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The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases Manipulating Mi Ma Microbiota in The Hong Kong Association for the Study of Liver Diseases Liver Dise Li sease The Hong Kong

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Ma Manipulating Mi Microbiota in Li Liver Dise sease

Jasmohan S Bajaj, MD Division of Gastroenterology, Hepatology and Nutrition, Virginia Commonwealth University and McGuire VA Medical Center, Richmond, Virginia, USA

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Out Outline and and Que uestions to be be as asked

  • Why is it relevant to study microbial change in liver disease?
  • What is lacking in the current microbial therapies for liver

disease?

  • What are the levels of therapy in reducing the severity of liver

disease?

  • Is microbial therapy going to be enough?

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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SLIDE 3

Mi Microbial Analysis and Outputs

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Animals Fungi

Phylogenetic Tree of Life: Microbes, Fungi and Humans

  • Proteobacteria
  • Gammaproteobacteria
  • Enterobacteriales
  • Enterobacteriaceae
  • Escherichia
  • Escherichia coli

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Products of bacterial metabolism

  • Carbohydrates : Short chain fatty acids
  • Phytochemicals: Phenolic acids
  • Protein: Phenolic acids, Ammonia, Polyamides
  • Fat: Bile acids with taurine and secondary bile acids
  • Xenobiotics: Carcinogens
  • Alcohol: Acetaldehyde

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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SLIDE 6

Mi Microbial Outputs

  • Type of bacteria
  • Presence/absence
  • Richness: count of individual bacterial types
  • Diversity: count of individual types and their

abundance

  • Relative abundance: percent present compared to the

total abundance

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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SLIDE 7

Levels of study in microbiome research

  • Which microbes are present in the GI tract? (culture-dependent or independent

techniques)

  • Stool
  • GI tract mucosa
  • In peripheral systems
  • What are GI tract microbes doing? (metatranscriptomics, metaproteomics,

metabonomics/metabolomics).

  • What microbial genes are present in the GI tract? (metagenomics)

Ultimately, the relationship with host state and outcomes is essential

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Relevance of f microbial change in liver disease

  • Liver diseases, especially alcohol and

NAFLD, initiate microbial change independent of liver injury

  • This microbial change could worsen the

liver injury phenotype

  • Cirrhosis of the liver, the end-stage of

fibrosis, can affect the microbiota

  • Microbial change, including bacterial

translocation, is associated with systemic and intestinal inflammation

Alcohol with/without Cirrhosis NAFLD with/without Cirrhosis

Mutlu et al AJP 2012, Hartmann et al Hepatol 2015, Boursier et al Hepatol 2017, Bajaj et Nature 2015 Chen et al Hepatol 2011, Bajaj et al J Hepatol 2014

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Bio iosensors: Keystone and In Indic icator organis isms

Keystone organisms: that has a disproportionately large effect on its environment relative to its abundance Adequate presence=Good health of the overall ecosystem Indicator organisms : that defines a trait

  • f the environment which are also

known as sentinel organisms, i.e.

  • rganisms which are ideal for

biomonitoring E.g. Coliforms to monitor water quality Ideal Biosensor: Combination of Keystone and Indicator Organisms

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Th The Cirr irrhosis is Dysbio iosis is Ratio io Paralle llels ls Cirr irrhosis is Se Severit ity

2.05 0.89 0.66 0.32

0.5 1 1.5 2 2.5

Healthy Controls Compensated

  • utpts

Decompensated

  • utpts

Infected inpatients

P<0.0001 Bajaj JS et al J Hepatol 2014, Bajaj JS Sci Rep 2015 Cirrhosis Dysbiosis ratio was also stable over time, worsened with the development of the first episode of hepatic encephalopathy and was worse in those who were subsequently hospitalized

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Mic icrobial change is is li linked to outcomes in in cir irrhosis

  • Microbial change can predict inpatient and
  • utpatient outcomes in cirrhotic patients
  • Microbiota are associated with an altered gut-

liver-brain axis resulting in Hepatic encephalopathy (HE)

Death in Cirrhotic Inpatients Hospitalizations in Outpatients

Cognitive function and brain inflammation and edema are related to microbes in cirrhosis= HE

Bajaj et AJP 2011/2013, Chen et al J Gastro Hepatol 2015, Bajaj et al J Hepatol 2014, Bajaj et al Hepatol 2015, Ahluwalia et al Sci Rep 2016

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SLIDE 12

Pathophysiology of HE

Bajaj JS Hepatology 2015, Dasarathy et al J Hepatol 2016

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Gut micr icrobio iota are re necessary fo for r bra rain in inf infla lammatio ion (micr icrogli lial l and glia lial) l) in in cirrh irrhotic ic mice ice

4 mouse groups: GF, GF made cirrhotic using CCL4 gavage, Conventional control and Conventional mice made cirrhotic using CCL4 gavage

