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Characterization of Bacterial Communities in Feces from Healthy Elderly Volunteers and Hospitalized Elderly Patients by Using Real-Time PCR and Effects of Antibiotic Treatment on the Fecal Microbiota
Open accessAbstract
Fecal bacteria were studied in healthy elderly volunteers (age, 63 to 90 years;n= 35) living in the local community, elderly hospitalized patients (age, 66 to 103;n= 38), and elderly hospitalized patients receiving antibiotic treatment (age, 65 to 100;n= 21). Group- and species-specific primer sets targeting 16S rRNA genes were used to quantitate intestinal bacteria by using DNA extracted from feces and real-time PCR. The principal difference between healthy elderly volunteers and both patient cohorts was a marked reduction in the Bacteroides-Prevotella group following hospitalization. Reductions in bifidobacteria,Desulfovibrio spp.,Clostridium clostridiiforme, and Faecalibacterium prausnitzii were also found in the hospitalized patients. However, total 16S rRNA gene copy numbers (per gram of wet weight of feces) were generally lower in the stool samples of the two groups of hospitalized patients compared to the number in the stool samples of elderly volunteers living in the community, so the relative abundance (percentage of the group- and species-specific rRNA gene copies in relation to total bacterial rRNA gene copies) of bifidobacteria,Desulfovibrio spp.,C. clostridiiforme, and F. prausnitzii did not change. Antibiotic treatment resulted in further reductions in the numbers of bacteria and their prevalence and, in some patients, complete elimination of certain bacterial communities. Conversely, the numbers of enterobacteria increased in the hospitalized patients who did not receive antibiotics, and due to profound changes in fecal microbiotas during antibiotic treatment, the opportunistic species Enterococcus faecalis proliferated.
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“Specific microbial taxa are also associated with reduced frailty in elderly populations, including Bacteroidetes”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Bartosch et al., 2004
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Cultivable and Pyrosequenced Fecal Microflora in Centenarians and Young Subjects
Drago, L., Toscano, M., Rodighiero, V., De Vecchi, E., & Mogna, G. (2012) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e3182693982 · Cited by 92
Jump, R., Polinkovsky, A., Hurless, K. N., Sitzlar, B. M., Eckart, K. E., Tomas, M. E., Deshpande, A., Nerandzic, M. M., & Donskey, C. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101267 · Cited by 92
The matter of the reproductive microbiome
Schoenmakers, S., Steegers‐Theunissen, R. P. M., & Faas, M. M. (2018) · Obstetric Medicine · doi:10.1177/1753495x18775899 · Cited by 91
Wang, Y., Ametaj, B. N., Ambrose, D. J., & Gänzle, M. G. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-19 · Cited by 92
Relative Abundance in Bacterial and Fungal Gut Microbes in Obese Children: A Case Control Study
Borgo, F., Verduci, E., Riva, A., Lassandro, C., Riva, E., Morace, G., & Borghi, E. (2016) · Childhood Obesity · doi:10.1089/chi.2015.0194 · Cited by 98
Rist, V. T. S., Weiss, E., Sauer, N., Mosenthin, R., & Eklund, M. (2013) · Anaerobe · doi:10.1016/j.anaerobe.2013.10.003 · Cited by 91
Compositional dynamics of the human intestinal microbiota with aging: Implications for health
Lakshminarayanan, B., Stanton, C., O’Toole, P. W., & Ross, R. P. (2014) · The journal of nutrition health & aging · doi:10.1007/s12603-014-0549-6 · Cited by 93
“…prolonged intestinal transit times, lack of physical activity, recurrent infections and frequent use of antibiotics and other medications (31, 35-38). the most dramatic changes in the composition of the intestinal microbiota in the elderly include reduction in numbers and species diversity…”
InfluentialBacillus coagulans GBI-30, 6086 Modulates Faecalibacterium prausnitzii in Older Men and Women
Nyangale, E. P., Farmer, S., Cash, H. A., Keller, D., Chernoff, D., & Gibson, G. R. (2015) · Journal of Nutrition · doi:10.3945/jn.114.199802 · Cited by 89
“Studies that involve probiotics were also reported (20, 21), although the issue of strain survivability through the upper GI tract occurs.”
