- Email: [email protected]
The study of antigenotoxic effects of dietary fibre is lost in a confused concept
Mutation Research 447 Ž2000. 319–322 www.elsevier.comrlocatermolmut Community address: www.elsevier.comrlocatermutres
Current Issues in Mutagenesis and Carcinogenesis No. 96
The study of antigenotoxic effects of dietary fibre is lost in a confused concept Lynnette R. Ferguson a,) , Philip J. Harris b a
Auckland Cancer Society Research Centre, Faculty of Medical and Health Sciences, The UniÕersity of Auckland, PriÕate Bag 92019, Auckland 1000, New Zealand b School of Biological Sciences, The UniÕersity of Auckland, PriÕate Bag 92019, Auckland, New Zealand
Keywords: Dietary fibre; Antigenotoxicity; Cancer
Considerable interest and debate have been generated by the publication of a large and well-conducted cohort study which failed to show that dietary fibre ŽDF. protects against cancers of the colon and rectum w1x. Explanations given include the possibilities that DF was estimated inappropriately w2x, that stool parameters rather than DF should be the relevant measure w3,4x, and that food intake was measured inappropriately w5x. An alternative explanation is that the results are indeed true ones, and that DF plays no protective role in colorectal or other cancers w6,7x. The debate has reached Mutation Research where, in this series of occasional articles, Santana-Rios and Dashwood w8x ask whether it is ‘‘time to discontinue antigenotoxicity studies of dietary fibre.’’ We disagree. Indeed, we question whether such studies have ever effectively started and we contend that it is time they did. A number of studies have now been published, purporting to examine the effects of DF in human populations. However, the results are often quite
)
Corresponding author. Tel.: q64-9-373-7599 ext. 6372; fax: q64-9-373-7502. E-mail address: [email protected] ŽL.R. Ferguson..
confusing and are becoming more so. We believe that one of the most important problems in interpreting some of the recent studies is the wide range of quite different materials, with different chemical structures and properties, that are now included in the term DF. Many definitions of DF have been proposed, but as Heaton w9x remarked in 1983, ‘‘the major source of DF by any definition is plant cell walls,’’ and ‘‘the common denominator in all concepts of DF is the plant cell wall.’’ Despite this, the range of materials now included in the term DF usually extends beyond just plant cell walls. This range includes components obtained from these walls such as pectin and cellulose preparations. It also includes non-starch polysaccharides from sources other than plant cell walls; these polysaccharides are often water-soluble and are used as food additives. It also includes polysaccharides produced by microorganisms, extracted from seaweed cell walls, and exuded from plants w10x. An associated problem is that the analytical methods for determining DF do not all quantify the same materials w11x. Thus, the DF content of a food depends on the method used to determine DF. For example, the AOAC method for determining total DF will not only include all of the materials indicated above, but will also include Mail-
0027-5107r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 7 - 5 1 0 7 Ž 9 9 . 0 0 2 2 3 - 7
320
L.R. Ferguson, P.J. Harrisr Mutation Research 447 (2000) 319–322
lard browning products and some resistant starch. With the development of ‘‘functional foods,’’ some authors wish to extend further the range of materials encompassed by DF to include resistant starch and certain oligosaccharides w12x. Furthermore, other authors take an even broader view and assume that cereal brans are DF! We believe that the fallacy is in assuming that, because a material can be included in the term DF, it must have health benefits. In fact, the available evidence suggests that these different materials have quite different effects on human health. Despite a plethora of literature purporting to show DF effects in animal or in vitro studies, the vast majority of these studies have not used whole plant cell walls. Studies purporting to show the effects of DF often use wheat bran, oat bran, or pectin preparations. However, cereal brans are