Gut microbiota in chronic kidney disease

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The tissue kallikrein produced by the connecting tubule is released into the urinary fluid. It is there that it acts on the filtered or locally secreted kininogen (KN) and finally produces bradykinin (BK). BK acts on its B2 receptor (BKRB2), activating the phospholipase C/diacylglycerol/protein kinase C (PLC/DAG/PKC) pathway by inducing the TRPV5 calcium channel localisation at the apical membrane level and favours the reabsorption of tubular calcium. 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More than 100 trillion germs (1014) cohabit with us throughout our lives, representing 10 times the number of cells that make up our body and constituting 1.5–2kg of our weight.<a class="elsevierStyleCrossRefs" href="#bib0570">1,2</a> The concentration of germs in the digestive tract gradually increases from the stomach to the colon, where they reach the highest concentration (up to 1011 microorganisms/g of faeces) and diversity. The gut microbiota plays an important role in metabolic, nutritional, physiological, and immunological processes, and constitutes a true ecosystem.<a class="elsevierStyleCrossRef" href="#bib0580">3</a> The human microbiome is our second genome, which has more than 3 million genes (100 times more genes than the human genome itself) and is the subject of research by the Human Microbiome Project Consortium.<a class="elsevierStyleCrossRefs" href="#bib0585">4–6</a>Originally, the gut microbiota is formed through the placenta, where low levels of non-pathogenic germs, especially the phyla firmicutes, bacteroidetes, and Fusobacteria are nested. In the first years of life, feeding, type of birth, hygiene, and use of antibiotics condition the formation of the intestinal microbiome.<a class="elsevierStyleCrossRefs" href="#bib0600">7,8</a> Different species of germs colonise and are originated during various events (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>The gut microbiota is established in the first 2–3 years of life as a dynamic ecosystem, dominated by bifidobacteria; their composition increases in richness and diversity until reaching their maximum complexity in adulthood, when the dominant species are bacteroidetes, firmicutes and actinobacteria.<a class="elsevierStyleCrossRefs" href="#bib0610">9–11</a>Bacterial communities that lie in the intestine are, therefore, a combination of different types and amounts of bacteria and 3 different groups of microbiota or enterotypes have been identified in humans.<a class="elsevierStyleCrossRef" href="#bib0625">12</a> The phylogenetic composition of intestinal microflora tends to be similar between individuals from the same region, from the same family and also with a similar diet which plays a significant role in their composition.<a class="elsevierStyleCrossRefs" href="#bib0630">13,14</a>Dietary habits affect the composition of the gut microbiota. Since the microbiota is in contact with a significant number of neural cells and immunological cells, it directs the maturation of the immune system in childhood and contributes to the maintenance of its homeostasis during life.<a class="elsevierStyleCrossRef" href="#bib0575">2</a> Complex polysaccharides, which are not digested by enzymes in the small intestine, are metabolised by the colon microflora. These polysaccharides are degraded and fermented in the large intestine and converted into short chain fatty acids (SCFAs) and gases (CO2 and H2). A high intestinal content of fructose promotes the formation of butyrate which is produced by bacteria. Dietary supplementation with specific polysaccharides may promote the growth of “healthy” germs (Bifidobacterium, Lactobacillus), the production of SCFA and it may decrease intestinal pH that inhibits the growth of pathogenic bacteria.<a class="elsevierStyleCrossRefs" href="#bib0640">15,16</a>In the ageing process, progressive damage occurs to the morphology and function of the different systems and the microbiota becomes less diverse and more dynamic, characterised by the predominance of bacteroidetes over firmicutes, with an increase of Protobacteria spp. and a decrease of Bifidobacterium. This is evidenced by rRNA techniques and it has been analysed as part of the study ELDERMET.<a class="elsevierStyleCrossRefs" href="#bib0650">17–19</a> Major changes in the microbiota are found in the colon of persons over 60 years of age. The significance of these changes is yet to be clarified.<a class="elsevierStyleCrossRef" href="#bib0665">20</a>Faecal bacteria such as Escherichia coli, which divides every 20min, are genetically prepared to be highly adaptative, and always survive even though their host ages. Without this plasticity, we probably would not have been able to cope with changes in lifestyle and dietary habits, as evidenced by the transition from the Palaeolithic to the dietary habits of Western societies.<a class="elsevierStyleCrossRef" href="#bib0670">21</a>Functionally, the gut microbiota provides nutrients and energy to the body through fermentation of nondigestible foods in the large intestine. The most important fermentation products deriving from the fermentation are the SCFA, which serve as a source of energy to intestinal cells and bacteria, and contribute to energy expenditure, satiety, and glucose homeostasis.<a class="elsevierStyleCrossRef" href="#bib0675">22</a> Other relevant functions of the gut microbiota are the endogenous synthesis of certain vitamins and amino acids, the metabolism of bile acids, or the maintenance of the integrity of intestinal barriers, which protect the host from pathogenic germs.Thus, the gut microbiota is involved in the maturation of the immune system in infancy and contributes to the maintenance of its homeostasis throughout life.<a class="elsevierStyleCrossRef" href="#bib0680">23</a>Gut microbiota in chronic kidney diseaseFrom the early stages of chronic kidney disease (CKD) there is a quantitative and qualitative alteration of intestinal microflora (dysbiosis); so the composition and metabolic activities of microflora are changed in CKD and this is a hot and innovative topic in nephrology literature. These alterations include changes in intestinal transit, decreased protein absorption, decrease in dietary fibre intake, treatment with oral iron and frequent use of antibiotics.All of this contributes to systemic inflammation and the accumulation of uraemic toxins that are absorbed by intestine and eliminated by the kidney. Inflammation and uraemic toxins play a central role in the pathophysiology of atherosclerosis, as well as in other complications associated with CKD<a class="elsevierStyleCrossRefs" href="#bib0685">24–27</a>; that will be reviewed below.Patients with CKD are polymedicated. Some drugs frequently prescribed to these patients may alter intestinal microflora, especially antibiotics,<a class="elsevierStyleCrossRefs" href="#bib0705">28,29</a> but others may also slow intestinal transit, phosphorus binders, ion exchange resins,<a class="elsevierStyleCrossRef" href="#bib0715">30</a> or iron supplements that may have an effect on microflora but it is not well defined.<a class="elsevierStyleCrossRefs" href="#bib0720">31,32</a>Change in intestinal barriers in chronic kidney diseaseChanges in intestinal barriers with an increased intestinal permeability is common in CKD (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>).<elsevierMultimedia ident="tbl0010"></elsevierMultimedia>Increasing urea levels and expanding bacteria with urease causes an increase ammonium production in the intestinal lumen and induce changes in intestinal pH that produces an alteration of intestinal permeability by affecting the tight junctions of the enterocyte. Vaziri et al. have demonstrated a marked reduction of tight junction proteins, claudin-1, occludin, and ZO1, in the colonic mucosa in CKD; this is associated with an infiltration of mononuclear leukocytes in the lamina propria and a marked thickening of the colon wall.<a class="elsevierStyleCrossRef" href="#bib0730">33</a> There is histological evidence of chronic inflammation of the intestinal tract including oesophagitis, gastritis, etc.<a class="elsevierStyleCrossRefs" href="#bib0730">33,34</a>The presence of frequent oedema and hypervolaemia in CKD may aggravate intestinal barrier dysfunction in CKD patients on, haemodialysis, or peritoneal dialysis. In addition, excessive ultrafiltration and episodes of hypotension during haemodialysis may cause episodes of transient intestinal ischaemia which increases the permeability of the intestinal barrier facilitating the passage of endotoxins.<a class="elsevierStyleCrossRef" href="#bib0730">33</a>In renal transplant patients, the investigation of the gut microbiota is in its infancy. It is known that inflammatory processes, such as graft ischaemia time, baseline disease and immunosuppressive drugs may play a relevant role in the alteration of the intestinal barrier.<a class="elsevierStyleCrossRefs" href="#bib0740">35,36</a>Intestinal microflora as a cause of inflammation in chronic kidney diseaseIn CKD, the decreased clearance of proinflammatory cytokines, is associated with the development of oxidative stress and inflammation. The later are contributing factors to the progression of the disease and its complications, including cardiovascular disease, cachexia, and anaemia. Oxidative stress and chronic inflammation stimulate the NF-κB transcription factor, which is the key regulator of proinflammatory cytokines and chemokines. Increased permeability of intestinal barriers in CKD patients favours the translocation of bacterial products of intestinal origin, as evidenced by the presence of DNA fragments of circulating intestinal pathogens (aerobic and anaerobic), both in patients in different stages of CKD and on renal replacement therapy.<a class="elsevierStyleCrossRefs" href="#bib0750">37–39</a> The increase in circulating bacterial products of intestinal origin activates innate immunity, promotes the inflammatory state associated with CKD and, increases the incidence of cardiovascular disease and mortality.<a class="elsevierStyleCrossRefs" href="#bib0765">40–42</a>Microbiota and uraemic toxins derived from the intestine in chronic kidney diseaseIntestinal production of uraemic toxinsThe origin of uraemic toxins in CKD is multiple. The importance of toxins generated by intestinal microbial metabolism<a class="elsevierStyleCrossRef" href="#bib0780">43</a> is increasingly recognised. Approximately 10g of proteins reach the colon daily, where they are degraded by intestinal bacteria to metabolites such as ammonium, amines, thiols, phenols and indoles. These colon fermentation products are eliminated through faeces, although a portion is absorbed and eliminated by the kidney, so these are accumulated in CKD.<a class="elsevierStyleCrossRef" href="#bib0785">44</a> In CKD, the uraemic toxins derived from intestinal microflora are:Phenols and indoles: p-cresol and indoxyl sulfate. Phenols include p-cresol, p-cresyl sulfate (PCS), p-cresyl glucuronide, phenylacetic acid, phenyl sulfate and phenol.<a class="elsevierStyleCrossRef" href="#bib0790">45</a><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">-p-Cresol/p-cresyl sulfate: products of phenylalanine and tyrosine metabolism of intestinal anaerobic bacteria. p-Cresol is conjugated in the intestinal wall to PCS and p-cresyl glucuronide in the liver. PCS is the main circulating metabolite of p-cresol.<a class="elsevierStyleCrossRef" href="#bib0795">46</a></li><li class="elsevierStyleListItem" id="lsti0010">-Phenol: mainly derives from ingestion, from the catabolism of tyrosine by intestinal bacteria, as well as from tobacco consumption.</li><li class="elsevierStyleListItem" id="lsti0015">-Phenylacetic acid: is the result of the degradation of phenylalanine.</li></ul>Among the indoles are indoxyl sulfate (IS) and indoleacetic acid.<a class="elsevierStyleCrossRef" href="#bib0790">45</a> Both originate from the degradation of tryptophan by intestinal bacteria and are subsequently sulfated in the liver into IS. Indoles and phenols are uraemic toxins bound to proteins.<a class="elsevierStyleCrossRef" href="#bib0800">47</a>Amines and polyamines: amines and polyamines are generated from intestinal microbial metabolism. An amino acid that is clinically relevant and of growing interest is trimethylamine N-oxide (TMAO). TMAO is produced by the intestinal metabolism of quaternary amines, such as choline/phosphatidylcholine, betaine, or l-carnitine. l-Carnitine, which is present in red meat, also induces the formation of TMAO and it is associated with an increase in cardiovascular disease.<a class="elsevierStyleCrossRef" href="#bib0805">48</a> Dietary sources of TMAO are red meats, meats in general, egg yolks, liver, dairy products and saltwater fish. In CKD, TMAO accumulates and its levels depends on the glomerular filtration, but its binding to proteins is low, and it is well eliminated with dialysis.Polyamines are organic cations including cadaverine, spermine, spermidine and putrescine. They come from the decarboxylation of l-arginine, l-ornithine or lysine in the intestine. In CKD patients, putrescine, spermidine, and spermine are increased in serum.<a class="elsevierStyleCrossRef" href="#bib0810">49</a> These molecules have been shown to interact with insulin and lipoproteins, and contribute to the acceleration of atherosclerosis along with other factors such as hypertriglyceridemia.<a class="elsevierStyleCrossRef" href="#bib0815">50</a>Biological and clinical consequences of the accumulation of uraemic toxinsThe aforementioned uraemic toxins have been associated with deleterious biological effects in different tissues and cell lines<a class="elsevierStyleCrossRefs" href="#bib0820">51,52</a> (<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>), and with an increased risk of the progression of CKD, morbidity and mortality.<ul class="elsevierStyleList" id="lis0010"><li class="elsevierStyleListItem" id="lsti0020">a)Progression of CKD: both IS and PCS are associated to the development of fibrosis, deterioration of renal function and disease progression.<a class="elsevierStyleCrossRefs" href="#bib0825">52,53</a> In vitro studies have shown a deleterious effects of these molecules on renal tubular cells.<a class="elsevierStyleCrossRef" href="#bib0835">54</a> In a prospective study in patients with stage 1–5 CKD, the predictive role of both molecules in disease progression was confirmed.<a class="elsevierStyleCrossRef" href="#bib0840">55</a> In experimental animals, a diet rich in choline or TMAO preduces progressive tubulointerstitial fibrosis and renal dysfunction.<a class="elsevierStyleCrossRef" href="#bib0845">56</a></li><li class="elsevierStyleListItem" id="lsti0025">b)Cardiovascular complications: in CKD patients, IS is associated with endothelial damage, arterial stiffness and aortic calcification<a class="elsevierStyleCrossRef" href="#bib0850">57</a>; and, in hemodialysis patients it is associated with atherosclerosis<a class="elsevierStyleCrossRef" href="#bib0855">58</a> and endothelial dysfunction,<a class="elsevierStyleCrossRef" href="#bib0860">59</a> it has a cardiac profibrotic effect, favours hypertrophy of myocardiocytes<a class="elsevierStyleCrossRef" href="#bib0865">60</a> and it is a predisposing factor of atrial fibrillation.<a class="elsevierStyleCrossRef" href="#bib0870">61</a> Similar vascular effects have been described with,<a class="elsevierStyleCrossRef" href="#bib0875">62</a> which is a predictor of cardiovascular risk in CKD patients.