![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
*
Division of Nutritional Sciences and Department of Animal Sciences, University of Illinois, Urbana, IL 61801 and
Carle Foundation Hospital, Urbana, IL 61801
1To whom correspondence should be addressed. E-mail: g-fahey{at}uiuc.edu.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
KEY WORDS: • fructooligosaccharides • fermentation • intestinal microbiota • short-chain fatty acids • infants
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
–4
). Therefore, various methods to alter these bacteria and their resultant SCFA are being studied increasingly, including prebiotics (3
). Fructans are the most widely recognized prebiotics and have been shown to alter the intestinal microflora of human adults and elderly people (3
,5
,6
).
Although prebiotics have been broadly investigated in adults and the elderly, relatively little work has been done to elucidate the effects of dietary components on the colonic microflora of infants. Previous studies indicate that breast-fed infants have a higher proportion of fecal bifidobacteria and a lower proportion of fecal pathogenic bacteria compared with proportions found in the feces of formula-fed infants (7
,8
). Additionally, it has been shown that the infant’s microflora and fermentative end products change to an adult profile after weaning from breast milk (7
,9
). This difference in microbial populations has been attributed to unique components that are found only in breast milk (10
). However, it is not known whether prebiotic supplementation can have bifidogenic effects similar to those of breast milk. Because few data are available on the effects of dietary components on the microbial populations in the infant colon, the objectives of this study were as follows: 1) to compare the fermentation of naturally occurring fructans by fecal bacteria naive to fructans, isolated from breast-fed and formula-fed infants at different stages corresponding to the introduction of cereals and then fruits and vegetables into their diets; and 2) to characterize the colonic bacterial populations of breast-fed and formula-fed infants at these key stages in their development.
|
SUBJECTS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
This study was approved by the University of Illinois Institutional Review Board and the Carle Foundation Hospital Institutional Review Board. Families of 1- to 2-mo-old infants born at Carle Foundation Hospital, Urbana, IL were recruited by mail, and parents were required to sign an informed consent form for their infant’s participation in the study. Inclusion criteria specified that the infants were full-term gestational age at birth, had not received antibiotics for at least 4 wk before stool collection, and were consuming either breast milk or a dairy-based infant formula exclusively (not a combination of the two). Infants were excluded from the study if they consumed cereal before 14 wk of age, consumed fruits or vegetables before 22 wk of age, or consumed meat before 30 wk of age. These dietary restrictions are in accordance with USDA Food and Nutrition Service guidelines (11
). In addition to following these guidelines and notifying research staff before introducing new foods, parents were required to avoid feeding their infants bananas and probiotic products throughout the study (up to 30 wk of age) because bananas are relatively rich in fructans (6 mg/g, dry matter) and probiotics have been shown to alter colonic bacterial populations (12
–14
). Subjects had no history of chronic illness and were generally healthy. Infants were between the 5th and 95th percentiles for physical growth as determined by the National Center for Health Statistics (15
) and had a rate of growth within normal growth channels. Minor illnesses did not preclude subject participation. After informed parental consent, nine infants (five breast-fed and four formula-fed) were selected for participation.
Sample collection and handling.
Freshly voided stools were collected from each of the five breast-fed and four formula-fed subjects at 3, 5 and 7 mo of age. These ages corresponded to the introduction of specific categories of solid foods into the diet. For the 3-mo measurement, infants consumed formula or breast milk only. For the 5-mo measurement, infants consumed formula or breast milk, and rice cereal to provide between 10 and 25% of total energy requirements. For the 7-mo measurement, infants consumed formula or breast milk, plus rice cereal and pureed fruits and vegetables to provide between 45 and 60% of total energy needs from solid foods. Parents completed a food diary for 2 d before each stool collection. Food Processor software (ESHA Research, Salem, OR) was used to calculate nutrient compositions of recorded infant diets (excluding formula and breast milk portions of the diet) as well as infant nutrient and energy requirements.
