The Role of the Gut Microbiota in the Pathogenesis of Parkinson's Disease
Open accessAbstract
It is well-recognized that the gut microbiota (GM) is crucial for gut function, metabolism, and energy cycles. The GM also has effects on neurological outcomes via many mechanisms, such as metabolite production and the gut-brain axis. Emerging evidence has gradually indicated that GM dysbiosis plays a role in several neurological diseases, such as Parkinson's disease (PD), Alzheimer's disease, depression, and multiple sclerosis. Several studies have observed that PD patients generally suffer from gastrointestinal disorders and GM dysbiosis prior to displaying motor symptoms, but the specific link between the GM and PD is not clearly understood. In this review, we aim to summarize what is known regarding the correlation between the GM and PD pathologies, including direct, and indirect evidence.
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More than 80% of patients with Parkinson's disease experience severe gastrointestinal symptoms such as constipation, nausea and vomiting.
“More than 80% of patients with Parkinson's disease experience a variety of severe gastrointestinal symptoms such as constipation, nausea and vomiting.9”
From The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options (2021) · cites this paper as [9]
Patients with PD have an intestinal microbiota disorder, specifically increased abundance of Lactobacillus and Enterobacteriaceae and decreased abundance of Prevotella, Clostridium coccoides, and Bacteroides fragilis.
“Patients with PD have an intestinal microbiota disorder, which is specifically manifested in the increased abundance of Lactobacillus and Enterobacteriaceae and the decreased abundance of Prevotella, Clostridium coccoides, and Bacteroides fragilis [9, 10].”
From Neuroprotective Effect of Ceftriaxone on MPTP‐Induced Parkinson’s Disease Mouse Model by Regulating Inflammation and Intestinal Microbiota (2021) · cites this paper as [10]
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Staging of brain pathology related to sporadic Parkinson’s disease
Braak, H., Tredici, K. D., Rüb, U., de Vos, R. A. I., Jansen Steur, E. N. H., & Braak, E. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00065-9 · Cited by 10,777 · see citing works
Pattern Recognition Receptors and Inflammation
Takeuchi, O., & Akira, S. (2010) · Cell · doi:10.1016/j.cell.2010.01.022 · Cited by 8,895 · see citing works
Dietary Modulation of the Human Colonic Microbiota: Introducing the Concept of Prebiotics
Gibson, G. R., & Roberfroid, M. B. (1995) · Journal of Nutrition · doi:10.1093/jn/125.6.1401 · Cited by 7,659 · see citing works
Enterotypes of the human gut microbiome
MetaHIT Consortium (additional members), Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., et al. (2011) · Nature · doi:10.1038/nature09944 · Cited by 7,548 · see citing works
Host-gut microbiota metabolic interactions
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012) · Science · doi:10.1126/science.1223813 · Cited by 4,760 · see citing works
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572 · see citing works
Structural and functional features of central nervous system lymphatic vessels
Louveau, A., Smirnov, I., Keyes, T. J., Eccles, J. D., Rouhani, S. J., Peske, J. D., Derecki, N. C., Castle, D., Mandell, J. W., Lee, K. S., et al. (2015) · Nature · doi:10.1038/nature14432 · 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
Mechanisms underlying inflammation in neurodegeneration
Glass, C. K., Saijo, K., Winner, B., Marchetto, M. C., & Gage, F. H. (2010) · Cell · doi:10.1016/j.cell.2010.02.016 · Cited by 3,580 · see citing works
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228 · see citing works
Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress
Tsigos, C., & Chrousos, G. P. (2002) · Journal of Psychosomatic Research · doi:10.1016/s0022-3999(02)00429-4 · Cited by 2,822 · see citing works
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735 · see citing works
Liu, J. Z., van Sommeren, S., Huang, H., Ng, S. C., Alberts, R., Takahashi, A., Ripke, S., Lee, J. C., Jostins, L., Shah, T., et al. (2015) · Nature Genetics · doi:10.1038/ng.3359 · Cited by 2,603 · see citing works
Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants
Hueck, C. J. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.2.379-433.1998 · Cited by 2,384 · see citing works
Singh, N., Gurav, A., Sivaprakasam, S., Brady, E., Padia, R., Shi, H., Thangaraju, M., Prasad, P. D., Manicassamy, S., Munn, D. H., et al. (2014) · Immunity · doi:10.1016/j.immuni.2013.12.007 · Cited by 2,368 · 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
