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Recent studies reveal a potential contribution of intestinal microbes in the expression of certain human cardio-metabolic diseases. The mechanisms through which intestinal microbiota and/or their metabolic products alter systemic homoeostasis and cardio-metabolic disease risks are just beginning to be dissected. Intervention studies in humans aiming to either selectively alter the composition of the intestinal microbiota or to pharmacologically manipulate the microbiota to influence production of their metabolites are crucial next steps. The intestinal microbiome represents a new potential therapeutic target for the treatment of cardio-metabolic diseases.
The human gut microbiome is a complex ecosystem, which harbours a staggering number of microbes—∼100 trillion—representing an estimated 5000 species.1 The collective genome of gut microbiota, termed the metagenome, contains close to 5 million genes. The recent development of high-throughput sequencing makes it feasible to examine the metagenome derived from stool samples, allowing for comprehensive analyses of intestinal microbiota composition. When metagenomic analysis is combined with clinical phenotypic data, it is known as a metagenome-wide association study.2 Despite the diversity between individuals, studies with serial stool collections show that the unique core gut microbiota composition of an individual remains remarkably stable over time,3,4 pointing towards intestinal bacteria as a potential risk factor for human cardio-metabolic disease. Indeed, in recent years the gut microbiome has increasingly been acknowledged as a novel contributor affecting host metabolism. Mounting evidence in mice and humans is accumulating showing that gut microbiota are linked with both cardiovascular health and the onset and development of metabolic disorders, such as type 2 diabetes mellitus (T2DM) and obesity.5 In this review, we will describe how specific changes in intestinal microbiota can affect host metabolism, and how these findings may give rise to novel therapeutic targets for obesity, diabetes, and cardiovascular disease (CVD).
Gut microbiota in obesity and type 2 diabetes mellitus
The prevalence of obesity and T2DM is increasing at an alarming pace worldwide, making obesity a primary public health concern. The pathophysiology of obesity, insulin resistance (IR), and T2DM are complex, and involve a combination of both genetic and environmental factors. Ingestion of food is a major environmental exposure, and it is processed through the filter of the intestinal microbial community. It is thus not surprising that there is growing appreciation that intestinal microbiota contribute to how a given individual experiences this environmental exposure, and accordingly, cardio-metabolic phenotypes.6 The human gut microbiota benefits the host in numerous ways, playing a pivotal role in both innate immune and metabolic functions. Gut microbiota can also provide functions not intrinsically available to humans, such as the synthesis of vitamin K, or biotransformation of other nutrients. Intestinal microbiota enables their host to extract calories from otherwise indigestible components of our diets, such as plant polysaccharides. It is suggested that gut microbiota also plays a role in harvesting energy from food and controlling energy homoeostasis, implicating gut microbiota as a potential contributor to the development of obesity and T2DM.7
Recent studies in both mice and humans show that an obese phenotype is associated with changes in the intestinal microbial composition compared with lean counterparts. Turnbaugh and colleagues8,9 first demonstrated that the obesity phenotype was a transmissible trait by showing caecal microbiome transplantation into germ-free mice (who have sterile intestines) resulted in efficient transmission of the obesity phenotype into recipients. The mechanism(s) involved appear to involve more efficient energy harvest from food with the obesity-related caecal microbiome. Bäckhed et al.10 have extended these observations and reported that germ-free mice are relatively protected from obesity following the institution of a Western high-fat sugar-rich diet. Conversely, colonization of germ-free mice with caecum-derived microbiota from normal mice (called 'conventional' because they are housed in conventional cages) resulted in a significant increase in the total body fat content without any change in dietary caloric intake.8 A potential mechanism for the more efficient energy harvest from food is suggested to occur via intestinal production of short-chain fatty acids (SCFA). Intestinal microbes ferment non-digestible carbohydrates in order to yield energy, leading to the production of SCFA in the form of acetate (60%), propionate (25%), and butyrate (15%)9; however, the concentration of faecal SCFA is highly dependable on the amount of daily dietary fibre intake.5 Short-chain fatty acids are readily absorbed in the plasma of the host via the intestinal epithelium, and thus can serve as an energy source, predominantly via metabolism in the liver.9,10 The role for intestinal bacteria in the production of SCFA is clearly demonstrated by the observation that germ-free rats and mice are characterized by reduced levels of intestinal SCFAs with a concomitant increase in faecal excretion of non-digestible carbohydrates.6 Moreover, both mouse models (ob/ob) and human disease states (e.g. metabolic syndrome) characterized by IR also tend to have decreased intestinal SCFA levels with a concomitant reduced excreted energy content in their faeces.9,11,12 The complexity of the relationship between gut microbiota composition and human metabolism is attested to by the observation that not only composition, but also relative proportions, as well as functional capacity (e.g. SCFA production) of bacteria, may determine the propensity towards obesity and IR.
Research into the role of gut microbiota in obesity and IR in humans has focused on the relative proportions of specific bacterial taxa, predominantly Bacteroidetes and Firmicutes.11–16 In this respect, two recent landmark papers elegantly demonstrated the diagnostic and clinical value of faecal microbiota composition in the development of obesity-associated IR and T2DM.17,18 Both studies also showed that T2DM subjects were characterized by a reduction in the number of Clostridiales bacteria, which produce the SCFA butyrate (e.g. Roseburia species and Faecalibacterium prausnitzii). Hence, these studies lend support to a role of butyrate-producing bacteria as regulators of human glucose and lipid metabolism, possibly via alterations in intestinal permeability driving chronic inflammation.5 Whereas Qin et al.17 reported an enrichment of Proteobacteria predicting T2DM; Karlsson et al.18 identified an enrichment of Lactobacillus gasseri and Streptococcus mutans (abundant in the mouth and upper intestinal tract) as a predictor of T2DM. Potential causality of these bacterial strains and T2DM is supported by the compositional changes of faecal microbiota, particularly of the SCFA butyrate-producing strains, following both faecal transplantation of lean donors as well as a gastric bypass procedure (Roux-en-Y gastric bypass),12,19,20 with both of these interventions being associated with a marked improvement of IR.