simply sources of plant cell walls; in particular, oat bran often contains no more than 20% wrw plant cell walls. Although pectin preparations are extracted from plant cell walls, they are chemically modified during the extraction. Furthermore, plant cell walls should not be regarded as simple mixtures of components, and experiments done with a particular extracted component probably have little relevance to the effects of whole cell walls. We also wish to emphasise that plant cell walls themselves vary enormously in structure and composition, depending on the plant cell type and species of food plant w13x. For example, the cell walls in wheat bran are very different in composition and properties from those in cabbage. Although plant cell walls are composed mostly of polysaccharides, the structures of these vary; walls may also contain many other components, including lignin or suberin, and proteins or glycoproteins. Our plea is to describe, in as great a detail as possible, the plant material containing the cell walls. As there is now increasing amounts known about the structure and composition of the cell walls of well described food plants at specified stages of development, this information could be applied to foods consumed in population studies. In vitro studies with well-described, specific types of pant cell walls and with well-described, specific non-starch polysaccharides not only illustrated that materials included in the term DF can be antigenotoxic, but also highlighted the differences between whole plant cell walls and non-starch polysaccharide
preparations both from plant cell walls and other sources. By adsorbing mutagens, whole plant cell walls that contain the hydrophobic polymers suberin and lignin can be antimutagenic w14x. Little or no adsorption occurs to the walls of parenchyma cells that do not contain these polymers but form the bulk of fruits and vegetables. Furthermore, no adsorption occurred in the water-soluble non-starch polysaccharides we tested w15x or starch granules, and we believe it is unlikely that such adsorption would occur in oligosaccharides. These studies also emphasised that the amount of adsorption depends not only on the DF material, but also on the chemical structure of the mutagen. At this stage, we have no formal proof that this in vitro mechanism for antigenotoxicity operates in vivo. Nevertheless, we found that a specific type of whole plant cell wall that contains suberin and which was the most effective in our in vitro studies also protected rats in vivo against the development of aberrant crypts, an early index of colon cancer, induced by the carcinogen 2-amino-3-methylimidazow4,5-f xquinoline ŽIQ. w16x. We suggested that these specific cell walls may show protection against genotoxic events in vivo through carcinogen adsorption andror reduced transit time andror increased faecal bulk, all effects that would reduce the probability of the interaction of carcinogen and colonocytes. On the contrary, Maziere et al. w17x showed that resistant starch failed to protect against the initiation of aberrant crypts in rats. This was not surprising to us since resistant starch has little effect on transit time or carcinogen adsorption w18x. In addition to reducing carcinogen bioavailability, other mechanisms have been proposed whereby DF, as distinct from intracellular phytochemicals, could be antigenotoxic in vivo. These mechanisms usually involve indirect effects w10x and include modulation of xenobiotic metabolism. At present, there are only a handful of antigenotoxicity studies on whole plant cell walls. This is not surprising since they are difficult to isolate in sufficient quantities to study well. However, there is also a dearth of well-controlled antigenotoxicity studies on other materials now often included in the term DF on either spontaneous mutagenesis, or against mutagens that are present in the human diet. These studies are important, since they will tell us about the effects on tumour initiation. We
L.R. Ferguson, P.J. Harrisr Mutation Research 447 (2000) 319–322
