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Adjusting for age improves identification of gut microbiome alterations in multiple diseases
Open accessAbstract
Interaction between disease-microbiome associations and ageing has not been explored in detail. Here, using age/region-matched sub-sets, we analysed the gut microbiome differences across five major diseases in a multi-cohort dataset constituting more than 2500 individuals from 20 to 89 years old. We show that disease-microbiome associations display specific age-centric trends. Ageing-associated microbiome alterations towards a disease-like configuration occur in colorectal cancer patients, thereby masking disease signatures. We identified a microbiome disease response shared across multiple diseases in elderly subjects that is distinct from that in young/middle-aged individuals, but also a novel set of taxa consistently gained in disease across all age groups. A subset of these taxa was associated with increased frailty in subjects from the ELDERMET cohort. The relevant taxa differentially encode specific functions that are known to have disease associations.
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“Members of the Bifidobacteriaceae, Akkermansiaceae, and Eubacteriaceae families that are associated with beneficial effects on intestinal and extra-intestinal health in both mice and humans”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [43]
In the citing paper
“However, some species are currently thought to modulate cholesterol and bile acid metabolism and are considered potential therapeutics [43].”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [43]
In the citing paper
“Age was also added to the feature-set, as this covariate has been shown to improve microbiome predictions in CRC (Ghosh et al., 2020).”
From Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3 (2021) · cites this paper as Ghosh et al., 2020
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“The Enterocloster genus (E. aldensis, E. asparagiformis, and E. bolteae) represents a vancomycin-sensitive clade of immunosuppressive bacteria, dominant in the intestinal microbiota of people and patients suffering from aging and chronic inflammatory disorders including cancer.39”
From Custom scoring based on ecological topology of gut microbiota associated with cancer immunotherapy outcome (2024) · cites this paper as [47]
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Cites
A metagenome-wide association study of gut microbiota in type 2 diabetes
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“not CRC), we compiled a list of known disease-associated markers from each of the original studies (Feng et al., 2015; Franzosa et al., 2019; Karlsson et al., 2013; Qin et al., 2012; Qin et al., 2014).”
BackgroundMethodResultInfluentialGut microbiota composition correlates with diet and health in the elderly
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O’Connor, E. M., Cusack, S., Harris, H. M. B., Coakley, M., Lakshminarayanan, B., O’Sullivan, O., et al. (2012) · Nature · doi:10.1038/nature11319 · Cited by 3,314 · cited 2×
“We observed that this association analysis of metabolite profiles reflects frailty-associated changes with respect to bioavailability of specific compounds, many of which have been previously shown to have corresponding associations with health, thereby validating our findings (Claesson et al., 2012).”
ResultSelf-citationGut metagenome in European women with normal, impaired and diabetic glucose control
Karlsson, F. H., Tremaroli, V., Nookaew, I., Bergström, G., Behre, C. J., Fagerberg, B., Nielsen, J., & Bäckhed, F. (2013) · Nature · doi:10.1038/nature12198 · Cited by 3,115 · cited 3×
“not CRC), we compiled a list of known disease-associated markers from each of the original studies (Feng et al., 2015; Franzosa et al., 2019; Karlsson et al., 2013; Qin et al., 2012; Qin et al., 2014).”
MethodResultPopulation-level analysis of gut microbiome variation
Falony, G., Joossens, M., Vieira-Silva, S., Wang, J., Darzi, Y., Faust, K., Kurilshikov, A., Bonder, M. J., Valles-Colomer, M., Vandeputte, D., et al. (2016) · Science · doi:10.1126/science.aad3503 · Cited by 2,400 · cited 1×
“region/ethnicity-specific variations, multiple studies have also shown age to be a strong covariate of microbiome composition (Falony et al., 2016).”
BackgroundReduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach
Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K., Pelletier, E., Frangeul, L., Nalin, R., Jarrin, C., Chardon, P., Marteau, P., et al. (2006) · Gut · doi:10.1136/gut.2005.073817 · Cited by 2,277 · cited 1×
“These species were previously implicated in Clostridium difficile resistance and IBD, respectively (Buffie et al., 2015; Manichanh et al., 2006).”
BackgroundMetaPhlAn2 for enhanced metagenomic taxonomic profiling
Truong, D. T., Franzosa, E. A., Tickle, T. L., Scholz, M., Weingart, G., Pasolli, E., Tett, A., Huttenhower, C., & Segata, N. (2015) · Nature Methods · doi:10.1038/nmeth.3589 · Cited by 2,185 · cited 1×
“A further advantage of the curatedMetagenomicData is that these microbiome profiles were created using uniform bioinformatic analysis of the sequenced reads (using metaphlan2 and humann2) (Franzosa et al., 2018; Truong et al., 2015).”
MethodAlterations of the human gut microbiome in liver cirrhosis
Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., Guo, J., Le Chatelier, E., Yao, J., Wu, L., et al. (2014) · Nature · doi:10.1038/nature13568 · Cited by 2,177 · cited 2×
“not CRC), we compiled a list of known disease-associated markers from each of the original studies (Feng et al., 2015; Franzosa et al., 2019; Karlsson et al., 2013; Qin et al., 2012; Qin et al., 2014).”
MethodResultDisentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota
MetaHIT consortium, Forslund, K., Hildebrand, F., Nielsen, T., Falony, G., Le Chatelier, E., Sunagawa, S., Prifti, E., Vieira-Silva, S., Gudmundsdottir, V., et al. (2015) · Nature · doi:10.1038/nature15766 · Cited by 2,116 · cited 4×
“Another recent study investigating the effect of metformin on the gut microbiome of two of the T2D cohorts analysed in the current study identified Lactobacillus salivarius to be affected by metformin, accompanied by an increase in Escherichia (Forslund et al., 2015).”
InfluentialGut microbiome structure and metabolic activity in inflammatory bowel disease
Franzosa, E. A., Sirota-Madi, A., Avila-Pacheco, J., Fornelos, N., Haiser, H. J., Reinker, S., Vatanen, T., Hall, A. B., Mallick, H., McIver, L. J., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0306-4 · Cited by 1,995 · cited 4×
“not CRC), we compiled a list of known disease-associated markers from each of the original studies (Feng et al., 2015; Franzosa et al., 2019; Karlsson et al., 2013; Qin et al., 2012; Qin et al., 2014).”
MethodResultInfluentialPrecision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile
Buffie, C. G., Bucci, V., Stein, R. R., McKenney, P. T., Ling, L., Gobourne, A., No, D., Liu, H., Kinnebrew, M., Viale, A., et al. (2015) · Nature · doi:10.1038/nature13828 · Cited by 1,872
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Items 101–200 of 234
Mitchelson, K. A. J., Tran, T. T. T., Dillon, E., Vlčková, K., Harrison, S. M., Ntemiri, A., Cunningham, K., Gibson, I., Finucane, F. M., O’Connor, E. M., et al. (2022) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202100819 · Cited by 20
Self-citationExploring the human gut microbiota targets in relation to the use of contemporary antidepressants
Lin, S.-K. K., Chen, H., Chen, C.-H., Chen, I., Lu, M., Hsu, C., Chiu, Y.-H., Wang, T.-Y., Chen, H., Chung, Y.-C. E., et al. (2023) · Journal of Affective Disorders · doi:10.1016/j.jad.2023.10.016 · Cited by 21
The gut microbiome and potential implications for early-onset colorectal cancer
Mukherji, R., & Weinberg, B. A. (2020) · Colorectal Cancer · doi:10.2217/crc-2020-0007 · Cited by 21
Practical Considerations in Diagnosing and Managing Early-Onset GI Cancers
Lumish, M. A., & Cercek, A. (2022) · Journal of Clinical Oncology · doi:10.1200/jco.21.02708 · Cited by 23
Strauss, J., Haskey, N., Ramay, H. R., Ghosh, T. S., Taylor, L., Yousuf, M., Ohland, C., McCoy, K. D., Ingram, R. J. M., Ghosh, S. K., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087323 · Cited by 19
“, citrulline, L-serine, Lasparagine, L-alanine, L-threonine), bile acid salts (deoxycholate) and taxa including Streptococcus anginosus, Asaccharobacter celatus and Enterorhabdus caecimuris found in this module have been associated with aging [36] and IBD [37].”
BackgroundSelf-citationGut microbiota influence frailty syndrome in older adults: mechanisms and therapeutic strategies
Wang, X., Fan, L., Meng, C., Wang, Y., Deng, L.-E., Yuan, Z., Zhang, J., Li, Y., & Lv, S. (2023) · Biogerontology · doi:10.1007/s10522-023-10082-7 · Cited by 20
“Furthermore, Ghosh et al. (Ghosh et al. 2020a) observed that the onset of frailty was not only associated with an increased consumption of SCFAs by intestinal bacteria (accompanied by a decrease in butyrate-producing intestinal bacteria) but also with an increased consumption of tryptophan as well as an increased prod…”
The Role of the Gut Microbiome in Health and Disease in the Elderly
Chen, L. A., & Boyle, K. (2024) · Current Gastroenterology Reports · doi:10.1007/s11894-024-00932-w · Cited by 22
“Increasing research suggests that natural, or “healthy”, aging leads to specific changes in gut microbiome composition, such as the loss of certain commensal genera, including Prevotella , Faecalibacterium , and Bifidobacterium , and the species Eubacterium rectale [16, 17].”
BackgroundO’Sullivan, J., Patel, S. H., Leventhal, G. E., Fitzgerald, R. S., Mendieta, E. J. L., Huseyin, C. E., Konstantinidou, N., Rutherford, E. M., Lavelle, A., Dabbagh, K., et al. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2450207 · Cited by 19
Gut microbiota in relation to frailty and clinical outcomes
D’Amico, F., Barone, M., Brigidi, P., & Turroni, S. (2023) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000926 · Cited by 19
“Also, frail individuals from the ELDERMET cohort were characterized by higher levels of lithocholic acid (and derivatives) and deoxycholic acid than nonfrail individuals [16].”
