Evaluation of fasted and fed state simulated and human intestinal fluids as solvent system in the Ussing chambers model to explore food effects on intestinal permeability

International Journal of Pharmaceutics

Volumn 478, Issue 2, 2015, Pages 736-744

  Wuyts, Benjamin ^a   Riethorst, Danny ^a   Brouwers, Joachim ^a   Tack, Jan ^b   Annaert, Pieter ^a   Augustijns, Patrick ^a  

^a DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Food effect; Human intestinal fluid; Permeability; Rat intestine; Ussing chambers

Indexed keywords

ATENOLOL; CAFFEINE; CARVEDILOL; CROMOGLYCATE DISODIUM; DARUNAVIR; DOXORUBICIN; FUROSEMIDE; INDOMETACIN; METOPROLOL; NAPROXEN; PIROXICAM; PROPRANOLOL; QUINIDINE; RANITIDINE; SALAZOSULFAPYRIDINE; THEOPHYLLINE; BILE ACID; DRUG; PHOSPHOLIPID; SOLVENT;

ANIMAL EXPERIMENT; AREA UNDER THE CURVE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG EXPOSURE; DRUG PENETRATION; DRUG SOLUBILITY; FOOD; HUMAN; INTESTINE ABSORPTION; INTESTINE EPITHELIUM; INTESTINE FLUID; INTESTINE MUCOSA PERMEABILITY; LIPOPHILICITY; MALE; MICELLE; NONHUMAN; NUTRITIONAL STATUS; OSMOLALITY; RAT; SODIUM TRANSPORT; TRANSCYTOSIS; ANIMAL; FOOD DRUG INTERACTION; ILEUM; IN VITRO STUDY; INTESTINAL SECRETIONS; METABOLISM; PERMEABILITY; PHYSIOLOGY; POSTPRANDIAL STATE; WISTAR RAT;

ANIMALS; BILE ACIDS AND SALTS; FASTING; FOOD-DRUG INTERACTIONS; HUMANS; ILEUM; IN VITRO TECHNIQUES; INTESTINAL ABSORPTION; INTESTINAL SECRETIONS; MALE; PERMEABILITY; PHARMACEUTICAL PREPARATIONS; PHOSPHOLIPIDS; POSTPRANDIAL PERIOD; RATS, WISTAR; SOLVENTS;

EID: 84919935669     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2014.12.021     Document Type: Article

References (85)

