Gut microbiota differences between healthy older adults and individuals with Parkinson’s disease: A systematic review
Open accessAbstract
The 'Dual Hit' hypothesis, stating that Parkinson's disease (PD) begins via olfactory pathways and the gut, and the gastrointestinal symptoms PD individuals face, have largely driven the interest of the gut's involvement in PD. Studies have since observed gut microbiota differences between PD groups and controls, with these alterations potentially relating to PD pathophysiology. However, differences in the studies' methodologies precludes unanimity on the relationships of gut microbiota to PD. Thirteen observational case-control studies investigating gut microbiota in PD and controls were reviewed to assess how microbiota abundance and diversity relates to PD. Nine studies showed butyrate producing gut microbiota had lower abundances in PD compared to controls. Three studies reported α-diversity was higher, with one reporting it was lower, in PD compared to controls. Given most studies show abundance, not diversity, differences of butyrate producing bacteria between groups, we propose abundance differences are more associated with PD than microbiota diversity. As current research is observational, investigating how specific bacteria and their metabolites may alter throughout PD progression is warranted.
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Diminished SCFA-producing species and SCFA levels are consistently reported in prodromal PD and PD patients compared with healthy controls, and may be correlated with clinical severity of PD.
“These findings are in concordance with a substantial body of literature that consistently reports diminished SCFAs-producing species and SCFA levels in prodromal stage of PD and PD patients compared to healthy controls, which may be correlated with the clinical severity of PD.52,322–331”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [324]
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Haehner, A., Hummel, T. R., & Reichmann, H. (2009) · Expert Review of Neurotherapeutics · doi:10.1586/ern.09.115 · Cited by 116 · see citing works
[24] Bacterial adhesion to and penetration of intestinal mucus in vitro
Cohen, P. S., & Laux, D. C. (1995) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(95)53026-6 · Cited by 76 · see citing works
Intestinal Mucin Inhibits Adhesion of Human Enteropathogenic Escherichia coli to HEp-2 Cells
Smith, C. J., Kaper, J. B., & Mack, D. R. (1995) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199510000-00004 · Cited by 35 · see citing works
The role of environmental agents in Parkinson's disease
Monte, D. A. D. (2001) · Clinical Neuroscience Research · doi:10.1016/s1566-2772(01)00020-2 · Cited by 32 · see citing works
Rocha, B. S., Correia, M., Barbosa, R. M., & Laranjinha, J. A. N. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.10.779 · Cited by 9 · see citing works
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Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
Loh, J. S., Mak, W. Q., Tan, L. K. S., Ng, C. X., Chan, H. H., Yeow, S. H., Foo, J. B., Ong, Y. S., How, C. W., & Khaw, K. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01743-1 · Cited by 1,193 · see citing works
The gut microbiota in anxiety and depression—A systematic review
Simpson, C. A., Diaz-Arteche, C., Eliby, D., Schwartz, O. S., Simmons, J. G., & Cowan, C. S. M. (2021) · Clinical Psychology Review · doi:10.1016/j.cpr.2020.101943 · Cited by 912 · see citing works
McGuinness, A. J., Davis, J. A., Dawson, S. L., Loughman, A., Collier, F., O’Hely, M., Simpson, C. A., Green, J., Marx, W., Hair, C., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01456-3 · Cited by 502 · see citing works
“These reviews align with our syntheses, and are also concordant with recent findings in other neurological and psychiatric conditions such as Parkinson’s disease [122], multiple sclerosis [123], autism spectrum disorder [124] and anxiety, which also report equivocal α-diversity findings [56].”
ResultSelf-citationAho, V. T. E., Houser, M. C., Pereira, P. A. B., Chang, J., Rudi, K., Paulin, L., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00427-6 · Cited by 435 · see citing works
Alli, S. R., Gorbovskaya, I., Liu, J. C. W., Kolla, N. J., Brown, L., & Müller, D. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094494 · Cited by 202 · see citing works
“Equivocal alpha diversity findings have also been reported in neuropsychiatric diseases with similar pathophysiologies to depression, including Parkinson’s disease [93], autism spectrum disorder [94], and anxiety [95].”