On designated collection days, parents collected a stool sample within 15 min of defecation and immediately contacted the investigator by phone for retrieval. Parents sealed stool samples to be used for in vitro fermentation studies in plastic bags with excess air expressed and placed them immediately into thermos bottles containing warm (
40°C) water. Stool samples for bacterial enumeration analyses were placed into preweighed Carey-Blair transport media containers (Meridian Diagnostics, Cincinnati, OH) and kept at ambient temperature.
Microbial enumeration.
Stool samples were serially diluted with diluent (16
) under anaerobic conditions within 4 h of collection. Total anaerobes and aerobes were enumerated using a 40% rumen fluid agar according to Bryant and Robinson (17
) and Mackie et al. (18
). Bifidobacteria were enumerated using a selective agar according to Muñoa and Pares (19
). Lactobacilli were cultured on Rogosa selective Lactobacillus agar (Difco, Detroit, MI) according to manufacturer’s directions. Clostridium perfringens was enumerated on a tryptose-sulfite-cycloserine agar with egg yolk (20
). Escherichia coli was enumerated using eosin methylene blue agar (Difco). Inoculating drops of three appropriate dilutions onto their respective plates maximized counting precision of the microbiota. After adsorption of the droplets, the plates were inverted and incubated either anaerobically or aerobically at 38°C for 48 h. Colonies were counted after 24–48 h incubation to determine colony-forming units (cfu)/g of feces. A cfu was defined as a distinct colony measuring at least 1 mm in diameter; cfu/g wet stool were calculated as follows:
 |
Fermentation procedures.
Substrates used in this study were pureed baby food vegetables manufactured by Beech-Nut (St. Louis, MO). The vegetables were white carrot, white salsify, gobo and sweet potato. Gobo and white salsify are root vegetables that contain high concentrations of naturally occurring fructans (12.4 and 18.3 g/100 g dry matter, respectively). Gobo puree was added to sweet potato puree at 20.8 g/100 g; salsify puree was added at 28.6 g/100 g; and white carrot puree was added at 27.7 g/100 g (as-is basis). The white salsify mixture and the gobo mixtures each contained 0.035 g FOS/g puree (dry matter basis). The carrot mixture contained <0.001 g FOS/g puree. The calculated total carbohydrate composition of these substrates ranged from 11.5 (gobo) to 17.5 g/100 g (salsify) dry matter (Ralston Analytical Laboratories, St. Louis, MO). Lyophilized substrates (300 mg) were weighed in duplicate into 50-mL (28 x 100 mm) polypropylene tubes. Blank tubes containing no substrate were fermented with each inoculum source to allow correction for SCFA production not arising from the substrates.
Substrates were fermented in vitro for 3, 6 and 12 h with fecal microflora obtained from each of three infants fed each possible diet combination (e.g., breast-fed only; breast-fed + rice cereal; formula-fed only; formula-fed + rice cereal). The in vitro experimental design was a randomized complete block, with fecal donor groups serving as blocks. Treatment design was a 3 x 3 factorial arrangement with three substrates and three fermentation periods (3, 6 and 12 h). Each block by treatment combination was assayed using duplicate fermentation tubes.
The composition of the semidefined medium used for the fermentation is presented in Table 1
. All components except for the vitamin solutions were mixed before autoclave sterilization. Filter-sterilized vitamin solutions were added immediately before dispensing the medium, which was maintained under anaerobic conditions after preparation. Aliquots (26 mL) of medium were aseptically transferred into fermentation tubes under a stream of CO2. To maintain anaerobic conditions, tubes were sealed with rubber stoppers equipped with one-way gas release valves. All tubes were stored at 4°C for 12 h to allow substrates to hydrate before initiating fermentations. Tubes were placed in a 37°C water bath at least 30 min before inoculation. Fecal samples were diluted 1:10 (wt/vol) in anaerobic dilution solution by blending for 15 s in a Waring blender under a stream of CO2. Blended, diluted feces were filtered through four layers of cheesecloth and sealed in serum bottles under CO2.
|
Chemical analyses.
