The Role of the Gut Microbiota and Probiotics in Non-Alcoholic Fatty Liver Disease (NAFLD) and Non-Alcoholic Steatohepatitis (NASH)

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1 The Role of the Gut Microbiota and Probiotics in Non-Alcoholic Fatty Liver Disease (NAFLD) and Non-Alcoholic Steatohepatitis (NASH) Dr Mayur R Joshi MBBS, BSc, AICSM Pharmaceutical Physician As more research is undertaken, more is understood about the impact of the human microbiome, in particular the gut microflora, on health. In recent years the complex relationship between the gut microbiota and the metabolic pathways in the body has been increasingly explored with implications for multiple disorders. Evidence has emerged that shows the link between the gut bacterial population and disorders of the endocrine system within the spectrum of metabolic syndrome. Included in this are Non-Alcoholic Fatty Liver Disease (NAFLD) and its sequelae Non-Alcoholic Steatohepatitis (NASH), cirrhosis and ultimately, hepatocellular carcinoma. NAFLD & NASH Non-alcoholic fatty liver disease (NAFLD) represents a spectrum of disorders ranging from fatty infiltration of liver cells, or hepatic steatosis, to steatohepatitis, fibrosis and eventually cirrhosis 1. Ultimately cirrhosis itself can lead to hepatocellular carcinoma 2. The histological, imaging and laboratory features of NAFLD are indistinguishable from alcohol induced steatosis and subsequent steatohepatitis and, therefore, the diagnosis is made in the absence of a history of significant alcohol intake. In the majority of cases, NAFLD develops in association with features of metabolic syndrome and insulin resistance (IR). Within the spectrum of metabolic syndrome one usually finds a cluster of clinical features, namely IR, glucose intolerance or full blown diabetes, obesity, hypertension and dyslipidaemia all of which result in a significantly increased associated cardiovascular risk. Epidemiology Non-alcoholic fatty liver disease (NAFLD) is the most common chronic liver disease worldwide, both in adults and in children 3. Due to its strong association with other metabolic diseases such as obesity and diabetes, the western world is seeing an increase in both incidence and prevalence of NAFLD and NASH 3. The statistics vary depending on the geographical region and diagnostic parameters but research suggests that up to 24% of the general population of developed countries is affected by NAFLD 4. The British Society of Gastroenterology suggests that this figure is closer to 33% for the UK population 5 whilst a Korean study suggested a prevalence of 51% 6. When associated with other diseases the prevalence of NAFLD increases dramatically particularly in patients with obesity (60 95%), type 2 diabetes mellitus (28 55%) and hyperlipidaemia (20 92%) 4. NAFLD affects 2.6% of children and this figure increases to between 22.5% % in the obese child population 7,8. Progression to NASH is a clinically significant event and epidemiological research suggests that its prevalence is 1.2% 4.8% 9. Importantly, studies from tertiary care centres, community-based and population-based databases suggest that liver disease is the third leading cause of death among people with NAFLD

2 Pathogenesis The pathogenesis of the disease is extremely complex, not fully understood and beyond the scope of this feature, however it is important to understand some of the basic mechanisms underlying its development. Early explanations suggested a 2-hit hypothesis with initial hepatic triglyceride (fat) accumulation, or steatosis, increasing the liver s susceptibility to further injury mediated by second hits from proinflammatory cytokines, oxidative stress and cellular dysfunction. This leads to hepatic inflammation, or steatohepatitis, and in turn, fibrosis 11,12. However, more recently, free fatty acids (FFA) have been attributed with a direct toxic effect which works in tandem with and, in fact, triggers other hepatotoxic pathways and prevents hepatic cellular regeneration, a third hit 13. Another contributory mechanism by which inflammatory pathways can be activated is the production of pro-inflammatory products by intestinal bacteria. There is a clear association between intestinal bacterial overgrowth and the development of NAFLD and NASH with some of the specific mechanisms being identified 14. An association between small intestinal bacterial overgrowth (SIBO) and severity of steatosis has been identified, adding further evidence to the hypothesis that the gut microflora plays a key role in the development of the disease 