BackgroundParkinson’s Disease and Gut Microbiota
Hirayama, M., & Ohno, K. (2021) · Annals of Nutrition and Metabolism · doi:10.1159/000518147 · Cited by 158 · see citing works
Implications of Gut Microbiota in Neurodegenerative Diseases
Zhang, H., Chen, Y., Wang, Z., Xie, G., Liu, M., Yuan, B., Chai, H., Wang, W., & Cheng, P. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.785644 · Cited by 157 · see citing works
Caffeine and Parkinson’s Disease: Multiple Benefits and Emerging Mechanisms
Ren, X., & Chen, J. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.602697 · Cited by 150 · see citing works
Differences in Alpha Diversity of Gut Microbiota in Neurological Diseases
Li, Z., Zhou, J., Liang, H., Ye, L., Lan, L., Lü, F., Wang, Q., Lei, T., Yang, X., Cui, P., et al. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.879318 · Cited by 146 · see citing works
“Considering that different diseases have different pathological processes, the relationship between gut microbiota and disease progression may be more complex than just altered alpha diversity (Nuzum et al., 2020).”
BackgroundKline, E. M., Houser, M. C., Herrick, M. K., Seibler, P., Klein, C., West, A. B., & Tansey, M. G. (2020) · Movement Disorders · doi:10.1002/mds.28411 · Cited by 131 · see citing works
“In some populations, exposure to tuberculosis itself increases the risk for iPD.(119) Beyond infection, the activity of gastrointestinal microbes is increasingly being investigated in relation to PD pathology.”
BackgroundHall, D. A., Voigt, R. M., Cantu-Jungles, T. M., Hamaker, B., Engen, P. A., Shaikh, M., Raeisi, S., Green, S. J., Naqib, A., Forsyth, C. B., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36497-x · Cited by 124 · see citing works
“5 times normal, (4) abnormal liver function defined by ALT/AST > 4 times normal or elevated bilirubin, (5) antibiotic use within the 12 weeks prior to enrollment, (6) consumption of probiotics, prebiotics, or synbiotics within four weeks prior to enrollment, (7) consumption of a non-standard diet (e.”
BackgroundDumitrescu, L., Marta, D., Dănău, A., Lefter, A., Tulbă, D., Cozma, L., Manole, E., Gherghiceanu, M., Ceafalan, L. C., & Popescu, B. O. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.689723 · Cited by 100 · see citing works
Han, D., Gao, P., Li, R., Tan, P., Xie, J., Zhang, R., & Li, J. (2020) · Journal of Advanced Research · doi:10.1016/j.jare.2020.07.010 · Cited by 93 · see citing works
Role of gut microbiota-derived signals in the regulation of gastrointestinal motility
Zheng, Z., Tang, J., Hu, Y., & Zhang, W. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.961703 · Cited by 91 · see citing works
Zang, Y., Lai, X., Li, C., Ding, D., Wang, Y., & Zhu, Y. (2023) · Mediators of Inflammation · doi:10.1155/2023/5127157 · Cited by 88 · see citing works
“2020 [47] SR May 27, 2018 to 13 Case-control Next-generation sequencing 11 PD 1587 6 Mediators of Inflammation”
Li, Y., Shao, L., Mou, Y., Zhang, Y., & Ping, Y. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1957407 · Cited by 81 · see citing works
“It has been suggested that α-diversity analysis and Firmicutes/Bacteroidetes (F/B) ratio, two frequently used criteria in microbiome analysis, are not reliable in investigating the association between GM alteration and PD.(6,39) Interestingly, we also found inconsistent results of α-diversity, F/B ratio and GM changes…”
BackgroundResultInfluentialGenome-Scale Metabolic Modeling of the Human Microbiome in the Era of Personalized Medicine
Heinken, A., Basile, A., Hertel, J., Thinnes, C. C., & Thiele, I. (2021) · Annual Review of Microbiology · doi:10.1146/annurev-micro-060221-012134 · Cited by 75 · 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
“Rotenone treatment markedly altered the gut bacterial composition and increased gut microbiota diversity (Figure 6), which is consistent with the higher diversity of intestinal microbiota in patients with PD compared to that in healthy people [47,50].”
