Inhibition of the Accumulation of Uremic Toxins in the Blood and Their Precursors in the Feces after Oral Administration of Lebenin®, a Lactic Acid Bacteria Preparation, to Uremic Patients Undergoing Hemodialysis
Abstract
The plasma levels of phenol, p-cresol, and indican are markedly increased in uremic patients, and cannot be efficiently reduced by hemodialysis. Such uremic toxins, which are produced in the intestine as bacterial putrefactive metabolites, accumulate to a great degree in the feces of hemodialysis patients. Oral administration of Lebenin®, a preparation consisting of antibiotic-resistant lactic acid bacteria, reduced the levels of fecal putrefactive metabolites to levels comparable with those of healthy subjects. Moreover, the plasma level of indican also significantly decreased in these Lebenin-treated patients. An analysis of the fecal microflora revealed that a disturbed composition of the microflora characterized by an overgrowth of aerobic bacteria is restored to normal by oral administration of Lebenin in hemodialysis patients. These results thus demonstate that oral administration of lactic acid bacteria in uremic patients is effective in reducing the levels of uremic toxins, especially that of indican, in the blood by inhibiting bacterial production by means of correcting the intestinal microflora.
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Beneficial effects of Lactobacillus could result from effects of this bacterium on permeability and immune status of the gut epithelium.
“Such beneficial effects of Lactobacillus could be the result of effects of this bacteria on the permeability and immune status of the gut epithelium.”
From The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease (2018) · cites this paper as [218]
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Vanholder, R. C., For the European Uremic Toxin Work Group (EUTox), Smet, R. D., Glorieux, G., Argilés, À., Baurmeister, U., Brunet, P., Clark, W. R., Cohen, G., Deyn, P. P. D., et al. (2003) · Kidney International · doi:10.1046/j.1523-1755.2003.00924.x · Cited by 1,716 · see citing works
Normal and Pathologic Concentrations of Uremic Toxins
Duranton, F., Cohen, G., Smet, R. D., Rodríguez, M., Jankowski, J., Vanholder, R. C., & Argilés, À. (2012) · Journal of the American Society of Nephrology · doi:10.1681/asn.2011121175 · Cited by 965 · see citing works
The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease
Yang, T., Richards, E. M., Pepine, C. J., & Raizada, M. K. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0018-2 · Cited by 753 · see citing works
The Gut Microbiome, Kidney Disease, and Targeted Interventions
Ramezani, A., & Raj, D. S. (2013) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013080905 · Cited by 753 · see citing works
The uremic solutes p-cresol and indoxyl sulfate inhibit endothelial proliferation and wound repair
Dou, L., Bertrand, E., Cérini, C., Faure, V., Sampol, J., Vanholder, R., Berland, Y., & Brunet, P. (2004) · Kidney International · doi:10.1111/j.1523-1755.2004.00399.x · Cited by 487 · see citing works
The Gut as a Source of Inflammation in Chronic Kidney Disease
Lau, W. L., Kalantar‐Zadeh, K., & Vaziri, N. D. (2015) · The Nephron journals/Nephron journals · doi:10.1159/000381990 · Cited by 462 · see citing works
Serum Trimethylamine-N-Oxide is Elevated in CKD and Correlates with Coronary Atherosclerosis Burden
Stubbs, J. R., House, J. A., Ocque, A. J., Zhang, S., Johnson, C., Kimber, C., Schmidt, K., Gupta, A., Wetmore, J. B., Nolin, T. D., et al. (2016) · Journal of the American Society of Nephrology · doi:10.1681/asn.2014111063 · Cited by 450 · see citing works
Metabolic surgery profoundly influences gut microbial–host metabolic cross-talk
Li, J. V., Ashrafian, H., Bueter, M., Kinross, J. K., Sands, C. J., le Roux, C. W., Bloom, S. R., Darzi, A. W., Athanasiou, T., Marchesi, J. R., et al. (2011) · Gut · doi:10.1136/gut.2010.234708 · Cited by 444 · see citing works
Uremic toxins originating from colonic microbial metabolism
Evenepoel, P., Meijers, B. K. I., Bammens, B., & Verbeke, K. (2009) · Kidney International · doi:10.1038/ki.2009.402 · Cited by 448 · see citing works
Microbiome–metabolome reveals the contribution of gut–kidney axis on kidney disease
Chen, Y., Chen, D., Chen, L., Liu, J., Vaziri, N. D., Guo, Y. P., & Zhao, Y. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-018-1756-4 · Cited by 430 · see citing works
Gryp, T., Vanholder, R. C., Vaneechoutte, M., & Glorieux, G. (2017) · Toxins · doi:10.3390/toxins9020052 · Cited by 413 · see citing works
“acidophilus decreased faecal p-cresol levels in healthy persons [85].”
