Reducing Intestinal Digestion and Absorption of Fat Using a Nature-Derived Biopolymer: Interference of Triglyceride Hydrolysis by Nanocellulose

ACS Nano

Volumn 12, Issue 7, 2018, Pages 6469-6479

  Deloid, Glen M ^a   Sohal, Ikjot Singh ^b   Lorente, Laura R ^a   Molina, Ramon M ^a   Pyrgiotakis, Georgios ^a   Stevanovic, Ana ^a   Zhang, Ruojie ^c   McClements, David Julian ^c   Geitner, Nicholas K ^d   Bousfield, Douglas W ^e   Ng, Kee Woei ^f   Loo, Say Chye Joachim ^f   Bell, David C ^g   Brain, Joseph ^a   Demokritou, Philip ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d Duke University   (United States)

^e The University of Maine   (United States)

^f NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^g HARVARD UNIVERSITY   (United States)

Author keywords

bioavailability; nanocellulose; pancreatic lipase; simulated digestion; triglyceride

Indexed keywords

BODY FLUIDS; CELLULOSE; DROPS; FATTY ACIDS; HYDROLYSIS; MOLECULAR DYNAMICS; NUTRITION; SALTS; SCANNING ELECTRON MICROSCOPY;

ENGINEERED NANOMATERIALS; FREE FATTY ACID; GASTROINTESTINAL TRACT; IN-VIVO EXPERIMENTS; INTESTINAL DIGESTION; INTESTINAL EPITHELIUM; PRIMARY MECHANISM; SOLUBILIZATION OF LIPIDS;

NANOCELLULOSE;

CELLULOSE; FAT; FOOD ADDITIVE; NANOMATERIAL; TRIACYLGLYCEROL;

ANIMAL; CHEMISTRY; DIGESTION; HUMAN; HYDROLYSIS; INTESTINE; INTESTINE ABSORPTION; MALE; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CELLULOSE; DIGESTION; FATS; FOOD ADDITIVES; HUMANS; HYDROLYSIS; INTESTINAL ABSORPTION; INTESTINES; MALE; NANOSTRUCTURES; RATS, WISTAR; TRIGLYCERIDES;

EID: 85048372668     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.8b03074     Document Type: Article

References (57)

