Abstract
Nanotechnology is widely used in the food industry to improve the color, taste, and texture of food products. However, concerns regarding potential undesirable health effects remain. It is expected that interaction of engineered nanomaterials (ENMs) with food ingredients will influence their behavior and the resulting corona. Nonetheless, there are limited systematic studies conducted to clarify this understanding to date. Herein, we investigated the behavior and corona formation of food grade titanium dioxide (TiO2) and silicon dioxide (SiO2) in solutions of model food ingredients including bovine serum albumin (BSA) and sucrose. Measurements using dynamic light scattering (DLS) showed that both TiO2 and SiO2 nanoparticles displayed a decrease in agglomerate sizes in the presence of both food ingredients. Both particles were negatively charged in all the conditions tested. Corona adsorption studies were carried out using multiple complementary methods including Fourier transform infrared (FTIR) spectroscopy, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-ToF-MS), transmission electron microscopy (TEM), micro bicinchoninic acid (BCA) protein assay, and thermogravimetric analysis (TGA). Comparative investigation showed that sucrose could disperse both particles more effectively than BSA and that SiO2 displayed greater adsorption capacity for both BSA and sucrose, compared to TiO2. Taken collectively, this study demonstrated the importance of considering food ingredient effects when mapping the behavior of ENMs in food products. Such understanding could be significant in the evaluation of biological effects, such as toxicity, of ENMs used in food products.
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References
Athinarayanan J, Alshatwi AA, Periasamy VS, Al-Warthan AA (2015) Identification of nanoscale ingredients in commercial food products and their induction of mitochondrially mediated cytotoxic effects on human mesenchymal stem cells. J Food Sci 80:N459–N464. https://doi.org/10.1111/1750-3841.12760
Athinarayanan J, Periasamy VS, Alsaif MA, Al-Warthan AA, Alshatwi AA (2014) Presence of nanosilica (E551) in commercial food products: TNF-mediated oxidative stress and altered cell cycle progression in human lung fibroblast cells. Cell Biol Toxicol 30:89–100. https://doi.org/10.1007/s10565-014-9271-8
Bellmann S, Carlander D, Fasano A, Momcilovic D, Scimeca JA, Waldman WJ, Gombau L, Tsytsikova L, Canady R, Pereira DIA, Lefebvre DE (2015) Mammalian gastrointestinal tract parameters modulating the integrity, surface properties, and absorption of food-relevant nanomaterials. Wiley Interdiscip Rev Nanomed Nanobiotechnol 7:609–622. https://doi.org/10.1002/wnan.1333
Bettini S, Boutet-Robinet E, Cartier C, Coméra C, Gaultier E, Dupuy J, Naud N, Taché S, Grysan P, Reguer S, Thieriet N, Réfrégiers M, Thiaudière D, Cravedi JP, Carrière M, Audinot JN, Pierre FH, Guzylack-Piriou L, Houdeau E (2017) Food-grade TiO2 impairs intestinal and systemic immune homeostasis, initiates preneoplastic lesions and promotes aberrant crypt development in the rat colon. Sci Rep 7:40373. https://doi.org/10.1038/srep40373
Canham L (2014) Porous silicon and functional foods. In: Handbook of Porous Silicon, pp 985–997. https://doi.org/10.1007/978-3-319-05744-6_101
Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V (2010) Time evolution of the nanoparticle protein corona. ACS Nano 4:3623–3632. https://doi.org/10.1021/nn901372t