BackgroundShao, Y., Lei, Z., Yuan, J., Yang, Y., Guo, Y., & Zhang, B. (2014) · The Journal of Microbiology · doi:10.1007/s12275-014-4347-y · Cited by 88
Influence of isomalto-oligosaccharides on intestinal microbiota in rats
Ketabi, A., Dieleman, L. A., & Gänzle, M. G. (2011) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2011.04984.x · Cited by 86
Effect of prebiotics on the human gut microbiota of elderly persons
Toward, R. E., Montandon, S., Walton, G., & Gibson, G. R. (2012) · Gut Microbes · doi:10.4161/gmic.19411 · Cited by 86
Akiyama, K., Nishioka, K., Khan, K. N., Tanaka, Y., Mori, T., Nakaya, T., & Kitawaki, J. (2019) · American Journal of Reproductive Immunology · doi:10.1111/aji.13147 · Cited by 84
Metabolomics Signatures of Aging: Recent Advances
Adav, S. S., & Wang, Y. (2021) · Aging and Disease · doi:10.14336/ad.2020.0909 · Cited by 95
“Lactobacilli, and Bacteroides have been linked to old age frailty and aging [128, 129].”
BackgroundChanges on fecal microbiota in rats exposed to permethrin during postnatal development
Nasuti, C., Coman, M. M., Olek, R. A., Fiorini, D., Verdenelli, M. C., Cecchini, C., Silvi, S., Fedeli, D., & Gabbianelli, R. (2016) · Environmental Science and Pollution Research · doi:10.1007/s11356-016-6297-x · Cited by 85
“A Real-Time quantitative PCR (QPCR) procedure was used for the quantification of the main bacterial groups of rats’ intestinal microbiota by using specific primers, chosen from literature (Rinttila et al. 2004; Fang and Hedin 2003; Byun et al. 2004; Langendijk et al. 1995; Bartosch et al., 2004) as shown in the Table…”
Maintenance of a healthy trajectory of the intestinal microbiome during aging: A dietary approach
Candela, M., Biagi, E., Brigidi, P., O’Toole, P. W., & de Vos, W. M. (2013) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2013.12.004 · Cited by 87
“Indeed, the decrease of Bacteroidetes seems to be more strictly related to frailty conditions, antibiotic treatment, hospitalization, rather than to the aging process itself (Bartosch et al., 2004; Hopkins et al., 2001; van Tongeren et al., 2005).”
BackgroundDiversity and metabolic impact of intestinalLactobacillusspecies in healthy adults and the elderly
Štšepetova, J., Sepp, E., Kolk, H., Lõivukene, K., Songisepp, E., & Mikelsaar, M. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114510004770 · Cited by 86
“The purified plasmids were quantified by spectrophotometry (Quibite; Invitrogen, Carlsbad, CA, USA) of multiple dilutions((27)).”
Contribution of the Intestinal Microbiota to Human Health: From Birth to 100 Years of Age
Cheng, J., Palva, A., de Vos, W. M., & Satokari, R. M. (2011) · Current topics in microbiology and immunology · doi:10.1007/82_2011_189 · Cited by 101
“In the elderly, antibiotics seem to fortify the age-related microbiota changes (Bartosch et al. 2004; Woodmansey et al. 2004; Claesson et al. 2010) and increase the risk of GI tract infections including Clostridium difficile infection.”
BackgroundWang, M., Radlowski, E. C., Monaco, M. H., Fahey, G. C., Jr., Gaskins, H. R., & Donovan, S. M. (2013) · Journal of Nutrition · doi:10.3945/jn.112.173096 · Cited by 80
Leu, R. K. L., Young, G. P., Hu, Y. C., Winter, J. M., & Conlon, M. A. (2013) · Digestive Diseases and Sciences · doi:10.1007/s10620-013-2844-1 · Cited by 82
“gnavus except 45 s annealing and 700 nM primer) [30].”
BackgroundLu, H., He, J.-Q., Wu, Z., Xu, W., Zhang, H., Ye, P., Yang, J., Zhen, S., & Li, L. (2013) · Microbial Ecology · doi:10.1007/s00248-013-0211-6 · Cited by 81
“DNAwas extracted from the feces and bacterial precipitates were made using a Qiagen Stool Kit (Qiagen, Hilden, Germany) with a modified protocol for cell lysis [3].”
