110
Views
20
CrossRef citations to date
0
Altmetric
Original Articles

Physiological approaches to determining gut endogenous amino acid flows in the mammal

, &
Pages 237-252 | Published online: 10 Jan 2009

References

  • Angkanaporn , K. , Ravindran , V. , Mollah , Y. and Bryden , W. L. 1997a . Secretion of homoarginine into the gut of chickens. . Vet. Res. Comm. , 21 : 161 – 67 .
  • Angkanaporn , K. , Ravindran , V. , Mollah , Y. and Bryden , W. L. 1997b . Homoarginine influences voluntary feed intake, tissue basic amino acid concentrations and arginase activity in chickens. . J. Nutr. , 127 : 1128 – 1136 .
  • Bastianelli, D. 1996 Ph.D. Thesis. Institut National Agronomique, Paris, France
  • Bergner , U. , Bergner , H. and Simon , O. 1984 . Untersuchungen zu endogenen N‐Umsatzprozessen an 15N‐markierten Schweinen. 2. Fäkale Exkretion von Aminosäuren und 15N‐markierten Aminosäuren bei unterschiedlichem Rohfasergehalt der Diäten . Arch. Anim. Nutr. , 34 : 505 – 517 .
  • Boisen , S. and Moughan , P. J. 1996 . Dietary influences on endogenous ileal protein and amino acid loss in the pig‐A review. . Acta Agri. Scand. , 46 : 154 – 164 .
  • Buraczewska , L . 1979 . Secretion of nitrogenous compounds in the small intestine of pigs . Acta Physiol. Pol. , 30 : 319 – 326 .
  • Buraczewski , S. 1980 . Aspects of protein digestion and metabolism in monogastric animals . Proc. of the 3rd EAAP Symp. on Protein Metabolism and Nutrition. European Association for Animal Production . 1980 , Braunschweig, Germany. Edited by: Oslage , H. J. and Rohr , K. pp. 179 – 195 . European Association for Animal Production Publication . No. 27.
  • Butts , C. A. 1991 . Endogenous Ileal Amino Acid Excretion in Monogastric Animals. , Palmerston North, , New Zealand : Massey University . Ph.D. Thesis
  • Butts , C. A. , Moughan , P. J. and Smith , W. C. 1992 . Protein nitrogen, peptide nitrogen and free amino acid nitrogen in endogenous digesta nitrogen at the terminal ileum of the rat. . J. Sci. Food Agric. , 59 : 291 – 98 .
  • Butts , C. A. , Moughan , P. J. , Smith , W. C. and Carr , D. H. 1993a . Endogenous lysine and other amino acid flows at the terminal ileum of the growing pig (20 kg bodyweight): The effect of protein‐free, synthetic amino acid, peptide and protein alimentation. . J. Sci. Food Agric. , 61 : 31 – 40 .
  • Butts , C. A. , Moughan , P. J. , Smith , W. G. , Reynolds , G. W. and Garrick , D. J. 1993b . The effect of food dry matter intake on endogenous ileal amino acid excretion determined under peptide alimentation in the 50 kg liveweight pig. . J. Sci. Food Agric. , 62 : 235 – 43 .
  • Chung , T. K. and Baker , D. H. 1992 . Apparent and true digestibility of a crystalline amino acid mixture and of casein: Comparison of values obtained with ileal‐cannulated pigs and cecectomized cockerels. . J. Anim. Sci. , 70 : 3781 – 90 .
  • Corring , T. 1980a . The adaptation of digestive enzymes to the diet: Its physiological significance. . Reprod. Nutr. Dev. , 20 : 1217 – 1235 .
  • Corring , T. and Saucier , R. 1972 . Sécrétion pancréatique sur porc fistulé adaptation a la teneur en protéines du régime. . Ann. Biol. Biochem. Biophys. , 12 : 233 – 241 .
  • Darragh , A. J. , Moughan , P. J. and Smith , W. C. 1990 . The effect of amino acid and peptide alimentation on the determination of endogenous amino acid flow at the terminal ileum of the rat. . J. Sci. Food Agric. , 51 : 47 – 56 .
  • de Lange , C. F. M. , Sauer , W. C. , Mosenthin , R. and Souffrant , W. B. 1989 . The effect of feeding different protein‐free diets on the recovery and amino acid composition of endogenous protein collected from the distal ileum and feces in pigs. . J. Anim. Sci. , 67 : 746 – 754 .