note, for example, that certain dietary oligosaccharides have been tested on a transplantable tumour model w19x; however, this tells us nothing about their effects on critical early mutagenic events. It would be naıve ¨ to assume that all materials, now often included in the term DF, are antigenotoxic. Although the data up until now have not been entirely consistent, in general epidemiology has shown that DF protects against cancer w20x. The study by Fuchs et al. w1x is the first major study that suggests otherwise. When the term DF was first used, most of the DF in western diets was consumed in the form of whole plant cell walls in fruits, vegetables, and cereals. However, increasingly higher proportions of other materials are making up the total amount of DF consumed. Some of the first ‘‘fibre-enriched’’ foods had water-soluble, non-starch polysaccharides added to them to increase their content of DF. Currently, there is a trend to increase the content of resistant starch and oligosaccharides. It is sobering to consider the possibility that, at least some of these materials are not beneficial and are actually diluting the beneficial effects of whole plant cell walls. Indeed, the first human intervention study for a preparation rich in a specific water-soluble, non-starch polysaccharide has now been published w21x. Far from protecting against carcinogenesis, this preparation enhanced it. Nevertheless, a whole industry is developing based on materials included in foods under the DF banner. For the most part, we simply do not know whether they will be antigenotoxic, anticarcinogenic, or neither. We, therefore ,believe that there is a justification for restricting the term DF to whole plant cell walls. We believe DF should not include intracellular materials, components obtained from plant cell walls, or non-starch polysaccharides from sources other than plant cell walls. Although the latter two materials will be quantified in the AOAC method, they can be accounted for when they are added to foods. These materials should be described in terms of their chemical structure and source. In conclusion, despite an apparently large literature of antigenotoxic effects of DF, there are only very few studies in appropriate animal models that actually reflect antigenotoxic effects Žor otherwise. of whole plant cell walls, or other DF that are currently being eaten. Indeed, as we have previously
321
pointed out, some of the protection found in many of the animal studies using wheat bran could result from the effects of various protective intracellular phytochemicals and not the effects of DF w22,23x. This is also likely to be true to other cereals, fruits, and vegetables that appear protective in human or animal studies. Nevertheless, we wish to emphasise that this does not mean that DF cannot be protective. Indeed, as indicated above, we have shown that certain types of whole cell walls ŽDF. can indeed protect, at least against the formation of aberrant crypts w16x. Additionally, as Santana-Rios and Dashwood w8x rightly point out, we should be putting equal weight onto studies of intracellular phytochemicals in protective DF sources. Only with an adequate number of well-conducted studies on well described DF can we begin to sort out the true role of DF in protection against carcinogenesis. References w1x C.S. Fuchs, E.L. Giovannucci, G.A. Colditz, D.J. Hunetr, M.J. Stamfer, B. Rosner, F.E. Speizer, W.C. Willett, Dietary fibre and the risk of colorectal cancer adenoma in women, N. Engl. J. Med. 340 Ž1999. 169–176. w2x J.H. Cummings, D.A.T. Southgate, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w3x N.D. Ravin, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w4x K.W. Heaton, S.J. Lewis, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w5x Z. Madar, A. Stark, N. Engl. J. Med. 340 Ž1999. 1926, Letter to the editor. w6x J.D. Potter, Fiber and colorectal cancer — where to now? N. Engl. J. Med. 340 Ž1999. 223–224. w7x K.M. Mohandas, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w8x G. Santana-Rios, R.H. Dashwood, Time to discontinue antigenotoxicity studies of dietary fiber? Mutat. Res., 429, 269–271. w9x K.W. Heaton, Dietary fibre: concepts and definition, in: Fibre in Human and Animal Nutrition, G. Wallace, L. Bell ŽEds.., R. Soc. N. Z., Bull. 20 Wellington, New Zealand, 1983, pp. 19–21. w10x P.J. Harris, L.R. Ferguson, Dietary fibre: its composition and role in protection against colorectal cancer, Mutat. Res. 290 Ž1993. 97–110. w11x P.J. Harris, L.R. Ferguson, Dietary fibres may protect or enhance carcinogenesis, Mutat. Res. 443 Ž1999. 95–110. w12x J.W. Devries, L. Prosky, B. Li, S. Cho, A historical perspective on defining dietary fibre, Cereal Foods World 44 Ž1999. 367–370. w13x A. Bacic, P.J. Harris, B.A. Stone, Structure and function of
