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Expert Opinion on Drug Delivery Volume 5, 2008 - Issue 1
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Review

Nanoparticle strategies for the oral delivery of insulin

Christiane Damgé Director of Research at the National Institute for Health and Medical Research (INSERM), University Louis Pasteur, Faculty of Medicine, Institute of Physiology, 11, rue Humann, 67000-Strasbourg, France +33 90 24 31 21; +33 90 24 34 44; [email protected]
,
Catarina Pinto Reis University Louis Pasteur, Faculty of Medicine, Institute of Physiology, 11, rue Humann, 67000-Strasbourg, France
, , PhD Student &
Philippe Maincent Laboratory of Pharmaceutical Technology, INSERM U734-EA 3452, Faculty of Pharmacy, 5, rue Lebrun, BP 80403, 54001-Nancy Cedex, France
Pages 45-68 | Published online: 21 Dec 2007

Bibliography

  • Banting FG, Best CH, Collip JB, Campbell WR, Fletcher AA. Pancreatic extracts in the treatment of diabetes mellitus. Preliminary report. Can Med Assoc J 1922;12:141-6
  • Daneman D. Type 1 diabetes. Lancet 2006;367(9513):847-58
  • International Diabetes Federation. Diabetes Atlas. Third Ed. Brussels; 2006
  • Owens DR, Zinman B, Bolli G. Alternative routes of insulin delivery. Diabet Med 2003;20(11):886-98
  • Brange J, Langkjoer L. Insulin formulation and delivery. In: Sanders LM, Hendren RW, editors. Protein Delivery: Physical Systems. New York Plenum Press; 1997. p. 343-411
  • Peppas NA, Kavimandan NJ. Nanoscale analysis of protein and peptide absorption: insulin absorption using complexation and pH-sensitive hydrogels as delivery vehicles. Eur J Pharm Sci 2006;29(3-4):183-97
  • Berger M. Oral insulin 1922 – 1992: the history of continuous ambition and failure. In: Berger M, Gries FA, editors. Frontiers in Insulin Pharmacology. Stuttgart: Thieme Verlag; 1993. p. 144-8
  • Liu H, Tang R, Pan WS, Zhang Y, Liu H. Potential utility of various protease inhibitors for improving the intestinal absorption of insulin in rats. J Pharm Pharmacol 2003;55(11):1523-9
  • Bendayan M, Ziv E, Gingras D, Ben-Sasson R, Bar-On H, Kidron M. Biochemical and morpho-cytochemical evidence for the intestinal absorption of insulin in control and diabetic rats. Comparison between the effectiveness of duodenal and colon mucosa. Diabetologia 1994;37(2):119-26
  • Ziv E, Bendayan M. Intestinal absorption of peptides through the enterocytes. Microsc Res Tech 2000;49(4):346-52
  • Yamamoto A, Taniguchi T, Rikyuu K, et al. Effects of various protease inhibitors on the intestinal absorption and degradation of insulin in rats. Pharm Res 1994;11(10):1496-500
  • Morishita M, Goto T, Peppas NA, et al. Mucosal insulin delivery systems based on complexation polymer hydrogels: effect of particle size on insulin enteral absorption. J Control Rel 2004;97(1):115-24
  • Shao Z, Li Y, Chermak T, Mitra AK. Cyclodextrins as mucosal absorption promoters of insulin. II. Effects of beta-cyclodextrin derivatives on alpha-chymotryptic degradation and enteral absorption of insulin in rats. Pharm Res 1994;11(8):1174-9
  • Mesiha MS, Ponnapula S, Plakogiannis F. Oral absorption of insulin encapsulated in artificial chyles of bile salts, palmitic acid and alpha-tocopherol dispersions. Int J Pharm 2002;249(1-2):1-5
  • Eaimtrakarn S, Rama Prasad YV, Ohno T, et al. Absorption enhancing effect of labrasol on the intestinal absorption of insulin in rats. J Drug Target 2002;10(3):255-60
