitudinal study. J Am Coll Surg 211:8–15CrossRefPubMed
15.
go back to reference Durrani O, Morrisroe S, Jackman S, Averch T (2006) Analysis of stone disease in morbidly obese patients undergoing gastric bypass surgery. J Endourol/Endourol Soc 20:749–752CrossRef Durrani O, Morrisroe S, Jackman S, Averch T (2006) Analysis of stone disease in morbidly obese patients undergoing gastric bypass surgery. J Endourol/Endourol Soc 20:749–752CrossRef
16.
go back to reference Earnest DL (1987) Enteric hyperoxaluria. Adv Intern Med 24:407–427 Earnest DL (1987) Enteric hyperoxaluria. Adv Intern Med 24:407–427
17.
go back to reference Earnest DL, Johnson G, Williams HE, Admirand WH (1974) Hyperoxaluria in patients with ileal resection: an abnormality in dietary oxalate absorption. Gastroenterology 66:1114–1122PubMed Earnest DL, Johnson G, Williams HE, Admirand WH (1974) Hyperoxaluria in patients with ileal resection: an abnormality in dietary oxalate absorption. Gastroenterology 66:1114–1122PubMed
18.
go back to reference Earnest DL, Williams HE, Admirand WH (1975) A physicochemical basis for treatment of enteric hyperoxaluria. Trans Assoc Am Phys 88:224–234PubMed Earnest DL, Williams HE, Admirand WH (1975) A physicochemical basis for treatment of enteric hyperoxaluria. Trans Assoc Am Phys 88:224–234PubMed
19.
go back to reference Encinosa WE, Bernard DM, Chen CC, Steiner CA (2006) Healthcare utilization and outcomes after bariatric surgery. Med Care 44:706–712CrossRefPubMed Encinosa WE, Bernard DM, Chen CC, Steiner CA (2006) Healthcare utilization and outcomes after bariatric surgery. Med Care 44:706–712CrossRefPubMed
20.
go back to reference Freel RW, Hatch M, Earnest DL, Goldner AM (1980) Oxalate transport across the isolated rat colon. A re-examination. Biochim Biophys Acta 600:838–843CrossRefPubMed Freel RW, Hatch M, Earnest DL, Goldner AM (1980) Oxalate transport across the isolated rat colon. A re-examination. Biochim Biophys Acta 600:838–843CrossRefPubMed
21.
go back to reference Frizzell RA, Koch MJ, Schultz SG (1976) Ion transport by rabbit colon. I. Active and passive components. J Membrane Biol 27:297–316CrossRef Frizzell RA, Koch MJ, Schultz SG (1976) Ion transport by rabbit colon. I. Active and passive components. J Membrane Biol 27:297–316CrossRef
22.
go back to reference Gaginella TS, Lewis JC, Phillips SF (1976) Ricinoleic acid effects on rabbit intestine: an ultrastructural study. Mayo Clin Proc 51:569–573PubMed Gaginella TS, Lewis JC, Phillips SF (1976) Ricinoleic acid effects on rabbit intestine: an ultrastructural study. Mayo Clin Proc 51:569–573PubMed
23.
go back to reference Green ML, Hatch M, Freel RW (2005) Ethylene glycol induces hyperoxaluria without metabolic acidosis in rats. Am J Physiol Renal Physiol 289:F536–F543CrossRefPubMed Green ML, Hatch M, Freel RW (2005) Ethylene glycol induces hyperoxaluria without metabolic acidosis in rats. Am J Physiol Renal Physiol 289:F536–F543CrossRefPubMed
24.
go back to reference Hatch M, Cornelius J, Allison M, Sidhu H, Peck A, Freel RW (2006) Oxalobacter sp. reduces urinary oxalate excretion by promoting enteric oxalate secretion. Kidney Int 69:691–698CrossRefPubMed Hatch M, Cornelius J, Allison M, Sidhu H, Peck A, Freel RW (2006) Oxalobacter sp. reduces urinary oxalate excretion by promoting enteric oxalate secretion. Kidney Int 69:691–698CrossRefPubMed
25.
go back to reference Hatch M, Freel RW (2003) Renal and intestinal handling of oxalate following oxalate loading in rats. Am J Nephrol 23:18–26CrossRefPubMed Hatch M, Freel RW (2003) Renal and intestinal handling of oxalate following oxalate loading in rats. Am J Nephrol 23:18–26CrossRefPubMed
26.
go back to reference Hatch M, Freel RW (2008) The roles and mechanisms of intestinal oxalate transport in oxalate homeostasis. Seminars Nephrol 28:143–151CrossRef Hatch M, Freel RW (2008) The roles and mechanisms of intestinal oxalate transport in oxalate homeostasis. Seminars Nephrol 28:143–151CrossRef
27.