<a class="elsevierStyleCrossRefs" href="#bib0880">63,64</a> In hemodialysis patients PCS and IS have been associated with peripheral vascular disease and thrombosis of vascular access.<a class="elsevierStyleCrossRef" href="#bib0890">65</a> A recent meta-analysis confirms the relationship of these molecules to cardiovascular risk in CKD.<a class="elsevierStyleCrossRef" href="#bib0895">66</a>Likewise, indoleacetic acid is associated with oxidative stress and inflammation markers, and it is a predictor of mortality and cardiovascular events in CKD.<a class="elsevierStyleCrossRef" href="#bib0900">67</a>Elevated levels of TMAO predicts coronary atherosclerotic burden<a class="elsevierStyleCrossRef" href="#bib0845">56</a> and mortality in patients with CKD,<a class="elsevierStyleCrossRefs" href="#bib0905">68,69</a> although this is not shown in all reports.<a class="elsevierStyleCrossRef" href="#bib0915">70</a></li><li class="elsevierStyleListItem" id="lsti0030">c)Anaemia: IS has been associated with anaemia of the renal patient; it interfere with the adequate production of erythropoietin<a class="elsevierStyleCrossRefs" href="#bib0920">71,72</a> and increased eryptosis (programmed cell death of red blood cells).<a class="elsevierStyleCrossRef" href="#bib0930">73</a> Polyamines are associated to anaemia in renal patients, through an intra-erythrocytic effect,<a class="elsevierStyleCrossRef" href="#bib0935">74</a> reduces erythropoiesis, and inhibit the activity of erythropoietin.</li><li class="elsevierStyleListItem" id="lsti0035">d)Alterations of bone-mineral metabolism: IS reduces bone formation by promoting oxidative stress in osteoblasts and inducing resistance to PTH, which favours the development adynamic bone.<a class="elsevierStyleCrossRef" href="#bib0940">75</a> There is a positive correlation between FGF-23 and IS serum levels, suggesting an association between this molecule and metabolic bone disease in uraemic patients.<a class="elsevierStyleCrossRef" href="#bib0945">76</a> Likewise, less bone remodelling has been observed in uraemic rats with higher IS after a parathyroidectomy.<a class="elsevierStyleCrossRef" href="#bib0950">77</a></li><li class="elsevierStyleListItem" id="lsti0040">e)Insulin resistance: In CKD patients the catabolism of insulin is reduced and often, they also have insulin resistance, which is associated with an increased risk of mortality; it seems that insulin resistance is related to some of the uraemic toxins.<a class="elsevierStyleCrossRef" href="#bib0955">78</a></li></ul><elsevierMultimedia ident="tbl0015"></elsevierMultimedia>Prevention and treatment of dysbiosisIn recent years there is a growing interest in restoring the symbiosis of intestinal microflora in CKD aiming to reduce the generation of uraemic toxins, oxidative stress, and inflammation.<a class="elsevierStyleCrossRef" href="#bib0960">79</a><ul class="elsevierStyleList" id="lis0015"><li class="elsevierStyleListItem" id="lsti0045">a)High fibre diet: a high fibre diet increases the production of SCFA, which provides energy to the intestinal flora and allows amino acids that reach the colon to be incorporated into bacterial proteins and be excreted instead of being fermented into uraemic solutes. In addition, SCFAs are used as substrate by the intestinal mucosa helping to maintain their functionality and integrity. Fibre increases intestinal transit reducing the time for fermentation of amino acids and improves the composition of microflora which reduces the production of undesirable solutes. In CKD patients, there is a direct relationship between dietary protein/fibre ratio and PCS and IS levels, so a diet with a low protein/fibre ratio should be beneficial.<a class="elsevierStyleCrossRef" href="#bib0965">80</a> In healthy subjects, a vegetarian diet, as compared with the omnivore diet, reduces the generation IS or PCS; this effect was related to the higher fibre and lower protein content of the vegetarian diet.<a class="elsevierStyleCrossRef" href="#bib0970">81</a> A very low protein diet (0.3g/kg body weight/day) supplemented with amino acid keto-analogues also reduces IS levels in patients with CKD.<a class="elsevierStyleCrossRef" href="#bib0975">82</a>Several therapeutic interventions have recently explored to improve the dysbiosis of the intestinal microflora, reduce the absorption of uraemic toxins and the passage of endotoxins from the intestinal lumen.</li><li class="elsevierStyleListItem" id="lsti0050">b)Prebiotics, probiotics, and symbiotics: the generation of uraemic toxins could be reduced by selectively increasing saccharolyticbacteria (which digest dietary fibre) and decreasing proteolytic bacteria (protein and amino acid fermenters) in the colon. The main regulator of metabolism of colon bacteria is the availability of nutrients and specifically the rate of fermentable carbohydrates vs. nitrogen.Prebiotics are non-digestible food components which, through selective fermentation, allow for specific changes in the composition or activity in gastrointestinal microflora, which are beneficial to the health and well-being of the host. Prebiotics stimulate the growth or activity of one or a limited number of bacteria in the colon; they may increase carbohydrate fermentables vs. nitrogen; they include inulin, fructooligosaccharides, galactooligosaccharides, etc. Inulin enriched with oligofructose reduces the generation of PCS and the serum concentrations in hemodialysis patients, but has no effect on IS.<a class="elsevierStyleCrossRef" href="#bib0980">83</a> Resistant starch reduces IS levels in hemodialysis patients and reduces PCS but not significantly.<a class="elsevierStyleCrossRef" href="#bib0985">84</a> In a CKD rat model, a diet rich in resistant starch delayed the progression of CKD and attenuated oxidative stress and inflammation.<a class="elsevierStyleCrossRef" href="#bib0990">85</a> Currently, a randomised, crossover, double-blind, phase 2 clinical trial in patients with stage 3b-4 CKD is examining the effect of the supplementation of arabinoxylan-oligosaccharides on plasma levels of PCS and indole derivatives urinary excretion of these compounds and insulin resistance are also examined.<a class="elsevierStyleCrossRef" href="#bib0995">86</a>Probiotics are defined as “living micro-organisms” that, being administered in adequate amounts, provide a health benefit to the host. A recent review evaluates the potential benefits of probiotics in general and especially in CKD.<a class="elsevierStyleCrossRef" href="#bib1000">87</a> The efficacy of probiotics to decrease levels of uraemic toxins and to delay the progression of CKD has been investigated in in vitro models, animal models and in patients with CKD. However, to date, there are no large-scale quality intervention studies and studies on clinical events to support their widespread use. There are only small studies, most of which,<a class="elsevierStyleCrossRefs" href="#bib1005">88,92–95</a> but not all,<a class="elsevierStyleCrossRef" href="#bib1050">97</a> observe a decrease in uraemic toxin levels. Administration of Bifidobacterium longum in enteric capsules to patients with CKD had minimal effects on the progression of the disease in patients with CKD.<a class="elsevierStyleCrossRef" href="#bib1020">91</a> However, a randomised, double-blind trial in patients on peritoneal dialysis observed a significant reduction in serum proinflammatory endotoxin and cytokine levels, an increase in serum IL-10 levels, and the preservation of residual renal function after 6 months of treatment with a probiotic<a class="elsevierStyleCrossRef" href="#bib1045">96</a> (<a class="elsevierStyleCrossRef" href="#tbl0020">Table 4</a>).<elsevierMultimedia ident="tbl0020"></elsevierMultimedia>Symbiotics are probiotic supplements combined with prebiotics. In hemodialysis patients, on treatment with a symbiotic there is a decrease in the level of PCS, but not those of IS,<a class="elsevierStyleCrossRef" href="#bib1055">98</a> which was confirmed in another study.<a class="elsevierStyleCrossRef" href="#bib1075">102</a> Another study observed a delay in the progression of CKD with symbiotic treatment,<a class="elsevierStyleCrossRef" href="#bib1065">100</a> while another study did not observe a significant improvement in inflammation markers.<a class="elsevierStyleCrossRef" href="#bib1080">103</a> Finally, a randomised, double-blind, crossover study in patients with CKD<a class="elsevierStyleCrossRef" href="#bib1085">104</a> demonstrated a reduction in PCS levels, a non-significant decrease in IS and an increase in bifidobacteria and reduction of faecal ruminococcus, but no change in inflammation markers, oxidative stress, or endotoxins, although a slight increase in albuminuria was observed (<a class="elsevierStyleCrossRef" href="#tbl0025">Table 5</a>).<elsevierMultimedia ident="tbl0025"></elsevierMultimedia>One of the major limitations of probiotic or symbiotic therapy is that no study has yet demonstrated the sustained survival of probiotics in the dysbiotic colon of patients with CKD. There are also no studies that have evaluated the effect of these treatments on the levels of TMAO in this population. In choosing probiotics, the contribution of urease-containing bacteria must be considered, since they may increase intestinal ammonia generation, which may damage epithelial tight junctions, and increase intestinal permeability to the passage of endotoxins from the intestinal lumen.<a class="elsevierStyleCrossRefs" href="#bib0730">33,34</a></li><li class="elsevierStyleListItem" id="lsti0055">c)Adsorptive therapies: the use of oral sorbents could decrease uraemic toxins and circulating intestinal endotoxins. AST-120 oral sorbents decrease IS levels in a dose-dependent manner.<a class="elsevierStyleCrossRef" href="#bib1090">105</a> In addition, a reduction in the IS, PCS, or phenyl sulfate and oxidative stress levels have been described in patients on haemodialysis.<a class="elsevierStyleCrossRef" href="#bib1095">106</a> Other authors have reported that the administration of AST-120 improves the erythropoietic response to CERA.<a class="elsevierStyleCrossRef" href="#bib1100">107</a> AST-120 improves intestinal barrier dysfunction and decreases endotoxin plasma levels, inflammation markers and oxidative stress in a CKD model in rats.<a class="elsevierStyleCrossRef" href="#bib1105">108</a></li></ul>Although small randomised, controlled studies in experimental animals and retrospective studies in patients have indicated a nephroprotective effect of AST-120 (reviewed by Schulman et al.<a class="elsevierStyleCrossRef" href="#bib1110">109</a>), a subsequent large randomised, controlled trial in patients with CKD was unable to confirm this.<a class="elsevierStyleCrossRef" href="#bib1110">109</a> The study had some methodological limitations, but also suggested the possibility that the objective of treating specific uraemic toxins may not be sufficient. However, another retrospective study of the long-term effects of AST-120 on patients with stage 3–5 CKD showed a reduction in the risk of progression to dialysis, mortality, cardiac events and vascular accident vs. those patients who did not receive it.<a class="elsevierStyleCrossRef" href="#bib1115">110</a>Although a beneficial effect of sevelamer on IS and PCS has been described in in vitro studies, in vivo studies in mice or patients have not demonstrated a reduction in the levels of these uraemic toxins.<a class="elsevierStyleCrossRef" href="#bib1120">111</a> However, sevelamer does reduce endotoxin levels and systemic inflammation in patients on haemodialysis.<a class="elsevierStyleCrossRefs" href="#bib1125">112,113</a>Key concepts<ul class="elsevierStyleList" id="lis0020"><li class="elsevierStyleListItem" id="lsti0060">1.In CKD, there is a dysbiosis of the intestinal microflora.</li><li class="elsevierStyleListItem" id="lsti0065">2.Intestinal microflora generate uraemic toxins that are absorbed and accumulate in CKD, and are associated with increased oxidative stress and inflammation.</li><li class="elsevierStyleListItem" id="lsti0070">3.In CKD, there is an increase in the permeability of the intestinal barrier that allows the passage into the systemic circulation of endotoxins and other bacterial products that aggravate the inflammatory state of CKD.</li><li class="elsevierStyleListItem" id="lsti0075">4.Changes in diet composition could improve microflora dysbiosis in CKD, reduce uraemic toxin levels, or restore intestinal mucosal permeability in CKD patients.</li><li class="elsevierStyleListItem" id="lsti0080">5.The use of probiotics, prebiotics or symbiotics opens an alternative in the treatment of intestinal dysbiosis associated with CKD, and may play a role in slowing the progression of CKD and in preventing relevant associated complications such as mortality and cardiovascular risk.</li></ul>Conflicts of interestThe authors have no conflicts of interest to declare." "textoCompletoSecciones" => array:1 [ "secciones" => array:9 [ 0 => array:3 [ "identificador" => "xres818668" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec815710" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres818667" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec815711" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "What are the microbiota and the microbiome?" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Gut microbiota in chronic kidney disease" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Change in intestinal barriers in chronic kidney disease" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Intestinal microflora as a cause of inflammation in chronic kidney disease" ] 2 => array:3 [ "identificador" => "sec0025" "titulo" => "Microbiota and uraemic toxins derived from the intestine in chronic kidney disease" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0030" "titulo" => "Intestinal production of uraemic toxins" ] 1 => array:2 [ "identificador" => "sec0035" "titulo" => "Biological and clinical consequences of the accumulation of uraemic toxins" ] ] ] 3 => array:2 [ "identificador" => "sec0040" "titulo" => "Prevention and treatment of dysbiosis" ] 4 => array:2 [ "identificador" => "sec0045" "titulo" => "Key concepts" ] ] ] 6 => array:2 [ "identificador" => "sec0050" "titulo" => "Conflicts of interest" ] 7 => array:2 [ "identificador" => "xack274713" "titulo" => "Acknowledgements" ] 8 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2016-03-08" "fechaAceptado" => "2016-05-10" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec815710" "palabras" => array:5 [ 0 => "Chronic kidney disease" 1 => "Gut microbiota" 2 => "Dysbiosis" 3 => "Uraemic toxins" 4 => "Inflammation" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec815711" "palabras" => array:5 [ 0 => "Enfermedad renal crónica" 1 => "Microbiota intestinal" 2 => "Disbiosis" 3 => "Toxinas urémicas" 4 => "Inflamación" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "The intestinal microflora maintains a symbiotic relationship with the host under normal conditions, but its imbalance has recently been associated with several diseases.In chronic kidney disease (CKD), dysbiotic intestinal microflora has been reported with an increase in pathogenic flora compared to symbiotic flora. An enhanced permeability of the intestinal barrier, allowing the passage of endotoxins and other bacterial products to the blood, has also been shown in CKD. By fermenting undigested products that reach the colon, the intestinal microflora produce indoles, phenols and amines, among others, that are absorbed by the host, accumulate in CKD and have harmful effects on the body. These gut-derived uraemic toxins and the increased permeability of the intestinal barrier in CKD have been associated with increased inflammation and oxidative stress and have been involved in various CKD-related complications, including cardiovascular disease, anaemia, mineral metabolism disorders or the progression of CKD. The use of prebiotics, probiotics or synbiotics, among other approaches, could improve the dysbiosis and/or the increased permeability of the intestinal barrier in CKD.This article describes the situation of the intestinal microflora in CKD, the alteration of the intestinal barrier and its clinical consequences, the harmful effects of intestinal flora-derived uraemic toxins, and possible therapeutic options to improve this dysbiosis and reduce CKD-related complications." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "La microflora intestinal mantiene una relación simbiótica con el huésped en condiciones normales, sin embargo, su alteración se ha asociado recientemente con numerosas enfermedades.En la enfermedad renal crónica (ERC) se ha descrito una disbiosis en la microflora intestinal con un aumento de la flora patógena sobre la simbionte. Además, la permeabilidad de la barrera intestinal está aumentada, lo que permite el paso de endotoxinas y otros productos bacterianos a la sangre. La microflora intestinal, mediante la fermentación de productos no digeridos que alcanzan el colon, produce indoles, fenoles, o aminas, entre otros, que son absorbidos por el huésped, se acumulan en la ERC y tienen efectos deletéreos sobre el organismo. Estas toxinas urémicas generadas en el intestino y el aumento de la permeabilidad de la barrera intestinal en la ERC se han asociado a un aumento de la inflamación y el estrés oxidativo, y están implicados en diversas complicaciones asociadas a la ERC, como la enfermedad cardiovascular, la anemia, las alteraciones del metabolismo mineral o la progresión de la ERC. El uso de prebióticos, probióticos o simbióticos, entre otras aproximaciones, podrían mejorar la disbiosis o el aumento de la permeabilidad de la barrera intestinal en la ERC.En este artículo se revisan la situación de la microflora intestinal en la ERC, la alteración de la barrera intestinal y sus consecuencias clínicas, los efectos deletéreos de las toxinas urémicas derivadas de la microflora intestinal, así como las posibles opciones terapéuticas para mejorar esta disbiosis y reducir las complicaciones de la ERC." ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "Please cite this article as: Guldris SC, Parra EG, Amenós AC. Microbiota intestinal en la enfermedad renal crónica. Nefrología. 2017;37:9–19." ] ] "multimedia" => array:5 [ 0 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Exposure \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Intestinal flora \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vaginal canal \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bifidobacterium, bacteroids, Lactobacillus, prevotella, enterococci, streptococci, Clostridiaeceae \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Post-caesarean delivery \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Staphylococcus, Corynebacterium Propionibacterium. Lower amount of Bifidobacterium and bacteroides \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Breast-feeding \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bifidobacterium, bacteroides, Lactobacillus, clostridia, actinobacteria and firmicutes \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Artificial breastfeeding \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bacteroides, clostridia, Enterobacteriaceae \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1376005.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Intestinal microflora in relation to perinatal events.<a class="elsevierStyleCrossRefs" href="#bib0585">4,5</a>" ] ] 1 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "CKD, chronic kidney disease; ACKD, advanced chronic kidney disease." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Intestinal tract \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Normal \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">CKD/ACKD \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Stomach \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">No change \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Helicobacter \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Duodenum \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Staphylococcus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Streptococcus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactococcus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Jejunum \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Enterococcus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Streptococcus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ileum \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Enterobacteriaceae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bacteroides \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Clostridium \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bacterial fragments \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Colon \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Firmicutes \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased: \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bacteroides \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Proteobacteria, \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Actinobacteria \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Enterobacteria, E. coli, \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Proteus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Acinetobacter, Proteus spp. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Clostridium Lactobacilli \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Decreased: \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Prevotellaceae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus, Bifidobacterium spp. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Fusobacterium \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Aerobic overgrowth of at least 100 times \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TM7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increase of Clostridium perfringens \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1376003.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Gut microbiota changes in CKD." ] ] 2 => array:9 [ "identificador" => "tbl0015" "etiqueta" => "Table 3" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "fuente" => "Source: Modified and extended from Biagi et al.<a class="elsevierStyleCrossRef" href="#bib0650">17</a>" "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at3" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "PAA, phenylacetic acid; IAA, indole acetic acid; IS, indoxyl sulfate; OAT, organic acid transporters; PC, p-cresol; PCS, p-cresyl sulfate; PTH, parathyroid hormone; RAS, renin–angiotensin system; ROS, oxygen free radicals; TMAO, trimethylamine N-oxide." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Organ/tissue \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Toxin \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Effect \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Endothelium \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased senescence \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Induction of ROS and decrease in NO production \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS and PCS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased expression of ICAM-1, MCP-1 and tissue factor \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased adhesion of leukocytes to the endothelium \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PCS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Inhibition of proliferation, viability, and repair \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IAA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased release of endothelial microparticles \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased endothelial permeability \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased ROS and inflammation and tissue factor expression \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Apoptosis of endothelial cell progenitors \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vascular smooth muscle fibre \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased proliferation \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased production of tissue factor \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PAA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased ROS and expression of osteoblastic proteins \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased ROS production \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vessels \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased aortic calcification and stiffness, expression of osteoblastic markers and OAT \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS and PCS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased cellular senescence \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TMAO \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased rolling and adhesion of leukocytes to the vessel \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Accelerated atherosclerosis \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Leukocytes \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PCS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Activation of the oxidative burst \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased adhesion to the endothelium \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS and IAA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased expression of mononuclear cell tissue factor \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TMAO \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased expression of scavenger receptors in macrophages \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cardiac cells \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Hypertrophy of cardiomyocytes, production of collagen by myofibroblasts and inflammation \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Heart \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Myocardial hypertrophy, cardiac fibrosis and oxidative stress \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Renal tubular cells \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PCS and IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Activation of RAS, mesenchymal epithelial transition, and fibrosis \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased expression of proinflammatory genes and cytokines \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PCS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased methylation of the klotho gene and fibrosis \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased tubular damage \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS and IAA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased expression of MCP-1, ICAM-1, TGF-β and Smad3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased oxidative stress, inhibition of proliferation, increased expression of PAI-1 and NF-κB activation \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PCS, IS, IAA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Decreased cell viability \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Kidneys \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased fibrosis and angiotensinogen expression \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Decreased klotho expression and increased senescence \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IAA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased glomerulosclerosis \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TMAO \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased monocyte infiltration \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased glomerular sclerosis and interstitial fibrosis \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased tubulointerstitial fibrosis and collagen deposition \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Adipocytes \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PCS and IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Increased insulin resistance \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Osteoclasts \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Alteration of differentiation and function \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Osteoblasts \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PCS and IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Decreased cell viability and cell proliferation and increased ROS production \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IS \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Decreases PTH receptor expression \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Promotes apoptosis \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">PAA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Inhibits proliferation and differentiation \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1376002.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Effects of different uraemic toxins at the cellular and tissue level." ] ] 3 => array:8 [ "identificador" => "tbl0020" "etiqueta" => "Table 4" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at4" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "Cr, creatinine; PD, peritoneal dialysis; CKD, chronic kidney disease; HD, haemodialysis; IL, interleukin; P, phosphorus; CRP, C-reactive protein." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Author and year \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Probiotic \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Type of study \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Results \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Hida et al., 1996<a class="elsevierStyleCrossRef" href="#bib1005">88</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lebenin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Observational, patients in HD (n=25), 4 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ Indicate in faeces and serum ↓ p-Cresol in faeces \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Simenhoff et al., 1996<a class="elsevierStyleCrossRef" href="#bib1010">89</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus acidophilus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Observational, patients in HD (n=8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ Dimethylamine ↓ Nitrosodimethylamine \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Takayama et al., 2003<a class="elsevierStyleCrossRef" href="#bib1015">90</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bifidobacterium longum JCM008 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Non-randomised, placebo-controlled. Patients in HD (n=22), 5 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ Indoxyl sulfate \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ando et al., 2003<a class="elsevierStyleCrossRef" href="#bib1020">91</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bifidobacterium longum \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Observational, patients with CKD (n=27), 6 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Reduction of the progression of CKD in patients with con Cr ≥4mg/dl or P≥4mg/dl \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Taki et al., 2005<a class="elsevierStyleCrossRef" href="#bib1025">92</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bifidobacterium longum \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Non-randomised, placebo-controlled. Patients in HD (n=27), 12 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ Indoxyl sulfate, homocysteine and triglycerides \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ranganathan et al., 2009<a class="elsevierStyleCrossRef" href="#bib1030">93</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus acidophilus KB31, Streptococcus thermophilus KB27, Bifidobacterium longum KB35 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Randomised, double-blind, crossover, placebo-controlled. Patients with CKD 3–4 (n=16), 6 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">BUN Uric acid ↑ Quality of life \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ranganathan et al., 2010<a class="elsevierStyleCrossRef" href="#bib1035">94</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus acidophilus KB31, Streptococcus thermophilus KB27, Bifidobacterium longum KB35 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Multicentre, randomised, double-blind, placebo-controlled. Patients with CKD 3–4 (n=46), 6 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">BUN ↑ Quality of life Insurance \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Miranda Alatriste et al., 2014<a class="elsevierStyleCrossRef" href="#bib1040">95</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus casei shirota \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Randomised, placebo-controlled, patients with CKD 3–4 (n=30), 8 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ Urea \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Wang et al., 2015<a class="elsevierStyleCrossRef" href="#bib1045">96</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bifidobacterium bifidum A218, Bifidobacterium catenulatum A302, Bifidobacterium longum A101, Lactobacillus plantarum A87 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Randomised, double-blind, placebo-controlled, patients in PD (n=39), 6 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ TNF-α, IL-5, IL-6 and endotoxin ↑ IL-10 Residual preservation of kidney function \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Natarajan et al., 2014<a class="elsevierStyleCrossRef" href="#bib1050">97</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Renadyl \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Randomised, double-blind, placebo-controlled, patients in HD (n=22), 8 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">No changes in quality of life Tendency towards reduction of indoxyl glucuronide, CRP and leucocyte count \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1376004.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Clinical studies with probiotics in patients with CKD and their effects." ] ] 4 => array:8 [ "identificador" => "tbl0025" "etiqueta" => "Table 5" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at5" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "CRD, chronic kidney disease; GI, gastrointestinal; HD, haemodialysis; NO, nonsignificant; P, phosphorus; CRP, C-reactive protein; PCS, p-cresyl sulfate." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Author and year \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Symbiotic \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Study \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Results \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Nakabayashi et al., 2010<a class="elsevierStyleCrossRef" href="#bib1055">98</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus casei shirota, Bifidobacterium breve yakult and galactooligosaccharides \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Observational, patients in HD (n=9), 4 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ p-Cresol in plasma Normalisation of bowel habits Association of p-cresol and constipation \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ogawa et al., 2012<a class="elsevierStyleCrossRef" href="#bib1060">99</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Bifidobacterium longum JBL01 and oligosaccharides \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Observational, patients in HD (n=15). Control group patients in HD (n=16), 4 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ P levels that returned to baseline 2 weeks later \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pavan et al., 2014<a class="elsevierStyleCrossRef" href="#bib1065">100</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Probiotic and prebiotic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Prospective, open, randomised, placebo-controlled. Patients with CKD 3–5 (n=24), 12 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Reduction in the progression of CKD \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cruz-Mora et al., 2014<a class="elsevierStyleCrossRef" href="#bib1070">101</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus acidophilus, Bifidobacterium lactis and inulin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Double-blind, randomised, placebo-controlled. Patients in HD (n=18), 2 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↑ Bifidobacteria in faeces ↓ Lactobacilli in faeces (in the 2 groups) Improvements of GI symptoms \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Guida et al., 2014<a class="elsevierStyleCrossRef" href="#bib1075">102</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus plantarum, Lactobacillus casei subsp. Rhamnosus, Lactobacillus gasseri, Bifidobacterium infantis, Bifidobacterium longum, Lactobacillus acidophilus, Lactobacillus salivarius, Lactobacillus sporogenes and Streptococcus thermophilus inulin and resistant tapioca starch \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Randomised, double-blind, placebo-controlled. Patients with CKD 3–4 (n=30), 4 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">↓ p-Cresol in plasma With no changes in GI symptoms \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Viramontes-Hörner et al., 2015<a class="elsevierStyleCrossRef" href="#bib1080">103</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus acidophilus and Bifidobacterium lactis+prebiotic (inulin) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Randomised, double-blind, placebo-controlled. Patients in HD (n=42), 2 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Tendency to diminish levels of CRP and TNF-α. Improvement of GI symptoms \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Rossi et al., 2014<a class="elsevierStyleCrossRef" href="#bib1085">104</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lactobacillus, bifidobacteria and Streptococcus generates+inulin, fructooligosaccharides and galactooligosaccharides \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Randomised, double-blind, crossover, placebo-controlled. Patients with CKD 4–5, 6 weeks with a washout of 4 weeks \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Decreased PCS, decreased NS of IS Increased bifidobacteria and decreased ruminococcaceae in faeces. No changes in oxidative stress or inflammation markers and slight increase in albuminuria \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1376001.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Clinical studies with symbiotics in patients with CKD and their effects." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:113 [ 0 => array:3 [ "identificador" => "bib0570" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Development of the human infant intestinal microbiota" "autores" => array:1 [ 0 => array:2 [ …2] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1371/journal.pbio.0050177" "Revista" => array:5 [ "tituloSerie" => "PLoS Biol" "fecha" => "2007" "volumen" => "5" "paginaInicial" => "e177" "link" => array:1 [ …1] ] ] ] ] ] ] 1 => array:3 [ "identificador" 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Microbiota intestinal en la enfermedad renal crónica

Secundino Cigarran Guldrisa,

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secundino.cigarran.guldris@sergas.es

Corresponding author.

, Emilio González Parrab, Aleix Cases Amenósc

a Sección de Nefrología, Hospital Da Costa, Burela, Lugo, Spain

b Servicio de Nefrología, Fundación Jiménez Díaz, Universidad Autónoma de Madrid, Madrid, Spain

c Servicio de Nefrología, Hospital Clinic, Universitat de Barcelona, Barcelona, Spain

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            "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Schematic model showing how tissue kallikrein participates in the regulation of the TRPV5 calcium epithelial channel in the late distal convoluted tubule&#46; The tissue kallikrein produced by the connecting tubule is released into the urinary fluid&#46; It is there that it acts on the filtered or locally secreted kininogen &#40;KN&#41; and finally produces bradykinin &#40;BK&#41;&#46; BK acts on its B2 receptor &#40;BKRB<span class="elsevierStyleInf">2</span>&#41;&#44; activating the phospholipase C&#47;diacylglycerol&#47;protein kinase C &#40;PLC&#47;DAG&#47;PKC&#41; pathway by inducing the TRPV5 calcium channel localisation at the apical membrane level and favours the reabsorption of tubular calcium&#46; BK is degraded by neutral endopeptidase &#40;NEP&#41; and renal CYP kinase&#46;</p>"
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        "titulo" => "Microbiota intestinal en la enfermedad renal cr&#243;nica"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">What are the microbiota and the microbiome&#63;</span><p id="par0005" class="elsevierStylePara elsevierViewall">Since Hippocrates &#40;400 BC&#41; established that &#8220;death lies in the intestines&#8221;&#44; their influence on the health of human beings has been well known&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">The germs that inhabit our body are called the microbiota&#44; and their collective genomes&#44; the microbiome&#46; More than 100 trillion germs &#40;10<span class="elsevierStyleSup">14</span>&#41; cohabit with us throughout our lives&#44; representing 10 times the number of cells that make up our body and constituting 1&#46;5&#8211;2<span class="elsevierStyleHsp" style=""></span>kg of our weight&#46;<a class="elsevierStyleCrossRefs" href="#bib0570"><span class="elsevierStyleSup">1&#44;2</span></a> The concentration of germs in the digestive tract gradually increases from the stomach to the colon&#44; where they reach the highest concentration &#40;up to 10<span class="elsevierStyleSup">11</span> microorganisms&#47;g of faeces&#41; and diversity&#46; The gut microbiota plays an important role in metabolic&#44; nutritional&#44; physiological&#44; and immunological processes&#44; and constitutes a true ecosystem&#46;<a class="elsevierStyleCrossRef" href="#bib0580"><span class="elsevierStyleSup">3</span></a> The human microbiome is our second genome&#44; which has more than 3 million genes &#40;100 times more genes than the human genome itself&#41; and is the subject of research by the Human Microbiome Project Consortium&#46;<a class="elsevierStyleCrossRefs" href="#bib0585"><span class="elsevierStyleSup">4&#8211;6</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Originally&#44; the gut microbiota is formed through the placenta&#44; where low levels of non-pathogenic germs&#44; especially the phyla firmicutes&#44; bacteroidetes&#44; and <span class="elsevierStyleItalic">Fusobacteria</span> are nested&#46; In the first years of life&#44; feeding&#44; type of birth&#44; hygiene&#44; and use of antibiotics condition the formation of the intestinal microbiome&#46;<a class="elsevierStyleCrossRefs" href="#bib0600"><span class="elsevierStyleSup">7&#44;8</span></a> Different species of germs colonise and are originated during various events &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">The gut microbiota is established in the first 2&#8211;3 years of life as a dynamic ecosystem&#44; dominated by bifidobacteria&#59; their composition increases in richness and diversity until reaching their maximum complexity in adulthood&#44; when the dominant species are bacteroidetes&#44; firmicutes and actinobacteria&#46;<a class="elsevierStyleCrossRefs" href="#bib0610"><span class="elsevierStyleSup">9&#8211;11</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Bacterial communities that lie in the intestine are&#44; therefore&#44; a combination of different types and amounts of bacteria and 3 different groups of microbiota or enterotypes have been identified in humans&#46;<a class="elsevierStyleCrossRef" href="#bib0625"><span class="elsevierStyleSup">12</span></a> The phylogenetic composition of intestinal microflora tends to be similar between individuals from the same region&#44; from the same family and also with a similar diet which plays a significant role in their composition&#46;<a class="elsevierStyleCrossRefs" href="#bib0630"><span class="elsevierStyleSup">13&#44;14</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">Dietary habits affect the composition of the gut microbiota&#46; Since the microbiota is in contact with a significant number of neural cells and immunological cells&#44; it directs the maturation of the immune system in childhood and contributes to the maintenance of its homeostasis during life&#46;<a class="elsevierStyleCrossRef" href="#bib0575"><span class="elsevierStyleSup">2</span></a> Complex polysaccharides&#44; which are not digested by enzymes in the small intestine&#44; are metabolised by the colon microflora&#46; These polysaccharides are degraded and fermented in the large intestine and converted into short chain fatty acids &#40;SCFAs&#41; and gases &#40;CO<span class="elsevierStyleInf">2</span> and H<span class="elsevierStyleInf">2</span>&#41;&#46; A high intestinal content of fructose promotes the formation of butyrate which is produced by bacteria&#46; Dietary supplementation with specific polysaccharides may promote the growth of &#8220;healthy&#8221; germs &#40;<span class="elsevierStyleItalic">Bifidobacterium</span>&#44; <span class="elsevierStyleItalic">Lactobacillus</span>&#41;&#44; the production of SCFA and it may decrease intestinal pH that inhibits the growth of pathogenic bacteria&#46;<a class="elsevierStyleCrossRefs" href="#bib0640"><span class="elsevierStyleSup">15&#44;16</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">In the ageing process&#44; progressive damage occurs to the morphology and function of the different systems and the microbiota becomes less diverse and more dynamic&#44; characterised by the predominance of bacteroidetes over firmicutes&#44; with an increase of <span class="elsevierStyleItalic">Protobacteria</span> spp&#46; and a decrease of <span class="elsevierStyleItalic">Bifidobacterium</span>&#46; This is evidenced by rRNA techniques and it has been analysed as part of the study ELDERMET&#46;<a class="elsevierStyleCrossRefs" href="#bib0650"><span class="elsevierStyleSup">17&#8211;19</span></a> Major changes in the microbiota are found in the colon of persons over 60 years of age&#46; The significance of these changes is yet to be clarified&#46;<a class="elsevierStyleCrossRef" href="#bib0665"><span class="elsevierStyleSup">20</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">Faecal bacteria such as <span class="elsevierStyleItalic">Escherichia coli</span>&#44; which divides every 20<span class="elsevierStyleHsp" style=""></span>min&#44; are genetically prepared to be highly adaptative&#44; and