BackgroundYe, H., Ghosh, T. S., Hueston, C. M., Vlčková, K., Golubeva, A. V., Hyland, N. P., & O’Toole, P. W. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2282796 · Cited by 19
“11 Furthermore, F. prausnitzii has been negatively associated with frailty in a twin study.”
BackgroundInfluentialSelf-citationGut Microbiota Composition and Metabolic Potential of Long-Living People in China
Zhang, S., Ning, R., Zeng, B., Deng, F., Kong, F., Guo, W., Zhao, J., & Li, Y. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.820108 · Cited by 18
Longitudinal gut microbiome dynamics in relation to age and senescence in a wild animal population
Worsley, S. F., Davies, C. S., Lee, C. Z., Mannarelli, M., Burke, T. A., Komdeur, J., Dugdale, H. L., & Richardson, D. S. (2024) · Molecular Ecology · doi:10.1111/mec.17477 · Cited by 19
“This also contrasts with long-term studies on humans (Claesson et al., 2011; Ghosh et al., 2020; Wilmanski et al., 2021), and a recent longitudinal study on wild macaques ( Macaca assamensis ) (Sadoughi et al., 2022), which identified increasing GM heterogeneity amongst individuals in older age…”
Kennedy, M. S., & Chang, E. B. (2025) · Journal of Clinical Investigation · doi:10.1172/jci193969 · Cited by 17
“Ghosh et al. identified distinct microbiome signatures for IBD among different age groups (58), Kedia et al. showed that the UC microbiome varies across categories of disease severity (59), and multiple groups have shown associations between CD flare localization and microbiota composition (38, 60).”
Diet, Gut Microbiome, and Their End Metabolites Associate With Acute Pancreatitis Risk
Yazıcı, C., Thaker, S., Castellanos, K., Rashdan, H., Huang, Y., Sarraf, P., Boulay, B. R., Grippo, P. J., Gaskins, H. R., Danielson, K. K., et al. (2023) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000597 · Cited by 16
O’Toole, P. W. (2024) · Microbial Biotechnology · doi:10.1111/1751-7915.14477 · Cited by 14
“…unhealthy ageing, and while direct evidence for mechanisms is still lacking, these taxa have been linked to the production of metabolites including deoxycholic and lithoc-olic acids, para-cresol, ethanol, acetone, ammonia and trimethylamine (Ghosh, Das, et al., 2020; Ghosh, Rampelli et al., 2020).”
BackgroundInfluentialSelf-citationHealthy and Unhealthy Aging and the Human Microbiome
Simbirtseva, K., & O’Toole, P. W. (2024) · Annual Review of Medicine · doi:10.1146/annurev-med-042423-042542 · Cited by 16
Self-citationAntioxidant Potential of Xanthohumol in Disease Prevention: Evidence from Human and Animal Studies
Piekara, J., & Piasecka‐Kwiatkowska, D. (2024) · Antioxidants · doi:10.3390/antiox13121559 · Cited by 16
“The formation of the intestinal microbiome as a result of antibiotic therapy, an un-healthy lifestyle and a given stage of life, and even the method of birth and lactation, may predispose to the development of food intolerances and allergies, gastrointestinal diseases, and even cancer [75–77].”
Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
Cai, P., Xiong, J., Sha, H., Dai, X., & Lü, J. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1123544 · Cited by 15
“The gut microbiotas are significantly varied as over human lifetime (Falony et al., 2016; Greenhalgh et al., 2016; Ghosh et al., 2020), thus a key challenge is to distinguish the alterations in microbial assembly over CRC progression from these as human aged.”
BackgroundAging Gut Microbiome in Healthy and Unhealthy Aging
Yangyanqiu, W., Qu, Z., Chu, J., & Han, S. (2024) · Aging and Disease · doi:10.14336/ad.2024.0331 · Cited by 17
“An imbalanced gut microbiota can trigger abnormal immune responses, increasing the risk of inflammatory gastrointestinal diseases or diabetes [28-32].”
Yang, Z., Yang, M., Deehan, E. C., Cai, C., Madsen, K. L., Wine, E., Li, G., Li, J., Liu, J., & Zhang, Z. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2387796 · Cited by 17
“186 Studies should account for variation in other confounding variables such as demographics (age 187 and gender 188 ) and lifestyle factors (such as habitual diet).”
BackgroundFood for healthier aging: power on your plate
Mafra, D., Ugochukwu, S. A., Borges, N. A., Cardozo, L., Stenvinkel, P., & Shiels, P. G. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2107611 · Cited by 15
“A recent meta-analysis with metage-nomics datasets to evaluate possible interactions between age and the microbiome in different diseases concluded that age is a major confounder in studies linking the microbiome to disease (Ghosh et al. 2020).”
MethodColorectal microbiota after removal of colorectal cancer
Cronin, P., Murphy, C. L., Barrett, M., Ghosh, T. S., Pellanda, P., O’Connor, E. M., Zulquernain, S. A., Kileen, S., McCourt, M., Andrews, E. J., et al. (2022) · NAR Cancer · doi:10.1093/narcan/zcac011 · Cited by 14
Self-citationZhang, F., Zhang, X., Fu, J., Duan, Z., Qiu, W., Cai, Y., Ma, W., Zhou, H., Chen, Y., Zheng, J., et al. (2023) · Microorganisms · doi:10.3390/microorganisms11082087 · Cited by 14
“A previous report found that the aging-associated microbiome masked the microbial signatures of colorectal cancer because of the interaction between the cancer microbiome and aging [24].”
