Gut Microbial Ecosystem in Parkinson Disease: New Clinicobiological Insights from Multi‐Omics
Abstract
OBJECTIVE: Gut microbiome alterations in Parkinson disease (PD) have been reported repeatedly, but their functional relevance remains unclear. Fecal metabolomics, which provide a functional readout of microbial activity, have scarcely been investigated. We investigated fecal microbiome and metabolome alterations in PD, and their clinical relevance. METHODS: Two hundred subjects (104 patients, 96 controls) underwent extensive clinical phenotyping. Stool samples were analyzed using 16S rRNA gene sequencing. Fecal metabolomics were performed using two platforms, nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography-mass spectrometry. RESULTS: Fecal microbiome and metabolome composition in PD was significantly different from controls, with the largest effect size seen in NMR-based metabolome. Microbiome and NMR-based metabolome compositional differences remained significant after comprehensive confounder analyses. Differentially abundant fecal metabolite features and predicted functional changes in PD versus controls included bioactive molecules with putative neuroprotective effects (eg, short chain fatty acids [SCFAs], ubiquinones, and salicylate) and other compounds increasingly implicated in neurodegeneration (eg, ceramides, sphingosine, and trimethylamine N-oxide). In the PD group, cognitive impairment, low body mass index (BMI), frailty, constipation, and low physical activity were associated with fecal metabolome compositional differences. Notably, low SCFAs in PD were significantly associated with poorer cognition and low BMI. Lower butyrate levels correlated with worse postural instability-gait disorder scores. INTERPRETATION: Gut microbial function is altered in PD, characterized by differentially abundant metabolic features that provide important biological insights into gut-brain pathophysiology. Their clinical relevance further supports a role for microbial metabolites as potential targets for the development of new biomarkers and therapies in PD. ANN NEUROL 2021;89:546-559.
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Alterations in the various bacteria, fungi, viruses, and other biological kingdoms that make up the gut microbiome are associated with PD.
“It has been shown that alterations in the various bacteria, fungi, viruses, and other biological kingdoms that make up the gut microbiome are associated with PD [18].”
From The gut–brain axis in early Parkinson’s disease: from prodrome to prevention (2025) · cites this paper as [18]
Lower levels of butyrate are linked to postural instability, gait disorders, MDS-UPDRS part III motor scores and depression among Parkinson's disease patients showing a reduced count of Faecalibacterium.
“lower levels of butyrate are linked to postural instability, gait disorders, Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) part III motor scores and depression among PD patients showing a reduced count of Faecalibacterium [59,60,61,62,63]”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [61]
Cites
1 retracted
Retracted: Gut Microbiome Signatures of Risk and Prodromal Markers of Parkinson Disease
Heinzel, S., Aho, V. T. E., Suenkel, U., von Thaler, A., Schulte, C., Deuschle, C., Paulin, L., Hantunen, S., Brockmann, K., Eschweiler, G. W., et al. (2020) · Annals of Neurology · doi:10.1002/ana.25788 · Cited by 95 · see citing works
RetractedHuman gut microbiome viewed across age and geography
Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., et al. (2012) · Nature · doi:10.1038/nature11053 · Cited by 7,815 · see citing works
Kalia, L. V., & Lang, A. E. (2015) · The Lancet · doi:10.1016/s0140-6736(14)61393-3 · Cited by 6,412 · see citing works
Self-citationParada Venegas, D., De la Fuente, M. K., Landskron, G., González, M. J., Quera, R., Dijkstra, G., Harmsen, H. J. M., Faber, K. N., & Hermoso, M. A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00277 · Cited by 3,820 · see citing works
The Human Intestinal Microbiome in Health and Disease
Lynch, S. V., & Pedersen, O. (2016) · New England Journal of Medicine · doi:10.1056/nejmra1600266 · Cited by 3,637 · see citing works
The role of short-chain fatty acids in microbiota–gut–brain communication
Dalile, B., Van Oudenhove, L., Vervliet, B., & Verbeke, K. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0157-3 · Cited by 3,357 · see citing works
Gut 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 · see citing works
Short-chain fatty acids in control of body weight and insulin sensitivity
Canfora, E. E., Jocken, J. W., & Blaak, E. E. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.128 · Cited by 2,298 · see citing works
Gut 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
Probiotics and prebiotics in intestinal health and disease: from biology to the clinic
Sanders, M. E., Merenstein, D. J., Reid, G., Gibson, G. R., & Rastall, R. A. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0173-3 · Cited by 2,059 · see citing works
Gut 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 · see citing works
Gut microbiota are related to Parkinson's disease and clinical phenotype
Scheperjans, F., Aho, V., Pereira, P. A. B., Koskinen, K., Paulin, L., Pekkonen, E., Haapaniemi, E., Kaakkola, S., Eerola‐Rautio, J., Pohja, M., et al. (2015) · Movement Disorders · doi:10.1002/mds.26069 · Cited by 1,968 · see citing works
Lees, A. J., Hardy, J., & Revesz, T. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60492-x · Cited by 1,956 · see citing works
Composition, variability, and temporal stability of the intestinal microbiota of the elderly
Claesson, M. J., Cusack, S., O'Sullivan, O., Greene-Diniz, R., de Weerd, H., Flannery, E., Marchesi, J. R., Falush, D., Dinan, T., Fitzgerald, G., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000097107 · Cited by 1,754 · see citing works
The pros, cons, and many unknowns of probiotics
Suez, J., Zmora, N., Segal, E., & Elinav, E. (2019) · Nature Medicine · doi:10.1038/s41591-019-0439-x · Cited by 1,398 · see citing works