The epidemiology of Parkinson's disease: risk factors and prevention
Ascherio, A., & Schwarzschild, M. A. (2016) · The Lancet Neurology · doi:10.1016/s1474-4422(16)30230-7 · Cited by 1,843 · see citing works
Dysbiosis and the immune system
Levy, M., Kolodziejczyk, A. A., Thaiss, C. A., & Elinav, E. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.7 · Cited by 1,769 · see citing works
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Braak, H., R�b, U., Gai, W. P., & Del Tredici, K. (2003) · Journal of Neural Transmission · doi:10.1007/s00702-002-0808-2 · Cited by 1,683 · see citing works
The interplay between the intestinal microbiota and the brain
Collins, S. M., Surette, M., & Bercik, P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2876 · Cited by 1,611 · see citing works
Regulation of intestinal epithelial permeability by tight junctions
Suzuki, T. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1070-x · Cited by 1,365 · see citing works
Braak, H., de Vos, R. A. I., Bohl, J., & Del Tredici, K. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.11.012 · Cited by 1,354 · see citing works
Alzheimer's Disease and Parkinson's Disease
Nussbaum, R. L., & Ellis, C. E. (2003) · New England Journal of Medicine · doi:10.1056/nejm2003ra020003 · Cited by 1,351 · see citing works
Type III Secretion Machines: Bacterial Devices for Protein Delivery into Host Cells
Galán, J. E., & Collmer, A. (1999) · Science · doi:10.1126/science.284.5418.1322 · Cited by 1,323 · see citing works
Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation
Browne, H. P., Forster, S. C., Anonye, B. O., Kumar, N., Neville, B. A., Stares, M. D., Goulding, D., & Lawley, T. D. (2016) · Nature · doi:10.1038/nature17645 · Cited by 1,299 · 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
Diet, gut microbiota and immune responses
Maslowski, K. M., & Mackay, C. R. (2011) · Nature Immunology · doi:10.1038/ni0111-5 · Cited by 1,261 · 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
Cognitive decline in Parkinson disease
Aarsland, D., Creese, B., Politis, M., Chaudhuri, K. R., ffytche, D. H., Weintraub, D., & Ballard, C. (2017) · Nature Reviews Neurology · doi:10.1038/nrneurol.2017.27 · Cited by 1,027 · see citing works
Gastrointestinal Dysfunction in Parkinson’s Disease
Fasano, A., Visanji, N. P., Liu, L. W. C., Lang, A. E., & Pfeiffer, R. F. (2015) · The Lancet Neurology · doi:10.1016/s1474-4422(15)00007-1 · Cited by 1,016 · 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
Direct evidence of Parkinson pathology spread from the gastrointestinal tract to the brain in rats
Holmqvist, S., Chutna, O., Bousset, L., Aldrin-Kirk, P., Li, W., Björklund, T., Wang, Z.-Y., Roybon, L., Melki, R., & Li, J.-Y. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1343-6 · Cited by 925 · see citing works
Self-citationGastrointestinal dysfunction in Parkinson's disease
Pfeiffer, R. F. (2003) · The Lancet Neurology · doi:10.1016/s1474-4422(03)00307-7 · Cited by 925 · see citing works
Physiology of the Autonomic Nervous System
McCorry, L. K. (2007) · American Journal of Pharmaceutical Education · doi:10.5688/aj710478 · Cited by 891 · 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
Frequency of Bowel Movements and the Future Risk of Parkinson’s Disease
Abbott, R. D., Petrovitch, H., White, L. R., Masaki, K. H., Tanner, C. M., Curb, J. D., Grandinetti, A., Blanchette, P. L., Popper, J. S., & Ross, G. W. (2001) · Neurology · doi:10.1212/wnl.57.3.456 · Cited by 839 · 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
Enteroendocrine Cells: Chemosensors in the Intestinal Epithelium
Gribble, F. M., & Reimann, F. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105439 · Cited by 683 · see citing works
Fecal microbiota transplantation and emerging applications
Borody, T. J., & Khoruts, A. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2011.244 · Cited by 677 · see citing works
Exercise Modifies the Gut Microbiota with Positive Health Effects
Monda, V., Villano, I., Messina, A., Valenzano, A., Esposito, T., Moscatelli, F., Viggiano, A., Cibelli, G., Chieffi, S., Monda, M., et al. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/3831972 · Cited by 654 · see citing works
Liang, S., Wang, T., Hu, X., Luo, J., Li, W., Wu, X., Duan, Y., & Jin, F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.033 · Cited by 651 · see citing works
Self-citationColonic inflammation in Parkinson's disease
Devos, D., Lebouvier, T., Lardeux, B., Biraud, M., Rouaud, T., Pouclet, H., Coron, E., Bruley des Varannes, S., Naveilhan, P., Nguyen, J.-M., et al. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.09.007 · Cited by 627 · see citing works
Should we standardize the 1,700-year-old fecal microbiota transplantation?