BackgroundQiao, C., He, M., Wang, S., Jiang, X., Wang, F., Li, X., Tan, S., Chao, Z., Xin, W., Gao, S., et al. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1250891 · Cited by 14
“For example, alterations in the gut microbiota have been linked to age-related diseases such as type 2 diabetes, cardiovascular disease, and cognitive decline (Pascale et al., 2019; Ghosh et al., 2020; Pellanda et al., 2021).”
BackgroundDisease-associated microbiome signature species in the gut
Li, J., & O’Toole, P. W. (2024) · PNAS Nexus · doi:10.1093/pnasnexus/pgae352 · Cited by 15
“…signa - ture species include many of the “usual suspects” identified across multiple noncommunicable diseases with microbiome alterations (5, 26, 27), characterized by a depletion of short-chain fatty acid producers and an enrichment of opportunistic pathogens in diseases (Table S1), while…”
BackgroundSelf-citationTranslating the Microbiome: What’s the Target?
O’Toole, P. W., Ghosh, T. S., Goswami, S., Manghi, P., Segata, N., & Shanahan, F. (2023) · Gastroenterology · doi:10.1053/j.gastro.2023.04.008 · Cited by 12
Self-citationNon-Genomic Hallmarks of Aging—The Review
Holmannová, D., Borský, P., Kovaříková, H., Štveráková, T., Vošmik, M., Hruška, L., Fiala, Z., & Borská, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015468 · Cited by 13
“Certain bacterial species seem to promote longevity [215].”
BackgroundGut microb-aging and its relevance to frailty aging
Cosquer, G. L., Vergnolle, N., & Motta, J. (2024) · Microbes and Infection · doi:10.1016/j.micinf.2024.105309 · Cited by 16
Changes in M6A methylation: A key factor in the vicious cycle of flora -gut aging
Ding, M., Yan, J., Chen, Y., Liu, J., Chao, G., & Zhang, S. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102351 · Cited by 12
Normal Gut Microbiomes in Diverse Populations: Clinical Implications
Shete, O., & Ghosh, T. S. (2024) · Annual Review of Medicine · doi:10.1146/annurev-med-051223-031809 · Cited by 12
Self-citationNakazeko, T., Shobako, N., Shioya, N., Iwama, Y., Hirano, Y., Fujii, S., Nakamura, F., & Honda, K. (2023) · Nutrients · doi:10.3390/nu15204317 · Cited by 11
Dai, L., Schurgers, L., Shiels, P. G., & Stenvinkel, P. (2021) · Clinical Science · doi:10.1042/cs20201452 · Cited by 11
Role of gene regulation and inter species interaction as a key factor in gut microbiota adaptation
Gao, S., Khan, M. I., Kalsoom, F., Liu, Z., Chen, Y., & Chen, Z. (2022) · Archives of Microbiology · doi:10.1007/s00203-022-02935-5 · Cited by 11
“When the organism has a trend to lose microbiota diversity, it more likely leads to gut dysbiosis, subsequently making the immune system unable to cope with the challenges of different factors that promote cancer occurrence (Galloway-Pena et al. 2017; Ghosh et al. 2020; Low et al. 2020; Chen et al. 2021).”
BackgroundIdentification of age-associated microbial changes via long-read 16S sequencing
Toh, K. Y., Toh, T. S., Chua, K. P., Rajakumar, P. D., Lee, J. W. J., & Chong, C. W. (2024) · Gut Pathogens · doi:10.1186/s13099-024-00650-8 · Cited by 9
“Following the age cut-offs used by several prior studies [9, 26, 27], participants were grouped into different age groups, as follows: (1) young (age < 36; n = 25), (2) middle-aged (36 ≤ age < 56; n = 30), and (3) old (age ≥ 56; n = 28).”
MethodLi, Y., Gong, Q., He, W., & Ke, J. (2025) · BMC Geriatrics · doi:10.1186/s12877-025-05725-y · Cited by 10
Gut microbiome dynamics and functional shifts in healthy aging: insights from a metagenomic study
Ai, X., Huang, C., Liu, Q.-T., Duan, R., Ma, X., Li, L.-Z., Shu, Z., Miao, Y., Shen, H., Lv, Y., et al. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1629811 · Cited by 13
The nonindustrialised microbiome in a modern world
Shanahan, F., Ghosh, T. S., Molloy, M. G., & O’Toole, P. W. (2022) · Clinical Science · doi:10.1042/cs20220203 · Cited by 10
Self-citationHrubesz, G., Leigh, J., & Ng, T. L. (2024) · Translational Breast Cancer Research · doi:10.21037/tbcr-24-14 · Cited by 10
Ruiz‐Rico, M., Ye, H., O’Callaghan, T. F., O’Toole, P. W., & McCarthy, E. K. (2025) · PLoS ONE · doi:10.1371/journal.pone.0332631 · Cited by 8
“Our research group previously identified a group of taxa whose loss was associated with multiple pathological changes in the elderly and was distinct from that of healthy young/middle-aged individuals [21].”