BackgroundInfluentialRole of the Gut Microbiome in Uremia: A Potential Therapeutic Target
Ramezani, A., Massy, Z. A., Meijers, B., Evenepoel, P., Vanholder, R., & Raj, D. S. (2016) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2015.09.027 · Cited by 394 · see citing works
Synbiotics Easing Renal Failure by Improving Gut Microbiology (SYNERGY)
Rossi, M., Johnson, D. W., Morrison, M., Pascoe, E. M., Coombes, J. S., Forbes, J. M., Szeto, C., McWhinney, B. C., Ungerer, J. P. J., & Campbell, K. L. (2016) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.05240515 · Cited by 379 · see citing works
A Bench to Bedside View of Uremic Toxins
Vanholder, R. C., Baurmeister, U., Brunet, P., Cohen, G., Glorieux, G., & Jankowski, J. (2008) · Journal of the American Society of Nephrology · doi:10.1681/asn.2007121377 · Cited by 355 · see citing works
Inflammation in Renal Diseases: New and Old Players
Andrade‐Oliveira, V., Foresto‐Neto, O., Watanabe, I. K. M., Zatz, R., & Câmara, N. O. S. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01192 · Cited by 330 · see citing works
“Growing evidence has shown significant changes in the gut microbiota of CKD patients in terms of individual species (Hida et al., 1996; Wang I et al., 2012; Vaziri et al., 2013).”
BackgroundThe Impact of CKD on Uremic Toxins and Gut Microbiota
Rysz, J., Franczyk, B., Ławiński, J., Olszewski, R., Ciałkowska-Rysz, A. D., & Gluba-Brzózka, A. (2021) · Toxins · doi:10.3390/toxins13040252 · Cited by 314 · see citing works
“[7] observed significantly higher amount of Clostridium perfringens in these patients.”
BackgroundResultMeijers, B. K. I., Preter, V. D., Verbeke, K., Vanrenterghem, Y. F. C., & Evenepoel, P. (2009) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfp414 · Cited by 301 · see citing works
“Bifidobacterium infantis, Lactobacillus acidophilus and Enterococcus faecalis) did not reduce p-cresol serum concentrations [30].”
BackgroundEvenepoel, P., Poesen, R., & Meijers, B. (2017) · Pediatric Nephrology · doi:10.1007/s00467-016-3527-x · Cited by 305 · see citing works
Protein nutrition and malnutrition in CKD and ESRD
Zha, Y., & Qian, Q. (2017) · Nutrients · doi:10.3390/nu9030208 · Cited by 292 · see citing works
“As illustrated in Figure 2, altered gut microbiome profile, evidenced in even the early stages of CKD [31] and in ESRD [32,33], plays an important role in the genesis of inflammation.”
BackgroundIndoxyl Sulfate—Review of Toxicity and Therapeutic Strategies
Leong, S. C., & Sirich, T. L. (2016) · Toxins · doi:10.3390/toxins8120358 · Cited by 273 · see citing works
Alteration of the gut microbiota in Chinese population with chronic kidney disease
Jiang, S., Xie, S., Lv, D., Wang, P., He, H., Zhang, T., Zhou, Y., Lin, Q., Zhou, H., Jiang, J., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-02989-2 · Cited by 265 · see citing works
Probiotics and chronic kidney disease
Koppe, L., Mafra, D., & Fouque, D. P. (2015) · Kidney International · doi:10.1038/ki.2015.255 · Cited by 264 · see citing works
Therapeutical use of probiotic formulations in clinical practice
Iannitti, T., & Palmieri, B. (2010) · Clinical Nutrition · doi:10.1016/j.clnu.2010.05.004 · Cited by 262 · see citing works
“62 demonstrated that Lebenin, a preparation consisting of antibiotic-resistant lactic acid bacteria, administred orally is able to reduce the levels of fecal putrefactive metabolites to levels comparable with those of healthy subjects.”
