Exploring the connection between the gut microbiome and parkinson's disease symptom progression and pathology: implications for supplementary treatment options
Open accessAbstract
The contribution of the microbiota to induce gastrointestinal inflammation is hypothesized to be a key component of alpha-synuclein (aSyn) aggregation within the gastrointestinal (GI) tract in the pathological progression of Parkinson’s disease (PD). The function of the GI tract is governed by a system of neurons that form part of the enteric nervous system (ENS). The ENS hosts 100–500 million nerve cells within two thin layers lining the GI tract. The gut-brain axis (GBA) is the major communication pathway between the ENS and the central nervous system. It has become increasingly clear that the microbiota in the gut are key regulators of GBA function and help to maintain homeostasis in the immune and endocrine systems. The GBA may act as a possible etiological launching pad for the pathogenesis of age-related neurodegenerative diseases, such as PD, because of an imbalance in the gut microbiota. PD is a multi-faceted illness with multiple biological, immunological, and environmental factors contributing to its pathological progression. Interestingly, individuals with PD have an altered gut microbiota compared to healthy individuals. However, there is a lack of literature describing the relationship between microbiota composition in the gut and symptom progression in PD patients. This review article examines how the pathology and symptomology of PD may originate from dysregulated signaling in the ENS. We then discuss by targeting the imbalance within the gut microbiota such as prebiotics and probiotics, some of the prodromal symptoms might be alleviated, possibly curtailing the pathological spread of aSyn and ensuing debilitating motor symptoms.
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Disruption of GFAP in the enteric nervous system suggests that the gut microbiota affects gut neuromuscular structure as well as function, and that imbalance in the gut microbiota may act as a potential trigger for degenerative diseases.
“Additionally, disruption of GFAP in the ENS suggests that the gut microbiota affects gut neuromuscular structure as well as function, and that imbalance in the gut microbiota may act as a potential trigger for degenerative diseases (81).”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [81]
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Spillantini, M. G., Schmidt, M. L., Lee, V. M.-Y., Trojanowski, J. Q., Jakes, R., & Goedert, M. (1997) · Nature · doi:10.1038/42166 · Cited by 8,382 · see citing works
Mutation in the α-Synuclein Gene Identified in Families with Parkinson's Disease
Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., et al. (1997) · Science · doi:10.1126/science.276.5321.2045 · Cited by 8,240 · see citing works
Dauer, W., & Przedborski, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00568-3 · Cited by 5,469 · see citing works
Poewe, W., Seppi, K., Tanner, C. M., Halliday, G. M., Brundin, P., Volkmann, J., Schrag, A.-E., & Lang, A. E. (2017) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2017.13 · Cited by 5,415 · see citing works
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J.-J., Blugeon, S., Bridonneau, C., Furet, J.-P., Corthier, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804812105 · Cited by 4,413 · see citing works
Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease
Sampson, T. R., Debelius, J. W., Thron, T., Janssen, S., Shastri, G. G., Ilhan, Z. E., Challis, C., Schretter, C. E., Rocha, S., Gradinaru, V., et al. (2016) · Cell · doi:10.1016/j.cell.2016.11.018 · Cited by 3,622 · see citing works
Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis
Yano, J. M., Yu, K., Donaldson, G. P., Shastri, G. G., Ann, P., Ma, L., Nagler, C. R., Ismagilov, R. F., Mazmanian, S. K., & Hsiao, E. Y. (2015) · Cell · doi:10.1016/j.cell.2015.02.047 · Cited by 3,614 · see citing works
Dorsey, E. R., Elbaz, A., Nichols, E., Abbasi, N., Abd-Allah, F., Abdelalim, A., Adsuar, J. C., Ansha, M. G., Brayne, C., Choi, J.-Y. J., et al. (2018) · The Lancet Neurology · doi:10.1016/s1474-4422(18)30295-3 · Cited by 2,816 · see citing works
Stages in the development of Parkinson’s disease-related pathology
Braak, H., Ghebremedhin, E., Rüb, U., Bratzke, H., & Del Tredici, K. (2004) · Cell and Tissue Research · doi:10.1007/s00441-004-0956-9 · Cited by 2,689 · see citing works
The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems.