always survive even though their host ages&#46; Without this plasticity&#44; we probably would not have been able to cope with changes in lifestyle and dietary habits&#44; as evidenced by the transition from the Palaeolithic to the dietary habits of Western societies&#46;<a class="elsevierStyleCrossRef" href="#bib0670"><span class="elsevierStyleSup">21</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">Functionally&#44; the gut microbiota provides nutrients and energy to the body through fermentation of nondigestible foods in the large intestine&#46; The most important fermentation products deriving from the fermentation are the SCFA&#44; which serve as a source of energy to intestinal cells and bacteria&#44; and contribute to energy expenditure&#44; satiety&#44; and glucose homeostasis&#46;<a class="elsevierStyleCrossRef" href="#bib0675"><span class="elsevierStyleSup">22</span></a> Other relevant functions of the gut microbiota are the endogenous synthesis of certain vitamins and amino acids&#44; the metabolism of bile acids&#44; or the maintenance of the integrity of intestinal barriers&#44; which protect the host from pathogenic germs&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Thus&#44; the gut microbiota is involved in the maturation of the immune system in infancy and contributes to the maintenance of its homeostasis throughout life&#46;<a class="elsevierStyleCrossRef" href="#bib0680"><span class="elsevierStyleSup">23</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Gut microbiota in chronic kidney disease</span><p id="par0055" class="elsevierStylePara elsevierViewall">From the early stages of chronic kidney disease &#40;CKD&#41; there is a quantitative and qualitative alteration of intestinal microflora &#40;dysbiosis&#41;&#59; so the composition and metabolic activities of microflora are changed in CKD and this is a hot and innovative topic in nephrology literature&#46; These alterations include changes in intestinal transit&#44; decreased protein absorption&#44; decrease in dietary fibre intake&#44; treatment with oral iron and frequent use of antibiotics&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">All of this contributes to systemic inflammation and the accumulation of uraemic toxins that are absorbed by intestine and eliminated by the kidney&#46; Inflammation and uraemic toxins play a central role in the pathophysiology of atherosclerosis&#44; as well as in other complications associated with CKD<a class="elsevierStyleCrossRefs" href="#bib0685"><span class="elsevierStyleSup">24&#8211;27</span></a>&#59; that will be reviewed below&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Patients with CKD are polymedicated&#46; Some drugs frequently prescribed to these patients may alter intestinal microflora&#44; especially antibiotics&#44;<a class="elsevierStyleCrossRefs" href="#bib0705"><span class="elsevierStyleSup">28&#44;29</span></a> but others may also slow intestinal transit&#44; phosphorus binders&#44; ion exchange resins&#44;<a class="elsevierStyleCrossRef" href="#bib0715"><span class="elsevierStyleSup">30</span></a> or iron supplements that may have an effect on microflora but it is not well defined&#46;<a class="elsevierStyleCrossRefs" href="#bib0720"><span class="elsevierStyleSup">31&#44;32</span></a></p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Change in intestinal barriers in chronic kidney disease</span><p id="par0070" class="elsevierStylePara elsevierViewall">Changes in intestinal barriers with an increased intestinal permeability is common in CKD &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">Increasing urea levels and expanding bacteria with urease causes an increase ammonium production in the intestinal lumen and induce changes in intestinal pH that produces an alteration of intestinal permeability by affecting the tight junctions of the enterocyte&#46; Vaziri et al&#46; have demonstrated a marked reduction of tight junction proteins&#44; claudin-1&#44; occludin&#44; and ZO1&#44; in the colonic mucosa in CKD&#59; this is associated with an infiltration of mononuclear leukocytes in the lamina propria and a marked thickening of the colon wall&#46;<a class="elsevierStyleCrossRef" href="#bib0730"><span class="elsevierStyleSup">33</span></a> There is histological evidence of chronic inflammation of the intestinal tract including oesophagitis&#44; gastritis&#44; etc&#46;<a class="elsevierStyleCrossRefs" href="#bib0730"><span class="elsevierStyleSup">33&#44;34</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">The presence of frequent oedema and hypervolaemia in CKD may aggravate intestinal barrier dysfunction in CKD patients on&#44; haemodialysis&#44; or peritoneal dialysis&#46; In addition&#44; excessive ultrafiltration and episodes of hypotension during haemodialysis may cause episodes of transient intestinal ischaemia which increases the permeability of the intestinal barrier facilitating the passage of endotoxins&#46;<a class="elsevierStyleCrossRef" href="#bib0730"><span class="elsevierStyleSup">33</span></a></p><p id="par0085" class="elsevierStylePara elsevierViewall">In renal transplant patients&#44; the investigation of the gut microbiota is in its infancy&#46; It is known that inflammatory processes&#44; such as graft ischaemia time&#44; baseline disease and immunosuppressive drugs may play a relevant role in the alteration of the intestinal barrier&#46;<a class="elsevierStyleCrossRefs" href="#bib0740"><span class="elsevierStyleSup">35&#44;36</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Intestinal microflora as a cause of inflammation in chronic kidney disease</span><p id="par0090" class="elsevierStylePara elsevierViewall">In CKD&#44; the decreased clearance of proinflammatory cytokines&#44; is associated with the development of oxidative stress and inflammation&#46; The later are contributing factors to the progression of the disease and its complications&#44; including cardiovascular disease&#44; cachexia&#44; and anaemia&#46; Oxidative stress and chronic inflammation stimulate the NF-&#954;B transcription factor&#44; which is the key regulator of proinflammatory cytokines and chemokines&#46; Increased permeability of intestinal barriers in CKD patients favours the translocation of bacterial products of intestinal origin&#44; as evidenced by the presence of DNA fragments of circulating intestinal pathogens &#40;aerobic and anaerobic&#41;&#44; both in patients in different stages of CKD and on renal replacement therapy&#46;<a class="elsevierStyleCrossRefs" href="#bib0750"><span class="elsevierStyleSup">37&#8211;39</span></a> The increase in circulating bacterial products of intestinal origin activates innate immunity&#44; promotes the inflammatory state associated with CKD and&#44; increases the incidence of cardiovascular disease and mortality&#46;<a class="elsevierStyleCrossRefs" href="#bib0765"><span class="elsevierStyleSup">40&#8211;42</span></a></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Microbiota and uraemic toxins derived from the intestine in chronic kidney disease</span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Intestinal production of uraemic toxins</span><p id="par0095" class="elsevierStylePara elsevierViewall">The origin of uraemic toxins in CKD is multiple&#46; The importance of toxins generated by intestinal microbial metabolism<a class="elsevierStyleCrossRef" href="#bib0780"><span class="elsevierStyleSup">43</span></a> is increasingly recognised&#46; Approximately 10<span class="elsevierStyleHsp" style=""></span>g of proteins reach the colon daily&#44; where they are degraded by intestinal bacteria to metabolites such as ammonium&#44; amines&#44; thiols&#44; phenols and indoles&#46; These colon fermentation products are eliminated through faeces&#44; although a portion is absorbed and eliminated by the kidney&#44; so these are accumulated in CKD&#46;<a class="elsevierStyleCrossRef" href="#bib0785"><span class="elsevierStyleSup">44</span></a> In CKD&#44; the uraemic toxins derived from intestinal microflora are&#58;</p><p id="par0100" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Phenols and indoles&#58; p-cresol and indoxyl sulfate</span>&#46; Phenols include p-cresol&#44; p-cresyl sulfate &#40;PCS&#41;&#44; p-cresyl glucuronide&#44; phenylacetic acid&#44; phenyl sulfate and phenol&#46;<a class="elsevierStyleCrossRef" href="#bib0790"><span class="elsevierStyleSup">45</span></a><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">-</span><p id="par0105" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">p-Cresol&#47;p-cresyl sulfate</span>&#58; products of phenylalanine and tyrosine metabolism of intestinal anaerobic bacteria&#46; p-Cresol is conjugated in the intestinal wall to PCS and p-cresyl glucuronide in the liver&#46; PCS is the main circulating metabolite of p-cresol&#46;<a class="elsevierStyleCrossRef" href="#bib0795"><span class="elsevierStyleSup">46</span></a></p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">-</span><p id="par0110" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Phenol</span>&#58; mainly derives from ingestion&#44; from the catabolism of tyrosine by intestinal bacteria&#44; as well as from tobacco consumption&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">-</span><p id="par0115" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Phenylacetic acid</span>&#58; is the result of the degradation of phenylalanine&#46;</p></li></ul></p><p id="par0120" class="elsevierStylePara elsevierViewall">Among the <span class="elsevierStyleItalic">indoles</span> are indoxyl sulfate &#40;IS&#41; and indoleacetic acid&#46;<a class="elsevierStyleCrossRef" href="#bib0790"><span class="elsevierStyleSup">45</span></a> Both originate from the degradation of tryptophan by intestinal bacteria and are subsequently sulfated in the liver into IS&#46; Indoles and phenols are uraemic toxins bound to proteins&#46;<a class="elsevierStyleCrossRef" href="#bib0800"><span class="elsevierStyleSup">47</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Amines and polyamines&#58;</span> amines and polyamines are generated from intestinal microbial metabolism&#46; An amino acid that is clinically relevant and of growing interest is trimethylamine N-oxide &#40;TMAO&#41;&#46; TMAO is produced by the intestinal metabolism of quaternary amines&#44; such as choline&#47;phosphatidylcholine&#44; betaine&#44; or <span class="elsevierStyleSmallCaps">l</span>-carnitine&#46; <span class="elsevierStyleSmallCaps">l</span>-Carnitine&#44; which is present in red meat&#44; also induces the formation of TMAO and it is associated with an increase in cardiovascular disease&#46;<a class="elsevierStyleCrossRef" href="#bib0805"><span class="elsevierStyleSup">48</span></a> Dietary sources of TMAO are red meats&#44; meats in general&#44; egg yolks&#44; liver&#44; dairy products and saltwater fish&#46; In CKD&#44; TMAO accumulates and its levels depends on the glomerular filtration&#44; but its binding to proteins is low&#44; and it is well eliminated with dialysis&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">Polyamines are organic cations including cadaverine&#44; spermine&#44; spermidine and putrescine&#46; They come from the decarboxylation of <span class="elsevierStyleSmallCaps">l</span>-arginine&#44; <span class="elsevierStyleSmallCaps">l</span>-ornithine or lysine in the intestine&#46; In CKD patients&#44; putrescine&#44; spermidine&#44; and spermine are increased in serum&#46;<a class="elsevierStyleCrossRef" href="#bib0810"><span class="elsevierStyleSup">49</span></a> These molecules have been shown to interact with insulin and lipoproteins&#44; and contribute to the acceleration of atherosclerosis along with other factors such as hypertriglyceridemia&#46;<a class="elsevierStyleCrossRef" href="#bib0815"><span class="elsevierStyleSup">50</span></a></p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Biological and clinical consequences of the accumulation of uraemic toxins</span><p id="par0135" class="elsevierStylePara elsevierViewall">The aforementioned uraemic toxins have been associated with deleterious biological effects in different tissues and cell lines<a class="elsevierStyleCrossRefs" href="#bib0820"><span class="elsevierStyleSup">51&#44;52</span></a> &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#44; and with an increased risk of the progression of CKD&#44; morbidity and mortality&#46;<ul class="elsevierStyleList" id="lis0010"><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">a&#41;</span><p id="par0140" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Progression of CKD</span>&#58; both IS and PCS are associated to the development of fibrosis&#44; deterioration of renal function and disease progression&#46;<a class="elsevierStyleCrossRefs" href="#bib0825"><span class="elsevierStyleSup">52&#44;53</span></a> In vitro studies have shown a deleterious effects of these molecules on renal tubular cells&#46;<a class="elsevierStyleCrossRef" href="#bib0835"><span class="elsevierStyleSup">54</span></a> In a prospective study in patients with stage 1&#8211;5 CKD&#44; the predictive role of both molecules in disease progression was confirmed&#46;<a class="elsevierStyleCrossRef" href="#bib0840"><span class="elsevierStyleSup">55</span></a> In experimental animals&#44; a diet rich in choline or TMAO preduces progressive tubulointerstitial fibrosis and renal dysfunction&#46;<a class="elsevierStyleCrossRef" href="#bib0845"><span class="elsevierStyleSup">56</span></a></p></li><li class="elsevierStyleListItem" id="lsti0025"><span class="elsevierStyleLabel">b&#41;</span><p id="par0145" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Cardiovascular complications</span>&#58; in CKD patients&#44; IS is associated with endothelial damage&#44; arterial stiffness and aortic calcification<a class="elsevierStyleCrossRef" href="#bib0850"><span class="elsevierStyleSup">57</span></a>&#59; and&#44; in hemodialysis patients it is associated with atherosclerosis<a class="elsevierStyleCrossRef" href="#bib0855"><span class="elsevierStyleSup">58</span></a> and endothelial dysfunction&#44;<a class="elsevierStyleCrossRef" href="#bib0860"><span class="elsevierStyleSup">59</span></a> it has a cardiac profibrotic effect&#44; favours hypertrophy of myocardiocytes<a class="elsevierStyleCrossRef" href="#bib0865"><span class="elsevierStyleSup">60</span></a> and it is a predisposing factor of atrial fibrillation&#46;<a class="elsevierStyleCrossRef" href="#bib0870"><span class="elsevierStyleSup">61</span></a> Similar vascular effects have been described with&#44;<a class="elsevierStyleCrossRef" href="#bib0875"><span class="elsevierStyleSup">62</span></a> which is a predictor of cardiovascular risk in CKD patients&#46;<a class="elsevierStyleCrossRefs" href="#bib0880"><span class="elsevierStyleSup">63&#44;64</span></a> In hemodialysis patients PCS and IS have been associated with peripheral vascular disease and thrombosis of vascular access&#46;<a class="elsevierStyleCrossRef" href="#bib0890"><span class="elsevierStyleSup">65</span></a> A recent meta-analysis confirms the relationship of these molecules to cardiovascular risk in CKD&#46;<a class="elsevierStyleCrossRef" href="#bib0895"><span class="elsevierStyleSup">66</span></a></p><p id="par0150" class="elsevierStylePara elsevierViewall">Likewise&#44; indoleacetic acid is associated with oxidative stress and inflammation markers&#44; and it is a predictor of mortality and cardiovascular events in CKD&#46;<a class="elsevierStyleCrossRef" href="#bib0900"><span class="elsevierStyleSup">67</span></a></p><p id="par0155" class="elsevierStylePara