Cerebellum Cortex Kang, Bajaj et al Hepatology 2016

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Current mic icrobial therapies need more precision

Pre-cirrhosis

  • Probiotics: very poor evidence in NAFLD

and alcoholic liver disease with multiple formulations used and for very small durations

Cirrhosis : Hepatic Encephalopathy

  • Probiotics: Good data with VSL#3 for

readmission prevention but not recurrence of hepatic encephalopathy

  • Prebiotics/Laxatives: Poor evidence for

lactulose and mechanistically likely to be a laxative

  • Antibiotics: Rifaximin has the best

evidence profile but it is expensive and also does not prevent all HE episodes

Bass et al NEJM 2010, Dhiman et al Gastro 2014, Sharma et al Gastro 2009, Bajaj et al Metab Brain Dis 2011, Bajaj et al Hepatol 2017

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Levels of therapy in reducing the severity of liver disease

  • Control etiology: Not likely microbial
  • Affect inflammatory milieu locally and

systemically: Oral cavity

  • Change gut microbial composition and hopefully

function: FMT, Proton pump inhibitors, Engineered bacteria and Dietary modification

  • Change gut microbial interaction with other

microbiota: Interaction with fungi

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Systemic and Local In Inflammatory Control

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Oral Mic icrobiota is is dif ifferent from stool l mic icrobiota compositionally in in healt lthy controls ls and in in cir irrhotic patie ients

Human Microbiome Project Nature, Bajaj et al Hepatol 2015

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Perio iodontal l therapy im improves gut mic icrobiota and endotoxemia ia

#p<0.05 pre vs post *p<0.05 cirrhosis vs controls Cirrhosis Controls Pre-therapy Post-therapy Pre- therapy Post-therapy MELD score 9.5±3.3 8.6±2.7* _ _ WBC count 6.11±1.90 5.67±1.85* 7.12±1.7 7.01±1.5 Endotoxin(EU/ml, median, IQR) 0.18(0.05)* 0.12(0.07)# 0.11(0.09) 0.14(0.10) TNF (pg/ml, median, IQR) 17.3(9.1)* 15.1 (8.3)*# 12.1(6.3) 9.5(10.1)*

Bajaj et al Am J Physiol 2018

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Or Oral al-Gu Gut-He Hepati tic c Axis

Control the etiology Prevent Decompensation Liver Transplant Periodontal Therapy Avoid smoking Avoid alcohol Oral hygiene Non-absorbable Abx Probiotics Avoid unnecessary PPI

Acharya, Sahingur and Bajaj JCI Insight 2018

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Mi Microbial Comp mposition and Functional Change

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  • 0.1
  • 0.3
  • 0.4
0.1 0.3 0.4 0.5
  • 0.1
  • 0.3
  • 0.4
0.1 0.3 0.4 0.5 0.7

Microbiota changes Yellow: PRE Red=POST

Proton Pump In Inhib ibit itors In Init itiation and Wit ithdrawal l can Change Mic icrobiota in in Liv iver Dis isease

PPIs Exacerbate Murine Alcoholic Liver Injury Through Enterococcus Adding PPIs Oralizes Stool Microbiota in Compensated Cirrhosis and Healthy Controls Similar changes are found in Advanced Cirrhosis with Reversal after PPI Withdrawal Adding PPIs Withdrawing PPIs Llorente et al Nat Comm 2017, Bajaj et al AJP 2014, Bajaj et al Am J Gastro 2018

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Ma Manipulation of microbiota: Fecal Mic icrobiota Transplant

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Particula lar challenges of f FMT in in HE

  • Generally a much more advanced population
  • Prone to potentially life-threatening infections, including those that

are initiated from the gut

  • Avoiding antibiotics post-FMT may not be feasible
  • Many are already on rifaximin and SBP prophylaxis
  • Directed donor vs. universal donor?

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Case Report of f FMT in in th the management of hepatic ic encephalopathy

Kao et al Hepatology 2015

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Bajaj et al Hepatology 2017

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Fecal Mic icrobiota Transplant Changes Mic icrobial Function

micromoles

D20 D5 Base D20 D5 Base D20 D5 Base FMT S FMT S FMT S FMT S FMT S FMT S FMT S FMT S FMT S

3500 3000 2500 2000 1500 1000 500

FMT 1

Acetate Propionate Butyrate

Ratio compared to total BAs

D20 D5 Base D20 D5 Base D20 D5 Base FMT S FMT S FMT S FMT S FMT S FMT S FMT S FMT S FMT S

1.0 0.8 0.6 0.4 0.2 0.0

FMT 1

Secondary/Total Conjugated/Total Sulfated/Total

Seconds change

FMT SOC

100 50

  • 50
  • 100
  • 150
  • 200
  • 250

Stroop Day 0 minus Day 20 (Positive indicates improvement)