Human gut microbiome: Hopes, threats and promises
Cani, P. D. (2018) · Gut · doi:10.1136/gutjnl-2018-316723 · Cited by 1,386 · see citing works
Unger, M. M., Spiegel, J., Dillmann, K.-U., Grundmann, D., Philippeit, H., Bürmann, J., Faßbender, K., Schwiertz, A., & Schäfer, K.-H. (2016) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2016.08.019 · Cited by 1,159 · see citing works
Human metabolic phenotype diversity and its association with diet and blood pressure
Holmes, E., Loo, R. L., Stamler, J., Bictash, M., Yap, I. K. S., Chan, Q., Ebbels, T., De Iorio, M., Brown, I. J., Veselkov, K. A., et al. (2008) · Nature · doi:10.1038/nature06882 · Cited by 1,054 · see citing works
Self-citationMatsen, F. A., IV, Kodner, R. B., & Armbrust, E. V. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-538 · Cited by 1,026 · see citing works
Forsyth, C. B., Shannon, K. M., Kordower, J. H., Voigt, R. M., Shaikh, M., Jaglin, J. A., Estes, J. D., Dodiya, H. B., & Keshavarzian, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028032 · Cited by 974 · see citing works
Hill‐Burns, E. M., Debelius, J. W., Morton, J. T., Wissemann, W. T., Lewis, M. R., Wallen, Z. D., Peddada, S. D., Factor, S. A., Molho, E., Zabetian, C. P., et al. (2017) · Movement Disorders · doi:10.1002/mds.26942 · Cited by 874 · see citing works
CSF and blood biomarkers for Parkinson's disease
Parnetti, L., Gaetani, L., Eusebi, P., Paciotti, S., Hansson, O., El-Agnaf, O., Mollenhauer, B., Blennow, K., & Calabresi, P. (2019) · The Lancet Neurology · doi:10.1016/s1474-4422(19)30024-9 · Cited by 673 · see citing works
Janeiro, M., Ramírez, M., Milagro, F., Martínez, J., & Solas, M. (2018) · Nutrients · doi:10.3390/nu10101398 · Cited by 631 · cited 1× · see citing works
“Conversely, several experimental studies suggested that TMAO may protect against neurodegenerative disorders, by promoting the proper folding of proteins (including α-synuclein) and preventing the formation of pathological insoluble fibrils.(55) We also found significant alterations of sphingolipid metabolism in PD, c…”
BackgroundBrain-Gut-Microbiota Axis in Parkinson’s Disease
Mulak, A. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i37.10609 · Cited by 583 · see citing works
Metabolic phenotyping in clinical and surgical environments
Nicholson, J. K., Holmes, E. C., Kinross, J. K., Darzi, A. W., Takáts, Z., & Lindon, J. C. (2012) · Nature · doi:10.1038/nature11708 · Cited by 548 · see citing works
The gut microbiome in human neurological disease: A review
Tremlett, H., Bauer, K. C., Appel‐Cresswell, S., Finlay, B. B., & Waubant, E. (2017) · Annals of Neurology · doi:10.1002/ana.24901 · Cited by 535 · see citing works
Statin therapy is associated with lower prevalence of gut microbiota dysbiosis
Vieira‐Silva, S., Falony, G., Belda, E., Nielsen, T., Aron‐Wisnewsky, J., Chakaroun, R., Forslund, S. K., Assmann, K. E., Valles‐Colomer, M., Nguyen, T. T. D., et al. (2020) · Nature · doi:10.1038/s41586-020-2269-x · Cited by 492 · see citing works
Role of TLR4 in the gut-brain axis in Parkinson's disease: A translational study from men to mice
Perez-Pardo, P., Dodiya, H. B., Engen, P. A., Forsyth, C. B., Huschens, A. M., Shaikh, M., Voigt, R. M., Naqib, A., Green, S. J., Kordower, J. H., et al. (2019) · Gut · doi:10.1136/gutjnl-2018-316844 · Cited by 467 · see citing works
Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How?
Geerlings, S. Y., Kostopoulos, I., de Vos, W. M., & Belzer, C. (2018) · Microorganisms · doi:10.3390/microorganisms6030075 · Cited by 452 · see citing works
Gut Microbiota, Muscle Mass and Function in Aging: A Focus on Physical Frailty and Sarcopenia
Ticinesi, A., Nouvenne, A., Cerundolo, N., Catania, P., Prati, B., Tana, C., & Meschi, T. (2019) · Nutrients · doi:10.3390/nu11071633 · Cited by 418 · see citing works
Enterotoxigenic Bacteroides fragilis : a Rogue among Symbiotes
Sears, C. L. (2009) · Clinical Microbiology Reviews · doi:10.1128/cmr.00053-08 · Cited by 412 · see citing works
A Randomized Clinical Trial of High-Dosage Coenzyme Q10 in Early Parkinson Disease
The Parkinson Study Group QE3 Investigators, Beal, M. F., Oakes, D., Shoulson, I., Henchcliffe, C., Galpern, W. R., Haas, R., Juncos, J. L., Nutt, J. G., Voss, T., et al. (2014) · JAMA Neurology · doi:10.1001/jamaneurol.2014.131 · Cited by 410 · see citing works
Unraveling gut microbiota in Parkinson's disease and atypical parkinsonism
Barichella, M., Severgnini, M., Cilia, R., Cassani, E., Bolliri, C., Caronni, S., Ferri, V., Cancello, R., Ceccarani, C., Faierman, S., et al. (2019) · Movement Disorders · doi:10.1002/mds.27581 · Cited by 393 · see citing works
Gut microbial molecules in behavioural and neurodegenerative conditions
Needham, B. D., Kaddurah-Daouk, R., & Mazmanian, S. K. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-00381-0 · Cited by 379 · see citing works
Gut microbiota in Parkinson's disease: Temporal stability and relations to disease progression
Aho, V. T. E., Pereira, P. A. B., Voutilainen, S., Paulin, L., Pekkonen, E., Auvinen, P., & Scheperjans, F. (2019) · eBioMedicine · doi:10.1016/j.ebiom.2019.05.064 · Cited by 361 · see citing works
Mullin, S., Smith, L., Lee, K., D'Souza, G., Woodgate, P. J. W., Elflein, J., Hällqvist, J., Toffoli, M., Streeter, A., Hosking, J., et al. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2019.4611 · Cited by 360 · see citing works
The role of small intestinal bacterial overgrowth in Parkinson's disease
Fasano, A., Bove, F., Gabrielli, M., Petracca, M., Zocco, M. A., Ragazzoni, E., Barbaro, F., Piano, C., Fortuna, S., Tortora, A., et al. (2013) · Movement Disorders · doi:10.1002/mds.25522 · Cited by 344 · see citing works
Glutamatergic Signaling Along The Microbiota-Gut-Brain Axis
Baj, A., Moro, E., Bistoletti, M., Orlandi, V. T., Crema, F., & Giaroni, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20061482 · Cited by 330 · see citing works
Microbiota composition and metabolism are associated with gut function in Parkinson's disease
