Normal aging is associated with significant changes in the function of most organs and tissues, such as decreased taste thresholds, hypochlorhydria due to atrophic gastritis, and decreased liver blood flow and size (11). The GI tract is no exception, and there is increased evidence of impaired gastrointestinal function with aging (3,11-13). In the GI tract of the elderly, the age-related changes include decreased acid secretion by the gastric mucosa, and greater permeability of mucosal membranes which have been linked to increase in circulating antibodies to components of the intestinal microbiota in elderly subjects. Therefore, certain microbes which can take advantage of new ecological niches are assumed to become predominant inhabitants, leading to a dramatic shift in the composition of the gut microbiota upon age.
Although the knowledge about the age-related alteration of the human intestinal microbiota is still limited, the structure of the intestinal microbiota in the healthy elderly has been suggested to be different from that of the healthy adults. This phenomenon is considered to be a result of aging, but it may also accelerate senescence.
As early as in the 1960s, the scientific attention has been focused to characterize the intestinal microbiota of the elderly. In several works conduced in the different geographic regions, reduced presence of bifidobacteria was often observed in the fecal microbiota of the elderly compared to that of the healthy adults, as well as more putrefactive bacteria Enterobacteriaceae, Streptococcus, Staphylococcus, Proteus and C. perfringens (14-17).
Mitsuoka and his colleagues (18,19) analyzed the composition of the intestinal microbiota in the various stages of life and observed an age-dependent change in the composition of the fecal microbiota. Bifidobacteria were less present in the fecal microbiota of senile (65- to 85-year-old) persons than in those of younger adults, while more lactobacilli and clostridia were found in the fecal samples of the elderly.
Mitsuoka and coworkers (20) compared the fecal flora of the elderly (61-95 years old) with healthy adults (31.8 + 6.6 years old) using optimized culture procedures for members of the anaerobic microbiota. Total bacterial count, Bidifobacterium Veillonella, Eubacterium were decreased significantly, whereas C. perfringens and Lactobacillus were increased significantly. Furthermore, the frequencies of occurrence in Bifidobacterium,
Micrococaceae was decreased, while those of C. perfringens, other Clostridium sp., and yeasts were increased significantly in the elderly compared with that of the healthy adults.
Using the same method, Benno and Mitsuoka (21) did not find significant differences in Bacteroidaceae, Eubacterium, Peptostreptococcus and Megasphaera between the healthy elderly and healthy adults. However, Bifidobacterium (Bif. adolescentis and Bif. longum), Enterococcus were less in the elderly compared with the healthy adults, while lecithinase-negative Clostridium and C. paraputrificum were increased in the elderly.
Recently, non-culture-dependent molecular methods have been used to investigate the intestinal microbiota (22). The advent of these molecular methods, which do not rely on our ability to culture bacteria prior to quantification, allow additional information to be gained on the gut microbiota as a whole. Another method that allows ecological analysis without the need to culture the organism is that of community cellular fatty acid (CFA) analysis. Numerous environmental factors affect bacterial fatty acid synthesis, but certain signature fatty acids have been used to indicate the presence of specific groups of organisms in soil and marine environments, and have also been used to study community structure in human fecal samples.
Direct polymerase chain reaction analysis was performed on elderly persons' fecal samples (22). Over 280 clones were generated and characterized by sequence analyses, providing a molecular taxonomic inventory. Phylogenetic analysis showed that the microbiota of the elderly was more diversified than that of younger adults. The proportion of unknown molecular species was very high among the clones derived from fecal samples of elderly persons. It is evident from this study that the fecal microbiota of the elderly person is very complex. The microbial diversity of the intestinal microbiota appears to be increased with age. This is in contrast to the microbial diversity of babies, which was found to be extremely low: only nine species were detected within each clone's library.
Hopkins et al. (23) studied fresh fecal samples obtained from seven adults, five elderly individuals, and four geriatric patients diagnosed with C. difficile-associated diarrhea. Selected fecal bacteria were investigated using viable counting procedures, 16S rRNA abundance measurements and community CFA profile. The principal microbiological differences between adults and the elderly were the occurrence of higher numbers of enterobacteria and a lower number of anaerobe populations in the elderly group. Another important finding of this study was the lower number of bifidobacteria observed in the group of elderly patients.
Hopkins and Macfarlane (24) isolated bacteria from fecal samples of healthy young adults, elderly subjects, and elderly patients with Clostridium difficile-associated diarrhea (CDAD). The isolated bacteria were identified to species level on the basis of their CFA profiles with Microbial Identification System (MIDI, Inc., Newark, DE) (MIDI). While Bacteroides species diversity increased in the feces of the elderly individuals, bifidobacteria diversity dramatically decreased with age.
These observations indicate that aging may diminish bifidobacteria, and significantly increase clostridia, including C. perfringens, and allow a slight increase of lactobacilli, streptococci, and enterobacteriacea. The total bacterial counts and anaerobes/aerobes in the intestinal microbiota of the elderly are relatively lower than those of the healthy infants and young adults.
Historically, bifidobacteria have been considered to be the most important organisms for infants while lactobacilli, especially L. acidophilus, were considered the predominant beneficial bacterium for adults (5). However, bifidobacteria have recently been suggested to be more important throughout life as beneficial intestinal bacteria than lactobacilli (25,26). These ecological studies on the intestinal microbiota of the elderly indicate that bifidobacteria rather than lactobacilli are often decreased upon age. Although some changes also happen upon age in other groups of bacteria, they are non-specific, not constant, and very individual. Furthermore, a decrease in bifidobacteria has often been observed in the intestinal microbiota of various young patients (23,27,28). Therefore, a decrease in bifidobacteria in the intestinal microbiota could be considered as an important hallmark for aging and disease of the human GI tract.
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