  • Morishita M, Kamei N, Ehara J, Isowa K, Takayama K. A novel approach using functional peptides for efficient intestinal absorption of insulin. J Control Rel 2007;118(2):177-84
  • Xia CQ, Wang J, Shen WC. Hypoglycemic effect of insulin–transferrin conjugate in streptozotocin-induced diabetic rats. J Pharmacol Exp Ther 2000;295(2):594-600
  • Still JG. Development of oral insulin: progress current status. Diabetes Metab Res Rev 2002;18(suppl 1):S29-S37
  • Kipnes M, Dandona P, Tripathy D, Still JG, Kosutic G. Control of postprandial plasma glucose by an oral insulin product (HIM2) in patients with type 2 diabetes. Diabetes Care 2003;26(2):421-6
  • Wajcberg E, Miyazaki Y, Triplitt C, Cersosimo E, Defronzo RA. Dose-response effect of a single administration of oral hexyl-insulin monoconjugate 2 in healthy nondiabetic subjects. Diabetes Care 2004;27(12):2868-73
  • Clement S, Dandona P, Still JG, Kosutic G. Oral modified insulin (HIM2) in patients with type 1 diabetes mellitus: results from a Phase I/II clinical trial. Metabolism 2004;53(1):54-8
  • Cui F, Shi K, Zhang L, Tao A, Kawashima Y. Biodegradable nanoparticles loaded with insulin-phospholipid complex for oral delivery: preparation, in vitro characterization and in vivo evaluation. J Control Rel 2006;114(2):242-50
  • Dapergolas G, Gregoriadis G. Hypoglycaemic effect of liposome-entrapped insulin administered intragastrically into rats. Lancet 1976;ii:824-7
  • Saffran M, Pansky B, Colin Budd G, Williams FE. Insulin and the gastrointestinal tract. J Control Rel 1997;46(1-2):89-98
  • Fernández-Urrusuno R, Calvo P, Remuñán-López C, Vila-Jato JL, Alonso MJ. Enhancement of nasal absorption of insulin using chitosan nanoparticles. Pharm Res 1999;16(10):1576-81
  • Jung T, Kamm W, Breitenbach A, Kaiserling E, Xiao JX, Kissel T. Biodegradable nanoparticles for oral delivery of peptides: is there a role for polymers to affect mucosal uptake? Eur J Pharm Biopharm 2000;50(1):147-60
  • Vila A, Sánchez A, Tobío M, Calvo P, Alonso MJ. Design of biodegradable particles for protein delivery. J Control Rel 2002;78(1-3):15-24
  • Delie F, Blanco-Prieto MJ. Polymeric nanoparticulates to improve oral bioavailability of peptide drugs. Molecules 2005;10:65-80
  • Des Rieux A, Fievez V, Garinot M, Schneider YJ, Preat V. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J Control Rel 2006;116(1):1-27
  • Illum L. Nanoparticulate systems for nasal delivery of drugs: a real improvement over simple systems? J Pharm Sci 2007;96(3):473-83
  • Pinto Reis C, Neufeld RJ, Ribeiro AJ, Veiga F. Nanoencapsulation. II. Biomedical applications and current status of peptide and protein nanoparticulate delivery systems. Nanomed Nanotechnol Biol Med 2006;2(2):53-65
  • Carino GP, Mathiowitz E. Oral insulin delivery. Adv Drug Deliv Rev 1999;35(2-3):249-57
  • Sadrzadeh N, Glembourtt MJ, Stevenson CL. Peptide drug delivery strategies for the treatment of diabetes. J Pharm Sci 2007;96(8):1925-54
  • Hakweh M, Ponchel G, Fattal E. Particle uptake by Peyer's patches: a pathway for drug and vaccine delivery. Expert Opin Drug Deliv 2004;1(1):141-63
  • O'Hagan DT. The intestinal uptake of particles and the implications for drug and antigen delivery. J Anat 1996;189(Pt 3):477-82
  • Smith JM, Dornish M, Wood EJ. Involement of protein kinase C in chitosan glutamate-mediated tight junction disruption. Biomaterials 2005;26:3269-76
  • Bai JP, Chang LL. Transepithelial transport of insulin. I. Insulin degradation by insulin-degrading enzyme in small intestinal epithelium. Pharm Res 1995;12(8):1171-5