PHES composite score

FMT SOC

7.5 5.0 2.5 0.0

  • 2.5
  • 5.0

PHES Day 0 minus Day 20 (Negative indicates improvement)

Specific Microbes Reduce Ammonia And improve survival In Murine models In Humans FMT improves cognition, restores SCFA and Bile Acid profile SCFA Bile Acids Shen et al JCI 2015, Kao et al Hepatol 2015 Bajaj et al Hepatol 2017, Bajaj et al Hepatol 2018

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Medit iterranean die iet in in cir irrhosis=better div iversity and lo lower hospit itali lizations compared to Western Die iet

  • Cohort of 296 Turkish and US-based

controls, compensated and decompensated cirrhotic patients was included and followed for 90 days

  • Turkish subjects had similar diversity

due to greater consumption of fermented milk products.

  • There was a significantly lower risk of 90 day hospitalization in Turkish compared to

American cirrhotic patients

  • On Cox and binary logistic regression, microbial diversity was protective against 90-day

hospitalizations, along with coffee/tea, vegetable and cereal intake.

Bajaj JS, Idilman R et al, Hepatol 2018

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SLIDE 28

Slide courtesy of Synlogic Pharmaceuticals

Eng Engineering Probiotic Bac Bacteria to Co Consu nsume Ammonia

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SLIDE 29

Microbial In Interactions

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Bacterial and fu fungal in interactions are relevant in in li liver dis isease

Fungi Worsen Alcoholic Liver Injury In Murine models Gut Fungi are Related to Gut Bacterial Diversity and Worsen with Antibiotic use, being replaced by Candida Yang et al JCI 2017, Bajaj et al Gut 2017

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However, are cir irrhosis and chronic liv liver dis isease mic icrobial dis iseases? In In other words wit ithout controlling the liv liver dis isease etio iology, can we expect an im improvement by ju just affecting the mic icrobiota?

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Liv iver cir irrhosis requir ires liv liver in inju jury ry: mic icrobes potentia iate but do not cause it it in independently

Stool Donor Systemic Inflamm- ation Liver Inflamm- ation Liver injury/ cirrhosis Bacterial translocation

Healthy human

+

  • Non-drinking

Cirrhotic human

+ +

  • Non-drinking

Cirrhotic with HE

+ +

  • Actively drinking

non-cirrhotic human

+ +

Only if fed alcohol Only if fed alcohol

Actively drinking cirrhotic human

+ +

  • +

Kang et al Hepatology 2016, Kang et al Clin Transl Gastro 2016, Llopis et al Gut 2015, Kang et al Hepatol Comm 2017

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Con Conclu lusio sions

  • Microbial changes are an integral part of the altered gut-liver axis in cirrhosis and

pre-cirrhotic liver disease

  • They are complicit but not necessarily causative of liver injury without the direct

liver injury also

  • Microbial treatment in liver disease has to be accompanied by treatment of the

liver disease etiology

  • Current therapies can be improved by precision changes in microbiota
  • Specific means by which we can potentially improve outcomes
  • Regular dental cleaning and avoid periodontitis
  • Withdraw unnecessary PPI use
  • Consider the use of antibiotics that can encourage fungal infections
  • Focus on therapies related to bacterial function
  • Emphasis on fermented, probiotic foods
  • Make every effort to combine microbial therapy with etiological therapy as well

The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases The Hong Kong Association for the Study of Liver Diseases

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Ac Acknowledgements

VCU Microbiology/Immunology

  • Phillip Hylemon, PhD
  • Huiping Zhou, PhD
  • DJ Kang, MS
  • Genta Kakiyama, PhD

VCU/VA Gastroenterology and Hepatology

  • Arun J Sanyal, MD
  • Douglas M Heuman, MD
  • William M Pandak, MD
  • Richard K Sterling, MD
  • R Todd Stravitz, MD
  • Velimir Luketic, MD
  • Puneet Puri, MD
  • Michael Fuchs, MD
  • Muhammad S Siddiqui, MD
  • Scott C Matherly, MD
  • Binu John, MD
  • Hannah Lee, MD

GMU Environmental Sciences

  • Patrick M Gillevet, PhD
  • Masoumeh Sikaroodi, PhD
  • Naga Betrapally, MS
  • Swati Dalmet, MS

VCU/VA coordination

  • Melanie White, RN
  • Edith Gavis, RN
  • Jill Meador, RN
  • Andrew Fagan, BS

Funding: VA Merit Review I0CX001076, RO1DK089713, RO1AA020203

University of California, Davis

Oliver Fiehn Sili Fan

Inst for Liver Diseases, London

I Jane Cox Roger Williams

Imperial College, London

Mark McPhail Simon D Taylor-Robinson

OpenBiome

Zain Kassam Majdi Osman Emilee Tu Audrey Abend

UC San Diego

B Schnabl

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