1. A.M. Al-Mohizea Influence of intestinal efflux pumps on the absorption and transport of furosemide Saudi Pharm. J. SPJ Off. Publ. Saudi Pharm. Soc. 18 2010 97 101
2. N. Aoyagi, N. Kaniwa, and H. Ogota Effects of food on bioavailability of two indomethacin capsules containing different sizes of particles Chem. Pharm. Bull. (Tokyo) 38 1990 1338 1340
3. B.J. Aungst, N.H. Nguyen, J.P. Bulgarelli, and K. Oates-Lenz The influence of donor and reservoir additives on Caco-2 permeability and secretory transport of HIV protease inhibitors and other lipophilic compounds Pharm. Res. 17 2000 1175 1180
4. J. Blanchard, and S.J.A. Sawers Comparative pharmacokinetics of caffeine in young and elderly men J. Pharmacokinet. Biopharm. 11 1983 109 126
5. J. Brouwers, J. Tack, F. Lammert, and P. Augustijns Intraluminal drug and formulation behavior and integration in in vitro permeability estimation: a case study with amprenavir J. Pharm. Sci. 95 2006 372 383
6. D.U. Busto, R. Bendayan, and E.M. Sellers Clinical pharmacokinetics of non-opiate abused drugs Clin. Pharmacokinet 16 1989 1 26
7. G. Cheymol, J.M. Poirier, P.A. Carrupt, B. Testa, J. Weissenburger, J.C. Levron, and E. Snoeck Pharmacokinetics of beta-adrenoceptor blockers in obese and normal volunteers Br. J. Clin. Pharmacol. 43 1997 563 570
8. S. Clarysse, J. Brouwers, J. Tack, P. Annaert, and P. Augustijns Intestinal drug solubility estimation based on simulated intestinal fluids: comparison with solubility in human intestinal fluids Eur J. Pharm. Sci. Off. J. Eur. Fed. Pharm. Sci. 43 2011 260 269
9. S. Clarysse, D. Psachoulias, J. Brouwers, J. Tack, P. Annaert, G. Duchateau, C. Reppas, and P. Augustijns Postprandial changes in solubilizing capacity of human intestinal fluids for BCS class II drugs Pharm. Res. 26 2009 1456 1466
10. A. Collett, N.B. Higgs, E. Sims, M. Rowland, and G. Warhurst Modulation of the permeability of H2 receptor antagonists cimetidine and ranitidine by P-glycoprotein in rat intestine and the human colonic cell line Caco-2 J. Pharmacol. Exp. Ther. 288 1999 171 178
11. Dahlgren, D.; Roos, C.; Sjögren, E.; Lennernäs, H.; 2014. Direct In Vivo Human Intestinal Permeability (Peff) Determined with Different Clinical Perfusion and Intubation Methods. J. Pharm. Sci. (in press).
12. B.M. Davit, D.P. Conner, B. Fabian-Fritsch, S.H. Haidar, X. Jiang, D.T. Patel, P.R.H. Seo, K. Suh, C.L. Thompson, and L.X. Yu Highly variable drugs: observations from bioequivalence data submitted to the FDA for new generic drug applications AAPS J. 10 2008 148 156
13. Deferme, S.; Annaert, P.; Augustijns, P.; 2008. In Vitro Screening Models to Assess Intestinal Drug Absorption and Metabolism, in: Ehrhardt, C.; Kim, K.-J. (Eds.), Drug Absorption Studies, Biotechnology: Pharmaceutical Aspects. Springer US, pp. 182-215.
14. S. Deferme, R. Mols, W. Van Driessche, and P. Augustijns Apricot extract inhibits the P-gp-mediated efflux of talinolol J. Pharm. Sci. 91 2002 2539 2548
15. D.D. Deshmukh, W.R. Ravis, and G.V. Betageri Improved delivery of cromolyn from oral proliposomal beads Int. J. Pharm. 358 2008 128 136
16. P.V. Desmond, P.J. Harman, N. Gannoulis, M. Kamm, and M.L. Mashford The effect of an antacid and food on the absorption of cimetidine and ranitidine J. Pharm. Pharmacol. 42 1990 352 354
17. D. Fleisher, C. Li, Y. Zhou, L.H. Pao, and A. Karim Drug: meal and formulation interactions influencing drug absorption after oral administration clinical implications Clin. Pharmacokinet. 36 1999 233 254