Substrate dry matter and organic matter were determined as described by the AOAC (21
). Samples to be analyzed for SCFA (2 mL) were mixed with 0.5 mL m-phosphoric acid (250 g/L), precipitated at ambient temperature for 30 min and centrifuged at 25,000 x g for 20 min. The supernatant was aspirated and frozen in microfuge tubes at -20°C overnight. After freezing, the supernatant was thawed and centrifuged at 13,000 x g for 10 min. Concentrations of SCFA were determined via gas chromatography. Briefly, supernatant concentrations of acetate, propionate and butyrate were determined using a Hewlett-Packard 5890A Series II gas chromatograph (Agilent, Wilmington, DE) and a glass column (180 cm x 4 mm i.d.) packed with 10% SP-1200/1% H3PO4 on 80/100 mesh Chromosorb WAW (Supelco, Bellefonte, PA). Nitrogen was the carrier gas and a flow rate of 75 mL/min was used. Oven, detector and injector temperatures were 125, 175 and 180°C, respectively. Blank tube SCFA concentrations were used to correct for nonsubstrate SCFA production.
Statistical analyses.
In vitro and bacterial data were analyzed separately. In vitro fermentation data were analyzed as a randomized complete block with infant donors serving as blocks. The factorial treatments included substrate and fermentation period. The statistical model included substrate, diet, fermentation time, substrate x time, substrate x diet, diet x time, and substrate x time x diet. All analyses were performed according to the general linear models (GLM) procedure of SAS (22
). Least-squares means are reported along with the pooled SEM for all treatments within a given time point. When overall treatment differences were detected (P < 0.05), individual means were compared by the least significant difference method (23
). Overall effects of diet, substrate and time were analyzed using nonorthogonal contrasts (24
).
Bacterial data were analyzed as a completely randomized design. Treatment means are reported along with the SEM. Analyses were performed on treatment differences within each infant according to the GLM procedure of SAS (22
). Effects of diet and substrate were analyzed using nonorthogonal contrasts (23
). Due to small sample size and data variability, differences of P < 0.10 were considered significant.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Breast-fed and formula-fed infants consumed similar amounts of rice cereal (15.4 and 18.2% of total energy needs, respectively; data not shown, P > 0.20). When pureed fruits and vegetables were included in the diet, breast-fed and formula-fed infants continued to consume similar amounts of energy from solid foods (56.2 and 59.7% of total energy needs, respectively). These quantities were well within the targeted ranges (10–25% of total energy needs from rice cereal, and 45–60% of total energy needs from cereal, fruits and vegetables).
Nutrient composition of ingested solid foods also did not differ between breast-fed and formula-fed infants (P > 0.20). When only rice cereal was fed, the percentage of energy contributed by solid food carbohydrates was 93.3% for breast-fed infants and 93.1% for formula-fed infants. Similarly, protein contributed 6.7 and 6.8% of total energy, and fat contributed 0.1 and 0.8% of total energy for breast-fed and formula-fed infants, respectively. When fruits and vegetables were included in the diet, carbohydrate consumption was 88.7 and 90.2% of total energy requirements; protein consumption was 6.2 and 4.9% of total energy requirements, and fat consumption was 5.0 and 4.9% of total energy requirements for breast-fed and formula-fed infants, respectively. However, fiber consumption differed (P < 0.10) between the two groups of infants. Although both groups consumed negligible amounts of dietary fiber when eating only rice cereal, breast-fed infants consumed an average of 6.4 g/d and formula-fed infants consumed an average of 3.0 g/d when fruits and vegetables were included in the diet.
Substrate chemical composition.
The absolute dry matter content of substrates (before lyophilization) ranged from 12.1 (carrot) to 15.0 g/100 g (gobo). After lyophilization, dry matter content of substrates varied from 88.7 (salsify) to 91.3 g/100 g (carrot). Organic matter content ranged from 92.8 (carrot) to 95.0 g/100 g (gobo and salsify). Because both fructan-containing substrates exhibited somewhat higher organic matter concentrations than carrot, SCFA data are expressed per gram of organic matter.
SCFA production.
