Altered Microbiomes Distinguish Alzheimer’s Disease from Amnestic Mild Cognitive Impairment and Health in a Chinese Cohort
Open accessAbstract
OBJECTIVE: (Background): Alzheimer's disease (AD), clinically characterized by the progressive neurodegenerative condition and cognitive impairment, is one of the main causes of disability in elder people worldwide. Recently, several animal studies indicated that the 'gut-brain' axis might contribute to the amyloid deposition of AD. However, data about gut dysbiosis in human AD remains scarce in the literature, especially including the whole process of AD. In this prospective and cross-sectional study, we aimed at identifying differences in microbiome between patients with AD (Pre-onset stage amnestic mild cognitive impairment, aMCI; and AD) and the normal cognition healthy controls (HC). Additionally, the potential association between IM and clinical characteristics of AD was evaluated. METHODS: A total of 97 subjects (33 AD, 32 aMCI, and 32 HC) were recruited in the study. The composition of gut bacterial communities was determined by 16S ribosomal RNA Miseq sequencing. In addition, Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) was used to predict function shift of intestinal microbiota. The Mini-Mental State Examination (MMSE), Montreal Cognitive Assessment (MoCA) or Clinical Dementia Rating (CDR) scores were used to evaluate the severity of cognitive impairment in patients. RESULTS: The fecal microbial diversity was decreased in AD patients compared with aMCI patients and HC. And the microbial composition was distinct among aMCI, AD and healthy control groups. Among bacterial taxa, the proportion of phylum Firmicutes was significantly reduced (P = 0.008), whereas Proteobacteria (P = 0.024) was highly enriched in the AD compared with HC. In addition, similar alterations were observed at the order, class and family levels of these two phyla. And Gammaproteobacteria, Enterobacteriales and Enterobacteriaceae showed a progressive enriched prevalence from HC to aMCI and AD patients. Further, a significant correlation was observed between the clinical severity scores of AD patients and the abundance of altered microbiomes. Moreover, the KEGG results showed the increased modules related to glycan biosynthesis and metabolism in AD and aMCI patients and decreased pathways related to immune system in AD patients. Importantly, the discriminating models based on predominant microbiota could effectively distinguish aMCI and AD from HC (AUC = 0.890, 0.940, respectively), and also AD from aMCI (AUC = 0.925). Notably, the models based on the abundance of family Enterobacteriaceae could distinguish AD from both aMCI (AUC = 0.688) and HC (AUC = 0.698). CONCLUSIONS: Distinct microbial communities, especially enriched Enterobacteriaceae, were associated with patients with AD when compared with predementia stage aMCI and healthy subjects. These novel findings will give new clues to understand the disease and provide new therapeutic target for intervention or a marker for this disease.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Enterobacteriaceae is thought to be implicated in both PD and AD.
“Furthermore, we found that MPTP-treated mice presented elevated levels of Enterobacteriaceae (Figure 5), which is thought to be implicated in both PD and AD [68].”
From Neuroprotective Effects of Bifidobacterium breve CCFM1067 in MPTP-Induced Mouse Models of Parkinson’s Disease (2022) · cites this paper as [68]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,841 · see citing works
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624 · see citing works
Self-citationThe Clinical Dementia Rating (CDR): Current version and scoring rules
Morris, J. C. (1993) · Neurology · doi:10.1212/wnl.43.11.2412-a · Cited by 9,882 · see citing works
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
Langille, M. G. I., Zaneveld, J., Caporaso, J. G., McDonald, D., Knights, D., Reyes, J. A., Clemente, J. C., Burkepile, D. E., Vega Thurber, R. L., Knight, R., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2676 · Cited by 9,116 · see citing works