Zhang, F., Luo, W., Shi, Y., Fan, Z., & Ji, G. (2012) · American Journal of Gastroenterology · doi:10.1038/ajg.2012.251 · Cited by 619 · see citing works
Epithelial Barriers in Homeostasis and Disease
Marchiando, A. M., Graham, W. V., & Turner, J. R. (2010) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev.pathol.4.110807.092135 · Cited by 612 · see citing works
A timeline for Parkinson's disease
Hawkes, C. H., Del Tredici, K., & Braak, H. (2010) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2009.08.007 · Cited by 594 · see citing works
The gut-brain axis: is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis?
Houser, M. C., & Tansey, M. G. (2017) · npj Parkinson's Disease · doi:10.1038/s41531-016-0002-0 · Cited by 588 · see citing works
Microbiota restoration: natural and supplemented recovery of human microbial communities
Reid, G., Younes, J. A., van der Mei, H. C., Gloor, G. B., Knight, R. D., & Busscher, H. J. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2473 · Cited by 585 · see citing works
Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease
Sulzer, D. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.009 · Cited by 583 · see citing works
Rao, A. V., Bested, A. C., Beaulne, T. M., Katzman, M. A., Iorio, C., Berardi, J. M., & Logan, A. C. (2009) · Gut Pathogens · doi:10.1186/1757-4749-1-6 · Cited by 577 · 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
de Rijk, M. C., Launer, L. J., Berger, K., Breteler, M. M. B., Dartigues, J. F., Baldereschi, M., Fratiglioni, L., Lobo, A., Martinez-Lage, J., Trenkwalder, C., et al. (2000) · PubMed · Cited by 528 · see citing works
Pan-Montojo, F., Anichtchik, O., Dening, Y., Knels, L., Pursche, S., Jung, R., Jackson, S., Gille, G., Spillantini, M. G., Reichmann, H., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008762 · Cited by 524 · see citing works
Intestinal dysbiosis and lowered serum lipopolysaccharide-binding protein in Parkinson's disease
Hasegawa, S., Goto, S., Tsuji, H., Okuno, T., Asahara, T., Nomoto, K., Shibata, A., Fujisawa, Y., Minato, T., Okamoto, A., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0142164 · Cited by 523 · see citing works
Identifying personal microbiomes using metagenomic codes
Franzosa, E. A., Huang, K. H., Meadow, J. F., Gevers, D., Lemon, K. P., Bohannan, B. J. M., & Huttenhower, C. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423854112 · Cited by 504 · see citing works
Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells
Bohórquez, D. V., Shahid, R. A., Erdmann, A., Kreger, A. M., Wang, Y., Calakos, N., Wang, F., & Liddle, R. A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci78361 · Cited by 484 · see citing works
Estaki, M., Pither, J., Baumeister, P., Little, J. P., Gill, S. K., Ghosh, S., Ahmadi-Vand, Z., Marsden, K. R., & Gibson, D. L. (2016) · Microbiome · doi:10.1186/s40168-016-0189-7 · Cited by 476 · see citing works
Is alpha-synuclein in the colon a biomarker for premotor Parkinson’s disease? Evidence from 3 cases
Shannon, K. M., Keshavarzian, A., Dodiya, H. B., Jakate, S., & Kordower, J. H. (2012) · Movement Disorders · doi:10.1002/mds.25020 · Cited by 464 · see citing works
Vagotomy and Parkinson disease: A Swedish register–based matched-cohort study
Liu, B., Fang, F., Pedersen, N. L., Tillander, A., Ludvigsson, J. F., Ekbom, A., Svenningsson, P., Chen, H., & Wirdefeldt, K. (2017) · Neurology · doi:10.1212/wnl.0000000000003961 · Cited by 447 · see citing works
Role of the intestinal microbiome in health and disease: from correlation to causation
de Vos, W. M., & de Vos, E. A. (2012) · Nutrition Reviews · doi:10.1111/j.1753-4887.2012.00505.x · Cited by 440 · see citing works
Fava, F., Gitau, R., Griffin, B. A., Gibson, G. R., Tuohy, K. M., & Lovegrove, J. A. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.33 · Cited by 435 · see citing works
Medical records documentation of constipation preceding Parkinson disease
