Effect of a Probiotic Supplement Containing Lactobacillus Acidophilus and Bifidobacterium Animalis Lactis on Urine Oxalate in Calcium Stone Formers with Hyperoxaluria: A Randomized, Placebo-controlled, Double-blind and In-vitro Trial
Urology Journal,
Vol. 19 No. 03 (2022),
6 June 2022
,
Page 179-188
https://doi.org/10.22037/uj.v19i03.6789
Abstract
Purpose: To determine the effect of a probiotic supplement containing native Lactobacillus acidophilus (L. acidophilus) and Bifidobacterium animalis lactis (B. lactis) on 24-hour urine oxalate in recurrent calcium stone formers with hyperoxaluria. Moreover, the in-vitro oxalate degradation capacity and the intestinal colonization of consumed probiotics were evaluated.
Materials and Methods: The oxalate degrading activity of L. acidophilus and B. lactis were evaluated in-vitro. The presence of oxalyl-CoA decarboxylase (oxc) gene in the probiotic species was assessed. One hundred patients were randomized to receive the probiotic supplement or placebo for four weeks. The 24-hour urine oxalate and the colonization of consumed probiotics were assessed after weeks four and eight.
Results: Although the oxc gene was present in both species, only L. acidophilus had a good oxalate degrading activity, in-vitro. Thirty-four patients from the probiotic and thirty patients from the placebo group finished the study. The urine oxalate changes were not significantly different between groups (57.21 ± 11.71 to 49.44 ± 18.14 mg/day for probiotic, and 56.43 ± 9.89 to 50.47 ± 18.04 mg/day for placebo) (P = .776). The probiotic consumption had no significant effect on urine oxalate, both in univariable (P = .771) and multivariable analyses (P = .490). The consumed probiotics were not detected in the stool samples of most participants.
Conclusion: Our results showed that the consumption of a probiotic supplement containing L. acidophilus and B. lactis did not affect urine oxalate. The results may be due to a lack of bacterial colonization in the intestine.
Keywords:
- Lactobacillus acidophilus, Bifidobacterium animalis subsp. lactis, Hyperoxaluria, Probiotics, Urolithiasis, Calcium oxalate.
How to Cite
Tavasoli, S., Jalali, S. ., Naji, M. ., Borumandnia, N. ., Shakiba Majd, G. ., Basiri, A. ., Khosravi Darani, K. ., Karamad, D. ., Tajabadi-Ebrahimi, M. ., & Taheri, M. . (2021). Effect of a Probiotic Supplement Containing Lactobacillus Acidophilus and Bifidobacterium Animalis Lactis on Urine Oxalate in Calcium Stone Formers with Hyperoxaluria: A Randomized, Placebo-controlled, Double-blind and In-vitro Trial. Urology Journal, 19(03), 179–188. https://doi.org/10.22037/uj.v19i03.6789
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17. Campieri C, Campieri M, Bertuzzi V, et al. Reduction of oxaluria after an oral course of lactic acid bacteria at high concentration. Kidney Int. 2001;60:1097-105.
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19. Tavasoli S, Alebouyeh M, Naji M, et al. The association of the intestinal oxalate degrading bacteria with recurrent calcium kidney stone formation and hyperoxaluria: a case-control study. BJU Int. 2020;125:133-43.
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23. Tobin JM, Garland SM, Jacobs SE, Pirotta M, Tabrizi SN. Rapid assay to assess colonization patterns following in-vivo probiotic ingestion. BMC Res Notes. 2013;6:252.
24. Kim SE, Choi SC, Park KS, et al. Change of Fecal Flora and Effectiveness of the Short-term VSL#3 Probiotic Treatment in Patients With Functional Constipation. J Neurogastroenterol Motil. 2015;21:111-20.
25. Walker AW, Martin JC, Scott P, Parkhill J, Flint HJ, Scott KP. 16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice. Microbiome. 2015;3:26.
26. Bhasin B, Ürekli HM, Atta MG. Primary and secondary hyperoxaluria: Understanding the enigma. World J Nephrol. 2015;4:235-44.
27. Burns Z, Knight J, Fargue S, Holmes R, Assimos D, Wood K. Future treatments for hyperoxaluria. Curr Opin Urol. 2020;30:171-6.
28. Siener R, Bade DJ, Hesse A, Hoppe B. Dietary hyperoxaluria is not reduced by treatment with lactic acid bacteria. J Transl Med. 2013;11:306.
29. Lieske JC, Tremaine WJ, De Simone C, et al. Diet, but not oral probiotics, effectively reduces urinary oxalate excretion and calcium oxalate supersaturation. Kidney Int. 2010;78:1178-85.
30. Ferraz RR, Marques NC, Froeder L, et al. Effects of Lactobacillus casei and Bifidobacterium breve on urinary oxalate excretion in nephrolithiasis patients. Urol Res. 2009;37:95-100.
31. Azcarate-Peril MA, Bruno-Barcena JM, Hassan HM, Klaenhammer TR. Transcriptional and functional analysis of oxalyl-coenzyme A (CoA) decarboxylase and formyl-CoA transferase genes from Lactobacillus acidophilus. Appl Environ Microbiol. 2006;72:1891-9.
