11/12/2020

Promoting Gut Commensalism in the Intensive Care Unit

Leslie A. Hamilton, PharmD, FCCP, FCCM, BCPS, BCCCP Associate Professor University of Tennessee Health Science Center College of Pharmacy [email protected]

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Objectives

 To describe the effects of selected medications on the gut  To compare and contrast the effects of parenteral and enteral nutrition on the microbiome  To critique the use of oral decontamination and the subsequent effects on gut  To determine the best practices for stress ulcer prophylaxis with regard to the microbiome  To assess the role of antibiotics in microbiome changes

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Disclosures

 Nothing to disclose

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What is the microbiome?

 Important for overall defense  Viruses, , protists, , and bacteria  Physical mass of several kilograms  Bacteria provide ~10 trillion organisms from 10 major groups  Firmicutes, Bacteriodetes, and Actinobacteria

Am J Physiol Gastrointest Liver Physiol 2017;312:G246-56.

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Microbiome

 The majority of the gut’s are housed in the colon  Bacteria in the gastrointestinal (GI) tract assist in:  Metabolism  Synthesis of certain enzymes and vitamins  Energy production  Drug metabolism

Nutr Clin Pract 2018;33:614-24.

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Image from: https://phys.org/news/2016-03-gut-microbiome-remarkably-stable.html (accessed 8/27/20)

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Medication Class Clinical Changes Effect on Microbiome Dysmotility, decreased Delayed gastric emptying, microbiome diversity, Opioids dysmotility propagation of some pathogenic organisms

Decreased microbiome diversity, decreased elimination Stress Ulcer Prophylaxis Changes in pH of gastric bacteria, overgrowth of acid-intolerant bacteria

Changes in bile salts and Enteral Nutrition Changes in nutrition elimination through translocation

Impaired mucosal immunity, Parenteral Nutrition Changes in nutrition changes in elimination through translocation

Elimination and suppression of Bacterial growth suppression, Antibiotics bacteria development of resistance

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Opioids

 Used frequently in intensive care unit (ICU) setting  Alterations in microbiome may explain some mechanisms of tolerance and addiction  Common side effects relating to GI tract:  Nausea, vomiting, constipation  Changes in gastric motility and emptying

Curr Opin Pharmacol 2017;37:126-30.

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Opioids

 Mechanism of changes:  Relaxation of smooth muscle fibers  Reduced gastric tone  Stimulation of retrograde duodenal contractions  Mu receptors  Found on neurons, myenteric, and submucosal plexus

Curr Opin Pharmacol 2017;37:126-30. Curr Opin Crit Care 2018;24:118-23. 9

Opioids

 Mu receptors:  Reduced motility and secretion  Found on B and T-cells and macrophages  Animal studies have shown morphine can reduce T-cell maturation and change cytokine secretion  May reduce antibody production and major histocompatibility complex

Toxicol Pathol 2017;45:150-6.

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Morphine

 Morphine  Metabolized by liver and hydrolyzed by beta- glucuronidase  Bacteroides and bifidobacteria are major sources of beta-glucuronidase  Affects how morphine is metabolized

Toxicol Pathol 2017;45:150-6.

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Opioids

 Lead to less diversity in microorganisms  May lead to greater resistance and increase virulence factors  May lead to increased risk of Clostridioides difficile and Citrobacter rodentium

Curr Opin Crit Care 2018;24:118-23. Toxicol Pathol 2017;45:150-6. 12

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Stress Ulcer Prophylaxis

 Used in the treatment of gastroesophageal reflux, in GI bleeding, can prevent stress ulcers in ICU patients  Most often proton pump inhibitors (PPI) or histamine-2 receptor blockers (H2B)  Decreased gastric acidity, may lead to colonization of microorganisms

Aliment Pharmacol Ther 2018;47:332-45. Clin Lab Med 2014;34:771-85. 13

PPIs

 PPIs are associated with pH changes in the stomach and proximal duodenum  Fewer changes in the small bowel  Also associated with:  Hypergastrinemia  Changes in luminal contents that affect absorption  Binding to non-gastric H+/K+-ATPases  May increase incidence of C. difficile (CDI) Aliment Pharmacol Ther 2018;47:332-45. Digestion 2018;97:195-204. Clin Lab Med 2014;34:771-85. 14

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PPIs

 Variable literature on PPI effects on microbiome  One study obtained saliva, gastric fluid, and fecal samples from patients  Compared samples in patients taking PPIs vs. not  Bacterial overgrowth in stomachs of PPI users caused by lack of organism killing due to ↑ pH instead of bacterial overgrowth

Clin Transl Gastroenterol 2015;6:e89.

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PPIs

 May cause decreases in:  May cause increases in:  Faecalibacterium   Clostridium   Erysipelotrichales 

Aliment Pharmacol Ther 2018;47:332-45. Clin Lab Med 2014;34:771-85. 16

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PPIs

 Positive effects:  Shown to have bacteriostatic activity in treatment of Helicobacter pylori  Omeprazole may inhibit in vitro growth of gram-positive and negative bacteria  More recent studies show that patients receiving enteral nutrition (EN) may not need stress ulcer prophylaxis

Aliment Pharmacol Ther 2018;47:332-45. J Crit Care 2018;43:108-13. 17

Antibiotics

 Importance of antimicrobial stewardship  Inappropriate use can lead to multidrug- resistant strains of:  Methicillin-resistant  Vancomycin-resistant Enterococcus  Gram-negative rods  Especially associated with broad-spectrum agents

Antimicrob Agents Chemother 2009;53:4264-9.

