2,453
Views
5
CrossRef citations to date
0
Altmetric
Article

Effects of dietary exposure to the engineered nanomaterials CeO2, SiO2, Ag, and TiO2 on the murine gut microbiome

ORCID Icon, , , , , , ORCID Icon, & ORCID Icon show all
Pages 934-950 | Received 28 Apr 2021, Accepted 03 Jun 2021, Published online: 11 Aug 2021

References

  • Aminov, R. I., A. W. Walker, S. H. Duncan, H. J. Harmsen, G. W. Welling, and H. J. Flint. 2006. “Molecular Diversity, Cultivation, and Improved Detection by Fluorescent in Situ Hybridization of a Dominant Group of Human Gut Bacteria Related to Roseburia Spp. or Eubacterium rectale.” Applied and Environmental Microbiology 72: 6371–6376. doi:10.1128/AEM.00701-06.
  • Arumugam, M., J. Raes, E. Pelletier, D. Le Paslier, T. Yamada, D. R. Mende, G. R. Fernandes, et al. MetaHIT Consortium (additional members). 2011. “Enterotypes of the Human Gut Microbiome.” Nature 473 (7346): 174–180. doi:10.1038/nature09944.
  • Augenlicht, L., L. Shi, J. Mariadason, C. Laboisse, and A. Velcich, 2003. “Repression of MUC2 Gene Expression by Butyrate, a Physiological Regulator of Intestinal Cell Maturation.” Oncogene 22 (32): 4983–4992. doi:10.1038/sj.onc.1206521.
  • Benjamini, Y., D. Drai, G. Elmer, N. Kafkafi, and I. Golani, 2001. “Controlling the False Discovery Rate in Behavior Genetics Research.” Behavioural Brain Research. 125 (1–2): 279–284. doi:10.1016/S0166-4328(01)00297-2.
  • Bergin, I. L., and F. A. Witzmann, 2013. “Nanoparticle Toxicity by the Gastrointestinal Route: evidence and Knowledge Gaps.” International Journal of Biomedical Nanoscience and Nanotechnology 3 (1–2): 163–210. doi:10.1504/IJBNN.2013.054515.
  • Binda, C., L. R. Lopetuso, G. Rizzatti, G. Gibiino, V. Cennamo, and A. Gasbarrini, 2018. “Actinobacteria: A Relevant Minority for the Maintenance of Gut Homeostasis.” Digestive and Liver Disease 50 (5): 421–428. doi:10.1016/j.dld.2018.02.012.
  • Bokulich, N. A., Chung, J., Battaglia, T., Henderson, N., Jay, M., Li, H. A., Wu, D. L, et al. 2016. “Antibiotics, Birth Mode, and Diet Shape Microbiome Maturation during Early Life.” Science Translational Medicine 8 (343): 343ra82–343ra82. doi:10.1126/scitranslmed.aad7121.
  • Bokulich, N. A., S. Subramanian, J. J. Faith, D. Gevers, J. I. Gordon, R. Knight, D. A. Mills, and J. G. Caporaso, 2013. “Quality-Filtering Vastly Improves Diversity Estimates from Illumina Amplicon Sequencing.” Nature Methods 10 (1): 57–59. doi:10.1038/nmeth.2276.
  • Bouwmeester, H., P. Brandhoff, H. J. P. Marvin, S. Weigel, and R. J. B. Peters, 2014. “State of the Safety Assessment and Current Use of Nanomaterials in Food and Food Production.” Trends in Food Science & Technology 40 (2): 200–210. doi:10.1016/j.tifs.2014.08.009.
  • Brinkmann, B. W., W. F. Beijk, R. C. Vlieg, S. J. T. Van Noort, J. Mejia, J. L. Colaux, S. Lucas, G. Lamers, W. Peijnenburg, and M. G. Vijver, 2021. “Adsorption of Titanium Dioxide Nanoparticles onto Zebrafish Eggs Affects Colonizing Microbiota.” Aquatic Toxicology 232: 105744. doi:10.1016/j.aquatox.2021.105744.