32. Federici F, Vitali B, Gotti R, et al. Characterization and heterologous expression of the oxalyl coenzyme A decarboxylase gene from Bifidobacterium lactis. Appl Environ Microbiol. 2004;70:5066-73.
33. Nugent SG, Kumar D, Rampton DS, Evans DF. Intestinal luminal pH in inflammatory bowel disease: possible determinants and implications for therapy with aminosalicylates and other drugs. Gut. 2001;48:571.
34. Alander M, Satokari R, Korpela R, et al. Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol. 1999;65:351-4.
35. Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, Shouche YS. Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep. 2016;6:34712.
36. Tang R, Jiang Y, Tan A, et al. 16S rRNA gene sequencing reveals altered composition of gut microbiota in individuals with kidney stones. Urolithiasis. 2018.
37. Ticinesi A, Nouvenne A, Meschi T. Gut microbiome and kidney stone disease: not just an Oxalobacter story. Kidney Int. 2019;96:25-7.
38. Stern JM, Moazami S, Qiu Y, et al. Evidence for a distinct gut microbiome in kidney stone formers compared to non-stone formers. Urolithiasis. 2016;44:399-407.
39. Liu M, Koh H, Kurtz ZD, et al. Oxalobacter formigenes-associated host features and microbial community structures examined using the American Gut Project. Microbiome. 2017;5:108.
40. Miller AW, Oakeson KF, Dale C, Dearing MD. Microbial Community Transplant Results in Increased and Long-Term Oxalate Degradation. Microb Ecol. 2016;72:470-8.
41. Assimos DG. Re: Microbial Community Transplant Results in Increased and Long-Term Oxalate Degradation. J Urol. 2016;196:1586-7.
2. Türk C, Neisius A, Petrik A, Seitz C, Skolarikos A, Thomas K. EAU Guidelines on Urolithiasis. http://uroweb.org/guideline/urolithiasis/. Accessed 6 Sep 2020.
3. Goldfarb DS, Modersitzki F, Asplin JR. A randomized, controlled trial of lactic acid bacteria for idiopathic hyperoxaluria. Clin J Am Soc Nephrol. 2007;2:745-9.
4. Brzica H, Breljak D, Burckhardt BC, Burckhardt G, Sabolic I. Oxalate: from the environment to kidney stones. Arh Hig Rada Toksikol. 2013;64:609-30.
5. Abratt VR, Reid SJ. Oxalate-degrading bacteria of the human gut as probiotics in the management of kidney stone disease. Adv Appl Microbiol. 2010;72:63-87.
6. Robijn S, Hoppe B, Vervaet BA, D'Haese PC, Verhulst A. Hyperoxaluria: a gut-kidney axis? Kidney Int. 2011;80:1146-58.
7. Mehta M, Goldfarb DS, Nazzal L. The role of the microbiome in kidney stone formation. Int J Surg. 2016;36:607-12.
8. Ticinesi A, Milani C, Guerra A, et al. Understanding the gut-kidney axis in nephrolithiasis: an analysis of the gut microbiota composition and functionality of stone formers. Gut. 2018;67:2097-106.
9. Lieske JC. Probiotics for prevention of urinary stones. Ann Transl Med. 2017;5:29.
10. Assimos DG. Re: dietary hyperoxaluria is not reduced by treatment with lactic acid bacteria. J Urol. 2014;191:1810.
11. Turroni S, Vitali B, Bendazzoli C, et al. Oxalate consumption by lactobacilli: evaluation of oxalyl-CoA decarboxylase and formyl-CoA transferase activity in Lactobacillus acidophilus. J Appl Microbiol. 2007;103:1600-9.
12. Turroni S, Bendazzoli C, Dipalo SC, et al. Oxalate-degrading activity in Bifidobacterium animalis subsp. lactis: impact of acidic conditions on the transcriptional levels of the oxalyl coenzyme A (CoA) decarboxylase and formyl-CoA transferase genes. Appl Environ Microbiol. 2010;76:5609-20.
13. Mogna L, Pane M, Nicola S, Raiteri E. Screening of different probiotic strains for their in vitro ability to metabolise oxalates: any prospective use in humans? J Clin Gastroenterol. 2014;48 Suppl 1:S91-5.
14. Klimesova K, Whittamore JM, Hatch M. Bifidobacterium animalis subsp. lactis decreases urinary oxalate excretion in a mouse model of primary hyperoxaluria. Urolithiasis. 2015;43:107-17.
15. Kwak C, Jeong BC, Ku JH, et al. Prevention of nephrolithiasis by Lactobacillus in stone-forming rats: a preliminary study. Urol Res. 2006;34:265-70.
16. Karamad D, Khosravi-Darani K, Hosseini H, Tavasoli S, Miller AW. Evaluation of Oxalobacter formigenes DSM 4420 biodegradation activity for high oxalate media content: An in vitro model. Biocatal Agric Biotechnol. 2019;22:101378.
