New Developments in Irritable Bowel Syndrome
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2 New Developments in Irritable Bowel Syndrome Mark Pimentel, MD, FRCP(C) Director, GI Motility Program Cedars-Sinai Medical Center
3 IBS Forks in the Road Not all decisions in how to handle IBS made things better. What seems like the easiest road to diagnose, characterize and treat IBS may have led us into problems which now have to be fixed.
4 Stress and IBS: Cause and Effect? Level 1 Evidence: Apply severe psychological stress to people and watch them develop IBS over time Level 2 Evidence: Compare psychological scores in IBS and compare to a disease comparable to IBS. Level 3 Evidence: Compare psychological scores between IBS and healthy people GOLD SILVER JUNK BONDS
5 Stress and IBS Military study: Shooting gun in combat Shooting another human Active combat Injured in combat Only Gastroenteritis was associated with IBS Porter CK, et al. Dig Dis Sci
6 Stress Due to Chronic Disease Not IBS? Shah E, et al. Ann Gastroenterol
7 IBS Timeline 1950 s 1960 s 1970 s 1980 s 1990 s 2000 s -Spastic Colitis -Spastic Colon -Irritable Bowel -Irritable bowel syndrome -Functional Bowel Disease IBS type -IBS IBS-D, IBS-C, IBS-A -IBS IBS-D, IBS-C, IBS-M, IBS-U
8 IBS Microbial Hypothesis Acute Gastroenteritis CdtB Toxin Autoimmunity to vinculin Gut ICC/neuronal Changes Bacterial Overgrowth IBS
9 D-IBS M-IBS C-IBS Non-Constipation-IBS
10 Breath Testing is Abnormal in IBS Forest plot of all age-sex matched studies Type of % % Author Breath Test OR (95% CI) CI) Weight Weight Grover sucrose 2.29 (0.89, 5.87) 5.87) Lupascu Pimentel glucose lactulose (3.52, 33.71) 33.71) (5.29, 80.69) 80.69) Parodi glucose 4.30 (1.24, 14.98) 14.98) Scarpellini Collin lactulose lactulose (7.35, 80.15) 80.15) (6.55, 49.71) 49.71) Overall (I-squared = 67.9%, p = 0.008) 9.64 (4.26, 21.82) 21.82) NOTE: Weights are from random effects analysis Shah. et al. Dig Dis Sci
11 Small Bowel Culture in IBS P<0.05 P< % 24% 4% 12% Posserud. et al. Gut. 2007;56: N=165 IBS, 26 controls
12 SIBO and IBS 60% 27.3% P=0.004 Pyleris. et al. DDS N=77 non-d-ibs, N=35 D-IBS
13 Bacteria quantity Log10 Single Organism PCR in IBS DUODENAL ASPIRATES P<0.05 P<0.05 N=77 non-d-ibs, N=35 D-IBS Pyleris. et al. Scand J Gastroenterol N=77 non-d-ibs, N=35 D-IBS
14 Agilent Plots of Normal and IBS IBS Healthy Control Pyleris. et al. Scand J Gastroenterol
15 Sequencing Results- Normal Small Bowel Normal Subjects Pyleris. et al. Scand J Gastroenterol
16 Sequencing Results- IBS Small Bowel IBS Subjects Pyleris. et al. Scand J Gastroenterol