  • Bubnov, R., L. Babenko, L. Lazarenko, M. Kryvtsova, O. Shcherbakov, N. Zholobak, O. Golubnitschaja, and M. Spivak, 2019. “Can Tailored Nanoceria Act as a Prebiotic? Report on Improved Lipid Profile and Gut Microbiota in Obese Mice.” EPMA Journal 10 (4): 317–335. doi:10.1007/s13167-019-00190-1.
  • Buesen, R., R. Landsiedel, U. G. Sauer, W. Wohlleben, S. Groeters, V. Strauss, H. Kamp, and B. Van Ravenzwaay, 2014. “Effects of SiO(2), ZrO(2), and BaSO(4) Nanomaterials with or without Surface Functionalization upon 28-Day Oral Exposure to Rats.” Archives of Toxicology 88 (10): 1881–1906. doi:10.1007/s00204-014-1337-0.
  • Callahan, B. J., P. J. Mcmurdie, M. J. Rosen, A. W. Han, A. J. Johnson, and S. P. Holmes, 2016. “DADA2: High-Resolution Sample Inference from Illumina Amplicon Data.” Nature Methods 13 (7): 581–583. doi:10.1038/nmeth.3869.
  • Cani, P. D., A. M. Neyrinck, F. Fava, C. Knauf, R. G. Burcelin, K. M. Tuohy, G. R. Gibson, and N. M. Delzenne, 2007. “Selective Increases of Bifidobacteria in Gut Microflora Improve High-Fat-Diet-Induced Diabetes in Mice through a Mechanism Associated with Endotoxaemia.” Diabetologia 50 (11): 2374–2383. doi:10.1007/s00125-007-0791-0.
  • Cao, X., Y. Han, M. Gu, H. Du, M. Song, X. Zhu, G. Ma, et al. 2020. “Foodborne Titanium Dioxide Nanoparticles Induce Stronger Adverse Effects in Obese Mice than Non-Obese Mice: Gut Microbiota Dysbiosis, Colonic Inflammation, and Proteome Alterations.” Small 16 (36): e2001858. doi:10.1002/smll.202001858.
  • Chang, P. V., L. Hao, S. Offermanns, and R. Medzhitov, 2014. “The Microbial Metabolite Butyrate Regulates Intestinal Macrophage Function via Histone Deacetylase Inhibition.” Proceedings of the National Academy of Sciences 111 (6): 2247–2252. doi:10.1073/pnas.1322269111.
  • Chawengkijwanich, C., and Y. Hayata, 2008. “Development of TiO2 Powder-Coated Food Packaging Film and Its Ability to Inactivate Escherichia coli in Vitro and in Actual Tests.” International Journal of Food Microbiology 123 (3): 288–292. doi:10.1016/j.ijfoodmicro.2007.12.017.
  • Chen, H., R. Zhao, B. Wang, C. Cai, L. Zheng, H. Wang, M. Wang, et al. 2017. “The Effects of Orally Administered Ag, TiO 2 and SiO 2 Nanoparticles on Gut Microbiota Composition and Colitis Induction in Mice.” NanoImpact 8: 80–88. doi:10.1016/j.impact.2017.07.005.
  • Chen, Z., S. Han, D. Zhou, S. Zhou, and G. Jia, 2019. “Effects of Oral Exposure to Titanium Dioxide Nanoparticles on Gut Microbiota and Gut-Associated Metabolism in Vivo.” Nanoscale 11 (46): 22398–22412. doi:10.1039/C9NR07580A.
  • De Clercq, N. C., A. K. Groen, J. A. Romijn, and M. Nieuwdorp, 2016. “Gut Microbiota in Obesity and Undernutrition.” Advances in Nutrition 7 (6): 1080–1089. doi:10.3945/an.116.012914.