Gut microbiota, inflammation, and lipid metabolism
The majority of obese subjects will eventually develop chronic (visceral) adipose tissue inflammation leading to production of pro-inflammatory cytokines21 and subsequent IR.22,23 Recent data have shown that variations in intestinal microbiota were associated with pro-inflammatory changes in adipose gene expression.24 In fact, several other lines of evidence point towards a direct relation between the intestine and visceral adipose tissue inflammation, as the macrophage infiltration (crown-like cells) in adipose tissue was directly correlated with a pro-inflammatory gene expression profile.25,26 As macrophages are part of our innate immune system, these findings imply that translocation of intestinal bacteria could play a role in the development of chronic inflammatory state. The innate immune system is capable of sensing various types of bacterial components via pattern recognition receptors, such as toll-like receptors (TLRs). It is known that alterations in the gut microbiota composition drive activation of TLRs by bacterial endotoxins [e.g. lipopolysaccharide (LPS)] and subsequent obesity.27 Thus, chronic low-dose LPS exposure in mice resulted in hepatic IR, hepatic steatosis, adipose tissue macrophages infiltration, dyslipidaemia, fasting hyperglycaemia, hyperinsulinaemia, and eventually obesity. Similar changes were seen in mice fed a high-fat diet,28,29 whereas mice deficient in TLR4 (the receptor that is directly involved in LPS binding) were, however, completely resistant to the development of these high-fat-diet-induced changes.27 It should be noted, however, that besides LPS, the intestinal microbiota is a source of many other pro-inflammatory bacterial, capsule-derived compounds (e.g. peptidoglycans, lipoproteins, and flagellins) that are able to activate innate inflammatory pathways.30,31 Recent murine data have shown that SCFAs are indeed involved in intestinal cell homoeostasis thus preventing increased permeability.32,33 Combined with the afore-mentioned bacteria-derived SCFAs affecting both intestinal permeability as well glucose and lipid metabolism,5 these observations provide the basis for a bi-directional cross-talk between the intestinal microbiota SCFA metabolism and bacterial translocation in the development of chronic adipose tissue inflammation and IR.
Gut microbiota and atherothrombosis
Cardiovascular disease represents the leading cause of mortality and morbidity in Western societies. Moreover, obesity, non-alcoholic fatty liver disease, and metabolic dyslipidaemia are associated with a further increase in CVD, independent from classic risk factors.34 Chronic low-grade inflammation, induced by intestinal microbiota-derived endotoxaemia, has been suggested as a potential contributing factor for both obesity and atherosclerosis.35 Obesity and chronic inflammation are associated with hypercoagulability, presumably as a result of both increased production of pro-coagulant vitamin K-dependent clotting factors (II, VII, IX, and X), as well as adipose tissue inflammation-associated reduction in fibrinolytic capacity.36 Considerable evidence shows that endotoxaemia, which is associated with enhanced intestinal bacterial translocation, elicits activation of the coagulation and inflammatory cascades.37 Solid evidence for the effect of the intestinal microbiota in hypercoagulability is however limited. A study in germ-free mice showed that gut microbiota can regulate tissue factor level expression in the intestinal microvasculature,38 but data are lacking in humans. Subsequent papers suggested that intestinal translocation can be facilitated via co-transport on dietary fat-derived chylomicrons promoting an inflammatory response,39,40 whereas parenteral infusion of lipids did not convey this effect.37 Increased levels of plasma endotoxin have also been linked to the development of CVD,41 and repetitive endotoxin injections in both mice and rabbits are reported to accelerate cholesterol-induced atherosclerosis.35,42,43 More specific, translocation of intact bacteria and subsequent captivation by vascular macrophages was also suggested in humans reporting bacterial DNA from the Porphyromonas gingivalis in 79% of the analysed carotid atherosclerotic plaques.44,45 Currently, only one prospective randomized controlled trial with antibiotic treatment in humans was executed and failed to reduce cardiovascular event rates.46 However, whether or not the chronic antibiotics exposure resulted in expansion of alternative resistant bacterial strains is unknown and moreover bacterial resistance to specific antibiotics precludes potential use in the clinic of long-term oral antibiotic treatment.
Recent studies identify a new pathway through which gut microbiota participate in CVD pathogenesis. In the setting of specific dietary nutrients characterized by a trimethylamine group [e.g. choline, phosphatidylcholine (PC), and carnitine], gut microbiota are shown to participate in the formation of a pro-atherogenic compound called trimethylamine-N-oxide (TMAO).47,48 Identified initially though metabolomics studies comparing analytes in plasma from subjects who experience a heart attack, stroke, or death in the 3 years following blood collection vs. age- and gender-matched subjects who do not experience a cardiovascular event, subsequent animal model and human clinical studies have shown that TMAO is directly related to atherosclerosis. Trimethylamine-N-oxide was shown to directly influence the propensity of macrophages to accumulate cholesterol and form foam cells in atherosclerotic lesions, as well as to alter cholesterol and sterol metabolism within multiple compartments including the liver and intestines49 Further, systemic levels of TMAO in several clinical cohorts have now been shown to independently associate with incident risks of heart attack, stroke, and death in both primary and secondary prevention subjects.47,50–51 Trimethylamine-N-oxide is produced in a two-step process, starting with degradation of dietary trimethylamines like free choline, PC, or carnitine by specific intestinal bacterial strains into the precursor trimethylamine (TMA). Trimethylamine is then efficiently absorbed into the circulation and converted by one or more members of the hepatic flavin monooxygenase (FMO) family, in particular FMO3, into TMAO.50,51 Flavin monooxygenase 3 is a known enzymatic source for TMAO in humans, based on the recent recognition of the aetiology of an uncommon genetic disorder called trimethylaminuria (also known as fish malodour syndrome). Patients with this metabolic condition are characterized by a genetically impaired capacity to convert TMA into TMAO. Studies using germ-free mice or mice treated with broad-spectrum antibiotics, suppressing the intestinal flora, demonstrate an essential role for gut microbiota in TMA and TMAO formation.47,50 Moreover, conventionalization of germ-free mice results in an increase and recovery of the plasma levels of TMAO, indicating towards an obligate role for intestinal microbiota in the generation of TMA from dietary choline including eggs, milk, liver, and red meat.49 As noted, another source of TMAO is dietary l-carnitine (a TMA structure similar to choline). Carnitine is an abundant nutrient in red meat. Recent studies show that gut microbiota also play a role in TMAO production from dietary l-carnitine in both mice and humans. Moreover, a strong correlation is observed between increased plasma concentrations of l-carnitine and TMAO levels in relation to increased risk of incident major adverse cardiac events in subjects, even following multivariate analyses.49,50 Of note, a recent meta-analysis suggested that the use of l-carnitine in patients immediately following an acute myocardial infarction was associated with a significant reduction in lethal ventricular arrhythmias and development of angina.52 However, review of the meta analyses demonstrates concerns about its validity, since 11 of the 13 studies included in the meta-analyses failed to show clinical benefit with short-term carnitine supplementation, including the two largest trials, one of which had over 1000 subjects. Moreover, the 2 of 13 studies that did show a benefit were each small (<100 subjects), making the positive results hypothesized in the meta-analyses difficult to reconcile with negative placebo-controlled trial results of the major studies included in the analyses. Regardless, it should be noted that the relationship proposed between dietary carnitine and atherosclerotic CVD pathogenesis refers to a process that takes decades to develop (atherosclerosis), and which appears at least in part to exert its pro-atherogenic effect via alterations in cholesterol and sterol metabolism. In contrast, the carnitine supplementation studies examined thus far have only focused on short-term effects in the post-myocardial infarction setting, where alternative phenotypes such as arrhythmias have been the major ones examined.