In general, SCFA production increased with fermentation time (P < 0.05) (Tables 2
3
4)
. As expected, acetate was the major SCFA present in fermentations using inoculum from solely breast-fed or formula-fed infants (P < 0.05) (Table 2
). Although individual treatments did not differ (P > 0.10) in quantity of SCFA produced when inoculum from solely breast-fed or solely formula-fed infants was used, inoculum from solely breast-fed infants produced greater (P < 0.05) molar proportions of acetate compared with the inoculum of solely formula-fed infants. However, propionate and butyrate molar percentages were greater (P < 0.05) in the inoculum of solely formula-fed infants. In both formula-fed and breast-fed infants, the type of substrate (i.e., fructan vs. carrot) did not affect (P > 0.10) molar percentages of acetate, propionate and butyrate that were produced by fermentation.
|
|
|
). Similar to solely breast-fed or formula-fed infants, inoculum of breast-fed infants produced higher proportions of acetate (P < 0.05) and lower proportions of propionate and butyrate (P < 0.05) compared with proportions produced by that of formula-fed infants. Fructan-containing substrates did not significantly affect proportions of individual SCFA produced compared with the carrot control.
The SCFA molar percentages produced by inoculum from infants fed fruit and vegetable purees (Table 4
) followed a trend similar to that observed in inoculum from solely breast-fed or formula fed or cereal-fed infants. The percentage of acetate produced decreased (P < 0.05) with fermentation time, whereas propionate and butyrate production increased (P < 0.05). Again, the fructan content of substrate fermented did not affect the molar percentages of individual SCFA that were produced in each infant group. However, at this age, there was no effect of breast-feeding vs. formula feeding on in vitro SCFA production.
When data were combined across solid food regimens (all liquid, rice cereal, fruits and vegetables), inoculum from infants who were breast-fed produced more acetate and less propionate than inoculum from formula-fed infants (P < 0.05). The addition of cereal to the diet of infants was associated with increased acetate and total SCFA production (P < 0.05). The addition of fruit and vegetable purees was associated with greater acetate, propionate, butyrate and total SCFA production in the inoculum of breast-fed infants compared with the solely liquid diets (P < 0.05). In general, fructan-containing vegetable substrates did not affect SCFA production by inoculum in any of the infant groups (P > 0.10).
Stool bacterial concentrations.
Stool bacterial concentrations (log10 cfu/g feces, as-is basis) were somewhat altered by diet (Table 5
). Diet did not affect total anaerobe or lactobacilli concentrations (P > 0.10). However, the addition of fruits and vegetables to the diets of breast-fed or formula-fed infants decreased total aerobe concentrations (P < 0.05). Dietary addition of rice cereal increased bifidobacteria concentrations in both breast-fed and formula-fed infants (P < 0.10). Concentrations of C. perfringens were higher in the feces of solely breast-fed infants compared with solely formula-fed infants regardless of solid food intake (P < 0.10). Furthermore, infants fed rice cereal had lower concentrations of C. perfringens than infants fed a totally liquid diet (P < 0.05). However, this reduction was negated by the addition of fruits and vegetables to the diets of either breast-fed or formula-fed infants because they exhibited increased (P < 0.05) concentrations of C. perfringens compared with cereal-fed infants. Stool E. coli concentrations were decreased when fruits and vegetables were included in the diet, regardless of breast milk or formula intake, compared with solely liquid-fed infants (P < 0.10).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
) who reported that in vitro fermentation of lactose with fecal inoculum from exclusively formula-fed infants produced propionate at a faster (P < 0.05) rate and to a greater (P < 0.05) extent compared with inoculum from exclusively breast-fed infants. Acetate production rate and quantity did not differ due to inoculum source, in contrast to the increased acetate production by breast-fed infants determined in our study.
In our study, the introduction of solid foods into the diets of infants was associated with increased SCFA production, regardless of breast- or formula-feeding regimen. Parrett et al. (26
) reported similar results. In vitro fermentation of simple sugars (glucose and lactose) by inoculum from exclusively breast-fed infants occurred to a greater extent than did fermentation of complex carbohydrates (FOS, soybean polysaccharide and guar gum). Furthermore, fecal bacteria from breast-fed infants did not develop the ability to produce SCFA from these complex carbohydrates until infants were of late weaning age (defined as 16 wk after first ingestion of solid foods).