  • Hinds KD, Kim SW. Effects of PEG conjugation on insulin properties. Adv Drug Del Rev 2002;54:505-30
  • Couvreur P, Barratt G, Fattal E, Legrand P, Vauthier C. Nanocapsule technology: a review. Crit Rev Ther Drug Carrier Syst 2002;19(2):99-134
  • Aboubakar M, Puisieux F, Couvreur P, Deyme M, Vauthier C. Study of the mechanism of insulin encapsulation in poly(isobutylcyanoacrylate) nanocapsules obtained by interfacial polymerization. J Biomed Mater Res 1999;47(4):568-76
  • Damgé C, Michel C, Aprahamian M, Couvreur P. New approach for oral administration of insulin with polyalkylcyanoacrylate nanocapsules as drug carrier. Diabetes 1988;37(2):246-51
  • Soppimath KS, Aminabhavi TM, Kulkarni AR, Rudzinski WE. Biodegradable polymeric nanoparticles as drug delivery devices. J Control Rel 2001;70(1-2):1-20
  • Pinto Reis C, Neufeld RJ, Ribeiro AJ, Veiga F. Nanoencapsulation. I. Methods for preparation of drug-loaded polymeric nanoparticles. Nanomed Nanotechnol, Biol Med 2006;2(1):8-21
  • Brange J, Langkjaer L. Chemical stability of insulin. 3. Influence of excipients, formulation, and pH. Acta Pharm Nord 1992;4(3):149-58
  • Damgé C, Michel C, Aprahamian M, Couvreur P, Devissaguet J. Nanocapsules as carriers for oral peptide delivery. J Control Rel 1990;13(2-3):233-9
  • Damgé C, Hillaire-Buys D, Puech R, Hoeltzel A, Michel C, Ribes G. Effects of orally administered insulin nanocapsules in normal and diabetic dogs. Diab Nutr Metab 1995;8:3-9
  • Damgé C, Vranckx H, Balschmidt P, Couvreur P. Poly(alkyl cyanoacrylate) nanospheres for oral administration of insulin. J Pharm Sci 1997;86(12):1403-9
  • Damgé C, Aprahamian M, Humbert W, Pinget M. Ileal uptake of polyalkyl-cyanoacrylate nanocapsules in the rat. J Pharm Pharmacol 2000;52(9):1049-56
  • Cournarie F, Auchere D, Chevenne D, Lacour B, Seiller M, Vauthier C. Absorption and efficiency of insulin after oral administration of insulin-loaded nanocapsules in diabetic rats. Int J Pharm 2002;242(1-2):325-8
  • Cournarie F, Cheron M, Besnard M, Vauthier C. Evidence for restrictive parameters in formulation of insulin-loaded nanocapsules. Eur J Pharm Biopharm 2004;57(2):171-9
  • Mesiha MS, Sidhom MB, Fasipe B. Oral and subcutaneous absorption of insulin poly(isobutylcyanoacrylate) nanoparticles. Int J Pharm 2005;288(2):289-93
  • Leobandung W, Ichikawa H, Fukumori Y, Peppas NA. Preparation of stable insulin-loaded nanospheres of poly(ethylene glycol) macromers and N-isopropyl acrylamide. J Control Rel 2002;80(1-3):357-63
  • Foss AC, Goto T, Morishita M, Peppas NA. Development of acrylic-based copolymers for oral insulin delivery. Eur J Pharm Biopharm 2004;57(2):163-9
  • Li MG, Lu WL, Wang JC, et al. Preparation and characterization of insulin nanoparticles employing chitosan and poly(methylmethacrylate/methylmethacrylic acid) copolymer. J Nanosci Nanotechnol 2006;6(9-10):2874-86
  • Sajeesh S, Sharma CP. Novel pH responsive polymethacrylic acid–chitosan–polyethylene glycol nanoparticles for oral peptide delivery. J Biomed Mater Res B Appl Biomater 2006;76(2):298-305
  • Sajeesh S, Sharma CP. Cyclodextrin–insulin complex encapsulated polymethacrylic acid based nanoparticles for oral insulin delivery. Int J Pharm 2006;325(1-2):147-54
  • Elvassore N, Bertucco A, Caliceti P. Production of insulin-loaded poly(ethylene glycol)/poly(l-lactide) (PEG/PLA) nanoparticles by gas antisolvent techniques. J Pharm Sci 2001;90(10):1628-36