Self-citationThe Gut Microbiome in Aging and Ovarian Cancer
Dominique, G. M., Hammond, C., & Stack, M. S. (2024) · Aging and Cancer · doi:10.1002/aac2.12071 · Cited by 8
“The first means of improvement of the gut microbiome in any situation is to increase consumption of fresh vegetables, as these contain large amounts of dietary fiber that feed desirable gut commensals [32, 92–95].”
BackgroundWang, H., Chen, Y., Han, Y., Mu, S., Wei, W., Lan, L., Li, X., Xiang, H., Tong, C., & Du, S. (2024) · Microbial Pathogenesis · doi:10.1016/j.micpath.2024.107030 · Cited by 8
Identifying fecal microbiota signatures of colorectal cancer in a Vietnamese cohort
Nhung, P. H., Le, H. T. T., Nguyen, Q. H., Huyen, D. T., Quyền, Đ. V., Song, L. H., Thuân, T. V., & Tran, T. T. T. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1388740 · Cited by 10
González, A., Fullaondo, A., & Odriozola, A. (2025) · Nutrients · doi:10.3390/nu17111877 · Cited by 8
“Although Sutterella has been reported as reduced in T2D, it is not included because it is a pro-inflammatory bacterium [36,44,45].”
Jonduo, M., Wawae, L., Masiria, G., Suda, W., Hattori, M., Takayasu, L., Abdad, M. Y., Greenhill, A. R., Horwood, P. F., Pomat, W. S., et al. (2020) · FEMS Microbiology Letters · doi:10.1093/femsle/fnaa161 · Cited by 7
Heterochronic Fecal Microbiota Transfer Reverses Hallmarks of the Aging Murine Gut, Eye and BrainPreprint
Parker, A., Romano, S., Ansorge, R., Aboelnoer, A., Gall, G. L., Savva, G. M., Telatin, A., Jones, E. J., Baker, D., Rudder, S. J., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3811833 · Cited by 8
Sorbie, A., Jiménez, R. D., & Benakis, C. (2022) · iScience · doi:10.1016/j.isci.2022.103998 · Cited by 7
“…however, are highly complex and high-dimensional, and affected by a multitude of confounding factors; thus, careful consideration of sample collection, study design, and bioinformatic analysis is necessary to ensure robust and reproducible results (Ghosh et al., 2020; Vujkovic-Cvijin et al., 2020).”
BackgroundInfluentialBajaj, A., Markandey, M., Samal, A., Goswami, S., Vuyyuru, S. K., Mohta, S., Kante, B., Kumar, P., Makharia, G., Kedia, S., et al. (2024) · Gut Pathogens · doi:10.1186/s13099-024-00654-4 · Cited by 7
“The inference of metabolic profiles for each gut micro-biome was performed using methods as described in previous studies [41, 42].”
MethodSelf-citationCharacteristics of tongue images and tongue coating bacteria in patients with colorectal cancer
Zheng, W., Wu, Y., Chu, J., Congjian, J., Zhanbo, Q., Nianga, J.-M., Wang, L., Zefeng, W., Jiaqun, H., Xiaojian, Y., et al. (2025) · BMC Microbiology · doi:10.1186/s12866-025-04014-3 · Cited by 8
“This genus’ significance extends beyond CRC, as it has been implicated in aging processes [53].”
Aznou, A., Drenth, J. P. H., Nieuwdorp, M., & Meijnikman, A. S. (2025) · Yearbook of pediatric endocrinology · doi:10.1210/jendso/bvaf130 · Cited by 8
“In healthy aging, increased microbial uniqueness and a reduction in core taxa such as Bacteroides are associated with anti-inflammatory compounds that promote autophagy and metabolic resilience [103].”
Baraille, M., Buttet, M., Grimm, P., Milojevic, V., Julliand, S., & Julliand, V. (2024) · PLoS ONE · doi:10.1371/journal.pone.0303029 · Cited by 7
Gut metagenomic features of frailty
Jarmukhanov, Z., Mukhanbetzhanov, N., Vinogradova, E. B., Kozhakhmetov, S., & Kushugulova, A. R. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1486579 · Cited by 6
“This observation aligns with recent studies suggesting that a loss in microbial diversity is a characteristic offrailty, potentially leading to systemic in fl ammation and metabolic dysregulation (Ghosh et al., 2020; Larson et al., 2022; Lim and Nam, 2023).”
Zheng, S., Lou, Y., Zhang, J., Wang, Y., & Lv, L. (2024) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2024.105741 · Cited by 6
Li, X., Zhang, B., Zheng, J., Chen, H., Zheng, J., Xu, X., Wang, W., Sun, C. M., Lin, W., Chen, K., et al. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01076-22 · Cited by 6
“As a result, individuals gradually acquire disease-related flora characteristics and gradually lose health-related flora characteristics (27).”