Carnitine is almost exclusively found in red meat. Therefore, examination of epidemiology studies examining meat ingestion and cardiovascular risks is of interest. Numerous large-scale studies have been performed. Perhaps one of the largest and most carefully performed is the results recently reported from composite of two prospective studies, from the Health Professionals Follow-up Study (n = 37 698; followed 1986–2008) and women from the Nurses' Health Study (n = 83 644; followed 1980–2008) who were free of CVD and cancer at baseline, and for whom dietary intake was assessed by validated food frequency questionnaires every 4 years53 For each 1-serving-per-day (3 oz.) of meat over the duration of follow-up, which varied between 20 and 28 years on average for the two studies, a 13% increase in all-cause mortality for unprocessed red meat, and 20% increase in mortality for processed red meat was observed. In contrast, however, in a very recent similar pooled analyses of eight Asian prospective cohort studies, higher red meat consumption was reported to be inversely associated with cardiovascular mortality.54 It also should be noted that another source of TMAO is seafood, including some but not all fish.55 Multiple epidemiological studies have shown beneficial effects of regular seafood consumption on the incidence of CVD,56 making recommendations about intake of specific dietary nutrients or meats/proteins and cardiovascular risks premature at present. Interestingly, in animal model studies, dietary TMAO directly augmented atherosclerosis, as did dietary choline or carnitine in the presence of intact gut microbes (and hence formation of TMAO). Moreover, both TMAO and choline or carnitine with intact gut microbiota and TMAO formation significantly inhibited the reverse cholesterol transport pathway, suggesting a plausible mechanistic explanation for the tight associations noted between TMAO, choline, and carnitine and incident cardiovascular risks.51 Also, (small) intestinal transit time of choline and carnitine comprising food particles might be impaired in obese subjects57 thus resulting in different TMA levels in the colon. In conjunction with the effect (suppression) on bile acid synthesis and composition by the TMAO pathway, this demonstrates the multiple distinct mechanistic links between TMAO producing diet—microbe pathways and atherothrombotic risk. Although a causal role of l-carnitine in CVD disease in humans is provocative, and requires further examination, discovery of this new pathway suggests that targeting the gut microbiota, either through efforts to change their composition, or through targeted small molecule or molecular approaches, may serve as a novel therapeutic for the prevention or treatment of CVD.
Intestinal microbiota as future diagnostic and therapeutic targets
The faecal intestinal microbiota is increasingly regarded an important participant in the development of obesity and its comorbidities. As currently available evidence is mainly based on in vitro and relatively small animal and human cohort studies, further work is required in order to dissect how altered intestinal microbiota can be used in a diagnostic or therapeutic setting. For example, long-term, prospective, and multi-ethnic cohort studies are needed to determine whether there are in fact substantial differences in predictors of faecal sample-derived microbiota between ethnic groups taking diet and gender into account, as both factors can influence the composition of the gut microbiota.6 Moreover, as intestinal uptake of dietary lipids and carbohydrates driving human obesity are mainly taking place in the small intestine5 rather than the distal colon, it is important to define the correlation between small intestinal microbiota composition in relation to that of the faecal sample. Moreover, environmental factors (e.g. composition of diet) introduce profound changes in intestinal microbiota composition,58 and the logistics of faecal sample (non-frozen) transport, handling and DNA isolation also influence results.59 A role for quantifying proportions of bacterial strains in faeces for use as a diagnostic tool and in cardiovascular risk prediction is thus neither recommended nor likely to provide useful clinical information in the near term future. In line, using faecal transplantation studies as a working tool might enable us to identify causally involved intestinal bacterial strains in human cardio-metabolism which may give rise to the development of novel, microorganism-based intervention strategies. Although promising, the links of specific gut microbial taxa with CVD phenotypes are associative, which makes it too early to induce real changes in clinical practice of cardiovascular risk assessment.18
In contrast to quantifying bacterial species within faeces, perhaps a more promising and clinically viable diagnostic is the quantification of blood levels of a microbial-dependent product that is biologically active and at least in animal models promotes atherosclerosis (i.e. TMAO). Indeed, while results are relatively new, those reported suggest great promise for TMAO as a strong cardiovascular diagnostic or prognostic marker. In multiple large clinical studies, plasma levels of TMAO were observed to predict prospective CVD risks, including incident heart attack, stroke and death over the ensuing 3-year follow-up period. The prognostic value of TMAO remained robust following multivariable adjustments for traditional risk factors and other cardiovascular diagnostic markers.47,49,50 Indeed, in one study (n = 4007 subjects), addition of TMAO to traditional risk factors was shown to substantially reclassify incident risks for major adverse cardiovascular events, and significantly augment prognostic value.49 Clinical studies thus far with TMAO have all been in relatively higher risk populations, and not within community-based cohorts with longer-term follow-up. Further studies are needed to determine the generalizability of the results with TMAO as a prognostic marker in alternative clinical cohorts, as well as whether plasma TMAO levels can either serve as a means of monitoring dietary efforts, or are modifiable with alternative interventions (Figure 1).
