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Intestinal flora during the first months of life: new perspectives

Published online by Cambridge University Press:  09 March 2007

C. A. Edwards*
Affiliation:
Department of Human Nutrition, Glasgow University, Yorkhill Hospitals, Glasgow, G3 8SJ, UK
A. M. Parrett
Affiliation:
Department of Human Nutrition, Glasgow University, Yorkhill Hospitals, Glasgow, G3 8SJ, UK
*
*Corresponding author: Dr C. Edwards, fax +44 141 201 9275, email [email protected]
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Abstract

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Increasing awareness that the human intestinal flora is a major factor in health and disease has led to different strategies to manipulate the flora to promote health. The complex microflora of the adult is difficult to change in the long term. There is greater impact of diet on the infant microflora. Manipulation of the flora particularly with probiotics has shown promising results in the prevention and treatment of diarrhoea and allergy. Before attempting to change the flora of the infant population in general, a greater understanding of the gut bacterial colonisation process is required. The critical stages of gut colonisation are after birth and during weaning. Lactic acid bacteria dominate the flora of the breast-fed infant. The formula-fed infant has a more diverse flora. The faeces of the breast-fed infant contain mainly acetic and lactic acid whereas the formula fed-infant has mainly acetic and propionic acid. Butyric acid is not a significant component in either group. The formula-fed infant also has higher faecal ammonia and other potentially harmful bacterial products. The composition of the microflora diversifies shortly before and particularly after weaning. The flora of the formula-fed infant develops more quickly than that of the breast-fed infant. Before embarking on any strategy to change the flora, the following questions should be considered: Should we retain a breast-fed style flora with limited ability to ferment complex carbohydrates? Can pro- and prebiotics achieve a flora with adult characteristics but with more lactic acid bacteria in weaned infants? Are there any health risks associated with such manipulations of the flora?

Type
Research Article
Copyright
Copyright © The Nutrition Society 2002

References

Archibald, FS (1983) Lactobacillus plantorum – an organism not requiring iron. FEMS Microbiology Letters 19, 2932.Google Scholar
Armstrong, EF, Eastwood, MA, Edwards, CA, Brydon, WG & Mac Intyre, CCA (1992) The effect of weaning diet on the subsequent colonic metabolism of dietary fibre in the adult rat. British Journal of Nutrition 68, 741751.CrossRefGoogle ScholarPubMed
Arvola, T, Laiho, K, Torkkeli, S, Mykkanene, H, Salminene, S, Maunula, L & Isolauri, E (1999) Prophylactic Lactobacillus GG reduces antibiotic associated diarrhoea in children with respiratory infections a randomised study. Pediatrics 104, e64.CrossRefGoogle Scholar
Augeron, C & Laboisse, CL (1984) Emergence of permanently differentiated cell clones of human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Research 44, 39613969.Google ScholarPubMed
Balmer, SE, Harvey, CS & Wharton, BA (1994) Diet and faecal flora in the newborn: nucleotides. Archives of Disease and Childhood 70, F137F140.CrossRefGoogle ScholarPubMed
Balmer, SE, Scott, PH & Wharton, BA (1989a) Diet and infant faecal flora: lactoferrin. Archives of Disease in Childhood 64, 16851690.CrossRefGoogle ScholarPubMed
Balmer, SE, Scott, PH & Wharton, BA (1989b) Diet and faecal flora of the newborn; casein and whey protein. Archives of Disease in Childhood 64, 16781684.CrossRefGoogle Scholar
Balmer, SE & Wharton, BA (1989) Diet and faecal flora of the new born: breast milk and infant formula. Archives of Disease in Childhood 64, 16721677.Google Scholar
Balmer, SE & Wharton, BA (1991) Diet and faecal flora in the newborn: iron. Archives of Disease in Childhood 66, 13901394.Google Scholar
Berggren, AM, Margareta, E, Nyman, GL, Ludquist, I & Bjorck, IME (1996) Influence of orally and rectally administered propionate on cholesterol and glucose metabolism in obese rats. British Journal of Nutrition 76, 287294.CrossRefGoogle ScholarPubMed
Bjorksten, B, Naaber, P, Sepp, E & Mikelsaar, M (1999) The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clinical and Experimental Allergy 29, 342346.CrossRefGoogle ScholarPubMed