  • de Lange , C. F. M. , Sauer , W. C. , Souffrant , W. B. and Lien , K. A. 1992 . 15N‐leucine and 15N‐isoleucine isotope dilution technique versus the 15N‐isotope dilution technique for determining the recovery of endogenous protein and amino acids in digesta collected from the distal ileum in pigs . J. Anim. Sci. , 70 : 1848 – 1856 .
  • de Lange , C. F. M. , Souffrant , W. B. and Sauer , W. C. 1990 . Real ileal protein and amino acid digestibilities in feedstuffs for growing pigs as determined with the 15N‐isotope dilution technique . J. Anim. Sci. , 68 : 409 – 418 .
  • Donkoh , A. , Moughan , P. J. and Morel , P. C. H. 1995 . Comparison of methods to determine the endogenous amino acid flow at the terminal ileum of the growing rat . J Sci. Food Agric. , 67 : 359 – 66 .
  • Drescher , K. , Hagemeister , H. , de Vrese , M. , Roos , N. , Middendorf , K. and Rantamäki , P. 1994 . Guanidination (homoarginine‐labelling) of proteins does affect prececal 15N recovery in pigs . Proc. VIth Intern. Symp. on Digestive Physiology in Pigs. 1994 , Germany. Edited by: Souffrant , W.‐B. and Hagemeister , H. pp. 64 – 66 . EAAP Publication No. 80
  • Erbersdobler , H. F. and Lee , K. H. 1991 . Protein digestibility and lysine bioavailability in native and heat treated casein using the homoarginine method in rats . Proc. of the VIth Intern. Symp. on Protein Metabolism and Nutrition. 1991 , Foulum, Denmark. Edited by: Eggum , B. O. , Boisen , S. , Barsting , C. , Danfær , A. and Hvelplund , T. pp. 88 – 102 . National Institute for Animal Science .
  • Fan , M. Z. , Sauer , W. C. and McBurney , M. I. 1995 . Estimation by regression analysis of endogenous amino acid levels in digesta collected from the distal ileum. . J. Anim. Sci. , 73 : 2319 – 28 .
  • Fauconneau , G. and Michel , M. C. 1970 . “ The role of the gastrointestinal tract in the regulation of protein metabolism ” . In Mammalian Protein Metabolism. , Edited by: Munro , H. N. Volume IV , 481 – 522 . London : Academic Press Inc. .
  • Feng , Yu. , Moughan , P. J. and Barry , T. N. 1995 . Effect of condensed tannin in cottonseed hulls on endogenous ileal amino acid loss in the growing rat. . J. Sci. Food Agric. , 68 : 451 – 55 .
  • Frik , R. , Hagemeister , H. , Roos , N. and de Vrese , M. 1997 . Effects of protein‐bound D‐amino acids on true protein digestibility determined by 15N‐and homoarginine‐labeling . Proc. of the VIIth Intern. Symp. on Digestive Physiology in Pigs. 1997 , Saint Malo, France. Edited by: Laplace , J. P. , Fevrier , C. and Barbeau , A. pp. 395 – 399 . Institut National de la Recherche Agronomique . EAAP Publication No. 88
  • Fuller , M. F. and Cadenhead , A. 1991 . Effect of the amount and composition of the diet on galac‐tosamine flow from the small intestine . Proc. of the Vth Intern. Symp. on Digestive Physiology in Pigs. Pudoc . 1991 , Wageningen, The Netherlands. Edited by: Verstagen , M. W. A. , Huisman , J. and den Hartog , L. A. pp. 330 – 333 . EAAP Publication No. 54
  • Gabert , V. M. , Canibe , N. , Jorgensen , H. , Eggum , B. O. and Sauer , W. C. 1997 . Use of 15N‐amino acid isotope dilution techniques to determine endogenous amino acids in ileal digesta in growing pigs . Acta Agric. Scand, Sect. A, Animal Sci. , 47 : 168 – 177 .
  • Gebhardt , G. , Köhler , R. and Zebrowska , T. 1978 . Untersuchungen zur Stickstoff‐und Aminosäurenresorption beim Schwein. 2. Der Verlauf der 15N‐Markierung in Chymus, Harn und Blut . Arch. Anim. Nutr. , 28 : 11 – 20 .