  • De Simone, C., A. Ciardi, A. Grassi, S. Lambert Gardini, S. Tzantzoglou, V. Trinchieri, S. Moretti, and E. Jirillo, 1992. “Effect of Bifidobacterium bifidum and Lactobacillus acidophilus on Gut Mucosa and Peripheral Blood B Lymphocytes.” Immunopharmacology and Immunotoxicology 14 (1–2): 331–340. doi:10.3109/08923979209009228.
  • Dekkers, S., P. Krystek, R. J. Peters, D. P. Lankveld, B. G. Bokkers, P. H. Van Hoeven-Arentzen, H. Bouwmeester, and A. G. Oomen, 2011. “Presence and Risks of Nanosilica in Food Products.” Nanotoxicology 5 (3): 393–405. doi:10.3109/17435390.2010.519836.
  • EFSA. 2016a. “Re-Evaluation of Titanium Dioxide (E 171) as a Food Additive.” EFSA Journal 14 (9): e04545. doi:10.2903/j.efsa.2016.4545.
  • EFSA. 2016b. “Scientific Opinion on the Re‐Evaluation of Silver (E 174) as Food Additive.” EFSA Journal 14 (1): 4364. doi:10.2903/j.efsa.2016.4364.
  • FDA. 2020. Title 21 of Code of the Federal Regulations, CFR §73.575. Titanium dioxide.
  • FDA. 2021. Title 21 of Code of the Federal Regulations, CFR §172.480. Silicon dioxide.
  • Griffiths, E. A., L. C. Duffy, F. L. Schanbacher, H. Qiao, D. Dryja, A. Leavens, J. Rossman, G. Rich, D. Dirienzo, and P. L. Ogra, 2004. “In Vivo Effects of Bifidobacteria and Lactoferrin on Gut Endotoxin Concentration and Mucosal Immunity in Balb/c Mice.” Digestive Diseases and Sciences 49 (4): 579–589. doi:10.1023/B:DDAS.0000026302.92898.ae.
  • Hadrup, N., K. Loeschner, A. Bergstrom, A. Wilcks, X. Gao, U. Vogel, H. L. Frandsen, E. H. Larsen, H. R. Lam, and A. Mortensen, 2012. “Subacute Oral Toxicity Investigation of Nanoparticulate and Ionic Silver in Rats.” Archives of Toxicology 86 (4): 543–551. doi:10.1007/s00204-011-0759-1.
  • Hardy, A., D. Benford, T. Halldorsson, M. J. Jeger, H. K. Knutsen, S. More, H. Naegeli, et al. 2018. “Guidance on Risk Assessment of the Application of Nanoscience and Nanotechnologies in the Food and Feed Chain: Part 1, Human and Animal Health.” EFSA Journal. 16: e05327.
  • Heo, M. B., M. Kwak, K. S. An, H. J. Kim, H. Y. Ryu, S. M. Lee, K. S. Song, I. Y. Kim, J. H. Kwon, and T. G. Lee, 2020. “Oral Toxicity of Titanium Dioxide P25 at Repeated Dose 28-Day and 90-Day in Rats.” Particle and Fibre Toxicology 17 (1): 34. doi:10.1186/s12989-020-00350-6.
  • Heyder, J., J. Gebhart, G. Rudolf, C. F. Schiller, and W. Stahlhofen, 1986. “Deposition of Particles in the Human Respiratory Tract in the Size Range 0.005–15 µm.” Journal of Aerosol Science 17 (5): 811–825-811–825. doi:10.1016/0021-8502(86)90035-2.
  • Hillman, E. T., A. J. Kozik, C. A. Hooker, J. L. Burnett, Y. Heo, V. A. Kiesel, C. J. Nevins, et al. 2020. “Comparative Genomics of the Genus Roseburia Reveals Divergent Biosynthetic Pathways That May Influence Colonic Competition among Species.” Microb Genom 6 (7). doi:10.1099/mgen.0.000399.
  • Hornung, B. V. H., R. D. Zwittink, and E. J. Kuijper, 2019. “Issues and Current Standards of Controls in Microbiome Research.” FEMS Microbiology Ecology 95 (5). doi:10.1093/femsec/fiz045.