BackgroundFrom Dysbiosis to Neurodegenerative Diseases through Different Communication Pathways: An Overview
Intili, G., Paladino, L., Rappa, F., Alberti, G., Plicato, A., Calabrò, F., Fucarino, A., Cappello, F., Bucchieri, F., Tomasello, G., et al. (2023) · Biology · doi:10.3390/biology12020195 · Cited by 61 · see citing works
“mechanisms of the amino acids, the carbohydrates, and the xenobiotics [32,33].”
BackgroundLiang, Y., Cui, L., Gao, J., Zhu, M., Zhang, Y., & Zhang, H. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02375-0 · Cited by 59 · see citing works
Gentile, F., Doneddu, P. E., Riva, N., Nobile‐Orazio, E., & Quattrini, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207471 · Cited by 57 · see citing works
“Two meta-analyses showed that higher abundances of families Verrucomicrobiaceae and Lactobacillaceae, and genera Akkermansia, Lactobacillus, Bifidobacterium were found in PD patients compared to controls, together with lower abundances of SCFA-producing bacteria, including families Lachnospiraceae and Prevotellaceae a…”
BackgroundResultMurray, N., Khalaf, S. Y. A., Bastiaanssen, T. F. S., Kaulmann, D., Lonergan, E., Cryan, J. F., Clarke, G. A., Khashan, A. S., & O’Connor, K. (2023) · Schizophrenia Bulletin · doi:10.1093/schbul/sbad049 · Cited by 60 · 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
“, shift in Firmicute / Bacteroidetes ratio) (Keshavarzian et al., 2015; Sun and Shen, 2018; Li et al., 2021; Unger et al., 2016; Nuzum et al., 2020; Bullich et al., 2019; Gerhardt and Mohajeri, 2018; Lin et al., 2019).”
Getachew, B., Csoka, A. B., Bhatti, A., Copeland, R., & Tizabi, Y. (2020) · Neurotoxicity Research · doi:10.1007/s12640-020-00238-5 · Cited by 51 · see citing works
Host-mycobiome metabolic interactions in health and disease
Begum, N., Harzandi, A., Lee, S., Uhlén, M., Moyes, D. L., & Shoaie, S. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2121576 · Cited by 48 · see citing works
Novel Pharmacotherapies in Parkinson’s Disease
Tizabi, Y., Getachew, B., & Aschner, M. (2021) · Neurotoxicity Research · doi:10.1007/s12640-021-00375-5 · Cited by 43 · see citing works
“This contention is further supported by the observation that the composition of the gut microbiota and SCFAs might be altered in patients with PD (Unger et al. 2016; Nuzum et al. 2020; Shin et al. 2020).”
ResultGut 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
Avagliano, C., Coretti, L., Lama, A., Pirozzi, C., Caro, C. D., Biase, D. D., Turco, L., Mollica, M. P., Paciello, O., Calignano, A., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126367 · Cited by 39 · see citing works
Guan, Y., Tang, G., Li, L., Shu, J., Zhao, Y., Huang, L., & Tang, J. (2024) · Archives of Pharmacal Research · doi:10.1007/s12272-023-01484-9 · Cited by 41 · see citing works
Chu, C., Li, T., Yu, L., Li, Y. H., Li, M., Guo, M., Zhao, J., Zhai, Q., Tian, F., & Chen, W. (2023) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.2c07606 · Cited by 38 · see citing works
The critical role of gut-brain axis microbiome in mental disorders
Basiji, K., Sendani, A. A., Ghavami, S. B., Farmani, M., Kazemifard, N., Sadeghi, A., Lotfali, E., & Aghdaei, H. A. (2023) · Metabolic Brain Disease · doi:10.1007/s11011-023-01248-w · Cited by 36 · see citing works
“Also, it was suggested a reduction in SCFA-producing bac - teria such as Lachnospiraceae , Blautia , Faecalibacterium , and Roseburia which may lead to PD development (Nuzum et al. 2020 ).”