  • Xiong XY, Li YP, Li ZL, et al. Vesicles from pluronic/poly(lactic acid) block copolymers as new carriers for oral insulin delivery. J Control Rel 2007;120(1-2):11-17
  • Barichello JM, Morishita M, Takayama K, Nagai T. Encapsulation of hydrophilic and lipophilic drugs in PLGA nanoparticles by the nanoprecipitation method. Drug Dev Ind Pharm 1999;25(4):471-6
  • Carino GP, Jacob JS, Mathiowitz E. Nanosphere based oral insulin delivery. J Control Rel 2000;65(1-2):261-9
  • Pan Y, Xu H, Zhao HY, Wei G, Zheng JM. Study on preparation and oral efficacy of insulin-loaded poly(lactic-co-glycolic acid) nanoparticles. Yao Xue Xue Bao 2002;37(5):374-7
  • Kumar PS, Ramakrishna S, Saini TR, Diwan PV. Influence of microencapsulation method and peptide loading on formulation of poly(lactide-co-glycolide) insulin nanoparticles. Pharmazie 2006;61(7):613-17
  • Cui FD, Tao AJ, Cun DM, Zhang LQ, Shi K. Preparation of insulin loaded PLGA-Hp55 nanoparticles for oral delivery. J Pharm Sci 2007;96(2):421-7
  • Attivi D, Wehrlé P, Ubrich N, Damgé C, Hoffman M, Maincent P. Formulation of insulin-loaded polymeric nanoparticles using response surface methodology. Drug Dev Ind Pharm 2005;31(2):179-89
  • Damgé C, Maincent P, Ubrich N. Oral delivery of insulin associated to polymeric nanoparticles in diabetic rats. J Control Rel 2007;117(2):163-70
  • Ma Z, Lim TM, LIM LY. Pharmacological activity of peroral chitosan-insulin nanoparticles in diabetic rats. Int J Pharm 2005;293(1-2):271-80
  • Mao S, Bakowsky U, Jintapattanakit A, Kissel T. Self-assembled polyelectrolyte nanocomplexes between chitosan derivatives and insulin. J Pharm Sci 2006;95(5):1035-48
  • Fan YF, Wang YN, Fan YG, Ma JB. Preparation of insulin nanoparticles and their encapsulation with biodegradable polyelectrolytes via the layer-by-layer adsorption. Int J Pharm 2006;324(2):158-67
  • Qian F, Cui F, Ding J, Tang C, Yin C. Chitosan graft copolymer nanoparticles for oral protein drug delivery: preparation and characterization. Biomacromolecules 2006;7(10):2722-7
  • Sarmento B, Ribeiro A, Veiga F, Ferreira D. Development and characterization of new insulin containing polysaccharide nanoparticles. Colloids Surf B Biointerfaces 2006;53(2):193-202
  • Sarmento B, Ribeiro A, Veiga F, Ferreira D, Neufeld R. Oral bioavailability of insulin contained in polysaccharide nanoparticles. Biomacromolecules 2007;8(10):3054-60
  • Krauland AH, Alonso MJ. Chitosan/cyclodextrin nanoparticles as macromolecular drug delivery system. Int J Pharm 2007;340(1-2):134-42
  • Bhumkar DR, Joshi HM, Sastry M, Pokharkar VB. Chitosan reduced gold nanoparticles as novel carriers for transmucosal delivery of insulin. Pharm Res 2007;24(8):1415-26
  • Jintapattanakit A, Junyaprasert VB, Mao S, Sitterberg J, Bakowsky U, Kissel T. Peroral delivery of insulin using chitosan derivatives: a comparative study of polyelectrolyte nanocomplexes and nanoparticles. Int J Pharm 2007;342(1-2):240-9
  • Pan Y, Li YJ, Zhao HY, et al. Bioadhesive polysaccharide in protein delivery system: chitosan nanoparticles improve the intestinal absorption of insulin in vivo. Int J Pharm 2002;249(1-2):139-47
  • Pan Y, Li YJ, Gao P, Ding PT, Xu H, Zheng JM. Enhancement of gastrointestinal absorption of chitosan-coated insulin-loaded poly(lactic-co-glycolic acid) nanoparticles. Yao Xue Xue Bao 2003;38(6):467-70
  • Pinto Reis C, Ribeiro AJ, Houng S, Veiga F, Neufeld RJ. Nanoparticulate delivery system for insulin: design, characterization and in vitro/in vivo bioactivity. Eur J Pharm Sci 2007;30(5):392-7