BackgroundDissecting the Ecological Structure of Health and Disease in the Global Gut Microbiome
Zhu, B., Chen, S., Diao, Y., Wang, W., Huang, Y., Liang, L., Lu, X., Han, R., Guo, M., Li, Z., et al. (2026) · Advanced Science · doi:10.1002/advs.202517087 · Cited by 5
“We further validated that MEFs derived from Wiredancer exhibit high stability in age-related changes [ 53, 54 ], inter-individual variability, and ecological transition patterns between healthy and unhealthy states.”
You, Q., Wang, K., Zhao, Z., Zhou, H., Lan, Z., Liang, H., Deng, R., Li, W., Shen, S., Wang, R., et al. (2025) · Journal of Medical Virology · doi:10.1002/jmv.70395 · Cited by 5
Forging the microbiome to help us live long and prosper
Rock, R. R., & Turnbaugh, P. J. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002087 · Cited by 5
“Recent investigation supports that host age contributes to differences between disease-associated microbiomes and those of healthy individuals [57].”
BackgroundGut Microbes: The Gut Brain Connection
Lynch, C. M. K., O’Riordan, K. J., Clarke, G. A., & Cryan, J. F. (2023) · Springer eBooks · doi:10.1007/978-3-031-46712-7_4 · Cited by 5
The influence of aging and the microbiome in multiple sclerosis and other neurologic diseases
Fettig, N. M., Pu, A., Osborne, L. C., & Gommerman, J. L. (2024) · Immunological Reviews · doi:10.1111/imr.13361 · Cited by 7
“26 When individuals were further stratified by the presence or absence of various comorbidities such as colorectal cancer, inflammatory bowel disease, or type 2 diabetes, disease-associated microbial signatures were significantly different within each age group, highlighting a complex interplay of…”
InfluentialMacCann, R., Li, J., Leon, A. A. G., Negi, R., Alalwan, D., Tinago, W., McGettrick, P., Cotter, A. G., LANDAY, A. L., Sabin, C. A., et al. (2025) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiaf043 · Cited by 4
“Meta-analysis also shows that increased abundance of oral microbes is associated with unhealthy aging, suggesting that microbial shifts in the oral cavity can contribute to inflammation and chronic diseases associated with aging [46].”
Self-citationMicrobe–Diet Interactions and Personalized Nutrition
Kujawska, M., & Hall, L. J. (2025) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-111523-121845 · Cited by 4
Gut microbiota associates with frailty in older women
Geraldi, M. V., Dwibedi, C. K., Jaiswal, R., Gregori, G., Zhou, X., Lv, B., Zheng, Y., Wang, X., Wu, H., Axelsson, K. F., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-75176-5 · Cited by 4
“Besides that, other FMI-associated species like E. citroniae , E. clostridioformis , E. asparagiformis , C. innocuum , E. lenta, Ruminococcus gnavus and Fla-vonifractor plautii were also previously identi fi ed as unhealthy aging markers 22,26 .”
InfluentialMohr, A. E., Jasbi, P., van Woerden, I., Chi, J., Gu, H., Bruening, M. M., & Whisner, C. M. (2024) · Gut Microbes Reports · doi:10.1080/29933935.2024.2387936 · Cited by 4
“45 78 Eubacterium ventriosum has been observed to decrease in centenarians 79 and is proposed as a biomarker for low risk of colorectal cancer, showing significant enrichment in healthy individuals compared to those with colorectal cancer in diverse populations.”
Gut microbiota in melanoma: Effects and pathogeneses
Liu, W., Yang, X., Zhou, Y., Huang, Z., & Huang, J. H. (2025) · Microbiological Research · doi:10.1016/j.micres.2025.128144 · Cited by 4
Hao, J., Li, Y., Yu, Y., Zheng, L., & Feng, F. (2023) · BMC Microbiology · doi:10.1186/s12866-023-02801-4 · Cited by 4
van Loenen, M. R., Remie, L. B., van Trijp, M. P. H., Jansen, M. G., Marques, J. P., Claassen, J. A. H. R., van de Rest, O., Vermeiren, Y., Smidt, N., Sikkes, S. A. M., et al. (2025) · JMIR Research Protocols · doi:10.2196/69814 · Cited by 8
“Dysbiosis of the gut microbiome can potentially impair the integrity of the intestinal barrier [77], thereby provoking a local inflammatory reaction that could eventually lead to systemic inflammation [78].”
Tekin, B., & Gurbanov, R. (2026) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-026-05017-6 · Cited by 4
“At the metabolite level, frailty is consistently associated with decreased SCFAs, primary BAs, and tryptophan metabolites, coupled with increased TMAO, SBA, PCS, and methylglyoxal, indicating broad inflammatory, endothelial, and metabolic stress (Ghosh et al. 2020; He et al. 2020).”