Mild cognitive impairment as a diagnostic entity
Petersen, R. C. (2004) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2004.01388.x · Cited by 7,864 · see citing works
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823 · see citing works
Sperling, R. A., Aisen, P. S., Beckett, L. A., Bennett, D. A., Craft, S., Fagan, A. M., Iwatsubo, T., Jack, C. R., Kaye, J., Montine, T. J., et al. (2011) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.03.003 · Cited by 7,155 · see citing works
Richness of human gut microbiome correlates with metabolic markers
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.-M., Kennedy, S., et al. (2013) · Nature · doi:10.1038/nature12506 · Cited by 4,662 · see citing works
Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS–ADRDA criteria
Dubois, B., Feldman, H. H., Jacova, C., DeKosky, S. T., Barberger-Gateau, P., Cummings, J., Delacourte, A., Galasko, D., Gauthier, S., Jicha, G., et al. (2007) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70178-3 · Cited by 4,411 · see citing works
Advancing research diagnostic criteria for Alzheimer's disease: the IWG-2 criteria
Dubois, B., Feldman, H. H., Jacova, C., Hampel, H., Molinuevo, J. L., Blennow, K., DeKosky, S. T., Gauthier, S., Selkoe, D., Bateman, R., et al. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70090-0 · Cited by 3,321 · see citing works
Role of the normal gut microbiota
Jandhyala, S. M. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i29.8787 · Cited by 3,001 · see citing works
Gut Microbiota in Human Adults with Type 2 Diabetes Differs from Non-Diabetic Adults
Larsen, N., Vogensen, F. K., van den Berg, F. W. J., Nielsen, D. S., Andreasen, A. S., Pedersen, B. K., Al-Soud, W. A., Sørensen, S. J., Hansen, L. H., & Jakobsen, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009085 · Cited by 2,952 · see citing works
Diagnostic and Statistical Manual of Mental Disorders
Raber, G., & Spokas, M. (2024) · doi:10.4135/9781071886229.n145 · Cited by 2,806 · see citing works
Microbiota and SCFA in lean and overweight healthy subjects
Schwiertz, A., Taras, D., Schäfer, K., Beijer, S., Bos, N. A., Donus, C., & Hardt, P. D. (2010) · Obesity · doi:10.1038/oby.2009.167 · Cited by 2,457 · see citing works
Altered fecal microbiota composition in patients with major depressive disorder
Jiang, H., Ling, Z., Zhang, Y., Mao, H., Ma, Z., Yin, Y., Wang, W., Tang, W., Tan, Z., Shi, J., et al. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.03.016 · Cited by 2,275 · see citing works
Self-citationAlterations 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 · see citing works
Self-citationGut microbiome alterations in Alzheimer’s disease
Vogt, N. M., Kerby, R. L., Dill-McFarland, K. A., Harding, S. J., Merluzzi, A. P., Johnson, S. C., Carlsson, C. M., Asthana, S., Zetterberg, H., Blennow, K., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-13601-y · Cited by 2,137 · see citing works
The neuroactive potential of the human gut microbiota in quality of life and depression
Valles-Colomer, M., Falony, G., Darzi, Y., Tigchelaar, E. F., Wang, J., Tito, R. Y., Schiweck, C., Kurilshikov, A., Joossens, M., Wijmenga, C., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-018-0337-x · Cited by 1,963 · see citing works
Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age
Mariat, D., Firmesse, O., Levenez, F., Guimarăes, V., Sokol, H., Doré, J., Corthier, G., & Furet, J.-P. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-123 · Cited by 1,755 · see citing works
The central nervous system and the gut microbiome
Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016) · Cell · doi:10.1016/j.cell.2016.10.027 · Cited by 1,513 · see citing works
A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites
Dodd, D., Spitzer, M. H., Van Treuren, W., Merrill, B. D., Hryckowian, A. J., Higginbottom, S. K., Le, A., Cowan, T. M., Nolan, G. P., Fischbach, M. A., et al. (2017) · Nature · doi:10.1038/nature24661 · Cited by 1,425 · see citing works