It is not likely that any differences in the nutrient composition of the self-selected diets significantly influenced our measurements. Although breast-fed infants consumed more fiber than formula-fed infants when fruits and vegetables were added to the diet, this likely influenced only total anaerobic bacterial counts, and is unlikely to account for any differences in individual bacterial populations (27
–29
). Furthermore, although fiber consumption influences in vivo SCFA production (30
), in vitro SCFA production in the present study was corrected for fecal inoculum SCFA using appropriate blanks.
The fructooligosaccharide content of vegetable substrates did not influence the pattern of SCFA produced in the current study. In another study, pure FOS produced numerically greater quantities of butyrate than did glucose, lactose or soybean polysaccharide substrates in in vitro fermentations using inoculum from breast-fed infants in early and late weaning stages, but these differences were not significant (26
). In contrast, acetate and propionate production from fermentation of pure FOS was similar to the production of these SCFA from the other carbohydrate substrates (26
). The lack of an effect of FOS on SCFA production in the current study may be attributed to relatively low concentrations of FOS in the substrates that were used (0.035 g FOS/g substrate, dry matter basis).
Total SCFA production and profiles have implications for colonic health. SCFA are the preferred energy source for colonic epithelial cells and have been shown to stimulate normal colonocyte proliferation (31
,32
). Propionate and butyrate have been shown to inhibit the growth of colon cancer cell lines (32
). Furthermore, SCFA have been suggested to enhance small intestinal glucose uptake (33
).
The data in this study showed that breast-fed and formula fed infants had similar fecal concentrations of bifidobacteria, lactobacilli and E. coli. Balmer and Wharton (34
) reported that a higher percentage of breast-fed infants harbored a bifidobacteria-dominated flora compared with formula-fed infants at ages 4 d (30 vs. 15%), 14 d (50 vs. 0%) and 28 d (39 vs. 10%). It is possible that the similarity in fecal bifidobacteria concentrations between breast-fed and formula-fed infants was due to taking measurements at an older age (3 mo) than did Balmer and Wharton (28 d) (34
). However, their data agree with the present study in that the predominance of lactobacilli, clostridia, and E. coli did not differ between breast- and formula-fed infants. Further supporting the results of the current study, Yoshioka et al. (35
) reported that at 28 d of age, breast-fed infants had greater fecal concentrations of bifidobacteria compared with concentrations in formula-fed infants (11.3 vs. 10.8 log10 cfu/g). Similar results were obtained for fecal lactobacilli concentrations (8.7 vs. 6.4 log10 cfu/g) of breast-fed and formula-fed infants, respectively. However, statistical analyses were not performed on these data, making it difficult to critically evaluate the numerical differences.
Similar to the present study, Stark and Lee (36
) determined that fecal bifidobacteria concentrations in solely breast-fed and formula-fed infants did not differ (10.6 and 10.3 log10 cfu/g). However, they reported a decrease in bifidobacteria concentration with the introduction of solid foods (10.2 and 9.8 log10 cfu/g for breast-fed and formula-fed infants, respectively), whereas we found an increase in bifidobacteria concentrations with the addition of cereal to the diet.
Irrespective of rice cereal or fruit and vegetable consumption, breast-fed infants in the current study tended to harbor higher concentrations of C. perfringens compared with formula-fed infants. These data agree with Benno and co-workers (37
) who reported that breast-fed infants (ages 28 to 46 d) had a more frequent (P < 0.01) occurrence of C. perfringens (18/35 individuals) and a greater (P < 0.001) fecal count (8.16 log10 cfu/g) than formula-fed infants within the same age range (occurrence, 5/35 individuals; count, 5.34 log10 cfu/g).
In the present study, E. coli concentrations were lower (P < 0.10) in the stools of infants consuming fruits and vegetables compared with solely breast-fed infants. This difference did not occur in infants fed solid foods. These results differ from those presented by Stark and Lee (36
) who reported that although the introduction of solid foods greatly disturbed the fecal flora of breast-fed infants, the flora of formula-fed infants was relatively stable.