BackgroundReduction of oxaluria after an oral course of lactic acid bacteria at high concentration
Campieri, C., Campieri, M., Bertuzzi, V., Swennen, E., Matteuzzi, D., Stefoni, S., Pirovano, F., Centi, C., Ulisse, S., Famularo, G., et al. (2001) · Kidney International · doi:10.1046/j.1523-1755.2001.0600031097.x · Cited by 239 · see citing works
Food as medicine: targeting the uraemic phenotype in chronic kidney disease
Mafra, D., Borges, N. A., Lindholm, B., Shiels, P. G., Evenepoel, P., & Stenvinkel, P. (2021) · Nature Reviews Nephrology · doi:10.1038/s41581-020-00345-8 · Cited by 238 · see citing works
Alterations of intestinal barrier and microbiota in chronic kidney disease
Sabatino, A., Regolisti, G., Brusasco, I., Cabassi, A., Morabito, S., & Fiaccadori, E. (2014) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfu287 · Cited by 227 · see citing works
Wang, I. ‐., Wu, Y. Y., Yang, Y., Ting, I., Lin, C. C., Yen, T., Chen, J.-H., Wang, C., Huang, C.-F., & Lin, H. (2015) · Beneficial Microbes · doi:10.3920/bm2014.0088 · Cited by 223 · see citing works
“Treatment with Bifidobacterium infantis, Lactobacillus acidophilus and Enterococcus faecalis reduced the serum levels of uremic toxin, indole, and inhibited overgrowth of aerobic bacteria (Hida et al., 1996).”
BackgroundInfluentialIndoxyl Sulfate: A Novel Cardiovascular Risk Factor in Chronic Kidney Disease
Hung, S., Kuo, K., Wu, C., & Tarng, D. (2017) · Journal of the American Heart Association · doi:10.1161/jaha.116.005022 · Cited by 216 · see citing works
Nakabayashi, I., Nakamura, M., Kawakami, K., Ohta, T., Kato, I., Uchida, K., & Yoshida, M. (2010) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfq624 · Cited by 215 · see citing works
“Prolonged transit time in the colon, abnormal intestinal flora and abnormal defecation (especially constipation) are frequently observed in HD patients [10–12].”
BackgroundProbiotic supplementation in diabetic hemodialysis patients has beneficial metabolic effects
Soleimani, A., Mojarrad, M. Z., Bahmani, F., Taghizadeh, M., Ramezani, M., Ebrahimi, M. T., Jafari, P., Esmaillzadeh, A., & Asemi, Z. (2016) · Kidney International · doi:10.1016/j.kint.2016.09.040 · Cited by 215 · see citing works
Gryp, T., Paepe, K. D., Vanholder, R. C., Kerckhof, F., Biesen, W. V., de Wiele, T. V., Verbeke, F., Speeckaert, M. M., Joossens, M., Couttenye, M. M., et al. (2020) · Kidney International · doi:10.1016/j.kint.2020.01.028 · Cited by 212 · see citing works
“Similar results were found in a culture-based study comparing HD and controls.(34) However, in other studies, using quantitative polymerase chain reaction and culture, a decrease in total fecal bacteria was found in CKD, non-dialyzed and dialyzed patients with end-stage kidney disease compared to controls.”
ResultWernimont, S. M., Radosevich, J., Jackson, M. I., Ephraim, E., Badri, D. V., MacLeay, J. M., Jewell, D. E., & Suchodolski, J. S. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01266 · Cited by 220 · see citing works
“However, one recent study showed that cats with CKD had decreased richness and diversity of the fecal microbiome compared with healthy cats (Summers et al., 2019), which is consistent with prior studies of the intestinal microbiome in humans with CKD (Hida et al., 1996; Vaziri et al., 2013).”
ResultInfluentialBammens, B., Evenepoel, P., Verbeke, K., & Vanrenterghem, Y. F. C. (2003) · Kidney International · doi:10.1046/j.1523-1755.2003.00310.x · Cited by 202 · see citing works
“We recognize that the serum levels of p-cresol found by our laboratory are higher than most other values reported in the literature [45, 46].”