1. Servin, A. D.; White, J. C. Nanotechnology in Agriculture: Next Steps for Understanding Engineered Nanoparticle Exposure and Risk. NanoImpact 2016, 1, 9-12, 10.1016/j.impact.2015.12.002
2. Schoepf, J. J.; Bi, Y.; Kidd, J.; Herckes, P.; Hristovski, K.; Westerhoff, P. Detection and Dissolution of Needle-like Hydroxyapatite Nanomaterials in Infant Formula. NanoImpact 2017, 5, 22-28, 10.1016/j.impact.2016.12.007
3. McClements, D. J.; DeLoid, G.; Pyrgiotakis, G.; Shatkin, J. A.; Xiao, H.; Demokritou, P. The Role of the Food Matrix and Gastrointestinal Tract in the Assessment of Biological Properties of Ingested Engineered Nanomaterials (IENMs): State of the Science and Knowledge Gaps. NanoImpact 2016, 3, 47-57, 10.1016/j.impact.2016.10.002
4. Bellmann, S.; Carlander, D.; Fasano, A.; Momcilovic, D.; Scimeca, J. A.; Waldman, W. J.; Gombau, L.; Tsytsikova, L.; Canady, R.; Pereira, D. I. A.; Lefebvre, D. E. Mammalian Gastrointestinal Tract Parameters Modulating the Integrity, Surface Properties, and Absorption of Food-Relevant Nanomaterials. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2015, 7, 609-622, 10.1002/wnan.1333
5. Szakal, C.; Roberts, S. M.; Westerhoff, P.; Bartholomaeus, A.; Buck, N.; Illuminato, I.; Canady, R.; Rogers, M. Measurement of Nanomaterials in Foods: Integrative Consideration of Challenges and Future Prospects. ACS Nano 2014, 8, 3128-3135, 10.1021/nn501108g
6. Yada, R. Y.; Buck, N.; Canady, R.; DeMerlis, C.; Duncan, T.; Janer, G.; Juneja, L.; Lin, M.; McClements, D. J.; Noonan, G.; Oxley, J.; Sabliov, C.; Tsytsikova, L.; Vazquez-Campos, S.; Yourick, J.; Zhong, Q.; Thurmond, S. Engineered Nanoscale Food Ingredients: Evaluation of Current Knowledge on Material Characteristics Relevant to Uptake from the Gastrointestinal Tract. Compr. Rev. Food Sci. Food Saf. 2014, 13, 730-744, 10.1111/1541-4337.12076
7. Eleftheriadou, M.; Pyrgiotakis, G.; Demokritou, P. Nanotechnology to the Rescue: Using Nano-Enabled Approaches in Microbiological Food Safety and Quality. Curr. Opin. Biotechnol. 2017, 44, 87-93, 10.1016/j.copbio.2016.11.012
8. Wang, H.; Du, L.-J.; Song, Z.-M.; Chen, X.-X. Progress in the Characterization and Safety Evaluation of Engineered Inorganic Nanomaterials in Food. Nanomedicine (London, U. K.) 2013, 8, 2007-2025, 10.2217/nnm.13.176
9. Strom, G.; Ohgren, C.; Ankerfors, M. Nanocellulose as an Additive in Foodstuff; Innventia: Stockholm, Sweden, 2013.
10. Shahabi-Ghahfarrokhi, I.; Khodaiyan, F.; Mousavi, M.; Yousefi, H. Green Bionanocomposite Based on Kefiran and Cellulose Nanocrystals Produced from Beer Industrial Residues. Int. J. Biol. Macromol. 2015, 77, 85-91, 10.1016/j.ijbiomac.2015.02.055
11. Peters, R. J. B.; van Bemmel, G.; Herrera-Rivera, Z.; Helsper, H. P. F. G.; Marvin, H. J. P.; Weigel, S.; Tromp, P. C.; Oomen, A. G.; Rietveld, A. G.; Bouwmeester, H. Characterization of Titanium Dioxide Nanoparticles in Food Products: Analytical Methods To Define Nanoparticles. J. Agric. Food Chem. 2014, 62, 6285-6293, 10.1021/jf5011885
12. Lim, J.-H.; Sisco, P.; Mudalige, T. K.; Sánchez-Pomales, G.; Howard, P. C.; Linder, S. W. Detection and Characterization of SiO2 and TiO2 Nanostructures in Dietary Supplements. J. Agric. Food Chem. 2015, 63, 3144-3152, 10.1021/acs.jafc.5b00392
13. Chen, H.; Seiber, J. N.; Hotze, M. ACS Select on Nanotechnology in Food and Agriculture: A Perspective on Implications and Applications. J. Agric. Food Chem. 2014, 62, 1209-1212, 10.1021/jf5002588