The results of the current study show that diet influences the quantity and profile of SCFA produced in vitro by bacteria obtained from the feces of healthy infants. Furthermore, microbial populations are influenced by breast-feeding vs. formula-feeding and by the introduction of solid foods into the infant’s diet. In turn, it is likely that differences in SCFA production may be attributed at least in part to differences in the bacterial types present in the inoculum. An understanding of the effect of diet on intestinal bacterial populations and on the quantity and proportions of SCFA produced during fermentation will assist in formulation of infant foods that may optimize intestinal health and well-being.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
Manuscript received 27 July 2001. Initial review completed 5 October 2001. Revision accepted 13 May 2002.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
1. Drasar, B. S. & Jenkins, D.J.A. (1976) Bacteria, diet, and large bowel cancer. Am. J. Clin. Nutr. 29:1410-1416.
2. Bowling, T. E., Ralmundo, A. H., Grimble, G. K. & Silk, D.B.A. (1993) Reversal by short-chain fatty acids of colonic fluid secretion induced by enteral feeding. Lancet 342:1266-1268.[Medline]
3. Gibson, G. R. & Roberfroid, M. R. (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125:1401-1412.
4. Aldoori, W. H. (1997) The protective role of dietary fiber in diverticular disease. Kritchevsky, D. Bonfield, C. eds. Dietary Fiber in Health and Disease 1997:291-308 Plenum Press New York, NY. .
5. Gibson, G. R., Beatty, E. R., Wang, X. & Cummings, J. H. (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108:975-982.[Medline]
6. Kleessen, B., Sykura, B., Zunft, H. J. & Blaut, M. (1997) Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am. J. Clin. Nutr. 65:1397-1402.
7. Mitsuoka, T. (1982) Recent trends in research on intestinal flora. Bifidobacteria Microflora 1:3-24.
8. Harmsen, H. J., Wildboer-Veloo, A.C.M., Raangs, G. C., Wagendorp, A. A., Klijn, N., Bindels, J. G. & Welling, G. W. (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30:61-67.[Medline]
9. Finegold, S. M., Sutter, V. L. & Mathisen, G. E. (1983) Normal indigenous intestinal flora. Hentges, D. J. eds. Human Intestinal Microflora in Health and Disease 1983:3-31 Academic Press London, UK. .
10. Levy, J. (1998) Immunonutrition: the pediatric experience. Nutrition 14:641-647.[Medline]
11. Committee on Nutrition (1980) On the feeding of supplemental foods to infants. Pediatrics 65:1178-1181.
12. Campbell, J. M., Bauer, L. L., Fahey, G. C., Jr., Hogarth, A.J.C.L., Wolf, B. W. & Hunter, D. E. (1997) Selected fructooligosaccharide (1-kestose, nystose, and 1F-ß-fructofuranosylnystose) composition of foods and feeds. J. Agric. Food Chem. 45:3076-3082.
13. Fuller, R. (1992) Probiotics: The Scientific Basis 1992 Chapman and Hall London, UK. .
14. Goldin, B. R. (1998) Health benefits of probiotics. Br. J. Nutr. 80:S203-S207.[Medline]
15. Hamill, P. V., Drizd, T. A., Johnson, C. L., Reed, R. B. & Roche, A. F. (1977) NCHS growth curves for children birth-18 years, United States. Vital Health Stat 11:1-74.
16. Bryant, M. P. & Burkey, L. A. (1953) Cultural methods and some characteristics of some of the more numerous groups of bacteria in the bovine rumen. J. Dairy Sci. 36:205-217.
17. Bryant, M. P. & Robinson, I. M. (1961) An improved nonselective culture medium for ruminal bacteria and its use in determining diurnal variation in numbers of bacteria in the rumen. J. Dairy Sci. 44:1446-1456.
18. Mackie, R. I., Gilchrist, M. C., Robberts, A. M., Hannah, P. E. & Schwartz, H. M. (1978) Microbiological and chemical changes in the rumen during the stepwise adaptation of sheep to high concentrate diets. J. Agric. Sci. (Camb.) 90:241-254.