(2015) · PubMed Central · Cited by 2,540 · see citing works
The gut microbiota influences blood-brain barrier permeability in mice
Braniste, V., Al-Asmakh, M., Kowal, C., Anuar, F., Abbaspour, A., Tóth, M., Korecka, A., Bakocevic, N., Ng, L. G., Kundu, P., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009759 · Cited by 2,530 · see citing works
Fiber and prebiotics: Mechanisms and health benefits
Slavin, J. (2013) · Nutrients · doi:10.3390/nu5041417 · Cited by 2,340 · 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
Dysbiosis of the gut microbiota in disease
Carding, S., Verbeke, K., Vipond, D. T., Corfe, B. M., & Owen, L. J. (2015) · Microbial Ecology in Health & Disease · doi:10.3402/mehd.v26.26191 · Cited by 1,710 · see citing works
The vagus nerve at the interface of the microbiota-gut-brain axis
Bonaz, B., Bazin, T., & Pellissier, S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00049 · Cited by 1,397 · see citing works
Kim, S., Kwon, S.-H., Kam, T.-I., Panicker, N., Karuppagounder, S. S., Lee, S., Lee, J. H., Kim, W. R., Kook, M., Foss, C. A., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.035 · Cited by 1,397 · see citing works
Genetics of Parkinson's DiseasePreprint
Klein, C., & Westenberger, A. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a008888 · Cited by 1,370 · see citing works
Colonic bacterial composition in Parkinson's disease
Keshavarzian, A., Green, S. J., Engen, P. A., Voigt, R. M., Naqib, A., Forsyth, C. B., Mutlu, E., & Shannon, K. M. (2015) · Movement Disorders · doi:10.1002/mds.26307 · Cited by 1,281 · see citing works
Faecalibacterium prausnitzii and human intestinal health
Miquel, S., Martín, R., Rossi, O., Bermúdez‐Humarán, L. G., Chatel, J., Sokol, H., Thomas, M., Wells, J. M., & Langella, P. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.06.003 · Cited by 1,239 · see citing works
Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders
Breit, S., Kupferberg, A., Rogler, G., & Hasler, G. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00044 · Cited by 1,189 · see citing works
GABA-modulating bacteria of the human gut microbiota
Strandwitz, P., Kim, K. H., Terekhova, D., Liu, J. K., Sharma, A., Levering, J., McDonald, D., Dietrich, D., Ramadhar, T. R., Lekbua, A., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0307-3 · Cited by 1,170 · 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
Clinical progression in Parkinson disease and the neurobiology of axons
Cheng, H., Ulane, C. M., & Burke, R. E. (2010) · Annals of Neurology · doi:10.1002/ana.21995 · Cited by 1,012 · cited 1× · see citing works
“Along with the emergence of the cardinal motor symptoms, it is also at this time that around 60–80% of dopaminergic neurons have degenerated in the substantia nigra (SN) and approximately 80% of dopamine levels are depleted in the nigrostriatal terminals [5, 6].”
BackgroundAnalysis of the microbiome: Advantages of whole genome shotgun versus 16S amplicon sequencing
Ranjan, R., Rani, A., Metwally, A., McGee, H. S., & Perkins, D. L. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.12.083 · Cited by 981 · 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
van de Wouw, M., Boehme, M., Lyte, J. M., Wiley, N., Strain, C., O'Sullivan, O., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2018) · The Journal of Physiology · doi:10.1113/jp276431 · Cited by 789 · see citing works
Dietary prebiotics: current status and new definition
Gibson, G. R., Scott, K. P., Rastall, R. A., Tuohy, K. M., Hotchkiss, A. T., Dubert‐Ferrandon, A., Gareau, M. G., Murphy, E. F., Saulnier, D. M. A., Loh, G., et al. (2010) · Food Science & Technology Bulletin Functional Foods · doi:10.1616/1476-2137.15880 · Cited by 783 · see citing works
Factors affecting the composition of the gut microbiota, and its modulation
Hasan, N., & Yang, H. (2019) · PeerJ · doi:10.7717/peerj.7502 · Cited by 763 · see citing works
Sun, M.-F., Zhu, Y.-L., Zhou, Z.-L., Jia, X.-B., Xu, Y.-D., Yang, Q., Cui, C., & Shen, Y.-Q. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.02.005 · Cited by 736 · see citing works
Romano, S., Savva, G. M., Bedarf, J. R., Charles, I. G., Hildebrand, F., & Narbad, A. (2021) · npj Parkinson's Disease · doi:10.1038/s41531-021-00156-z · Cited by 707 · see citing works
5-Hydroxytryptamine (serotonin) in the gastrointestinal tract