  • Hsu, P. I., C. Y. Pan, J. Y. Kao, F. W. Tsay, N. J. Peng, S. S. Kao, H. M. Wang, Taiwan Acid-Related Disease Study, G, et al. 2018. “Helicobacter pylori Eradication with Bismuth Quadruple Therapy Leads to Dysbiosis of Gut Microbiota with an Increased Relative Abundance of Proteobacteria and Decreased Relative Abundances of Bacteroidetes and Actinobacteria.” Helicobacter 23 (4): e12498. doi:10.1111/hel.12498.
  • Huang, X. Z., Z. R. Li, L. B. Zhu, H. Y. Huang, L. L. Hou, and J. Lin, 2014. “Inhibition of p38 Mitogen-Activated Protein Kinase Attenuates Butyrate-Induced Intestinal Barrier Impairment in a Caco-2 Cell Monolayer Model.” Journal of Pediatric Gastroenterology & Nutrition 59 (2): 264–269. doi:10.1097/MPG.0000000000000369.
  • Kampfer, AaM, M. Busch, and R. P. F. Schins, 2020. “Advanced in Vitro Testing Strategies and Models of the Intestine for Nanosafety Research.” Chemical Research in Toxicology 33 (5): 1163–1178. doi:10.1021/acs.chemrestox.0c00079.
  • Karlsson, F. H., V. Tremaroli, I. Nookaew, G. Bergstrom, C. J. Behre, B. Fagerberg, J. Nielsen, and F. Backhed, 2013. “Gut Metagenome in European Women with Normal, Impaired and Diabetic Glucose Control.” Nature 498 (7452): 99–103. doi:10.1038/nature12198.
  • Keller, A. A., S. Mcferran, A. Lazareva, and S. Suh, 2013. “Global Life Cycle Releases of Engineered Nanomaterials.” Journal of Nanoparticle Research 15 (6): 1–17. doi:10.1007/s11051-013-1692-4.
  • Kessler, R. 2011. “Engineered Nanoparticles in Consumer Products: Understanding a NewIngredient.” Environmental Health Perspectives 119 (3): A120–A125. doi:10.1289/ehp.119-a120.
  • Koh, A., F. D. Vadder, P. Kovatcheva-Datchary, and F. Bäckhed, 2016. “From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites.” Cell 165 (6): 1332–1345-1332–1345. doi:10.1016/j.cell.2016.05.041.
  • Kong, G., K. L. Cao, L. M. Judd, S. Li, T. Renoir, and A. J. Hannan, 2020. “Microbiome Profiling Reveals Gut Dysbiosis in a Transgenic Mouse Model of Huntington's Disease.” Neurobiology of Disease 135: 104268. doi:10.1016/j.nbd.2018.09.001.
  • Lamas, B., N. Martins Breyner, and E. Houdeau, 2020. “Impacts of Foodborne Inorganic Nanoparticles on the Gut Microbiota-Immune Axis: potential Consequences for Host Health.” Particle and Fibre Toxicology 17 (1): 19. doi:10.1186/s12989-020-00349-z.
  • Larsen, N., F. K. Vogensen, F. W. J. van den Berg, D. S. Nielsen, A. S. Andreasen, B. K. Pedersen, W. A. Al-Soud, S. J. Sørensen, L. H. Hansen, and M. Jakobsen, 2010. “Gut Microbiota in Human Adults with Type 2 Diabetes Differs from Non-Diabetic Adults.” PLOS One 5 (2): e9085. doi:10.1371/journal.pone.0009085.
  • Laukens, D., B. M. Brinkman, J. Raes, M. De Vos, and P. Vandenabeele, 2016. “Heterogeneity of the Gut Microbiome in Mice: guidelines for Optimizing Experimental Design.” FEMS Microbiology Reviews 40 (1): 117–132. doi:10.1093/femsre/fuv036.