ResultFeng, Y., Cao, G., Chen, D., Vaziri, N. D., Chen, L., Zhang, J., Wang, M., Guo, Y. P., & Zhao, Y. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03155-9 · Cited by 201 · see citing works
Intestinal Microbiota in Type 2 Diabetes and Chronic Kidney Disease
Sabatino, A., Regolisti, G., Cosola, C., Gesualdo, L., & Fiaccadori, E. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0841-z · Cited by 201 · see citing works
p-Cresyl Sulfate and Indoxyl Sulfate in Hemodialysis Patients
Meijers, B. K. I., de Loor, H., Bammens, B., Verbeke, K., Vanrenterghem, Y. F. C., & Evenepoel, P. (2009) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.02940509 · Cited by 175 · see citing works
The Role of the Gut Microbiome in Diabetes and Obesity-Related Kidney Disease
Zaky, A. A., Glastras, S. J., Wong, M. Y. W., Pollock, C. A., & Saad, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179641 · Cited by 174 · see citing works
Cason, C. A., Dolan, K. T., Sharma, G., Tao, M., Kulkarni, R. N., Helenowski, I., Doane, B. M., Avram, M. J., McDermott, M. M., Chang, E. B., et al. (2017) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2017.09.029 · Cited by 166 · see citing works
Dhondt, A., Vanholder, R., Biesen, W. V., et al. (2000) · Kidney International · doi:10.1046/j.1523-1755.2000.07606.x · Cited by 158 · see citing works
Borges, N. A., do Carmo, F. L., Stockler‐Pinto, M. B., de Brito, J. S., Dolenga, C. J. R., Ferreira, D. D. C., Nakao, L. S., Rosado, A. S., Fouque, D. P., & Mafra, D. (2017) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2017.06.010 · Cited by 155 · see citing works
“Hida et al. (1996)9 in a study involving 25 HD patients showed that a supplementation of a probiotic formulation (Bifidobacterium infantis, Lactobacillus acidophilus, and Enterococcus faecalis) for 4 weeks led to a reduction in fecal p-cresol, whereas the reduction in p-cresol plasma levels was…”
BackgroundJiang, S., Xie, S., Lv, D., Zhang, Y., Deng, J., Zeng, L., & Chen, Y. (2016) · Antonie van Leeuwenhoek · doi:10.1007/s10482-016-0737-y · Cited by 154 · see citing works
“A faecal analysis revealed an overgrowth of aerobic bacteria in hemodialysis patients (Hida et al. 1996).”
BackgroundMikusic, N. L. R., Kouyoumdzian, N. M., & Choi, M. R. (2020) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-020-02352-x · Cited by 154 · see citing works
The Gut: The Forgotten Organ in Uremia?
Schepers, E., Glorieux, G., & Vanholder, R. C. (2010) · Blood Purification · doi:10.1159/000245639 · Cited by 150 · see citing works
“In addition, the concentration of uremic solutes in the gut may also be influenced by excretion into the intestine, e.g. by the gall bladder. A further contributing factor is a shift in the composition of the intestinal flora due to the uremic condition, favoring overgrowth of bacteria producing toxic compounds (fig.…”
BackgroundTakayama, F., Taki, K., & Niwa, T. (2003) · American Journal of Kidney Diseases · doi:10.1053/ajkd.2003.50104 · Cited by 146 · see citing works
Gut dysbiosis: Ecological causes and causative effects on human disease
Winter, S., & Bäumler, A. J. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2316579120 · Cited by 152 · see citing works
“Fecal microbiota profiling reveals that a shift in the species composition, termed gut dysbiosis, is observed in diseases that include leading causes of human mor bidity and mortality, such as cardiovascular disease (CVD) (6), diabetes (7, 8), colorectal cancer (CRC) (9), chronic kidney disease (CKD) (10), and inflam…”
BackgroundInfluentialMicrobiota intestinal en la enfermedad renal crónica
Cigarrán, S., Parra, E. G., & Cases, A. (2016) · Nefrología · doi:10.1016/j.nefro.2016.05.008 · Cited by 142 · see citing works
Gut-Derived Protein-Bound Uremic Toxins
Graboski, A. L., & Redinbo, M. R. (2020) · Toxins · doi:10.3390/toxins12090590 · Cited by 137 · see citing works
Real-Time PCR Analysis of the Intestinal Microbiotas in Peritoneal Dialysis Patients
Wang, I., Lai, H., Yu, C., Liang, C., Chang, C., Kuo, H., Yang, Y., Lin, C., Lin, H., Liu, Y., et al. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05605-11 · Cited by 128 · see citing works
The Influence of CKD on Colonic Microbial Metabolism
Poesen, R., Windey, K., Neven, E., Kuypers, D. R. J., Preter, V. D., Augustijns, P., D’Haese, P. C., Evenepoel, P., Verbeke, K., & Meijers, B. K. I. (2015) · Journal of the American Society of Nephrology · doi:10.1681/asn.2015030279 · Cited by 123 · see citing works
Urea, a true uremic toxin: the empire strikes back
Lau, W. L., & Vaziri, N. D. (2016) · Clinical Science · doi:10.1042/cs20160203 · Cited by 122 · see citing works
Gryp, T., Huys, G. R. B., Joossens, M., Biesen, W. V., Glorieux, G., & Vaneechoutte, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21061986 · Cited by 122 · see citing works
“These elevated levels of aerobes, shown to inhibit anaerobic bacterial growth [23,30], could also negatively interfere with the activity of SCFA-generating bacteria.”