15,16. It is thought that the gut microbiota contributes to the development of NASH through the increased production of ethanol and lipopolysaccharides which stimulate inflammatory cytokine production through TNF-α and NF-κB mediated mechanisms 14. In addition, luminal bacteria metabolise dietary choline (which is required for hepatic lipid export) thereby promoting steatosis. These pathways, in turn, increase intestinal permeability thus enhancing hepatic exposure to other gut derived endotoxins that are directly or indirectly hepatotoxic 17. Clinical Management NAFLD and NASH are managed based on the progression and severity of the disease. Simple steatosis alone can be managed in the primary care setting with lifestyle modifications the mainstay of treatment 18. The main strategy is to manage obesity and other associated conditions within the spectrum of metabolic syndrome. This is then supplemented with treatment of specific liver related consequences. There are no targeted medications for NAFLD or NASH themselves although there are certain medications that have shown benefit in its management. Diet FFA Obesity and Insulin resistance Oxidative Stress Gut derived endotoxins Lipogenesis FFA Fibrosis/NASH Lipotoxicity Inflammatory Cytokines Bacterial Overgrowth Ethanol and LPS Hepatocyte Death Inadequate cell regeneration Figure 1. Even in this simplified format above it is clear to see the complex interplay between fat deposition, bacterial overgrowth and inflammatory pathways in the pathogenesis of NAFLD and NASH. (FFA: Free fatty Acids, LPS: lipopolysaccharides, NASH: Non-alcoholic steatohepatitis) Modified from Dowman et al The Clinical Use of Probiotics and Fibre

3 Lifestyle modification Lifestyle modification aimed at weight reduction and increased physical exercise is the first line treatment for all patients with NAFLD. That being said, the optimal diet for NAFLD patients has not yet been determined and, until further research is carried out, a calorie restricted diet (600Kcal less than a maintenance intake) should be recommended until target weight is achieved 19. A Mediterranean diet (high in monounsaturated fatty acids), as compared with a diet low in fat and high in carbohydrates, has been shown to reduce hepatic steatosis and improve insulin sensitivity in non-diabetic subjects with NAFLD 20. It has also been demonstrated that moderate intensity training, high intensity training and resistance exercise result in improvements in liver enzymes and reduction in liver fat, independent of weight loss 21. There is also a role for bariatric surgery in particularly obese patients in order to aid weight loss 22. Pharmacotherapy Lifestyle Modifications Metabolic syndrome Liver specific Cirrhosis Figure 2. There are four main areas to focus on when thinking about management strategies in NAFLD: lifestyle modification, targeting the components of the metabolic syndrome, liverdirected pharmacotherapy for high risk patients and managing the complications of cirrhosis. Adapted from Dyson et al Individual components of the metabolic syndrome such as diabetes, hypertension and dyslipidaemia are managed as they would be without the presence of NAFLD with appropriate medication. Metformin has been investigated as an adjunct to lifestyle changes in the management of NASH with varying results. It has been shown to aid weight loss and reduces risk of diabetes related morbidity and mortality 19. Its role in those patients with NAFLD, but no components of diabetes, is controversial and is therefore not a definitive recommendation in those patients. Other insulin sensitisers are recommended as second line treatment and there is some evidence to suggest they can improve inflammation and steatosis in NASH 23. In terms of liver directed pharmacotherapy, pioglitazone and vitamin E have been shown to have some benefit in patients with biopsy proven NASH. These benefits have been demonstrated in patients with or without associated diabetes. For example, a recent meta-analysis has demonstrated that pioglitazone treatment in NASH significantly improves steatosis, inflammation and to a lesser degree, fibrosis 24. While it appears to be an effective treatment there are concerns over its long term safety with the most serious reported risk being an increase in congestive cardiac failure, clearly an important consideration in patients already at risk of cardiovascular morbidity and mortality. The situation is similar with vitamin E whose efficacy in management of NASH has been demonstrated in a large trial showing improvements