Previous - Next
One example where the colonic fermentation of carbohydrate may be of importance both in the recovery of dietary energy and in reducing the energy losses associated with endogenous secretions, is cystic fibrosis (CF). We have studied a series of 16 children with CF on pancreatic replacement therapy and 20 healthy control children between 6 and 20 years of age. Gross and metabolizable energy intakes were estimated from 7-day records of weighed food intake using food composition tables and either heat of combustion values (MERRILL and WATT, 1973) or the modified Atwater factors (PAUL and SOUTHGATE, 1978). The faecal energy excretion was measured over 3 days. The microbial mass within the stool was determined according to the method of STEPHEN and CUMMINGS (1980). The results are summarised in Table 4.
Table 4. Studies were carried out in 16 children with cystic fibrosis, and 20 healthy controls between the ages of 6 and 20 years. Gross and metabolizable energy intakes were estimated from 7-day records of weighed food intake, using food composition tables and either heat of combustion values or the modified Atwater factors. The faecal energy excretion was measured over 3 days, and the microbial content of the stool was determined
CYSTIC FIBROSIS |
CONTROL |
||
GROSS ENERGY INTAKE |
(kJ/d) |
8998 |
9463 |
FIBRE ENERGY |
(kJ/d) 1 |
270 |
360 |
FAECAL MASS DRY WT |
(g/d) |
48 |
17 |
FAECAL MICROBIAL MASS DRY WT |
(g/d) |
16.6 |
4.3 |
FAECAL ENERGY |
(kJ/d) |
1240 |
337 |
AVAILABLE ENERGY |
(kJ/d) |
7758 |
9126 |
FAECAL MICROBIAL ENERGY |
(kJ/d) 2 |
395 |
87 |
HEXOSE REQUIRED TO SYNTHESISE FAECAL MICROBIAL MASS |
(g/d) 3 |
55 |
18 |
TOTAL ENERGY YIELD |
(kJ/d) 4 |
959 |
309 |
ENERGY AVAILABLE AS SCFA |
(kJ/d) 5 |
564 |
220 |
Assumes heat of combustion of dietary fibre = 17.5 kJ/g.1
2 Energy content of pooled CF microbial mass = 23.8 kJ/g. Energy content of pooled control microbial mass = 20.4 kJ/g.
3 Assumes 0.1 mol ATP to synthesise 1 g of microbial mass and that 33 g hexose fermentation will generate 1 mol ATP.
4 Assumes 17.5 kJ/g hexose.
5 Total energy yield minus faecal microbial energy.
Gross energy intakes were comparable between both groups with the potential energy from dietary NSP contributing approximately 3 to 4% of the gross energy intake. However, in CF children the faecal energy losses were considerable, substantially reducing the available energy. Faecal mass was nearly 3 times greater in the CF group, with a corresponding increase in the microbial mass in the stool. The microbial mass accounted for approximately 35% and 25% of the dry mass of the stool in CF and controls respectively. This percentage is lower than that reported for adults by STEPHEN and CUMMINGS (1980) and may reflect the higher intake of non-digestible polysaccharides in their subjects.
In order to estimate the amount of energy within the microbial mass, a portion of the dried microbial mass from each sample was pooled for both CF and control subjects and the energy content was determined by bomb calorimetry. Using these values (approximately 20 to 25 kJ (4.8 to 6.0 kcal)/g dry microbial mass), the daily excretion of energy could be estimated. It is clear that both the total faecal energy and the energy within the microbial mass of the stool were substantially greater than the energy within the dietary NSP consumed by the CF subjects. This would imply that a substantial amount of substrate other than dietary NSP had been fermented. Using the same approach as McNEIL (1984), it was possible to estimate the carbohydrate fermented and the total energy yielded by that fermentation. Subtraction of the energy within the faecal microbial mass from this total energy yield provides a value for the amount of energy that may be made available through SCFA absorption. From these calculations it would appear that colonic fermentation may provide an additional 7.3% energy (range 3.0 to 12.5%) in the CF group compared to 2.4% in the control group (range 1.0 to 3.6%).
This interpretation indicates that
the colonic fermentation of carbohydrate affords the opportunity to recover, at least in
part, some of the energy from either unabsorbed starches and sugars or endogenous
secretions that would otherwise be lost in the stool in children with cystic fibrosis.
It has been recommended that the
requirements for energy be based upon determinations of energy expenditure. These
measurements will give an indication of the metabolizable energy, but will not provide any
information on the dynamic processes that result in that expenditure, nor the dietary
intake that is required to satisfy that expenditure. The evidence would suggest that we
are now in a position to ask more specific questions about the ways in which the body
utilises energy and accomodates to changes in the available energy. Our work would suggest
that the metabolic activity of the lower gastrointestinal tract plays an important role in
this accommodation. The metabolic substrate available to the body cannot be simply
measured as the dietary intake, nor even as the dietary intake minus urinary and faecal
losses. The technology and techniques are available for the more refined study of the
interaction of diet with metabolism. Exploration of these areas is likely to provide
valuable new insights in the future.