Casals E, Puntes V (2012) Inorganic nanoparticle biomolecular corona: formation, evolution and biological impact. Nanomedicine 7:1917–1930. https://doi.org/10.2217/NNM.12.169
Chaudhry Q, Scotter M, Blackburn J, Ross B, Boxall A, Castle L, Aitken R, Watkins R (2008) Applications and implications of nanotechnologies for the food sector. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25:241–258. https://doi.org/10.1080/02652030701744538
Chen H, Zhao R, Wang B, Cai C, Zheng L, Wang H, Wang M, Ouyang H, Zhou X, Chai Z, Zhao Y, Feng W (2017) The effects of orally administered Ag, TiO2 and SiO2 nanoparticles on gut microbiota composition and colitis induction in mice. NanoImpact 8:80–88. https://doi.org/10.1016/j.impact.2017.07.005
Chen X-X, Cheng B, Yang YX, Cao A, Liu JH, du LJ, Liu Y, Zhao Y, Wang H (2013) Characterization and preliminary toxicity assay of nano-titanium dioxide additive in sugar-coated chewing gum. Small 9:1765–1774. https://doi.org/10.1002/smll.201201506
Chiang CK, Chen WT, Chang HT (2011) Nanoparticle-based mass spectrometry for the analysis of biomolecules. Chem Soc Rev 40:1269–1281. https://doi.org/10.1039/c0cs00050g
Cushen M, Kerry J, Morris M, Cruz-Romero M, Cummins E (2012) Nanotechnologies in the food industry—recent developments, risks and regulation. Trends Food Sci Technol 24:30–46. https://doi.org/10.1016/j.tifs.2011.10.006
Dekkers S, Krystek P, Peters RJB, Lankveld DPK, Bokkers BGH, van Hoeven-Arentzen PH, Bouwmeester H, Oomen AG (2011) Presence and risks of nanosilica in food products. Nanotoxicology 5:393–405. https://doi.org/10.3109/17435390.2010.519836
Dobrovolskaia MA, Patri AK, Zheng J, Clogston JD, Ayub N, Aggarwal P, Neun BW, Hall JB, McNeil SE (2009) Interaction of colloidal gold nanoparticles with human blood: effects on particle size and analysis of plasma protein binding profiles. Nanomedicine 5:106–117. https://doi.org/10.1016/j.nano.2008.08.001
Duman O, Tunç S (2009) Electrokinetic and rheological properties of Na-bentonite in some electrolyte solutions. Microporous Mesoporous Mater 117:331–338. https://doi.org/10.1016/j.micromeso.2008.07.007
Faust JJ, Doudrick K, Yang Y, Westerhoff P, Capco DG (2014) Food grade titanium dioxide disrupts intestinal brush border microvilli in vitro independent of sedimentation. Cell Biol Toxicol 30:169–188. https://doi.org/10.1007/s10565-014-9278-1
Garvas M, Testen A, Umek P, Gloter A, Koklic T, Strancar J (2015) Protein corona prevents TiO2 phototoxicity. PLoS One 10:e0129577. https://doi.org/10.1371/journal.pone.0129577
Gawali SL, Barick BK, Barick KC, Hassan PA (2017) Effect of sugar alcohol on colloidal stabilization of magnetic nanoparticles for hyperthermia and drug delivery applications. J Alloys Compd 725:800–806. https://doi.org/10.1016/j.jallcom.2017.07.206
Johnston H, Brown D, Kermanizadeh A, Gubbins E, Stone V (2012) Investigating the relationship between nanomaterial hazard and physicochemical properties: informing the exploitation of nanomaterials within therapeutic and diagnostic applications. J Control Release 164:307–313. https://doi.org/10.1016/j.jconrel.2012.08.018
Karlsson HL, Gustafsson J, Cronholm P, Moller L (2009) Size-dependent toxicity of metal oxide particles—a comparison between nano- and micrometer size. Toxicol Lett 188:112–118. https://doi.org/10.1016/j.toxlet.2009.03.014