go back to reference Hatch M, Freel RW, Goldner AM, Earnest DL (1981) Effect of bile salt on active oxalate transport in the colon. In: Kasper H, Goebell H (eds) Colon and nutrition. MTP Press Limited, Lancaster, Boston, The Hague Hatch M, Freel RW, Goldner AM, Earnest DL (1981) Effect of bile salt on active oxalate transport in the colon. In: Kasper H, Goebell H (eds) Colon and nutrition. MTP Press Limited, Lancaster, Boston, The Hague
28.
go back to reference Hatch M, Freel RW, Goldner AM, Earnest DL (1983) Comparison of effects of low concentrations of ricinoleic and taurochenodeoxycholate on colonic oxalate and chloride absorption. Gastroenterology 84:1181 Hatch M, Freel RW, Goldner AM, Earnest DL (1983) Comparison of effects of low concentrations of ricinoleic and taurochenodeoxycholate on colonic oxalate and chloride absorption. Gastroenterology 84:1181
29.
go back to reference Hatch M, Freel RW, Vaziri ND (1994) Intestinal excretion of oxalate in chronic renal failure. J Am Soc Nephrol 5:1339–1343PubMed Hatch M, Freel RW, Vaziri ND (1994) Intestinal excretion of oxalate in chronic renal failure. J Am Soc Nephrol 5:1339–1343PubMed
30.
go back to reference Hofmann AF, Laker MF, Dharmsathaphorn K, Sherr HP, Lorenzo D (1983) Complex pathogenesis of hyperoxaluria after jejunoileal bypass surgery. Oxalogenic substances in diet contribute to urinary oxalate. Gastroenterology 84:293–300PubMed Hofmann AF, Laker MF, Dharmsathaphorn K, Sherr HP, Lorenzo D (1983) Complex pathogenesis of hyperoxaluria after jejunoileal bypass surgery. Oxalogenic substances in diet contribute to urinary oxalate. Gastroenterology 84:293–300PubMed
31.
go back to reference Jandacek RJ, Heubi JE, Tso P (2004) A novel, noninvasive method for the measurement of intestinal fat absorption. Gastroenterology 127:139–144CrossRefPubMed Jandacek RJ, Heubi JE, Tso P (2004) A novel, noninvasive method for the measurement of intestinal fat absorption. Gastroenterology 127:139–144CrossRefPubMed
32.
go back to reference Kathpalia SC, Favus MJ, Coe FL (1984) Evidence for size and charge permselectivity of rat ascending colon. Effects of ricinoleate and bile salts on oxalic acid and neutral sugar transport. J Clin Investig 74:805–811CrossRefPubMedPubMedCentral Kathpalia SC, Favus MJ, Coe FL (1984) Evidence for size and charge permselectivity of rat ascending colon. Effects of ricinoleate and bile salts on oxalic acid and neutral sugar transport. J Clin Investig 74:805–811CrossRefPubMedPubMedCentral
33.
go back to reference Knauf F, Ko N, Jiang Z, Robertson WG, Van Itallie CM, Anderson JM, Aronson PS (2011) Net intestinal transport of oxalate reflects passive absorption and SLC26A6-mediated secretion. J Am Soc Nephrol 22:2247–2255CrossRefPubMedPubMedCentral Knauf F, Ko N, Jiang Z, Robertson WG, Van Itallie CM, Anderson JM, Aronson PS (2011) Net intestinal transport of oxalate reflects passive absorption and SLC26A6-mediated secretion. J Am Soc Nephrol 22:2247–2255CrossRefPubMedPubMedCentral
34.
go back to reference Kumar R, Lieske JC, Collazo-Clavell ML, Sarr MG, Olson ER, Vrtiska TJ, Bergstralh EJ, Li X (2011) Fat malabsorption and increased intestinal oxalate absorption are common after Roux-en-Y gastric bypass surgery. Surgery 149:654–661CrossRefPubMedPubMedCentral Kumar R, Lieske JC, Collazo-Clavell ML, Sarr MG, Olson ER, Vrtiska TJ, Bergstralh EJ, Li X (2011) Fat malabsorption and increased intestinal oxalate absorption are common after Roux-en-Y gastric bypass surgery. Surgery 149:654–661CrossRefPubMedPubMedCentral
35.
go back to reference Lieske JC, Mehta RA, Milliner DS, Rule AD, Bergstralh EJ, Sarr MG (2014) Kidney stones are common after bariatric surgery Kidney international Lieske JC, Mehta RA, Milliner DS, Rule AD, Bergstralh EJ, Sarr MG (2014) Kidney stones are common after bariatric surgery Kidney international
36.