18. E. Galia, E. Nicolaides, D. Hörter, R. Löbenberg, C. Reppas, and J.B. Dressman Evaluation of various dissolution media for predicting in vivo performance of Class I and II drugs Pharm. Res. 15 1998 698 705
19. T.W. Guentert, R.A. Upton, N.H. Holford, A. Bostrom, and S. Riegelman Gastrointestinal absorption of quinidine from some solutions and commercial tablets J. Pharmacokinet. Biopharm. 8 1980 243 255
20. D. Gurantz, M.F. Laker, and A.F. Hofmann Enzymatic measurement of choline-containing phospholipids in bile J. Lipid Res. 22 1981 373 376
21. M.M. Hammarlund, L.K. Paalzow, and B. Odlind Pharmacokinetics of furosemide in man after intravenous and oral administration. Application of moment analysis Eur. J. Clin. Pharmacol. 26 1984 197 207
22. I.S. Haslam, D.A. O'Reilly, D.J. Sherlock, A. Kauser, C. Womack, and T. Coleman Pancreatoduodenectomy as a source of human small intestine for Ussing chamber investigations and comparative studies with rat tissue Biopharm. Drug Dispos. 32 2011 210 221
23. C. Hilgendorf, H. Spahn-Langguth, C.G. Regårdh, E. Lipka, G.L. Amidon, and P. Langguth Caco-2 versus caco-2/HT29-MTX co-cultured cell lines: permeabilities via diffusion, inside- and outside-directed carrier-mediated transport J. Pharm. Sci. 89 2000 63 75
24. N. Holmstock, T.D. Bruyn, J. Bevernage, P. Annaert, R. Mols, J. Tack, and P. Augustijns Exploring food effects on indinavir absorption with human intestinal fluids in the mouse intestine Eur. J. Pharm. Sci. Off. J. Eur. Fed. Pharm. Sci. 49 2013 27 32
25. A. Hsu, G.R. Granneman, G. Cao, L. Carothers, A. Japour, T. El-Shourbagy, S. Dennis, J. Berg, K. Erdman, J.M. Leonard, and E. Sun Pharmacokinetic interaction between ritonavir and indinavir in healthy volunteers Antimicrob. Agents Chemother. 42 1998 2784 2791
26. S. Hu, M. Niu, F. Hu, Y. Lu, J. Qi, Z. Yin, and W. Wu Integrity and stability of oral liposomes containing bile salts studied in simulated and ex vivo gastrointestinal media Int. J. Pharm. 441 2013 693 700
27. F. Ingels, S. Deferme, E. Destexhe, M. Oth, G. Van den Mooter, and P. Augustijns Simulated intestinal fluid as transport medium in the Caco-2 cell culture model Int. J. Pharm 232 2002 183 192
28. F.M. Ingels, and P.F. Augustijns Biological, pharmaceutical, and analytical considerations with respect to the transport media used in the absorption screening system, Caco-2 J. Pharm. Sci. 92 2003 1545 1558
29. K. Ishida, M. Takaai, and Y. Hashimoto Pharmacokinetic analysis of transcellular transport of quinidine across monolayers of human intestinal epithelial Caco-2 cells Biol. Pharm. Bull. 29 2006 522 526
30. E. Jantratid, N. Janssen, H. Chokshi, K. Tang, and J.B. Dressman Designing biorelevant dissolution tests for lipid formulations: case example-lipid suspension of RZ-50 Eur. J. Pharm. Biopharm. 69 2008 776 785
31. K. Jauhiainen, S. Eksborg, L. Kangas, M. Perilä, and O. Alfthan The absorption of doxorubicin and mitomycin C in perioperative instillation An experimental and clinical study Eur. Urol. 11 1985 269 272
32. H.M. Jones, D.N. Parrott, G. Ohlenbusch, and T. Lavé Predicting pharmacokinetic food effects using biorelevant solubility media and physiologically based modelling Clin. Pharmacokinet. 45 2006 1213 1226
33. A. Karim Effects of food on the bioavailability of theophylline from controlled-release products in adults J. Allergy Clin. Immunol. 78 1986 695 703 Update on Theophylline