322
w14x
w15x
w16x
w17x
w18x
L.R. Ferguson, P.J. Harrisr Mutation Research 447 (2000) 319–322 plant cell walls, in: J. Preiss ŽEd.., The Biochemistry of Plants: Carbohydrates Vol. 14 Academic Press, San Diego, 1988, pp. 297–371. P.J. Harris, C.M. Triggs, A.M. Roberton, M.E. Watson, L.R. Ferguson, The adsorption of heterocyclic aromatic amines by model dietary fibres with contrasting compositions, Chem.Biol. Interact. 100 Ž1996. 13–25. P.J. Harris, A.M. Roberton, M.E. Watson, C.M. Triggs, L.R. Ferguson, The effects of soluble-fibre polysaccharides on the adsorption of a hydrophobic carcinogen to an insoluble dietary fibre, Nutr. Cancer 19 Ž1993. 43–54. L.R. Ferguson, P.J. Harris, Suberized plant cell walls suppress formation of heterocyclic amine-induced aberrant crypts in a rat model, Chem. Biol. Interact. 114 Ž1998. 191–209. S. Maziere, K. Meflah, E. Tavan, M. Champ, J.F. Narbonne, P. Cassand, Effect of resistant starch andror fat-soluble vitamins A and E on the initiation stage of aberrant crypts in rat colon, Nutr. Cancer 31 Ž1998. 168–177. L.R. Ferguson, C. Tasman-Jones, Hans Englyst, P.J. Harris, Comparative effects of three resistant starch preparations on
w19x
w20x
w21x
w22x
w23x
transit time and short chain fatty acid production in rats, Nutr. Cancer, in press. H.S. Taper, N. Delzenne, M.B. Roberfroid, Growth inhibition of transplantable mouse tumours by non-digestible carbohydrates, Int. J. Cancer 71 Ž1997. 1109–1112. B. Trock, E. Lanza, P. Greenwald, Dietary fibre, vegetables, and colon cancer: critical review and meta-analysis of the epidemiological evidence, J. Natl. Cancer Inst. 82 Ž1990. 650–661. J. Faivre, C. Bonithon-Kopp, O. Kronberg, U. Rath, A. Giacosa, A randomised trial of calcium and fibre supplementation in the prevention of recurrence of colorectal adenomas. A European intervention study, Gasteroenterology 116 Ž1999. GO238. L.R. Ferguson, P.J. Harris, Does wheat bran or does wheat dietary fibre protect against cancer?, Int. J. Cancer 78 Ž1998. 385–386. L.R. Ferguson, P.J. Harris, Protection against cancer by wheat bran: role of dietary fibre and phytochemicals, Eur. J. Cancer Prev. 8 Ž1999. 17–25.
Current Issues in Mutagenesis and Carcinogenesis No. 96
The study of antigenotoxic effects of dietary fibre is lost in a confused concept Lynnette R. Ferguson a,) , Philip J. Harris b a
Auckland Cancer Society Research Centre, Faculty of Medical and Health Sciences, The UniÕersity of Auckland, PriÕate Bag 92019, Auckland 1000, New Zealand b School of Biological Sciences, The UniÕersity of Auckland, PriÕate Bag 92019, Auckland, New Zealand
Keywords: Dietary fibre; Antigenotoxicity; Cancer
Considerable interest and debate have been generated by the publication of a large and well-conducted cohort study which failed to show that dietary fibre ŽDF. protects against cancers of the colon and rectum w1x. Explanations given include the possibilities that DF was estimated inappropriately w2x, that stool parameters rather than DF should be the relevant measure w3,4x, and that food intake was measured inappropriately w5x. An alternative explanation is that the results are indeed true ones, and that DF plays no protective role in colorectal or other cancers w6,7x. The debate has reached Mutation Research where, in this series of occasional articles, Santana-Rios and Dashwood w8x ask whether it is ‘‘time to discontinue antigenotoxicity studies of dietary fibre.’’ We disagree. Indeed, we question whether such studies have ever effectively started and we contend that it is time they did. A number of studies have now been published, purporting to examine the effects of DF in human populations. However, the results are often quite
)
Corresponding author. Tel.: q64-9-373-7599 ext. 6372; fax: q64-9-373-7502. E-mail address: [email protected] ŽL.R. Ferguson..