Cirstea, M. S., Yu, A. C., Golz, E., Sundvick, K., Kliger, D., Radisavljevic, N., Foulger, L. H., Mackenzie, M., Huan, T., Finlay, B. B., et al. (2020) · Movement Disorders · doi:10.1002/mds.28052 · Cited by 326 · see citing works
Yap, I. K. S., Angley, M. T., Veselkov, K., Holmes, E. C., Lindon, J. C., & Nicholson, J. K. (2010) · Journal of Proteome Research · doi:10.1021/pr901188e · Cited by 316 · see citing works
Self-citationA perspective on 16S rRNA operational taxonomic unit clustering using sequence similarity
Nguyen, N., Warnow, T. J., Pop, M., & White, B. A. (2016) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2016.4 · Cited by 296 · see citing works
Gut Microbiota and Metabolome Alterations Associated with Parkinson’s Disease
Vascellari, S., Palmas, V., Melis, M., Pisanu, S., Cusano, R., Uva, P., Perra, D., Madau, V., Sarchioto, M., Oppo, V., et al. (2020) · mSystems · doi:10.1128/msystems.00561-20 · Cited by 291 · see citing works
Enhancing glycolysis attenuates Parkinson’s disease progression in models and clinical databases
Cai, R., Zhang, Y., Simmering, J. E., Schultz, J. L., Li, Y., Fernandez-Carasa, I., Consiglio, A., Raya, A., Polgreen, P. M., Narayanan, N. S., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci129987 · Cited by 286 · see citing works
Small intestinal bacterial overgrowth in Parkinson's disease
Tan, A. H., Mahadeva, S., Thalha, A. M., Gibson, P. R., Kiew, C. K., Yeat, C. M., Ng, S. W., Ang, S. P., Chow, S. K., Tan, C. T., et al. (2014) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2014.02.019 · Cited by 274 · see citing works
Self-citationBeyond the paradigm: Combining mass spectrometry and nuclear magnetic resonance for metabolomics
Marshall, D. D., & Powers, R. (2017) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2017.01.001 · Cited by 274 · see citing works
The Role of Lipids Interacting with α-Synuclein in the Pathogenesis of Parkinson’s Disease
Galvagnion, C. (2017) · Journal of Parkinson s Disease · doi:10.3233/jpd-171103 · Cited by 265 · see citing works
A review on human fecal metabolomics: Methods, applications and the human fecal metabolome database
Karu, N., Deng, L., Slae, M., Guo, A. C., Sajed, T., Huynh, H. Q., Wine, E., & Wishart, D. S. (2018) · Analytica Chimica Acta · doi:10.1016/j.aca.2018.05.031 · Cited by 260 · see citing works
The Role of Lipids in Parkinson’s Disease
Xicoy, H., Wieringa, B., & Martens, G. J. M. (2019) · Cells · doi:10.3390/cells8010027 · Cited by 255 · see citing works
Baldini, F., Hertel, J., Sandt, E., Thinnes, C. C., Neuberger-Castillo, L., Pavelka, L., Betsou, F., Krüger, R., Thiele, I., Aguayo, G., et al. (2020) · BMC Biology · doi:10.1186/s12915-020-00775-7 · Cited by 230 · see citing works
Probiotics for Constipation in Parkinson Disease: A Randomized Placebo-Controlled Study
Tan, A. H., Lim, S.-Y., Chong, K. K., A Manap, M. A. A., Hor, J. W., Lim, J. L., Low, S. C., Chong, C. W., Mahadeva, S., & Lang, A. E. (2021) · Neurology · doi:10.1212/wnl.0000000000010998 · Cited by 226 · see citing works
Self-citationSrivastav, S., Neupane, S., Bhurtel, S., Katila, N., Maharjan, S., Choi, H., Hong, J. T., & Choi, D.-Y. (2019) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.03.021 · Cited by 212 · see citing works
Probiotic Bacillus subtilis protects against α-synuclein aggregation in C. elegans
Goya, M. E., Xue, F., Sampedro-Torres-Quevedo, C., Arnaouteli, S., Riquelme-Dominguez, L., Romanowski, A., Brydon, J., Ball, K. L., Stanley-Wall, N. R., & Doitsidou, M. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.078 · Cited by 205 · see citing works
Bowman, J. S., & Ducklow, H. W. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135868 · Cited by 190 · see citing works
Self-citationEthanol metabolism and its effects on the intestinal epithelial barrier
Elamin, E. E., Masclee, A., Dekker, J. P., & Jonkers, D. M. A. E. (2013) · Nutrition Reviews · doi:10.1111/nure.12027 · Cited by 187 · see citing works
Wang, M., Wan, J., Rong, H., He, F., Wang, H., Zhou, J., Cai, C., Wang, Y., Xu, R., Yin, Z., et al. (2019) · mSystems · doi:10.1128/msystems.00321-18 · Cited by 181 · see citing works
Prevalence of small intestinal bacterial overgrowth in Parkinson’s disease
Gabrielli, M., Bonazzi, P., Scarpellini, E., Bendia, E., Lauritano, E. C., Fasano, A., Ceravolo, M. G., Capecci, M., Rita Bentivoglio, A., Provinciali, L., et al. (2011) · Movement Disorders · doi:10.1002/mds.23566 · Cited by 175 · see citing works
Parkinson’s Disease and the Gastrointestinal Microbiome
Lubomski, M., Tan, A. H., Lim, S.-Y., Holmes, A. J., Davis, R. L., & Sue, C. M. (2020) · Journal of Neurology · doi:10.1007/s00415-019-09320-1 · Cited by 172 · see citing works
Self-citationBoertien, J. M., Pereira, P. A. B., Aho, V. T. E., & Scheperjans, F. (2019) · Journal of Parkinson s Disease · doi:10.3233/jpd-191711 · Cited by 169 · see citing works
Sharma, S., Taliyan, R., & Singh, S. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.05.052 · Cited by 142 · see citing works
Helicobacter pylori infection is associated with worse severity of Parkinson's disease
Tan, A. H., Mahadeva, S., Marras, C., Thalha, A. M., Kiew, C. K., Yeat, C. M., Ng, S. W., Ang, S. P., Chow, S. K., Loke, M. F., et al. (2014) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2014.12.009 · Cited by 132 · see citing works
Self-citationClavel, T., Lepage, P., & Charrier, C. (2014) · Springer eBooks · doi:10.1007/978-3-642-30138-4_343 · Cited by 126 · see citing works
Maier, E., Anderson, R. C., & Roy, N. C. (2014) · Nutrients · doi:10.3390/nu7010045 · Cited by 114 · see citing works
Tan, A. H., Hew, Y. C., Lim, S., Ramli, N. M., Kamaruzzaman, S. B., Tan, M. P., Grossmann, M., Ang, B. H., Tan, J. Y., Manap, M. A. A. A., et al. (2018) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2018.06.020 · Cited by 108 · see citing works
Self-citationSankowski, B., Księżarczyk, K., Raćkowska, E., Szlufik, S., Koziorowski, D., & Giebułtowicz, J. (2020) · Clinica Chimica Acta · doi:10.1016/j.cca.2019.10.038 · Cited by 105 · see citing works
The gut microbiome in Parkinson's disease: A culprit or a bystander?