Borenfreud, E, Schmid, E, Bendich, A & Franke, WS (1980) Constitutive aggregates of intermediate-sized filaments of the vimentin and cytokeratin type in cultured hepatoma cells and their dispersal by butyrate. Experimental Cell Research 127, 215235.Google Scholar
Bullen, CL, Tearle, PV & Stewart, MG (1977) The effects of humanised milks and supplemented breast milk on the faecal flora of infants. Journal of Medical Microbiology 10, 403413.Google Scholar
Bullen, CL & Willis, AT (1971) Resistance of the breast-fed infant to gastroenteritis. British Medical Journal 3, 338343.CrossRefGoogle ScholarPubMed
Bullen, JJ, Rodgers, HJ & Leigh, L (1972) Iron binding proteins in milk and resistance to E coli infections in infants. British Medical Journal 1, 6975.Google Scholar
Calvo, EB, Galindo, AC & Aspres, NB (1992) Iron status in exclusively breast-fed infants. Pediatrics 90, 375379.Google Scholar
Campieri, M & Gionchetti, P (2001) Bacteria as the cause of ulcerative colitis. Gut 48, 132135.CrossRefGoogle ScholarPubMed
Candido, EP, Reeves, R & Davie, JR (1978) Sodium butyrate inhibits histone deacetylase in cells. Cell 14, 105113.Google Scholar
Christian, MT, Edwards, CA & Weaver, LT (1999) Starch digestion in infancy. Journal of Pediatric Gastroenterology and Nutrition 29, 116124.Google Scholar
Christian, MT, Edwards, CA, Preston, T, Johnson, LA, Varley, R & Weaver, LT (2000) Patterns of colonic starch fermentation from infancy to adulthood. Proceedings of the Nutrition Society 59, 36A.Google Scholar
Edwards, CA, Hepburn, IC, Segal, I, Hassan, H, Vorster, E, Oosthuizen, W & Kruger, S (1998) Colonic fermentation capacity in young children from South African populations of low and high cancer risk. In Functional Properties of Non-digestible Carbohydrates, pp. 222224 [Guillon, F and Amado, R, editors]. Brussels: EU Commission DGX11.Google Scholar
Edwards, CA, Parrett, AM, Balmer, SE & Wharton, BA (1994) Faecal short chain fatty acids in breast-fed and formula-fed babies. Acta Paediatrica Scandinavica 83, 459462.CrossRefGoogle ScholarPubMed
Fay, JP & Faries, RN (1975) The inhibitory action of fatty acids on the growth of E coli. Journal of General Microbiology 91, 233240.CrossRefGoogle Scholar
Fuller, R (1991) Factors affecting the composition of the intestinal microflora of the human infant. In Nutritional Needs of the 6–12. Month Infant, pp. 121130 [Heird, WC, editor]. New York: Raven Press.Google Scholar
Gil, A, Corral, E, Maritnez, A & Molina, JA (1986) Effects of nucelotides on the microbial pattern of faeces of at term newborn infants. Journal of Clinical Nutrition and Gastroenterology 1, 3438.Google Scholar
Gillard, BK, Simbala, JA & Goodglick, L (1989) Reference intervals for isoenzymes in serum and plasma of infants and children. Clinical Chemistry 29, 11191123.Google Scholar
Gronlund, MM, Salimen, S, Mykkanen, H, Kero, P & Lahtonen, OP (1999) Development of intestinal bacterial enzymes in infants: relationship to mode of delivery and feeding. Acta Pathology Microbial Immunology Scandinavica 107, 655660.Google Scholar
Hague, A & Paraskeva, C (1995) The short-chain fatty acid butyrate induces apoptosis in colorectal tumour cell lines. European Journal of Cancer Prevention 4, 359364.CrossRefGoogle ScholarPubMed
Hamaker, BR, Rivera, K, Morales, E & Graham, GG (1991) Effects of dietary fiber and starch on faecal composition in preschool children consuming maize amaranth or cassava flours. Journal of Pediatric Gastroenterology and Nutrition 13, 5966.Google Scholar
Harmsen, HJM, Wibleboer-Veloo, ACM, Raangs, GC, Wagendorp, AA, Klijn, N, Bindels, JG & Wellings, GW (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants using molecular identification and detection methods. Journal of Pediatric Gastroenterology and Nutrition 30, 6167.Google Scholar
Heavey, PM, McBain, AJ, Rumney, CJ, Rowland, IR, Savage, SAH & Edwards, CA (2000) Metabolic properties of faecal samples from breast fed and formula fed babies. Proceedings of the Nutrition Society 59, 62A.Google Scholar
Howie, PW, Forsyth, JS, Ogston, SA, Clark, A & Florey, CD (1990) Protective effect of breast-feeding against infection. British Medical Journal 300, 1116.CrossRefGoogle ScholarPubMed
Isolauri, E (2001) Probiotics in the prevention and treatment of allergic disease. Pediatric Allergy and Immunology 12, Suppl. 14, 5659.Google Scholar