Recent studies implicate involvement of gut microbiota in development of complex metabolic phenotypes including obesity, IR, and CVD. In this active research area of cardio-metabolism, there are numerous research programmes evaluating the mechanisms by which intestinal microbiota alter human glucose, lipid metabolism, and alternative CVD relevant phenotypes. In animal model studies, transmissibility of traits and causality of gut microbiota as a contributor has been established in some studies. In human studies thus far, however, published studies are associative. There is a need to apply Koch's postulates (originally used for infectious disease) to differentiate association from causality in cardio-metabolic disease states. Further research is needed in order to allow us to use the gut microbiota composition and modulation as novel diagnostic or therapeutic strategies. Most importantly, experimental findings on correlations between microbial communities and specific cardio-metabolic phenotypes should be corroborated by more detailed mechanistic investigations, and ideally, therapeutic intervention studies in humans. We have yet to see that 'the time has come' for gut microbiota compositional manipulation or targeting by drugs for therapeutic gain in cardio-metabolic disease. However, the highly promising studies that have arisen over the past few years argue that not too long into the future, we may yet 'drug the microbiome' as a target for preventing or treating human diseases and promoting cardiovascular health.2
S.V. is supported by the 2012 EU RESOLVE consortium (grant number FP7-EU 305707); E.S.G.S.: grant from CVON (GENIUS) (number CVON2011-19). S.L.H. is supported by National Institutes of Health (NIH) and Office of Dietary Supplement grants R01 HL103866, and NIH grant P20 HL113452. He is also partially supported by a gift from the Leonard Krieger Fund.
Conflict of interest: S.L.H. reports being named as co-inventor on pending patents held by the Cleveland Clinic relating to cardiovascular diagnostics. S.L.H. also reports he has the right to receive royalty payments for inventions or discoveries related to cardiovascular diagnostics from Abbott Laboratories, Cleveland Heart Lab, Inc., Frantz Biomarkers, Liposcience, Inc., and Siemens. S.L.H. reports he has been paid as a consultant by the following companies: Cleveland Heart Lab, Inc., Esperion, Liposciences, Inc., Merck & Co., Inc., Pfizer, Inc., and Proctor & Gamble. S.L.H. reports he has received research funds from Abbott, Cleveland Heart Lab, Esperion and Liposciences, Inc., and Proctor & Gamble.
Supplementary data
The gut microbiome as novel cardio-metabolic target - the same pattern of bacteria for everybody?
Anja Sandek, MD (1) Stephan von Haehling, MD, PhD (1) Stefan D Anker, Prof, MD, PhD (1, 2)
(1) Division of Applied Cachexia Research, Department of Cardiology, Charite, Campus Virchow-Klinikum, Berlin, Germany (2) Department of Cardiology, University Goettingen, Goettingen, Germany
Address for Correspondence: Anja Sandek Division of Applied Cachexia Research Department of Cardiology University Hospital Charite Campus Virchow-Klinikum Augustenburger Platz 1 13353 Berlin Germany Phone: +49 (0) 30 450 55 33 99 Fax: +49 (0) 30 450 55 39 51 Email: firstname.lastname@example.com
Vinj? et al. have recently described how specific changes in intestinal microbiota can affect host metabolism, and how these findings may give rise to novel therapeutic targets for obesity, diabetes, and cardiovascular disease ( ). The gut microbiome is an interesting field as an increasing body of evidence suggests its correlation to metabolic and cardiovascular diseases. In their article, Vinj? et al. elucidate possible therapeutic strategies aimed at this very complex ecosystem of the human gut microbiome. The authors suggest faecal transplantation studies as a working tool to "...identify causally involved intestinal bacterial strains in human cardio-metabolism..." and to develop novel, microorganism based therapies. This strategy of faecal transplantation is intriguing. However, neither normal mice nor human beings are germ free. In contrast, there is a huge variability in the composition of gut bacteria which furthermore restores to this highly individual pattern in each human being within a couple of weeks even after antibiotic therapy. The genetic background of obesity and atherosclerosis we are facing and the highly individual pattern of gut microbiom lead to the assumption that we might not handle only with an intestinal dyscolonization e.g. in early childhood that might be simply treated by faecal transplantation but rather with a genetically determined highly individual intestinal mucosal pattern that only allows a specific composition of gut microbiom. Therefore, the results from germ free mice may have to be analysed with caution and have to be confirmed in a real world scenario. The comment of the authors themselves, that gut microbiota composition of an individual remains remarkably stable over time, underlines this and questions easiness and sustained success of faecal transplantation.
Furthermore, the perfusion of the intestinal wall may interfere with resided intestinal bacteria, especially with those adherent to the mucosa. In chronic heart failure e.g., a common cardiovascular comorbidity, increased sympathetic activity leads to a redistribution of blood flow away from the splanchnic circulation. In these patients, a decrease in intestinal mucosal pH has been observed at low levels of exercise indicating intestinal ischemia ( ). We have reported a higher concentration of juxtamucosal intestinal bacteria that have furthermore a higher extent of adherence to the mucosa in patients with heart failure as compared to control subjects on biopsies taken during sigmoidoscopy (2). As an inadequate mucosal perfusion is known to increase intestinal mucosal permeability ( ) and to be a potent activator of bacterial invasiveness, the capacity of the microbiom as the biggest source of proinflammatory lipopolysaccharide (LPS) has to be considered. The mechanisms, that prevent luminal bacteria from entering the circulation include a mucus layer, an epithelial cell barrier, immune cells within the intestinal mucosa, antimicrobial peptides, immunoglobulin A and last but not least the competition with other bacteria. The latter might become severely disturbed by faecal transplantation that may result in inappropriate intestinal inflammation the investigators should be aware of and screen for in faecal transplantation models. Therefore, a careful selection of the transplanting strains is commanded and possible interactions among the gut microbiom have to be taken into account in order to make sure that the LPS profile of the host's microbiom remains stable or even becomes better as several groups of patients (e.g. with heart failure) are at risk for bacterial translocation and subsequent both local intestinal and systemic inflammation.