in steatohepatitis 23 but there remains a concern over its long term safety with a potential increased risk of haemorrhagic stroke and prostate cancer 25,26. Clinical Need The brief overview of NAFLD and NASH above highlights the main points with regards to the clinical need for innovative management options. It is a growing problem with significant clinical implications affecting both adults and children. There is also no specific recommended pharmacotherapy for its treatment and the ones that are available have question marks over their efficacy and/or safety. There are other medications that have been explored but the evidence is minimal and so it is clear to see that new and safe therapies that can potentially help are invariably going to be welcomed by the clinical community. 45

4 Probiotics and NAFLD/NASH Given the importance of the gut microbiota in the development of NAFLD and NASH it comes as no surprise that this is a growing area of research within the probiotic community. Their ability to alter the intestinal microbial population, restore gut barrier function, interact with the immune system and modulate inflammatory responses has attracted great interest. Several in vitro and animal models have been used to identify specific mechanisms by which they may exert their beneficial effects in NAFLD. Mechanisms The most obvious mechanism by which probiotics help in NAFLD is their ability to modulate the bowel flora. Given that SIBO is a significant trigger in the pathogenesis, reducing the overgrowth of pathogenic bacteria is a logical first step. The way in which probiotics are able to do this has been well documented and is discussed elsewhere in this booklet but includes competition for nutrients, direct production of antimicrobials, lowering luminal ph and preventing adhesion and translocation of pathogens, amongst other mechanisms. Perhaps more interestingly, probiotics are able to modulate some of the pathways involved in the pathogenesis of the disease as discussed above. They are able to improve the barrier function of the gut and repair damaged intestinal linings through a number of complex pathways mediated by the enhancement of tight junction function, preventing local inflammation and preventing apoptosis of intestinal epithelial cells 27. As a result, the liver is exposed to fewer absorbed endotoxins as there are fewer pathogenic bacteria producing them and they are not absorbed as frequently due to the reduced intestinal permeability. In vitro and animal models have been used to demonstrate that probiotics also reduce inflammatory and oxidative damage to the liver through modulation of TNF-α and PPARα pathways 27,28. Other studies have shown that specific probiotics are able to reduce fat deposition, improve triglyceride content and reduce serum endotoxin levels in NAFLD rats 27,29. Clinical Evidence Given the volume of preclinical research demonstrating the mechanisms by which probiotics might improve NAFLD it is surprising to note that there are relatively few good quality clinical trials investigating their use in humans. That being said, the results from some of these trials are highly encouraging and certainly warrant further investigation. A study published in 2011 by Malaguarnera and colleagues looked at the effects of a synbiotic alongside lifestyle modifications in patients with NASH 30. The synbiotic contained a Bifidobacterium longum strain with fructooligosaccharide (FOS) as the prebiotic and was given for a total period of 24 weeks with multiple biochemical and histological variables assessed. All 66 patients with a diagnosis of NASH were given the same lifestyle modification advice and then randomised into equal groups to receive the synbiotic or placebo. Lifestyle advice included detailed dietary and exercise schedules and was monitored by dieticians. All 66 patients completed the study and improvements were seen in both groups. However, there were much greater improvements seen in the synbiotic group compared to placebo in a number of parameters: AST (P<0.05), LDL cholesterol (P<0.001), CRP (P<0.05), TNF-α (P<0.001), HOMA-IR (P<0.001), Serum endotoxin (P<0.001), Histological evidence of steatosis (P<0.05), NASH activity index (P<0.05) The synbiotic group had greater improvements in measures of liver function, inflammation, insulin resistance and endotoxin levels as well as improvements in grading of disease. Similar results were obtained by a group of researchers in 2013 looking at a multi-strain probiotic mixture with 7 strains of bacteria including 4 Lactobacilli, 2 bifidobacteria and a Streptococcus 31. A total of 64 patients with histologically confirmed NASH were recruited for the trial and all were given 46 The Clinical Use of Probiotics and Fibre