Jonsson, G, Midtvedt, AC, Norman, A & Midtvedt, T (1995) Intestinal microbial bile acid transformation in healthy children. Journal of Pediatric Gastroenterology and Nutrition 20, 394402.Google Scholar
Kalliomaki, M, Kirjavainen, P, Eerola, E, Kero, P, Salminen, S & Isolauri, E (2001) Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. Journal of Allergy and Clinical Immunology 107, 129134.Google Scholar
Kien, CL, Kepner, J, Grotjohn, K, Ault, K & McClean, RE (1992) Stable isotope method for estimating colonic acetate production in premature infants. Gastroenterology 102, 14581466.Google Scholar
Kunz, C & Rudolff, S (1993) Biological functions of oligosaccharides in human milk. Acta Paediatrica Scandinavica 82, 902912.CrossRefGoogle ScholarPubMed
Lebenthal, E & Lee, DC (1980) Development of functional response in human exocrine pancreas. Pediatrics 66, 556560.Google Scholar
Livesey, G (1990) Energy values of unavailable carbohydrates and diets. American Journal of Clinical Nutrition 51, 617637.Google Scholar
Lundequist, B, Nord, CE & Windberg, J (1985) The composition of the microflora in breast fed and bottle fed infants from birth to eight weeks. Acta Paediatrica Scandinavica 74, 4551.Google Scholar
McNeish, AS, Mayne, A, Ducker, DA & Hughes, CA (1983) Development of D-glucose absorption in the perinatal period. Journal of Pediatric Gastroenterology and Nutrition 2, S222S226.Google Scholar
Martin, F, Savage, SAH, Parrett, AM, Gramet, G, Dore, J & Edwards, CA (2000) Investigation of bacterial colonisation of the colon in breast-fed infants using novel techniques. Proceedings of the Nutrition Society 59, 64A.Google Scholar
Midtvedt, AC, Carlstedt-Duke, B & Midtvedt, T (1994) The establishment of mucin degrading microflora during the first two years of life. Journal of Pediatric Gastroenterology and Nutrition 18, 321326.Google Scholar
Midtvedt, AC, Carlstedt-Duke, B, Norin, KE, Saxerholt, H & Midtvedt, T (1988) Development of five metabolic activities associated with the intestinal microflora of healthy infants. Journal of Pediatric Gastroenterology and Nutrition 7, 559567.Google Scholar
Midtvedt, AC & Midtvedt, T (1992) Production of short chain fatty acids by the intestinal microflora during the first two years of human life. Journal of Pediatric Gastroenterology and Nutrition 18, 321326.Google Scholar
Midtvedt, AC & Midtvedt, T (1993) Conversion of cholesterol to coprostanol by the intestinal microflora during the first two years of human life. Journal of Pediatric Gastroenterology and Nutrition 17, 161168.Google ScholarPubMed
Moore, WEC, Cato, EP & Holdeman, LV (1978) Some current concepts in intestinal bacteriology. American Journal of Clinical Nutrition 31, 533542.Google Scholar
Norin, KE, Gustafsson, BE, Lindblad, BS & Midtvedt, T (1985) The establishment of some microflora associated biochemical characteristics in faeces from children during the first years of life. Acta Paediatrica Scandinavica 74, 207212.CrossRefGoogle ScholarPubMed
Onoue, M, Kado, S, Sakaitani, Y, Uchida, K & Morotomi, M (1997) Specific species of intestinal bacteria influence the induction of abeherrant crypt foci by 1,2 dimethylhydrazine in rats. Cancer Letters 113, 179186.Google Scholar
Ouwehand, AC, Isolauri, E, He, F, Hashimoto, H, Benno, Y & Salminen, S (2001) Differences in Bifidobacterium flora composition in allergic healthy infants. Journal of Allergy and Clinical Immunology 108, 144145.Google Scholar
Parrett, AM (2001) Development of colonic fermentation in early life. PhD Thesis, Glasgow University.Google Scholar
Parrett, AM & Edwards, CA (1997a) In vitro fermentation of carbohydrate by breast-fed and formula fed infants. Archives of Disease in Childhood 76, 249253.CrossRefGoogle ScholarPubMed
Parrett, AM & Edwards, CA (1997b) The effect of weaning on fermentation capacity in formula fed infants. Proceedings of the Nutrition Society 56, 309A.Google Scholar
Parrett, AM, Farley, K, Fletcher, A & Edwards, CA (2001) Comparison of faecal short chain fatty acids in breast-fed, formula-fed and mixed fed neonates. Proceedings of the Nutrition Society 60, 48A.Google Scholar
Parrett, AM, Khanna, S & Edwards, CA (2000) Excretion of faecal starch and fat in breast fed and formula fed infants during weaning. Proceedings of the Nutrition Society 59, 64A.Google Scholar