elsevierViewall">Elevated levels of TMAO predicts coronary atherosclerotic burden<a class="elsevierStyleCrossRef" href="#bib0845"><span class="elsevierStyleSup">56</span></a> and mortality in patients with CKD&#44;<a class="elsevierStyleCrossRefs" href="#bib0905"><span class="elsevierStyleSup">68&#44;69</span></a> although this is not shown in all reports&#46;<a class="elsevierStyleCrossRef" href="#bib0915"><span class="elsevierStyleSup">70</span></a></p></li><li class="elsevierStyleListItem" id="lsti0030"><span class="elsevierStyleLabel">c&#41;</span><p id="par0160" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Anaemia</span>&#58; IS has been associated with anaemia of the renal patient&#59; it interfere with the adequate production of erythropoietin<a class="elsevierStyleCrossRefs" href="#bib0920"><span class="elsevierStyleSup">71&#44;72</span></a> and increased eryptosis &#40;programmed cell death of red blood cells&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0930"><span class="elsevierStyleSup">73</span></a> Polyamines are associated to anaemia in renal patients&#44; through an intra-erythrocytic effect&#44;<a class="elsevierStyleCrossRef" href="#bib0935"><span class="elsevierStyleSup">74</span></a> reduces erythropoiesis&#44; and inhibit the activity of erythropoietin&#46;</p></li><li class="elsevierStyleListItem" id="lsti0035"><span class="elsevierStyleLabel">d&#41;</span><p id="par0165" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Alterations of bone-mineral metabolism</span>&#58; IS reduces bone formation by promoting oxidative stress in osteoblasts and inducing resistance to PTH&#44; which favours the development adynamic bone&#46;<a class="elsevierStyleCrossRef" href="#bib0940"><span class="elsevierStyleSup">75</span></a> There is a positive correlation between FGF-23 and IS serum levels&#44; suggesting an association between this molecule and metabolic bone disease in uraemic patients&#46;<a class="elsevierStyleCrossRef" href="#bib0945"><span class="elsevierStyleSup">76</span></a> Likewise&#44; less bone remodelling has been observed in uraemic rats with higher IS after a parathyroidectomy&#46;<a class="elsevierStyleCrossRef" href="#bib0950"><span class="elsevierStyleSup">77</span></a></p></li><li class="elsevierStyleListItem" id="lsti0040"><span class="elsevierStyleLabel">e&#41;</span><p id="par0170" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Insulin resistance</span>&#58; In CKD patients the catabolism of insulin is reduced and often&#44; they also have insulin resistance&#44; which is associated with an increased risk of mortality&#59; it seems that insulin resistance is related to some of the uraemic toxins&#46;<a class="elsevierStyleCrossRef" href="#bib0955"><span class="elsevierStyleSup">78</span></a></p></li></ul></p><elsevierMultimedia ident="tbl0015"></elsevierMultimedia></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Prevention and treatment of dysbiosis</span><p id="par0175" class="elsevierStylePara elsevierViewall">In recent years there is a growing interest in restoring the symbiosis of intestinal microflora in CKD aiming to reduce the generation of uraemic toxins&#44; oxidative stress&#44; and inflammation&#46;<a class="elsevierStyleCrossRef" href="#bib0960"><span class="elsevierStyleSup">79</span></a><ul class="elsevierStyleList" id="lis0015"><li class="elsevierStyleListItem" id="lsti0045"><span class="elsevierStyleLabel">a&#41;</span><p id="par0180" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">High fibre diet</span>&#58; a high fibre diet increases the production of SCFA&#44; which provides energy to the intestinal flora and allows amino acids that reach the colon to be incorporated into bacterial proteins and be excreted instead of being fermented into uraemic solutes&#46; In addition&#44; SCFAs are used as substrate by the intestinal mucosa helping to maintain their functionality and integrity&#46; Fibre increases intestinal transit reducing the time for fermentation of amino acids and improves the composition of microflora which reduces the production of undesirable solutes&#46; In CKD patients&#44; there is a direct relationship between dietary protein&#47;fibre ratio and PCS and IS levels&#44; so a diet with a low protein&#47;fibre ratio should be beneficial&#46;<a class="elsevierStyleCrossRef" href="#bib0965"><span class="elsevierStyleSup">80</span></a> In healthy subjects&#44; a vegetarian diet&#44; as compared with the omnivore diet&#44; reduces the generation IS or PCS&#59; this effect was related to the higher fibre and lower protein content of the vegetarian diet&#46;<a class="elsevierStyleCrossRef" href="#bib0970"><span class="elsevierStyleSup">81</span></a> A very low protein diet &#40;0&#46;3<span class="elsevierStyleHsp" style=""></span>g&#47;kg body weight&#47;day&#41; supplemented with amino acid keto-analogues also reduces IS levels in patients with CKD&#46;<a class="elsevierStyleCrossRef" href="#bib0975"><span class="elsevierStyleSup">82</span></a></p><p id="par0185" class="elsevierStylePara elsevierViewall">Several therapeutic interventions have recently explored to improve the dysbiosis of the intestinal microflora&#44; reduce the absorption of uraemic toxins and the passage of endotoxins from the intestinal lumen&#46;</p></li><li class="elsevierStyleListItem" id="lsti0050"><span class="elsevierStyleLabel">b&#41;</span><p id="par0190" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Prebiotics&#44; probiotics&#44; and symbiotics</span>&#58; the generation of uraemic toxins could be reduced by selectively increasing saccharolyticbacteria &#40;which digest dietary fibre&#41; and decreasing proteolytic bacteria &#40;protein and amino acid fermenters&#41; in the colon&#46; The main regulator of metabolism of colon bacteria is the availability of nutrients and specifically the rate of fermentable carbohydrates vs&#46; nitrogen&#46;</p><p id="par0195" class="elsevierStylePara elsevierViewall">Prebiotics are non-digestible food components which&#44; through selective fermentation&#44; allow for specific changes in the composition or activity in gastrointestinal microflora&#44; which are beneficial to the health and well-being of the host&#46; Prebiotics stimulate the growth or activity of one or a limited number of bacteria in the colon&#59; they may increase carbohydrate fermentables vs&#46; nitrogen&#59; they include inulin&#44; fructooligosaccharides&#44; galactooligosaccharides&#44; etc&#46; Inulin enriched with oligofructose reduces the generation of PCS and the serum concentrations in hemodialysis patients&#44; but has no effect on IS&#46;<a class="elsevierStyleCrossRef" href="#bib0980"><span class="elsevierStyleSup">83</span></a> Resistant starch reduces IS levels in hemodialysis patients and reduces PCS but not significantly&#46;<a class="elsevierStyleCrossRef" href="#bib0985"><span class="elsevierStyleSup">84</span></a> In a CKD rat model&#44; a diet rich in resistant starch delayed the progression of CKD and attenuated oxidative stress and inflammation&#46;<a class="elsevierStyleCrossRef" href="#bib0990"><span class="elsevierStyleSup">85</span></a> Currently&#44; a randomised&#44; crossover&#44; double-blind&#44; phase 2 clinical trial in patients with stage 3b-4 CKD is examining the effect of the supplementation of arabinoxylan-oligosaccharides on plasma levels of PCS and indole derivatives urinary excretion of these compounds and insulin resistance are also examined&#46;<a class="elsevierStyleCrossRef" href="#bib0995"><span class="elsevierStyleSup">86</span></a></p><p id="par0200" class="elsevierStylePara elsevierViewall">Probiotics are defined as &#8220;living micro-organisms&#8221; that&#44; being administered in adequate amounts&#44; provide a health benefit to the host&#46; A recent review evaluates the potential benefits of probiotics in general and especially in CKD&#46;<a class="elsevierStyleCrossRef" href="#bib1000"><span class="elsevierStyleSup">87</span></a> The efficacy of probiotics to decrease levels of uraemic toxins and to delay the progression of CKD has been investigated in in vitro models&#44; animal models and in patients with CKD&#46; However&#44; to date&#44; there are no large-scale quality intervention studies and studies on clinical events to support their widespread use&#46; There are only small studies&#44; most of which&#44;<a class="elsevierStyleCrossRefs" href="#bib1005"><span class="elsevierStyleSup">88&#44;92&#8211;95</span></a> but not all&#44;<a class="elsevierStyleCrossRef" href="#bib1050"><span class="elsevierStyleSup">97</span></a> observe a decrease in uraemic toxin levels&#46; Administration of <span class="elsevierStyleItalic">Bifidobacterium longum</span> in enteric capsules to patients with CKD had minimal effects on the progression of the disease in patients with CKD&#46;<a class="elsevierStyleCrossRef" href="#bib1020"><span class="elsevierStyleSup">91</span></a> However&#44; a randomised&#44; double-blind trial in patients on peritoneal dialysis observed a significant reduction in serum proinflammatory endotoxin and cytokine levels&#44; an increase in serum IL-10 levels&#44; and the preservation of residual renal function after 6 months of treatment with a probiotic<a class="elsevierStyleCrossRef" href="#bib1045"><span class="elsevierStyleSup">96</span></a> &#40;<a class="elsevierStyleCrossRef" href="#tbl0020">Table 4</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0020"></elsevierMultimedia><p id="par0205" class="elsevierStylePara elsevierViewall">Symbiotics are probiotic supplements combined with prebiotics&#46; In hemodialysis patients&#44; on treatment with a symbiotic there is a decrease in the level of PCS&#44; but not those of IS&#44;<a class="elsevierStyleCrossRef" href="#bib1055"><span class="elsevierStyleSup">98</span></a> which was confirmed in another study&#46;<a class="elsevierStyleCrossRef" href="#bib1075"><span class="elsevierStyleSup">102</span></a> Another study observed a delay in the progression of CKD with symbiotic treatment&#44;<a class="elsevierStyleCrossRef" href="#bib1065"><span class="elsevierStyleSup">100</span></a> while another study did not observe a significant improvement in inflammation markers&#46;<a class="elsevierStyleCrossRef" href="#bib1080"><span class="elsevierStyleSup">103</span></a> Finally&#44; a randomised&#44; double-blind&#44; crossover study in patients with CKD<a class="elsevierStyleCrossRef" href="#bib1085"><span class="elsevierStyleSup">104</span></a> demonstrated a reduction in PCS levels&#44; a non-significant decrease in IS and an increase in bifidobacteria and reduction of faecal ruminococcus&#44; but no change in inflammation markers&#44; oxidative stress&#44; or endotoxins&#44; although a slight increase in albuminuria was observed &#40;<a class="elsevierStyleCrossRef" href="#tbl0025">Table 5</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0025"></elsevierMultimedia><p id="par0210" class="elsevierStylePara elsevierViewall">One of the major limitations of probiotic or symbiotic therapy is that no study has yet demonstrated the sustained survival of probiotics in the dysbiotic colon of patients with CKD&#46; There are also no studies that have evaluated the effect of these treatments on the levels of TMAO in this population&#46; In choosing probiotics&#44; the contribution of urease-containing bacteria must be considered&#44; since they may increase intestinal ammonia generation&#44; which may damage epithelial tight junctions&#44; and increase intestinal permeability to the passage of endotoxins from the intestinal lumen&#46;<a class="elsevierStyleCrossRefs" href="#bib0730"><span class="elsevierStyleSup">33&#44;34</span></a></p></li><li class="elsevierStyleListItem" id="lsti0055"><span class="elsevierStyleLabel">c&#41;</span><p id="par0215" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Adsorptive therapies</span>&#58; the use of oral sorbents could decrease uraemic toxins and circulating intestinal endotoxins&#46; AST-120 oral sorbents decrease IS levels in a dose-dependent manner&#46;<a class="elsevierStyleCrossRef" href="#bib1090"><span class="elsevierStyleSup">105</span></a> In addition&#44; a reduction in the IS&#44; PCS&#44; or phenyl sulfate and oxidative stress levels have been described in patients on haemodialysis&#46;<a class="elsevierStyleCrossRef" href="#bib1095"><span class="elsevierStyleSup">106</span></a> Other authors have reported that the administration of AST-120 improves the erythropoietic response to CERA&#46;<a class="elsevierStyleCrossRef" href="#bib1100"><span class="elsevierStyleSup">107</span></a> AST-120 improves intestinal barrier dysfunction and decreases endotoxin plasma levels&#44; inflammation markers and oxidative stress in a CKD model in rats&#46;<a class="elsevierStyleCrossRef" href="#bib1105"><span class="elsevierStyleSup">108</span></a></p></li></ul></p><p id="par0220" class="elsevierStylePara elsevierViewall">Although small randomised&#44; controlled studies in experimental animals and retrospective studies in patients have indicated a nephroprotective effect of AST-120 &#40;reviewed by Schulman et al&#46;<a class="elsevierStyleCrossRef" href="#bib1110"><span class="elsevierStyleSup">109</span></a>&#41;&#44; a subsequent large randomised&#44; controlled trial in patients with CKD was unable to confirm this&#46;<a class="elsevierStyleCrossRef" href="#bib1110"><span class="elsevierStyleSup">109</span></a> The study had some methodological limitations&#44; but also suggested the possibility that the objective of treating specific uraemic toxins may not be sufficient&#46; However&#44; another retrospective study of the long-term effects of AST-120 on patients with stage 3&#8211;5 CKD showed a reduction in the risk of progression to dialysis&#44; mortality&#44; cardiac events and vascular accident vs&#46; those patients who did not receive it&#46;<a class="elsevierStyleCrossRef" href="#bib1115"><span class="elsevierStyleSup">110</span></a></p><p id="par0225" class="elsevierStylePara elsevierViewall">Although a beneficial effect of sevelamer on IS and PCS has been described in in vitro studies&#44; in vivo studies in mice or patients have not demonstrated a reduction in the levels of these uraemic toxins&#46;<a class="elsevierStyleCrossRef" href="#bib1120"><span class="elsevierStyleSup">111</span></a> However&#44; sevelamer does reduce endotoxin levels and systemic inflammation in patients on haemodialysis&#46;<a class="elsevierStyleCrossRefs" href="#bib1125"><span class="elsevierStyleSup">112&#44;113</span></a></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Key concepts</span><p id="par0230" class="elsevierStylePara elsevierViewall"><ul class="elsevierStyleList" id="lis0020"><li class="elsevierStyleListItem" id="lsti0060"><span class="elsevierStyleLabel">1&#46;</span><p id="par0235" class="elsevierStylePara elsevierViewall">In CKD&#44; there is a dysbiosis of the intestinal microflora&#46;</p></li><li class="elsevierStyleListItem" id="lsti0065"><span class="elsevierStyleLabel">2&#46;</span><p id="par0240" class="elsevierStylePara elsevierViewall">Intestinal microflora generate uraemic toxins that are absorbed and accumulate in CKD&#44; and are associated with increased oxidative stress and inflammation&#46;</p></li><li class="elsevierStyleListItem" id="lsti0070"><span class="elsevierStyleLabel">3&#46;</span><p id="par0245" class="elsevierStylePara elsevierViewall">In CKD&#44; there is an increase in the permeability of the intestinal barrier that allows the passage into the systemic circulation of endotoxins and other bacterial products that aggravate the inflammatory state of CKD&#46;</p></li><li class="elsevierStyleListItem" id="lsti0075"><span class="elsevierStyleLabel">4&#46;</span><p id="par0250" class="elsevierStylePara elsevierViewall">Changes in diet composition could improve microflora dysbiosis in CKD&#44; reduce uraemic toxin levels&#44; or restore intestinal mucosal permeability in CKD patients&#46;</p></li><li class="elsevierStyleListItem" id="lsti0080"><span class="elsevierStyleLabel">5&#46;</span><p id="par0255" class="elsevierStylePara elsevierViewall">The use of probiotics&#44; prebiotics or symbiotics opens an alternative in the treatment of intestinal dysbiosis associated with CKD&#44; and may play a role in slowing the progression of CKD and in preventing relevant associated complications such as mortality and cardiovascular risk&#46;</p></li></ul></p></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Conflicts of interest</span><p id="par0260" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare&#46;</p></span></span>"