BackgroundBai, F., You, L., Lei, H., & Li, X. (2024) · Experimental Gerontology · doi:10.1016/j.exger.2024.112444 · Cited by 36 · see citing works
“In a previous systematic review that focused on GM in PD cases (Boertien et al., 2019; Nuzum et al., 2020), the authors summarized the qualitative associations of GM and PD cases and drew conclusions that proposed abundance differences were more associated with PD than microbiota diversity.”
Gastrointestinal Dysfunction in Parkinson’s Disease
Safarpour, D., Sharzehi, K., & Pfeiffer, R. F. (2022) · Drugs · doi:10.1007/s40265-021-01664-1 · Cited by 36 · see citing works
“Alterations in the gut microbiota in the setting of PD have been reported by numerous investigators and there has been growing interest in the possibility that changes in the gut microbiota may play a role in the genesis of PD itself [40].”
BackgroundLi, 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
Kulcsarova, K., Bang, C., Berg, D., & Schaeffer, E. (2023) · Journal of Parkinson’s Disease · doi:10.3233/jpd-230206 · Cited by 40 · see citing works
“As for microbiome changes in PD, the broad heterogeneity of findings has a number of possible reasons [250]; however, brain-/body-first phenotypes [251].”
Backgroundvan Vuuren, M. J., Nell, T. A., Carr, J. A., Kell, D. B., & Pretorius, E. (2020) · Biomolecules · doi:10.3390/biom11010030 · Cited by 31 · see citing works
“, (2020) review literature that discussed gut microbiota differences between PD groups and controls, and suggested that were variations may potentially be the cause of PD pathophysiology [19].”
BackgroundInfluentialDifferences in the gut microbiome across typical ageing and in Parkinson's disease
Nuzum, N. D., Szymlek‐Gay, E. A., Loke, S., Dawson, S. L., Teo, W., Hendy, A. M., Loughman, A., & Macpherson, H. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109566 · Cited by 32 · see citing works
Self-citationPotential effects of the most prescribed drugs on the microbiota-gut-brain-axis: A review
Garg, K., & Mohajeri, M. H. (2024) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2024.110883 · Cited by 29 · see citing works
“…Cornebacterium, Alistipes, Escherichia and Megasphaera is reported in PD patients (Bell et al., 2019; Chapelet et al., 2019; Chen and Lin, 2022; Gerhardt and Mohajeri, 2018; Li et al., 2019; Nuzum et al., 2020; Pellegrini et al., 2018; Rajput et al., 2021; Ryman et al., 2023; Zhang et al., 2022).”
Parkinson's Disease and the Gut: Models of an Emerging Relationship
Bindas, A. J., Kulkarni, S., Koppes, R. A., & Koppes, A. N. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.03.071 · 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
Dong, R., Lin, H., Chen, X., Shi, R., Yuan, S., Li, J., Zhu, B., Xu, X., Shen, W., Wang, K., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.723840 · Cited by 24 · see citing works
Ahn, E. H., Liu, X., Alam, A. M., Kang, S. S., & Ye, K. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01910-2 · Cited by 22 · see citing works
“Thus, it has been proposed that the abundance differences are more associated with PD than microbiota diversity [41].”
BackgroundTo the Gut Microbiome and Beyond: The Brain-First or Body-First Hypothesis in Parkinson’s Disease
Nuzum, N. D., Loughman, A., Szymlek‐Gay, E. A., Teo, W., Hendy, A. M., & Macpherson, H. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.791213 · Cited by 21 · see citing works
Self-citationRees, J., Ryan, J. C., Laws, M., & Devine, A. (2023) · Nutritional Neuroscience · doi:10.1080/1028415x.2023.2233727 · Cited by 23 · 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
Vendrik, K. E. W., Chernova, V. O., Kuijper, E. J., Terveer, E. M., van Hilten, J. J., & Contarino, M. F. (2023) · BMJ Open · doi:10.1136/bmjopen-2023-071766 · Cited by 19 · see citing works
Han, W., Wang, N., Han, M., Ban, M., Sun, T., & Xu, J. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1029495 · Cited by 18 · see citing works
“Recent findings in other psychiatric disorders, such as Parkinson’s disease and autism spectrum disorder, have also reported equivocal alpha diversity findings (Ho et al., 2020; Nuzum et al., 2020).”
