Parkinson’s Disease and the Gastrointestinal Microbiome

Lubomski, Michal; Tan, Ai Huey; Lim, Shen-Yang; Holmes, Andrew J.; Davis, Ryan L.; Sue, Carolyn M.

doi:10.1007/s00415-019-09320-1

Cited by 172Parkinson's Disease Mechanisms and TreatmentsGut microbiota and healthGastrointestinal motility and disorders

Parkinson’s Disease and the Gastrointestinal Microbiome

Lubomski, Michal, Tan, Ai Huey, Lim, Shen-Yang, Holmes, Andrew J., Davis, Ryan L., Sue, Carolyn M.·2020·Journal of Neurology

DOI 10.1007/s00415-019-09320-1

Open this paper in CoChat — free account

Abstract

Recently, there has been a surge in awareness of the gastrointestinal microbiome (GM) and its role in health and disease. Of particular note is an association between the GM and Parkinson's disease (PD) and the realisation that the GM can act via a complex bidirectional communication between the gut and the brain. Compelling evidence suggests that a shift in GM composition may play an important role in the pathogenesis of PD by facilitating the characteristic ascending neurodegenerative spread of α-synuclein aggregates from the enteric nervous system to the brain. Here, we review evidence linking GM changes with PD, highlighting mechanisms supportive of pathological α-synuclein spread and intestinal inflammation in PD. We summarise existing patterns and correlations seen in clinical studies of the GM in PD, together with the impacts of non-motor symptoms, medications, lifestyle, diet and ageing on the GM. Roles of GM modulating therapies including probiotics and faecal microbiota transplantation are discussed. Encouragingly, alterations in the GM have repeatedly been observed in PD, supporting a biological link and highlighting it as a potential therapeutic target.

Integrity signals

Registry

Crossref · 10.1007/s00415-019-09320-1

Cites

165 of 165 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Intestinal inflammation is a crucial contributor to PD development.
“Intestinal inflammation is a crucial contributor to PD development [53,54,55,56].”
From Neuroprotective Effects of Bifidobacterium breve CCFM1067 in MPTP-Induced Mouse Models of Parkinson’s Disease (2022) · cites this paper as [56]