Cattaneo, A., Cattane, N., Galluzzi, S., Provasi, S., Lopizzo, N., Festari, C., Ferrari, C., Guerra, U. P., Paghera, B., Muscio, C., et al. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.08.019 · Cited by 1,382 · see citing works
Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342 · see citing works
Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs
Olson, J. K., & Miller, S. D. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.6.3916 · Cited by 1,215 · see citing works
Kelly, J. R., Kennedy, P. J., Cryan, J. F., Dinan, T. G., Clarke, G., & Hyland, N. P. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00392 · Cited by 1,110 · see citing works
Characterization of fecal microbial communities in patients with liver cirrhosis
Chen, Y., Yang, F., Lu, H., Wang, B., Chen, Y., Lei, D., Wang, Y., Zhu, B., & Li, L. (2011) · Hepatology · doi:10.1002/hep.24423 · Cited by 1,038 · see citing works
Self-citationThe role of the gut microbiota in NAFLD
Leung, C., Rivera, L., Furness, J. B., & Angus, P. W. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.85 · Cited by 1,020 · see citing works
Akbari, E., Asemi, Z., Daneshvar Kakhaki, R., Bahmani, F., Kouchaki, E., Tamtaji, O. R., Hamidi, G. A., & Salami, M. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00256 · Cited by 946 · see citing works
Identifying biologically relevant differences between metagenomic communities
Parks, D. H., & Beiko, R. G. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq041 · Cited by 942 · see citing works
Bacterial infection causes stress-induced memory dysfunction in mice
Gareau, M. G., Wine, E., Rodrigues, D. M., Cho, J. H., Whary, M. T., Philpott, D. J., MacQueen, G., & Sherman, P. M. (2011) · Gut · doi:10.1136/gut.2009.202515 · Cited by 909 · see citing works
Microbiota and diabetes: an evolving relationship
Tilg, H., & Moschen, A. R. (2014) · Gut · doi:10.1136/gutjnl-2014-306928 · Cited by 853 · see citing works
The Gut Microbiota and Alzheimer’s Disease
Jiang, C., Li, G., Huang, P., Liu, Z., & Zhao, B. (2017) · Journal of Alzheimer's Disease · doi:10.3233/jad-161141 · Cited by 852 · see citing works
Ren, Z., Li, A., Jiang, J., Zhou, L., Yu, Z., Lu, H., Xie, H., Chen, X., Shao, L., Zhang, R., et al. (2018) · Gut · doi:10.1136/gutjnl-2017-315084 · Cited by 770 · see citing works
Self-citationGram-negative bacterial molecules associate with Alzheimer disease pathology
Zhan, X., Stamova, B., Jin, L.-W., DeCarli, C., Phinney, B., & Sharp, F. R. (2016) · Neurology · doi:10.1212/wnl.0000000000003391 · Cited by 521 · see citing works
Analysis of Gut Microbiota in Patients with Parkinson’s Disease
Petrov, V. A., Saltykova, I. V., Zhukova, I. A., Alifirova, V. M., Zhukova, N. G., Dorofeeva, Y. B., Tyakht, A. V., Kovarsky, B. A., Alekseev, D. G., Kostryukova, E. S., et al. (2017) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-017-3700-7 · Cited by 487 · see citing works
Aberrant intestinal microbiota in individuals with prediabetes
Allin, K. H., Tremaroli, V., Caesar, R., Jensen, B. A. H., Damgaard, M. V., Bahl, M. I., Licht, T. R., Hansen, T. H., Nielsen, T., Dantoft, T. M., et al. (2018) · Diabetologia · doi:10.1007/s00125-018-4550-1 · Cited by 466 · see citing works
Molecular Characterisation of the Faecal Microbiota in Patients with Type II Diabetes
Wu, X., Ma, C., Han, L., Nawaz, M., Gao, F., Zhang, X., Yu, P., Zhao, C., Li, L., Zhou, A., et al. (2010) · Current Microbiology · doi:10.1007/s00284-010-9582-9 · Cited by 461 · see citing works
Self-citationYu, J., Li, J., & Huang, X. (2012) · BMC Psychiatry · doi:10.1186/1471-244x-12-156 · Cited by 461 · see citing works
Bonfili, L., Cecarini, V., Berardi, S., Scarpona, S., Suchodolski, J. S., Nasuti, C., Fiorini, D., Boarelli, M. C., Rossi, G., & Eleuteri, A. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-02587-2 · Cited by 453 · see citing works
Neuropeptides and the Microbiota-Gut-Brain Axis