Keshavarzian, A., Engen, P. A., Bonvegna, S., & Cilia, R. (2020) · Progress in brain research · doi:10.1016/bs.pbr.2020.01.004 · Cited by 104 · see citing works
Impaired oxidative decarboxylation of pyruvate in fibroblasts from patients with Parkinson's disease
Mytilineou, C., Werner, P., Molinari, S., Rocco, A. D., Cohen, G., & Yahr, M. D. (1994) · Journal of Neural Transmission - Parkinsons Disease and Dementia Section · doi:10.1007/bf02260943 · Cited by 92 · see citing works
Rane, P., Shields, J., Heffernan, M., Guo, Y., Akbarian, S., & King, J. A. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.026 · Cited by 78 · see citing works
Helicobacter pylori Eradication in Parkinson's Disease: A Randomized Placebo‐Controlled Trial
Tan, A. H., Lim, S., Mahadeva, S., Loke, M. F., Tan, J. Y., Ang, B. H., Chin, K. P., Adnan, A. F. M., Ong, S. M. C., Ibrahim, A. I., et al. (2020) · Movement Disorders · doi:10.1002/mds.28248 · Cited by 76 · see citing works
Self-citationCeramides in Parkinson’s Disease: From Recent Evidence to New Hypotheses
Plotegher, N., Bubacco, L., Greggio, E., & Civiero, L. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00330 · Cited by 63 · see citing works
Altered gut microbiome and metabolome in patients with multiple system atrophy
Tan, A. H., Chong, C. W., Song, S., Teh, C. S. J., Yap, I. K. S., Loke, M. F., Tan, Y. Q., Yong, H.-S., Mahadeva, S., Lang, A. E., et al. (2017) · Movement Disorders · doi:10.1002/mds.27203 · Cited by 52 · see citing works
Self-citationSakaue, S., Kasai, T., Mizuta, I., Suematsu, M., Osone, S., Azuma, Y., Imamura, T., Tokuda, T., Kanno, H., El‐Agnaf, O. M. A., et al. (2017) · npj Parkinson s Disease · doi:10.1038/s41531-017-0014-4 · Cited by 49 · see citing works
Finnicum, C. T., Beck, J. J., Dolan, C. V., Davis, C. M., Willemsen, G. A. H. M., Ehli, E. A., Boomsma, D. I., Davies, G. E., & de Geus, E. J. C. (2019) · BMC Microbiology · doi:10.1186/s12866-019-1602-8 · Cited by 31 · see citing works
Sodium salicylate protects against rotenone-induced Parkinsonism in rats
Madathil, S. K., Karuppagounder, S. S., & Mohanakumar, K. P. (2013) · Synapse · doi:10.1002/syn.21658 · Cited by 30 · see citing works
Actor, J. K. (2012) · Elsevier eBooks · doi:10.1016/b978-0-323-07447-6.00012-0 · Cited by 25 · see citing works
Global Fecal and Plasma Metabolic Dynamics Related to Helicobacter pylori Eradication
Yap, T. W.-C., Leow, A. H., Azmi, A. N., Callahan, D. L., Perez-Perez, G. I., Loke, M. F., Goh, K., & Vadivelu, J. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00536 · Cited by 16 · see citing works
Self-citationConsistency and Generalizability of Dietary Patterns in a Multiethnic Working Population
Eng, J. Y., Moy, F. M., Bulgiba, A. M., & Rampal, S. (2018) · Journal of the Academy of Nutrition and Dietetics · doi:10.1016/j.jand.2018.01.014 · Cited by 14 · see citing works
Gut microbiome signatures of risk and prodromal markers of Parkinson’s diseasePreprint
Heinzel, S., Aho, V. T. E., Suenkel, U., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2019.12.11.872481 · Cited by 4 · see citing works
Inflammatory bowel disease and risk of Parkinson’s disease
Ríos, J. P., Madrid-Navarro, C. J., Pérez-Navarro, M. J., Arillo, V. M. C., Mínguez‐Castellanos, A., & Sevilla, F. E. (2018) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2018.06.027 · Cited by 2 · see citing works
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Chen, C., Wang, J., Pan, D., Wang, X., Xu, Y., Yan, J., Wang, L., Yang, X., Yang, M., & Liu, G. (2023) · MedComm · doi:10.1002/mco2.315 · Cited by 545 · see citing works
The microbiome–gut–brain axis in Parkinson disease — from basic research to the clinic
Tan, A. H., Lim, S. Y., & Lang, A. E. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00681-2 · Cited by 392 · see citing works
Self-citationChen, S.-J., Chen, C.-C., Liao, H.-Y., Lin, Y.-T., Wu, Y.-W., Liou, J.-M., Wu, M.-S., Kuo, C.-H., & Lin, C.-H. (2022) · Neurology · doi:10.1212/wnl.0000000000013225 · Cited by 269 · see citing works
The Association Between the Gut Microbiota and Parkinson’s Disease, a Meta-Analysis
Shen, T., Yue, Y., He, T., Huang, C., Qu, B., Lv, W., & Lai, H.-Y. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.636545 · Cited by 219 · see citing works
“In addition, metabolome compositional differences such as the lower SCFAs were associated with poorer cognition, and lower butyrate levels were correlated with worse postural instability gait disorder scores in PD (Tan et al., 2020).”