ResultMore than just a number: the gut microbiota and brain function across the extremes of life
Nuzum, N. D., Deady, C., Kittel‐Schneider, S., Cryan, J. F., O’Mahony, S. M., & Clarke, G. A. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2418988 · Cited by 20 · see citing works
“10,39,40 Less research has been conducted on additional neurodegenerative conditions, e.g., Multiple Sclerosis (MS), Huntington's disease (HD), and Amyotrophic lateral Sclerosis (ALS), however these fields have been expanding in recent years.”
Self-citationGut microbiota of Parkinson’s disease in an appendectomy cohort: a preliminary study
Nakahara, K., Nakane, S., Ishii, K., Ikeda, T., & Ando, Y. (2023) · Scientific Reports · doi:10.1038/s41598-023-29219-2 · Cited by 18 · 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
“[23], in which reduced levels of SCFA-producing bacteria (particularly butyrate-producing bacteria) were common among people with PD.”
BackgroundXiromerisiou, G., Marogianni, C., Androutsopoulou, A., Ntavaroukas, P., Mysiris, D. S., & Papoutsopoulou, S. (2023) · Biology · doi:10.3390/biology12010093 · Cited by 17 · see citing works
Infectious Agents as Potential Drivers of α‐Synucleinopathies
Linard, M., Ravier, A., Mougué, L., Grgurina, I., Boutillier, A., Foubert‐Samier, A., Blanc, F., & Helmer, C. (2022) · Movement Disorders · doi:10.1002/mds.28925 · Cited by 16 · see citing works
The Association between Functional Dyspepsia and Metabolic Syndrome—The State of the Art
Volarić, M., Šojat, D., Majnarić, L. T., & Vučić, D. (2024) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph21020237 · Cited by 15 · see citing works
“There are differences in the composition of the gut microbiota between healthy people and people with metabolic, immunological, and neurological diseases [39,40,43,44].”
BackgroundShen, S., Zhang, C., Xu, Y.-M., & Shi, C.-H. (2021) · Journal of Parkinson s Disease · doi:10.3233/jpd-212929 · Cited by 15 · see citing works
“It has also been shown that not only the concentration of beneficial fecal short chain fatty acids (SCFA), but also the abundance of SCFA-producing bacteria were lower in the PD group than in the control group [95, 96].”
BackgroundXiang, M., Zheng, L., Pu, D., Lin, F., Ma, X., Ye, H., Pu, D., Zhang, Y., Wang, D., Wang, X., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.909729 · Cited by 14 · see citing works
Manole, E., Dumitrescu, L., Niculite, C. M., Popescu, B. O., & Ceafalan, L. C. (2021) · Biocell · doi:10.32604/biocell.2021.013452 · Cited by 14 · see citing works
“Endotoxins–Lipopolysaccharide Research has shown a correlation between PD and alterations in gut microbiota, as well as gastrointestinal inflammation (Heintz-Buschart et al., 2018; Hill-Burns et al., 2017; Houser et al., 2018; Houser and Tansey, 2017; Nuzum et al., 2020; Schwiertz et al., 2018).”
BackgroundInfluentialYao, L., Yang, Y., Yang, X., & Rezaei, M. J. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04151-2 · Cited by 13 · see citing works
“…to shifts in the gut microbiota composition in the fecal samples of PD patients, it was observed that the levels of short-chain fatty acids (SCFAs) (products of specific gut bacteria metabolism) in the feces of individuals with PD were significantly lower compared to those in healthy controls [81].”