17 Primary Outcome (4 Weeks After Tx) Primary Primary Primary Key Secondary Primary Key Secondary Key Secondary Other Key Secondary Other Secondary Other Secondary Other Secondary FDA Proposed FDA Proposed FDA Proposed FDA Proposed Pimentel. et al. NEJM Efficacy Odds Outcome Study Ratio (95% CI) p-value TARGET (1.10,2.12) SGA-IBS Efficacy TARGET 2 Weekly Odds 1.45 (1.05,2.01) Outcome Efficacy Combined Study Odds Ratio 1.49 (1.18,1.88) (95% CI) p-value Efficacy Outcome TARGET Study 1 Odds Ratio 1.53 (1.10,2.12) (95% CI) p-value Outcome SGA-IBS Study Ratio (95% CI) p-value TARGET (1.16,2.27) (1.05,2.01) (1.10,2.12) SGA-IBS IBS Weekly SGA-IBS Bloating Combined TARGET (1.10,2.12) (1.18,1.88) (1.05,2.01) Weekly TARGET 1.45 (1.05,2.01) Weekly Combined (1.08,2.06) (1.18,1.88) Combined (1.18,1.88) (1.23,1.96) TARGET (1.16,2.27) IBS Bloating TARGET (1.08,2.06) (1.16,2.27) Weekly IBS Bloating 1.62 (1.16,2.27) IBS Bloating Combined TARGET (1.26,2.47) (1.23,1.96) (1.08,2.06) Weekly 1.49 (1.08,2.06) Weekly SGA-IBS Daily TARGET Combined (1.13,2.24) (1.23,1.96) Combined 1.56 (1.23,1.96) TARGET (1.28,2.04) (1.26,2.47) < SGA-IBS Daily TARGET (1.01,1.97) (1.13,2.24) (1.26,2.47) SGA-IBS Bloating Daily (1.26,2.47) Combined TARGET (1.26,2.44) (1.28,2.04) (1.13,2.24) < SGA-IBS Daily Daily TARGET (1.13,2.24) Combined TARGET Combined (1.28,2.04) (1.21,1.92) (1.01,1.97) (1.28,2.04) < < IBS Bloating TARGET (1.01,1.97) (1.05,2.02) (1.26,2.44) (1.01,1.97) Daily IBS Bloating IBS Bloating Ab Pain Combined TARGET (1.21,1.92) (1.26,2.44) Daily TARGET (1.26,2.44) (1.05,2.03) Daily TARGET Combined (1.05,2.02) (1.21,1.92) IBS Ab Pain Combined TARGET (1.21,1.92) (1.13,1.78) (1.05,2.03) (1.05,2.02) Daily IBS Ab Pain (1.05,2.02) IBS Ab Pain Combined TARGET (1.13,1.78) (1.05,2.03) Daily TARGET (1.05,2.03) Daily TARGET Combined (1.02,1.92) (1.13,1.78) Ab Pain & Stool Combined 1.42 (1.13,1.78) TARGET (1.12,2.13) (1.02,1.92) Daily Ab Pain (FDA) & Stool Combined TARGET (1.17,1.84) (1.12,2.13) (1.02,1.92) Daily Ab Pain (FDA) & Stool 1.40 (1.02,1.92) Ab Pain & Stool Combined TARGET (1.08,2.03) (1.17,1.84) (1.12,2.13) Ab Daily Pain (FDA) Daily 1.55 (1.12,2.13) Daily (FDA) TARGET Combined (1.06,2.00) (1.08,2.03) (1.17,1.84) (FDA) Ab Pain Daily Combined 1.47 (1.17,1.84) Combined TARGET (1.17,1.83) (1.06,2.00) (1.08,2.03) (FDA) Ab Pain Daily (1.08,2.03) Ab Pain Daily Combined TARGET (1.17,1.83) (1.06,2.00) (FDA) TARGET (1.06,2.00) (1.25,2.59) (FDA) Stool Consist. TARGET Combined (1.25,2.59) (1.17,1.83) Stool Consist. Combined (1.17,1.83) (1.12,2.21) Daily (FDA) TARGET (1.12,2.21) (1.25,2.59) Daily Stool (FDA) Consist. Combined (1.25,2.59) (1.31,2.14) < Stool Consist. Combined TARGET (1.31,2.14) (1.12,2.21) < Daily (FDA) TARGET (1.12,2.21) Daily (FDA) Combined 1.67 (1.31,2.14) < Combined 1.67 (1.31,2.14) < Odds Ratio and 95% CI Favors PlaceboOdds Ratio and 95% Favors CI Rifaximin Favors PlaceboOdds Ratio and 95% Favors CI Rifaximin Favors Placebo Favors Rifaximin