Holzer, P., & Farzi, A. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_9 · Cited by 451 · see citing works
Altered Gut Microbiota in a Mouse Model of Alzheimer’s Disease
Zhang, L., Wang, Y., Xiayu, X., Shi, C., Chen, W., Song, N., Fu, X., Zhou, R., Xu, Y.-F., Huang, L., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170020 · Cited by 449 · see citing works
The prevalence of dementia in urban and rural areas of China
Jia, J., Wang, F., Wei, C., Zhou, A., Jia, X., Li, F., Tang, M., Chu, L., Zhou, Y.-L., Zhou, C., et al. (2013) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.01.012 · Cited by 447 · see citing works
Self-citationWillette, A. A., Bendlin, B. B., Starks, E. J., Birdsill, A. C., Johnson, S. C., Christian, B. T., Okonkwo, O. C., La Rue, A., Hermann, B. P., Koscik, R. L., et al. (2015) · JAMA Neurology · doi:10.1001/jamaneurol.2015.0613 · Cited by 418 · see citing works
Influence of gut microbiota on neuropsychiatric disorders
Cénit, M. C., Sanz, Y., & Codoñer‐Franch, P. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i30.5486 · Cited by 418 · see citing works
Chyan, Y., Pöeggeler, B., Omar, R., Chain, D. G., Frangione, B., Ghiso, J. A., & Pappolla, M. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.31.21937 · Cited by 409 · see citing works
Alteration of the fecal microbiota in Chinese patients with Parkinson’s disease
Qian, Y., Yang, X., Xu, S., Wu, C., Song, Y., Qin, N., Chen, S.-D., & Xiao, Q. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.02.016 · Cited by 409 · see citing works
Wang, B., Jiang, X., Cao, M., Ge, J., Bao, Q., Tang, L., Chen, Y., & Li, L. (2016) · Scientific Reports · doi:10.1038/srep32002 · Cited by 380 · see citing works
Self-citationMetabolic-cognitive syndrome: A cross-talk between metabolic syndrome and Alzheimer's disease
Frisardi, V., Solfrizzi, V., Seripa, D., Capurso, C. A., Santamato, A., Sancarlo, D., Vendemiale, G., Pilotto, A., & Panza, F. (2010) · Ageing Research Reviews · doi:10.1016/j.arr.2010.04.007 · Cited by 357 · see citing works
The Intestinal Metabolome: An Intersection Between Microbiota and Host
Ursell, L. K., Haiser, H. J., Treuren, W. V., Garg, N., Reddivari, L., Vanamala, J., Dorrestein, P. C., Turnbaugh, P. J., & Knight, R. D. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.03.001 · Cited by 357 · see citing works
Patterson, C. (2018) · Cited by 313 · see citing works
Neurotransmitter receptors and cognitive dysfunction in Alzheimer's disease and Parkinson's disease
Xu, Y., Yan, J., Zhou, P., Li, J., Gao, H., Xia, Y., & Wang, Q. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.02.002 · Cited by 303 · see citing works
Bonfili, L., Cecarini, V., Cuccioloni, M., Angeletti, M., Berardi, S., Scarpona, S., Rossi, G., & Eleuteri, A. M. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0973-4 · Cited by 277 · see citing works
Is the Gut Microbiota a New Factor Contributing to Obesity and Its Metabolic Disorders?
Harris, K. A., Kassis, A. N., Major, G. C., & Chou, C. J. (2012) · Journal of Obesity · doi:10.1155/2012/879151 · Cited by 274 · see citing works
Intestinal microbial dysbiosis aggravates the progression of Alzheimer’s disease in Drosophila
Wu, S.-C., Cao, Z.-S., Chang, K.-M., & Juang, J. (2017) · Nature Communications · doi:10.1038/s41467-017-00040-6 · Cited by 255 · see citing works
Köhler, C. A., Maes, M. H. J., Slyepchenko, A., Berk, M., Solmi, M., Lanctôt, K. L., & Carvalho, A. D. S. (2016) · Current Pharmaceutical Design · doi:10.2174/1381612822666160907093807 · Cited by 234 · see citing works
Mancuso, C., & Santangelo, R. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2017.12.009 · Cited by 232 · cited 2× · see citing works
“…been reported in AD transgenic mice model (Zhang et al., 2017a), and the depletion of Ruminococcus could lead to the compromised intestinal permeability, which thus facilitated the gut amyloid transferred to the systemic circulation and then accumulated in the brain (Mancuso and Santangelo, 2017).”