Sánchez-de-Lara-Sánchez, S., & Sánchez‐Pérez, A. M. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-220615 · Cited by 13 · see citing works
“• ADHD [132] • Anxiety, depression [133] • Bipolar disorder [134] • Schizophrenia [135] • Epilepsy [136] • Parkinson’s disease [137, 138] • Alzheimer’s disease [139, 140] Neuropathological findings in the brain of patients with Alzheimer’s disease (AD) are amyloid plaques composed of amyloid-(cid:2)…”
Moreno, L. O., Bagüés, A., Martı́nez, V., & Abalo, R. (2023) · Nutrients · doi:10.3390/nu15122775 · Cited by 11 · see citing works
The role of the gut microbiota in neuropsychiatric disorders and therapy
Zhang, F., Ding, K., Zhang, L., Liu, D., Dong, X., Wang, M., Zhou, F.-L., Sun, Y., Zhang, W., Yu, Y., et al. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102894 · Cited by 11 · see citing works
Impact of Phellinus gilvus mycelia on growth, immunity and fecal microbiota in weaned piglets
Sun, Y., Zhong, S. S., Deng, B., Jin, Q., Wu, J., Huo, J., Zhu, J., Zhang, C., & Li, Y. (2020) · PeerJ · doi:10.7717/peerj.9067 · Cited by 10 · see citing works
Gu, X. Q., Tang, J., & Chen, C. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1627406 · Cited by 9 · see citing works
The Enteric Nervous System as a Mediator of Microbiota‐Gut‐Brain Interactions in Parkinson's Disease
Valdetaro, L., Ricciardi, M. C., Almeida, P. G., Stockler‐Pinto, M. B., & Gomes, A. L. T. (2026) · Journal of Neurochemistry · doi:10.1111/jnc.70339 · Cited by 8 · see citing works
“Clinical investigations across diverse populations worldwide (Nuzum et al. 2020; Mehanna et al. 2023; Proano et al. 2023; Zhang, Tang, and Guo 2023) have linked alterations in bacterial phyla, families, and genera to the multiple phenotypes of the disease, as well as onset time, duration, and…”
Boziki, M. K., Theotokis, P., Kesidou, E., Nella, M., Bakirtzis, C., Karafoulidou, E., Tzitiridou‐Chatzopoulou, M., Doulberis, M., Kazakos, E. I., Deretzi, G., et al. (2024) · Neurology International · doi:10.3390/neurolint16060127 · Cited by 8 · see citing works
“To our knowledge, however, no clinical evidence of an association between Hp and/or other Helicobacter species with ALS in humans has been reported.”
Immune-microbiome interplay and its implications in neurodegenerative disorders
Uniyal, A., Tiwari, V., Rani, M., & Tiwari, V. (2021) · Metabolic Brain Disease · doi:10.1007/s11011-021-00807-3 · Cited by 9 · see citing works
“Further, several studies claim the fact that gut microbiome is altered in PD condition (Nuzum et al. 2020; Vascellari et al. 2021).”
BackgroundAn Overview of Gastrointestinal Dysfunction in Parkinsonian Syndromes
Talman, L. S., & Safarpour, D. (2023) · Seminars in Neurology · doi:10.1055/s-0043-1771461 · Cited by 8 · see citing works
Gut microbial dysbiosis aggravated Parkinson-like pathology induced by MPTP/probenecid
Chen, Q.-Z., Shang, J., Jiang, Y., Yang, Y., Zang, C., Ma, J., Dong, Y.-R., Wang, J., Zhou, N., Yang, X., et al. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115008 · Cited by 7 · see citing works
Alterations of Gut Microbiota and Microbial Metabolites in Parkinson’s Disease: A Systematic Review
Davoody, S., Vakili, K. G., Jazi, K., Fathi, M., Heidari‐Foroozan, M., Mofidi, S. A., Taremi, M., Taherkhani, A., Azadnajafabad, S., Hojjatipour, F., et al. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-05598-7 · Cited by 7 · see citing works
Gastrointestinal dysfunction in Parkinson's disease
Timpka, J., & Odin, P. (2021) · International review of movement disorders · doi:10.1016/bs.irmvd.2021.07.004 · Cited by 7 · see citing works
Hu, Y., Wang, H., Zhong, Y., & Sun, Y. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e38645 · Cited by 5 · see citing works
“This can bring about central nervous system glial cell activation, the generation of pro-inflammatory signaling molecules, and oxidative stress, which may be significant mechanisms contributing to the neurodegenerative process in PD [17].”