  • Hagemeister , H. and Erbersdobler , H. 1985 . Chemical labelling of dietary protein by transformation of lysine to homoarginine: A new technique to follow intestinal digestion and absorption . Proc. Nutr. Soc. , 44 : 133A
  • Hendriks , W. H. , Moughan , P. J. and Tarttelin , M. F. 1996 . Gut endogenous nitrogen and amino acid excretions in adult domestic cats fed a protein‐free diet or an enzymatically hydrolyzed casein‐based diet . J. Nutr. , 126 : 955 – 962 .
  • Hodgkinson , S. M. , Moughan , P. J. and Reynolds , G. W. 1997 . “ Effect oflive weight on endogenous ileal nitrogen and amino acid excretion in the growing pig ” . In Manipulating Pig Production , Edited by: Cranwell , P. D. 235 Werribee, , Australia : VI. Australasian Pig Science Association .
  • Huisman , J. , Heinz , T. , van der Poel , A. F. B. , van Leeuwen , P. , Souffrant , W. B. and Verstegen , M. W. A. 1992 . True protein digestibility and amounts of endogenous protein measured with the 15N‐dilu‐tion technique in piglets fed on peas (Pisum sativum) and common beans (Phaseolus vulgaris) . Brit. J. Nutr. , 68 : 101 – 110 .
  • Köhler , R. , Zebrowska , T. and Gebhardt , G. 1978 . Untersuchungen zur Stickstoff‐und Aminosäurenresorption beim Schwein. 3. Endogene Ausscheidung und Resorption des Stickstoffs. . Arch. Anim. Nutr. , 28 : 317 – 328 .
  • Krawielitzki , K. and Smulikowska , S. 1977 . Versuche zur Bestimmung des endogenen und exogenen fäkalen N‐Anteiles monogastrischer Tierarten. . Arch. Anim. Nutr. , 27 : 39 – 47 .
  • Krawielitzki , K. , Völker , T. , Smulikowska , S. , Bock , H. D. and Wünche , J. 1977 . Weitere Untersuchungen zum Multikompartment‐Modell des Proteinstoffwechsels . Arch. Anim. Nutr. , 27 : 609 – 627 .
  • Krawielitzki , K. , Zebrowska , T. , Kreienbring , F. , Schadereit , R. and Kowalczyk , J. 1996 . Absorption and secretion of exogenous and endogenous N along the digestive tract and kinetic parameters of protein metabolism in growing pigs. 1. Estimation by digesta exchange between 15N‐labelled and unlabelled pigs . J. Anim. Physiol. a. Anim. Nutr. , 76 : 46 – 56 .
  • Leibholz , J. 1982 . The flow of endogenous nitrogen in the digestive tract of young pigs. . Br. J. Nutr. , 48 : 509 – 517 .
  • Leterme , P. , Monmart , T. , Morandi , P. and Théwis , A. 1994 . Effect of oral and parenteral N nutrition vs N‐free nutrition on the endogenous amino acid flow at the ileum of the pig . Proc. VIth Intern. Symp. on Digestive Physiology in Pigs. 1994 , Germany. Edited by: Souffrant , W.‐B. and Hagemeister , H. pp. 60 – 63 . EAAP Publication No. 80
  • Leterme , P. , Théwis , A. , van Leeuwen , P. , Monmart , T. and Huisman , J. 1996a . Chemical composition of pea fibre isolates and their effect on the endogenous amino acid flow at the ileum of the pig. . J. Sci. Food Agric. , 72 : 127 – 34 .
  • Leterme , P. , Théwis , A. , François , E. , van Leeuwen , P. , Wathelet , B. and Huisman , J. 1996b . The use of 15N‐labeled dietary proteins for determining true ileal amino acid digestibilities is limited by their rapid recycling in the endogenous secretions of pigs . J. Nutr. , 126 : 2188 – 2198 .