18 Durability of Response (3 Months) Primary Efficacy Outcome SGA-IBS Weekly Study TARGET 1 TARGET 2 Combined Odds (95% CI) Ratio p-value 1.35 (1.00, 1.82) (1.13, 2.03) (1.17, 1.77) Key Secondary IBS Bloating Weekly TARGET 1 TARGET 2 Combined (0.95, 1.73) (1.16, 2.09) (1.15, 1.75) Other Secondary SGA-IBS Daily IBS Bloating Daily IBS Ab Pain Daily TARGET 1 TARGET 2 Combined TARGET 1 TARGET 2 Combined TARGET 1 TARGET 2 Combined (1.18, 2.18) (1.09, 1.99) (1.20, 1.83) (1.10, 2.04) (1.24, 2.25) (1.24, 1.89) (1.00, 1.83) (1.01, 1.81) (1.06, 1.61) < FDA Proposed TARGET 1 Ab Pain & Stool TARGET 2 Daily (FDA) Combined TARGET 1 Ab Pain Daily TARGET 2 (FDA) Combined TARGET 1 Stool Consist. TARGET 2 Daily (FDA) Combined (1.01, 1.83) (1.08, 1.92) (1.14, 1.72) (0.98, 1.75) (1.03, 1.83) (1.09, 1.64) (1.24, 2.33) (1.09, 2.00) (1.27, 1.97) < Odds Ratio and 95% CI Favors Placebo Favors Rifaximin Pimentel. et al. NEJM
19 Patients With Adequate Relief, % Alosetron * Treatment * * * * * * * * Follow-up Alosetron (n=279 ) Placebo (n=290 ) 10 0 *P<.05; Diarrhea-predominant intention to treat (ITT) population. Chey WD, et al. Am J Gastroenterol. 2004;99: Months
20 Randomize 1:1 TARGET 3 TRIAL Open-label Treatment Phase Double-blind Treatment Phases Screening 7-13 d PBO Study Day 1 Open-Label Rifaximin 550 TID x 2 weeks 2w RFX 4w f/u Maintenance Phase Variable up to 18w Non-Responders Withdrawn and proceed to EOS Phase First Repeat Treatment 2w RFX Primary Evaluation Period 2w PBO 4w f/u 4w f/u Maintenance Phase 6w 6w Second Repeat Treatment 2w RFX 2w PBO 4w f/u 4w f/u Follow up * * * * * Stool sample collection * Only patients with recurrent symptoms randomized 4 W EOS
21 Weekly Average Comparability of Symptom Severity TARGET 3 6 Open Label TARGET 3: All DBR Subjects (n=636) Worst abdominal pain over the last 24hr Double-blind BL Wk 1 Wk 2 Wk 3 Wk 4 Wk 5 Wk 6 BL Wk 1 Time Subjects Do Not Return to Baseline Symptom Severity Following Initial Therapy with Rifaximin Wk 2 Wk 3 Wk 4 Wk 5 Wk 6 Wk 7 Wk 8 Wk 9 Wk 10 Wk 11 Wk 12 Wk 13 Wk 14 Wk 15 Wk 16 Wk 17 Wk 18
22 D-IBS M-IBS C-IBS Constipation-IBS
23 Methane- Important in C-IBS Meta-analysis of studies % % Author Year OR (95% (95% CI) CI) Weight Weight Peled (0.20, (0.20, 3.56) 3.56) Fiedorek (1.60, (1.60, 11.68) 11.68) Pimentel (2.22, (2.22, 14.03) 14.03) Pimentel (2.48, (2.48, ) ) Majewski (0.70, (0.70, 4.67) 4.67) Bratten (1.14, (1.14, 4.33) 4.33) Parodi (0.79, (0.79, 4.51) 4.51) Hwang (8.73, (8.73, ) ) Attaluri (2.06, (2.06, 6.66) 6.66) Overall (I-squared = 64.6%, p = 0.004) 3.51 (2.00, (2.00, 6.16) 6.16) NOTE: Weights are from random effects analysis Kunkel. et al. Dig Dis Sci
24 Methane Slows Intestinal Transit n=5, p< % mean slowing of transit with CH 4 Pimentel. et al. Am J Physiol
25 Methanobrevibacter Smithii- the Cause of Constipation Kim. et al. Dig Dis Sci Hydrogen Producing IBS Stool Methane Producing IBS Stool