  • Sarmento B, Ferreira DC, Jorgensen L, Van de Weert M. Probing insulin's secondary structure after entrapment into alginate/chitosan nanoparticles. Eur J Pharm Biopharm 2007;65(1):10-17
  • Sarmento B, Ribeiro A, Veiga F, Sampaio P, Neufeld R, Ferreira D. Alginate/chitosan nanoparticles are effective for oral insulin delivery. Pharm Res; 2007;24(12):2198-206
  • Damgé C, Pinto Reis C, Ubrich N, Maincent P, Veiga F, Ribeiro A. Nanoparticules d'insuline à base d'alginate-dextran pour l'administration orale chez le rat diabétique. Diabet Metabol 2007;33:1S67
  • Zhang N, Ping Q, Huang G, Han X, Cheng Y, Xu W. Transport characteristics of wheat germ agglutinin-modified insulin-liposomes and solid lipid nanoparticles in a perfused rat intestinal model. J Nanosci Nanotechnol 2006;6(9-10):2959-66
  • Zhang N, Ping Q, Huang G, Xu W, Cheng Y, Han X. Lectin-modified solid lipid nanoparticles as carriers for oral administration of insulin. Int J Pharm 2006;327(1-2):153-9
  • Liu J, Gong T, Wang C, Zhong Z, Zhang Z. Solid lipid nanoparticles loaded with insulin by sodium cholate-phosphatidylcholine-based mixed micelles: preparation and characterization. Int J Pharm 2007;340(1-2):153-62
  • Sarmento B, Martins S, Ferreira D, Souto EB. Oral insulin delivery by means of solid lipid nanoparticles. Int J Nanomed 2007;(on-line early)
  • Chalasani KB, Russell-Jones GJ, Yandrapu SK, Diwan PV, Jain SK. A novel vitamin B12-nanosphere conjugate carrier system for peroral delivery of insulin. J Control Rel 2007;117(3):421-9
  • Cheng K, Lim LY. Insulin-loaded calcium pectinate nanoparticles: effects of pectin molecular weight and formulation pH. Drug Dev Ind Pharm 2004;30(4):359-67
  • Morcol T, Nagappan P, Nerenbaum L, Mitchell A, Bell SJ. Calcium phosphate–PEG–insulin–casein (CAPIC) particles as oral delivery systems for insulin. Int J Pharm 2004;277(1-2):91-7
  • Al Khouri Fallouh N, Roblot-Treupel L, Fessi H, Devissaguet JP, Puisieux F. Development of a new process for the manufacture of polyisobutylcyanoacrylate nanocapsules. Int J Pharm 1986;28(2-3):125-32
  • Michel C, Aprahamian M, Defontaine L, Couvreur P, Damgé C. The effect of site of administration in the gastrointestinal tract on the absorption of insulin from nanocapsules in diabetic rats. J Pharm Pharmacol 1991;43(1):1-5
  • Lowe PJ, Temple CS. Calcitonin and insulin in isobutylcyanoacrylate nanocapsules: protection against proteases and effect on intestinal absorption in rats. J Pharm Pharmacol 1994;46(7):547-52
  • Aboubakar M, Puisieux F, Couvreur P, Vauthier C. Physico-chemical characterization of insulin-loaded poly(isobutylcyanoacrylate) nanocapsules obtained by interfacial polymerization. Int J Pharm 1999;183(1):63-6
  • Radwan MA. Enhancement of absorption of insulin-loaded polyisobutylcyanoacrylate nanospheres by sodium cholate after oral and subcutaneous administration in diabetic rats. Drug Dev Ind Pharm 2001;27(9):981-9
  • Sullivan CO, Birkinshaw C. In vitro degradation of insulin-loaded poly (n-butylcyanoacrylate) nanoparticles. Biomaterials 2004;25(18):4375-82
  • MA Z, Yeoh HH, Lim LY. Formulation pH modulates the interaction of insulin with chitosan nanoparticles. J Pharm Sci 2002;91(6):1396-404
  • Tiyaboonchai W, Woiszwillo J, Sims RC, Middaugh CR. Insulin containing polyethylenimine–dextran sulfate nanoparticles. Int J Pharm 2003;255(1-2):139-51