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Antibiotics

Antibiotic Organism Affected Actinobacteria Azoles Firmicutes Beta-lactams Fusobacteria Clindamycin Fusobacteria Firmicutes (Fusobacteria) Fluoroquinolones Proteobacteria phyla Actinobacteria Nitrofurantoin Firmicutes Bacteriodetes Sulfonamides Firmicutes

PLoS One 2014;(4):1-7. ISME J 2016;10:707-20. Br J Nutr 2014;112:536-46. Genome Biol 2012;13:1-18. J Microbiol Methods 2013;92:387-97. J Antimicrob Chemother 2013;68:214-21. 19

Antibiotic-Induced Diarrhea

 Clindamycin, cephalosporins, and broad- spectrum penicillins show increased risk or antibiotic-associated diarrhea  A significant increase in risk has been associated with treatment for greater than three days (RR 2.28; 95% CI 1.23-4.21)

Antimicrob Agents Chemother 2009;53:4264-9.

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Antibiotic-Induced Diarrhea

 Meta-analysis of over 2 million adverse events submitted to FDA show clindamycin most association with CDI  Odds ratio 46.95 (95% CI 39.49 – 55.82)  Some antibiotics may have protective properties:  Doxycycline  Piperacillin-tazobactam

Int J Med Sci 2019;16:630-5. Antimicrob Agents Chemother 2013;57:2326-32. Infect Control Hosp Epidemiol 2008;29:44-50. BMC Infect Dis 2016;16:159. 21

Chlorhexidine Gluconate

 Used for topical oral decontamination  Antibacterial and antifungal properties with activity against:  Staphylococcus aureus   Some Actinomyces albicans  Relatively safe with mild adverse effects

Iran Endod J 2008;2:113-25.

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Chlorhexidine Gluconate

 Historically, a standard of care in the ICU for the prevention of ventilator-associated pneumonia (VAP)  Most recent evidence shows:  Inconsistencies with decreased VAP and nosocomial pneumonia incidence  No significant effect on morbidity or other patient-centered outcomes in mechanically ventilated patients

J Hosp Infect 2013;84:283-93. JAMA Internal Med 2014;174:751-61. Cochrane Database Syst Rev 2016;10:CD008367. 23

Use in Cardiac Surgery

 Evidence supports a significant reduction in nosocomial infection incidence in mechanically ventilated cardiac surgery patients with the use of chlorhexidine 0.12% oral rinse  Recommended standard practice by the 2003 CDC guidelines for ICU care of patients undergoing cardiac surgery, but not in other patient populations

Lancet Infect Dis 2011:11:845-54. Intensive Care Med 2018;44:1017-26. MMWF Recomm Rep 2004;53:1-36. 24

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Enteral Nutrition

 Enteral nutrition (EN) should be initiated with 24-48 hours  The GI tract forms a network that includes  Autonomic nervous system  Enteric nervous system  Help to innervate the majority of the body’s immune cells

J Parenter Enteral Nutr 2016;40:159-211. Am J Physiol Gastrointest Liver Physiol 2017;312:G246-56. 25

Levels of Defense

 Network has multiple levels of defense:  Allows for digestion  Prevents the development of infection  Releases appropriate antibodies  The GI tract mucosa prevents intraluminal bacteria and toxins from migrating from inside the GI tract

Lancet Gastroenterol Hepatol 2018;3:281-7.

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Mucosal Barrier

 The GI mucosal barrier consists of three layers:  Biochemical layer  Physical barrier  Immunological layer  In the absence of EN, these layers degrade and the mucosa becomes leaky, allowing bacteria to migrate to the submucosal tissue

Lancet Gastroenterol Hepatol 2018;3:281-7.

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Image from: https://courses.lumenlearning.com/suny-ap2/chapter/overview-of-the-digestive-system/ (accessed 8/31/20)

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Mucosal Barrier

 The GI mucosa also experiences rapid cell turnover  The entire mucosa is replaced every 3 – 6 days  For this cell turnover to occur, however, the mucosa must receive enough nutrients through an oral or enteral route

Lancet Gastroenterol Hepatol 2018;3:281-7.

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Organism Functions

 Organisms in the :  Protect against harmful pathogens  Synthesize certain vitamins  Assist with metabolism and excretion  Gut-associated lymphoid tissues (GALT) are also found in the GI tract  Release immunoglobulins to protect mucosal surfaces

Am J Physiol Gastrointest Liver Physiol 2017;312:G246-56.

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Enteral Nutrition

 To minimize the changes on the microbiome, enteral nutrition should remain the mainstay of nutrition support, with parenteral nutrition only used when necessary

Nutrients 2017;9:987.