BackgroundResultInfluentialThe Role of the Gut Microbiome on Chronic Kidney Disease
Sampaio‐Maia, B., Simões‐Silva, L., Pestana, M., Araújo, R., & Soares‐Silva, I. (2016) · Advances in applied microbiology · doi:10.1016/bs.aambs.2016.06.002 · Cited by 117 · see citing works
Cardiotoxicity of Uremic Toxins: A Driver of Cardiorenal Syndrome
Lekawanvijit, S. (2018) · Toxins · doi:10.3390/toxins10090352 · Cited by 118 · see citing works
“Probiotics [196,197] using good live microorganisms, prebiotics [198] using non-digestible dietary fiber to modify microbial environment, synbiotics [199,200] using combined probiotic and prebiotic treatment and laxatives [201] for accelerating colon transit of amino acid substrates, have been all demonstrated to redu…”
Taki, K., Takayama, F., & Niwa, T. (2005) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2004.09.028 · Cited by 108 · see citing works
p-Cresol: a toxin revealing many neglected but relevant aspects of uraemic toxicity
Vanholder, R. C., Smet, R. D., & Lesaffer, G. (1999) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/14.12.2813 · Cited by 108 · see citing works
Rossi, M., Klein, K., Johnson, D. W., & Campbell, K. L. (2012) · International Journal of Nephrology · doi:10.1155/2012/673631 · Cited by 105 · see citing works
Mafune, A., Iwamoto, T., Tsutsumi, Y., Nakashima, A., Yamamoto, I., Yokoyama, K., Yokoo, T., & Urashima, M. (2016) · Clinical and Experimental Nephrology · doi:10.1007/s10157-015-1207-y · Cited by 103 · see citing works
The intestine and the kidneys: a bad marriage can be hazardous
Vanholder, R. C., & Glorieux, G. (2015) · Clinical Kidney Journal · doi:10.1093/ckj/sfv004 · Cited by 101 · see citing works
“In haemodialysis patients, Lebenin®, a mixture of antibiotic-resistant lactic acid bacteria, resulted in a decrease in plasma indoxyl sulphate but not in phenol and p-cresol [86].”
BackgroundResultInfluentialMiyazaki, K., Masuoka, N., Mitsuyoshi, K. A. N. O., & Iizuka, R. (2013) · Beneficial Microbes · doi:10.3920/bm2012.0066 · Cited by 100 · see citing works
“In addition, a prolonged transit time in the colon and an abnormal intestinal flora are frequently observed in patients undergoing haemodialysis (Hida et al., 1996; Wu et al., 2004), who have high levels of phenols in their urine and blood.”
BackgroundP-cresol, a uremic retention solute, alters the endothelial barrier function in vitro
Dou, L., Anfosso, F. J., Sabatier, F., Moal, V., Glorieux, G., Smet, R. D., Vanholder, R., Dignat‐George, F., Sampol, J., Berland, Y., et al. (2004) · Thrombosis and Haemostasis · doi:10.1160/th03-07-0491 · Cited by 99 · see citing works
“High level of p-cresol in CRF results from an overgrowth of intestinal bacteria responsible for p-cresol overproduction (17), and also from a reduced clearance.”