Psychobiotics in Health, Longevity, and Neurological Disorders
Mohankumar, A., Kalaiselvi, D., Thiruppathi, G., Patteswari, D., Tawata, S., & Sundararaj, P. (2022) · Nutritional neurosciences · doi:10.1007/978-981-16-8158-5_2 · Cited by 3
Emerging tools for understanding the human microbiome
Ghosh, T. S., & Das, M. (2022) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2022.06.027 · Cited by 3
Self-citationHuang, G., Mao, Y., Zhang, W., Luo, Q., Xie, R., Huang, D., & Liang, Y. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1265028 · Cited by 3
Oral Microbial Translocation Genes in Gastrointestinal Cancers: Insights from Metagenomic Analysis
Wang, L., Wang, Q., & Zhou, Y. (2024) · Microorganisms · doi:10.3390/microorganisms12102086 · Cited by 4
“Colorectal cancer (CRC) and inflammatory bowel disease (IBD) are prevalent gastrointestinal conditions, with emerging evidence suggesting a link between their development and alterations in the gastrointestinal microbiota [8,14,15,56].”
BackgroundFecal microbiota transplantation for glaucoma; a potential emerging treatment strategy
Ebrahimi, R., Farsi, Y., & Nejadghaderi, S. A. (2024) · Current Research in Microbial Sciences · doi:10.1016/j.crmicr.2024.100314 · Cited by 4
On the Gut Microbiome as a Central Player in Aging: Mechanisms and Health Outcomes
Melnitskaia, A. A., Matchekhina, L. V., Константиновна, И. А., & Strazhesko, I. D. (2024) · Advances in Gerontology · doi:10.1134/s207905702560003x · Cited by 2
“…composition and functional possibilities of the microbiome change with aging, which can lead to the development of chronic inflammatory processes associated with the progression of age-associated diseases such as cardiovascular diseases, metabolic disorders, and neurodegenerative disorders [5–7].”
Faitová, T., Ilett, E. E., da Cunha‐Bang, C., Sengeløv, H., Brieghel, C., Gülay, A., Rafiq, S., Ravn, H. B., Zheng, C., Nielsen, R. V., et al. (2025) · Microbiology Spectrum · doi:10.1128/spectrum.00944-25 · Cited by 3
“However, this resemblance may also be partly age-related, as previous studies in type 2 diabetes and colorectal cancer showed age explained more microbiome variation than the disease itself (46).”
Gan, Y., Ning, R., Zhang, W., Xu, Y., Zhang, S., Zhang, Z., Xia, J., Dai, M., & Guo, W. (2025) · BMC Microbiology · doi:10.1186/s12866-025-04650-9 · Cited by 2
“Consistent with studies in other diseases, predictive models trained within age-homogeneous cohorts often achieve superior discriminatory power compared to those developed from mixed-age populations [60].”
Hashmi, M. A., Verma, S., Math, R. G. H., Muralidharan, S., Pranesh, G., Sahana, M. P., Hariharan, N., C, M., Kamath, V., Yaligod, V., et al. (2026) · Scientific Reports · doi:10.1038/s41598-026-35476-8 · Cited by 2
“Nine taxa, including Methanosaeta concilii , Bacteroides sartorii , Atopostipes suicloacalis , and Pseudomonas caeni , showed strong positive correlations with spermidine, a polyamine implicated in aging and autophagy 29.”
Self-citationPeng, L., Zhang, Z., Hu, Y., Chen, H., Tian, Y., & Ling, H. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1706811 · Cited by 2
Global trend of colorectal cancer, prevention, and control in China: challenges and strategies
Chen, H., Wang, Z., Yu, Y., Qiu, M., Yang, L., Meng, W., Wang, C., Li, Y., Li, L., Xu, H., et al. (2022) · Scientia Sinica Vitae · doi:10.1360/ssv-2022-0166 · Cited by 2
Hein, D., Coughlin, L. A., Poulides, N. A., Koh, A. Y., & Sanford, N. N. (2024) · Journal of Immunotherapy and Precision Oncology · doi:10.36401/jipo-23-30 · Cited by 2
“[10] Multiple studies have compared microbiome composition in early-versus aver-age-onset CRC to determine whether microbiome profiles can serve as a diagnostic biomarker and have prognostic or predictive value.”
BackgroundResultCalderón-Romero, P., Valderrama, B., Bastiaanssen, T. F. S., Lillo, P., Thumala, D., Clarke, G. A., Cryan, J. F., Slachevsky, A., González-Billault, C. E., & Court, F. A. (2026) · PLoS ONE · doi:10.1371/journal.pone.0343493 · Cited by 2
“Our results also suggested that female participants showed an increased potential to synthesise p-cresol (Fig 3A), a molecule whose abundance in the stool of aged humans has been linked with increased frailty in the ELDERMET cohort [82].”
Integrating cuproptosis and immunosenescence: A novel therapeutic strategy in cancer treatment
Firouzjaei, A. A., & Aghaee‐Bakhtiari, S. H. (2025) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2025.101983 · Cited by 4
“However, age-associated alterations in gut function, increased inflammation, and comorbidities can further disrupt this delicate balance, exacerbating immune senescence [234].”
