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Evaluating Immunotoxicity of Quaternary Ammonium Compounds

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Evaluating Immunotoxicity of Quaternary Ammonium Compounds Evaluating Immunotoxicity of Quaternary Ammonium Compounds Valerie A. McDonald Thesis submitted to the faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the degree of Master of Science in Biological Sciences Terry C. Hrubec, Co‐Chair Jill Sible, Co‐Chair Caroline N. Jones, Member Xin M. Luo, Member Aug 11th, 2017 Blacksburg, VA Keywords: Quaternary Ammonium Compounds, Immunotoxicity, Development, DIT, Microbiome, ADBAC, DDAC Evaluating Immunotoxicity of Quaternary Ammonium Compounds Valerie A. McDonald Abstract Alkyl dimethyl benzyl ammonium chloride (ADBAC) and didecyl dimethyl ammonium chloride (DDAC) are common quaternary ammonium compounds used as disinfectants in households, medical, and restaurant settings. They cause occupational skin and respiratory hazards in humans, and developmental and reproductive toxicity in mice. They also cause increased secretions of proinflammatory cytokines in cell lines and vaginal inflammation in porcine models; but have not been evaluated for developmental immunotoxicity. We assessed immunotoxicity in‐vitro with J774A.1 murine macrophage cell line by analyzing cytokine production and phagocytosis; and evaluated developmental immunotoxicity in CD‐1 mice by analyzing antibody production. Additionally, because of the associations between gut microbiome dysbiosis and immune disease, we monitored changes in the microbiome as a result of ADBAC+DDAC exposure. Production of cytokines TNF‐alpha and IL‐6 increased at low ADBAC+DDAC concentrations, and IL‐10 decreased in the murine macrophages with ADBAC+DDAC exposure. The phagocytic function of macrophages was also severely decreased. ADBAC+DDAC altered the mouse microbiome by decreasing the relative abundance of Bacteroides and increases in Clostridia in F0 and F1 generations. IgG primary and secondary responses were altered in F1 male mice; and IgA and IgM production were decreased in secondary response in F2 male mice. Since ADBAC+DDAC show signs of immunotoxicity in mice, further studies are needed to reassess risk for human exposure as ADBAC+DDAC may be contributing to immune disease. Evaluating Immunotoxicity of Quaternary Ammonium Compounds Valerie A. McDonald General Audience Abstract Disinfectants are used every day in households, hospitals, and restaurants. Two common ingredients in disinfectants are alkyl dimethyl benzyl ammonium chloride (ADBAC) and didecyl dimethyl ammonium chloride (DDAC). These chemicals can cause asthma and allergic dermatitis in humans. In animals, they cause reduced fertility, altered development, and tissue inflammation. Disinfectant exposure could potentially alter bacterial populations in the gut. Altered microbial populations are associated with many inflammatory diseases. This study evaluated ADBAC and DDAC for their ability to alter immune function and change bacterial populations in the gut. Exposure to ADBAC and DDAC caused inflammation and altered antibody production for two generations. ADBAC and DDAC exposure also significantly altered bacterial communities in the gut. Both changes in the immune function and changes in the gut bacteria could contribute to inflammatory disease. Humans are exposed frequently to ADBAC and DDAC. If these chemicals alter immune function in humans, they could be contributing significantly to human disease. Acknowledgements I would like to thank my advisor, Dr. Terry Hrubec, who has been a mentor, a role model, and a support figure to me. I would like to thank all of my lab mates for their work; you are both my friends and my co‐workers. iv Table of Contents Abstract…………………………………………….…………………………………………………………………....ii General Audience Abstract……………………………………………….……………………………………...iii Acknowledgments………………………………………………..………………………..………………………..iv List of Tables……………..………………………………...………………………………………………………….vi List of Figures……………..………………………………...…………………………………………………………vii Abbreviations………………………………………………………………………………………………………….x Literature Review………………………………………………………………..………….…………………….…1 Paper One: Decreased Macrophage Function Following in‐vitro ADBAC+DDAC Exposure ………………………………………………………………………………………….…..…………………………….…23 Paper Two: The Effect of ADBAC+DDAC on the Microbiome and Development of the Immune System…………………………………………………….....……………………………………………...38 Conclusions……………………………………………………………………………………………………………...106 References…………………………………………………….