BackgroundMicrobiota metabolites: Pivotal players of cardiovascular damage in chronic kidney disease
Cosola, C., Rocchetti, M. T., Cupisti, A., & Gesualdo, L. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.03.003 · Cited by 99 · see citing works
The Immunomodulatory Effect of the Gut Microbiota in Kidney Disease
Chi, M., Ma, K., Wang, J., Ding, Z., Li, Y., Zhu, S., Liang, X., Zhang, Q., Song, L., & Liu, C. (2021) · Journal of Immunology Research · doi:10.1155/2021/5516035 · Cited by 98 · see citing works
Probiotics can treat hepatic encephalopathy
Solga, S. F. (2003) · Medical Hypotheses · doi:10.1016/s0306-9877(03)00192-0 · Cited by 96 · see citing works
Gut-Derived Metabolites and Their Role in Immune Dysfunction in Chronic Kidney Disease
Glorieux, G., Gryp, T., & Perna, A. F. (2020) · Toxins · doi:10.3390/toxins12040245 · Cited by 95 · see citing works
“This was initially observed in culture-based approaches observing increased counts of aerobes and decreased counts of anaerobes in fecal samples [17] and increased counts of aerobes and anaerobes in the small intestines of non-dialyzed and dialyzed patients with end-stage kidney disease (ESKD) compared to controls [18…”
BackgroundMosterd, C. M., Kanbay, M., van den Born, B. H., van Raalte, D. H., & Rampanelli, E. (2021) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2021.101484 · Cited by 94 · see citing works
In Vitro and In Vivo Assessment of Intraintestinal Bacteriotherapy in Chronic Kidney Disease
Ranganathan, N., Patel, B. G., Ranganathan, P., et al. (2006) · ASAIO Journal · doi:10.1097/01.mat.0000191345.45735.00 · Cited by 90 · see citing works
Future Avenues to Decrease Uremic Toxin Concentration
Vanholder, R. C., Eloot, S., & Glorieux, G. (2015) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2015.08.029 · Cited by 87 · see citing works
Gut microbiome in chronic kidney disease
Wing, M. R., Patel, S. S., Ramezani, A., & Raj, D. S. (2015) · Experimental Physiology · doi:10.1113/ep085283 · Cited by 89 · see citing works
Snelson, M., Kellow, N. J., & Coughlan, M. T. (2018) · Advances in Nutrition · doi:10.1093/advances/nmy068 · Cited by 87 · see citing works
“Early studies in hemodialysis patients showed lower viable counts of beneficial bacterial genera such as Bifidobacteria, and greater viable counts of Clostridium perfringens and aerobic bacteria including Enterobacteriaceae and Enterococci species compared with control subjects (12).”
BackgroundGut microbiota, hypertension and chronic kidney disease: Recent advances
Sircana, A., Michieli, F. D., Parente, R., Framarin, L., Leone, N., Berrutti, M., Paschetta, E., Bongiovanni, D., & Musso, G. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.01.013 · Cited by 86 · see citing works
Reviews: Uremic Toxins: A New Focus on an Old Subject
Yavuz, A. H., Tetta, C., ERSOY, F. F., et al. (2005) · Seminars in Dialysis · doi:10.1111/j.1525-139x.2005.18313.x · Cited by 86 · see citing works
“4 mg/dl by 9 months, and remained stable thereafter (65).”
BackgroundCalaf, R., Cérini, C., Genovesio, C., Verhaeghe, P., Jourde‐Chiche, N., Bergé‐Lefranc, D., Gondouin, B., Dou, L., Morange, S., Argilés, À., et al. (2011) · Journal of Chromatography B · doi:10.1016/j.jchromb.2011.06.014 · Cited by 85 · see citing works
Probiotic Amelioration of Azotemia in 5/6th Nephrectomized Sprague-Dawley Rats
Ranganathan, N., Patel, B. G., Ranganathan, P., Marczely, J., Dheer, R., Chordia, T., Dunn, S., & Friedman, E. A. (2005) · The Scientific World JOURNAL · doi:10.1100/tsw.2005.86 · Cited by 81 · see citing works
“In recent years, efforts have been undertaken to mitigate uremia in animals and humans by administration of live cultures of naturally existing[9] or genetically engineered microbes[10,18].”
BackgroundKoppe, L., Fouque, D., & Soulage, C. (2018) · Toxins · doi:10.3390/toxins10040155 · Cited by 83 · see citing works
“In hemodialysis patients, several studies have reported a sharp reduction in fecal p-cresol production while plasma p-cresol only slightly decreased [58].”
BackgroundThe microbiome in chronic kidney disease patients undergoing hemodialysis and peritoneal dialysis
Simões‐Silva, L., Araújo, R., Pestana, M., Soares‐Silva, I., & Sampaio‐Maia, B. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.02.011 · Cited by 83 · see citing works
Carnagarin, R., Matthews, V. B., Zaldivia, M. T. K., Peter, K., & Schlaich, M. P. (2018) · British Journal of Pharmacology · doi:10.1111/bph.14481 · Cited by 82 · see citing works
“Similarly, Ang II receptor knockout in the subfornical organ of the brain ameliorates the BP in DOCA-salt hypertension (Hilzendeger et al., 2013).”
BackgroundVitetta, L., & Gobe, G. C. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201200714 · Cited by 82 · see citing works
“a) Measured using the Modification of Diet in Renal Disease formula [16].”