Gershon, M. D. (2013) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0b013e32835bc703 · Cited by 617 · see citing works
Zhao, Z., Ning, J., Bao, X.-Q., Shang, M., Ma, J., Li, G., & Zhang, D. (2021) · Microbiome · doi:10.1186/s40168-021-01107-9 · Cited by 616 · see citing works
Vanuytsel, T., van Wanrooy, S., Vanheel, H., Vanormelingen, C., Verschueren, S., Houben, E., Salim Rasoel, S., Tόth, J., Holvoet, L., Farré, R., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-305690 · Cited by 615 · see citing works
Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., & Theodorou, V. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.024 · Cited by 612 · see citing works
Fecal microbiota transplantation: Review and update
Wang, J.-W., Kuo, C.-H., Kuo, F.-C., Wang, Y.-K., Hsu, W.-H., Yu, F.-J., Hu, H.-M., Hsu, P.-I., Wang, J.-Y., & Wu, D.-C. (2019) · Journal of the Formosan Medical Association · doi:10.1016/j.jfma.2018.08.011 · Cited by 576 · see citing works
The Synucleinopathies: Twenty Years On
Goedert, M., Jakes, R., & Spillantini, M. G. (2017) · Journal of Parkinson s Disease · doi:10.3233/jpd-179005 · Cited by 566 · see citing works
Wang, H.-X., & Wang, Y.-P. (2016) · Chinese Medical Journal · doi:10.4103/0366-6999.190667 · Cited by 546 · see citing works
Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses
Wakabayashi, K., Takahashi, H., Takeda, S., Ohama, E., & Ikuta, F. (1988) · Acta Neuropathologica · doi:10.1007/bf00687767 · Cited by 528 · see citing works
Helicobacter pylori infection: An overview of bacterial virulence factors and pathogenesis
Kao, C., Sheu, B., & Wu, J.-J. (2016) · Biomedical Journal · doi:10.1016/j.bj.2015.06.002 · Cited by 527 · 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
Gut microbiota and the neuroendocrine system
Farzi, A., Fröhlich, E. E., & Holzer, P. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0600-5 · Cited by 478 · see citing works
The effects of probiotics on depressive symptoms in humans: a systematic review
Wallace, C. J. K., & Milev, R. (2017) · Annals of General Psychiatry · doi:10.1186/s12991-017-0138-2 · Cited by 471 · see citing works
Chen, S. G., Stribinskis, V., Rane, M. J., Demuth, D. R., Gozal, E., Roberts, A. M., Jagadapillai, R., Liu, R., Choe, K., Shivakumar, B., et al. (2016) · Scientific Reports · doi:10.1038/srep34477 · Cited by 463 · see citing works
Determinants of dopaminergic neuron loss in Parkinson's disease
Surmeier, D. J. (2018) · FEBS Journal · doi:10.1111/febs.14607 · Cited by 455 · see citing works
Epidemiology of Parkinson's disease
Elbaz, A., Carcaillon‐Bentata, L., Kab, S., & Moisan, F. (2015) · Revue Neurologique · doi:10.1016/j.neurol.2015.09.012 · Cited by 450 · see citing works
A gut bacterial amyloid promotes α-synuclein aggregation and motor impairment in mice
Sampson, T. R., Challis, C., Jain, N., Moiseyenko, A., Ladinsky, M. S., Shastri, G. G., Thron, T., Needham, B. D., Horvath, I., Debelius, J. W., et al. (2020) · eLife · doi:10.7554/elife.53111 · Cited by 439 · see citing works
Aho, 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
Imaging the Role of Inflammation in Mood and Anxiety-related Disorders
Felger, J. C. (2017) · Current Neuropharmacology · doi:10.2174/1570159x15666171123201142 · Cited by 432 · see citing works
Brain-First versus Gut-First Parkinson’s Disease: A Hypothesis
Borghammer, P., & Van Den Berge, N. (2019) · Journal of Parkinson’s Disease · doi:10.3233/jpd-191721 · Cited by 419 · see citing works
Role of microbiota-derived short-chain fatty acids in nervous system disorders
Mirzaei, R., Bouzari, B., Hosseini‐Fard, S. R., Mazaheri, M., Ahmadyousefi, Y., Abdi, M., Jalalifar, S., Karimitabar, Z., Teimoori, A., Keyvani, H., et al. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111661 · Cited by 400 · see citing works
Escherichia coli Pathobionts Associated with Inflammatory Bowel Disease
Mirsepasi‐Lauridsen, H. C., Vallance, B. A., Krogfelt, K. A., & Petersen, A. M. (2019) · Clinical Microbiology Reviews · doi:10.1128/cmr.00060-18 · Cited by 374 · see citing works
Braak, H., & Del Tredici, K. (2017) · Journal of Parkinson’s Disease · doi:10.3233/jpd-179001 · Cited by 372 · see citing works