26 Stool M. smithii level by qpcr M. Smithii Is the Source of Methane in C-IBS 10 6 Breath Methane Positive (>3ppm) Constipated 10 4 Breath Methane Negative (<3ppm) Normal
27 Methanobrevibacter Smithii or Methane as a Test Dictates Treatment CH4 Eradication P=0.001 Clinical Response P=0.01 Low. et al. Gastroenterol and Hepatol
28 Methane Positive C-IBS Double Blind Placebo Controlled Trial Constipation VAS score P=0.01 Pimentel. et al. Dig Dis Sci
29 VAS score After Treatment Bloating Level by Group P<0.01 Pimentel. et al. Dig Dis Sci
30 VAS score Final Visit Constipation Severity Based on Methane >3ppm Analysis of the Neomycin + Rifaximin Group P=0.04 Pimentel. et al. ACG
31 SIBO Treatment Strategy IBS SYMPTOMS LACTULOSE BREATH TEST Hydrogen Positive Methane Positive Rifaximin Rifaximin+Neomycin Symptom Re-evaluation/Retest No Response Pimentel. Am J Gastroenterol Prokinetic Investigate
32 IBS Microbial Hypothesis Acute Gastroenteritis CdtB Toxin Autoimmunity to vinculin Gut ICC/neuronal Changes Bacterial Overgrowth IBS
33 Risk of PI-IBS Increases 7-Fold After Infectious Gastroenteritis* Study (year/bacteria) Ji (2005/Shigella) Mearin (2005/Salmonella) Wang (2004/Unspecified) Okhuysen (2004/Unspecified) Cumberland (2003/Unspecified) llnyckyj (2003/Unspecified) Parry (2003/Bacterial NOS) Rodriguez (1999/Bacterial NOS) Pooled estimate Protective Effect Increased Risk OR (95% Cl) 2.8 ( ) 8.7 ( ) 10.7 ( ) 10.1 ( ) 6.6 ( ) 2.7 ( ) 9.9 ( ) 11.3 ( ) 7.3 ( ) 9.8% IBS in cases vs 1.2% IBS in controls OR *Systematic review of 8 studies involving 588,061 subjects; follow-up ranged from 3 to 12 months. Halvorsen HA, et al. Am J Gastroenterol. 2006;101:
34 OR for IBS After Acute Gastroenteritis* Characteristics of Acute Illness Identify Patients at Risk for PI-IBS 10 8 P= P= P=.029 P=.006 P=.001 P= Age Female Diarrhea >7 d Bloody Stools Abdominal Cramps *Identified from multiple logistic regression analysis from 2069 participating in the Walkerton Health Study. Marshall JK, et al. Gastroenterology. 2006;131: Weight Loss >10 lbs
35 Post-Infectious IBS = IBS Shah, et al. J Neurogastroenterol Motil, 2012.
36 Mechanism: Rat Model (SIBO = IBS) n=33 n=33 C. jejuni Stool = Campy- No Acute Gastroenteritis Stool = Campy+ Acute Gastroenteritis 3 Months After Recovery Stool Consistency Evaluation Stool = Campy- Recovery Pimentel. et al. Dig Dis Sci, Bacterial Quantitation by RT-PCR of Duodenum, Jejunum, Ileum
37 Mechanism: Rat Model (SIBO = IBS) 17% 21% 27% 6.7% Pimentel. et al. Dig Dis Sci, months after Campylobacter jejuni infection
38 Rectal Lymphocytes % in Rats Mechanism: Rat Model (SIBO = IBS) P<0.001 Persistent altered stool consistency P<0.01 Increased rectal lymphocytes P=0.84 P<0.01 Pimentel. et al. Dig Dis Sci, 2008.