For this purpose, it seems helpful to analyse not only stool bacteria as these do not necessarily have to reflect the composition of juxtamucosal species, but also to include the analysis of juxtamucosal bacterial strains adherent to the mucosa on biopsies into faecal transplantation models. In the article by Vinj? et al. the beneficial metabolic effects of faecal flora transplantation of lean subjects for changes of fat and glucose absorption, an improvement in insulin sensitivity, less systemic inflammation and therefore potentially less atherosclerosis are pointed out. However, this raises the question what gut microbiom may be useful for patients suffering not from obesity associated with inflammation but from cachexia in chronic diseases, such as cardiac, renal and pulmonary cachexia, all associated with systemic inflammation, too. This indicates the need for research into an individualized modulation of gut microbiom by well balanced distinct patterns of bacteria in the patients with cardiovascular diseases. Vinj? et al. refer to an enrichment of specific stool bacteria such as Proteobacteria, distilled from associative faecal metagenomic studies ( ), Lactobacillus gasseri and Streptococcus mutans that would have been able to predict type 2 diabetes mellitus (1). Finally, the authors claim "...potential causality of these bacterial strains and..." type 2 diabetes mellitus that would be supported "...by the compositional changes of faecal microbiota following faecal transplantation of lean donors.". This restriction to very few species that may be responsible for health and disease is tempting. However, it does not reflect the huge variability of bacteria within the ecosystem gut. In their conclusion, the authors express the "...need to apply Koch's postulates (originally used for infectious disease) to differentiate association from causality in cardio- metabolic disease states.". However, the value of Koch's principles might be seriously limited in case of polymicrobials. The polymicrobial community can not be grown elsewhere by transfection of single strains and the investigation of isolated microorganisms does not explain how the polymicrobial community functions or why it can flourish under conditions, which are deadly for each of the constituents ( ). Their composite structure in relation to propagation and response to environmental challenges need to be monitored and studied in order to understand polymicrobial balances and last but not least infections in this very promising active research area of cardio-metabolism.
Conflict of Interest:
None declared
Dr. Sandek and colleagues;
We do not disagree with Dr Sandek and colleagues that some more work is needed to optimally understand how to leverage "drugging of the microbiome" for the treatment of cardiometabolic diseases. Moreover, we agree that germfree mice do not reflect normal physiology. In line, we agree that next to fecal sample microbiota analyses one should also take adhering mucosal bacteria into account; we already combine fecal microbiota analyses with intestinal biopsies in previous fecal transplant studies (Vrieze et al, Gastroenterology 2012). We however believe that the current data argue that this is an important new frontier, and that the "time has come" to pursue therapies that target the microbial community. No doubt therapies will be developed for varied metabolic diseases and changes in phenotype where gut microbiota are implicated through a variety of approaches, depending on the target, using methods ranging from fecal transplantation, probiotics, prebiotics, to small molecule drugs.
Best Regards,
Stanley L Hazen, MD, PhD; Sarah Vinje; Erik Stroes; Max Nieuwdorp
Conflict of Interest:
None declared


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Top 10 Worst Singers Ever
The Contenders: Page 6
Why her? She is creative and interesting. Take her off the list. She is talented.
I love her! She was on T.V.!
She should not be on this list!
I think almost every thing in this list Is very messed up
I hate the list why is one of the best singer also in the
Worst one 💩
TAKE him OFF THIS LIST, stop hating on Shawn guys. He's talented as hell. He writes good songs like Something Big and tries to inspire teens and prevent suicide. He's a GOOD singer with a sweet voice and nice emotion. And he's down to earth. Shawn, I'll forever be a part of the #MENDESARMY because you inspire teen boys like me. Just keep your healthy down to earth attitude and don't be like Bieber. love you Shawn. Haters need to go away
He sucks. All of the pop artists we have today suck. I could sing like him, my cat could sing like him. just with a little bit of autotune. But this wannabe uses a lot of autotune. I heard him sing once at a Taylor Swift concert. He was terrible. Heck he can't even do his own concerts!
All autotune and no talent. His is songs are boring and that picture makes me want to puke.
Why is he all the way down HERE? He's TERRIFYING! His videos, lyrics, and songs are nasty as hell.V 7 Comments
This hack can't rap to save his life
She sounds like Kermit the frog
She is a good singer
Voice is way too high for me.
Goat😂😂😂 she sounds so much like a goat, and then goes and plays a goat on zootopia, I love those producersV 12 Comments
Her singing makes Rebecca Black's singing sound like Barbra Streisand. She is absolutely terrible and the worst singer (opera or otherwise) of all time. These people obviously have never heard Jenkins sing if they think that Justin Bieber is the worst singer ever. Otherwise, she would have been number one.
Look her up on YouTube, and I DARE you to say that she's a better singer than Justin Bieber. I dare you to say she's a better singer than anyone. If everyone who voted on this list heard her voice, she would be number one in the rankings.
Hearing her voice should make obvious she must be in top 3 at least.
Oh my goodness she hurts my ears listening to her. No wonder her movie is a comedy.V 1 Comment
ARE YOU KIDDING ME?! No way... Paul is one of the greatest singers in the world how he can be on this list?
I'll bet Justin Bieber or one of his stupid fans put him on here. Same with Lennon, Michael Jackson, Mercury, and Presley. McCartney and all of the artists I just mentioned minus Bieber are awesome! Bieber is the worst singer ever and deserves the top spot. Long live Paul! Long live John! Long live the Beatles! Down with Bieber and One Direction!
WHAT?! HOW is Paul McCartney on this list?
I thought this was a list of the worst singers ever. Not the people who changed music.
He is one of like 3 of the best bandV 23 Comments
Why is Tom Jones on this list? He is awesome!
He is reasonable if you are into pensioners music
This list is a joke when John Lennon is included. The guy was a great singer and song writer who sadly died way too young. Whoever put him on this list is a idiot.
I love john lennon, he was my great grand uncle so no this list is stupid!
I'm done with humanity. John Lennon is on a worst singers list, I've scrolled through 200 and I haven't found the only true deserver of the worst singer of all time, Ross Lynch. Ross Lynch is an absolute disgrace to singers.
None of the Beatles are badV 17 Comments
Are you kidding me? Hayley's a great singer even if she isn't the greatest.
Who put her on this list, she's a phenomenal singer and really pretty. You haters may not see it but she can probably sing better than you and has an awesome sense of spunk.
She is amazing. I love her band, Paramore
I don't like how I always get attacked for not liking Paramore. I don't like them AT ALL. Hayley gets all the attention, and her voice isn't special.V 8 Comments
Her husky are too loud... She can't sing.. Bad voice.. Najwa latif is better than you
She can't sing
She was very overrated
The worst singer ever
She is the worst singer in this world
She can't sing
WHY IS JARED LETO ON THIS LIST?!? He's an amazing singer and he has at least a 3 octave vocal range! This list is wrong, wrong, wrong!