  • Leterme , P. , Théwis , A. , Genot , L. , François , E. and Wathelet , B. 1993 . “ Determination of the true ileal digestibility of amino acids in pigs by means of 15N‐labelled diets ” . In Nitrogen Flow in Pig Production and Environmental Consequences. Edited by: Verstegen , M. , den Hartog , L. , van Kempen , G. and Metz , J. 49 – 54 . Wageningen EAAP Publ. No. 69, Pudoc
  • Lien , K. A. , Sauer , W. C. , Mosenthin , R. , Souffrant , W. B. and Dugan , M. E. R. 1997 . Evaluation of the 15N‐isotope dilution technique for determining the recovery of endogenous protein in ileal digestion of pigs: effect of dilution in the precursor pool for endogenous nitrogen secretion . J. Anim. Sci. , 75 : 148 – 158 .
  • Low , A. G. 1980 . Nutrient absorption in pigs. . J. Sci. Food Agric. , 31 : 1087 – 130 .
  • Mahé , S. , Roos , N. , Benamouzig , R. , Sick , H. , Baglieri , A. , Huneau , J. and Tome , D. 1994 . True exogenous and endogenous nitrogen fraction in human's jejunum after feeding low amounts of 15N‐labeled casein . J. Nutr. , 124 : 548 – 555 .
  • Makkink , C. A. , Heinz , T. , Souffrant , W. B. and Verstegen , M. W. A. 1997 . Endogenous N losses at the terminal ileum of young piglets fed diets based on four different protein sources . J. Anim. Feed Sci. , 6 : 219 – 234 .
  • Marty , B. J. , Chavez , E. R. and de Lange , C. F. M. 1994 . Recovery of amino acids at the distal ileum for determining apparent and true ileal amino acid digestibilities in growing pigs fed various heat‐processed full‐fat soybean products . J. Anim. Sci. , 72 : 2029 – 37 .
  • McNeil , N. I. 1988 . Nutritional implication of human and mammalian large intestinal function. . World Rev. Nutr. Diet. , 56 : 1 – 42 .
  • Millward , D. J. , Garlick , P. J. , James , W. P. T. , Sender , P. M. and Waterlow , J. C. 1976 . “ Protein turnover ” . In Protein Metabolism and Nutrition. , EAAP Publication No. 16 Edited by: Cole , D. J. A. , Boorman , K. N. , Buttery , P. J. , Lewis , D. , Neale , R. J. and Swan , H. 49 – 69 . London, , England : Butterworths .
  • Moughan , P. J. , Buttery , P. J. , Essex , C. P. and Soar , J. B. 1992 . Evaluation of the isotope dilution technique for determining ileal endogenous nitrogen excretion in the rat. . J. Sci. Food Agric. , 58 : 165 – 72 .
  • Moughan , P. J. , Darragh , A. J. , Smith , W. C. and Butts , C. A. 1990 . Perchloric and trichloroacetic acids as précipitants of protein in endogenous ileal digesta from the rat . J. Sci. Food Agric. , 52 : 13 – 21 .
  • Moughan , P. J. and Rutherfurd , S. M. 1990 . Endogenous flow of total lysine and other amino acids at the distal ileum of the protein‐or peptide‐fed rat: The chemical labelling of gelatine protein by transformation of lysine to homoarginine. . J. Sci. Food Agric. , 52 : 179 – 192 .
  • Moughan , P. J. and Rutherfurd , S. M. 1991 . Endogenous lysine flow at the distal ileum of the protein‐fed rat: Investigation of the effect of protein source using radioactively labelled acetylated lysine or lysine transformed to homoarginine. . J. Sci. Food Agric. , 55 : 163 – 174 .
  • Moughan , P. J. and Schutten , G. 1991 . Composition of nitrogen‐containing fractions in digesta from the distal ileum of pigs fed a protein‐free diet. . J. Nutr. , 121 : 1570 – 1574 .
  • Munro , H. N. and Goldberg , D. M. 1964 . “ The effect of protein intake on the protein and nucleic acid metabolism of the intestinal mucosal cell ” . In The Role of the Gastrointestinal Tract in Protein Metabolism. , Edited by: Munro , H. N. 189 – 98 . Oxford, , England : Blackwell Scientific Publications .
  • Muramatsu , T. 1990 . Nutrition and whole‐body protein turnover in the chicken in relation to mammalian species. . Nutr. Res. Rev. , 3 : 211 – 228 .
  • Nehring , K. and Haesler , E. 1954 . Untersuchungen über die biologische Wertigkeit von Eiweißfutterstoffen 1. Die Bestimmung der Biologischen Wertigkeit und der Ergänzungswirkung von Eiweißfutterstoffen durch Versuche an wachsenden Ratten . Arch. Anim. Nutr. Beih. , 5 : 110 – 126 .