Zou, H., Zhu, T., Chen, X., & Lu, Y. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1606922 · Cited by 2
Microbiome of Young and Later-Onset Colorectal Cancer
Galbraith, N. J., & White, M. G. (2025) · Surgical Clinics of North America · doi:10.1016/j.suc.2025.06.002 · Cited by 2
Gastrointestinal Physiology and Aging
Pitchumoni, C. S. (2021) · Springer eBooks · doi:10.1007/978-3-319-90761-1_6-1 · Cited by 2
Wang, D., Russel, W. A., Macdonald, K. M., Leon, V. M. D., Ay, A. A., & Belanger, K. D. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1272711 · Cited by 2
“Health status and environmental factors are likely better predictors of microbiome composition than age (82, 83), or at least must be taken into account when considering the complex interactions between aging and gut microbiota (84, 85).”
BackgroundAlmeida, A. S., Tran, T. T. T., Ghosh, T. S., Ribière, C., Foley, C., Azevedo, L. A., Pellanda, P., Frei, W., Hueston, C. M., Kumar, R. S., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.24.432654 · Cited by 2
Self-citationShiels, P. G. (2023) · Journal of Internal Medicine · doi:10.1111/joim.13691 · Cited by 2
van Loenen, M. R., Remie, L. B., van Trijp, M. P. H., Jansen, M. G., Marques, J. P., Claassen, J. A. H. R., van de Rest, O., Vermeiren, Y., Smidt, N., Sikkes, S. A. M., et al. (2024) · doi:10.2196/preprints.69814 · Cited by 2
The gut microbiome as a central player in aging: mechanisms and health outcomes
Melnitskaia, A. A., Matchekhina, L. V., Константиновна, И. А., & Strazhesko, I. D. (2024) · Problems of Geroscience · doi:10.37586/2949-4745-3-2024-154-160 · Cited by 2
Vulcănescu, D. D., Bagiu, I. C., Șușan, M. M., Sorop, V. B., Harich, O. O., Oprisoni, A. L., Galiș, R., & Horhat, F. G. (2025) · Children · doi:10.3390/children12091258 · Cited by 1
Seyoum, Y., de Lucia, C., Khalifa, K. N., Bergland, A. K., Aarsland, D., & van der Giezen, M. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2570862 · Cited by 1
Mechanistic advances and emerging technologies redefining lung aging research
Wheeler, L. F., Lehmann, M., & Melo-Narváez, M. C. (2026) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00912.2025 · Cited by 1
The human gut microbiome across the life course
Ponsero, A. J., Bahcivanci, B., Hayhoe, A., Acharjee, A., & Özkurt, E. (2026) · FEBS Letters · doi:10.1002/1873-3468.70361 · Cited by 1
Dutta, S., Dutta, T. K., Nanda, P. K., Dhar, P., Das, A. K., & Bhunia, A. K. (2026) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-026-11136-1 · Cited by 2
Ni, Z., Xie, J., Zhang, Z., Zhang, K., Ding, J., Chang, M., Su, Y., Zhang, Y., Yao, M., Wang, C., et al. (2026) · iMeta · doi:10.1002/imt2.70148 · Cited by 1
The Changing Demographics of Colorectal Cancer
Lo, J. H.-J., & Ciombor, K. K. (2022) · Advances in Oncology · doi:10.1016/j.yao.2022.02.008 · Cited by 1
Individualizing Pharmacogenomic Test Results in the Context of the Microbiome
Haga, S. B. (2020) · Personalized Medicine · doi:10.2217/pme-2020-0077 · Cited by 2
Gastrointestinal Physiology and Aging
Pitchumoni, C. S. (2021) · Springer eBooks · doi:10.1007/978-3-030-30192-7_6 · Cited by 1
Lactobacillus rhamnosus CBT-LR5 Improves Lipid Metabolism by Enhancing Vitamin Absorption
Kim, D.-J., Kim, T. Y., Yoon, Y.-S., Ryu, Y., & Chung, M. J. (2022) · Microbiology and Biotechnology Letters · doi:10.48022/mbl.2208.08008 · Cited by 1
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Self-citation
Metadata
- Authors
- Ghosh, T. S., Das, M., Jeffery, I. B., & O'Toole, P. W.
- Affiliations
- University College Cork (IE)
- APC Microbiome Ireland, University College Cork, Cork, Ireland
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2020-03-11
- Volume
- 9
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC7065848
- OpenAlex
- W3011436618
- Cited by
- 233
- References
- 45
- Citations by year
- 2026: 30 · 2025: 29 · 2024: 56 · 2023: 38 · 2022: 37 · 2021: 23 · 2020: 20
- FWCI
- 9.65
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Lenus, The Irish Health Repository (Dr Steevens Hospital Library) (submittedVersion)
- Funders
- Science Foundation Ireland (APC/SFI/12/RC/2273, 13/SIRG/2128)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- gut microbiota, aging, age adjustment, colorectal cancer, frailty, multi-cohort analysis
- MeSH terms
- Gastrointestinal Microbiome, Adult, Age Factors, Aged, Aged, 80 and over, Data Interpretation, Statistical, Disease Susceptibility, Female, Humans, Male, Middle Aged, Reproducibility of Results, Computational Biology, Metagenome, Young Adult, Metagenomics, Microbiota, Dysbiosis
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