BackgroundGut bacterial profiles in Parkinson's disease: A systematic review
Li, Z., Liang, H., Lu, L., Lu, L., Zheng, C., Fan, Y., Wu, B., Zou, T., Luo, X., Xinchun, Z., et al. (2022) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13990 · Cited by 217 · see citing works
Parkinson’s disease and gut microbiota: from clinical to mechanistic and therapeutic studies
Zhang, X., Tang, B., & Guo, J. (2023) · Translational Neurodegeneration · doi:10.1186/s40035-023-00392-8 · Cited by 205 · see citing works
Gut Microbiota: A Novel Therapeutic Target for Parkinson’s Disease
Zhu, M., Liu, X., Ye, Y., Yan, X., Cheng, Y., Zhao, L., Chen, F., & Ling, Z. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.937555 · Cited by 177 · see citing works
Probiotics synergized with conventional regimen in managing Parkinson’s disease
Sun, H., Zhao, F., Liu, Y., Ma, T., Jin, H., Quan, K., Leng, B., Zhao, J., Yuan, X., Li, Z., et al. (2022) · npj Parkinson's Disease · doi:10.1038/s41531-022-00327-6 · Cited by 136 · see citing works
Gut microbiome in Parkinson's disease: New insights from meta-analysis
Toh, T. S., Chong, C. W., Lim, S., Bowman, J. S., Cirstea, M. S., Lin, C., Chen, C., Appel‐Cresswell, S., Finlay, B. B., & Tan, A. H. (2021) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2021.11.017 · Cited by 133 · see citing works
Self-citationThe Relationship Between the Gut Microbiome and Neurodegenerative Diseases
Zhu, X., Li, B., Lou, P., Dai, T., Chen, Y., Zhuge, A., Yuan, Y., & Li, L. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00730-8 · Cited by 134 · see citing works
Spichak, S., Bastiaanssen, T. F. S., Berding, K., Vlckova, K., Clarke, G., Dinan, T. G., & Cryan, J. F. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.044 · Cited by 127 · see citing works
Air Pollution and the Risk of Parkinson's Disease: A Review
Murata, H., Barnhill, L. M., & Bronstein, J. M. (2022) · Movement Disorders · doi:10.1002/mds.28922 · Cited by 126 · see citing works
Short‐chain fatty acids: bridges between diet, gut microbiota, and health
Wang, L., He, L., Xu, L., & Li, S. (2024) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.16619 · Cited by 125 · see citing works
The Role of Microbiome in Brain Development and Neurodegenerative Diseases
Nandwana, V., Nandwana, N. K., Das, Y., Saito, M., Panda, T., Das, S., Almaguel, F. A., Hosmane, N. S., & Das, B. C. (2022) · Molecules · doi:10.3390/molecules27113402 · Cited by 113 · see citing works
Potential roles of gut microbiota and microbial metabolites in Parkinson’s disease
Zheng, S.-Y., Li, H.-X., Xu, R.-C., Miao, W.-T., Dai, M.-Y., Ding, S.-T., & Liu, H.-D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101347 · Cited by 101 · see citing works
Heravi, F. S., Naseri, K., & Hu, H. (2023) · Nutrients · doi:10.3390/nu15204365 · Cited by 105 · see citing works
Varesi, A., Campagnoli, L. I. M., Fahmideh, F., Pierella, E., Romeo, M., Ricevuti, G., Nicoletta, M., Chirumbolo, S., & Pascale, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012289 · Cited by 88 · see citing works
Duan, W.-X., Wang, F., Liu, J., & Liu, C. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01123-9 · Cited by 78 · see citing works
Chen, S., & Lin, C. (2022) · Journal of Biomedical Science · doi:10.1186/s12929-022-00839-6 · Cited by 81 · see citing works
Chu, C., Yu, L., Li, Y. H., Guo, H., Zhai, Q., Chen, W., & Tian, F. (2023) · Nutrients · doi:10.3390/nu15071737 · Cited by 71 · see citing works
Physical activity and lifestyle modifications in the treatment of neurodegenerative diseases
Santiago, J. A., & Potashkin, J. A. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1185671 · Cited by 70 · see citing works
Mudimela, S., Vishwanath, N. K., Pillai, A., Morales, R., Marrelli, S. P., Barichello, T., & Giridharan, V. V. (2022) · Drug Discovery Today · doi:10.1016/j.drudis.2022.08.002 · Cited by 70 · see citing works
dos Santos, J. C. C., Oliveira, L. F., Noleto, F. M., Gusmão, C. T. P., Brito, G. A. D. C., & Viana, G. S. D. B. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.373673 · Cited by 67 · see citing works
Layunta, E., Buey, B., Mesonero, J. E., & Latorre, E. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.748254 · Cited by 67 · see citing works
Advances in Proteomic and Metabolomic Profiling of Neurodegenerative Diseases
Schuh, A. F. S., Bieger, A., Borelli, W. V., Portley, M. K., Awad, P. S., & Bandrés‐Ciga, S. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.792227 · Cited by 63 · see citing works
Romano, S., Wirbel, J., Ansorge, R., Schudoma, C., Ducarmon, Q. R., Narbad, A., & Zeller, G. (2025) · Nature Communications · doi:10.1038/s41467-025-56829-3 · Cited by 68 · see citing works
Lubomski, M., Xu, X., Holmes, A. J., Muller, S., Yang, J. Y. H., Davis, R. L., & Sue, C. M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.875261 · Cited by 59 · see citing works
Aljeradat, B., Kumar, D., Abdulmuizz, S., Kundu, M., Almealawy, Y. F., Batarseh, D. R., Atallah, O., Ennabe, M., Alsarafandi, M., Alan, A., et al. (2024) · Pathophysiology · doi:10.3390/pathophysiology31020019 · Cited by 63 · see citing works
Role of the Gut Bacteria-Derived Metabolite Phenylacetylglutamine in Health and Diseases
Krishnamoorthy, N. K., Kalyan, M., Hediyal, T. A., Anand, N., Kendaganna, P. H., Pendyala, G., Yelamanchili, S. V., Yang, J. P., Chidambaram, S. B., Sakharkar, M. K., et al. (2024) · ACS Omega · doi:10.1021/acsomega.3c08184 · Cited by 54 · see citing works
Evidences for a Role of Gut Microbiota in Pathogenesis and Management of Epilepsy