19. Muñoa, F. J. & Pares, R. (1988) Selective medium for isolation and enumeration of Bifidobacterium spp. Appl. Environ. Microbiol. 54:1715-1718.
20. Food and Drug Administration (1992) Method #196: Bacteriological Analytical Manual 7th ed. 1992 FDA Arlington, VA. .
21. Association of Official Analytical Chemists (1984) Official Methods of Analysis 14th ed. 1984 AOAC Washington, DC. .
22. SAS Institute Inc (1992) SAS User’s Guide: Statistics, Version 6.10 1992 SAS Institute Cary, NC. .
23. Carmer, S. G. & Swanson, M. R. (1973) An evaluation of ten pair-wise multiple comparison procedures by Monte Carlo methods. J. Am. Stat. Assoc. 68:66-74.
24. Steele, R.G.D. & Torrie, J. H. (1980) Principles and Procedures of Statistics: A Biometrical Approach 2nd ed. 1980 McGraw-Hill Publishing Co New York. .
25. Lifschitz, C. H., Wolin, M. J. & Reeds, P. J. (1990) Characterization of carbohydrate fermentation in feces of formula-fed and breast-fed infants. Pediatr. Res. 27:165-169.[Medline]
26. Parrett, A. M., Edwards, C. A. & Lokerse, E. (1997) Colonic fermentation capacity in vitro: development during weaning in breast-fed infants is slower for complex carbohydrates than for sugars. Am. J. Clin. Nutr. 65:927-933.
27. Fuchs, H. M., Dorfman, S. & Floch, M. H. (1976) The effect of dietary fiber supplementation in man. II. Alteration in fecal physiology and bacterial flora. Am. J. Clin. Nutr. 29:1443-1447.
28. Gorbach, S. L., Nahas, L., Lerner, P. I. & Weinstein, L. (1967) Studies of intestinal microflora: I. Effects of diet age, and periodic sampling on numbers of fecal microorganisms in man. Gastroenterology 53:845-855.[Medline]
29. Rao, A. V., Shiwnarian, N., Koo, M. & Jenkins, D.J.A. (1994) Effects of fiber-rich foods on the composition of intestinal microflora. Nutr. Res. 14:523-535.
30. Cummings, J. H. (1991) Production and metabolism of short-chain fatty acids in humans. Roche, A. F. eds. Short-Chain Fatty Acids: Metabolism and Clinical Importance: Report of the Tenth Ross Conference on Medical Research 1991:11-16 Ross Laboratories Columbus, OH. .
31. Roediger, W.E.W. (1980) Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21:793-798.
32. Scheppach, W., Bartram, P., Richter, A., Richter, F., Liepold, H., Dusel, G., Hofstetter, G., Ruthlein, J. & Kasper, H. (1992) Effect of short-chain fatty acids on the human colonic mucosa in vitro. J. Parenter. Enteral Nutr. 16:43-48.
33. Tappenden, K. A., Thomson, A.B.R., Wild, G. E. & McBurney, M. I. (1997) Short-chain fatty acid-supplemented total parenteral nutrition enhances functional adaptation to intestinal resection in rats. Gastroenterology 112:792-802.[Medline]
34. Balmer, S. E. & Wharton, B. A. (1989) Diet and faecal flora in the newborn: breast milk and infant formula. Arch. Dis. Child. 64:1672-1677.
35. Yoshioka, H., Iseki, K. & Fujita, K. (1983) Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 72:317-321.
36. Stark, P. L. & Lee, A. (1982) The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J. Med. Microbiol. 15:189-203.
37. Benno, Y., Sawada, K. & Mitsuoka, T. (1984) The intestinal microflora of infants: composition of fecal flora in breast-fed and bottle-fed infants. Microbiol. Immunol. 28:975-986.[Medline]
This article has been cited by other articles:
|
|
 |
|
  K. Knipping, E. C. A. M. van Esch, S. C. Wijering, S. van der Heide, A. E. Dubois, and J. Garssen In Vitro and In Vivo Anti-Allergic Effects of Arctium lappa L. Experimental Biology and Medicine, November 1, 2008; 233(11): 1469 - 1477. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