Effect of Age on Treatment Outcomes in C lostridium difficile Infection
Louie, T., Miller, M. A., Crook, D. W., Lentnek, A. L., Bernard, L., High, K. P., Shue, Y., & Gorbach, S. L. (2013) · Journal of the American Geriatrics Society · doi:10.1111/jgs.12090 · Cited by 81
Microbiologic factors affecting Clostridium difficile recurrence
Chilton, C. H., Pickering, D. S., & Freeman, J. (2017) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2017.11.017 · Cited by 81
Gut Microbiota in Bipolar Depression and Its Relationship to Brain Function: An Advanced Exploration
Lu, Q., Lai, J., Lu, H., Ng, C. H., Huang, T., Zhang, H., Ding, K., Wang, Z., Jiang, J., Hu, J., et al. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00784 · Cited by 83
“DNA was extracted from the feces and precipitates with the Qiagen Stool Kit (Qiagen, Hilden, Germany), according to a modified protocol for cell lysis (41).”
MethodHigh-throughput analysis of the impact of antibiotics on the human intestinal microbiota composition
Ladirat, S. E., Schols, H. A., Nauta, A., Schoterman, M. H. C., Keijser, B. J. F., Montijn, R. C., Gruppen, H., & Schuren, F. H. J. (2012) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2012.12.011 · Cited by 82
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Salazar, N., López, P., Valdés, L., Margolles, A., Suárez, A., Patterson, Á. M., Cuervo, A., Reyes-Gavilán, C. G. D. L., Ruas-Madiedo, P., Gonzalez, S., et al. (2013) · Journal of the American College of Nutrition · doi:10.1080/07315724.2013.827047 · Cited by 80
Acharya, C., & Bajaj, J. S. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.10.056 · Cited by 79
The Pioneer Gut Microbiota in Human Neonates Vaginally Born at Term—A Pilot Study
Karlsson, C., Molin, G., Cilio, C., & Ahrné, S. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e318225f765 · Cited by 83
Alterations in intestinal microbiota of elderly Irish subjects post-antibiotic therapy
O’Sullivan, Ó., Coakley, M., Lakshminarayanan, B., Conde, S., Claesson, M. J., Cusack, S., Fitzgerald, A. J., O’Toole, P. W., Stanton, C., & Ross, R. P. (2012) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dks348 · Cited by 77
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Matijašić, B. B., Obermajer, T., Lipoglavšek, L., Sernel, T., Locatelli, I., Kos, M., Šmid, A., & Rogelj, I. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10743 · Cited by 81
“…MA), 0.2 μM of each of the 2 oligonucleotide primers listed in Supplementary Table S1 (http://dx.doi.org/10.3168/jds.2015-10743; Malinen et al., 2003; Bartosch et al., 2004; Rinttilä et al., 2004; Fierer et al., 2005; Songjinda et al., 2007; Savard et al., 2011), and 1 μL of the isolated fecal…”
BackgroundInfluentialZhou, X., Kong, X., Lian, G., Blachier, F., Geng, M., & Yin, Y. (2014) · Nutrition Research · doi:10.1016/j.nutres.2014.08.008 · Cited by 75
Metadata
- Authors
- Bartosch, S., Fite, A., Macfarlane, G. T., & McMurdo, M. E. T.
- Affiliations
- University of Dundee (GB)
- MRC Microbiology and Gut Biology Group
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2004-06
- Volume
- 70
- Issue
- 6
- Pages
- 3575-3581
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC427772
- OpenAlex
- W2109744701
- Cited by
- 762
- References
- 51
- Citations by year
- 2026: 15 · 2025: 29 · 2024: 12 · 2023: 31 · 2022: 36 · 2021: 51 · 2020: 49 · 2019: 36 · 2018: 38 · 2017: 63 · 2016: 59 · 2015: 65 · 2014: 44 · 2013: 46 · 2012: 46
- FWCI
- 4.63
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion)
- Funders
- Medical Research Council
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- fecal microbiota, older adults, hospitalized patients, antibiotic therapy, Bifidobacterium, Desulfovibrio, Faecalibacterium prausnitzii, 16S rRNA gene quantification, Enterobacteriaceae, Enterococcus faecalis, intestinal bacteria, community-acquired infections
- MeSH terms
- Aged, Aged, 80 and over, Anti-Bacterial Agents, Bacteria, Bacterial Infections, DNA, Bacterial, DNA, Ribosomal, Feces, Hospitalization, Humans, RNA, Ribosomal, 16S, Species Specificity, Polymerase Chain Reaction, Ecosystem, DNA Primers, Gene Dosage, Genes, rRNA
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