34. C.J. Kenyon, G. Hooper, D. Tierney, J. Butler, J. Devane, and I.R. Wilding The effect of food on the gastrointestinal transit and systemic absorption of naproxen from a novel sustained release formulation J. Control. Release 34 1995 31 36
35. J.-E. Kim, H.-J. Cho, J.S. Kim, C.-K. Shim, S.-J. Chung, M.-H. Oak, I.-S. Yoon, and D.-D. Kim The limited intestinal absorption via paracellular pathway is responsible for the low oral bioavailability of doxorubicin Xenobiotica 43 2013 579 591
36. R. Kirsten, K. Nelson, D. Kirsten, and B. Heintz Clinical pharmacokinetics of vasodilators. Part II Clin. Pharmacokinet. 35 1998 9 36
37. J. Kraan, L. Borgström, G.H. Koëter, M. Laseur, J.H. Jonkman, and O.E. de Noord Creation of four consecutive instantaneous steady-state plasma concentration plateaus of theophylline and enprofylline by repeated infusions with exponentially decreasing delivery rates Eur. J. Clin. Pharmacol. 35 1988 657 661
38. H. Lage, and M. Dietel Effect of the breast-cancer resistance protein on atypical multidrug resistance Lancet Oncol. 1 2000 169 175
39. A. Lampen, A. Bader, T. Bestmann, M. Winkler, L. Witte, and J.T. Borlak Catalytic activities, protein- and mRNA-expression of cytochrome P450 isoenzymes in intestinal cell lines Xenobiotica 28 1998 429 441
40. K. Lee, and D.R. Thakker Saturable transport of H2-antagonists ranitidine and famotidine across Caco-2 cell monolayers J. Pharm. Sci. 88 1999 680 687
41. K.-J. Lee, R. Mower, T. Hollenbeck, J. Castelo, N. Johnson, P. Gordon, P.J. Sinko, K. Holme, and Y.-H. Lee Modulation of nonspecific binding in ultrafiltration protein binding studies Pharm. Res. 20 2003 1015 1021
42. I. Legen, M. Salobir, and J. Kerč Comparison of different intestinal epithelia as models for absorption enhancement studies. Int. J. Pharm Proceedings of the 5th Central European Symposium on Pharmaceutical Technology and Biotechnology Proceedings of the 5th Central European Symposium on Pharmaceutical Technology and Biotechnology 291 2005 183 188
43. H. Lennernäs Human jejunal effective permeability and its correlation with preclinical drug absorption models J. Pharm. Pharmacol. 49 1997 627 638
44. H. Lennernäs Intestinal permeability and its relevance for absorption and elimination Xenobiotica 37 2007 1015 1051
45. E. Liang, J. Proudfoot, and M. Yazdanian Mechanisms of transport and structure-permeability relationship of sulfasalazine and its analogs in Caco-2 cell monolayers Pharm. Res. 17 2000 1168 1174
46. H. Liedholm, E. Whlin-Boll, and A. Melander Mechanisms and variations in the food effect on propranolol bioavailability Eur. J. Clin. Pharmacol. 38 1990 469 475
47. A. Lindahl, A.L. Ungell, L. Knutson, and H. Lennernäs Characterization of fluids from the stomach and proximal jejunum in men and women Pharm. Res. 14 1997 497 502
48. T.P. Lombardi, J.S. Bertino, A. Goldberg, E. Middleton, and R.L. Slaughter The effects of a beta-2 selective adrenergic agonist and a beta-nonselective antagonist on theophylline clearance J. Clin. Pharmacol. 27 1987 523 529
49. A.M. Marino, M. Yarde, H. Patel, S. Chong, and P.V. Balimane Validation of the 96 well Caco-2 cell culture model for high throughput permeability assessment of discovery compounds Int. J. Pharm. 297 2005 235 241
50. C. Markopoulos, F. Thoenen, D. Preisig, M. Symillides, M. Vertzoni, N. Parrott, C. Reppas, and G. Imanidis Biorelevant media for transport experiments in the Caco-2 model to evaluate drug absorption in the fasted and the fed state and their usefulness Eur. J. Pharm. Biopharm. 86 2014 438 448 Off. J. Arbeitsgemeinschaft Für Pharm. Verfahrenstechnik EV