BackgroundAggregation of alpha-synuclein in enteric neurons does not impact function in vitro
Bindas, A. J., Nichols, K. N., Roth, N. J., Brady, R., Koppes, A. N., & Koppes, R. A. (2022) · Scientific Reports · doi:10.1038/s41598-022-26543-x · Cited by 6 · see citing works
“As increased butyrate levels have been linked to positive effects to PD 1,24–26 , future work must parse out how butyrate may support a reduction of PFF tag signal and whether such clearance induces or avoids subsequent toxicity.”
InfluentialThe Role of the Gut Microbiome in Bipolar Disorder and its Common Medical Comorbidities
Jones, G. H., Pinjari, O. F., Vecera, C. M., Smith, K., Barrera, A., & Machado‐Vieira, R. (2023) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2023.101078 · Cited by 5 · see citing works
Kanda, A., Mazumder, A., Das, S., & Prabhakar, V. (2023) · Journal of Natural Remedies · doi:10.18311/jnr/2023/33944 · Cited by 4 · see citing works
The Influence of Gut Microbiota in Psychosis
Murray, N., Ghomi, R. H., Nemani, K., & O’Connor, K. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-99971-7.00018-7 · Cited by 3 · see citing works
Elford, J. D., Heesbeen, E. J., van der Plaats, N. A., Garssen, J., Kraneveld, A. D., Groenink, L., & Perez‐Pardo, P. (2026) · npj Parkinson s Disease · doi:10.1038/s41531-025-01236-0 · Cited by 2 · see citing works
Zhang, Z., Zhang, B., Yu, W., Jia, Q., Zhu, R., Li, M., Li, J., Wang, Y., Yu, L., Song, Z., et al. (2026) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2026.125421 · Cited by 2 · see citing works
The Microbial and Metabolic Link Between Gut and Brain
Salamalek, R., Shareef, Y., Abdulridha, F., & Soliman, S. S. M. (2025) · Springer eBooks · doi:10.1007/978-981-96-1305-2_17 · Cited by 1 · see citing works
Dietary tributyrin supplementation in Parkinson’s disease: An open-label target engagement study
Bohnen, J. L. B., Roytman, S., Wigstrom, T. P., Vangel, R., Barr, J. E., Carli, G., Parks, S. M., Mittal, H., Martino, C., Kanel, P., et al. (2025) · Neurotherapeutics · doi:10.1016/j.neurot.2025.e00791 · Cited by 1 · see citing works
“Deficiencies in colonic butyrate-producing bacteria have been identified in the setting of PD [44,131 – 133].”
InfluentialTherapeutic potential of phytochemicals and role of gut microbiota in neurodegenerative diseases
Gupta, S. K., & Sharma, R. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-36372-6.00014-8 · Cited by 1 · see citing works
Can bacteria control the human brain?
Berdichevskiy, G. M., Ермоленко, Е. И., Suvorov, A. N., & Didur, M. D. (2025) · Communicative & Integrative Biology · doi:10.1080/19420889.2025.2603138 · Cited by 1 · see citing works
“Some authors associate Alzheimer’s disease with a decrease in butyrate levels in the body [14,15].”