  • Nyachoti , C. M. , de Lange , C. F. M. and Schulze , H. 1997a . The homoarginine method for determining true ileal lysine digestibilities in casein, barley and canola meal fed to growing pigs . Proc. VIIth Intern. Symp. on Digestive Physiology in Pigs. 1997a , Saint Malo, France. Edited by: Laplace , J. P. , Fevrier , C. and Barbeau , A. pp. 408 – 412 . Institut National de la Recherche Agronomique . EAAP Publication No. 88
  • Nyachoti , C. M. , de Lange , C. F. M. , McBride , B. W. and Schulze , H. 1997b . Significance of endogenous gut nitrogen losses in the nutrition of growing pigs: A review. . Can. J. Anim. Sci. , 77 : 149 – 163 .
  • Ravindran , V. , Imbeah , M. , Angkanaporn , K. and Bryden , W.L. 1996 . Guanidination of lysine in cottonseed protein. . J. Agric. Food Chem. , 44 : 1812 – 1815 .
  • Rodriguez , J. V. , Dubin , M. , Carillo , M. C. and Rodriguez Garay , E. A. 1982 . Influence of a protein‐free diet on bile secretion in the rat . Nutr. Rep. Int. , 26 (1) : 147 – 155 .
  • Rodriguez , J. V. , Dubin , M. , Carillo , M. C. , Monti , J. and Rodriguez Garay , E. A. 1983 . Effect of a protein‐free diet on biliary lipids and protein secretion in the rat. . Nutr. Rep. Int. , 26 (1) : 1261 – 1266 .
  • Roos , N. , Pfeuffer , M. and Hagemeister , H. 1994 . Labelling with 15N as compared with homoarginine suggests a lower prececal digestibility of casein in pigs . J. Nutr. , 124 : 2404 – 2409 .
  • Rutherfurd , S. M. and Moughan , P. J. 1990 . Guanidination of lysine in selected dietary proteins. . J. Agric. Food Chem. , 38 : 209 – 211 .
  • Sauer , W. C. and Ozimek , L. 1986 . Digestibility of amino acids in swine: Results and their practical application. . Livest. Prod. Sci. , 15 : 367 – 88 .
  • Sauer , W. C. 1982 . “ Endogenous nitrogen in balance studies ” . In Physiologie Digestive Chez le Porc. , Edited by: Laplace , J. P. , Corring , T. and Rérat , A. 199 – 204 . Paris, , France : Institut National de la Recherche Agronomique .
  • Schadereit , R. , Krawielitzki , K. , Zebrowska , T. , Kowalczyk , J. and Kreienbring , F. 1995 . Intestinal nitrogen flow, total nitrogen and 15N balance in pigs labelled intravenously with 15N‐leucine and fed a meat meal diet . J. Anim. Feed Sci. , 4 : 207 – 215 .
  • Schmitz , M. , Hagemeister , H. and Erbersdobler , H. F. 1991 . Homoarginine labelling is suitable for determination of protein absorption in miniture pigs. . J. Nutr. , 121 : 1575 – 1580 .
  • Schneeman , B. O. , Chang , I. , Smith , L. B. and Lyman , R. L. 1977 . Effect of dietary amino acids, casein, and soybean trypsin inhibitor on pacreatic protein secretion in rats. . J. Nutr. , 107 : 281 – 288 .
  • Schulze , H. , Butts , C. A. , Moughan , P. J. and Verstegen , M. W. A. 1995 . The 15N‐isotope dilution method for determining ileal endogenous nitrogen excretion in the young (10 kg liveweight) pig. . J. Sci. Food Agric. , 69 : 41 – 50 .
  • Schulze , H. , van Leeuwen , P. , Verstegen , M. W. A. , Huisman , J. , Souffrant , W. B. and Ahrens , F. 1994 . Effect of the level of dietary Neutral Detergent Fiber on ileal apparent digestibility and ileal nitrogen losses in pigs. . J. Anim. Sci. , 72 : 2362 – 2368 .
  • Schuttert , G. , Moughan , P. J. and Jackson , F. 1991 . In vitro determination of the extent of hydrolysis of homoarginine by arginase in the small intestine of the growing rat . J. Agric. Food Chem. , 39 : 511 – 513 .