  • Le, K. A., Y. Li, X. Xu, W. Yang, T. Liu, X. Zhao, Y. G. Tang, et al. 2012. “Alterations in Fecal Lactobacillus and Bifidobacterium Species in Type 2 Diabetic Patients in Southern China Population.” Frontiers in Physiology 3: 496.
  • Lee, J., J.-S. Jeong, S. Y. Kim, S.-J. Lee, Y.-J. Shin, W.-J. Im, S.-H. Kim, et al. 2019. “Safety Assessment of Cerium Oxide Nanoparticles: Combined Repeated-Dose Toxicity With Reproductive/Developmental Toxicity Screening Andbiodistribution in Rats.” Nanotoxicology 14 (5): 696–710. doi:10.1080/17435390.2020.1751322.
  • Li, X., Y. Zhang, B. Li, J. Cui, N. Gao, H. Sun, Q. Meng, et al. 2019. “Prebiotic Protects against Anatase Titanium Dioxide Nanoparticles-Induced Microbiota-Mediated Colonic Barrier Defects.” NanoImpact 14: 100164. doi:10.1016/j.impact.2019.100164.
  • Lim, M. Y., H. J. You, H. S. Yoon, B. Kwon, J. Y. Lee, S. Lee, Y. M. Song, K. Lee, J. Sung, and G. Ko, 2017. “The Effect of Heritability and Host Genetics on the Gut Microbiota and Metabolic Syndrome.” Gut 66 (6): 1031–1038. doi:10.1136/gutjnl-2015-311326.
  • Liu, H., J. Wang, T. He, S. Becker, G. Zhang, D. Li, and X. Ma, 2018. “Butyrate: A Double-Edged Sword for Health?” Advances in Nutrition 9 (1): 21–29. doi:10.1093/advances/nmx009.
  • Louis, P., and H. J. Flint, 2009. “Diversity, Metabolism and Microbial Ecology of Butyrate-Producing Bacteria from the Human Large Intestine.” FEMS Microbiology Letters 294 (1): 1–8. doi:10.1111/j.1574-6968.2009.01514.x.
  • Maynard, A., and E. Michelson, 2005. The Nanotechnology Consumer Products Inventory. Woodrow Wilson International Center for Scholars.
  • Mcmurdie, P. J., and S. Holmes, 2013. “Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data.” PLOS One. 8 (4): e61217. doi:10.1371/journal.pone.0061217.
  • Mu, W., Y. Wang, C. Huang, Y. Fu, J. Li, H. Wang, X. Jia, and Q. Ba, 2019. “Effect of Long-Term Intake of Dietary Titanium Dioxide Nanoparticles on Intestine Inflammation in Mice.” Journal of Agricultural and Food Chemistry 67 (33): 9382–9389. doi:10.1021/acs.jafc.9b02391.
  • Murphy, E. F., P. D. Cotter, S. Healy, T. M. Marques, O. O'sullivan, F. Fouhy, S. F. Clarke, et al. 2010. “Composition and Energy Harvesting Capacity of the Gut Microbiota: relationship to Diet, Obesity and Time in Mouse Models.” Gut 59 (12): 1635–1642. doi:10.1136/gut.2010.215665.
  • Neyrinck, A. M., S. Possemiers, W. Verstraete, F. De Backer, P. D. Cani, and N. M. Delzenne, 2012. “Dietary Modulation of Clostridial Cluster XIVa Gut Bacteria (Roseburia Spp.) by Chitin-Glucan Fiber Improves Host Metabolic Alterations Induced by High-Fat Diet in Mice.” Journal of Nutritional Biochemistry 23 (1): 51–59. doi:10.1016/j.jnutbio.2010.10.008.
  • O'hara, A. M., and F. Shanahan, 2006. “The Gut Flora as a Forgotten Organ.” EMBO Reports 7 (7): 688–693. doi:10.1038/sj.embor.7400731.
  • Oberdorster, G., E. Oberdorster, and J. Oberdorster, 2005. “Nanotoxicology: An Emerging Discipline Evolving from Studies of Ultrafine Particles.” Environmental Health Perspectives 113: 823–839.
