Environmental chemicals, Staphylococcus aureus, and antimicrobial resistance. NAS Workshop
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1 Environmental chemicals, Staphylococcus aureus, and antimicrobial resistance NAS Workshop January 14, 2019 Meghan F. Davis, DVM, MPH, PhD Assistant Professor Department of Environmental Health & Engineering, JHSPH Department of Molecular & Comparative Pathobiology, JHSOM Elizabeth Matsui; Meredith McCormack; Lesliam Quiros Alcala; Shanna Ludwig; Jonathan Shahbazian 1
2 Outline Motivation: How infectious diseases and environmental stressors interact Case example: Staphylococcus aureus Antimicrobial resistance Infection outcomes Asthma outcomes 2 Davis MF, Rankin SC, Schurer JM, Cole S, Conti L, Rabinowitz P for the COHERE Expert Review Group. Checklist for One Health Epidemiological Reporting of Evidence (COHERE). One Health 2017.
3 The Environmental Health Paradigm How exposures cause disease and how we can reduce exposure or response to prevent disease (improve the health of the public) Exposure Internal dose Biologically effective dose Early biological effects Altered structure and function 2015/2016, Johns Hopkins University. All rights reserved. Clinical disease 3
4 Exposure Internal dose Biologically effective dose Toxicology Early biological effects Altered structure and function 2015/2016, Johns Hopkins University. All rights reserved. Clinical disease 4
5 Exposure Epidemiology 2015/2016, Johns Hopkins University. All rights reserved. Clinical disease 5
6 A place for infectious disease in exposure assessment 6 Feingold, B. J., Vegosen, L., Davis, M., Leibler, J. H., Peterson, A. E., & Silbergeld, E. K. A niche for infectious disease in environmental health: rethinking the toxicological paradigm. Environmental Health Perspectives, 2010.
7 Rethinking how microbes fit into the environmental health paradigm Environment Water Animals Vectors Food Soil + Air Dust Pathogens Infectious dose Shedding Infected cells; agent replication Infxn Death Acute dz Chronic dz Recovery Based on: Feingold, B. J., Vegosen, L., Davis, M., Leibler, J. H., Peterson, A. E., & Silbergeld, E. K. A niche for infectious disease in environmental health: rethinking the toxicological paradigm. Environmental Health Perspectives, 2010.
8 Antimicrobial drugs & disinfectants Environment Water Animals Vectors Food Soil + Air Dust Drug-resistant Pathogens Infectious dose Shedding Infected cells; agent replication Infxn Death Acute dz Chronic dz Recovery Based on: Feingold, B. J., Vegosen, L., Davis, M., Leibler, J. H., Peterson, A. E., & Silbergeld, E. K. A niche for infectious disease in environmental health: rethinking the toxicological paradigm. Environmental Health Perspectives, 2010.
9 Example: Methicillin-resistant S. aureus in home dust S. aureus colonizes a third of the U.S. population Colonization is a risk factor for later infection Home contamination rates range from % (reservoir) 9 Davis et al., The role of the household in transmission of methicillin-resistant S. aureus and other staphylococci. The Lancet Infectious Diseases 2012
10 S. aureus nasal colonization & the environmental reservoir Time 10
11 S. aureus nasal colonization & the environmental reservoir Time 11
12 S. aureus nasal colonization & the environmental reservoir Time 12
13 MRSA contamination in homes of people with recent infxn Risk factors for multidrug resistance: Human or pet use of antimicrobial drugs Use of disinfectants on EPA list of MRSA-cidal products Rural residence 13 Shahbazian JH, Hahn PD, Ludwig S, Ferguson J, Baron P, Christ A, Spicer K, Tolomeo P, Torrie AM, Bilker WB, Cluzet VC, Hu B, Julian K, Nachamkin I, Rankin SC, Morris DO, Lautenbach E, and Davis MF. Multidrug and mupirocin resistance in environmental methicillin-resistant Staphylococcus aureus (MRSA) collected from the homes of people diagnosed with a community-onset (CO-) MRSA infection. Applied and Environmental Microbiology 2017, 83(22):e
14 Example: host adaptation of S. aureus CC398 Origin as a methicillin-susceptible S. aureus (MSSA) colonizing humans Jump to livestock associated with: methicillin-resistance gene acquisition tetracycline-resistance gene acquisition Putative selection pressure from tetracycline use in livestock Potential association with zinc Zinc supplementation of livestock feed 14 Price, L. B., Stegger, M., Hasman, H., Aziz, M., Larsen, J., Andersen, P. S., et al. (2012). Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mbio, 3(1), e
15 Example: Lead and S. aureus colonization Scenario 1: Prior Pb exposure in human host prevents colonization by susceptible strains (MSSA) Scenario 2: MRSA strains selected by later Pb exposure in human host Scenario 3: MRSA strains selected by later Pb exposure in the environment 15 Eggers, S., Safdar, N., & Malecki, K. M. (2018). Heavy metal exposure and nasal Staphylococcus aureus colonization: analysis of the National Health and Nutrition Examination Survey (NHANES). Environmental Health : a Global Access Science Source, 17(1),
16 Non-infectious roles of bacteria Inflammation Innate immune response Endotoxin: Gram-negative bacterial lipopolysaccharide (LPS) Enterotoxin: Secreted proteins from Staphylococcus aureus and related bacteria (Gram-positive bacterium) Superantigens: antigens that cause nonspecific T-cell activation & cytokine release 16 Feingold, B. J., Vegosen, L., Davis, M., Leibler, J. H., Peterson, A. E., & Silbergeld, E. K. A niche for infectious disease in environmental health: rethinking the toxicological paradigm. Environmental Health Perspectives, 2010.