14. Athinarayanan, J.; Periasamy, V. S.; Alsaif, M. A.; Al-Warthan, A. A.; Alshatwi, A. A. 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. 2014, 30, 89-100, 10.1007/s10565-014-9271-8
15. Athinarayanan, J.; Alshatwi, A. A.; Periasamy, V. S.; Al-Warthan, A. A. Identification of Nanoscale Ingredients in Commercial Food Products and Their Induction of Mitochondrially Mediated Cytotoxic Effects on Human Mesenchymal Stem Cells. J. Food Sci. 2015, 80, N459-64, 10.1111/1750-3841.12760
16. Pyrgiotakis, G.; Vasanthakumar, A.; Gao, Y.; Eleftheriadou, M.; Toledo, E.; DeAraujo, A.; McDevitt, J.; Han, T.; Mainelis, G.; Mitchell, R.; Demokritou, P. Inactivation of Foodborne Microorganisms Using Engineered Water Nanostructures (EWNS). Environ. Sci. Technol. 2015, 49, 3737-3745, 10.1021/es505868a
17. Pyrgiotakis, G.; Vedantam, P.; Cirenza, C.; McDevitt, J.; Eleftheriadou, M.; Leonard, S. S.; Demokritou, P. Optimization of a Nanotechnology Based Antimicrobial Platform for Food Safety Applications Using Engineered Water Nanostructures (EWNS). Sci. Rep. 2016, 6, 21073, 10.1038/srep21073
18. Khan, R. A.; Salmieri, S.; Dussault, D.; Uribe-Calderon, J.; Kamal, M. R.; Safrany, A.; Lacroix, M. Production and Properties of Nanocellulose-Reinforced Methylcellulose-Based Biodegradable Films. J. Agric. Food Chem. 2010, 58, 7878-7885, 10.1021/jf1006853
19. Mariano, M.; El Kissi, N.; Dufresne, A. Cellulose Nanocrystals and Related Nanocomposites: Review of Some Properties and Challenges. J. Polym. Sci., Part B: Polym. Phys. 2014, 52, 791-806, 10.1002/polb.23490
20. Nair, S. S.; Zhu, J.; Deng, Y.; Ragauskas, A. J. High Performance Green Barriers Based on Nanocellulose. Sustainable Chem. Processes 2014, 2, 23, 10.1186/s40508-014-0023-0
21. Ong, K. J.; Shatkin, J. A.; Nelson, K.; Ede, J. D.; Retsina, T. Establishing the Safety of Novel Bio-Based Cellulose Nanomaterials for Commercialization. NanoImpact 2017, 6, 19-29, 10.1016/j.impact.2017.03.002
22. Costanzo, L. S. Physiology, 5 th ed.; Saunders Elsevier: Philadelphia, PA, 2014.
23. Nelson, D. L.; Cox, M. M. Lehninger Principles of Biochemistry, 7 th ed.; W. H. Freeman, 2017.
24. Pyrgiotakis, G.; Luu, W.; Zhang, Z.; Vaze, N.; DeLoid, G.; Rubio, L.; Bell, D.; Bousfield, D.; Demokritou, P.; Graham, W. A. C. Development of High Throughput, High Precision Synthesis Platforms and Characterization Methodologies for Toxicological Studies of Nanocellulose. Cellulose 2018, 25, 2303-2319, 10.1007/s10570-018-1718-2
25. Maldonado-Valderrama, J.; Wilde, P.; Macierzanka, A.; Mackie, A. The Role of Bile Salts in Digestion. Adv. Colloid Interface Sci. 2011, 165, 36-46, 10.1016/j.cis.2010.12.002
26. Corstens, M. N.; Berton-Carabin, C. C.; Kester, A.; Fokkink, R.; van den Broek, J. M.; de Vries, R.; Troost, F. J.; Masclee, A. A. M.; Schroën, K. Destabilization of Multilayered Interfaces in Digestive Conditions Limits Their Ability to Prevent Lipolysis in Emulsions. Food Struct. 2017, 12, 54-63, 10.1016/j.foostr.2016.07.004
27. Golding, M.; Wooster, T. J. The Influence of Emulsion Structure and Stability on Lipid Digestion. Curr. Opin. Colloid Interface Sci. 2010, 15, 90-101, 10.1016/j.cocis.2009.11.006
28. Sandra, S.; Decker, E. A.; McClements, D. J. Effect of Interfacial Protein Cross-Linking on the in Vitro Digestibility of Emulsified Corn Oil by Pancreatic Lipase. J. Agric. Food Chem. 2008, 56, 7488-7494, 10.1021/jf800741w
29. Sarkar, A.; Horne, D. S.; Singh, H. Pancreatin-Induced Coalescence of Oil-in-Water Emulsions in an in Vitro Duodenal Model. Int. Dairy J. 2010, 20, 589-597, 10.1016/j.idairyj.2009.12.007