17. Campieri C, Campieri M, Bertuzzi V, et al. Reduction of oxaluria after an oral course of lactic acid bacteria at high concentration. Kidney Int. 2001;60:1097-105.
18. Karamad D, Khosravi-Darani K, Hosseini H, Tavasoli S. Analytical procedures and methods validation for oxalate content estimation. Biointerface Res Appl Chem. 2019;9:4305-10.
19. Tavasoli S, Alebouyeh M, Naji M, et al. The association of the intestinal oxalate degrading bacteria with recurrent calcium kidney stone formation and hyperoxaluria: a case-control study. BJU Int. 2020;125:133-43.
20. Goldfarb DS, MacDonald PA, Gunawardhana L, Chefo S, McLean L. Randomized controlled trial of febuxostat versus allopurinol or placebo in individuals with higher urinary uric acid excretion and calcium stones. Clin J Am Soc Nephrol. 2013;8:1960-7.
21. Farmer KC. Methods for measuring and monitoring medication regimen adherence in clinical trials and clinical practice. Clin Ther. 1999;21:1074-90; discussion 3.
22. Noori N, Honarkar E, Goldfarb DS, et al. Urinary lithogenic risk profile in recurrent stone formers with hyperoxaluria: a randomized controlled trial comparing DASH (Dietary Approaches to Stop Hypertension)-style and low-oxalate diets. Am J Kidney Dis. 2014;63:456-63.
23. Tobin JM, Garland SM, Jacobs SE, Pirotta M, Tabrizi SN. Rapid assay to assess colonization patterns following in-vivo probiotic ingestion. BMC Res Notes. 2013;6:252.
24. Kim SE, Choi SC, Park KS, et al. Change of Fecal Flora and Effectiveness of the Short-term VSL#3 Probiotic Treatment in Patients With Functional Constipation. J Neurogastroenterol Motil. 2015;21:111-20.
25. Walker AW, Martin JC, Scott P, Parkhill J, Flint HJ, Scott KP. 16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice. Microbiome. 2015;3:26.
26. Bhasin B, Ürekli HM, Atta MG. Primary and secondary hyperoxaluria: Understanding the enigma. World J Nephrol. 2015;4:235-44.
27. Burns Z, Knight J, Fargue S, Holmes R, Assimos D, Wood K. Future treatments for hyperoxaluria. Curr Opin Urol. 2020;30:171-6.
28. Siener R, Bade DJ, Hesse A, Hoppe B. Dietary hyperoxaluria is not reduced by treatment with lactic acid bacteria. J Transl Med. 2013;11:306.
29. Lieske JC, Tremaine WJ, De Simone C, et al. Diet, but not oral probiotics, effectively reduces urinary oxalate excretion and calcium oxalate supersaturation. Kidney Int. 2010;78:1178-85.
30. Ferraz RR, Marques NC, Froeder L, et al. Effects of Lactobacillus casei and Bifidobacterium breve on urinary oxalate excretion in nephrolithiasis patients. Urol Res. 2009;37:95-100.
31. Azcarate-Peril MA, Bruno-Barcena JM, Hassan HM, Klaenhammer TR. Transcriptional and functional analysis of oxalyl-coenzyme A (CoA) decarboxylase and formyl-CoA transferase genes from Lactobacillus acidophilus. Appl Environ Microbiol. 2006;72:1891-9.
32. Federici F, Vitali B, Gotti R, et al. Characterization and heterologous expression of the oxalyl coenzyme A decarboxylase gene from Bifidobacterium lactis. Appl Environ Microbiol. 2004;70:5066-73.
33. Nugent SG, Kumar D, Rampton DS, Evans DF. Intestinal luminal pH in inflammatory bowel disease: possible determinants and implications for therapy with aminosalicylates and other drugs. Gut. 2001;48:571.
34. Alander M, Satokari R, Korpela R, et al. Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol. 1999;65:351-4.
35. Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, Shouche YS. Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep. 2016;6:34712.
36. Tang R, Jiang Y, Tan A, et al. 16S rRNA gene sequencing reveals altered composition of gut microbiota in individuals with kidney stones. Urolithiasis. 2018.
37. Ticinesi A, Nouvenne A, Meschi T. Gut microbiome and kidney stone disease: not just an Oxalobacter story. Kidney Int. 2019;96:25-7.
38. Stern JM, Moazami S, Qiu Y, et al. Evidence for a distinct gut microbiome in kidney stone formers compared to non-stone formers. Urolithiasis. 2016;44:399-407.
39. Liu M, Koh H, Kurtz ZD, et al. Oxalobacter formigenes-associated host features and microbial community structures examined using the American Gut Project. Microbiome. 2017;5:108.
40. Miller AW, Oakeson KF, Dale C, Dearing MD. Microbial Community Transplant Results in Increased and Long-Term Oxalate Degradation. Microb Ecol. 2016;72:470-8.
41. Assimos DG. Re: Microbial Community Transplant Results in Increased and Long-Term Oxalate Degradation. J Urol. 2016;196:1586-7.
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