Kharazian B, Hadipour NL, Ejtehadi MR (2016) Understanding the nanoparticle-protein corona complexes using computational and experimental methods. Int J Biochem Cell Biol 75:162–174. https://doi.org/10.1016/j.biocel.2016.02.008
Lesniak A, Fenaroli F, Monopoli MP, Berg CA, Dawson KA, Salvati A (2012) Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6:5845–5857
Lorenzetti M, Drame A, Šturm S, Novak S (2017) TiO2 (nano)particles extracted from sugar-coated confectionery. J Nanomater 2017:1–14. https://doi.org/10.1155/2017/6298307
Lynch I, Cedervall T, Lundqvist M, Cabaleiro-Lago C, Linse S, Dawson KA (2007) The nanoparticle-protein complex as a biological entity; a complex fluids and surface science challenge for the 21st century. Adv Colloid Interf Sci 134-135:167–174. https://doi.org/10.1016/j.cis.2007.04.021
Lynch I, Dawson KA (2008) Protein-nanoparticle interactions. Nano Today 3:40–47. https://doi.org/10.1016/s1748-0132(08)70014-8
Monopoli MP, Åberg C, Salvati A, Dawson KA (2012) Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol 7:779–786. https://doi.org/10.1038/nnano.2012.207
Park J, Blick RH (2013) A silicon nanomembrane detector for matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) of large proteins. Sensors (Basel) 13:13708–13716. https://doi.org/10.3390/s131013708
Reyes-Coronado D, Rodriguez-Gattorno G, Espinosa-Pesqueira ME, Cab C, de Coss R, Oskam G (2008) Phase-pure TiO2 nanoparticles: anatase, brookite and rutile. Nanotechnology 19:145605. https://doi.org/10.1088/0957-4484/19/14/145605
Rossi M, Cubadda F, Dini L, Terranova ML, Aureli F, Sorbo A, Passeri D (2014) Scientific basis of nanotechnology, implications for the food sector and future trends. Trends Food Sci Technol 40:127–148. https://doi.org/10.1016/j.tifs.2014.09.004
Setyawati MI, Khoo PKS, Eng BH, Xiong S, Zhao X, Das GK, Tan TTY, Loo JSC, Leong DT, Ng KW (2013a) Cytotoxic and genotoxic characterization of titanium dioxide, gadolinium oxide, and poly(lactic-co-glycolic acid) nanoparticles in human fibroblasts. J Biomed Mater Res A 101:633–640. https://doi.org/10.1002/jbm.a.34363
Setyawati MI, Tay CY, Chia SL, Goh SL, Fang W, Neo MJ, Chong HC, Tan SM, Loo SCJ, Ng KW, Xie JP, Ong CN, Tan NS, Leong DT (2013b) Titanium dioxide nanomaterials cause endothelial cell leakiness by disrupting the homophilic interaction of VE-cadherin. Nat Commun 4:1673. https://doi.org/10.1038/ncomms2655
Smolkova B, El Yamani N, Collins AR, Gutleb AC, Dusinska M (2015) Nanoparticles in food. Epigenetic changes induced by nanomaterials and possible impact on health. Food Chem Toxicol 77:64–73. https://doi.org/10.1016/j.fct.2014.12.015
Song L, Yang K, Jiang W, Du P, Xing B (2012) Adsorption of bovine serum albumin on nano and bulk oxide particles in deionized water. Colloids Surf B Biointerfaces 94:341–346. https://doi.org/10.1016/j.colsurfb.2012.02.011
Tedja R, Lim M, Amal R, Marquis C (2012) Effects of serum adsorption on cellular uptake profile and consequent impact of titanium dioxide nanoparticles on human lung cell lines. ACS Nano 6:4083–4093
Tunç S, Duman O, Kancı B (2012) Rheological measurements of Na-bentonite and sepiolite particles in the presence of tetradecyltrimethylammonium bromide, sodium tetradecyl sulfonate and Brij 30 surfactants. Colloids Surf A Physicochem Eng Asp 398:37–47. https://doi.org/10.1016/j.colsurfa.2012.02.006