Diet rapidly and reproducibly alters the human gut microbiome
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., et al. (2014) · Nature · doi:10.1038/nature12820 · Cited by 10,100 · 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
Linking long-term dietary patterns with gut microbial enterotypes
Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.-Y., Keilbaugh, S. A., Bewtra, M., Knights, D., Walters, W. A., Knight, R., et al. (2011) · Science · doi:10.1126/science.1208344 · Cited by 6,513 · see citing works
Diversity, stability and resilience of the human gut microbiota
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012) · Nature · doi:10.1038/nature11550 · Cited by 5,533 · 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
Proteobacteria: Microbial signature of dysbiosis in gut microbiota
Shin, N.-R., Whon, T. W., & Bae, J.-W. (2015) · Trends in Biotechnology · doi:10.1016/j.tibtech.2015.06.011 · Cited by 3,954 · see citing works
The gut microbiota--masters of host development and physiology
Sommer, F., & Bäckhed, F. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2974 · Cited by 3,681 · 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
Microbiota Modulate Behavioral and Physiological Abnormalities Associated with Neurodevelopmental Disorders
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283 · 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
Altered fecal microbiota composition in patients with major depressive disorder
Jiang, H., Ling, Z., Zhang, Y., Mao, H., Ma, Z., Yin, Y., Wang, W., Tang, W., Tan, Z., Shi, J., et al. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.03.016 · Cited by 2,275 · see citing works
The prevalence of Parkinson's disease: a systematic review and meta-analysis
Pringsheim, T., Jette, N., Frolkis, A., & Steeves, T. D. L. (2014) · Movement Disorders · doi:10.1002/mds.25945 · Cited by 2,188 · see citing works
Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers
Peng, L., Li, Z.-R., Green, R. S., Holzmanr, I. R., & Lin, J. (2009) · The Journal of Nutrition · doi:10.3945/jn.109.104638 · Cited by 2,130 · 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 neuroactive potential of the human gut microbiota in quality of life and depression
Valles-Colomer, M., Falony, G., Darzi, Y., Tigchelaar, E. F., Wang, J., Tito, R. Y., Schiweck, C., Kurilshikov, A., Joossens, M., Wijmenga, C., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-018-0337-x · Cited by 1,963 · see citing works
Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity
Zhernakova, A., Kurilshikov, A., Bonder, M. J., Tigchelaar, E. F., Schirmer, M., Vatanen, T., Mujagic, Z., Vila, A. V., Falony, G., Vieira-Silva, S., et al. (2016) · Science · doi:10.1126/science.aad3369 · Cited by 1,914 · see citing works
Extensive impact of non-antibiotic drugs on human gut bacteria
Maier, L., Pruteanu, M., Kuhn, M., Zeller, G., Telzerow, A., Anderson, E. E., Brochado, A. R., Fernandez, K. C., Dose, H., Mori, H., et al. (2018) · Nature · doi:10.1038/nature25979 · Cited by 1,905 · 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 1,837 · 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
Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen
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 impact of diet and lifestyle on gut microbiota and human health
Conlon, M., & Bird, A. (2014) · Nutrients · doi:10.3390/nu7010017 · Cited by 1,567 · see citing works
Gut Dysbiosis Is Linked to Hypertension
Yang, T., Santisteban, M. M., Rodriguez, V., Li, E., Ahmari, N., Carvajal, J. M., Zadeh, M., Gong, M., Qi, Y., Zubcevic, J., et al. (2015) · Hypertension · doi:10.1161/hypertensionaha.115.05315 · Cited by 1,478 · see citing works
Clostridium difficile Infection
Leffler, D. A., & LaMont, J. T. (2015) · New England Journal of Medicine · doi:10.1056/nejmra1403772 · Cited by 1,461 · see citing works
The Application of Ecological Theory Toward an Understanding of the Human Microbiome
Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. M., & Relman, D. A. (2012) · Science · doi:10.1126/science.1224203 · Cited by 1,437 · see citing works
Gastric α-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology
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
Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342 · cited 1× · see citing works
“Accordingly, this intricate network shares a crucial role in maintaining the vital physiological interplay between the gastrointestinal tract and the brain [37].”
Background
Parkinson's disease
Samii, A., Nutt, J. G., & Ransom, B. R. (2004) · The Lancet · doi:10.1016/s0140-6736(04)16305-8 · Cited by 1,305 · 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
The maternal microbiota drives early postnatal innate immune development
Gomez de Agüero, M., Ganal-Vonarburg, S. C., Fuhrer, T., Rupp, S., Uchimura, Y., Li, H., Steinert, A., Heikenwalder, M., Hapfelmeier, S., Sauer, U., et al. (2016) · Science · doi:10.1126/science.aad2571 · Cited by 1,231 · see citing works