New insights in non-motor symptoms in Parkinson’s disease
Falup‐Pecurariu, C., Fanciulli, A., Borgohain, R., Chaudhuri, К. R., & Metta, V. (2024) · Frontiers research topics · doi:10.3389/978-2-8325-4722-9 · Cited by 1 · see citing works
Associations Between the Microbiome and Neurocognitive and Neuropsychiatric Function
Lundwall, R. A. (2024) · doi:10.1093/oso/9780192870414.003.0024 · Cited by 1 · see citing works
Zhao, Q., Han, M., Du, Y., Zheng, J., Cao, Z., Lu, Y., & Lu, Y. (2023) · Research Square · doi:10.21203/rs.3.rs-3340050/v1
Microbiota–brain interactions in aging and neurodegeneration
Foster, J. A., & Clarke, G. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-814800-6.00009-1
Caffeine and its potential use in Parkinson's disease
Bagchi, A., & Biswas, S. (2024) · Tea in Health and Disease Prevention · doi:10.1016/b978-0-443-14158-4.00027-0
Sirkadiyen Ritim ve Bağırsak Mikrobiyotası: Sağlığın Senkronize Uyumu
Pınarlı, Ç., Karaağaç, R. M., & Usta, E. (2025) · Current Perspectives on Health Sciences · doi:10.58208/cphs.1596137
Aho, V. T. E., Houser, M. C., B., P. P. A., Chang, J., Rudi, K., Paulin, L. G., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Figshare · doi:10.6084/m9.figshare.13787926
Aho, V. T. E., Houser, M. C., B., P. P. A., Chang, J., Rudi, K., Paulin, L. G., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Figshare · doi:10.6084/m9.figshare.13787920
Aho, V. T. E., Houser, M. C., B., P. P. A., Chang, J., Rudi, K., Paulin, L. G., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Figshare · doi:10.6084/m9.figshare.13787932
Aho, V. T. E., Houser, M. C., B., P. P. A., Chang, J., Rudi, K., Paulin, L. G., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Figshare · doi:10.6084/m9.figshare.13787947
Aho, V. T. E., Houser, M. C., B., P. P. A., Chang, J., Rudi, K., Paulin, L. G., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Figshare · doi:10.6084/m9.figshare.13787935
Aho, V. T. E., Houser, M. C., B., P. P. A., Chang, J., Rudi, K., Paulin, L. G., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Figshare · doi:10.6084/m9.figshare.13787956
Aho, V. T. E., Houser, M. C., B., P. P. A., Chang, J., Rudi, K., Paulin, L. G., Hertzberg, V., Auvinen, P., Tansey, M. G., & Scheperjans, F. (2021) · Figshare · doi:10.6084/m9.figshare.13787941
Wang, S., Zhu, Y., Wang, J., Jin, W., Li, N., Li, Z., Chang, Y., Jiang, C. Q., & Wang, T. (2026) · Scientific Reports · doi:10.1038/s41598-026-43865-2
“Lachnospiraceae , Coprococcus , Ruminococcus , Blautia , and Roseburia are important SCFA-producing bacteria, and their abundance is significantly decreased in patients with PD 36,42–44 .”
Yu, T., & Fan, H. D. (2026) · Postgraduate Medical Journal · doi:10.1093/postmj/qgag017
Zhang, F., Xu, W., Zeng, R., Chen, J., & Huang, J. (2026) · Gut Microbes · doi:10.1080/19490976.2026.2649440
“61 Studies on several diseases have reported both positive and negative associations of α - diversity with disease status.”
- Authors
- Nuzum, N. D., Loughman, A., Szymlek-Gay, E. A., Hendy, A., Teo, W.-P., & Macpherson, H.
- Affiliations
- Deakin University (AU)
- Corresponding author
- Nuzum, Nathan D.
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2020-05
- Volume
- 112
- Pages
- 227-241
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W3005406928
- Cited by
- 103
- References
- 94
- Citations by year
- 2026: 9 · 2025: 9 · 2024: 15 · 2023: 21 · 2022: 20 · 2021: 20 · 2020: 9
- FWCI
- 1.68
- Type
- journal article
- Language
- en
- Open access
- green
- figshare.com
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- NIE Digital Repository (National Institute of Education, Nanyang Technological University) (submittedVersion)
- Funders
- Australian Government Research Training Program Scholarship
- 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, butyrate-producing bacteria, microbial diversity, olfactory dysfunction, gastrointestinal symptoms, older adults, bacterial metabolites
- MeSH terms
- Gastrointestinal Microbiome, Aging, Humans, Parkinson Disease
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