Lyte, M. (2014) · Gut Microbes · doi:10.4161/gmic.28682 · Cited by 225 · see citing works
Dysbiosis of small intestinal microbiota in liver cirrhosis and its association with etiology
Chen, Y., Ji, F., Guo, J., Shi, D., Fang, D., & Li, L. (2016) · Scientific Reports · doi:10.1038/srep34055 · Cited by 205 · see citing works
Self-citationCirculating metabolites and general cognitive ability and dementia: evidence from 11 cohort studies
van der Lee, S. J., Teunissen, C. E., Pool, R., Shipley, M. J., Teumer, A., Chouraki, V., Melo van Lent, D., Tynkkynen, J., Fischer, K., Hernesniemi, J., et al. (2018) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2017.11.012 · Cited by 197 · see citing works
Ling, Z., Jin, C., Xie, T., Cheng, Y., Li, L., & Wu, N. (2016) · Scientific Reports · doi:10.1038/srep30673 · Cited by 185 · see citing works
Self-citationLevey, A. I., Lah, J. J., Goldstein, F. C., Steenland, K., & Bliwise, D. L. (2006) · Clinical Therapeutics · doi:10.1016/j.clinthera.2006.07.006 · Cited by 180 · see citing works
Zhao, Y., Cong, L., Jaber, V. R., & Lukiw, W. J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01064 · Cited by 170 · see citing works
Chinese Version and Norms of the Mini-Mental State Examination
Guo, N. (1988) · Rehabilitation practice and science · doi:10.6315/3005-3846.1745 · Cited by 156 · see citing works
Relevance of gutmicrobiota in cognition, behaviour and Alzheimer’s disease
de J.R. De-Paula, V., Forlenza, A. S., & Forlenza, O. V. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.07.007 · Cited by 145 · see citing works
Zhang, Z.-H., Wu, Q., Zheng, R., Chen, C., Chen, Y., Liu, Q., Hoffmann, P. R., Ni, J., & Song, G.-L. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3229-16.2017 · Cited by 128 · see citing works
Realdon, O., Rossetto, F., Nalin, M., Baroni, I., Cabinio, M., Fioravanti, R., Saibene, F. L., Alberoni, M., Mantovani, F., Romano, M. T., et al. (2016) · BMC Psychiatry · doi:10.1186/s12888-016-1132-y · Cited by 92 · see citing works
Glucose Metabolism: A Sweet Relief of Alzheimer’s Disease
Duran-Aniotz, C. A., & Hetz, C. A. (2016) · Current Biology · doi:10.1016/j.cub.2016.07.060 · Cited by 85 · see citing works
Immunoregulatory effect of mast cells influenced by microbes in neurodegenerative diseases
Girolamo, F., Coppola, C., & Ribatti, D. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.06.017 · Cited by 60 · see citing works
de Jager, C. A., Honey, T. E. M., Birks, J., & Wilcock, G. K. (2010) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.2448 · Cited by 34 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Chen, C., Liao, J., Xia, Y., Liu, X., Jones, R., Haran, J., McCormick, B., Sampson, T. R., Alam, A., & Ye, K. (2022) · Gut · doi:10.1136/gutjnl-2021-326269 · Cited by 491 · see citing works
Fecal Microbiota Transplantation in Neurological Disorders
Vendrik, K. E. W., Ooijevaar, R. E., de Jong, P. R. C., Laman, J. D., van Oosten, B. W., van Hilten, J. J., Ducarmon, Q. R., Keller, J. J., Kuijper, E. J., & Contarino, M. F. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00098 · Cited by 413 · see citing works
β-glucan attenuates cognitive impairment via the gut-brain axis in diet-induced obese mice
Shi, H., Yu, Y., Lin, D., Zheng, P., Zhang, P., Hu, M., Wang, Q., Pan, W., Yang, X., Hu, T., et al. (2020) · Microbiome · doi:10.1186/s40168-020-00920-y · Cited by 264 · see citing works
Self-citationThe gut microbiome in Alzheimer’s disease: what we know and what remains to be explored
Chandra, S., Sisodia, S. S., & Vassar, R. J. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00595-7 · Cited by 278 · see citing works
Sun, J., Zhang, Y., Kong, Y., Ye, T., Yu, Q., Kumaran Satyanarayanan, S., Su, K.-P., & Liu, J. (2022) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2022.08.003 · Cited by 255 · see citing works