Parrett, AM, Lokerse, E & Edwards, CA (1997) Colonic fermentation in vitro: development during weaning in breast fed infants is slower for complex carbohydrates than for sugars. American Journal of Clinical Nutrition 65, 927933.Google Scholar
Pathmakanthan, S, Meance, S & Edwards, CA (2000) Probiotics: a review of human studies to date and methodological approaches. Microbial Ecology in Health and Disease 12, Suppl. 2, 1030.Google Scholar
Roberts, AK, Chierrici, R, Sawatzki, G, Hill, MJ, Volpato, S & Vigi, V (1992) Supplementation of an adapted formula with bovine lactoferrin 1. Effect on the infant faecal flora. Acta Paediatrica Scandinavica 81, 119124.Google Scholar
Roediger, WEW (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424429.CrossRefGoogle ScholarPubMed
Rossiter, MA, Barrownman, JA, Dand, A & Wharton, BA (1974) Amylase content of mixed saliva in children. Acta Paediatrica Scandinavica 63, 389392.Google Scholar
Rueda, R, Sabatel, JL, Maldonado, J, Moilna-Font, JA & Gil, A (1998) Addition of gangliosides to an adapted milk formula modifies levels of faecal microflora in preterm newborn infants. Journal of Pediatrics 133, 9094.Google Scholar
Ruppin, H, Bar-meir, S, Soergel, KH, Wood, CM & Schmitt, MG (1980) Absorption of SCFA by the colon. Gastroenterology 78, 15001507.Google Scholar
Saavadra, JM, Bauman, NA, Oung, I, Pernan, JA & Yolken, RH (1994) Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus. Lancet 344, 10461049.CrossRefGoogle Scholar
Sghir, A, Gramet, G, Suau, A, Rochet, V, Pochart, P & Dore, J (2000) Quantification of bacterial groups within human faecal flora by oligonucleotide probe hybridisation. Applied and Environmental Microbiology 66, 22632266.CrossRefGoogle Scholar
Siimes, MA, Vuori, E & Kuitenen, P (1979) Breast milk iron: a decline in concentration during the course of lactation. Acta Paediatrica Scandinavica 68, 2931.CrossRefGoogle Scholar
Simhon, A, Douglas, JR, Drasar, BS & Soothill, JH (1982) Effect of feeding on infants' faecal flora. Archives of Disease in Childhood 57, 5458.Google ScholarPubMed
Szylit, O & Andrieux, C (1993) Physiological and pathophysiological effects of carbohydrate fermentation. World Review of Nutrition and Diet 74, 88122.CrossRefGoogle ScholarPubMed
Tannock, GW (2000) Molecular assessment of the intestinal microflora. American Journal of Clinical Nutrition 73, s401s414.Google Scholar
Tannock, GW, Fuller, R, Smith, SL & Hall, MA (1990) Plasmid profiling of members of the family enterobacteriaceae, lactobacilli and bifidobacteria to study the transmission of bacteria from mother to infant. Journal of Clinical Microbiology 28, 12251228.Google Scholar
Vaughan, EE, Schhut, F, Heilig, HGHJ, Zoetendal, EG, de Vos, WM & Akkermans, ADL (2000) A molecular view of the intestinal ecosystem. Current Issues in Intestinal Microbiology 1, 112.Google Scholar
Venter, CS, Vorster, HH & Cummings, JH (1990) Effects of dietary propionate on carbohydrate and lipid metabolism in human volunteers. American Journal of Gastroenterology 85, 549553.Google Scholar
Verity, K & Edwards, CA (1994) Resistant starch in young children. Proceedings of the Nutrition Society 53, 105A.Google Scholar
White, A, Freeth, S & O'Brien, M (1992) Office of Population Census and Surveys Infant Feeding Study 1990. London: HM Stationery Office.Google Scholar
Wold, AE (1998) The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora? Allergy 53, Suppl. 46, 2025.CrossRefGoogle ScholarPubMed
Wolever, TMS, Fernandes, J & Venketeshwer Rao, A (1996) Serum acetate:propionate ratio is related to serum cholesterol in men but not women. Journal of Nutrition 126, 27902797.Google Scholar
Wolever, TMS, Spadafora, P & Eshius, H (1991) Interaction between colonic acetate and propionate in humans. American Journal of Clinical Nutrition 53, 681687.Google Scholar
Yokoyama, MT, Tabori, C, Miller, ER & Hogberg, GS (1982) The effects of antibiotics in weaning pigs measuring growth and excretions of volatile phenolic and aromatic metabolites. American Journal of Clinical Nutrition 35, 14171422.Google Scholar
Younoszai, MK (1974) Jejunal absorption of hexose in infants and adults. Journal of Pediatrics 85, 446448.Google Scholar
Zetterstrom, R, Bennet, R & Nord, KE (1994) Early infant feeding and microecology of the gut. Acta Pediatrica Japonica 36, 562571.Google Scholar
Zoppi, G, Andreotti, P, Pajna-Ferrarra, F, Njai, DM & Gaburro, D (1972) Exocrine pancreas function in premature and full term neonates. Pediatric Research 6, 880886.Google Scholar