High Fat Diet-Induced Gut Microbiota Exacerbates Inflammation and Obesity in Mice via the TLR4 Signaling Pathway
Kim, K., Gu, W., Lee, I., Joh, E., & Kim, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047713 · Cited by 1,184 · see citing works
Short chain fatty acids and gut microbiota differ between patients with Parkinson's disease and age-matched controls
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
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
The microbiome-gut-brain axis in health and disease
Dinan, T. G., & Cryan, J. F. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2016.09.007 · Cited by 1,111 · see citing works
Gut Microbiota and Extreme Longevity
Biagi, E., Franceschi, C., Rampelli, S., Severgnini, M., Ostan, R., Turroni, S., Consolandi, C., Quercia, S., Scurti, M., Monti, D., et al. (2016) · Current Biology · doi:10.1016/j.cub.2016.04.016 · Cited by 1,025 · see citing works
Treating Clostridium difficile infection with fecal microbiota transplantation
Bakken, J. S., Borody, T., Brandt, L. J., Brill, J. V., Demarco, D. C., Franzos, M. A., Kelly, C., Khoruts, A., Louie, T., Martinelli, L. P., et al. (2011) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2011.08.014 · Cited by 1,003 · see citing works
The microbiome-gut-brain axis: from bowel to behavior
Cryan, J. F., & O’Mahony, S. M. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01664.x · Cited by 990 · see citing works
Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children
Kang, D.-W., Park, J. G., Ilhan, Z. E., Wallstrom, G., LaBaer, J., Adams, J. B., & Krajmalnik-Brown, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068322 · Cited by 976 · see citing works
Increased Intestinal Permeability Correlates with Sigmoid Mucosa alpha-Synuclein Staining and Endotoxin Exposure Markers in Early Parkinson's Disease
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
Brain-gut-microbe communication in health and disease
Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00094 · Cited by 952 · see citing works
Parkinson's disease and Parkinson's disease medications have distinct signatures of the gut microbiome
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
A meta‐analysis of coffee drinking, cigarette smoking, and the risk of Parkinson's disease
Hernán, M. A., Takkouche, B., Caamaño‐Isorna, F., & Gestal‐Otero, J. J. (2002) · Annals of Neurology · doi:10.1002/ana.10277 · Cited by 818 · cited 1× · see citing works
“Furthermore, although debated, epidemiological studies suggest a smoking history may confer approximately 60% reduced risk of developing PD, whilst coffee consumption was found to reduce the risk by 30% [108, 109].”
Background
Vagotomy and subsequent risk of <scp>P</scp> arkinson's disease
Svensson, E., Horváth‐Puhó, E., Thomsen, R. W., Djurhuus, J. C., Pedersen, L., Borghammer, P., & Sørensen, H. T. (2015) · Annals of Neurology · doi:10.1002/ana.24448 · Cited by 806 · see citing works
Minocycline Prevents Nigrostriatal Dopaminergic Neurodegeneration in the MPTP Model of Parkinson’s Disease
Du, Y., Ma, Z., Lin, S., Dodel, R. C., Gao, F., Bales, K. R., Triarhou, L. C., Chernet, E., Perry, K. W., Nelson, D. L. G., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.251341998 · Cited by 789 · see citing works
Gut Microbiome Metagenomics Analysis Suggests a Functional Model for the Development of Autoimmunity for Type 1 Diabetes
Brown, C. T., Davis-Richardson, A. G., Giongo, A., Gano, K. A., Crabb, D. B., Mukherjee, N., Casella, G., Drew, J. C., Ilonen, J., Knip, M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025792 · Cited by 778 · see citing works
Characterization of Bacterial Communities in Feces from Healthy Elderly Volunteers and Hospitalized Elderly Patients by Using Real-Time PCR and Effects of Antibiotic Treatment on the Fecal Microbiota
Bartosch, S., Fite, A., Macfarlane, G. T., & McMurdo, M. E. T. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.6.3575-3581.2004 · Cited by 762 · cited 2× · see citing works
“Antibiotic therapy affects the diversity of the GM and is associated with reduced abundance of Bifidobacteria, as well as Bacteroides and Prevotella groups [130].”
Background
Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice
Asano, Y., Hiramoto, T., Nishino, R., Aiba, Y., Kimura, T., Yoshihara, K., Koga, Y., & Sudo, N. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00341.2012 · Cited by 659 · 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
Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress
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
The Gut Microbiome and the Brain
Galland, L. (2014) · Journal of Medicinal Food · doi:10.1089/jmf.2014.7000 · Cited by 648 · see citing works
Neurotransmitters: The Critical Modulators Regulating Gut–Brain Axis
Mittal, R., Debs, L. H., Patel, A. P., Nguyen, D., Patel, K. V., O’Connor, G., Grati, M., Mittal, J., Yan, D. L. S., Eshraghi, A. A., et al. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25518 · Cited by 644 · see citing works
Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults
Weir, T. L., Manter, D. K., Sheflin, A. M., Barnett, B. A., Heuberger, A. L., & Ryan, E. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070803 · Cited by 642 · see citing works
Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naive Parkinson's disease patients
Bedarf, J. R., Hildebrand, F., Coelho, L. P., Sunagawa, S., Bahram, M., Goeser, F., Bork, P., & Wüllner, U. (2017) · Genome Medicine · doi:10.1186/s13073-017-0428-y · Cited by 642 · see citing works
Colonic 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
Identifying prodromal Parkinson's disease: Pre‐Motor disorders in Parkinson's disease
Postuma, R. B., Aarsland, D., Barone, P., Burn, D. J., Hawkes, C. H., Oertel, W. H., & Ziemssen, T. (2012) · Movement Disorders · doi:10.1002/mds.24996 · Cited by 615 · 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
Brain-Gut-Microbiota Axis in Parkinson’s Disease
Mulak, A. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i37.10609 · Cited by 583 · see citing works
The nasal and gut microbiome in Parkinson's disease and idiopathic rapid eye movement sleep behavior disorder
Heintz‐Buschart, A., Pandey, U., Wicke, T., Sixel‐Döring, F., Janzen, A., Sittig‐Wiegand, E., Trenkwalder, C., Oertel, W. H., Mollenhauer, B., & Wilmes, P. (2018) · Movement Disorders · doi:10.1002/mds.27105 · Cited by 554 · see citing works
Human gut microbiome: the second genome of human body
Zhu, B., Wang, X., & Li, L. (2010) · Protein & Cell · doi:10.1007/s13238-010-0093-z · Cited by 535 · see citing works
The gut microbiome in human neurological disease: A review
Tremlett, H., Bauer, K. C., Appel‐Cresswell, S., Finlay, B. B., & Waubant, E. (2017) · Annals of Neurology · doi:10.1002/ana.24901 · Cited by 535 · see citing works
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
Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers
Schmidt, K., Cowen, P. J., Harmer, C. J., Tzortzis, G., Errington, S., & Burnet, P. W. J. (2015) · Psychopharmacology · doi:10.1007/s00213-014-3810-0 · Cited by 522 · see citing works
Diet and the development of the human intestinal microbiome
Voreades, N., Kozil, A., & Weir, T. L. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00494 · Cited by 495 · 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
Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions
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
Role of TLR4 in the gut-brain axis in Parkinson's disease: A translational study from men to mice
Perez-Pardo, P., Dodiya, H. B., Engen, P. A., Forsyth, C. B., Huschens, A. M., Shaikh, M., Voigt, R. M., Naqib, A., Green, S. J., Kordower, J. H., et al. (2019) · Gut · doi:10.1136/gutjnl-2018-316844 · Cited by 467 · see citing works
Prevalence of anxiety in Parkinson's disease: A systematic review and meta‐analysis
Broen, M. P. G., Narayen, N. E., Kuijf, M. L., Dissanayaka, N. N. W., & Leentjens, A. F. G. (2016) · Movement Disorders · doi:10.1002/mds.26643 · Cited by 457 · 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
The type and quantity of dietary fat and carbohydrate alter faecal microbiome and short-chain fatty acid excretion in a metabolic syndrome ‘at-risk’ population
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
Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms
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
Alteration of the fecal microbiota in Chinese patients with Parkinson’s disease
Qian, Y., Yang, X., Xu, S., Wu, C., Song, Y., Qin, N., Chen, S.-D., & Xiao, Q. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.02.016 · Cited by 409 · see citing works
Structural changes of gut microbiota in Parkinson's disease and its correlation with clinical features
Li, W., Wu, X., Hu, X., Wang, T., Liang, S., Duan, Y., Jin, F., & Qin, B. (2017) · Science China Life Sciences · doi:10.1007/s11427-016-9001-4 · Cited by 406 · see citing works
Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice
Pan-Montojo, F., Schwarz, M., Winkler, C., Arnhold, M., O'Sullivan, G. A., Pal, A., Said, J., Marsico, G., Verbavatz, J.-M., Rodrigo-Angulo, M., et al. (2012) · Scientific Reports · doi:10.1038/srep00898 · Cited by 405 · see citing works
Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
Galley, J. D., Nelson, M. C., Yu, Z., Dowd, S. E., Walter, J., Kumar, P., Lyte, M., & Bailey, M. T. (2014) · BMC Microbiology · doi:10.1186/1471-2180-14-189 · Cited by 398 · see citing works
Exploring Braak’s hypothesis of Parkinson’s disease
Rietdijk, C. D., Perez-Pardo, P., Garssen, J., van Wezel, R. J. A., & Kraneveld, A. D. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00037 · Cited by 395 · 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
Unraveling gut microbiota in Parkinson's disease and atypical parkinsonism
Barichella, M., Severgnini, M., Cilia, R., Cassani, E., Bolliri, C., Caronni, S., Ferri, V., Cancello, R., Ceccarani, C., Faierman, S., et al. (2019) · Movement Disorders · doi:10.1002/mds.27581 · Cited by 393 · see citing works