5 lifestyle advice and metformin. They were randomised into equal groups to receive the probiotic mixture or a placebo for 28 weeks. Liver function was assessed using measurements of hepatic enzymes, and ultrasound was performed to grade the extent of the liver disease. This was done at baseline and after treatment with monitoring throughout the 6 month period. After the treatment period there were improvements in all parameters in both groups as would be expected. However, there was significantly better improvement in the probiotic group with the main results summarised below: ALT Baseline ALT Post Treatment period Metformin + Probiotic Normal Grade 1 Grade 2 Grade 3 Figure 6. Ultrasound graded steatosis after six months of treatment. 38.7% of patients had a normal grade ultrasound in the metformin/ probiotic group; 61.3% patients had grade 1 ultrasound appearances and none of patient had grade 2, 3. The differences were statistically significant as compared to the Metformin/ placebo group (P=0.01). AST Baseline AST Post Treatment period Metformin + Probiotics Metformin + Probiotics Figures 3 & 4. Improvements were seen in ALT and AST in both groups but the synbiotic group showed significantly greater improvements as shown by the p values. The above results show a clear improvement in liver function and these are corroborated by the dramatic improvements seen in the ultrasound grading of the liver. The probiotic group also showed a significantly greater improvement in BMI at the end of the study. These results were further corroborated in 2014 by another group of researchers using the same mixture in patients with NAFLD 32. A total of 52 patients were enrolled in this study and received dietary and lifestyle advice. They were then randomised to receive the probiotic mixture or placebo. Both groups showed improvements in ALT, AST, γ-gt, hs-crp, TNF-α and BMI when compared to baseline. However, the group receiving the probiotic mixture showed significantly greater improvements compared to placebo in all biochemical parameters (p<0.001 in all tests). There was no difference seen between the two groups in the change in BMI (p=0.13). Metformin + Probiotic Normal Grade 1 Grade 2 Grade 3 Figure 5. Ultrasound graded steatosis before intervention. None of the patients had a normal grade ultrasound. 47

6 Conclusion The effects of probiotics in NAFLD and NASH are yet to be conclusively evaluated but the preclinical and initial clinical data shows huge potential for their use as a safe and effective treatment option for these patients. In addition, other clinical trials have been performed with encouraging results in diabetes, cholesterol reduction and metabolic syndrome demonstrating the potential of probiotics to be used as an adjunct to treatment in metabolic disorders 33,34,35. As more is learned about the way in which probiotics are able to exert their beneficial effects more products will become part of the routine therapy for these complex disorders. About the author: Dr Mayur R Joshi MBBS, BSc, AICSM Dr Joshi is a fully registered doctor and has spent most of his clinical work in colorectal surgery, before working for Probiotics International as a Medical Advisor. Dr Mayur Joshi is currently working as a Pharmaceutical Physician. References: 1 Dowman JK, Tomlinson JW, & Newsome PN. Pathogenesis of nonalcoholic fatty liver disease. Qjm 2010; 103:2, Sanyal AJ, Yoon SK, & Lencioni R. The etiology of hepatocellular carcinoma and consequences for treatment. The oncologist 2010; 15:(Supplement 4), Eslamparast T, Eghtesad S, Hekmatdoost A & Poustchi H.Probiotics and nonalcoholic fatty liver disease. Middle East journal of digestive diseases 2013; 5:3, Alba LM, and Lindor K. Non-alcoholic fatty liver disease. Alimentary pharmacology & therapeutics 2003; 17.8: British Society of Gastroenterology, Clinical Commissioning Report. NASH and Non alcoholic Fatty Liver Disease. uk/clinical/commissioning-report/nash-and-non-alcoholic-fatty-liverdisease.html 6 Lee JY, Kim KM, Lee SG. Prevalence and risk factors of non-alcoholic fatty liver disease in potential living liver donors in Korea: a review of 589 consecutive liver biopsies in a single center. Journal of hepatology 2007; 47: Tominaga K, Kurata JH, Chen YK. Prevalence of fatty liver in Japanese children and relationship to obesity. Digestive Diseases and Sciences 1995; 4: Franzese A, Vajro