Let me tell you why Jared is in thi list. He only sings thanks to computers on recording studios. When he performs at the concerts just sings
Take him off! He's an amazing live performer!
NO! Bono is so awesome! He has such a beautiful voice.
Who ever put him on the list should be given to Saran at once
Lol he was on south park as a villain
Bono is crap, it's a fact and South Park proved it. - MorbidCannibalSlayerV 3 Comments
Why is M.Shadows on here?! He's on of the greatest singer I've ever heard. Everyone who says a7x sucks or he sucks must listen to rap or pop or must be living under a rock.
What people do not know music, best voice ever. Great lyric writer amazing voice.
And I'm so tired of you
One of the best metal singers of today. NOT an emo you bitch.V 2 Comments
This guy can barely make coherent syllables, let alone say anything that sounds remotely like English!
Hey Desiigner really is the king of rap...oops forgot to add a "C" at the beginning of 'rap'. - Spark_Of_LifeV 1 Comment
How do people like this excuse of a rapper?V 1 Comment
This guy tops the list here. He is a wannabe who singing should be considered a crime. Google him and see for yourself.
Wow, how do they even allow such awful music on the internet. And a pedophile no less... yes it's true
I Googled this guy. I found a criminal record. Man his face is ugly and his vocals are the equivalent of chalk scraping on a blackboard. Not for me. I can see why he's here. I bet he hits the top of the list soon. No honor being on this list. I wouldn't want my name here.
Should be #1 on this listV 3 Comments
Why is he even on the list! He can really play the guitar, but not the best singer
He is a jerk for leaving Katy PerryV 1 Comment
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FilterChicago, IL
Great work life balance and great culture (in 579 reviews)
Great place to start your career (in 238 reviews)
Long working hours typical of Big 4 (in 1776 reviews)
The only i found is lack of work life balance (in 1695 reviews)
I have been working at EY full-time (More than 5 years)
- Performance-driven environment, rewards high performers
- Work with talented individuals and teams
- Incredible parental leave policy
- Variety in clients, industries, and projects
- heavy travel which can be a pro, depending on what you want
I have been working at EY full-time (More than 3 years)
The people are awesome. Great exposure to key client stakeholders, and great depth of project work.
Behind technologically. Red tape over getting some things done that is not always clearly defined.
Advice to Management
Practice what you preach (Once held a session on why to stay with EY, when all of senior management were experienced hires)
I have been working at EY full-time (Less than a year)
- Meet a lot of good people
- Exposure to a variety of clients depending on division
- Flexibility
- Pay and benefits can be better
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I worked at EY full-time (More than a year)
Good brand name. Good training ground for consulting skills. Training center is good. Large number of practices though difficult to move within them.
Not ethical in how they bill or the value they deliver. Mostly talk.
Example - on a large healthcare insurance, EY had placed 300 consultants. Most had no or minimal work. Lot of busy work was created by EY just to bill and rip off the client. The hours were brutal with consultants sitting in small sweaty conference rooms all day. EY leadership was ruthless and mostly unethical. Unimaginable work conditions. EY bent to a new low to please the CIO known for mistreating consultants.
EY has gone to a new low to meet their vision 2020.
Beware in the interviews. Ask around what the real work would entail. Some practices are just doing body shopping to meet their goals.
If they don't change their way, they will become history. They have done a disservice to the consulting profession.
Advice to Management
Treat employees with respect, be ethical in how you bill.
I have been working at EY full-time (More than 10 years)
Great people-friendly culture, hard-working, no bad apples
No real downsides, the pay is good, you need to be willing and able to earn your pay
I have been working at EY full-time (More than a year)
Leadership lives values. Ability to free think and innovate. Very collaborative and supportive environment
Could do a better job at data management/business reporting.
I worked at EY full-time (More than a year)
Great people, Brand, Career opportunities
Workload, long hours, internal politics
Helpful (1)
I worked at EY full-time (More than 3 years)
Great learning and analytical rigor of typical management consulting firms
Reputation still lags in management consulting industry. Although, with acquisition of Parthenon, EY is a more robust and competitive player
I have been working at EY full-time (More than 5 years)
The company culture is great
There are great people to work with
You will gain experience 3 times faster when compared to industry
You will have exposure to high executives and people from different industires
A lot of travelling comes with the profession (but that could be a Pro if you like getting tons of miles and hotel points for personal travel)
The bonus is not so great
Advice to Management
Consider increasing variable compensation tied to performance to incentive employers to achieve their goals and be comparable to other consulting companies
I have been working at EY full-time (More than a year)
People are great, support is available through experience managers and counseling families. Projects your on and the team your working with determine a lot.
There's obviously a lot of travel. Reimbursement is decent. A lot of upper managers work in silos on projects. Seem to only really care about utilization.
Advice to Management
Teach frameworks and provide mentorship
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John Lydon has secured prime position as one of the most recognizable icons in the annals of music history. As Johnny Rotten, he was the lead singer of the Sex Pistols - the world's most notorious band, who shot to fame in the mid-1970s with singles such as 'Anarchy in the UK' and 'God Save the Queen'. So revolutionary was his influence, he was even... more...
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Ansonia Language Lessons
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Ansonia Language Lessons
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How it Works
From finding the perfect teacher to managing payments, scheduling and tracking your progress, we take care of all the details, so you can focus on learning. Learn More
Search for a teacher
Compare hundreds of teachers based on the criteria that matter to you, including background checks, age and experience.
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When you've found the perfect match, schedule your lessons online using the teacher's real-time availability.
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Your teacher will welcome you with a personalized curriculum to meet your specific goals and you'll be able to manage your entire schedule through our free online account.
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No problem. Our online lesson platform connects you with any teacher, anywhere. All you need is a reliable Internet connection, a webcam and a microphone.
Zero travel time is great for a busy schedule.
Typically priced lower than local lessons.
Online students stick with lessons as long as local students.
Language Lesson Reviews from Students
Students are raving about their Language instructors on TakeLessons. Check out some of these recent reviews.
Review by Thomas
"Preeti is able to teach and explain Hindi to someone like me who has almost no knowledge of the language. She is able to tailor the lesson to my needs and
is very patient. She has also been very flexible with my sometimes crazy schedule, and has always been able to reschedule without issue"
Seattle, WA teacher: Prefeti A.
Review by Chandelle
Manchester, NH teacher: Krista D.
Review by Antonio
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Houston, TX teacher: Carla D.