confusing and are becoming more so. We believe that one of the most important problems in interpreting some of the recent studies is the wide range of quite different materials, with different chemical structures and properties, that are now included in the term DF. Many definitions of DF have been proposed, but as Heaton w9x remarked in 1983, ‘‘the major source of DF by any definition is plant cell walls,’’ and ‘‘the common denominator in all concepts of DF is the plant cell wall.’’ Despite this, the range of materials now included in the term DF usually extends beyond just plant cell walls. This range includes components obtained from these walls such as pectin and cellulose preparations. It also includes non-starch polysaccharides from sources other than plant cell walls; these polysaccharides are often water-soluble and are used as food additives. It also includes polysaccharides produced by microorganisms, extracted from seaweed cell walls, and exuded from plants w10x. An associated problem is that the analytical methods for determining DF do not all quantify the same materials w11x. Thus, the DF content of a food depends on the method used to determine DF. For example, the AOAC method for determining total DF will not only include all of the materials indicated above, but will also include Mail-
0027-5107r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 7 - 5 1 0 7 Ž 9 9 . 0 0 2 2 3 - 7
320
L.R. Ferguson, P.J. Harrisr Mutation Research 447 (2000) 319–322
lard browning products and some resistant starch. With the development of ‘‘functional foods,’’ some authors wish to extend further the range of materials encompassed by DF to include resistant starch and certain oligosaccharides w12x. Furthermore, other authors take an even broader view and assume that cereal brans are DF! We believe that the fallacy is in assuming that, because a material can be included in the term DF, it must have health benefits. In fact, the available evidence suggests that these different materials have quite different effects on human health. Despite a plethora of literature purporting to show DF effects in animal or in vitro studies, the vast majority of these studies have not used whole plant cell walls. Studies purporting to show the effects of DF often use wheat bran, oat bran, or pectin preparations. However, cereal brans are simply sources of plant cell walls; in particular, oat bran often contains no more than 20% wrw plant cell walls. Although pectin preparations are extracted from plant cell walls, they are chemically modified during the extraction. Furthermore, plant cell walls should not be regarded as simple mixtures of components, and experiments done with a particular extracted component probably have little relevance to the effects of whole cell walls. We also wish to emphasise that plant cell walls themselves vary enormously in structure and composition, depending on the plant cell type and species of food plant w13x. For example, the cell walls in wheat bran are very different in composition and properties from those in cabbage. Although plant cell walls are composed mostly of polysaccharides, the structures of these vary; walls may also contain many other components, including lignin or suberin, and proteins or glycoproteins. Our plea is to describe, in as great a detail as possible, the plant material containing the cell walls. As there is now increasing amounts known about the structure and composition of the cell walls of well described food plants at specified stages of development, this information could be applied to foods consumed in population studies. In vitro studies with well-described, specific types of pant cell walls and with well-described, specific non-starch polysaccharides not only illustrated that materials included in the term DF can be antigenotoxic, but also highlighted the differences between whole plant cell walls and non-starch polysaccharide