Savica, R., Carlin, J. M., Grossardt, B. R., Bower, J. H., Ahlskog, J. E., Maraganore, D. M., Bharucha, A. E., & Rocca, W. A. (2009) · Neurology · doi:10.1212/wnl.0b013e3181c34af5 · Cited by 431 · see citing works
Lebouvier, T., Neunlist, M., Bruley des Varannes, S., Coron, E., Drouard, A., N'Guyen, J.-M., Chaumette, T., Tasselli, M., Paillusson, S., Flamand, M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012728 · Cited by 427 · see citing works
Stokholm, M. G., Danielsen, E. H., Hamilton‐Dutoit, S. J., & Borghammer, P. (2016) · Annals of Neurology · doi:10.1002/ana.24648 · Cited by 415 · see citing works
Substantial Production of Dopamine in the Human Gastrointestinal Tract
Eisenhofer, G., Åneman, A., Friberg, P., Hooper, D., Fåndriks, L., Lonroth, H., Hunyady, B., & Mezey, E. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.11.4339 · Cited by 394 · see citing works
Hui, K. Y., Fernandez-Hernandez, H., Hu, J., Schaffner, A., Pankratz, N., Hsu, N.-Y., Chuang, L.-S., Carmi, S., Villaverde, N., Li, X., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aai7795 · Cited by 384 · see citing works
Bacterial Neuroactive Compounds Produced by Psychobiotics
Wall, R., Cryan, J. F., Ross, R. P., Fitzgerald, G. F., Dinan, T. G., & Stanton, C. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0897-4_10 · Cited by 362 · 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
Mechanisms of Molecular Mimicry Involving the Microbiota in Neurodegeneration
Friedland, R. P. (2015) · Journal of Alzheimer's Disease · doi:10.3233/jad-142841 · Cited by 338 · see citing works
Fecal microbiota transplantation: past, present and future
Aroniadis, O. C., & Brandt, L. J. (2013) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32835a4b3e · Cited by 336 · see citing works
Voices from within: gut microbes and the CNS
Forsythe, P., & Kunze, W. A. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1028-z · Cited by 336 · see citing works
Olfactory loss may be a first sign of idiopathic Parkinson's disease
Haehner, A., Hummel, T. R., Hummel, C., Sommer, U., Junghanns, S., & Reichmann, H. (2007) · Movement Disorders · doi:10.1002/mds.21413 · Cited by 333 · see citing works
Small Intestinal Bacterial Overgrowth: Roles of Antibiotics, Prebiotics, and Probiotics
Quigley, E. M. M., & Quera, R. (2006) · Gastroenterology · doi:10.1053/j.gastro.2005.11.046 · Cited by 328 · see citing works
Kelly, L. P., Carvey, P. M., Keshavarzian, A., Shannon, K. M., Shaikh, M., Bakay, R. A. E., & Kordower, J. H. (2014) · Movement Disorders · doi:10.1002/mds.25736 · Cited by 308 · see citing works
Dodiya, H. B., Forsyth, C. B., Voigt, R. M., Engen, P. A., Patel, J., Shaikh, M., Green, S. J., Naqib, A., Roy, A., Kordower, J. H., et al. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.12.012 · Cited by 305 · see citing works
Esophageal Lewy bodies associated with ganglion cell loss in achalasia
Qualman, S. J., Haupt, H. M., Yang, P. H., & Hamilton, S. R. (1984) · Gastroenterology · doi:10.1016/0016-5085(84)90079-9 · Cited by 305 · see citing works
Parkinson's Disease: The Dual Hit Theory Revisited
Hawkes, C. H., Del Tredici, K., & Braak, H. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04365.x · Cited by 303 · see citing works
Qualman, S. J., Haupt, H. M., Yang, P. H., & Hamilton, S. R. (1984) · PubMed · Cited by 295 · see citing works
Structural alterations of the intestinal epithelial barrier in Parkinson’s disease
Clairembault, T., Leclair‐Visonneau, L., Coron, E., Bourreille, A., Dily, S. L., Vavasseur, F., Heymann, M., Neunlist, M., & Derkinderen, P. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0196-0 · Cited by 292 · see citing works
Ganapathy, V., Thangaraju, M., Prasad, P. D., Martin, P. M., & Singh, N. (2013) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2013.08.006 · Cited by 290 · 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
Ageing and gut microbes: Perspectives for health maintenance and longevity
Biagi, E., Candela, M., Turroni, S., Garagnani, P., Franceschi, C., & Brigidi, P. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2012.10.005 · Cited by 276 · 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