  • Lin YH, Mi FL, Chen CT, et al. Preparation and characterization of nanoparticles shelled with chitosan for oral insulin delivery. Biomacromolecules 2007;8(1):146-52
  • Pinto-Alphandary H, Aboubakar M, Jaillard D, Couvreur P, Vauthier C. Visualization of insulin-loaded nanocapsules: in vitro and in vivo studies after oral administration to rats. Pharm Res 2003;20(7):1071-84
  • Allemann E, Leroux JC, Gurny R. Polymeric nano-microparticles for the oral delivery of peptides and peptidomimetics. Adv Drug Deliv Rev 1998;34(2-3):171-89
  • Li MG, Lu WL, Wang JC, et al. Distribution, transition, adhesion and release of insulin loaded nanoparticles in the gut of rats. Int J Pharm 2007;329(1-2):182-91
  • Caliceti P, Salmaso S, Elvassore N, Bertucco A. Effective protein release from PEG/PLA nanoparticles produced by compressed gas anti-solvent precipitation techniques. J Control Rel 2004;94(1):195-205
  • Joshi HM, Bhumkar DR, Joshi K, Pokharkar V, Sastry M. Gold nanoparticles as carriers for efficient transmucosal insulin delivery. Langmuir 2006;22(1):300-5
  • Norris DA, Puri N, Sinko PJ. The effect of physical barriers and properties on the oral absorption of particulates. Adv Drug Deliv Rev 1998;34(2-3):135-54
  • Aprahamian M, Michel C, Humbert W, Devissaguet JP, Damgé C. Transmucosal passage of polyalkylcyanoacrylate nanocapsules as a new drug carrier in the small intestine. Biol Cell 1987;61(1-2):69-76
  • Van Der Merwe SM, Verhoef JC, Verheijden JH, Kotzé AF, Junginger HE. Trimethylated chitosan as polymeric absorption enhancer for improved peroral delivery of peptide drugs. Eur J Pharm Biopharm 2004;58(2):225-35
  • Pillion DJ, Ganapathy V, Leibach FH. Identification of insulin receptors on the mucosal surface of colon epithelial cells. J Biol Chem 1985;260(9):5244-7
  • Fernandez-Moreno MD, Serrano-Rios M, Prieto JC. Identification of insulin receptors in epithelial cells from duodenum, jejunum, ileum, caecum, colon and rectum in the rat. Diabete Metab 1987;13(2):135-9
  • Swaan PW. Recent advances in intestinal macromolecular drug delivery via receptor-mediated transport pathways. Pharm Res 1998;15(6):826-34
  • Kreuter J. Peroral administration of nanoparticles. Adv Drug Deliv Rev 1991;7(1):71-86
  • Saï P, Damgé C, Rivereau AS, Hoeltzel A, Gouin E. Prophylactic oral administration of metabolically active insulin entrapped in isobutylcyanoacrylate nanocapsules reduces the incidence of diabetes in nonobese diabetic mice. J Autoimmun 1996;9(6):713-22
  • Radwan MA, Aboul-Enein HY. The effect of oral absorption enhancers on the in vivo performance of insulin-loaded poly(ethylcyanoacrylate) nanospheres in diabetic rats. J Microencapsul 2002;19(2):225-35
  • Lenaerts V, Nagelkerke JF, Van Berkel TJ, et al. In vivo uptake of polyisobutyl cyanoacrylate nanoparticles by rat liver Kupffer, endothelial, and parenchymal cells. J Pharm Sci 1984;73(7):980-2
  • Modi P, Mihic M, Lewin A. The evolving role of oral insulin in the treatment of diabetes using a novel RapidMist System. Diabetes Metab Res Rev 2002;18(Suppl 1):S38-S42
  • Guevara-Aguirre J, Guevara-Aguirre M, Saavedra J, Bernstein G, Rosenbloom AL. Comparison of oral insulin spray and subcutaneous regular insulin at mealtime in type 1 diabetes. Diabetes Technol Ther 2007;9(4):372-6
  • Kidron M, Dinh S, Menachem Y, et al. A novel per-oral insulin formulation: proof of concept study in non-diabetic subjects. Diabet Med 2004;21(4):354-7

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