We are grateful to those colleagues
who have allowed us to quote from work that has not yet been published. The investigations
described in this paper have been made possible by support from: Cystic Fibrosis Research
Trust, The Hedley Foundation, Nestle Nutrition Research Grant Programme, The Rank Prize
Funds, The Rank Foundation, The Wellcome Trust and The Wessex Medical School Trust.
AHMED, F., JONES, D.B., JACKSON, A.A.: The interaction of vitamin A deficiency and rotavirus infection in the mouse. Br. J. Nutr., 63, 363-373 (1990a).
AHMED, F., JONES, D.B., JACKSON, A.A.: Effect of undernutrition on the immune response to rotavirus infection in mice. Ann. Nutr. Metab., 34, 21-31 (1990b).
ASHWORTH, A.: Growth rates in children recovering from protein-calorie malnutrition. Br. J. Nutr., 23, 835-845 (1969a).
ASHWORTH, A.: Metabolic rates during recovery from protein-calorie malnutrition: the need for a new concept of specific dynamic action. Nature, 223, 407-409 (1969b).
ASHWORTH, A.: Ad lib. feeding during recovery from malnutrition. Br. J. Nutr., 31, 109-112 (1974).
ASHWORTH, A.: Regulation of weight and height during recovery from severe malnutrition. In: Proc. 9th Int. Congr. Nutr. Vol. 2, pp. 280-285, A. CHAVEZ, H. BOURGES, S. BASTA (Eds.). S. Karger, Basel, Switzerland, 1975.
ATWATER, W.O., BRYANT, A.P.: The availability and fuel value of food materials. Rep. Storrs Agric. Exp. Stat., 1900, 73-110 (1899).
BEARD, J.: Feed efficiency and norepinephrine turnover in iron deficiency. Proc. Soc. Exp. Biol. Med., 184, 337-344 (1987).
BROOKE, O.G., ASHWORTH, A.: The influence of malnutrition on the postprandial metabolic rate and respiratory quotient. Br. J. Nutr., 27, 407-415 (1972).
BROOKE, O.G., WHEELER, E.F.: High energy feeding in protein-energy malnutrition. Arch. Dis. Child., 51, 968-971 (1976).
BROWN, J.C.W., MAZDAI, G., STRAIN, J.J.: The effect of copper deficiency on plasma homocysteine in the rat. Proc. Nutr. Soc., in press (1990).
CHAN, H., WATERLOW, J.C.: The protein requirement of infants at the age of about one year. Br. J. Nutr., 20, 775-782 (1966).
COOPER, E.S., BUNDY, D.A.P.: Trichuris is not trivial. Parasitology Today, 4, 301-306 (1988)
CORBETT, J.L., LENG, R.A., YOUNG, B.A.: Measurement of energy expenditure by grazing sheep and the amount of energy supplied by volatile fatty acids produced in the rumen. In: Energy Metabolism of Farm Animals, pp. 177-186, K. L. BLAXTER, J. KIELANOWSKI, G. THORBEK (Eds.). Oriel Press, Newcastle-upon-Tyne, U.K., 1969.
CUMMINGS, J.H.: Dietary fibre. Br. Med. Bull., 37, 65-70 (1981).
CUMMINGS, J.H.: Microbial digestion of complex carbohydrates in man. Proc. Nutr. Soc., 43, 35-44 (1984).
CUMMINGS, J.H., ENGLYST, H.N.: Fermentation in the human large intestine and the available substrates. Am. J. Clin. Nutr., 45, 1243-1255 (1987).
DORUP, I., CLAUSEN, T.: Effects of potassium deficiency on growth and protein synthesis in skeletal muscle and the heart of rats. Br. J. Nutr., 62, 269-284 (1989).
ELWYN, D.H., GUMP, F.E., MUNRO, H.N., ILES, M., KINNEY, J.M.: Changes in nitrogen balance of depleted patients with increasing infusions of glucose. Am. J. Clin. Nutr., 32, 1597-1611 (1979).
EMOND, A.M.: The spleen in sickle cell disease in childhood. MD Thesis, University of Cambridge, U.K., 1987.
FAO/WHO/UNU Expert Consultation: Energy and Protein Requirements. Technical Report Series 724. WHO, Geneva, 1985.
FORBES, G.B., KREIPE, R.E., LIPINSKI, B.A., HODGMAN, C.H.: Body composition changes during recovery from anorexia nervosa: comparison of two dietary regimes. Am. J. Clin. Nutr., 40, 1137-1145 (1984).