preparations both from plant cell walls and other sources. By adsorbing mutagens, whole plant cell walls that contain the hydrophobic polymers suberin and lignin can be antimutagenic w14x. Little or no adsorption occurs to the walls of parenchyma cells that do not contain these polymers but form the bulk of fruits and vegetables. Furthermore, no adsorption occurred in the water-soluble non-starch polysaccharides we tested w15x or starch granules, and we believe it is unlikely that such adsorption would occur in oligosaccharides. These studies also emphasised that the amount of adsorption depends not only on the DF material, but also on the chemical structure of the mutagen. At this stage, we have no formal proof that this in vitro mechanism for antigenotoxicity operates in vivo. Nevertheless, we found that a specific type of whole plant cell wall that contains suberin and which was the most effective in our in vitro studies also protected rats in vivo against the development of aberrant crypts, an early index of colon cancer, induced by the carcinogen 2-amino-3-methylimidazow4,5-f xquinoline ŽIQ. w16x. We suggested that these specific cell walls may show protection against genotoxic events in vivo through carcinogen adsorption andror reduced transit time andror increased faecal bulk, all effects that would reduce the probability of the interaction of carcinogen and colonocytes. On the contrary, Maziere et al. w17x showed that resistant starch failed to protect against the initiation of aberrant crypts in rats. This was not surprising to us since resistant starch has little effect on transit time or carcinogen adsorption w18x. In addition to reducing carcinogen bioavailability, other mechanisms have been proposed whereby DF, as distinct from intracellular phytochemicals, could be antigenotoxic in vivo. These mechanisms usually involve indirect effects w10x and include modulation of xenobiotic metabolism. At present, there are only a handful of antigenotoxicity studies on whole plant cell walls. This is not surprising since they are difficult to isolate in sufficient quantities to study well. However, there is also a dearth of well-controlled antigenotoxicity studies on other materials now often included in the term DF on either spontaneous mutagenesis, or against mutagens that are present in the human diet. These studies are important, since they will tell us about the effects on tumour initiation. We
L.R. Ferguson, P.J. Harrisr Mutation Research 447 (2000) 319–322
note, for example, that certain dietary oligosaccharides have been tested on a transplantable tumour model w19x; however, this tells us nothing about their effects on critical early mutagenic events. It would be naıve ¨ to assume that all materials, now often included in the term DF, are antigenotoxic. Although the data up until now have not been entirely consistent, in general epidemiology has shown that DF protects against cancer w20x. The study by Fuchs et al. w1x is the first major study that suggests otherwise. When the term DF was first used, most of the DF in western diets was consumed in the form of whole plant cell walls in fruits, vegetables, and cereals. However, increasingly higher proportions of other materials are making up the total amount of DF consumed. Some of the first ‘‘fibre-enriched’’ foods had water-soluble, non-starch polysaccharides added to them to increase their content of DF. Currently, there is a trend to increase the content of resistant starch and oligosaccharides. It is sobering to consider the possibility that, at least some of these materials are not beneficial and are actually diluting the beneficial effects of whole plant cell walls. Indeed, the first human intervention study for a preparation rich in a specific water-soluble, non-starch polysaccharide has now been published w21x. Far from protecting against carcinogenesis, this preparation enhanced it. Nevertheless, a whole industry is developing based on materials included in foods under the DF banner. For the most part, we simply do not know whether they will be antigenotoxic, anticarcinogenic, or neither. We, therefore ,believe that there is a justification for restricting the term DF to whole plant cell walls. We believe DF should not include intracellular materials, components obtained from plant cell walls, or non-starch polysaccharides from sources other than plant cell walls. Although the latter two materials will be quantified in the AOAC method, they can be accounted for when they are added to foods. These materials should be described in terms of their chemical structure and source. In conclusion, despite an apparently large literature of antigenotoxic effects of DF, there are only very few studies in appropriate animal models that actually reflect antigenotoxic effects Žor otherwise. of whole plant cell walls, or other DF that are currently being eaten. Indeed, as we have previously
321