BackgroundMethodArtificial Cell Therapy: New Strategies for the Therapeutic Delivery of Live Bacteria
Prakash, S., & Jones, M. L. (2005) · BioMed Research International · doi:10.1155/jbb.2005.44 · Cited by 82 · see citing works
Gut microbiota and inflammation in chronic kidney disease patients
Mafra, D., & Fouque, D. P. (2015) · Clinical Kidney Journal · doi:10.1093/ckj/sfv026 · Cited by 81 · see citing works
Microbiota issue in CKD: how promising are gut-targeted approaches?
Cosola, C., Rocchetti, M. T., Sabatino, A., Fiaccadori, E., Iorio, B. R. D., & Gesualdo, L. (2018) · Journal of Nephrology · doi:10.1007/s40620-018-0516-0 · Cited by 78 · see citing works
Impact of Gut Dysbiosis on Neurohormonal Pathways in Chronic Kidney Disease
Jazani, N. H., Savoj, J., Lustgarten, M. S., Lau, W. L., & Vaziri, N. D. (2019) · Diseases · doi:10.3390/diseases7010021 · Cited by 82 · see citing works
Summers, S., Quimby, J. M., Isaiah, A., Suchodolski, J. S., Lunghofer, P. J., & Gustafson, D. L. (2018) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.15389 · Cited by 80 · see citing works
The Colon: An Overlooked Site for Therapeutics in Dialysis Patients
Poesen, R., Meijers, B. K. I., & Evenepoel, P. (2013) · Seminars in Dialysis · doi:10.1111/sdi.12082 · Cited by 79 · see citing works
“(128) Indoxyl sulfate p-Cresol 20 Lactic acid bacilli (Lebenin) 30% serum indoxyl sulfate No change serum p-cresol Campieri et al.”
BackgroundSato, E., Saigusa, D., Mishima, E., Uchida, T., Miura, D., Morikawa, T., Kisu, K., Sekimoto, A., Saito, R., Oe, Y., et al. (2017) · Toxins · doi:10.3390/toxins10010019 · Cited by 79 · see citing works
“The present findings are consistent with those of clinical studies reporting that prebiotics and probiotics were more effective at reducing PCS levels than IS levels [38,39].”
ResultThe gut–kidney–heart axis in chronic kidney disease
Sumida, K., & Kovesdy, C. P. (2019) · Physiology International · doi:10.1556/2060.106.2019.19 · Cited by 79 · see citing works
Uremic Toxins Affect Erythropoiesis during the Course of Chronic Kidney Disease: A Review
Hamza, E., Metzinger, L., & Meuth, V. M. (2020) · Cells · doi:10.3390/cells9092039 · Cited by 77 · see citing works
“7 251 108 [34,35] Middle molecule β-2 microglobulin (mg/L) <2.”
Barnes, K. J., Rowland, A., Polasek, T. M., et al. (2014) · European Journal of Clinical Pharmacology · doi:10.1007/s00228-014-1709-7 · Cited by 76 · see citing works
Indoxyl sulphate and kidney disease: Causes, consequences and interventions
Ellis, R. J., Small, D. M., Vesey, D. A., Johnson, D. W., Francis, R. S., Vitetta, L., Gobe, G. C., & Morais, C. (2015) · Nephrology · doi:10.1111/nep.12580 · Cited by 75 · see citing works
“It is yet to be elucidated whether OATs influence albumin-bound IS.”
BackgroundInfluentialIndoxyl sulfate, a valuable biomarker in chronic kidney disease and dialysis
Tan, X. L., Cao, X., Zou, J., Shen, B., Zhang, X., Liu, Z., Lv, W., Teng, J., & Ding, X. (2016) · Hemodialysis International · doi:10.1111/hdi.12483 · Cited by 73 · see citing works
Intestinal-Renal Syndrome: Mirage or Reality?
Ritz, E. (2011) · Blood Purification · doi:10.1159/000321848 · Cited by 74 · see citing works
“One approach to reduce the cumulation of the above putrefactive metabolites in feces and plasma in uremic patients consisted of administering antibiotic-resistant lactic acid bacteria, which caused a significant decrease in the fecal and plasma concentrations of indican [”
BackgroundZeng, Y., Dai, Z., Lu, F., Lu, Z., Liu, X., Cha, C., Qu, P., Li, D., Hua, Z., Qu, Y.-N., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.8160 · Cited by 73 · see citing works
“Like studies by Hide et al [36], the total number of bacteria in our study exhibited no any significant difference between each group, while the number of C.”