GOLDEN, M.H.N.: The consequence of protein deficiency in man and its relationship to the features of kwashiorkor. In: Nutritional Adaptation in Man, pp. 169-187, K. BLAXTER, J.C. WATERLOW (Eds.). John Libbey, London, 1985.
GOLDEN, M.H.N., GOLDEN, B.E.: Effect of zinc supplementation on the dietary intake, rate of weight gain, and energy cost of tissue deposition in children recovering from severe malnutrition. Am. J. Clin. Nutr., 34, 900-908 (1981).
GÖRANZON, H., FORSUM, E.: Metabolizable energy in humans in two diets containing different sources of dietary fiber. Calculations and analysis. J. Nutr., 117, 267-273 (1986).
GRANTHAM-McGREGOR S., POWELL, C. WALKER, S.: Nutritional supplements, stunting and child development. Lancet ii, 909-910 (1989).
HANSEN-SMITH, F.M., PICOU D., GOLDEN, M.H.N.: Growth of muscle fibres during recovery from severe malnutrition in Jamaican infants. Br. J. Nutr., 41, 275-282 (1979).
HARPER, A.E., BENEVENGA, N.J., WOHLHUETER, R.M.: Effect of ingestion of disproportionate amounts of amino acids. Physiol. Rev., 50, 428-458 (1970).
HOSKINS, L.C., BOULDING, E.T.: Mucin degradation in human colon ecosystems. J. Clin. Invest., 67, 163-172 (1982).
JACKSON, A.A.: Optimizing amino acid and protein supply and utilization in the newborn. Proc. Nutr. Soc., 48, 293-301 (1989).
JACKSON, A.A.: Protein requirements for catch-up growth. Proc. Nutr. Soc. (1990).
JACKSON, A.A., PICOU D., REEDS, P.J.: The energy cost of repleting tissue deficits during recovery from protein energy malnutrition. Am. J. Clin. Nutr., 30, 1514-1517 (1977).
JACKSON, A.A., PICOU D., LANDMAN, J.: The non-invasive measurement of urea kinetics in normal man by a constant infusion of 15N15N-urea. Hum. Nutr.: Clin. Nutr., 38C, 339-354 (1984).
KASHYAP, S., SCHULZE, K., FORSYTH, M., ZUCKER, C., DELL, R.B., RAMAKRISHNAN, R., HEIRD, W.C.: Growth, nutrient retention, and metabolic response in low birthweight infants fed varying intakes of protein and energy. J. Pediatr., 113, 713-721 (1988).
KELLER, W.: The epidemiology of stunting. In: Linear Growth Retardation in Less Developed Countries, J.C. WATERLOW (Ed.). Nestle Nutrition, Raven Press, New York, 1987.
KENNEDY, N., BADALOO, A.V., JACKSON, A.: Adaptation to a marginal intake of energy in young children. Br. J. Nutr., 63, 145-154 (1990).
KERR, D., ASHWORTH, A., PICOU D., POULTER, N., SEAKINS, A., SPADY, D., WHEELER, E.: Accelerated recovery from infant malnutrition with high calorie feeding. In: Endocrine Aspects of Malnutrition, pp. 467-486. L.I. GARDNER, I.P. AMACHER (Eds.). Kroc Foundation Symposia No. 1, Santa Ynes, CA, 1973.
KLEIBER, M.: Dietary deficiencies and energy metabolism. Nutr. Abstr. Rev., 15, 207-221 (1945).
LUNN, P.G., AUSTIN, S.: Dietary manipulation of plasma albumin concentration. J. Nutr., 113, 1791-1802 (1983).
MACLEAN, W.C., GRAHAM, G.G.: The effect of energy intake on nitrogen content of weight gained by recovering malnourished children. Am. J. Clin. Nutr., 33, 903-909 (1980).
McNEIL, N.I.: The contribution of the large intestine to energy supplies in man. Am. J. Clin. Nutr., 39, 338-342 (1984).
MERRILL, A.L., WATT, B.K.: Energy value of foods: basis and derivation. USDA Agriculture Handbook No. 74, 1973.
MILLER, D.S., PAYNE, P.R.: A theory of protein metabolism J. Theor. Biol., 5, 398-411 (1963).
MILLER, T.L., WOLLIN M.J.: Fermentation by saccharolytic intestinal bacteria. Am. J. Clin. Nutr. 32, 164-172 (1979).
NALDER, B.N., MAHONEY, A.W., RAMAKRISHNAN, R., HENDRICKS, D.G.: Sensitivity of the immunological response to the nutritional status of rats. J. Nutr., 102, 535-542 (1972).
PATRICK, J., REEDS, P.J., JACKSON, A.A., SEAKINS, A., PICOU D.I.M.: Total body water in malnutrition: the possible role of energy intake. Br. J. Nutr., 39, 417-424 (1978).