Taur, Y., Coyte, K. Z., Schlüter, J., Robilotti, E. V., Figueroa, C. J., Gjonbalaj, M., Littmann, E. R., Ling, L., Miller, L., Gyaltshen, Y., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aap9489 · Cited by 370 · see citing works
<scp>Meta‐Analysis</scp> of Gut Dysbiosis in Parkinson's Disease
Nishiwaki, H., Ito, M., Ishida, T., Hamaguchi, T., Maeda, T., Kashihara, K., Tsuboi, Y., Ueyama, J., Shimamura, T., Mori, H., et al. (2020) · Movement Disorders · doi:10.1002/mds.28119 · Cited by 370 · see citing works
Fukui, H. (2016) · Inflammatory Intestinal Diseases · doi:10.1159/000447252 · Cited by 358 · see citing works
Uemura, N., Yagi, H., Uemura, M. T., Hatanaka, Y., Yamakado, H., & Takahashi, R. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0257-5 · Cited by 328 · see citing works
Tryptophan Metabolism by Gut Microbiome and Gut-Brain-Axis: An in silico Analysis
Kaur, H., Bose, C., & Mande, S. S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01365 · Cited by 320 · see citing works
The Role of Gut Microbiota in Intestinal Inflammation with Respect to Diet and Extrinsic Stressors
Lobionda, S., Sittipo, P., Kwon, H. Y., & Lee, Y. K. (2019) · Microorganisms · doi:10.3390/microorganisms7080271 · Cited by 319 · see citing works
Gut Microbiota beyond Bacteria—Mycobiome, Virome, Archaeome, and Eukaryotic Parasites in IBD
Matijašić, M., Meštrović, T., Paljetak, H. Č., Perić, M., Barešić, A., & Verbanac, D. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082668 · Cited by 293 · see citing works
Andrews, Z. B., Erion, D., Beiler, R., Liu, Z.-W., Abizaid, A., Zigman, J., Elsworth, J. D., Savitt, J. M., DiMarchi, R., Tschöp, M., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3890-09.2009 · Cited by 289 · see citing works
Gut microbial metabolites in depression: understanding the biochemical mechanisms
Caspani, G., Kennedy, S. H., Foster, J. A., & Swann, J. R. (2019) · Microbial Cell · doi:10.15698/mic2019.10.693 · Cited by 285 · see citing works
Park, J.-S., Lee, E.-J., Lee, J.-C., Kim, W.-K., & Kim, H.-S. (2007) · International Immunopharmacology · doi:10.1016/j.intimp.2006.08.015 · Cited by 278 · see citing works
Liu, W.-H., Chuang, H.-L., Huang, Y.-T., Wu, C.-C., Chou, G.-T., Wang, S., & Tsai, Y.-C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.046 · Cited by 269 · see citing works
Jaglin, M., Rhimi, M., Philippe, C., Pons, N., Bruneau, A., Goustard, B., Daugé, V., Maguin, E., Naudon, L., & Rabot, S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00216 · Cited by 269 · see citing works
Liu, Y., Zhao, J., & Guo, W. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.02201 · Cited by 268 · see citing works
Gut microbiota in patients with Parkinson's disease in southern China
Lin, A., Zheng, W., He, Y., Tang, W., Wei, X., He, R., Huang, W., Su, Y., Huang, Y., Zhou, H., et al. (2018) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2018.05.007 · Cited by 253 · 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
Parkinson's Disease and Systemic Inflammation
Ferrari, C. C., & Tarelli, R. (2011) · Parkinson s Disease · doi:10.4061/2011/436813 · Cited by 218 · see citing works
Liu, J., Wang, F., Liu, S., Du, J., Hu, X., Xiong, J., Fang, R., Chen, W., & Sun, J. (2017) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2017.08.3235 · Cited by 218 · see citing works
Neuropathological evidence of body-first vs. brain-first Lewy body disease
Borghammer, P., Horsager, J., Andersen, K. B., Berge, N. V. D., Raunio, A., Murayama, S., Parkkinen, L., & Myllykangas, L. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105557 · Cited by 218 · see citing works
Regulation of gut luminal serotonin by commensal microbiota in mice
Hata, T., Asano, Y., Yoshihara, K., Kimura-Todani, T., Miyata, N., Zhang, X.-T., Takakura, S., Aiba, Y., Koga, Y., & Sudo, N. (2017) · PLOS ONE · doi:10.1371/journal.pone.0180745 · Cited by 211 · see citing works
The Bacterial Curli System Possesses a Potent and Selective Inhibitor of Amyloid Formation
Evans, M. L., Chorell, E., Taylor, J. D., Ådén, J., Götheson, A., Li, F., Koch, M., Sefer, L., Matthews, S., Wittung-Stafshede, P. E., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2014.12.025 · Cited by 210 · see citing works
Life style risks of Parkinson?s disease: Association between decreased water intake and constipation
Ueki, A., & Otsuka, M. (2004) · Journal of Neurology · doi:10.1007/s00415-004-1706-3 · Cited by 190 · see citing works