Urrutia-Ortega IM, Garduño-Balderas LG, Delgado-Buenrostro NL, Freyre-Fonseca V, Flores-Flores JO, González-Robles A, Pedraza-Chaverri J, Hernández-Pando R, Rodríguez-Sosa M, León-Cabrera S, Terrazas LI, van Loveren H, Chirino YI (2016) Food-grade titanium dioxide exposure exacerbates tumor formation in colitis associated cancer model. Food Chem Toxicol 93:20–31. https://doi.org/10.1016/j.fct.2016.04.014
Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780. https://doi.org/10.3762/bjnano.6.181
Wang H, Du L-J, Song Z-M, Chen X-X (2013) Progress in the characterization and safety evaluation of engineered inorganic nanomaterials in food. Nanomedicine 8:2007–2025. https://doi.org/10.2217/NNM.13.176
Weir A, Westerhoff P, Fabricius L, Hristovski K, von Goetz N (2012) Titanium dioxide nanoparticles in food and personal care products. Environ Sci Technol 46:2242–2250. https://doi.org/10.1021/es204168d
Wells MA, Abid A, Kennedy IM, Barakat AI (2012) Serum proteins prevent aggregation of Fe2O3 and ZnO nanoparticles. Nanotoxicology 6:837–846. https://doi.org/10.3109/17435390.2011.625131
Wiechers JW, Musee N (2010) Engineered inorganic nanoparticles and cosmetics: facts, issues, knowledge gaps and challenges. J Biomed Nanotechnol 6:408–431. https://doi.org/10.1166/jbn.2010.1143
Wu J, Wang C, Sun J, Xue Y (2011) Neurotoxicity of silica nanoparticles: brain localization and dopaminergic neurons damage pathways. ACS Nano 5:4476–4489
Xiong S, George S, Yu H, Damoiseaux R, France B, Ng KW, Loo JS (2013) Size influences the cytotoxicity of poly (lactic-co-glycolic acid) (PLGA) and titanium dioxide (TiO2) nanoparticles. Arch Toxicol 87:1075–1086. https://doi.org/10.1007/s00204-012-0938-8
Yada RY, Buck N, Canady R, DeMerlis C, Duncan T, Janer G, Juneja L, Lin M, McClements DJ, Noonan G, Oxley J, Sabliov C, Tsytsikova L, Vázquez-Campos S, Yourick J, Zhong Q, Thurmond S (2014) Engineered nanoscale food ingredients: evaluation of current knowledge on material characteristics relevant to uptake from the gastrointestinal tract. Compr Rev Food Sci Food Saf 13:730–744. https://doi.org/10.1111/1541-4337.12076
Yang Y, Faust JJ, Schoepf J, Hristovski K, Capco DG, Herckes P, Westerhoff P (2016) Survey of food-grade silica dioxide nanomaterial occurrence, characterization, human gut impacts and fate across its lifecycle. Sci Total Environ 565:902–912. https://doi.org/10.1016/j.scitotenv.2016.01.165
Zanganeh S, Spitler R, Erfanzadeh M, Alkilany AM, Mahmoudi M (2016) Protein corona: opportunities and challenges. Int J Biochem Cell Biol 75:143–147. https://doi.org/10.1016/j.biocel.2016.01.005
Zhao Y, Howe JL, Yu Z, Leong DT, Chu JJ, Loo JS, Ng KW (2013) Exposure to titanium dioxide nanoparticles induces autophagy in primary human keratinocytes. Small 9:387–392. https://doi.org/10.1002/smll.201201363
Acknowledgements
The authors would like to acknowledge Dr. Ch’ng Ai Lee, Helen Phang and Dr. Wu Yuansheng from AVA for their technical assistance and critical assessment of this work. The authors would also like to acknowledge the Facility for Analysis, Characterisation, Testing and Simulation (FACTS) at NTU for technical assistance in TEM and XRD analyses.
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Yusoff, R., Nguyen, L.T.H., Chiew, P. et al. Comparative differences in the behavior of TiO2 and SiO2 food additives in food ingredient solutions. J Nanopart Res 20, 76 (2018). https://doi.org/10.1007/s11051-018-4176-8
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DOI: https://doi.org/10.1007/s11051-018-4176-8