Amlerová, J., Šroubek, J., Angelucci, F., & Hort, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115576 · Cited by 52 · see citing works
Voigt, R. M., Wang, Z., Brown, J. M., Engen, P. A., Naqib, A., Goetz, C. G., Hall, D. A., Metman, L. V., Shaikh, M., Forsyth, C. B., et al. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105780 · Cited by 51 · see citing works
Gastrointestinal disorders in Parkinson’s disease and other Lewy body diseases
Hirayama, M., Nishiwaki, H., Hamaguchi, T., & Ohno, K. (2023) · npj Parkinson s Disease · doi:10.1038/s41531-023-00511-2 · Cited by 51 · 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
Stroke and Vascular Cognitive Impairment: The Role of Intestinal Microbiota Metabolite TMAO
Tu, R., & Xia, J. (2024) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527322666230203140805 · Cited by 47 · see citing works
Müller-Nedebock, A. C., Dekker, M. C. J., Farrer, M. J., Hattori, N., Lim, S., Mellick, G. D., Rektorová, I., Salama, M., Schuh, A. F. S., Stoessl, A. J., et al. (2023) · npj Parkinson s Disease · doi:10.1038/s41531-023-00535-8 · Cited by 47 · see citing works
Self-citationWang, R., Gu, Z., Wang, Y., Yin, X., Liu, W., Chen, W., Huang, Y., Wu, J., Yang, S., Feng, L., et al. (2022) · Advanced Functional Materials · doi:10.1002/adfm.202206670 · Cited by 43 · see citing works
Multiomics Implicate Gut Microbiota in Altered Lipid and Energy Metabolism in Parkinson’s Disease
Pereira, P. A. B., Trivedi, D. K., Silverman, J., Duru, I. C., Paulin, L., Auvinen, P., & Scheperjans, F. (2022) · npj Parkinson s Disease · doi:10.1038/s41531-022-00300-3 · Cited by 40 · see citing works
Cho, J. H., Chae, C. W., Lim, J. R., Jung, Y. H., Han, S. J., Yoon, J. H., Park, J. Y., & Han, H. J. (2024) · Autophagy · doi:10.1080/15548627.2024.2323785 · Cited by 39 · see citing works
Gut dysbiosis and age-related neurological diseases in females
Korf, J. M., Ganesh, B. P., & McCullough, L. D. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105695 · Cited by 41 · see citing works
Gut Microbial Dysbiosis and Cognitive Impairment in Bipolar Disorder: Current Evidence
Dai, W., Liu, J., Yan, Q., Teng, Z., Li, S., Yuan, H., Huang, J., Xiang, H., Tang, H., Wang, B., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.893567 · Cited by 41 · see citing works
The Gut‐Brain Axis in Parkinson disease: Emerging Concepts and Therapeutic Implications
Menozzi, E., Schapira, A. H. V., & Borghammer, P. (2025) · Movement Disorders Clinical Practice · doi:10.1002/mdc3.70029 · Cited by 40 · see citing works
The faecal metabolome and mycobiome in Parkinson's disease
Pablo‐Fernández, E. D., Gebeyehu, G. G., Flain, L., Slater, R., Frau, A., Ijaz, U. Z., Warner, T. T., & Probert, C. S. (2022) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2022.01.005 · Cited by 36 · see citing works
Tan, A. H., Chuah, K. H., Beh, Y. Y., Schee, J. P., Mahadeva, S., & Lim, S. (2023) · Journal of Movement Disorders · doi:10.14802/jmd.22220 · Cited by 36 · see citing works
Self-citationGut Metagenome as a Potential Diagnostic and Predictive Biomarker in Slow Transit Constipation
Tian, H., Ye, C., Yang, B. K., Cui, J., Zheng, Z., Wu, C., Zhou, S., Lv, X., Qin, N., Qin, H., et al. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2021.777961 · Cited by 34 · see citing works
The gut–brain axis in early Parkinson’s disease: from prodrome to prevention
Oliver, P. J., Civitelli, L., & Hu, M. T. (2025) · Journal of Neurology · doi:10.1007/s00415-025-13138-5 · Cited by 42 · see citing works
“In this model outlined by Braak et al., early α-synuclein induction sites are found in the brain, including the dorsal motor nucleus or the vagus and the olfactory bulb, with spread”
Zacharias, H. U., Kaleta, C., Cossais, F., Schaeffer, E., Berndt, H., Best, L., Dost, T., Glüsing, S., Groussin, M., Poyet, M., et al. (2022) · Metabolites · doi:10.3390/metabo12121222 · Cited by 36 · see citing works
Li, Q., Meng, L., Chen, L., Shi, X., Tu, L., Zhou, Q. G., Yu, J.-L., Liao, X., Zeng, Y., & Yuan, Q. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1185375 · Cited by 36 · see citing works
Therapeutic Prospect of New Probiotics in Neurodegenerative Diseases
Bi, M., Liu, C., Wang, Y., & Liu, S. (2023) · Microorganisms · doi:10.3390/microorganisms11061527 · Cited by 34 · see citing works
Luo, X., Liu, Y., Balck, A., Klein, C., & Fleming, R. M. T. (2024) · npj Parkinson s Disease · doi:10.1038/s41531-024-00732-z · Cited by 34 · see citing works
Fecal Calprotectin in Parkinson’s Disease and Multiple System Atrophy
Hor, J. W., Lim, S., Khor, E.-S., Chong, K. K., Song, S., Ibrahim, N. M., Teh, C. S. J., Chong, C. W., Hilmi, I. N., & Tan, A. H. (2021) · Journal of Movement Disorders · doi:10.14802/jmd.21085 · Cited by 33 · see citing works
Self-citationRelationship among Parkinson’s disease, constipation, microbes, and microbiological therapy
Yuan, X.-Y., Chen, Y., & Liu, Z. (2024) · World Journal of Gastroenterology · doi:10.3748/wjg.v30.i3.225 · Cited by 35 · see citing works
Brain-gut-microbiota axis in Parkinson’s disease: A historical review and future perspective
Dong, S., Sun, M., He, C. H., & Cheng, H. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.02.015 · Cited by 32 · see citing works
Marć, M. A., Jastrząb, R., & Mytych, J. (2022) · Nutrients · doi:10.3390/nu14193967 · Cited by 33 · see citing works
Bi, M., Feng, L., He, J., Liu, C., Wang, Y., Jiang, H., & Liu, S. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101759 · Cited by 32 · see citing works