30. Sarkar, A.; Murray, B.; Holmes, M.; Ettelaie, R.; Abdalla, A.; Yang, X. In Vitro Digestion of Pickering Emulsions Stabilized by Soft Whey Protein Microgel Particles: Influence of Thermal Treatment. Soft Matter 2016, 12, 3558-3569, 10.1039/C5SM02998H
31. Sarkar, A.; Li, H.; Cray, D.; Boxall, S. Composite Whey Protein-cellulose Nanocrystals at Oil-Water Interface: Towards Delaying Lipid Digestion. Food Hydrocolloids 2018, 77, 436-444, 10.1016/j.foodhyd.2017.10.020
32. DeLoid, G. M.; Wang, Y.; Kapronezai, K.; Lorente, L. R.; Zhang, R.; Pyrgiotakis, G.; Konduru, N. V.; Ericsson, M.; White, J. C.; De La Torre-Roche, R.; Xiao, H.; McClements, D. J.; Demokritou, P. An Integrated Methodology for Assessing the Impact of Food Matrix and Gastrointestinal Effects on the Biokinetics and Cellular Toxicity of Ingested Engineered Nanomaterials. Part. Fibre Toxicol. 2017, 14, 40, 10.1186/s12989-017-0221-5
33. Akoh, C. C.; Min, D. B. Food Lipids: Chemistry, Nutrition and Biotechnology, 3 rd ed.; CRC Press: Boca Raton, FL, 2008.
34. Williams, H. D.; Trevaskis, N. L.; Charman, S. A.; Shanker, R. M.; Charman, W. N.; Pouton, C. W.; Porter, C. J. H. Strategies to Address Low Drug Solubility in Discovery and Development. Pharmacol. Rev. 2013, 65, 315-499, 10.1124/pr.112.005660
35. Devraj, R.; Williams, H. D.; Warren, D. B.; Mullertz, A.; Porter, C. J. H.; Pouton, C. W. In Vitro Digestion Testing of Lipid-Based Delivery Systems: Calcium Ions Combine with Fatty Acids Liberated from Triglyceride Rich Lipid Solutions to Form Soaps and Reduce the Solubilization Capacity of Colloidal Digestion Products. Int. J. Pharm. 2013, 441, 323-333, 10.1016/j.ijpharm.2012.11.024
36. Ghasemifard, S.; Hermon, K.; Turchini, G. M.; Sinclair, A. J. Metabolic Fate (Absorption, β-Oxidation and Deposition) of Long-Chain n-3 Fatty Acids Is Affected by Sex and by the Oil Source (Krill Oil or Fish Oil) in the Rat. Br. J. Nutr. 2015, 114, 684-692, 10.1017/S0007114515002457
37. Sarkar, A.; Zhang, S.; Murray, B.; Russell, J. A.; Boxal, S. Modulating in Vitro Gastric Digestion of Emulsions Using Composite Whey Protein-Cellulose Nanocrystal Interfaces. Colloids Surf., B 2017, 158, 137-146, 10.1016/j.colsurfb.2017.06.037
38. McClements, D. J.; DeLoid, G.; Pyrgiotakis, G.; Shatkin, J. A.; Xiao, H.; Demokritou, P. The Role of the Food Matrix and Gastrointestinal Tract in the Assessment of Biological Properties of Ingested Engineered Nanomaterials (IENMs): State of the Science and Knowledge Gaps. NanoImpact 2016, 3-4, 47, 10.1016/j.impact.2016.10.002
39. Koeneman, B. A.; Zhang, Y.; Westerhoff, P.; Chen, Y.; Crittenden, J. C.; Capco, D. G. Toxicity and Cellular Responses of Intestinal Cells Exposed to Titanium Dioxide. Cell Biol. Toxicol. 2010, 26, 225-238, 10.1007/s10565-009-9132-z
40. Guo, Z.; Martucci, N. J.; Moreno-Olivas, F.; Tako, E.; Mahler, G. J. Titanium Dioxide Nanoparticle Ingestion Alters Nutrient Absorption in an in Vitro Model of the Small Intestine. NanoImpact 2017, 5, 70-82, 10.1016/j.impact.2017.01.002
41. Setyawati, M. I.; Sevencan, C.; Bay, B.-H.; Xie, J.; Zhang, Y.; Demokritou, P.; Leong, D. T. Nano-TiO2 Drives Epithelial -Mesenchymal Transition in Intestinal Epithelial Cancer Cells. Small 2018, 10.1002/smll.201800922
42. Bhattacharya, K.; Kiliç, G.; Costa, P. M.; Fadeel, B. Cytotoxicity Screening and Cytokine Profiling of Nineteen Nanomaterials Enables Hazard Ranking and Grouping Based on Inflammogenic Potential. Nanotoxicology 2017, 11, 809-826, 10.1080/17435390.2017.1363309