51. W.D. Mason, N. Winer, G. Kochak, I. Cohen, and R. Bell Kinetics and absolute bioavailability of atenolol Clin. Pharmacol. Ther. 25 1979 408 415
52. A. Melander, K. Danielson, B. Scherstén, and E. Wåhlin Enhancement of the bioavailability of propranolol and metoprolol by food Clin. Pharmacol. Ther. 22 1977 108 112
53. A. Melander, P. Stenberg, H. Liedholm, B. Scherstén, and E. Wåhlin-Boll Food-induced reduction in bioavailability of atenolol Eur. J. Clin. Pharmacol. 16 1979 327 330
54. D.T. Morgan Clinical pharmacokinetics and pharmacodynamics of carvedilol Clin. Pharmacokinet. 26 1994 335 346
55. H.J. Motulsky, and R.E. Brown Detecting outliers when fitting data with nonlinear regression - a new method based on robust nonlinear regression and the false discovery rate BMC Bioinformatics 7 2006 123
56. K.V.R. Murthy, and V. Raju Development and validation of new discriminative dissolution method for carvedilol tablets Indian J. Pharm Sci. 73 2011 527
57. P. Nejdfors, M. Ekelund, B. Jeppsson, and B.R. Weström Mucosal in vitro permeability in the intestinal tract of the pig the rat, and man: species- and region-related differences Scand. J. Gastroenterol. 35 2000 501 507
58. S. Neuhoff, A.-L. Ungell, I. Zamora, and P. Artursson pH-Dependent passive and active transport of acidic drugs across Caco-2 cell monolayers Eur. J. Pharm. Sci 25 2005 211 220
59. V. Pade, and S. Stavchansky Estimation of the relative contribution of the transcellular and paracellular pathway to the transport of passively absorbed drugs in the Caco-2 cell culture model Pharm. Res. 14 1997 1210 1215
60. K. Palm, P. Stenberg, K. Luthman, and P. Artursson Polar molecular surface properties predict the intestinal absorption of drugs in humans Pharm. Res. 14 1997 568 571
61. N. Patel, B. Forbes, S. Eskola, and J. Murray Use of simulated intestinal fluids with Caco-2 cells and rat ileum Drug Dev. Ind. Pharm. 32 2006 151 161
62. B.L. Pedersen, H. Brøndsted, H. Lennernäs, F.N. Christensen, A. Müllertz, and H.G. Kristensen Dissolution of hydrocortisone in human and simulated intestinal fluids Pharm. Res. 17 2000 183 189
63. E.M. Persson, A.-S. Gustafsson, A.S. Carlsson, R.G. Nilsson, L. Knutson, P. Forsell, G. Hanisch, H. Lennernäs, and B. Abrahamsson The effects of food on the dissolution of poorly soluble drugs in human and in model small intestinal fluids Pharm. Res. 22 2005 2141 2151
64. D. Psachoulias, M. Vertzoni, K. Goumas, V. Kalioras, S. Beato, J. Butler, and C. Reppas Precipitation in and supersaturation of contents of the upper small intestine after administration of two weak bases to fasted adults Pharm. Res. 28 2011 3145 3158
65. C.G. Regårdh, K.O. Borg, R. Johansson, G. Johnsson, and L. Palmer Pharmacokinetic studies on the selective beta1-receptor antagonist metoprolol in man J. Pharmacokinet. Biopharm. 2 1974 347 364
66. B.D. Rege, L.X. Yu, A.S. Hussain, and J.E. Polli Effect of common excipients on Caco-2 transport of low-permeability drugs J. Pharm. Sci. 90 2001 1776 1786
67. Y. Sambuy, I. De Angelis, G. Ranaldi, M.L. Scarino, A. Stammati, and F. Zucco The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics Cell Biol. Toxicol. 21 2005 1 26
68. V. Sekar, D. Kestens, S. Spinosa-Guzman, M. De Pauw, E. De Paepe, T. Vangeneugden, E. Lefebvre, and R.M.W. Hoetelmans The effect of different meal types on the pharmacokinetics of darunavir (TMC114)/ritonavir in HIV-negative healthy volunteers J. Clin. Pharmacol. 47 2007 479 484