  • Simon , O. 1989 . “ Metabolism of proteins and amino acids ” . In Protein Metabolism in Farm Animals , Edited by: Bock , H.‐D. , Eggum , B. O. , Low , A. G. , Simon , O. and Zebrewska , T. 273 – 366 . Oxford, , England : Oxford University Press .
  • Simon , O. , Bergner , H. , Münchmeyer , R. and Zebrowska , T. 1983 . Untersuchungen zur Magen‐und Pankreasekretion beim Schwein. . Arch. Anim. Nutr. , 33 : 532 – 541 .
  • Simon , O. , Zebrowska , T. , Münchmeyer , R. , Bergner , H. and Rohrmann , H. 1986 . Studies on the secretion of amino acids and urea into the gastrointestinal tract of pigs. 1. Secretion of leucine into the stomach and upper part of the duodenum during continous intravenous infusion of 14C‐leucine. . Arch. Anim. Nutr. , 36 : 5 – 16 .
  • Siriwan , P. , Bryden , W. L. and Annison , E. F. 1994 . Use of guanidinated dietary protein to measure losses of endogenous amino acids in poultry. . Br. J. Nutr. , 71 : 515 – 529 .
  • Skilton , G. A. , Moughan , P. J. and Smith , W. C. 1988 . Determination of endogenous amino acid flow at the terminal ileum of the rat. . J. Sci. Food Agric. , 44 : 227 – 235 .
  • Snook , J. T. and Meyer , J. H. 1964 . Response of digestive enzymes to dietary protein. . J. Nutr. , 82 : 409 – 414 .
  • Souffrant , W. B. 1991 . Endogenous nitrogen losses during digestion in pigs . Proc. Vth Int. Symp. on Digestive Physiology in Pigs . 1991 , Pudoc, Wageningen. Edited by: Verstegen , M. W. A. , Huisman , J. and den Hartog , L. A. pp. 147 – 166 . EAAP Publ. No. 54
  • Souffrant , W. B. , Février , C. , Laplace , J. P. and Hennig , U. 1997 . Comparison of methods to estimate ileal endogenous nitrogen and amino acids in piglets . Proc. VIIth Internat. Symp. Digestive Physiology in Pigs. 1997 , St. Malo. Edited by: Laplace , J. P. , Février , C. and Barbeau , A. pp. 591 – 595 . EAAP Publ. No. 88
  • Souffrant , W. B. , Köhler , R. and Gebhardt , G. 1981 . Untersuchungen zur Bestimmung der endogenen N‐Sekretion im Dünndarm bei Schweinen. . Arch. Anim. Nutr. , 31 : 35 – 43 .
  • Souffrant , W. B. , Köhler , R. and Gebhardt , G. 1982 . “ Déterinmationde l'azote endogène dans le contenus digestifs par le technique isotopique (15N) ” . In Physiologie Digestive chez les Porc. , Edited by: Laplace , J. P. , Corring , T. and Rérat , A. 175 – 187 . Paris : INRA Publications . Les colloques de l'INRA No. 12
  • Souffrant , W. B. , Rérat , A. , Laplace , J. P. , Darcy‐Vrillon , B. , Köhler , R. , Corring , T. and Gebhardt , G. 1993 . Exogenous and endogenous contributions to nitrogen fluxes in the digestive tract of pigs fed a casein diet. III. Recycling of endogenous nitrogen. . Reprod. Nutr. Dev. , 33 : 373 – 382 .
  • Taverner M. R. 1979 Ph. D. Thesis, University of New England, Australia
  • Wünsche , J. , Herrmann , U. , Meinl , M. , Hennig , U. , Kreienbring , F. and Zwierz , P. 1987 . Einfluss exogener Faktoren auf die präzäkale Nährstoff‐und Aminosäurenresorption, ermittelt an Schweinen mit Ileo‐Rektal‐Anastomosen. . Arch. Anim. Nutr. , 37 : 745 – 764 .
  • Zebrowska , T. , Kowalczyk , J. , Krawielitzki , K. , Hennig , U. and Schadereit , R. 1992 . Studies on absorption and secretion of 15N endogenous nitrogen along the digestive tract of pigs . J. Anim. Feed Sci. , 1 : 151 – 163 .

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.