pointed out, some of the protection found in many of the animal studies using wheat bran could result from the effects of various protective intracellular phytochemicals and not the effects of DF w22,23x. This is also likely to be true to other cereals, fruits, and vegetables that appear protective in human or animal studies. Nevertheless, we wish to emphasise that this does not mean that DF cannot be protective. Indeed, as indicated above, we have shown that certain types of whole cell walls ŽDF. can indeed protect, at least against the formation of aberrant crypts w16x. Additionally, as Santana-Rios and Dashwood w8x rightly point out, we should be putting equal weight onto studies of intracellular phytochemicals in protective DF sources. Only with an adequate number of well-conducted studies on well described DF can we begin to sort out the true role of DF in protection against carcinogenesis. References w1x C.S. Fuchs, E.L. Giovannucci, G.A. Colditz, D.J. Hunetr, M.J. Stamfer, B. Rosner, F.E. Speizer, W.C. Willett, Dietary fibre and the risk of colorectal cancer adenoma in women, N. Engl. J. Med. 340 Ž1999. 169–176. w2x J.H. Cummings, D.A.T. Southgate, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w3x N.D. Ravin, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w4x K.W. Heaton, S.J. Lewis, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w5x Z. Madar, A. Stark, N. Engl. J. Med. 340 Ž1999. 1926, Letter to the editor. w6x J.D. Potter, Fiber and colorectal cancer — where to now? N. Engl. J. Med. 340 Ž1999. 223–224. w7x K.M. Mohandas, N. Engl. J. Med. 340 Ž1999. 1925, Letter to the editor. w8x G. Santana-Rios, R.H. Dashwood, Time to discontinue antigenotoxicity studies of dietary fiber? Mutat. Res., 429, 269–271. w9x K.W. Heaton, Dietary fibre: concepts and definition, in: Fibre in Human and Animal Nutrition, G. Wallace, L. Bell ŽEds.., R. Soc. N. Z., Bull. 20 Wellington, New Zealand, 1983, pp. 19–21. w10x P.J. Harris, L.R. Ferguson, Dietary fibre: its composition and role in protection against colorectal cancer, Mutat. Res. 290 Ž1993. 97–110. w11x P.J. Harris, L.R. Ferguson, Dietary fibres may protect or enhance carcinogenesis, Mutat. Res. 443 Ž1999. 95–110. w12x J.W. Devries, L. Prosky, B. Li, S. Cho, A historical perspective on defining dietary fibre, Cereal Foods World 44 Ž1999. 367–370. w13x A. Bacic, P.J. Harris, B.A. Stone, Structure and function of
322
w14x
w15x
w16x
w17x
w18x
L.R. Ferguson, P.J. Harrisr Mutation Research 447 (2000) 319–322 plant cell walls, in: J. Preiss ŽEd.., The Biochemistry of Plants: Carbohydrates Vol. 14 Academic Press, San Diego, 1988, pp. 297–371. P.J. Harris, C.M. Triggs, A.M. Roberton, M.E. Watson, L.R. Ferguson, The adsorption of heterocyclic aromatic amines by model dietary fibres with contrasting compositions, Chem.Biol. Interact. 100 Ž1996. 13–25. P.J. Harris, A.M. Roberton, M.E. Watson, C.M. Triggs, L.R. Ferguson, The effects of soluble-fibre polysaccharides on the adsorption of a hydrophobic carcinogen to an insoluble dietary fibre, Nutr. Cancer 19 Ž1993. 43–54. L.R. Ferguson, P.J. Harris, Suberized plant cell walls suppress formation of heterocyclic amine-induced aberrant crypts in a rat model, Chem. Biol. Interact. 114 Ž1998. 191–209. S. Maziere, K. Meflah, E. Tavan, M. Champ, J.F. Narbonne, P. Cassand, Effect of resistant starch andror fat-soluble vitamins A and E on the initiation stage of aberrant crypts in rat colon, Nutr. Cancer 31 Ž1998. 168–177. L.R. Ferguson, C. Tasman-Jones, Hans Englyst, P.J. Harris, Comparative effects of three resistant starch preparations on
w19x
w20x
w21x
w22x
w23x
transit time and short chain fatty acid production in rats, Nutr. Cancer, in press. H.S. Taper, N. Delzenne, M.B. Roberfroid, Growth inhibition of transplantable mouse tumours by non-digestible carbohydrates, Int. J. Cancer 71 Ž1997. 1109–1112. B. Trock, E. Lanza, P. Greenwald, Dietary fibre, vegetables, and colon cancer: critical review and meta-analysis of the epidemiological evidence, J. Natl. Cancer Inst. 82 Ž1990. 650–661. J. Faivre, C. Bonithon-Kopp, O. Kronberg, U. Rath, A. Giacosa, A randomised trial of calcium and fibre supplementation in the prevention of recurrence of colorectal adenomas. A European intervention study, Gasteroenterology 116 Ž1999. GO238. L.R. Ferguson, P.J. Harris, Does wheat bran or does wheat dietary fibre protect against cancer?, Int. J. Cancer 78 Ž1998. 385–386. L.R. Ferguson, P.J. Harris, Protection against cancer by wheat bran: role of dietary fibre and phytochemicals, Eur. J. Cancer Prev. 8 Ž1999. 17–25.