Meta-analysis of randomized controlled trials of the effects of probiotics in Parkinson's disease
Chu, C., Yu, L., Li, Y. H., Guo, H., Zhai, Q., Chen, W., & Tian, F. (2023) · Food & Function · doi:10.1039/d2fo03825k · Cited by 32 · see citing works
Oral and gut microbial profiling in periodontitis and Parkinson’s disease
Yay, E., Yılmaz, M., Toygar, H. U., Balcı, N., Rivas, C. A., Kılıç, B. B., Zirh, A. T., Paster, B. J., & Kantarcı, A. (2024) · Journal of Oral Microbiology · doi:10.1080/20002297.2024.2331264 · Cited by 29 · see citing works
Chu, X., Hou, Y., Meng, Q., Croteau, D. L., Wei, Y. Q., De, S., Becker, K. G., & Bohr, V. A. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.993615 · Cited by 29 · see citing works
Gut dysbiosis as a potential driver of Parkinson’s and Alzheimer’s disease pathogenesis
Pfaffinger, J. M., Hays, K. E., Seeley, J., Babu, P. R., & Ryznar, R. J. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1600148 · Cited by 28 · see citing works
Microbiota Dysbiosis in Parkinson Disease—In Search of a Biomarker
Nowak, J. M., Kopczyński, M. H., Friedman, A., Koziorowski, D., & Figura, M. (2022) · Biomedicines · doi:10.3390/biomedicines10092057 · Cited by 28 · see citing works
Gut microbiota–astrocyte axis: new insights into age-related cognitive decline
Zhang, L., Wei, J., Liu, X., Li, D., Pang, X., Chen, F., Cao, H., & Lei, P. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-23-01776 · Cited by 28 · see citing works
Abraham, D. S., Nguyen, T. P. P., & Willis, A. W. (2021) · Movement Disorders · doi:10.1002/mds.28561 · Cited by 27 · see citing works
The association of traumatic brain injury, gut microbiota and the corresponding metabolites in mice
Wang, S., Zhu, K., Hou, X., & Hou, L. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147450 · Cited by 27 · see citing works
Dietary patterns affect Parkinson's disease via the microbiota-gut-brain axis
Chu, C., Yu, L., Chen, W., Tian, F., & Zhai, Q. (2021) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2021.07.004 · Cited by 26 · see citing works
Buty and the beast: the complex role of butyrate in Parkinson’s disease
Elford, J. D., Becht, N. N., Garssen, J., Kraneveld, A. D., & Perez‐Pardo, P. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1388401 · Cited by 27 · see citing works
Lin, F., Rensing, C., Pang, Z., Zou, J., Lin, S., Letuma, P., Zhang, Z., & Lin, W. (2022) · Field Crops Research · doi:10.1016/j.fcr.2022.108521 · Cited by 26 · see citing works
Nutritional Intake and Gut Microbiome Composition Predict Parkinson’s Disease
Lubomski, M., Xu, X., Holmes, A. J., Müller, S., Yang, J. Y. H., Davis, R. L., & Sue, C. M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.881872 · Cited by 26 · see citing works
The relationship between Parkinson’s disease and gastrointestinal diseases
Zeng, J., Wang, X., Pan, F., & Mao, Z. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.955919 · Cited by 26 · see citing works
Riegelman, E., Xue, K. S., Wang, J.-S., & Tang, L. (2024) · Nutrients · doi:10.3390/nu16132041 · Cited by 29 · see citing works
The connection between gut microbiota and its metabolites with neurodegenerative diseases in humans
Fabi, J. P. (2024) · Metabolic Brain Disease · doi:10.1007/s11011-024-01369-w · Cited by 25 · see citing works
Omics data integration suggests a potential idiopathic Parkinson’s disease signature
Žagare, A., Preciat, G., Nickels, S., Luo, X., Monzel, A. S., Gomez‐Giro, G., Robertson, G., Jaeger, C., Sharif, J., Koseki, H., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05548-w · Cited by 25 · see citing works
Huang, C., Sun, Y. H., Liao, S.-R., Chen, Z.-X., Lin, H.-F., & Shen, W. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.869931 · Cited by 23 · see citing works
Augustin, A. D., Guennec, A. D. L., Umamahesan, C., Kendler-Rhodes, A., Tucker, R. M., Chekmeneva, E., Takis, P. G., Lewis, M. R., Balasubramanian, K., Desouza, N., et al. (2023) · Clinical and Translational Medicine · doi:10.1002/ctm2.1152 · Cited by 22 · see citing works
The link between the gut microbiome, inflammation, and Parkinson’s disease
Nie, S., & Ge, Y. (2023) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-023-12789-6 · Cited by 23 · see citing works
Jia, X., Chen, Q., Zhang, Y., & Asakawa, T. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1296713 · Cited by 22 · see citing works
Park, S. J., Kim, K. W., & Lee, E. J. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-00994 · Cited by 23 · see citing works
Santos‐Lobato, B. L., Gardinassi, L. G., Bortolanza, M., Peti, A. P. F., Pimentel, Â. V., Faccioli, L. H., Bel, E. A. D., & Tumas, V. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02625-1 · Cited by 21 · see citing works
Multi-omics studies reveal ameliorating effects of physical exercise on neurodegenerative diseases
Guo, Y., Wang, S., Chao, X., Li, D., Wang, Y., Guo, Q., & Chen, T. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1026688 · Cited by 21 · see citing works
Mateo, D., Marquès, M., Domingo, J. L., & Torrente, M. (2023) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32959 · Cited by 21 · see citing works
Unraveling the gut-brain axis: the impact of steroid hormones and nutrition on Parkinson’s disease
Neufeld, P. M., Nettersheim, R., Matschke, V., Vorgerd, M., Stahlke, S., & Theiß, C. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.391304 · Cited by 21 · see citing works
Gut microbiota metabolites: potential therapeutic targets for Alzheimer’s disease?