PAUL, A.A., SOUTHGATE, D.A.T.: McCance & Widdowson's The Composition of Foods. Fourth Revised Edition. MRC Special Report No. 927. HMSO, London, 1978.
PAYNE, P.R., JACOB, M.: Effect of environmental temperature on utilization of dietary protein by the growing rat. J. Nutr., 87, 221-227 (1965).
PICOU D., PHILLIPS, M.: Urea metabolism in malnourished and recovered children receiving a high or low protein diet. Am. J. Clin. Nutr., 25, 1261-1266 (1972).
PICOU D., REEDS, P.J., JACKSON, A.A., POULTER, N.: The measurement of muscle mass in children using [15-N]-creatine. Pediatr. Res., 10, 184-188 (1976).
PULLAR, J.D., WEBSTER, A.J.F.: The energy cost of fat and protein deposition in the rat. Br. J. Nutr., 37, 355-363 (1977),
REEDS, P.J., JACKSON, A.A., PICOU D., POULTER, N.: Muscle mass and composition in malnourished infants and children and changes seen after recovery. Pediatr. Res., 12, 613-618 (1978).
REEDS, P.J. LOBLEY G.E.: A comparison of skeletal muscle mass in rabbits as measured by dissection and by creatine dilution. Proc. Nutr. Soc., in press (1990).
ROEDIGER, W.E.W.: Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut, 21, 793-798 (1980).
RUBENSTEIN, R., HOWARD, A.V., WRONG, O.M.: In vivo dialysis of faeces as a method of stool analysis. IV. The organic anion component. Clin. Sci., 37, 549-564 (1969).
RUDMAN, D., MILLIKAN, W.J., RICHARSON, T.J., BIXLER, T.J., STACKHOUSE, J., McGARRITY, W.C.: Elemental balances during intravenous hyperalimentation of underweight adult subjects. J. Clin. Invest., 55, 94-104 (1975).
SOUTHGATE, D.A.T., DURNIN, J.V.G.A.: Calorie conversion factors. An experimental reassessment of the factors used in the calculation of the energy value of human diets. Br. J. Nutr., 24, 517-535 (1970).
STEPHEN, J.M.L., WATERLOW, J.C.: Effect of malnutrition on activity of two enzymes concerned with amino acid metabolism in human liver. Lancet, i, 118-119 (1968).
STEPHEN, A.M., CUMMINGS, J.H.: The microbial contribution to human faecal mass. J. Med. Microbiol., 13, 45-56 (1980).
TANNER, J.M.: Foetus into Man: Physical Growth from Conception to Maturity. Open Books, London, 1978.
TORUN, B., VITERI, F.E.: Energy requirements of pre-school children and effects of varying energy intake on protein metabolism. In: Protein Energy Requirements of Developing Countries: Evaluation of New Data, Suppl. 5, pp. 229-241, B. TORUN, V.R. YOUNG, W.M. RAND (Eds.). UNU, Tokyo, 1981.
WALKER, S.P., GOLDEN, M.H.N.: Growth in length of children recovering from malnutrition. Eur. J. Clin. Nutr., 42, 395-404 (1988).
WALSER, M., BODENLOS, L.J.: Urea metabolism in man. J. Clin. Invest., 38, 1617-1626 (1959).
WATERLOW, J.C.: The rate of recovery of malnourished infants in relation to the protein and calorie levels of the diet. J. Trop. Pediatr., 7, 16-22 (1961).
WATERLOW, J.C.: Notes on the assessment and classification of protein-energy malnutrition in children. Lancet, ii, 87-89 (1973).
WATERLOW, J.C.: Linear growth retardation in less developed countries. Nestle Nutrition, Raven Press, New York, 1987.
WATERLOW, J.C., JACKSON, A.A.: Nutrition and protein turnover in man. Br. Med. Bull., 37, 5-10 (1981).
WEBSTER, A.J.F.: Comparative aspects of energy exchange. In: Comparative Nutrition, pp. 37-54, K. BLAXTER, I. MACDONALD (Eds.). John Libbey, London, 1988.
WHITEHEAD, R.G., PAUL, A.A.: Comparative infant nutrition in man and other animals. In: Comparative Nutrition, pp. 199-213, K. BLAXTER, I. MACDONALD (Eds.). John Libbey, London, 1988.
WHYTE, R.K., BAYLEY, H.S., SINCLAIR, J.C.: Energy intake and nature of growth in low birth weight infants. Can. J. Physiol. Pharmacol., 63, 565-570 (1985).
WIDDOWSON, E.M.: Harmony of growth. Lancet, i, 901-905 (1970).
WISKER, E., MALTZ, A., FELDHEIM, W.: Metabolizable energy of diets low or high in dietary fiber from cereals when eaten by humans. J. Nutr., 118, 945-952 (1988).