Progression of Parkinson's disease is associated with gut dysbiosis: Two-year follow-up study
Minato, T., Maeda, T., Fujisawa, Y., Tsuji, H., Nomoto, K., Ohno, K., & Hirayama, M. (2017) · PLOS ONE · doi:10.1371/journal.pone.0187307 · Cited by 248 · see citing works
Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia
Jessen, K., & Mirsky, R. (1983) · The Journal of Neuroscience · doi:10.1523/jneurosci.03-11-02206.1983 · Cited by 246 · see citing works
An Enteroendocrine Cell – Enteric Glia Connection Revealed by 3D Electron Microscopy
Bohórquez, D. V., Samsa, L. A., Roholt, A., Medicetty, S., Chandra, R., & Liddle, R. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089881 · Cited by 242 · see citing works
Phylogeny, culturing, and metagenomics of the human gut microbiota
Walker, A. W., Duncan, S. H., Louis, P., & Flint, H. J. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2014.03.001 · Cited by 239 · see citing works
Davey, K. J., Cotter, P. D., O'Sullivan, O., Crispie, F., Dinan, T. G., Cryan, J. F., & O'Mahony, S. M. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.83 · Cited by 236 · see citing works
α-Synuclein in gut endocrine cells and its implications for Parkinson’s disease
Chandra, R., Hiniker, A., Kuo, Y.-M., Nussbaum, R. L., & Liddle, R. A. (2017) · JCI Insight · doi:10.1172/jci.insight.92295 · Cited by 236 · see citing works
Levodopa in Parkinson’s Disease: Current Status and Future Developments
Tambasco, N., Romoli, M., & Calabresi, P. (2017) · Current Neuropharmacology · doi:10.2174/1570159x15666170510143821 · Cited by 236 · see citing works
Gut microbiota: Implications in Parkinson's disease
Parashar, A., & Malairaman, U. (2017) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2017.02.002 · Cited by 231 · see citing works
Neuropathological basis of nonmotor manifestations of Parkinson's disease
Adler, C. H., & Beach, T. G. (2016) · Movement Disorders · doi:10.1002/mds.26605 · Cited by 230 · see citing works
Gastrointestinal dysfunction in Parkinson's disease
Edwards, L., Quigley, E., & Pfeiffer, R. (1992) · Neurology · doi:10.1212/wnl.42.4.726 · Cited by 226 · see citing works
Parkinson’s disease: premotor clinico-pathological correlations
Wolters, E. C., & Braak, H. (2006) · Springer eBooks · doi:10.1007/978-3-211-45295-0_47 · Cited by 216 · see citing works
The human enteric nervous system
Schemann, M., & Neunlist, M. (2004) · Neurogastroenterology & Motility · doi:10.1111/j.1743-3150.2004.00476.x · Cited by 213 · see citing works
Meta-analyses on prevalence of selected Parkinson's nonmotor symptoms before and after diagnosis
Chen, H., Zhao, E. J., Zhang, W., Lu, Y., Liu, R., Huang, X., Ciesielski-Jones, A. J., Justice, M. A., Cousins, D. S., & Peddada, S. (2015) · Translational Neurodegeneration · doi:10.1186/2047-9158-4-1 · Cited by 212 · see citing works
Jim, K. K., Engelen-Lee, J.-Y., van der Sar, A. M., Bitter, W., Brouwer, M. C., ENDE, A. V. D., Veening, J., van de Beek, D., & Vandenbroucke‐Grauls, C. M. J. E. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0655-y · Cited by 209 · see citing works
Stool Immune Profiles Evince Gastrointestinal Inflammation in Parkinson's Disease
Houser, M. C., Chang, J., Factor, S. A., Molho, E., Zabetian, C. P., Hill‐Burns, E. M., Payami, H., Hertzberg, V., & Tansey, M. G. (2018) · Movement Disorders · doi:10.1002/mds.27326 · Cited by 200 · see citing works
Many faces of Parkinson's disease: non-motor symptoms of Parkinson's disease
Lee, H. M., & Koh, S.-B. (2015) · Journal of Movement Disorders · doi:10.14802/jmd.15003 · Cited by 191 · see citing works
Enteric <scp>GFAP</scp> expression and phosphorylation in Parkinson's disease
Clairembault, T., Kamphuis, W., Leclair‐Visonneau, L., Rolli‐Derkinderen, M., Coron, E., Neunlist, M., Hol, E. M., & Derkinderen, P. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12742 · Cited by 191 · see citing works