43. Menas, A. L.; Yanamala, N.; Farcas, M. T.; Russo, M.; Friend, S.; Fournier, P. M.; Star, A.; Iavicoli, I.; Shurin, G. V.; Vogel, U. B.; Fadeel, B.; Beezhold, D.; Kisin, E. R.; Shvedova, A. A. Fibrillar vs Crystalline Nanocellulose Pulmonary Epithelial Cell Responses: Cytotoxicity or Inflammation?. Chemosphere 2017, 171, 671-680, 10.1016/j.chemosphere.2016.12.105
44. Endes, C.; Camarero-Espinosa, S.; Mueller, S.; Foster, E. J.; Petri-Fink, A.; Rothen-Rutishauser, B.; Weder, C.; Clift, M. J. D. A Critical Review of the Current Knowledge Regarding the Biological Impact of Nanocellulose. J. Nanobiotechnol. 2016, 14, 78, 10.1186/s12951-016-0230-9
45. NCD Risk Factor Collaboration (NCD-RisC) Trends in Adult Body-Mass Index in 200 Countries from 1975 to 2014: A Pooled Analysis of 1698 Population-Based Measurement Studies with 19.2 Million Participants. Lancet 2016, 387, 1377-1396, 10.1016/S0140-6736(16)30054-X
46. Bray, G. A.; Kim, K. K.; Wilding, J. P. H. World Obesity Federation. Obesity: A Chronic Relapsing Progressive Disease Process. A Position Statement of the World Obesity Federation. Obes. Rev. 2017, 18, 715-723, 10.1111/obr.12551
47. Withrow, D.; Alter, D. A. The Economic Burden of Obesity Worldwide: A Systematic Review of the Direct Costs of Obesity. Obes. Rev. 2011, 12, 131-141, 10.1111/j.1467-789X.2009.00712.x
48. Wang, Y. C.; McPherson, K.; Marsh, T.; Gortmaker, S. L.; Brown, M. Health and Economic Burden of the Projected Obesity Trends in the USA and the UK.. Lancet 2011, 378, 815-825, 10.1016/S0140-6736(11)60814-3
49. Sumithran, P.; Prendergast, L. A.; Delbridge, E.; Purcell, K.; Shulkes, A.; Kriketos, A.; Proietto, J. Long-Term Persistence of Hormonal Adaptations to Weight Loss. N. Engl. J. Med. 2011, 365, 1597-1604, 10.1056/NEJMoa1105816
50. Polidori, D.; Sanghvi, A.; Seeley, R. J.; Hall, K. D. How Strongly Does Appetite Counter Weight Loss? Quantification of the Feedback Control of Human Energy Intake. Obesity 2016, 24, 2289-2295, 10.1002/oby.21653
51. Bessesen, D. H.; Van Gaal, L. F. Progress and Challenges in Anti-Obesity Pharmacotherapy. Lancet Diabetes Endocrinol. 2018, 6, 237, 10.1016/S2213-8587(17)30236-X
52. Maljaars, P. W. J.; Peters, H. P. F.; Mela, D. J.; Masclee, A. A. M. Ileal Brake: A Sensible Food Target for Appetite Control. A Review. Physiol. Behav. 2008, 95, 271-281, 10.1016/j.physbeh.2008.07.018
53. Yin, S.; Biedermannova, L.; Vondrasek, J.; Dokholyan, N. V. MedusaScore: An Accurate Force Field-Based Scoring Function for Virtual Drug Screening. J. Chem. Inf. Model. 2008, 48, 1656-1662, 10.1021/ci8001167
54. Andersen, H. C. Molecular Dynamics Simulations at Constant Pressure and/or Temperature. J. Chem. Phys. 1980, 72, 2384-2393, 10.1063/1.439486
55. Hermoso, J.; Pignol, D.; Kerfelec, B.; Crenon, I.; Chapus, C.; Fontecilla-Camps, J. C. Lipase Activation by Nonionic Detergents. The Crystal Structure of the Porcine Lipase-Colipase-Tetraethylene Glycol Monooctyl Ether Complex. J. Biol. Chem. 1996, 271, 18007-18016, 10.1074/jbc.271.30.18007
56. Hanwell, M. D.; Curtis, D. E.; Lonie, D. C.; Vandermeersch, T.; Zurek, E.; Hutchison, G. R. Avogadro: An Advanced Semantic Chemical Editor, Visualization, and Analysis Platform. J. Cheminf. 2012, 4, 17, 10.1186/1758-2946-4-17
57. Saitoh, L.; Ohno, H.; Matsuo, S. Structure and Mechanical Behavior of Cellulose Nanofiber and Micro-Fibrils by Molecular Dynamics Simulation. Soft Nanosci. Lett. 2013, 3, 58-67, 10.4236/snl.2013.33011