………………………………………………………....108 v List of Tables Literature Review Table 1 Summary of Uses for ADBAC; page 19 Table 2 Summary of Uses for DDAC; page 20 Paper 1 Table 1: Summary of Phagocytosis Data from Murine Macrophages; page 30 Table 2: Summary of Cytokine Production; page 32 vi List of Figures Paper 1 Figures Figure 1: Murine Macrophage Viability after ADBAC+DDAC Exposure; page 30 Figure 2: J774A.1 murine macrophages exposure to ADBAC+DDAC and fluorescent beads demonstrated decreased uptake; page 31 Paper 2 Figures Figure 1: Summary of Key Experimental Time-points; page 48 Figure 2: Male Mice During ADBAC+DDAC Exposure; page 49 Figure 3: Food intake and calculated received average each week over six week dosing period; Page 50 Figure 4: IgM F1 Female Primary Response on day 26 and 35; page 51 Figure 5: IgM F1 Males Secondary Response on Day 40; page 51 Figure 6: IgM F1 Female Primary Response on Days 26 and 35; page 52 Figure 7: IgM F1 Female Secondary Response on Day 40; page 52 Figure 8: IgM F2 Male Primary Response on Day 26 and 35; page 53 Figure 9: IgM F2 Males Secondary Response on Day 40; page 54 Figure 10: IgM F2 Female Primary Response on Days 26 and 35; page 55 Figure 11: IgM F2 Female Primary Response on Days 26 and 35; page 55 Figure 12: Comparison between the F2 and F1 Male Responses; page 56 Figure 13: Comparison between the F2 and F1 Female Responses; page 57 vii Figure 14: IgA F1 Males Primary Response on Days 26 and 35; page 58 Figure 15: IgA F1 Males Secondary Response Day 40; page 58 Figure 16: IgA F1 Female Primary Response on Days 26 and 35; page 59 Figure 17: IgA F1 Females Secondary Response; page 60 Figure 18: IgA F2 Males Primary Response on Days 26 and 35; page 60 Figure 19: IgA F2 Males Secondary Response on Day 40; page 61 Figure 20: IgA F2 Females Primary Response on Days 26 and 35; page 62 Figure 21: IgA F2 Females Secondary Response on Day 40; page 62 Figure 22: IgA F2 Compared to F1 Response; page 63 Figure 23: IgA F2 vs F2 Females; page 64 Figure 24: IgG F1 Males Primary Response on days 26 and 35; page 65 Figure 25: IgG F1 Males Secondary Response on Day 40 ;page 65 Figure 26: IgG F1 Female Primary Response; page 67 Figure 27: IgG F1 Female Secondary Response; page 67 Figure 28: IgG F2 Males Primary Response Days 26 and 35; page 68 Figure 29: IgG F2 Males Secondary Response on Day 40; page 68 Figure 30: IgG Comparison Between F1 and F2 Males; page 69 Figure 31: IgG F2 Females Primary Response on Days 26 and 35; page 69 Figure 32: IgG F2 Females Secondary Response on Day 40; page 70 Figure 33: IgG Comparison between F1 and F2 females; page 70 viii Figure 34: Diversity of F0 Females Before ADBAC+DDAC Dose; page 72 Figure 35: Diversity of F0 Males Before ADBAC+DDAC Dose; page 73 Figure 36: Diversity of F0 Females One Week After Dose; page 74 Figure 37: Relative Abundance of Different Genera After Dose Start in Female; page 75 Figure 38: Diversity of F0 Males One Week After Dose; page 76 Figure 39: Relative Abundance of Different Genera After Dose Start Males; page 77 Figure 40: Diversity of F1 Females Day 23; page 79 Figure 41: Relative Abundence of Different Genera F1 Females; Day 23 page 80 Figure 42: F1 Diversity of Males Day 23; page 81 Figure 43: Relative Abundance of Genera F1 Males Day 24; page 82 Figure 44: Diversity of F1 Female Day 40; page 84 Figure 45: Relative Abundance of Genera in F1 Females Day 40; page 85 Figure 46: Diversity of F1 Males Day 40; page 86 Figure 47: Diversity of F2 Female Day 40; page 87 Figure 48: Relative Abundance of Genera in F2 Females Day 40; page 89 ix Abbreviations Alkyl dimethyl benzyl ammonium chloride (ADBAC), Analysis of variance (ANOVA), Antigen Presenting Cell (APC), Benzalkonium chloride (BAC), Bisphenol A (BPA), Bovine serum Albumin (BSA), Delayed type hypersensitivity (DTH), Developmental immunotoxicity (DIT), Didecyl dimethyl ammonium chloride (DDAC), Dioctyltin dichloride (DOTC), Di(2-ethylhexyl) phthlate (DEHP), Enzyme linked Immunosorbent assay (ELISA), Extended One Generation Reproductive Toxicity Study (EOGRTS), Gut microbiome (GM), Immunoglobulin M (IgM), Immunoglobulin G (IgG), Immunoglobulin A (IgA), Interferon (INF), Interleukin-1-Beta (IL-1β), Interleukin-8 (IL-8), Interluekin- 18 (IL-18), Interluekin‐1 (IL-1), Interleukin-12 (IL-12), Interleukin-6 (IL-6), Interleukin-12 (IL-12), Interleukin-10 (IL-10), Keyhole limpet hemocyanin (KLH), Lipid Polysaccharide (LPS), Lowest observed adverse effect level (LOAEL), Nitric oxide (NO), Neural tube defects (NTDs), Non steroidal anti-inflammatory drug (NSAID), No observed adverse effect level (NOAEL), Phosphate buffered saline (PBS), Plaque-forming cell assay (PFC), Polyvinyl Chloride (PVC), Principal component analysis (PCA), Sheep red blood cells (SRBC), T-cell dependent antibody response (TDAR), The Organization for Economic Cooperation and Development (OECD), Tumor necrosis factor (TNF-α), Quaternary Ammonium Compound (QAC) x I. Literature Review Introduction The purpose of this review is to provide an overview of the general immune system, move into toxicity type and testing methods, and how the immune system is tied into the microbiome and give
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