69. Å. Sjöberg, M. Lutz, C. Tannergren, C. Wingolf, A. Borde, and A.-L. Ungell Comprehensive study on regional human intestinal permeability and prediction of fraction absorbed of drugs using the Ussing chamber technique Eur. J. Pharm. Sci. Off. J. Eur. Fed. Pharm. Sci. 48 2013 166 180
70. L. Smetanova, V. Stetinova, D. Kholova, J. Kvetina, J. Smetana, and Z. Svoboda Caco-2 cells and biopharmaceutics classification system (BCS) for prediction of transepithelial transport of xenobiotics (model drug: caffeine) Neuro Endocrinol. Lett. 30 Suppl. 1 2009 101 105
71. D.E. Smith, E.T. Lin, and L.Z. Benet Absorption and disposition of furosemide in healthy volunteers: measured with a metabolite-specific assay Drug Metab. Dispos. Biol. Fate Chem. 8 1980 337 342
72. R. Sowjanya, S. Duraivel, K.P. Sampath Kumar, and B. Debjit Formulation and evaluation of transdermal patches of carvedilol J. Chem. Pharm. Sci. 6 2013 250 253
73. J. Stappaerts, B. Wuyts, J. Tack, P. Annaert, and P. Augustijns Human and simulated intestinal fluids as solvent systems to explore food effects on intestinal solubility and permeability European Journal of Pharmaceutical Sciences 63C 2014 178 186 Off. J. Eur. Fed. Pharm. Sci
74. U.S. Food and Drug Administration, 2011. Drug Development and Drug Interactions: Table of Substrates, Inhibitors and Inducers [WWW Document]. URL http://www.fda.gov/drugs/developmentapprovalprocess/developmentresources/druginteractionslabeling/ucm093664 htm#PgpTransport (accessed 09.28.14).
75. A.L. Ungell, S. Nylander, S. Bergstrand, A. Sjöberg, and H. Lennernäs Membrane transport of drugs in different regions of the intestinal tract of the rat J. Pharm. Sci. 87 1998 360 366
76. H. van de Waterbeemd, D.A. Smith, and B.C. Jones Lipophilicity in PK design: methyl, ethyl, futile J. Comput. Aided Mol. Des. 15 2001 273 286
77. T. Walle, U.K. Walle, T.D. Cowart, E.C. Conradi, and T.E. Gaffney Selective induction of propranolol metabolism by smoking: additional effects on renal clearance of metabolites J. Pharmacol. Exp. Ther. 241 1987 928 933
78. E. Watanabe, M. Takahashi, and M. Hayashi A possibility to predict the absorbability of poorly water-soluble drugs in humans based on rat intestinal permeability assessed by an in vitro chamber method Eur. J. Pharm. Biopharm. 58 2004 659 665
79. P.G. Welling Effects of food on drug absorption Annu. Rev. Nutr. 16 1996 383 415
80. P. Winstanley, and M. Orme The effects of food on drug bioavailability Br. J. Clin. Pharmacol. 28 1989 621 628
81. E. Woo, and D.J. Greenblatt Effect of food on enteral absorption of quinidine Clin. Pharmacol. Ther. 27 1980 188 193
82. B. Wuyts, J. Brouwers, R. Mols, J. Tack, P. Annaert, and P. Augustijns Solubility profiling of HIV protease inhibitors in human intestinal fluids J. Pharm. Sci. 102 2013 3800 3807
83. K.C. Yeh, E.T. Berger, G.O. Breault, B.W. Lei, and F.G. McMahon Effect of sustained release on the pharmacokinetic profile of indomethacin in man Biopharm. Drug Dispos. 3 1982 219 230
84. X. Zhang, K.I. Collins, and L.M. Greenberger Functional evidence that transmembrane 12 and the loop between transmembrane 11 and 12 form part of the drug-binding domain in P-glycoprotein encoded by MDR1 J. Biol. Chem. 270 1995 5441 5448
85. C. Zhu, L. Jiang, T.-M. Chen, and K.-K. Hwang A comparative study of artificial membrane permeability assay for high throughput profiling of drug absorption potential Eur. J. Med. Chem. 37 2002 399 407