Effects of Probiotics on Cognitive Reactivity, Mood, and Sleep Quality
Marotta, A., Sarno, E., Del Casale, A., Pane, M., Mogna, L., Amoruso, A., Felis, G. E., & Fiorio, M. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00164 · Cited by 186 · see citing works
Fecal microbiota transplantation therapy for Parkinson's disease: A preliminary study
Xue, L.-J., Yang, X.-Z., Tong, Q., Shen, P., Ma, S.-J., Wu, S.-N., Zheng, J.-L., & Wang, H.-G. (2020) · Medicine · doi:10.1097/md.0000000000022035 · Cited by 186 · see citing works
Evaluation of fecal microbiota transplantation in Parkinson's disease patients with constipation
Kuai, X.-Y., Yao, X.-H., Xu, L.-J., Zhou, Y.-Q., Zhang, L.-P., Liu, Y., Pei, S.-F., & Zhou, C.-L. (2021) · Microbial Cell Factories · doi:10.1186/s12934-021-01589-0 · Cited by 179 · see citing works
Zhou, W., Bercury, K. K., Cummiskey, J., Luong, N., Lebin, J. A., & Freed, C. R. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.211029 · Cited by 178 · see citing works
Comparative Analysis of 16S rRNA Gene and Metagenome Sequencing in Pediatric Gut Microbiomes
Peterson, D., Bonham, K. S., Rowland, S., Pattanayak, C. W., & Klepac‐Ceraj, V. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.670336 · Cited by 178 · see citing works
Feng, W., Wu, Y., Chen, G., Fu, S., Li, B., Huang, B., Wang, D., Wang, W., & Liu, J. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000490981 · Cited by 176 · see citing works
Hsieh, T.-H., Kuo, C.-W., Hsieh, K.-H., Shieh, M.-J., Peng, C.-W., Chen, Y.-C., Chang, Y.-L., Huang, Y.-Z., Chen, C.-C., Chang, P.-K., et al. (2020) · Brain Sciences · doi:10.3390/brainsci10040206 · Cited by 174 · 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
Serotonin in the gut: Blessing or a curse
Banskota, S., Ghia, J., & Khan, W. I. (2018) · Biochimie · doi:10.1016/j.biochi.2018.06.008 · Cited by 166 · see citing works
The premotor phase of Parkinson's disease
TOLOSA, E. S., Compta, Y., & Gaig, C. (2007) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2007.06.007 · Cited by 165 · see citing works
Nair, A. T., Ramachandran, V., Joghee, N. M., Shanish Antony, A., & Ramalingam, G. (2018) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm17105 · Cited by 156 · see citing works
Enteric nervous system α-synuclein immunoreactivity in idiopathic REM sleep behavior disorder
Sprenger, F., Stefanova, N., Gelpí, E., Seppi, K., Navarro‐Otano, J., Offner, F. A., Vilas, D., Valldeoriola, F., Pont‐Sunyer, C., Aldecoa, I., et al. (2015) · Neurology · doi:10.1212/wnl.0000000000002126 · Cited by 146 · see citing works
Probiotics may have beneficial effects in parkinson’s disease: In vitro evidence
Magistrelli, L., Amoruso, A., Mogna, L., Graziano, T., Cantello, R., Pane, M., & Comi, C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00969 · Cited by 144 · see citing works
The Gut and Parkinson's Disease—A Bidirectional Pathway
Santos, S. F., de Oliveira, H. L., Yamada, E. S., Neves, B. C., & Pereira, A. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00574 · Cited by 144 · 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
Sulakhiya, K., Keshavlal, G. P., Bezbaruah, B. K., Dwivedi, S., Gurjar, S. S., Munde, N., Jangra, A., Lahkar, M., & Gogoi, R. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.11.031 · Cited by 140 · see citing works
Frucht, S. J. (2004) · The Neurologist · doi:10.1097/01.nrl.0000131146.08278.a5 · Cited by 139 · see citing works
Exposure to bacterial endotoxin generates a distinct strain of α-synuclein fibril
Kim, C., Lv, G., Lee, J. S., Jung, B. C., Masuda-Suzukake, M., Hong, C.-S., Valera, E., Lee, H.-J., Paik, S. R., Hasegawa, M., et al. (2016) · Scientific Reports · doi:10.1038/srep30891 · Cited by 138 · see citing works
Zacharowski, K., Zacharowski, P. A., Koch, A., Baban, A., Tran, N., Berkels, R., Papewalis, C., Schulze-Osthoff, K., Knuefermann, P., Zähringer, U., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601527103 · Cited by 134 · 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
Gastrointestinal Dysfunctions in Parkinson’s Disease: Symptoms and Treatments
Poirier, A.-A., Aubé, B., Côté, M., Morin, N., Di Paolo, T., & Soulet, D. (2016) · Parkinson s Disease · doi:10.1155/2016/6762528 · Cited by 130 · see citing works
Fecal Microbiota Transplantation: Is It Safe?