Phillips, R. J., Walter, G. C., Wilder, S. L., Baronowsky, E. A., & Powley, T. L. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.074 · Cited by 189 · see citing works
Biedermann, L., Brülisauer, K., Zeitz, J., Frei, P., Scharl, M., Vavricka, S. R., Fried, M., Loessner, M. J., Rogler, G., & Schuppler, M. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000129 · Cited by 178 · see citing works
Microbial amyloids – functions and interactions within the host
Schwartz, K., & Boles, B. R. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2012.12.001 · Cited by 177 · see citing works
Does Parkinson’s disease start in the gut?
Lionnet, A., Leclair‐Visonneau, L., Neunlist, M., Murayama, S., Takao, M., Adler, C. H., Derkinderen, P., & Beach, T. G. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1777-8 · Cited by 177 · see citing works
Mills, C. E., Tzounis, X., Oruña-Concha, M. J., Mottram, D. S., Gibson, G. R., & Spencer, J. P. E. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114514003948 · Cited by 173 · see citing works
The nonmotor symptoms of Parkinson's disease—An overview
Lim, S., & Lang, A. E. (2010) · Movement Disorders · doi:10.1002/mds.22786 · Cited by 171 · see citing works
REM S leep B ehavior D isorder in P arkinson's D isease and O ther S ynucleinopathies
Louis, E. K. S., Boeve, A. R., & Boeve, B. F. (2017) · Movement Disorders · doi:10.1002/mds.27018 · Cited by 168 · see citing works
Varankovich, N. V., Nickerson, M. T., & Korber, D. R. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00685 · Cited by 164 · see citing works
Starke Belege: Parkinson könnte im Verdauungstrakt beginnen
(2017) · Fortschritte der Neurologie · Psychiatrie · doi:10.1055/s-0043-113319 · Cited by 162 · see citing works
Perl, D. P., Warren, C. O., & Calne, D. B. (1998) · Annals of Neurology · doi:10.1002/ana.410440705 · Cited by 159 · see citing works
Gut dysfunction in Parkinson's disease
Mukherjee, A., Biswas, A., & Das, S. K. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i25.5742 · Cited by 156 · see citing works
Colonic mucosal α-synuclein lacks specificity as a biomarker for Parkinson disease
Visanji, N. P., Marras, C., Kern, D. S., AlDakheel, A., Gao, A. F., Liu, L. W. C., Lang, A. E., & Hazrati, L. (2015) · Neurology · doi:10.1212/wnl.0000000000001240 · Cited by 142 · see citing works
Mechanistic links between gut microbial community dynamics, microbial functions and metabolic health
Ha, C. W. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i44.16498 · Cited by 137 · see citing works
How does parkinson's disease begin? Perspectives on neuroanatomical pathways, prions, and histology
Borghammer, P. (2017) · Movement Disorders · doi:10.1002/mds.27138 · Cited by 136 · see citing works
Bested, A. C., Logan, A. C., & Selhub, E. M. (2013) · Gut Pathogens · doi:10.1186/1757-4749-5-5 · Cited by 135 · see citing works
Hyposmia and executive dysfunction as predictors of future Parkinson's disease: a prospective study
Ponsen, M. M., Stoffers, D., Twisk, J. W. R., Wolters, E. C., & Berendse, H. W. (2009) · Movement Disorders · doi:10.1002/mds.22534 · Cited by 127 · see citing works
Gut feelings about smoking and coffee in Parkinson's disease
Derkinderen, P., Shannon, K. M., & Brundin, P. (2014) · Movement Disorders · doi:10.1002/mds.25882 · Cited by 115 · see citing works
Association between Parkinson's Disease and Helicobacter Pylori
Çamcı, G., & Oğuz, S. (2016) · Journal of Clinical Neurology · doi:10.3988/jcn.2016.12.2.147 · Cited by 109 · see citing works
Calcium, mitochondrial dysfunction and slowing the progression of Parkinson's disease
Surmeier, D. J., Halliday, G. M., & Simuni, T. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.08.001 · Cited by 99 · see citing works
Pellegrini, C., Fornai, M., Colucci, R., Tirotta, E., Blandini, F., Levandis, G., Cerri, S., Segnani, C., Ippolito, C., Bernardini, N., et al. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0608-5 · Cited by 91 · see citing works
[Physiology of the autonomic nervous system].