  • Paassen, N. B.-V., A. Vincent, P. J. Puiman, M. Van Der Sluis, J. Bouma, G. Boehm, J. B. Van Goudoever, I. Van Seuningen, and I. B. Renes, 2009. “The Regulation of Intestinal Mucin MUC2 Expression by Short-Chain Fatty Acids: implications for Epithelial Protection.” Biochemical Journal 420 (2): 211–219. 211–219. doi:10.1042/BJ20082222.
  • Park, J. C., and S. H. Im, 2020. “Of Men in Mice: The Development and Application of a Humanized Gnotobiotic Mouse Model for Microbiome Therapeutics.” Experimental & Molecular Medicine 52 (9): 1383–1396. doi:10.1038/s12276-020-0473-2.
  • Peng, L., Z. R. Li, R. S. Green, I. R. Holzman, and J. Lin, 2009. “Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers.” The Journal of Nutrition 139 (9): 1619–1625. doi:10.3945/jn.109.104638.
  • Pietroiusti, A., A. Magrini, and L. Campagnolo, 2016. “New Frontiers in Nanotoxicology: Gut Microbiota/Microbiome-Mediated Effects of Engineered Nanomaterials.” Toxicology and Applied Pharmacology 299: 90–95. doi:10.1016/j.taap.2015.12.017.
  • Pinget, G., J. Tan, B. Janac, N. O. Kaakoush, A. S. Angelatos, J. O'Sullivan, Y. C. Koay, et al. 2019. “Impact of the Food Additive Titanium Dioxide (E171) on Gut Microbiota-Host Interaction.” Frontiers in Nutrition 6: 57. doi:10.3389/fnut.2019.00057.
  • Rico, C. M., S. Majumdar, M. Duarte-Gardea, J. R. Peralta-Videa, and J. L. Gardea-Torresdey, 2011. “Interaction of Nanoparticles with Edible Plants and Their Possible Implications in the Food Chain.” Journal of Agricultural and Food Chemistry 59 (8): 3485–3498. doi:10.1021/jf104517j.
  • Ruiz-Rodriguez, P. E., D. Meshulam, and U. Lesmes, 2014. “Characterization of Pickering O/W Emulsions Stabilized by Silica Nanoparticles and Their Responsiveness to in Vitro Digestion Conditions.” Food Biophysics 9 (4): 406–415. doi:10.1007/s11483-014-9346-3.
  • Schwab, M., V. Reynders, S. Loitsch, D. Steinhilber, J. Stein, and O. Schroder, 2007. “Involvement of Different Nuclear Hormone Receptors in Butyrate-Mediated Inhibition of Inducible NF Kappa B Signalling.” Molecular Immunology 44 (15): 3625–3632. doi:10.1016/j.molimm.2007.04.010.
  • Schwiertz, A., D. Taras, K. Schafer, S. Beijer, N. A. Bos, C. Donus, and P. D. Hardt, 2010. “Microbiota and SCFA in Lean and Overweight Healthy Subjects.” Obesity 18 (1): 190–195. doi:10.1038/oby.2009.167.
  • Snijders, A. M., S. A. Langley, Y. M. Kim, C. J. Brislawn, C. Noecker, E. M. Zink, S. J. Fansler, et al. 2017. “Influence of Early Life Exposure, Host Genetics and Diet on the Mouse Gut Microbiome and Metabolome.” Nature Microbiology 2 (2): 16221. doi:10.1038/nmicrobiol.2016.221.
  • Sofranko, A., T. Wahle, H. J. Heusinkveld, B. Stahlmecke, M. Dronov, D. Pijnenburg, R. Hilhorst, K. Lamann, C. Albrecht, and R. P. F. Schins, 2021. “Evaluation of the Neurotoxic Effects of Engineered Nanomaterials in C57BL/6J Mice in 28-Day Oral Exposure Studies.” Neurotoxicology 84: 155–171. doi:10.1016/j.neuro.2021.03.005.