Microbiota from Alzheimer’s patients induce deficits in cognition and hippocampal neurogenesis
Grabrucker, S., Marizzoni, M., Silajdžić, E., Lopizzo, N., Mombelli, E., Nicolas, S., Dohm-Hansen, S., Scassellati, C., Moretti, D. V., Rosa, M., et al. (2023) · Brain · doi:10.1093/brain/awad303 · Cited by 236 · see citing works
Wu, L., Han, Y., Zheng, Z., Peng, G., Liu, P., Yue, S., Zhu, S., Chen, J., Lv, H., Shao, L., et al. (2021) · Nutrients · doi:10.3390/nu13010228 · Cited by 227 · see citing works
Self-citationThe Potential Role of Gut Microbiota in Alzheimer’s Disease: From Diagnosis to Treatment
Varesi, A., Pierella, E., Romeo, M., Piccini, G. B., Alfano, C., Bjørklund, G., Oppong, A., Ricevuti, G., Esposito, C., Chirumbolo, S., et al. (2022) · Nutrients · doi:10.3390/nu14030668 · Cited by 225 · see citing works
Microbial-derived metabolites as a risk factor of age-related cognitive decline and dementia
Connell, E., Le Gall, G., Pontifex, M. G., Sami, S., Cryan, J. F., Clarke, G., Müller, M., & Vauzour, D. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00548-6 · Cited by 208 · see citing works
The links between the gut microbiome, aging, modern lifestyle and Alzheimer's disease
Askarova, S., Umbayev, B., Masoud, A.-R., Kaiyrlykyzy, A., Safarova, Y., Tsoy, A., Olzhayev, F., & Kushugulova, A. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00104 · Cited by 208 · see citing works
Liao, J.-F., Cheng, Y.-F., You, S.-T., Kuo, W.-C., Huang, C.-W., Chiou, J.-J., Hsu, C.-C., Hsieh-Li, H.-M., Wang, S., & Tsai, Y.-C. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.07.036 · Cited by 159 · see citing works
Ueda, A., Shinkai, S., Shiroma, H., Taniguchi, Y., Tsuchida, S., Kariya, T., Kawahara, T., Kobayashi, Y., Kohda, N., Ushida, K., et al. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100398 · Cited by 155 · see citing works
Cheng, Y., Tan, G., Zhu, Q., Wang, C., Ruan, G., Ying, S., Qie, J., Hu, X., Xiao, Z., Xu, F., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2284247 · Cited by 147 · see citing works
Barrio, C., Arias-Sánchez, S., & Martín-Monzón, I. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105640 · Cited by 143 · see citing works
Gut Metagenomics-Derived Genes as Potential Biomarkers of Parkinson’s Disease
Qian, Y., Yang, X., Xu, S., Huang, P., Li, B., Du, J., He, Y., Su, B., Xu, L.-M., Wang, L., et al. (2020) · Brain · doi:10.1093/brain/awaa201 · Cited by 139 · see citing works
A peripheral signature of Alzheimer’s disease featuring microbiota-gut-brain axis markers
Marizzoni, M., Mirabelli, P., Mombelli, E., Coppola, L., Festari, C., Lopizzo, N., Luongo, D., Mazzelli, M., Naviglio, D., Blouin, J.-L., et al. (2023) · Alzheimer's Research & Therapy · doi:10.1186/s13195-023-01218-5 · Cited by 121 · see citing works
Microbial involvement in Alzheimer disease development and progression
Bulgart, H. R., Neczypor, E. W., Wold, L. E., & Mackos, A. R. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00378-4 · Cited by 116 · see citing works
Pan, W., Zhao, J., Wu, J., Xu, D., Meng, X., Jiang, P., Shi, H., Ge, X., Yang, X., Hu, M., et al. (2023) · Microbiome · doi:10.1186/s40168-023-01471-8 · Cited by 113 · see citing works
Self-citationLiu, P., Jia, X., Chen, Y., Yu, Y., Zhang, K., Lin, Y., Wang, B., & Peng, G. (2021) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13451 · Cited by 87 · see citing works
Self-citationAltered gut microbiota in adults with subjective cognitive decline: the SILCODE study
Sheng, C., Lin, L., Lin, H., Wang, X., Han, Y., & Liu, S.-L. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210259 · Cited by 78 · see citing works