de ESPANES, E. M. (1953) · PubMed · Cited by 85 · see citing works
Linking Smoking, Coffee, Urate, and Parkinson’s Disease – A Role for Gut Microbiota?
Scheperjans, F., Pekkonen, E., Kaakkola, S., & Auvinen, P. (2015) · Journal of Parkinson’s Disease · doi:10.3233/jpd-150557 · Cited by 83 · see citing works
CARD15 variants in patients with sporadic Parkinson’s disease
Bialecka, M., Kurzawski, M., Klodowska-Duda, G., Opala, G., Juzwiak, S., Kurzawski, G., Tan, E.-K., & Drozdzik, M. (2007) · Neuroscience Research · doi:10.1016/j.neures.2006.11.012 · Cited by 79 · see citing works
Perez-Pardo, P., de Jong, E. M., Broersen, L. M., van Wijk, N., Attali, A., Garssen, J., & Kraneveld, A. D. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00057 · Cited by 74 · see citing works
Lewy bodies in the lower sacral parasympathetic neurons of a patient with Parkinson's disease
Oyanagi, K., Wakabayashi, K., Ohama, E., Takeda, S., Horikawa, Y., Morita, T., & Ikuta, F. (1990) · Acta Neuropathologica · doi:10.1007/bf00294619 · Cited by 68 · see citing works
Nonmotor Symptoms in Parkinson's Disease
Stacy, M. A. (2011) · International Journal of Neuroscience · doi:10.3109/00207454.2011.620196 · Cited by 61 · see citing works
Bhattarai, Y. (2018) · Neurogastroenterology & Motility · doi:10.1111/nmo.13366 · Cited by 59 · see citing works
(2000) · Neurology · doi:10.1212/wnl.54.11.21a · Cited by 57 · see citing works
Foo, A. S. C., Soong, T. W., Yeo, T. T., & Lim, K. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00089 · Cited by 56 · see citing works
Implementation and Refinement of a Problem-based Learning Model: A Ten-Year Experience
Ross, L. A., Crabtree, B. L., Theilman, G. D., et al. (2007) · American Journal of Pharmaceutical Education · doi:10.5688/aj710117 · Cited by 54 · see citing works
Trends in inpatient antiparkinson drug use in the USA, 2001–2012
Crispo, J. A. G., Fortin, Y., Thibault, D. P., et al. (2015) · European Journal of Clinical Pharmacology · doi:10.1007/s00228-015-1881-4 · Cited by 49 · see citing works
The Hypothalamic-Pituitary-Adrenal—Immune Axis
Lilly, M. P. (1992) · Archives of Surgery · doi:10.1001/archsurg.1992.01420120097017 · Cited by 46 · see citing works
Gut microbes metabolize Parkinson's disease drug
O’Neill, C. (2019) · Science · doi:10.1126/science.aax8937 · Cited by 35 · see citing works
Unger, M. M., Möller, J. C., Mankel, K., Schmittinger, K., Eggert, K. M., Stamelou, M., Stiasny‐Kolster, K., Bohne, K., Bodden, M., Mayer, G., et al. (2011) · Movement Disorders · doi:10.1002/mds.23933 · Cited by 26 · see citing works
Does Parkinson's disease start in the gut?