  • Szentkuti, L., H. Riedesel, M. L. Enss, K. Gaertner, and W. Von Engelhardt, 1990. “Pre-Epithelial Mucus Layer in the Colon of Conventional and Germ-Free Rats.” The Histochemical Journal 22 (9): 491–497. doi:10.1007/BF01007234.
  • Tamanai-Shacoori, Z., I. Smida, L. Bousarghin, O. Loreal, V. Meuric, S. B. Fong, M. Bonnaure-Mallet, and A. Jolivet-Gougeon, 2017. “Roseburia Spp.: A Marker of Health?” Future Microbiology 12 (2): 157–170. doi:10.2217/fmb-2016-0130.
  • Turnbaugh, P. J., and J. I. Gordon, 2009. “The Core Gut Microbiome, Energy Balance and Obesity.” The Journal of Physiology 587 (17): 4153–4158. doi:10.1113/jphysiol.2009.174136.
  • van den Brule, S., J. Ambroise, H. Lecloux, C. Levard, R. Soulas, P.-J. D. Temmerman, M. Palmai-Pallag, E. Marbaix, and D. Lison, 2015. “Dietary Silver Nanoparticles Can Disturb the Gut Microbiota in Mice.” Particle and Fibre Toxicology 13 (1): 38. doi:10.1186/s12989-016-0149-1.
  • Vance, M. E., T. Kuiken, E. P. Vejerano, S. P. Mcginnis, M. F. Hochella, Jr., D. Rejeski, and M. S. Hull, 2015. “Nanotechnology in the Real World: Redeveloping the Nanomaterial Consumer Products Inventory.” Beilstein Journal of Nanotechnology 6: 1769–1780. doi:10.3762/bjnano.6.181.
  • Verleysen, E., N. Waegeneers, F. Brassinne, S. De Vos, I. O. Jimenez, S. Mathioudaki, and J. Mast, 2020. “Physicochemical Characterization of the Pristine E171 Food Additive by Standardized and Validated Methods.” Nanomaterials 10 (3): 592. doi:10.3390/nano10030592.
  • Vogt, N. M., R. L. Kerby, K. A. Dill-Mcfarland, S. J. Harding, A. P. Merluzzi, S. C. Johnson, C. M. Carlsson, et al. 2017. “Gut Microbiome Alterations in Alzheimer's Disease.” Scientific Reports 7 (1): 13537. doi:10.1038/s41598-017-13601-y.
  • Wang, Y., and K. A. Lecao, 2020. “Managing Batch Effects in Microbiome Data.” Briefings in Bioinformatics 21 (6): 1954–1970. doi:10.1093/bib/bbz105.
  • Wang, Z., G. Xiao, Y. Yao, S. Guo, K. Lu, and Z. Sheng, 2006. “The Role of Bifidobacteria in Gut Barrier Function after Thermal Injury in Rats.” Journal of Trauma 61: 650–657.
  • Wilding, L. A., C. M. Bassis, K. Walacavage, S. Hashway, P. R. Leroueil, M. Morishita, A. D. Maynard, M. A. Philbert, and I. L. Bergin, 2016. “Repeated Dose (28-Day) Administration of Silver Nanoparticles of Varied Size and Coating Does Not Significantly Alter the Indigenous Murine Gut Microbiome.” Nanotoxicology 10 (5): 513–520. doi:10.3109/17435390.2015.1078854.
  • Willemsen, L. E., M. A. Koetsier, S. J. Van Deventer, and E. A. Van Tol, 2003. “Short Chain Fatty Acids Stimulate Epithelial Mucin 2 Expression through Differential Effects on Prostaglandin E(1) and E(2) Production by Intestinal Myofibroblasts.” Gut 52 (10): 1442–1447. doi:10.1136/gut.52.10.1442.