Review by Nicole
"Ed was wonderful as he not only pointed out mistakes I had made, but spent the time discussing with me WHY the correction was necessary. He was very quick
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Denver, CO teacher: Ed C.
Review by Khloe & Kennedy
"Although the reception was poor, the girls enjoyed their instructor,"
Wichita, KS teacher: Sunho K.
Review by Kelsey
"Joy is very friendly and helpful. She tailors every session to what I am working towards and will integrate any and all materials I have or she can find.
Great experience so far!"
Fayetteville, AR teacher: Joy B.
Review by Jewel
"Roman is patient, focused and congenial. It's easy to learn quickly with persistent study, and he motivates and pushes his students to do their best, maki
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San Diego, CA teacher: Roman N.
Review by Kory and Deb
"We had our first lesson last Sunday and it was a great experience. Youngju is awesome!!! I think that's all I need to say. I look forward to our many less
Baltimore, MD teacher: Youngju S.
Review by Isreal
"He's awesome with my kids 9&11. They both have totally different learning styles and he's focused on there individual needs. He's teaching them on subject
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And they're not alone!
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8 Essential Japanese Greetings
Greetings are an important part of any language and allow you to connect and communicate. So whether you're learning the language or planning a trip to Japan, you can learn some of the most common Japanese greetings with language teacher Carol Beth L. Greetings are one of the first, most basic things you will learn when you study any new language. They are invaluable and necessary elements that allow you to connect with others. The way in which you address someone can also tell a lot abou … Read More
8 Essential Japanese Greetings
Greetings are an important part of any language and allow you to connect and communicate. So whether you're learning the language or planning a trip to Japan, you can learn some of the most common Japanese greetings with language teacher Carol Beth L. Greetings are one of the first, most basic things you will learn when you study any new language. They are invaluable and necessary elements that allow you to connect with others. The way in which you address someone can also tell a lot abou
List of 100+ Common Irregular French Verbs
Not all French verbs follow the regular rules. Brush up on the most common irregular verbs in French with this list of over one hundred verbs you need to know. Common Irregular French Verbs aller - to go Je vais Tu vas Il/Elle va Nous allons Vous allez Ils/Elles vont Past Participle allé avoir - to have J'ai Tu as Il/Elle a Nous avons Vous avez Ils/Elles ont Past Participle eu dire - to say, to tell Je dis Tu dis Il/Elle dit Nous disons Vous dites Ils/Elles disent
10 Tricky Spanish Tongue Twisters to Try Today!
You may have tried some other methods for improving your Spanish pronunciation, but what about something a little more challenging? In this article, teacher Emmanuel N. demonstrates some fun Spanish tongue twisters that are harder to say than they appear... Tongue twisters (or trabalenguas) are found in many languages, and they can be very amusing for children and adults alike. But did you know that tongue twisters can also help improve your pronunciation as you're learning to s
Top 5 YouTube Channels That Will Help You Speak German
Are you looking for an alternative way to learn German? Or, do you simply want to supplement your current German lessons? Learning how to speak German has never been easier, thanks to the many online resources available today. In particular, YouTube has emerged as a popular platform for students who want to learn how to speak German. YouTube is a great learning tool, as it lets you try tutorials from a wide variety of instructors and enables you to learn on your own time. There are ton
Video: How to Roll Your R's | Spanish Lessons
Having trouble rolling your R's in Spanish? You're not alone! Check out this helpful video for tips from TakeLessons teacher Sheila S... As an opera singer and voice teacher, its my job to know how to pronounce all languages and to be able to teach how to properly pronounce them. If you're learning how to speak Spanish, you'll also need to learn how to roll your R's. This can be a challenge to some American students, because we produce our R sound very differently in English


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German football club bans stars from getting tattoos
Berlin: A top German football club has banned its players from getting tattoos, saying it could hamper the performances of players on the pitch.
Werder Bremen believes that the discomfort following tattooing, combined with the risks of infection, could affect players' performances on the field, the Daily Mail reports.
Bremen``s goalkeeper Tim Wiese, midfielder Marko Arnautovic and defender Naldo all have considerable numbers of ``tats.``
Now, according to the new rules they won't be allowed to get any more tattoos.
Last season Hamburg, a rival of Werder Bremen, sidelined 24-year-old striker Eljero Elia after one of his tattoos went septic, the paper said.
At times, the pain was so bad he was even unable to wear his strip during training sessions, it added.
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Our blog
Read about our work, our team, and some of our most recent accomplishments.
Meet the Procuremenati – USDS' Acquisition Experts
USDS has a small team of acquisition experts applying methods from the private sector for acquiring and managing digital tools and services. Every day we encourage agencies to use contracting strategies that get the most value for taxpayers' money.
Meet the Team - February 2017
New year, new faces. Meet a few folks who recently joined the U.S. Digital Service.
Driving Positive Change – A Conversation with Margaret Stewart
Liz Odar of the U.S. Digital Service spoke with Margaret Stewart, Vice President of Product Design at Facebook, about the challenges of designing for a massive audience and using design as a force for good.
Staying with the U.S. Digital Service
Matt Cutts originally signed on for a three month tour of duty with the U.S. Digital Service. Here's why he's staying on as Acting Administrator.
You'll Never Be The Same Again
Mikey Dickerson, Administrator of the U.S. Digital Service, says farewell and reflects on the importance of building a tradition of public service in the tech industry.
How the U.S. Digital Service Is Making America's Import System More Efficient
USDS worked alongside CBP to improve testing, move applications to the cloud, and transparently present availability and business metrics to the public.


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By : Mike/ Tags : /Category : Scrub Away The Chicken Skin Bumps/0 Comment
Ashlee Simpson FINALLY shows off her baby bump in black workout gear – Daily Mail
Daily MailAshlee Simpson FINALLY shows off her baby bump in black workout gearDaily MailBut this time around, Ashlee Simpson is making sure she doesn't add too many pounds by staying consistent with her workouts. The 30-year-old actress was seen exiting Tracy Anderson gym in Studio City, California with her burgeoning bump on show and …
Girls, do U have issues w/razor bumps?? I have just the …
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Simpsons Writer Reveals How They Predicted Trump Would Win
A writer for The Simpsons has explained how he was able to accurately predict that Donald Trump would win the presidential race over 16 years ago.