Zhang, S., Lu, J., Jin, Z., Xu, H., Zhang, D., Chen, J., & Wang, J. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1459655 · Cited by 24 · see citing works
Liu, J., Zhang, Y., Ye, T., Yu, Q., Yu, J., Yuan, S., Gao, X., Wan, X., Zhang, R., Han, W., et al. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c06998 · Cited by 20 · see citing works
Psychobiotic Properties of Lactiplantibacillus plantarum in Neurodegenerative Diseases
Chiano, M. D., Sallustio, F., Fiocco, D., Rocchetti, M. T., Spano, G., Pontrelli, P., Moschetta, A., Gesualdo, L., Gadaleta, R. M., & Gallone, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179489 · Cited by 20 · see citing works
Marzouk, N. H., Rashwan, H. H., El-Hadidi, M. S., Ramadan, R., & Mysara, M. (2025) · npj Parkinson s Disease · doi:10.1038/s41531-025-00950-z · Cited by 19 · see citing works
Shi, J., Wang, Y., Chen, D., Xu, X., Li, W., Li, K., He, J., Su, W., & Luo, Q. (2023) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-023-12410-w · Cited by 19 · see citing works
Zhao, R., Mu, B., Wang, D., XinHuang, Ma, Q., & Lu, M. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04584-9 · Cited by 19 · see citing works
Tao, W., Zhang, Y., Wang, B., Nie, S., Li, F., Xiao, J., & Wu, Y. (2024) · Journal of Advanced Research · doi:10.1016/j.jare.2024.03.023 · Cited by 19 · see citing works
Frailty and cognitive impairment in Parkinson’s disease: a systematic review
Sousa-Fraguas, M. C., Fuentes, G. R., & Conejo, N. M. (2022) · Neurological Sciences · doi:10.1007/s10072-022-06347-7 · Cited by 17 · see citing works
Ye, L., Dong, N., Xiong, W., Li, J., Li, R., Heng, H., Chan, E. W., & Chen, S. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.801587 · Cited by 14 · see citing works
The gut microbiome and cognition in Parkinson’s disease: a systematic review
Grant, H., Anderton, R. S., Gasson, N., & Lawrence, B. J. (2022) · Nutritional Neuroscience · doi:10.1080/1028415x.2022.2110189 · Cited by 16 · see citing works
Peter, I., & Strober, W. (2023) · Journal of Parkinson s Disease · doi:10.3233/jpd-230021 · Cited by 16 · see citing works
Underneath the Gut–Brain Axis in IBD—Evidence of the Non-Obvious
Boldyreva, L. V., Evtushenko, A. A., Lvova, M. N., Morozova, K. N., & Владимировна, К. Е. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252212125 · Cited by 16 · see citing works
Pharmacomicrobiomics: a new field contributing to optimizing drug therapy in Parkinson’s disease
Zhang, Y., Mo, C., Ai, P., He, X., Xiao, Q., & Yang, X. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2454937 · Cited by 17 · see citing works
Barbu, A. C., Stoleru, S., Zugravu, A., Poenaru, E., Dragomir, A.-F., Costescu, M., Aurelian, S. M., Shhab, Y., Stoleru, C. M., Coman, O. A., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms27010271 · Cited by 15 · see citing works
Identification of gut metabolites associated with Parkinson’s disease using bioinformatic analyses
Yan, J., Feng, X., Zhou, X., Zhao, M., Xiao, H., Li, R., & Shen, H. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.927625 · Cited by 15 · see citing works
High levels of Bifidobacteriaceae are associated with the pathogenesis of Parkinson’s disease
Zuo, S., Wang, H., Zhao, Q., Tang, J., Wang, M., Zhang, Y., Sang, M., Tian, J., & Wang, P. (2023) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.1054627 · Cited by 15 · see citing works
Branched-Chain Amino Acids in Parkinson’s Disease: Molecular Mechanisms and Therapeutic Potential
Huang, H.-Y., Tsao, S., & Yeh, T. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26146992 · Cited by 14 · see citing works
Multi-omics and high-spatial-resolution omics: deciphering complexity in neurological disorders
Liu, X., Li, F., Czosnyka, M., Czosnyka, Z. H., Yu, H., Tong, X., Xing, Y., Li, H., Pu, K., Feng, K., et al. (2025) · GigaScience · doi:10.1093/gigascience/giaf137 · Cited by 16 · see citing works
Cassotta, M. (2022) · ALTEX · doi:10.14573/altex.2203161 · Cited by 14 · see citing works
Kang, S. H., Lee, J., & Koh, S. (2021) · Journal of Movement Disorders · doi:10.14802/jmd.21074 · Cited by 13 · see citing works
- Authors
- Tan, A. H., Chong, C. W., Lim, S., Yap, I. K. S., Teh, C. S. J., Loke, M. F., Song, S., Tan, J. Y., Ang, B. H., Tan, Y. Q., Kho, M. T., Bowman, J., Mahadeva, S., Yong, H. S., & Lang, A. E.
- Affiliations
- University of Malaya (MY)
- Monash University Malaysia (MY)
- Sarawak Research and Development Council Kuching Malaysia
- Xiamen University Malaysia (MY)
- IMU University (MY)
- Scripps Institution of Oceanography (US)
- Toronto Western Hospital (CA)
- Corresponding author
- Chong, Chun Wie
- ORCID
- Venue
- Annals of Neurology
- Publisher
- Wiley
- Published
- 2021-01-11
- Volume
- 89
- Issue
- 3
- Pages
- 546-559
- ISSN
- 0364-5134 (ISSN-L)
- 1531-8249
- OpenAlex
- W3108955779
- Cited by
- 196
- References
- 77
- Citations by year
- 2026: 26 · 2025: 37 · 2024: 39 · 2023: 39 · 2022: 40 · 2021: 15
- FWCI
- 7.62
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- Parkinson's disease, gut microbiota, fecal metabolome, short-chain fatty acids, butyrate, gut-brain axis, neurodegeneration, cognitive impairment, body mass index, frailty, constipation, biomarkers, trimethylamine N-oxide, ceramide, salicylates, coenzyme Q10
- MeSH terms
- Gastrointestinal Microbiome, Frailty, Aged, Ceramides, Chromatography, Liquid, Constipation, Fatty Acids, Volatile, Feces, Female, Humans, Male, Methylamines, Middle Aged, Parkinson Disease, RNA, Ribosomal, 16S, Salicylates, Mass Spectrometry, Sphingosine, Thinness, Ubiquinone, Metabolomics, Sedentary Behavior, Cognitive Dysfunction, Proton Magnetic Resonance Spectroscopy
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