Park, S., & Seo, G. S. (2021) · Clinical Endoscopy · doi:10.5946/ce.2021.072 · Cited by 123 · see citing works
Gazewood, J. D., Richards, D., & Clebak, K. T. (2013) · PubMed · Cited by 117 · see citing works
Control of gastrointestinal motility by the “gut brain” – the enteric nervous system
Schemann, M. (2005) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/01.scs.0000180285.51365.55 · Cited by 115 · see citing works
Meta‐analysis: Association of <i>Helicobacter pylori</i> infection with Parkinson's diseases
Shen, X., Yang, H., Wu, Y., Zhang, D., & Jiang, H. (2017) · Helicobacter · doi:10.1111/hel.12398 · Cited by 114 · see citing works
Protection of dopaminergic cells from MPP+-mediated toxicity by histone deacetylase inhibition
Kidd, S. K., & Schneider, J. S. (2010) · Brain Research · doi:10.1016/j.brainres.2010.07.041 · Cited by 113 · see citing works
Becker, A., Schmartz, G. P., Gröger, L., Grammes, N., Galata, V., Philippeit, H., Weiland, J., Ludwig, N., Meese, E., Tierling, S., et al. (2022) · Genomics, Proteomics & Bioinformatics · doi:10.1016/j.gpb.2021.08.009 · Cited by 102 · see citing works
Musa, N. H., Mani, V., Lim, S. M., Vidyadaran, S., Majeed, A. B. A., & Ramasamy, K. (2017) · Journal of Dairy Research · doi:10.1017/s0022029917000620 · Cited by 100 · see citing works
Vakharia, K. V., & Hinson, J. P. (2004) · Endocrinology · doi:10.1210/en.2004-0882 · Cited by 95 · see citing works
Chorell, E., Andersson, E. K., Evans, M. L., Jain, N., Götheson, A., Ådén, J., Chapman, M. R., Almqvist, F., & Wittung-Stafshede, P. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0140194 · Cited by 88 · see citing works
α-Synuclein Is Expressed in Different Tissues During Human Fetal Development
Baltic, S., Perović, M., Mladenović, A., Zogovic, N. S., Ruždijić, S., Rakić, L., & Kanazir, S. (2004) · Journal of Molecular Neuroscience · doi:10.1385/jmn:22:3:199 · Cited by 88 · see citing works
Gut Inflammation in Association With Pathogenesis of Parkinson’s Disease
Chen, Q.-Q., Haikal, C., Li, W., & Li, J. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00218 · Cited by 88 · see citing works
Integrated neural and endocrine control of gastrointestinal function
Furness, J. B. (2016) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-27592-5_16 · Cited by 87 · see citing works
Endoplasmic Reticulum Stress Contributes to Helicobacter Pylori VacA-Induced Apoptosis
Akazawa, Y., Isomoto, H., Matsushima, K., Kanda, T., Minami, H., Yamaghchi, N., Taura, N., Shiozawa, K., Ohnita, K., Takeshima, F., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082322 · Cited by 84 · see citing works
Association ofHelicobacter pyloriwith Parkinson's Disease
Kandadai, R. M., Borgohain, R., Reddy, V. C., Bandaru, V. C. S. S., & Turaga, S. (2017) · Journal of Clinical Neurology · doi:10.3988/jcn.2017.13.2.181 · Cited by 72 · see citing works
Quinolinic Acid Amyloid-like Fibrillar Assemblies Seed α-Synuclein Aggregation
Tavassoly, O., Sade, D., Bera, S., Shaham‐Niv, S., Vocadlo, D. J., & Gazit, E. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.08.002 · Cited by 71 · see citing works
Dopamine Transporter Activity Is Modulated by α-Synuclein*
Butler, B., Saha, K., Rana, T., Becker, J., Sambo, D. O., Davari, P., Goodwin, J., & Khoshbouei, H. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.691592 · Cited by 65 · see citing works
Gastrointestinal Biopsies for the Diagnosis of Alpha-Synuclein Pathology in Parkinson’s Disease
Cersosimo, M. G. (2015) · Gastroenterology Research and Practice · doi:10.1155/2015/476041 · Cited by 61 · see citing works
Statin Decreases Helicobacter pylori Burden in Macrophages by Promoting Autophagy
Liao, W., Huang, M.-Z., Wang, M. L., Lin, C., Lu, T.-L., Lo, H., Pan, Y., Sun, Y., Kao, M.-C., Lim, H.-J., et al. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00203 · Cited by 60 · see citing works
