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Gut. 2001 Feb; 48(2): 198–205.
PMCID: PMC1728209

Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles


BACKGROUND—The normal intestinal microflora plays an important role in host metabolism and provides a natural defence mechanism against invading pathogens. Although the microbiota in adults has been extensively studied, little is known of the changes that occur in the microflora with aging. These may have important consequences in elderly people, many of whom are receiving antibiotic therapy and who are most susceptible to intestinal dysbiosis.
AIMS—To characterise the major groups of faecal bacteria in subjects of different ages using a combination of cultural, molecular, and chemotaxonomic approaches.
METHODS—Comparative microbiological studies were made on four different subject groups: children (16 months to seven years, n=10), adults (21-34 years, n=7), healthy elderly subjects (67-88 years, n=5), and geriatric patients (68-73 years, n=4) diagnosed with Clostridium difficile diarrhoea. Selected faecal bacteria were investigated using viable counting procedures, 16S ribosomal RNA (rRNA) abundance measurements, and the occurrence of specific signature fatty acids in whole community fatty acid methyl ester profiles.
RESULTS—The principal microbiological difference between adults and children was the occurrence of higher numbers of enterobacteria in the latter group, as determined by viable counts (p<0.05) and 16S rRNA (p<0.01) measurements. Moreover, a greater proportion of children's faecal rRNA was hybridised by the three probes (bifidobacteria, enterobacteria, bacteroides-porphyromonas-prevotella) used in the study, indicating a less developed gut microbiota. Species diversity was also markedly lower in the Clostridium difficile associated diarrhoea group, which was characterised by high numbers of facultative anaerobes and low levels of bifidobacteria and bacteroides. Although it was a considerably less sensitive diagnostic tool, cellular fatty acid analysis correlated with viable bacterial counts and 16S rRNA measurements in a number of bacteria, including bacteroides.
CONCLUSIONS—Polyphasic analysis of faecal bacteria showed that significant structural changes occur in the microbiota with aging, and this was especially evident with respect to putatively protective bifidobacteria. Reductions in these organisms in the large bowel may be related to increased disease risk in elderly people.

Keywords: intestinal bacteria; aging; cellular fatty acids; ribosomal RNA; Clostridium difficile infection