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          "titulo" => "What are the microbiota and the microbiome&#63;"
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          "titulo" => "Gut microbiota in chronic kidney disease"
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              "titulo" => "Change in intestinal barriers in chronic kidney disease"
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              "titulo" => "Intestinal microflora as a cause of inflammation in chronic kidney disease"
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              "titulo" => "Microbiota and uraemic toxins derived from the intestine in chronic kidney disease"
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                  "identificador" => "sec0030"
                  "titulo" => "Intestinal production of uraemic toxins"
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                  "titulo" => "Biological and clinical consequences of the accumulation of uraemic toxins"
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              "titulo" => "Prevention and treatment of dysbiosis"
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            0 => "Chronic kidney disease"
            1 => "Gut microbiota"
            2 => "Dysbiosis"
            3 => "Uraemic toxins"
            4 => "Inflammation"
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          "palabras" => array:5 [
            0 => "Enfermedad renal cr&#243;nica"
            1 => "Microbiota intestinal"
            2 => "Disbiosis"
            3 => "Toxinas ur&#233;micas"
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    "resumen" => array:2 [
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The intestinal microflora maintains a symbiotic relationship with the host under normal conditions&#44; but its imbalance has recently been associated with several diseases&#46;</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">In chronic kidney disease &#40;CKD&#41;&#44; dysbiotic intestinal microflora has been reported with an increase in pathogenic flora compared to symbiotic flora&#46; An enhanced permeability of the intestinal barrier&#44; allowing the passage of endotoxins and other bacterial products to the blood&#44; has also been shown in CKD&#46; By fermenting undigested products that reach the colon&#44; the intestinal microflora produce indoles&#44; phenols and amines&#44; among others&#44; that are absorbed by the host&#44; accumulate in CKD and have harmful effects on the body&#46; These gut-derived uraemic toxins and the increased permeability of the intestinal barrier in CKD have been associated with increased inflammation and oxidative stress and have been involved in various CKD-related complications&#44; including cardiovascular disease&#44; anaemia&#44; mineral metabolism disorders or the progression of CKD&#46; The use of prebiotics&#44; probiotics or synbiotics&#44; among other approaches&#44; could improve the dysbiosis and&#47;or the increased permeability of the intestinal barrier in CKD&#46;</p><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">This article describes the situation of the intestinal microflora in CKD&#44; the alteration of the intestinal barrier and its clinical consequences&#44; the harmful effects of intestinal flora-derived uraemic toxins&#44; and possible therapeutic options to improve this dysbiosis and reduce CKD-related complications&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">La microflora intestinal mantiene una relaci&#243;n simbi&#243;tica con el hu&#233;sped en condiciones normales&#44; sin embargo&#44; su alteraci&#243;n se ha asociado recientemente con numerosas enfermedades&#46;</p><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">En la enfermedad renal cr&#243;nica &#40;ERC&#41; se ha descrito una disbiosis en la microflora intestinal con un aumento de la flora pat&#243;gena sobre la simbionte&#46; Adem&#225;s&#44; la permeabilidad de la barrera intestinal est&#225; aumentada&#44; lo que permite el paso de endotoxinas y otros productos bacterianos a la sangre&#46; La microflora intestinal&#44; mediante la fermentaci&#243;n de productos no digeridos que alcanzan el colon&#44; produce indoles&#44; fenoles&#44; o aminas&#44; entre otros&#44; que son absorbidos por el hu&#233;sped&#44; se acumulan en la ERC y tienen efectos delet&#233;reos sobre el organismo&#46; Estas toxinas ur&#233;micas generadas en el intestino y el aumento de la permeabilidad de la barrera intestinal en la ERC se han asociado a un aumento de la inflamaci&#243;n y el estr&#233;s oxidativo&#44; y est&#225;n implicados en diversas complicaciones asociadas a la ERC&#44; como la enfermedad cardiovascular&#44; la anemia&#44; las alteraciones del metabolismo mineral o la progresi&#243;n de la ERC&#46; El uso de prebi&#243;ticos&#44; probi&#243;ticos o simbi&#243;ticos&#44; entre otras aproximaciones&#44; podr&#237;an mejorar la disbiosis o el aumento de la permeabilidad de la barrera intestinal en la ERC&#46;</p><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">En este art&#237;culo se revisan la situaci&#243;n de la microflora intestinal en la ERC&#44; la alteraci&#243;n de la barrera intestinal y sus consecuencias cl&#237;nicas&#44; los efectos delet&#233;reos de las toxinas ur&#233;micas derivadas de la microflora intestinal&#44; as&#237; como las posibles opciones terap&#233;uticas para mejorar esta disbiosis y reducir las complicaciones de la ERC&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Guldris SC&#44; Parra EG&#44; Amen&#243;s AC&#46; Microbiota intestinal en la enfermedad renal cr&#243;nica&#46; Nefrolog&#237;a&#46; 2017&#59;37&#58;9&#8211;19&#46;</p>"
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                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Exposure&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Intestinal flora&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vaginal canal&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bifidobacterium</span>&#44; bacteroids&#44; <span class="elsevierStyleItalic">Lactobacillus</span>&#44; prevotella&#44; enterococci&#44; streptococci&#44; <span class="elsevierStyleItalic">Clostridiaeceae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Post-caesarean delivery&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus</span>&#44; <span class="elsevierStyleItalic">Corynebacterium Propionibacterium</span>&#46; Lower amount of <span class="elsevierStyleItalic">Bifidobacterium</span> and bacteroides&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Breast-feeding&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bifidobacterium</span>&#44; bacteroides&#44; <span class="elsevierStyleItalic">Lactobacillus</span>&#44; clostridia&#44; actinobacteria and firmicutes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Artificial breastfeeding&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Bacteroides&#44; clostridia&#44; <span class="elsevierStyleItalic">Enterobacteriaceae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Intestinal microflora in relation to perinatal events&#46;<a class="elsevierStyleCrossRefs" href="#bib0585"><span class="elsevierStyleSup">4&#44;5</span></a></p>"
        ]
      ]
      1 => array:8 [
        "identificador" => "tbl0010"
        "etiqueta" => "Table 2"
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          "leyenda" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">CKD&#44; chronic kidney disease&#59; ACKD&#44; advanced chronic kidney disease&#46;</p>"
          "tablatextoimagen" => array:1 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Intestinal tract&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Normal&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">CKD&#47;ACKD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Stomach&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">No change&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Helicobacter</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Duodenum&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Streptococcus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactococcus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Jejunum&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Enterococcus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Streptococcus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ileum&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Enterobacteriaceae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bacteroides</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Clostridium</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Bacterial fragments&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Colon&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Firmicutes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased&#58;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bacteroides</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Proteobacteria&#44;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Actinobacteria&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Enterobacteria&#44; <span class="elsevierStyleItalic">E&#46; coli</span>&#44;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Proteus&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Acinetobacter&#44; <span class="elsevierStyleItalic">Proteus</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Clostridium</span><br><span class="elsevierStyleItalic">Lactobacilli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Decreased&#58;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Prevotellaceae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus</span>&#44; <span class="elsevierStyleItalic">Bifidobacterium</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Fusobacterium</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Aerobic overgrowth of at least 100 times&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TM7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increase of <span class="elsevierStyleItalic">Clostridium perfringens</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Gut microbiota changes in CKD&#46;</p>"
        ]
      ]
      2 => array:9 [
        "identificador" => "tbl0015"
        "etiqueta" => "Table 3"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "fuente" => "<span class="elsevierStyleItalic">Source</span>&#58; Modified and extended from Biagi et al&#46;<a class="elsevierStyleCrossRef" href="#bib0650"><span class="elsevierStyleSup">17</span></a>"
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at3"
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          "leyenda" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">PAA&#44; phenylacetic acid&#59; IAA&#44; indole acetic acid&#59; IS&#44; indoxyl sulfate&#59; OAT&#44; organic acid transporters&#59; PC&#44; p-cresol&#59; PCS&#44; p-cresyl sulfate&#59; PTH&#44; parathyroid hormone&#59; RAS&#44; renin&#8211;angiotensin system&#59; ROS&#44; oxygen free radicals&#59; TMAO&#44; trimethylamine N-oxide&#46;</p>"
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              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Organ&#47;tissue&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Toxin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Effect&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Endothelium&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased senescence&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Induction of ROS and decrease in NO production&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS and PCS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased expression of ICAM-1&#44; MCP-1 and tissue factor&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased adhesion of leukocytes to the endothelium&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PCS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Inhibition of proliferation&#44; viability&#44; and repair&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IAA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased release of endothelial microparticles&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased endothelial permeability&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased ROS and inflammation and tissue factor expression&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Apoptosis of endothelial cell progenitors&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vascular smooth muscle fibre&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased proliferation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased production of tissue factor&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PAA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased ROS and expression of osteoblastic proteins&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased ROS production&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vessels&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased aortic calcification and stiffness&#44; expression of osteoblastic markers and OAT&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS and PCS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased cellular senescence&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TMAO&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased rolling and adhesion of leukocytes to the vessel&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Accelerated atherosclerosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Leukocytes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PCS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Activation of the oxidative burst&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased adhesion to the endothelium&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS and IAA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased expression of mononuclear cell tissue factor&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TMAO&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased expression of scavenger receptors in macrophages&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cardiac cells&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Hypertrophy of cardiomyocytes&#44; production of collagen by myofibroblasts and inflammation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Heart&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Myocardial hypertrophy&#44; cardiac fibrosis and oxidative stress&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Renal tubular cells&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PCS and IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Activation of RAS&#44; mesenchymal epithelial transition&#44; and fibrosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased expression of proinflammatory genes and cytokines&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PCS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased methylation of the klotho gene and fibrosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased tubular damage&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS and IAA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased expression of MCP-1&#44; ICAM-1&#44; TGF-&#946; and Smad3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased oxidative stress&#44; inhibition of proliferation&#44; increased expression of PAI-1 and NF-&#954;B activation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PCS&#44; IS&#44; IAA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Decreased cell viability&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Kidneys&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased fibrosis and angiotensinogen expression&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Decreased klotho expression and increased senescence&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IAA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased glomerulosclerosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TMAO&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased monocyte infiltration&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased glomerular sclerosis and interstitial fibrosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased tubulointerstitial fibrosis and collagen deposition&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Adipocytes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PCS and IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Increased insulin resistance&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Osteoclasts&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Alteration of differentiation and function&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Osteoblasts&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PCS and IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Decreased cell viability and cell proliferation and increased ROS production&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">IS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Decreases PTH receptor expression&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Promotes apoptosis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PAA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Inhibits proliferation and differentiation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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          "leyenda" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Cr&#44; creatinine&#59; PD&#44; peritoneal dialysis&#59; CKD&#44; chronic kidney disease&#59; HD&#44; haemodialysis&#59; IL&#44; interleukin&#59; P&#44; phosphorus&#59; CRP&#44; C-reactive protein&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Author and year&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Probiotic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Type of study&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Results&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Hida et al&#46;&#44; 1996<a class="elsevierStyleCrossRef" href="#bib1005"><span class="elsevierStyleSup">88</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Lebenin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Observational&#44; patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>25&#41;&#44; 4 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; Indicate in faeces and serum<br>&#8595; p-Cresol in faeces&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Simenhoff et al&#46;&#44; 1996<a class="elsevierStyleCrossRef" href="#bib1010"><span class="elsevierStyleSup">89</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus acidophilus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Observational&#44; patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>8&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; Dimethylamine<br>&#8595; Nitrosodimethylamine&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Takayama et al&#46;&#44; 2003<a class="elsevierStyleCrossRef" href="#bib1015"><span class="elsevierStyleSup">90</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bifidobacterium longum</span> JCM008&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Non-randomised&#44; placebo-controlled&#46; Patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>22&#41;&#44; 5 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; Indoxyl sulfate&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ando et al&#46;&#44; 2003<a class="elsevierStyleCrossRef" href="#bib1020"><span class="elsevierStyleSup">91</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bifidobacterium longum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Observational&#44; patients with CKD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#41;&#44; 6 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Reduction of the progression of CKD in patients with con Cr &#8805;4<span class="elsevierStyleHsp" style=""></span>mg&#47;dl or P<span class="elsevierStyleHsp" style=""></span>&#8805;<span class="elsevierStyleHsp" style=""></span>4<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Taki et al&#46;&#44; 2005<a class="elsevierStyleCrossRef" href="#bib1025"><span class="elsevierStyleSup">92</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bifidobacterium longum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Non-randomised&#44; placebo-controlled&#46; Patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#41;&#44; 12 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; Indoxyl sulfate&#44; homocysteine and triglycerides&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ranganathan et al&#46;&#44; 2009<a class="elsevierStyleCrossRef" href="#bib1030"><span class="elsevierStyleSup">93</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus acidophilus</span> KB31&#44; <span class="elsevierStyleItalic">Streptococcus thermophilus</span> KB27&#44; <span class="elsevierStyleItalic">Bifidobacterium longum</span> KB35&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Randomised&#44; double-blind&#44; crossover&#44; placebo-controlled&#46; Patients with CKD 3&#8211;4 &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>16&#41;&#44; 6 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">BUN<br>Uric acid<br>&#8593; Quality of life&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ranganathan et al&#46;&#44; 2010<a class="elsevierStyleCrossRef" href="#bib1035"><span class="elsevierStyleSup">94</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus acidophilus</span> KB31&#44; <span class="elsevierStyleItalic">Streptococcus thermophilus</span> KB27&#44; <span class="elsevierStyleItalic">Bifidobacterium longum</span> KB35&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Multicentre&#44; randomised&#44; double-blind&#44; placebo-controlled&#46; Patients with CKD 3&#8211;4 &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>46&#41;&#44; 6 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">BUN<br>&#8593; Quality of life<br>Insurance&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Miranda Alatriste et al&#46;&#44; 2014<a class="elsevierStyleCrossRef" href="#bib1040"><span class="elsevierStyleSup">95</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus casei shirota</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Randomised&#44; placebo-controlled&#44; patients with CKD 3&#8211;4 &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>30&#41;&#44; 8 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; Urea&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Wang et al&#46;&#44; 2015<a class="elsevierStyleCrossRef" href="#bib1045"><span class="elsevierStyleSup">96</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bifidobacterium bifidum</span> A218&#44; <span class="elsevierStyleItalic">Bifidobacterium catenulatum</span> A302&#44; <span class="elsevierStyleItalic">Bifidobacterium longum</span> A101&#44; <span class="elsevierStyleItalic">Lactobacillus plantarum</span> A87&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Randomised&#44; double-blind&#44; placebo-controlled&#44; patients in PD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>39&#41;&#44; 6 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; TNF-&#945;&#44; IL-5&#44; IL-6 and endotoxin<br>&#8593; IL-10<br>Residual preservation of kidney function&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Natarajan et al&#46;&#44; 2014<a class="elsevierStyleCrossRef" href="#bib1050"><span class="elsevierStyleSup">97</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Renadyl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Randomised&#44; double-blind&#44; placebo-controlled&#44; patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>22&#41;&#44; 8 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">No changes in quality of life<br>Tendency towards reduction of indoxyl glucuronide&#44; CRP and leucocyte count&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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          "leyenda" => "<p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">CRD&#44; chronic kidney disease&#59; GI&#44; gastrointestinal&#59; HD&#44; haemodialysis&#59; NO&#44; nonsignificant&#59; P&#44; phosphorus&#59; CRP&#44; C-reactive protein&#59; PCS&#44; p-cresyl sulfate&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Author and year&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Symbiotic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Study&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Results&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Nakabayashi et al&#46;&#44; 2010<a class="elsevierStyleCrossRef" href="#bib1055"><span class="elsevierStyleSup">98</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus casei shirota</span>&#44; <span class="elsevierStyleItalic">Bifidobacterium breve yakult</span> and galactooligosaccharides&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Observational&#44; patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>9&#41;&#44; 4 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; p-Cresol in plasma<br>Normalisation of bowel habits<br>Association of p-cresol and constipation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ogawa et al&#46;&#44; 2012<a class="elsevierStyleCrossRef" href="#bib1060"><span class="elsevierStyleSup">99</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Bifidobacterium longum</span> JBL01 and oligosaccharides&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Observational&#44; patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>15&#41;&#46; Control group patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>16&#41;&#44; 4 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; P levels that returned to baseline 2 weeks later&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pavan et al&#46;&#44; 2014<a class="elsevierStyleCrossRef" href="#bib1065"><span class="elsevierStyleSup">100</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Probiotic and prebiotic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Prospective&#44; open&#44; randomised&#44; placebo-controlled&#46; Patients with CKD 3&#8211;5 &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>24&#41;&#44; 12 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Reduction in the progression of CKD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cruz-Mora et al&#46;&#44; 2014<a class="elsevierStyleCrossRef" href="#bib1070"><span class="elsevierStyleSup">101</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus acidophilus</span>&#44; <span class="elsevierStyleItalic">Bifidobacterium lactis</span> and inulin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Double-blind&#44; randomised&#44; placebo-controlled&#46; Patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>18&#41;&#44; 2 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8593; Bifidobacteria in faeces<br>&#8595; <span class="elsevierStyleItalic">Lactobacilli</span> in faeces &#40;in the 2 groups&#41;<br>Improvements of GI symptoms&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Guida et al&#46;&#44; 2014<a class="elsevierStyleCrossRef" href="#bib1075"><span class="elsevierStyleSup">102</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus plantarum</span>&#44; <span class="elsevierStyleItalic">Lactobacillus casei</span> subsp&#46; <span class="elsevierStyleItalic">Rhamnosus&#44; Lactobacillus gasseri</span>&#44; <span class="elsevierStyleItalic">Bifidobacterium infantis</span>&#44; <span class="elsevierStyleItalic">Bifidobacterium longum</span>&#44; <span class="elsevierStyleItalic">Lactobacillus acidophilus</span>&#44; <span class="elsevierStyleItalic">Lactobacillus salivarius</span>&#44; <span class="elsevierStyleItalic">Lactobacillus sporogenes</span> and <span class="elsevierStyleItalic">Streptococcus thermophilus</span> inulin and resistant tapioca starch&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Randomised&#44; double-blind&#44; placebo-controlled&#46; Patients with CKD 3&#8211;4 &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>30&#41;&#44; 4 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8595; p-Cresol in plasma<br>With no changes in GI symptoms&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Viramontes-H&#246;rner et al&#46;&#44; 2015<a class="elsevierStyleCrossRef" href="#bib1080"><span class="elsevierStyleSup">103</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus acidophilus</span> and <span class="elsevierStyleItalic">Bifidobacterium lactis</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>prebiotic &#40;inulin&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Randomised&#44; double-blind&#44; placebo-controlled&#46; Patients in HD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>42&#41;&#44; 2 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Tendency to diminish levels of CRP and TNF-&#945;&#46; Improvement of GI symptoms&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Rossi et al&#46;&#44; 2014<a class="elsevierStyleCrossRef" href="#bib1085"><span class="elsevierStyleSup">104</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Lactobacillus</span>&#44; bifidobacteria and <span class="elsevierStyleItalic">Streptococcus</span> generates<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>inulin&#44; fructooligosaccharides and galactooligosaccharides&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Randomised&#44; double-blind&#44; crossover&#44; placebo-controlled&#46; Patients with CKD 4&#8211;5&#44; 6 weeks with a washout of 4 weeks&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Decreased PCS&#44; decreased NS of IS<br>Increased bifidobacteria and decreased ruminococcaceae in faeces&#46; No changes in oxidative stress or inflammation markers and slight increase in albuminuria&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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          "en" => "<p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Clinical studies with symbiotics in patients with CKD and their effects&#46;</p>"
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Article information

ISSN: 20132514
Original language: English

DOI:10.1016/j.nefroe.2017.01.017

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