go back to reference Matlaga BR, Shore AD, Magnuson T, Clark JM, Johns R, Makary MA (2009) Effect of gastric bypass surgery on kidney stone disease. J Urol 181:2573–2577CrossRefPubMed Matlaga BR, Shore AD, Magnuson T, Clark JM, Johns R, Makary MA (2009) Effect of gastric bypass surgery on kidney stone disease. J Urol 181:2573–2577CrossRefPubMed
37.
go back to reference Nelson WK, Houghton SG, Milliner DS, Lieske JC, Sarr MG (2005) Enteric hyperoxaluria, nephrolithiasis, and oxalate nephropathy: potentially serious and unappreciated complications of Roux-en-Y gastric bypass. Surg Obesity Related Diseases 1:481–485CrossRef Nelson WK, Houghton SG, Milliner DS, Lieske JC, Sarr MG (2005) Enteric hyperoxaluria, nephrolithiasis, and oxalate nephropathy: potentially serious and unappreciated complications of Roux-en-Y gastric bypass. Surg Obesity Related Diseases 1:481–485CrossRef
38.
39.
go back to reference Siener R, Glatz S, Nicolay C, Hesse A (2004) The role of overweight and obesity in calcium oxalate stone formation. Obes Res 12:106–113CrossRefPubMed Siener R, Glatz S, Nicolay C, Hesse A (2004) The role of overweight and obesity in calcium oxalate stone formation. Obes Res 12:106–113CrossRefPubMed
40.
go back to reference Sinha MK, Collazo-Clavell ML, Rule A, Milliner DS, Nelson W, Sarr MG, Kumar R, Lieske JC (2007) Hyperoxaluric nephrolithiasis is a complication of Roux-en-Y gastric bypass surgery. Kidney Int 72:100–107CrossRefPubMed Sinha MK, Collazo-Clavell ML, Rule A, Milliner DS, Nelson W, Sarr MG, Kumar R, Lieske JC (2007) Hyperoxaluric nephrolithiasis is a complication of Roux-en-Y gastric bypass surgery. Kidney Int 72:100–107CrossRefPubMed
41.
go back to reference Sjostrom L, Peltonen M, Jacobson P, Sjostrom CD, Karason K, Wedel H, Ahlin S, Anveden A, Bengtsson C, Bergmark G, Bouchard C, Carlsson B, Dahlgren S, Karlsson J, Lindroos AK, Lonroth H, Narbro K, Naslund I, Olbers T, Svensson PA, Carlsson LM (2012) Bariatric surgery and long-term cardiovascular events. JAMA 307:56–65CrossRefPubMed Sjostrom L, Peltonen M, Jacobson P, Sjostrom CD, Karason K, Wedel H, Ahlin S, Anveden A, Bengtsson C, Bergmark G, Bouchard C, Carlsson B, Dahlgren S, Karlsson J, Lindroos AK, Lonroth H, Narbro K, Naslund I, Olbers T, Svensson PA, Carlsson LM (2012) Bariatric surgery and long-term cardiovascular events. JAMA 307:56–65CrossRefPubMed
42.
go back to reference Spak E, Bjorklund P, Helander HF, Vieth M, Olbers T, Casselbrant A, Lonroth H, Fandriks L (2010) Changes in the mucosa of the Roux-limb after gastric bypass surgery. Histopathology 57:680–688CrossRefPubMed Spak E, Bjorklund P, Helander HF, Vieth M, Olbers T, Casselbrant A, Lonroth H, Fandriks L (2010) Changes in the mucosa of the Roux-limb after gastric bypass surgery. Histopathology 57:680–688CrossRefPubMed
43.
go back to reference Stauffer JQ (1977) Hyperoxaluria and intestinal disease. The role of steatorrhea and dietary calcium in regulating intestinal oxalate absorption. Am J Digestive Diseases 22:921–928CrossRef Stauffer JQ (1977) Hyperoxaluria and intestinal disease. The role of steatorrhea and dietary calcium in regulating intestinal oxalate absorption. Am J Digestive Diseases 22:921–928CrossRef
44.
go back to reference Taylor EN, Curhan GC (2006) Body size and 24-hour urine composition. Am J Kidney Diseases 48:905–915CrossRef Taylor EN, Curhan GC (2006) Body size and 24-hour urine composition. Am J Kidney Diseases 48:905–915CrossRef
Metadata
Title
The mechanistic basis of hyperoxaluria following gastric bypass in obese rats
Authors
Marguerite Hatch
Benjamin K. Canales
Publication date
01-06-2016
Publisher
Springer Berlin Heidelberg
Published in
Urolithiasis / Issue 3/2016
Print ISSN: 2194-7228
Electronic ISSN: 2194-7236
DOI
https://doi.org/10.1007/s00240-015-0836-7

Other articles of this Issue 3/2016

Urolithiasis 3/2016 Go to the issue