In the episode 'Bart to the Future', Donald Trump wins a fictional race to the White House – a storyline that has since become reality.
According to writer Dan Greaney, when he wrote the episode he was attempting to portray an American public that had collectively gone insane, which then resulted in Trump becoming President.
Disclose.tv reports:
This choice allows Lisa to come in and pick up the pieces as his replacement, the story structure that the episode needed.
The Simpsons episode included some details that were eerily replicated in real life.
The most noticeable of these was the electoral college board featured in the episode detailing Democrat, and Republican states was an almost perfect replica of the results of the Trump vs. Clinton election.
The creator of The Simpsons, Matt Groening has previously agreed with this explanation for the choice of Trump as the fictional President stating that they chose, 'the most absurd placeholder joke name we could think of at the time.'
The jocular nature of the selection of Trump as president in the episode suggests that The Simpsons staff involved in 'Bart to the Future' must have been extremely surprised and amused, first to see Trump selected as a candidate and then as President of the United States.
Sean Adl-Tabatabai
Latest posts by Sean Adl-Tabatabai (see all)
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Ali G is always fun to watch, especially when he's talking green. Here's a short video I found on Living Small, where he talks with some guests on recycling and other green stuff. Respect!
Raz @ Eco-Libris
Eco-Libris: plant a tree for every book you read!
Smurfs Up! Tiny Blue Belgians Change The World
4 hours ago


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Permanent jobs in Ascot
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Found 37 jobs
Interior Designer
Our client offers a high quality Commercial Interior Design service and are looking for an experienced Designer to join their team. Key Responsibilit
Customer Success Manager - Part Time
Have you got experience of working in HR or Recruitment, and are looking for a flexible Part Time role? You'll be someone who enjoys working with
Project Manager - Boutique Consultancy
Bored of the London Commute? Want to work for a boutique company? I am currently working with a boutique project management consultancy, who are look
CNC Machinist / Assembly Technician
The Company A Leading Manufacturer The Role · The role will require and autonomous worker with a right first time & can-do attitude &mid
Sales Executive
Sales Executive, Ascot - £21,000+ Commission Monday - Friday 9:00 - 5:00 An exciting opportunity has arisen with our client based in Ascot, c
Field Service Engineer ANPR/CCTV
Kinect Recruitment are currently seeking multiple Field Service Engineers to join an expanding team, the successful candidates will be part of small t
Restaurant Manager
We are now looking to recruit a Restaurant Manager for a new luxury home opening in Ascot in early 2017. Salary: £19,000 - £24,000 DOE
Qualified Nursery Nurse - Ascot
Our client is looking for enthusiastic nursery practitioners to work in their nursery setting in Ascot, Berkshire, immediate start. Working alongside
DBS Chef Private School
Chef de Partie wanted for a private school. Covering day-to-day school requirements as well as events such as weddings, dinners, etc. We can offer fle
General Site Assistant
Working for a private school, driving the school van, operating a space vac to clean the gutters, litter picking and delivering the laundry throughout
Hotel Maintenance Engineer
Hotel Maintenance Engineer (Shift Based Role) Ascot £22,297 + 28 Days Holiday + Hotel Discount + Product Discount + Life Assurance + Pension
Domestic Gas Engineer
Domestic gas engineers required for permanant roles based in Ascot Your new company A building services provider in Ascot are currently recruiting
Painters required in Sunningdale and Ascot
Core Atlantic are pleased to offer an excellent opportunity for the right candidate. The Position of Painter is available in Sunningdale A leading Ma
Head Chef
We are recruiting a Head Chef with experience of commissioning to assist with commissioning our restaurants in our luxury care home in Ascot. You wil
Domestic Gas Engineer
Domestic Gas Engineer £30,000-£32,000 + Overtime & Company Van Ascot The Role We are currently looking to recruit an experienced G
Logistics / Parts / Engineer Scheduler
Engineering Service Coordinator Advantage Resourcing are currently recruiting for a reputable specialist manufacturing company, within a scientific
Event Team Member required for ad-hoc dates
Are you available for work on all the following dates below? If you are and would enjoy working in a fun yet professional environment - we would love
Senior Chef - Contract Catering £11 per hour
Senior Chef - Education Catering - £11 per hour - Term Time only - &pou
Sous Chef
Sous Chef - Windsor/Ascot - Niche fine Dining Establishment Salary: £28,000+ per annum Holiday Package Pension Scheme) Immediat
Luxury Spa Therapist
My client is a ground-breaking luxury Spa with breath-taking views of the surrounding parkland. They offer a range of natural and luxurious treatments


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Had my steak cooked to perfection and the best Stuffed Pepper Appetizer that I ever had. Simply Delicious.
My family and I have never been disappointed in the food we ordered at Saltgrass. They have a good variety of food on their menu. Their steaks are unbeatable. It's a place where adults could sit down and have a quiet dinner. They also have a good selection on their Kid's Menu for your children. Their servers are knowledgeable and...
Every time we are in the area we eat here. My DH gets the 9 oz. filet and he just loves bite. Most beef does not agree with him. But he eats this and there is not an issue. I get something different every time. Had the brisket tacos and they were really good. We drive from Kansas to see...
I am a steak lover. Anyone who knows me will say the same. I can't always hit the high-end steak houses, whether for convenience purposes, or because my company would freak out at the price! Saltgrass is the next best thing. The atmosphere is more upscale than the other steak houses, service was good, and the quality of the food...
Go to restaurant for a great steak and excellent service. Not cheap but you get what you pay for. Will definitely go here again.
We arrived Friday evening around six thirty wait was estimated 40 minutes it was 50. Waiter was pleasant, well decorated good atmosphere.
Cowboy ribeye is excellent, cooked perfect even without butter as requested. Salads, baked potatoes, and yams all were great. large bread roll served with all dinners.
I ordered the 16 ounce rib eye. Disappointing. It was chewy and undercooked. That was not what I expected for a $26.49 dollar meal. The Caesar salad was very good. My wife loved the Fondeaux Spinach. I thought the wine was pricey at $7 - $9 for house wines. The wine portions were also on the low side.
Our server,...
It's usually crowded on weekends the have call ahead seating which it great because when you arrive they usually take you right away.
Each time I go the meals are great. Service is good and good atmosphere. Meals are reasonably priced for a steak house. Steaks are good and season well.
Great food, great service, great place. Everyone was welcoming and ready to help and answer any questions we had.
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