17 Infectious Agent as Exposure First Exposure Second Exposure Nth Exposure Acute disease 17
18 Non-infectious roles of bacteria Inflammation Allergy Th2-biased response Typically requires prior exposure / sensitization (IgE) 18 Feingold, B. J., Vegosen, L., Davis, M., Leibler, J. H., Peterson, A. E., & Silbergeld, E. K. A niche for infectious disease in environmental health: rethinking the toxicological paradigm. Environmental Health Perspectives, 2010.
19 Infectious Agent as Exposure First Exposure Sensitization Second Exposure Exacerbation Nth Exposure Worse disease 19
20 Example: Impacts of S. aureus on asthma may vary by age Outcomes, OR [95% CI] Whole population Age 6-30yo Age 31-85yo S. aureusage int Sample size n=16,234 n=8,703 n=7,531 Selected wheeze outcomes Wheeze in past yr 1.02 [0.87, 1.20] 1.35 [1.06, 1.73]* 0.85 [0.68, 1.06] p=0.006 Nocturnal wheeze 1.05 [0.84, 1.34] 1.52 [1.15, 2.00]** 0.79 [0.53, 1.18] p=0.01 ER for wheeze 1.28 [1.00, 1.62]* 1.50 [1.10, 2.03]* 1.11 [0.70, 1.78] p=0.26 Meds for wheeze 0.93 [0.75, 1.14] 1.52 [1.08, 2.14]* 0.64 [0.48, 0.84]** p<0.001 Selected asthma outcomes Asthma ever 1.07 [0.92, 1.23] 1.25 [0.99, 1.56] 0.92 [0.76, 1.11] p=0.04 ER for asthma 1.44 [0.89, 2.31] 1.97 [1.05, 3.73]* 0.85 [0.37, 1.94] p=0.09 bold: p<0.05 *p<0.05, **p<0.01, ***p< Davis MF, Peng R, McCormack MC*, and Matsui EC*. Staphylococcus aureus colonization is associated with wheeze and asthma among U.S. children and young adults. Journal of Allergy and Clinical Immunology 2015.
21 Staphylococcal exposures in home dust are common Asthma Control Evaluation (ACE) Multicenter, randomized controlled trial (completed) Part of the Inner City Asthma Consortium year old inner city children with asthma, n=546 Gene Sample Any detection, n (%) S. aureus (femb) Median [25th, 75th%ile] gene copies per g dust n= (81%) [3022, 46204] SEA n= (62%) 2681 [<LOD, 13442] SEB n= (36%) <LOD [<LOD, 3741] SEC n= (36%) <LOD <LOD, 3205] 21 Davis MF, Ludwig S, Brigham EP, McCormack MC, and Matsui EC. Effect of home exposure to Staphylococcus aureus on asthma in adolescents. Journal of Allergy and Clinical Immunology PMID:
22 Adjusted associations between SA/SE and 2-wk symptoms Outcome S. aureus SEA SEB SEC Reduced activity (OR) 1.00 [0.96, 1.05] 1.12 *** [1.07, 1.17] 1.09 *** [1.05, 1.13] 1.06 *** [1.03, 1.10] Woken by asthma (OR) 1.00 [0.95, 1.07] 1.04 [0.98, 1.10] 1.03 [0.96, 1.09] 1.07 ** [1.02, 1.12] Wheeze (OR) 0.97 [0.94, 1.00] 1.01 [0.98, 1.05] 1.00 [0.97, 1.03] 0.98 [0.95, 1.02] ACT Score (β) 0.03 [-0.10, 0.17] [-0.22, 0.06] [-0.22, 0.05] [-0.20, 0.06] Adjusted for age, sex, race/ethnicity, annual income $15,000, smoking exposure, number of positive skin tests, and recommended treatment step; OR: odds ratio; Lower ACT score indicates worse asthma; *p 0.05; **p 0.01; ***p Davis MF, Ludwig S, Brigham EP, McCormack MC, and Matsui EC. Effect of home exposure to Staphylococcus aureus on asthma in adolescents. Journal of Allergy and Clinical Immunology PMID:
23 Host factors may modify associations Adolescent participants without a history of eczema had worse symptoms when exposed to home dust SEA 23 Davis MF, Ludwig S, Brigham EP, McCormack MC, and Matsui EC. Effect of home exposure to Staphylococcus aureus on asthma in adolescents. Journal of Allergy and Clinical Immunology PMID:
24 Acknowledgments Elizabeth Matsui Meredith McCormack Lesliam Quiros Alcala Ebbing Lautenbach & the CURE trial Davis lab group: Dr. Shanna Ludwig, Dr. Kathryn Dalton, Jonathan Shahbazian, Isha Pandya, Jackie Ferguson, Jonathan Josephs-Spaulding, Andrea Christ, Kris Spicer, Isabel Jimenez-Bush, Ayanna Crear, Dr. Katie Sabella 24 Fisher Center Discovery Program, Morris Animal Foundation, JH Center for a Livable Future, JH Innovation Award, NIH Office of the Director BREATHE Center Inner-City Asthma Consortium / Asthma Control Evaluation cohort
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