Self-citationLi, T., Chu, C., Yu, L., Zhai, Q., Wang, S., Zhao, J., Zhang, H., Chen, W., & Tian, F. (2022) · Nutrients · doi:10.3390/nu14214678 · Cited by 76 · see citing works
Pentón-Rol, G., Marín-Prida, J., & McCarty, M. F. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210408123807 · Cited by 73 · see citing works
Lei, W., Cheng, Y., Liu, X., Gao, J., Zhu, Z., Ding, W., Xu, X., Li, Y., Ling, Z., Jiang, R., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1582119 · Cited by 68 · see citing works
Nutrition, gut microbiota, and alzheimer’s disease
Romanenko, M., Kholin, V., Koliada, A., & Vaiserman, A. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.712673 · Cited by 56 · see citing works
Multi-omics analysis reveals the key factors involved in the severity of the Alzheimer’s disease
Meng, L., Jin, H., Yulug, B., Altay, O., Li, X., Hanoglu, L., Cankaya, S., Coskun, E., Idil, E., Nogaylar, R., et al. (2024) · Alzheimer's Research & Therapy · doi:10.1186/s13195-024-01578-6 · Cited by 49 · see citing works
Altered gut microbiota in older adults with mild cognitive impairment: a case-control study
Fan, K.-C., Lin, C.-C., Liu, Y.-C., Chao, Y.-P., Lai, Y.-J., Chiu, Y.-L., & Chuang, Y.-F. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1162057 · Cited by 47 · see citing works
Regulation of microglial physiology by the microbiota
Cook, J., & Prinz, M. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2125739 · Cited by 49 · see citing works
Gut microbiome and Alzheimer’s disease: What we know and what remains to be explored
Kapoor, B., Biswas, P., Gulati, M., Rani, P., & Gupta, R. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102570 · Cited by 46 · see citing works
The Role of Genetic, Environmental, and Dietary Factors in Alzheimer’s Disease: A Narrative Review
Mertaş, B., & Boşgelmez, İ. İ. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031222 · Cited by 35 · see citing works
Buawangpong, N., Pinyopornpanish, K., Phrommintikul, A., Chindapan, N., Devahastin, S., Chattipakorn, N., & Chattipakorn, S. C. (2022) · Food & Function · doi:10.1039/d2fo02021a · Cited by 12 · see citing works
- Authors
- Liu, P., Wu, L., Peng, G., Han, Y., Tang, R., Ge, J., Zhang, L., Jia, L., Yue, S., Zhou, K., Li, L., Luo, B., & Wang, B.
- Affiliations
- First Affiliated Hospital Zhejiang University (CN)
- Zhejiang Academy of Medical Sciences (CN)
- Zhejiang University of Technology (CN)
- Corresponding author
- Li, Lanjuan
- Luo, Benyan
- Wang, Baohong
- ORCID
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2019-08
- Volume
- 80
- Pages
- 633-643
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W2944415973
- Cited by
- 669
- References
- 71
- Citations by year
- 2026: 73 · 2025: 121 · 2024: 128 · 2023: 105 · 2022: 115 · 2021: 84 · 2020: 39 · 2019: 4
- FWCI
- 20.01
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Brain Behavior and Immunity (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China
- Natural Science Foundation of Zhejiang Province
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- Alzheimer's disease, amnestic mild cognitive impairment, gut microbiota, gut dysbiosis, gut-brain axis, Firmicutes, Proteobacteria, Enterobacteriaceae, fecal microbiota, microbial diversity, cognitive impairment severity, glycan metabolism, immune pathways, diagnostic biomarkers, Chinese population, dementia risk prediction, amyloid deposition, 16S rRNA gene sequencing
- MeSH terms
- Gastrointestinal Microbiome, Aged, Aged, 80 and over, Alzheimer Disease, Amnesia, Brain, China, Cognition, Cross-Sectional Studies, Feces, Female, Humans, Male, Neuropsychological Tests, Prospective Studies, RNA, Ribosomal, 16S, Cohort Studies, Biomarkers, Area Under Curve, Asian People, Cognitive Dysfunction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review