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Parenteral Nutrition

 Parenteral nutrition (PN) should be restricted to those with restrictions to EN with the need for prolonged alternate forms of nutrition  With PN, gut atrophy occurs and GALT levels ↓  Leads to changes in T lymphocytes and neutrophils and ↓ in memory B cells

J Parenter Enteral Nutr 2016;40:159-211.

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Effects of PN

 Lower amounts of cytokines and immunoglobulin A are produced in the intestines and lungs  With epithelial layer interruption, decreased production of antimicrobial defense mechanisms, and translocation of microbes and toxins  Overproduction of certain bacteria can activate toll-like receptors, which modulates GI tract inflammation Am J Physiol Gastrointest Liver Physiol 2017;312:G246-56. Curr Opin Clin Nutr Metab Care 2015;18:496-500. 33

Effects of PN

 Use of nutrition solely from a parenteral source can increase tumor necrosis factor, which regulates cell growth and death, and shift to more cell destruction

Curr Opin Clin Nutr Metab Care 2015;18:496-500.

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Change in Bacteria with PN

Decreases Increases Bacteroides fragilis Actinobacteria Firmicutes Bacteroidetes Enterobacteriaceae Proteobacteria

Am J Physiol Gastrointest Liver Physiol 2017;312:G246-56.

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Intestinal Failure

 Multiple factors affecting microbiome in patients with intestinal failure:  Amount of remaining portions of the GI anatomy  Bowel resection can change pH, oxygen concentrations, and bile acid circulation, in addition to changes in bacterial flora  Use of EN + PN  Other medications

J Parenter Enteral Nutr 2019;43:194-205.

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Intestinal Failure

 Review of patients in intestinal failure found:  Decreased diversity of microorganisms  Increase in Lactobacillus and Proteobacteria  Especially Enterobacteriaceae and Gammaproteobacteria  Reduced amounts of Bacteroidetes and Firmicutes

J Parenter Enteral Nutr 2019;43:194-205.

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Intestinal Failure

 Other complications include:  D-lactic acidosis  Intestinal failure-associated liver disease  Both may be contributed to by bacterial overgrowth of certain microorganisms  In patients with parenteral nutrition- associated liver disease (PNALD), bile acid composition is altered due to the change in the

Nutrients 2017;9:987.

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Intestinal Failure

 In patients with a normal microbiome:  Bacteria conjugate bile acids to other forms  Regulate metabolism  Assist with absorption of fat and vitamins  In patients with intestinal failure, there has been some association with microbiome changes and development of PNALD

Nutrients 2017;9:987.

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Intestinal Failure

 Patients with intestinal failure have changes in their bile acid composition and excretion  This may lead to:  Inflammation  Changes in microorganisms  PNALD

Nutrients 2017;9:987.

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Conclusions

 Practitioners often underestimate the critical role of the microbiome  Institution of policies and protocols for appropriate use of opioids and PPIs  Antibiotics should be used judiciously  Focus on those with the narrowest spectrum  De-escalate appropriately  Prevent development of multi-drug resistant organisms

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Conclusions

 Utilizing EN is vital in maintaining native gut flora  If PN is required, limit its use to the shortest duration necessary  These strategies can preserve the microbiome and contribute to gut commensalism

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Promoting Gut Commensalism in the Intensive Care Unit

Leslie A. Hamilton, PharmD, FCCP, FCCM, BCPS, BCCCP Associate Professor University of Tennessee Health Science Center College of Pharmacy [email protected]

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24 MSPEN Annual Fall Conference and Chapter Meeting 2020 Promoting Gut Commensalism in the Intensive Care Unit Leslie A. Hamilton, PharmD, FCCP, FCCM, BCPS, BCCCP

Learning Objectives:

1. To describe the effects of selected medications on the gut microbiome 2. To compare and contrast the effects of parenteral and enteral nutrition on the microbiome 3. To critique the use of oral decontamination and the subsequent effects on gut bacteria 4. To determine the best practices for stress ulcer prophylaxis with regard to the microbiome 5. To assess the role of antibiotics in microbiome changes

Assessment Questions:

1. In ICU patients, which is the most protective of the gut’s microbiome? a. Enteral Nutrition b. Parenteral Nutrition c. Famotidine d. Pantoprazole 2. In which patient population has chlorhexidine gluconate 0.12% mouth rinse consistently shown a decrease in nosocomial a. All ICU patients who are mechanically ventilated b. Only non-mechanically ventilate trauma and burn ICU patients c. Cardiothoracic surgery patients receiving mechanical ventilation d. ICU patients who have antibiotic exposure within the previous 90 days 3. Which of the following is the primary mechanism for changes in the microbiome with opiates? a. Bacterial growth suppression b. Impaired mucosal immunity c. Dysmotility d. Changes in bile salts 4. Which scenario presents a greater risk for developing antibiotic-associated diarrhea or Clostridioides difficile infection in the ICU setting? a. A ten-day course of clindamycin 900 mg every 6 hours b. A pre-op and post-op dose of vancomycin IV 1500 mg c. A three-day course of amoxicillin 500 mg PO three times daily d. A seven-day course of doxycycline 100 mg PO twice daily