Gershanik, O. S. (2018) · Arquivos de Neuro-Psiquiatria · doi:10.1590/0004-282x20170188 · Cited by 19 · see citing works
Colonic mucosal α-synuclein lacks specificity as a biomarker for Parkinson disease
Ruffmann, C., & Parkkinen, L. (2015) · Neurology · doi:10.1212/wnl.0000000000001904 · Cited by 12 · see citing works
Fecal Microbiota Transplantation: Expanding Horizons for Clostridium difficile Infections and Beyond
Borody, T. J., Peattie, D. A., & Mitchell, S. (2015) · Antibiotics · doi:10.3390/antibiotics4030254 · Cited by 7 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [73]Houser MC Chang J Factor SA Molho ES Zabetian CP Hillburns EM Stool immune profiles evince gastrointestinal inflammation in Parkinson's disease. Neurobiol Dis. (1997) 30: 125– 43. PMC5992021 29572994
Cited by
Sorted by citations
Function and therapeutic value of astrocytes in neurological diseases
Lee, H.-G., Wheeler, M. A., & Quintana, F. J. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00390-x · Cited by 662 · 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
The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options
Wang, Q., Luo, Y., Ray Chaudhuri, K., Reynolds, R., Tan, E.-K., & Pettersson, S. (2021) · Brain · doi:10.1093/brain/awab156 · Cited by 281 · 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
Metta, V., Leta, V., Mrudula, K. R., Prashanth, L. K., Goyal, V., Borgohain, R., Chung-Faye, G., & Chaudhuri, K. R. (2022) · Journal of Neurology · doi:10.1007/s00415-021-10567-w · Cited by 130 · see citing works
Zhou, X., Lu, J., Wei, K., Wei, J., Tian, P., Yue, M., Wang, Y., Hong, D., Li, F., Wang, B., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/9424582 · Cited by 85 · see citing works
Self-citationA prebiotic diet modulates microglial states and motor deficits in α-synuclein overexpressing mice
Abdel-Haq, R., Schlachetzki, J. C., Boktor, J. C., Cantu-Jungles, T. M., Thron, T., Zhang, M., Bostick, J. W., Khazaei, T., Chilakala, S., Morais, L. H., et al. (2022) · eLife · doi:10.7554/elife.81453 · Cited by 82 · see citing works
Liu, X., Du, Z. R., Wang, X., Sun, X. R., Zhao, Q., Zhao, F., Wong, W. T., Wong, K. H., & Dong, X.-L. (2022) · Food Research International · doi:10.1016/j.foodres.2022.111067 · Cited by 77 · see citing works
Wu, G., Jiang, Z., Pu, Y., Chen, S., Wang, T., Wang, Y., Xu, X., Wang, S., Jin, M., Yao, Y., et al. (2022) · BMC Neurology · doi:10.1186/s12883-021-02544-7 · Cited by 67 · see citing works
Association of Parkinson’s Disease With Microbes and Microbiological Therapy
Chen, Z.-J., Liang, C.-Y., Yang, L.-Q., Ren, S.-M., Xia, Y.-M., Cui, L., Li, X.-F., & Gao, B.-L. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.619354 · Cited by 45 · see citing works
Self-citation
- Authors
- Yang, D., Zhao, D., Ali Shah, S. Z., Wu, W., Lai, M., Zhang, X., Li, J., Guan, Z., Zhao, H., Li, W., Gao, H., Zhou, X., & Yang, L.
- Affiliations
- China Agricultural University (CN)
- Corresponding author
- Yang, Lifeng
- ORCID
- Venue
- Frontiers in Neurology
- Publisher
- Frontiers Media SA
- Published
- 2019-11-06
- Volume
- 10
- Pages
- 1155-1155
- ISSN
- 1664-2295 (ISSN-L)
- PMC
- PMC6851172
- OpenAlex
- W2985623760
- Cited by
- 162
- References
- 137
- Citations by year
- 2026: 15 · 2025: 19 · 2024: 37 · 2023: 16 · 2022: 27 · 2021: 34 · 2020: 14
- FWCI
- 2.51
- Type
- journal article
- Language
- en
- Update notices
- corrigendum (2020-02-06)
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Neurology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Basic Research Program of China
- 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
- gut microbiota, Parkinson's disease, gut dysbiosis, gut-brain axis, neurodegeneration, gastrointestinal diseases, microbiome metabolites, pathogenesis
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