ResultGut microbiota composition and frailty in elderly patients with Chronic Kidney Disease
Margiotta, E., Miragoli, F., Callegari, M. L., Vettoretti, S., Caldiroli, L., Meneghini, M., Zanoni, F., & Messa, P. (2020) · PLoS ONE · doi:10.1371/journal.pone.0228530 · Cited by 71 · see citing works
The Association between Gut Microbiota and Uremia of Chronic Kidney Disease
Kim, J. E., Kim, H.-E., Park, J. I., Cho, H., Kwak, M., Kim, B.-Y., Yang, S. H., Lee, J. P., Kim, D., Joo, K., et al. (2020) · Microorganisms · doi:10.3390/microorganisms8060907 · Cited by 60 · see citing works
“observed elevated contents of several gut bacteria in patients on hemodialysis compared to healthy controls [31].”
BackgroundResultGastrointestinal Microbiota in Patients with Chronic Kidney Disease: A Systematic Review
Chung, S.-Y., Barnes, J. L., & Astroth, K. S. (2019) · Advances in Nutrition · doi:10.1093/advances/nmz028 · Cited by 69 · see citing works
Evenepoel, P., Bammens, B., Verbeke, K., & Vanrenterghem, Y. F. C. (2006) · Kidney International · doi:10.1038/sj.ki.5001523 · Cited by 69 · see citing works
Short-chain Fatty Acids: A Link Between Prebiotics And Microbiota In Chronic Kidney Disease
Esgalhado, M., Kemp, J. A., Damasceno, N. R. T., Fouque, D. P., & Mafra, D. (2017) · Future Microbiology · doi:10.2217/fmb-2017-0059 · Cited by 71 · see citing works
Gut microbiota in chronic kidney disease
Cigarrán, S., Parra, E. G., & Cases, A. (2017) · Nefrología (English Edition) · doi:10.1016/j.nefroe.2017.01.017 · Cited by 69 · see citing works
Tian, N., Li, L., Ng, J. K., & Li, P. K. (2022) · Nutrients · doi:10.3390/nu14194044 · Cited by 65 · see citing works
“Early studies have shown a distinct reduction in fecal p-cresol while plasma p-cresol was only slightly decreased in the hemodialysis population [53].”
BackgroundRaizada, M. K., Joe, B., Bryan, N. S., Chang, E. B., Dewhirst, F. E., Borisy, G. G., Galis, Z. S., Henderson, W. A., José, P. A., Ketchum, C. J., et al. (2017) · Hypertension · doi:10.1161/hypertensionaha.117.09699 · Cited by 65 · see citing works
“The number of aerobic bacteria such as Enterobacteria and Enterococci was found to be ≈100 times higher in patients on maintenance hemodialysis than in controls.(39) Among anaerobic bacteria, hemodialysis patients had lower counts for Bifidobacteria and higher counts for Clostridium perfringens.”
BackgroundThe Kidney–Gut Axis: Implications for Nutrition Care
Rossi, M., Johnson, D. W., & Campbell, K. L. (2015) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2015.01.017 · Cited by 66 · see citing works
- Authors
- Hida, M., Aiba, Y., Sawamura, S., Suzuki, N., Satoh, T., & Koga, Y.
- Affiliations
- Tokai University (JP)
- Wakamoto Pharmaceutical (Japan) (JP)
- Kidney Centre (PK)
- ORCID
- Koga, Yasuhiro
- Venue
- Nephron
- Publisher
- S. Karger AG
- Published
- 2008-12-24
- Volume
- 74
- Issue
- 2
- Pages
- 349-355
- ISSN
- 1660-8151 (ISSN-L)
- 2235-3186
- OpenAlex
- W2075674899
- Cited by
- 295
- References
- 0
- Citations by year
- 2026: 4 · 2025: 13 · 2024: 9 · 2023: 15 · 2022: 19 · 2021: 14 · 2020: 20 · 2019: 21 · 2018: 24 · 2017: 18 · 2016: 16 · 2015: 21 · 2014: 12 · 2013: 15 · 2012: 5
- FWCI
- 5.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Nephron journals/Nephron journals (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Nephrology › Dialysis and Renal Disease Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- lactic acid bacteria, uremic toxins, hemodialysis, indican, p-cresol, phenols, gut microbiota, oral administration, uremic patients
- MeSH terms
- Administration, Oral, Adult, Bacteria, Aerobic, Bacteria, Anaerobic, Bifidobacterium, Capsules, Cresols, Feces, Female, Renal Dialysis, Humans, Indican, Lactobacillus acidophilus, Male, Middle Aged, Phenols, Enterococcus faecalis, Uremia, Phenol
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