  • Williams, K., J. Milner, M. D. Boudreau, K. Gokulan, C. E. Cerniglia, and S. Khare, 2015. “Effects of Subchronic Exposure of Silver Nanoparticles on Intestinal Microbiota and Gut-Associated Immune Responses in the Ileum of Sprague-Dawley Rats.” Nanotoxicology 9 (3): 279–289. doi:10.3109/17435390.2014.921346.
  • World Health Organization. 2010. FAO/WHO Expert Meeting on the Application of Nanotechnologies in the Food and Agriculture Sectors: Potential Food Safety Implications: Meeting Report. Rome: World Health Organization.
  • Wostmann, B. S. 1981. “The Germfree Animal in Nutritional Studies.” Annual Review of Nutrition 1 (1): 257–279. doi:10.1146/annurev.nu.01.070181.001353.
  • Wu, J., C. Li, J. Zhang, N. W. Menzies, P. M. Bertsch, P. Wang, and P. M. Kopittke, 2020. “Release of Silver from Nanoparticle-Based Filter Paper and the Impacts to Mouse Gut Microbiota.” Environmental Science: NANO 7 (5): 1554–1565. doi:10.1039/C9EN01387C.
  • Wu, X., C. Ma, L. Han, M. Nawaz, F. Gao, X. Zhang, P. Yu, et al. 2010. “Molecular Characterisation of the Faecal Microbiota in Patients with Type II Diabetes.” Current Microbiology 61 (1): 69–78. doi:10.1007/s00284-010-9582-9.
  • Yan, J., D. Wang, K. Li, Q. Chen, W. Lai, L. Tian, B. Lin, Y. Tan, X. Liu, and Z. Xi, 2020. “Toxic Effects of the Food Additives Titanium Dioxide and Silica on the Murine Intestinal Tract: Mechanisms Related to Intestinal Barrier Dysfunction Involved by Gut Microbiota.” Environmental Toxicology and Pharmacology 80: 103485. doi:10.1016/j.etap.2020.103485.
  • Younes, M., G. Aquilina, L. Castle, K. H. Engel, P. Fowler, M. J. Frutos Fernandez, P. Furst, et al. 2021. “Safety Assessment of Titanium Dioxide (E171) as a Food Additive.” EFSA Journal 19: e06585.
  • Zamankhan, F., V. Pirouzfar, F. Ommi, and M. Valihesari, 2018. “Investigating the Effect of MgO and CeO2 Metal Nanoparticle on the Gasoline Fuel Properties: empirical Modeling and Process Optimization by Surface Methodology.” Environmental Science and Pollution Research 25 (23): 22889–22902. doi:10.1007/s11356-018-2066-3.
  • Zelante, T., R. G. Iannitti, C. Cunha, A. De Luca, G. Giovannini, G. Pieraccini, R. Zecchi, et al. 2013. “Tryptophan Catabolites from Microbiota Engage Aryl Hydrocarbon Receptor and Balance Mucosal Reactivity via Interleukin-22.” Immunity 39 (2): 372–385. doi:10.1016/j.immuni.2013.08.003.
  • Zhang, J., Y. Nazarenko, L. Zhang, L. Calderon, K. B. Lee, E. Garfunkel, S. Schwander, et al. 2013. “Impacts of a Nanosized Ceria Additive on Diesel Engine Emissions of Particulate and Gaseous Pollutants.” Environmental Science & Technology 47 (22): 13077–13085. doi:10.1021/es402140u.
  • Zhang, S., X. Jiang, S. Cheng, J. Fan, X. Qin, T. Wang, Y. Zhang, et al. 2020. “Titanium Dioxide Nanoparticles via Oral Exposure Leads to Adverse Disturbance of Gut Microecology and Locomotor Activity in Adult Mice.” Archives of Toxicology 94 (4): 1173–1190. doi:10.1007/s00204-020-02698-2.
  • Zhang, Y., M. Mortimer, and L.-H. Guo, 2020. “Interplay between Engineered Nanomaterials and Microbiota.” Environmental Science: Nano 7 (9): 2454–2485. doi:10.1039/D0EN00557F.