Vedder, H., Schreiber, W., Yassouridis, A., Gudewill, S., Galanos, C., & Pollmächer, T. (1999) · Inflammation Research · doi:10.1007/s000110050408 · Cited by 58 · see citing works
From the baker to the bedside: yeast models of Parkinson's disease
Menezes, R., Tenreiro, S., Macedo, D., dos Santos, C. N., & Outeiro, T. F. (2015) · Microbial Cell · doi:10.15698/mic2015.08.219 · Cited by 54 · see citing works
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
Alfa, M. J., Strang, D. G., Tappia, P. S., Olson, N. L., DeGagné, P., Bray, D., Murray, B.-L., & Hiebert, B. M. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2017.00260 · Cited by 48 · see citing works
Environmental triggers of Parkinson's disease – Implications of the Braak and dual-hit hypotheses
Chen, H., Wang, K., Scheperjans, F., & Killinger, B. A. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105601 · Cited by 44 · see citing works
Wang, H., Dou, S., Zhu, J., Shao, Z., Wang, C., & Cheng, B. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147023 · Cited by 33 · see citing works
Helicobacter pylorilipopolysaccharide induces apoptosis of cultured guinea pig gastric mucosal cells
Kawahara, T., Teshima, S., Kuwano, Y., Oka, A., Kishi, K., & Rokutan, K. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.281.3.g726 · Cited by 31 · see citing works
Parkinson’s Disease and the Gut: Future Perspectives for Early Diagnosis
Harsányiová, J., Buday, T., & Trancikova, A. K. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00626 · Cited by 27 · see citing works
Anxiety in Parkinson’s Disease: Correlation with Depression and Quality of Life
Upneja, A., Paul, B. S., Jain, D., Choudhary, R., & Paul, G. (2021) · Journal of Neurosciences in Rural Practice · doi:10.1055/s-0041-1722840 · Cited by 27 · see citing works
Lipopolysaccharide Increases Plasma Levels of Corticotropin-Releasing Hormone in Rats
Goebel, M., Stengel, A., Wang, L., Reeve, J. R., & Taché, Y. (2010) · Neuroendocrinology · doi:10.1159/000322590 · Cited by 25 · see citing works
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Luo, T., Che, Q., Guo, Z., Song, T., Zhao, J., & Xu, D. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1442854 · Cited by 45 · see citing works
Hong, D., Zhang, C., Wu, W., Lu, X., & Zhang, L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1133546 · Cited by 38 · see citing works
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Chaudhary, S. A., Chaudhary, S. S., & Rawat, S. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1617106 · Cited by 42 · see citing works
Kerstens, R., & Joyce, P. (2024) · Biomedicines · doi:10.3390/biomedicines12081738 · Cited by 20 · see citing works
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Beheshti, I. (2025) · Cells · doi:10.3390/cells14100710 · Cited by 18 · see citing works
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Schmitt, V., Masanetz, R. K., Weidenfeller, M., Ebbinghaus, L. S., Süß, P., Rosshart, S. P., von Hörsten, S., Zunke, F., Winkler, J., & Xiang, W. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114574 · Cited by 16 · see citing works
Santos, S., Salinas, I., Almeida, N., & Caicedo, A. (2025) · Engineering Microbiology · doi:10.1016/j.engmic.2025.100222 · Cited by 13 · see citing works
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Candeias, E., Pereira-Santos, A. R., Empadinhas, N., Cardoso, S. M., & Esteves, A. R. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-240524 · Cited by 16 · see citing works
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Jha, S. S., Jeyaraman, N., Jeyaraman, M., Ramasubramanian, S., Muthu, S., Santos, G. S., da Fonseca, L. F., & Lana, J. F. (2025) · World Journal of Orthopedics · doi:10.5312/wjo.v16.i3.102274 · Cited by 13 · see citing works
Yang, J., Song, X., Yan, S., Li, Q., & Yang, W. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1739329 · Cited by 12 · see citing works