39 8 C+/SIBO+ 8 C+/SIBO- 8 C- CD117 immunostain of duodenal, jejunal, ileal cross-sections (Dako Cytomation, Inc; Carpinteria, CA) Randomized and coded 2 independent, blinded readers reported as DMP ICC per villus
40 ICC Level and SIBO * P<0.05 vs. C- # P<0.001 vs. C- * # * Jee. et al. World J Gastroenterol
41 Ileal ICC in Controls Jee. et al. World J Gastroenterol x
42 Ileal ICC in C+/SIBO- Jee. et al. World J Gastroenterol x
43 Ileal ICC in C+/SIBO+ Jee. et al. World J Gastroenterol x
44 Cytolethal Distending Toxin (CDT) C. jejuni E. Coli Salmonella Shigella Cytolethal Distending Toxin (CDT) A B All cause IBS Cell Entry G2 Phase Unknown Arrest
45 Cytolethal Distending Toxin (CDT) Wild type Campy CdtB (-) Campy Campy + Rifaximin Daily stool for Campy (length of colonization) 3 months later stool evaluation Bacterial quantitative PCR of small bowel
46 CDT and Rifaximin in IBS: Rat Model Campy CdtB- P-value Rifaximin P-value Stool % wet weight 60.1± ± ± Consistency 1.51± ±0.27 < ±0.30 < Standard Deviation Proportion with normal bowel form all 3 days Note: No significant differences were seen between CDT- and Rifaximin treated arms of the study. Neurogastroenterol Motil ± ±2.4 < ±2.3 < % 50.0% <0.01 OR= % < OR=6.7
47 Molecular Mimicry Ganglia DMP ICC Pre-immune Serum Anti-CDT Antibodies
48 IBS Mechanism/Nerve Damage GANGLIA OF HUMAN ILEAL SECTIONS wab S-100 S wab Anti-CdtB is also Anti-glial in humans Morales. et al. Dig Dis Sci
49 Vinculin- The Link to IBS
50 Vinculin Focal adhesion plaques Actin filaments
51 Molecular Mimicry/Autoimmunity Cytolethal Distending Toxin B Human Vinculin
52 Molecular Mimicry/Autoimmunity Cytolethal Distending Toxin B Human Vinculin
53 Vinculin Expression and SIBO Rats with single or double infection, SIBO or no SIBO
54 Immunization Trial Recombinant CdtB Campylobacter Sprague-Dawley Rats
55 Vinculin Expression and Small Bowel Bacterial Levels % of rats with Elevated Small Bowel Bacteria Triantafyllou. DDW, 2014.
56 Blood Test For IBS D-IBS subjects (N=2375) Subjects with IBD (N=142) which included Crohn s disease (N=73) and ulcerative colitis (N=69) Subjects with celiac disease (N=121) Healthy subjects (N=43)
57 Blood Test For IBS 1 AUC=0.81 (95% CI, ) marker Anti-CdtB Anti-vinculin AUC=0.62 (95% CI, ) Anti-vinculin Ab Anti-CdtB Ab specificity
58 IBS Pathophysiologic Sequence Food Poisoning Bacterial Toxin? Autoimmunity Gut Nerve Damage Bacterial Overgrowth IBS E. Coli C. jejuni Shigella Salmonella Cytolethal Distending Toxin (CDT B) Anti-vinculin -Reduced ICC -Reduced MMC -Breath testing -Culture -qpcr -deep sequencing Antibiotics
59 IBS/SIBO WORKSHEET 3.0 STRESS Molecular Mimicry PROKINETIC CRF Acute Gastroenteritis Immune response Anti-CDT Ab Other Ab Anti-vinculin antibody Reduced DMP-ICC SMALL BOWEL DYSMOTILITY COLON Immunity to Infection METHANE SLOW TRANSIT C-IBS SIBO/ IBS ANTIBIOTIC HYDROGEN D- AND M-IBS
60 Conclusions Small intestinal bacterial changes are seen in at least 60% of IBS. M. smithii (methane production) slows transit and is associated with constipation Breath testing strategizes the treatment for IBS Acute gastroenteritis causes IBS C. jejuni gastroenteritis causes SIBO in rats through CdtB neurotoxicity CdtB can cause autoimmunity to vinculin via molecular mimicry Serum anti-cdtb and anti-vinculin can distinguish IBS from IBD IBS is an organic disease
61 Acknowledgements Motility Research Team/Endocrine Team Gene Kim Stacy Weitsman Walter Morales Shari Chua Gillian Barlow, PhD Chris Chang, MD, PhD Sequencing Team Vincent Funari, PhD Jie Tang, PhD Jordan Brown Ruchi Mathur, MD, FRCP(C) Mark Goodarzi, MD, PhD Michelle Jones, PhD Zachary Marsh Emily Marsh Venkata Pokkunuri Ali Rezaie, MD, MPH Pat Guerry, PhD Mark Riddle, MD Michael Prouty, MD Brooks Cash, MD Evangelos Giamarellos-Bourboulis, MD Emmanouill Pyleris, MD Katerina Pistikis, MD Kostas Triantafyllou, MD
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