P, Argenziano A. Liver involvement in obese children. Ultrasonography and liver enzyme levels at diagnosis and during followup in an Italian population. Digestive Diseases and Sciences 1997; 42: Das K, & Kar P. Non-alcoholic steatohepatitis. Journal of the Association of Physicians of India 2005; 53: Vernon G, Baranova A, & Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Alimentary pharmacology & therapeutics 2011; 34:3, Day CP, James OF. Steatohepatitis: a tale of two hits? Gastroenterology; : Day CP. From fat to inflammation. Gastroenterology; : Jou J, Choi SS, Diehl AM. Mechanisms of disease progression in nonalcoholic fatty liver disease. Seminars in Liver Disease 2008; 28: Compare D, Coccoli P, Rocco A, Nardone OM, De Maria S, Cartenì M & Nardone, G. Gut liver axis: the impact of gut microbiota on nonalcoholic fatty liver disease. Nutrition, Metabolism and Cardiovascular Diseases 2012; 22:6, Nagata K, Suzuki H, Sakaguchi S. Common pathogenic mechanism in development progression of liver injury caused by non-alcoholic or alcoholic steatohepatitis. Journal of Toxicological Sciences 2007; 32:5:453e Diamant M, Blaak EE, de Vos WM. Do nutrient-gut-microbiota interactions play a role in human obesity, insulin resistance and type 2 diabetes? Obesity Reviews; (4):272e Riordan SM, Duncombe VM, Thomas MC, Nagree A, Bolin TD, McIver CJ, et al. Small intestinal bacterial overgrowth, intestinal permeability, and non-alcoholic steatohepatitis. Gut 2002; 50:1: Dyson J, & Day C. Treatment of non-alcoholic fatty liver disease. Digestive Diseases 2014; 32:5, Dyson JK, Anstee QM, & McPherson S. Non-alcoholic fatty liver disease: a practical approach to treatment. Frontline gastroenterology 2014; 5:4, Ryan MC, Itsiopoulos C, Thodis T. The Mediterranean diet improves hepatic steatosis and insulin sensitivity in individuals with non-alcoholic fatty liver disease. Journal of Hepatology 2013; 59: Little JP, Gillen JB, Percival ME. Low-volume high-intensity interval training reduces hyperglycemia and increases muscle mitochondrial capacity in patients with type 2 diabetes. Journal of Applied Physiology 2011; 111: NICE. NICE Clinical guidelines. CG43 Obesity: the prevention, identification, assessment and management of overweight and obesity in adults and children Sanyal AJ, Chalasani N, Kowdley KV. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. New England Journal of Medicine 2010; 362: Boettcher E, Csako G, Pucino F. Meta-analysis: pioglitazone improves liver histology and fibrosis in patients with non-alcoholic steatohepatitis. 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7 28 Esposito E, Iacono A, Bianco G, Autore G, Cuzzocrea S, Vajro P, Canani RB, Calignano A, Raso GM, Meli R. Probiotics reduce the inflammatory response induced by a high-fat diet in the liver of young rats. Journal of Nutrition 2009; 139: Endo H, Niioka M, Kobayashi N, Tanaka M, Watanabe T. Butyrateproducing probiotics reduce nonalcoholic fatty liver disease progression in rats: new insight into the probiotics for the gut-liver axis. PLoS One 2013; 8: e Malaguarnera M, Vacante M, Antic T, Giordano M, Chisari G, Acquaviva R, & Galvano F. Bifidobacterium longum with fructo-oligosaccharides in patients with non-alcoholic steatohepatitis. Digestive diseases and sciences 2012; 57(2), Shavakhi A, Minakari M, Firouzian H, Assali R, Hekmatdoost A, & Ferns G. Effect of a Probiotic and Metformin on Liver Aminotransferases in Non-alcoholic Steatohepatitis: A Double Blind Randomized Clinical Trial. International journal of preventive medicine 2013; 4(5), Eslamparast T, Poustchi H, Zamani F, Sharafkhah M, Malekzadeh R, & Hekmatdoost A. Synbiotic supplementation in non-alcoholic fatty liver disease: a randomized, double-blind, placebo-controlled pilot study. The American journal of clinical nutrition 2014; 99:3, Eslamparast T, Zamani F, Hekmatdoost A, Sharafkhah M, Eghtesad S, Malekzadeh R, & Poustchi H. Effects of synbiotic supplementation on insulin resistance in subjects with the metabolic syndrome: a randomised, double-blind, placebo-controlled pilot study. British Journal of Nutrition2014; Panwar H, Rashmi HM, Batish VK, & Grover S. Probiotics as potential biotherapeutics in the management of type 2 diabetes prospects and perspectives. Diabetes/metabolism research and reviews 2013; 29:2, Lye HS, Kuan CY, Ewe JA, Fung WY, & Liong MT. The improvement of hypertension by probiotics: effects on cholesterol, diabetes, renin, and phytoestrogens. International journal of molecular sciences 2009; 10:9,

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