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Selected References

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  • Lovat LB. Age related changes in gut physiology and nutritional status. Gut. 1996 Mar;38(3):306–309. [PMC free article] [PubMed]
  • Waterlow JC. Protein-energy malnutrition: the nature and extent of the problem. Clin Nutr. 1997 Mar;16 (Suppl 1):3–9. [PubMed]
  • Ellis-Pegler RB, Crabtree C, Lambert HP. The faecal flora of children in the United Kingdom. J Hyg (Lond) 1975 Aug;75(1):135–142. [PMC free article] [PubMed]
  • Stark PL, Lee A. The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J Med Microbiol. 1982 May;15(2):189–203. [PubMed]
  • Gorbach SL, Nahas L, Lerner PI, Weinstein L. Studies of intestinal microflora. I. Effects of diet, age, and periodic sampling on numbers of fecal microorganisms in man. Gastroenterology. 1967 Dec;53(6):845–855. [PubMed]
  • Benno Y, Nakao H, Uchida K, Mitsuoka T. Impact of the advances in age on the gastrointestinal microflora of beagle dogs. J Vet Med Sci. 1992 Aug;54(4):703–706. [PubMed]
  • Ljungberg B, Nilsson-Ehle I, Edlund C, Nord CE. Influence of ciprofloxacin on the colonic microflora in young and elderly volunteers: no impact of the altered drug absorption. Scand J Infect Dis. 1990;22(2):205–208. [PubMed]
  • Pollard AJ, Galassini R, van der Voort EM, Booy R, Langford P, Nadel S, Ison C, Kroll JS, Poolman J, Levin M. Humoral immune responses to Neisseria meningitidis in children. Infect Immun. 1999 May;67(5):2441–2451. [PMC free article] [PubMed]
  • Pollard AJ, Galassini R, Rouppe van der Voort EM, Hibberd M, Booy R, Langford P, Nadel S, Ison C, Kroll JS, Poolman J, et al. Cellular immune responses to Neisseria meningitidis in children. Infect Immun. 1999 May;67(5):2452–2463. [PMC free article] [PubMed]
  • Percival RS, Marsh PD, Challacombe SJ. Serum antibodies to commensal oral and gut bacteria vary with age. FEMS Immunol Med Microbiol. 1996 Aug;15(1):35–42. [PubMed]
  • Doré J, Sghir A, Hannequart-Gramet G, Corthier G, Pochart P. Design and evaluation of a 16S rRNA-targeted oligonucleotide probe for specific detection and quantitation of human faecal Bacteroides populations. Syst Appl Microbiol. 1998 Mar;21(1):65–71. [PubMed]
  • Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, Doré J. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol. 1999 Nov;65(11):4799–4807. [PMC free article] [PubMed]
  • Schultsz C, Van Den Berg FM, Ten Kate FW, Tytgat GN, Dankert J. The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology. 1999 Nov;117(5):1089–1097. [PubMed]
  • Peltonen R, Ling WH, Hänninen O, Eerola E. An uncooked vegan diet shifts the profile of human fecal microflora: computerized analysis of direct stool sample gas-liquid chromatography profiles of bacterial cellular fatty acids. Appl Environ Microbiol. 1992 Nov;58(11):3660–3666. [PMC free article] [PubMed]
  • Peltonen R, Nenonen M, Helve T, Hänninen O, Toivanen P, Eerola E. Faecal microbial flora and disease activity in rheumatoid arthritis during a vegan diet. Br J Rheumatol. 1997 Jan;36(1):64–68. [PubMed]
  • Eerola E, Möttönen T, Hannonen P, Luukkainen R, Kantola I, Vuori K, Tuominen J, Toivanen P. Intestinal flora in early rheumatoid arthritis. Br J Rheumatol. 1994 Nov;33(11):1030–1038. [PubMed]
  • Newton DF, Cummings JH, Macfarlane S, Macfarlane GT. Growth of a human intestinal Desulfovibrio desulfuricans in continuous cultures containing defined populations of saccharolytic and amino acid fermenting bacteria. J Appl Microbiol. 1998 Aug;85(2):372–380. [PubMed]
  • Macfarlane GT, Cummings JH, Allison C. Protein degradation by human intestinal bacteria. J Gen Microbiol. 1986 Jun;132(6):1647–1656. [PubMed]
  • Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990 Jun;56(6):1919–1925. [PMC free article] [PubMed]
  • Raskin L, Poulsen LK, Noguera DR, Rittmann BE, Stahl DA. Quantification of methanogenic groups in anaerobic biological reactors by oligonucleotide probe hybridization. Appl Environ Microbiol. 1994 Apr;60(4):1241–1248. [PMC free article] [PubMed]
  • Stahl DA, Flesher B, Mansfield HR, Montgomery L. Use of phylogenetically based hybridization probes for studies of ruminal microbial ecology. Appl Environ Microbiol. 1988 May;54(5):1079–1084. [PMC free article] [PubMed]
  • Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, Welling GW. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol. 1995 Aug;61(8):3069–3075. [PMC free article] [PubMed]
  • Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol. 1998 Sep;64(9):3336–3345. [PMC free article] [PubMed]
  • Sghir A, Gramet G, Suau A, Rochet V, Pochart P, Dore J. Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl Environ Microbiol. 2000 May;66(5):2263–2266. [PMC free article] [PubMed]
  • Welling GW, Elfferich P, Raangs GC, Wildeboer-Veloo AC, Jansen GJ, Degener JE. 16S ribosomal RNA-targeted oligonucleotide probes for monitoring of intestinal tract bacteria. Scand J Gastroenterol Suppl. 1997;222:17–19. [PubMed]
  • Macfarlane GT, Cummings JH. Probiotics and prebiotics: can regulating the activities of intestinal bacteria benefit health? BMJ. 1999 Apr 10;318(7189):999–1003. [PMC free article] [PubMed]
  • Yamazaki S, Machii K, Tsuyuki S, Momose H, Kawashima T, Ueda K. Immunological responses to monoassociated Bifidobacterium longum and their relation to prevention of bacterial invasion. Immunology. 1985 Sep;56(1):43–50. [PMC free article] [PubMed]
  • Gibson GR, Wang X. Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J Appl Bacteriol. 1994 Oct;77(4):412–420. [PubMed]
  • Tojo M, Oikawa T, Morikawa Y, Yamashita N, Iwata S, Satoh Y, Hanada J, Tanaka R. The effects of Bifidobacterium breve administration on campylobacter enteritis. Acta Paediatr Jpn. 1987 Feb;29(1):160–167. [PubMed]
  • Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology. 1995 Apr;108(4):975–982. [PubMed]
  • Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995 Jun;125(6):1401–1412. [PubMed]
  • Haack SK, Garchow H, Odelson DA, Forney LJ, Klug MJ. Accuracy, reproducibility, and interpretation of Fatty Acid methyl ester profiles of model bacterial communities. Appl Environ Microbiol. 1994 Jul;60(7):2483–2493. [PMC free article] [PubMed]
  • Campbell JM, Fahey GC, Jr, Lichtensteiger CA, Demichele SJ, Garleb KA. An enteral formula containing fish oil, indigestible oligosaccharides, gum arabic and antioxidants affects plasma and colonic phospholipid fatty acid and prostaglandin profiles in pigs. J Nutr. 1997 Jan;127(1):137–145. [PubMed]

Figures and Tables

Figure 1
Viable counts of bacteroides, bifidobacteria, enterobacteria, and total anaerobes in faeces of different age groups. Results are mean (SEM) in children (n=5), adults (n=7), elderly subjects (n=4), and in patients with Clostridium difficile associated ...
Figure 2
Viable counts of clostridia, lactobacilli, and enterococci in faeces obtained from children (n=5), adults (n=7), elderly subjects (n=4), and patients with Clostridium difficile associated diarrhoeal (CDAD, n=4).
Figure 3
16S rRNA concentrations in faeces. Results are mean (SEM) in children (n=10), adults (n=7), elderly subjects (n=5), and in patients with C difficile associated diarrhoea (CDAD, n=4). BPP, Bacteroides-Porphyromonas-Prevotella.     ...

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