Advances in autonomic dysfunction research in Parkinson’s disease
Xu, H., Zheng, X., Xing, X., Bi, Z., Wang, D., Zhang, C., Wei, L., Jin, Y., & Xu, S. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1468895 · Cited by 11 · see citing works
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Verma, O., Faizan, M., Goswami, S., & Singh, M. P. (2025) · Archives of Toxicology · doi:10.1007/s00204-025-04088-y · Cited by 9 · see citing works
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Kopalli, S. R., Wankhede, N. L., Rahangdale, S. R., Sammeta, S. S., Aglawe, M. M., Koppula, S., Taksande, B. G., Upaganlawar, A., Umekar, M. J., & Kale, M. B. (2026) · Biogerontology · doi:10.1007/s10522-026-10389-1 · Cited by 6 · see citing works
Johri, S., Chan, D., Massey, R. S., Knight, D., DeRosa, M. C., Holahan, M. R., & Prakash, R. (2025) · npj Biosensing · doi:10.1038/s44328-025-00057-8 · Cited by 5 · see citing works
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Anwar, L., Ahmad, E., Imtiaz, M., Ahmad, M. I., Aziz, M. F., & Ibad, T. (2024) · Cureus · doi:10.7759/cureus.70337 · Cited by 6 · see citing works
Jakova, E., Aigbogun, O. P., Moutaoufik, M. T., Allen, K. J. H., Munir, O., Brown, D., Taghibiglou, C., Babu, M., Phenix, C. P., Krol, E. S., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179386 · Cited by 4 · see citing works
Cossais, F., Hoernke, M., Schröder, K., Lucius, R., Bottner, M. B., Egberts, J. D., Richter, F., & Wedel, T. (2025) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2025.02.009 · Cited by 3 · see citing works
Chambilo, B., Dhiver, T., Sahu, K., & Parashar, R. (2025) · Neurological Sciences and Neurophysiology · doi:10.4103/nsn.nsn_39_25 · Cited by 2 · see citing works
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Vijay, A., Ahmad, F., Sudesh, R., & Balakrishnan, A. (2024) · Springer eBooks · doi:10.1007/978-981-99-8803-7_3 · Cited by 2 · see citing works
Hosseini, L., Farshbaf‐Khalili, A., Jazani, A. M., & Maghsoumi‐Norouzabad, L. (2025) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-025-04740-5 · Cited by 1 · see citing works
Jin, Y., Ren, R., Tian, X., & Ye, D. (2026) · Frontiers in Neurology · doi:10.3389/fneur.2026.1720699 · Cited by 1 · see citing works
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Mafra, H. T., & de Souza, J. P. P. (2024) · Brazilian Journal of Health Review · doi:10.34119/bjhrv7n4-011
Aguena, M. Y., Ogata, A. C. D. O., Baptista, J. V. D. C. N., Pereira, L. F. S., Ramalho, G. O., Hubner, M. L. R. D. P., Forti, L. K., Senssulini, V. L., de Melo, S. O. S., Meireles, I. S., et al. (2025) · International Journal of Health Science · doi:10.22533/at.ed.159552515015
Yuan, C., & Jin, N. (2026) · Acupuncture & Electro-Therapeutics Research · doi:10.1177/03601293261444540
- Authors
- Chan, D. G., Ventura, K., Villeneuve, A., Du Bois, P., & Holahan, M. R.
- Affiliations
- Carleton University (CA)
- Department of Neuroscience, Carleton University, Ottawa, ON, Canada
- Corresponding author
- Chan, Dennis G.
- Venue
- Journal of Parkinson's Disease
- Publisher
- SAGE Publications
- Published
- 2022-12-16
- Volume
- 12
- Issue
- 8
- Pages
- 2339-2352
- ISSN
- 1877-7171 (ISSN-L)
- 1877-718X
- PMC
- PMC9837702
- OpenAlex
- W4306747523
- Cited by
- 24
- References
- 122
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 7 · 2023: 2
- FWCI
- 0.72
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Parkinson s Disease (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- Parkinson's disease, gut microbiota, gut-brain axis, enteric nervous system, alpha-synuclein aggregation, gastrointestinal inflammation, symptom progression, prebiotics, probiotics, neurodegeneration, motor symptoms
- MeSH terms
- Gastrointestinal Microbiome, Central Nervous System, Homeostasis, Humans, Parkinson Disease, Enteric Nervous System
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