Probiotics and prebiotic fiber for constipation associated with Parkinson disease: An RCT
Barichella, M., Pacchetti, C., Bolliri, C., Cassani, E., Iorio, L., Pusani, C., Pinelli, G., Privitera, G., Cesari, I., Faierman, S. A., et al. (2016) · Neurology · doi:10.1212/wnl.0000000000003127 · Cited by 390 · see citing works
Alterations in the colonic flora and intestinal permeability and evidence of immune activation in chronic constipation
KHALIF, I., QUIGLEY, E., KONOVITCH, E., & MAXIMOVA, I. (2005) · Digestive and Liver Disease · doi:10.1016/j.dld.2005.06.008 · Cited by 382 · 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
Premotor and nonmotor features of Parkinson's disease
Goldman, J. G., & Postuma, R. (2014) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000112 · Cited by 342 · 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 Composition and Frailty
van Tongeren, S. P., Slaets, J. P. J., Harmsen, H. J. M., & Welling, G. W. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.10.6438-6442.2005 · Cited by 333 · see citing works
Like prions: the propagation of aggregated tau and α-synuclein in neurodegeneration
Goedert, M., Masuda-Suzukake, M., & Falcon, B. (2017) · Brain · doi:10.1093/brain/aww230 · Cited by 323 · see citing works
Gut microbiota in Parkinson disease in a northern German cohort
Hopfner, F., Künstner, A., Müller, S. H., Künzel, S., Zeuner, K. E., Margraf, N. G., Deuschl, G., Baines, J. F., & Kuhlenbäumer, G. (2017) · Brain Research · doi:10.1016/j.brainres.2017.04.019 · Cited by 318 · see citing works
Inflammatory bowel disease increases the risk of Parkinson’s disease: a Danish nationwide cohort study 1977–2014
Villumsen, M., Aznar, S., Pakkenberg, B., Jess, T., & Brudek, T. (2018) · Gut · doi:10.1136/gutjnl-2017-315666 · Cited by 315 · see citing works
Progression of intestinal permeability changes and alpha-synuclein expression in a mouse model of Parkinson's disease
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
Chronic stress-induced gut dysfunction exacerbates Parkinson's disease phenotype and pathology in a rotenone-induced mouse model of Parkinson's disease
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
Changes of colonic bacterial composition in Parkinson's disease and other neurodegenerative diseases
Gerhardt, S., & Mohajeri, M. H. (2018) · Nutrients · doi:10.3390/nu10060708 · Cited by 298 · see citing works
A natural product inhibits the initiation of α-synuclein aggregation and suppresses its toxicity
Perni, M., Galvagnion, C., Maltsev, A. S., Meisl, G., Müller, M. B. D., Challa, P. K., Kirkegaard, J. B., Flagmeier, P., Cohen, S. I. A., Cascella, R., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610586114 · Cited by 296 · 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
Fermented Milk Containing Lactobacillus casei Strain Shirota Preserves the Diversity of the Gut Microbiota and Relieves Abdominal Dysfunction in Healthy Medical Students Exposed to Academic Stress
Kato-Kataoka, A., Nishida, K., Takada, M., Kawai, M., Kikuchi-Hayakawa, H., Suda, K., Ishikawa, H., Gondo, Y., Shimizu, K., Matsuki, T., et al. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.04134-15 · Cited by 288 · see citing works
Pathological correlates of gastrointestinal dysfunction in Parkinson's disease
Cersosimo, M. G., & Benarroch, E. E. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.10.014 · Cited by 284 · 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
The vermiform appendix impacts the risk of developing Parkinson’s disease
Killinger, B. A., Madaj, Z., Sikora, J. W., Rey, N. L., Haas, A. J., Vepa, Y., Lindqvist, D., Chen, H., Thomas, P. M., Brundin, P., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aar5280 · Cited by 274 · see citing works
The impact of gut microbiota on brain and behaviour
Dinan, T. G., & Cryan, J. F. (2015) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000221 · Cited by 267 · see citing works
Alterations of the Host Microbiome Affect Behavioral Responses to Cocaine
Kiraly, D. D., Walker, D. M., Calipari, E. S., Labonté, B., Issler, O., Peña, C. J., Ribeiro, E., Russo, S. J., & Nestler, E. J. (2016) · Scientific Reports · doi:10.1038/srep35455 · Cited by 264 · 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 · cited 2× · see citing works
“(genus), Lachnospiraceae (family), Blautia, Roseburia, Dorea and Faecalibacterium (genus) in PD patients [12, 13, 69, 70, 72, 75, 76, 87-93].”
Background
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
Antipsychotics and the gut microbiome: olanzapine-induced metabolic dysfunction is attenuated by antibiotic administration in the rat
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
Impact of Coffee Consumption on the Gut Microbiota: A Human Volunteer Study
Jaquet, M., Rochat, I., Moulin, J., Cavin, C., & Bibiloni, R. (2009) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2009.01.011 · Cited by 232 · 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
Microbial endocrinology
Lyte, M. (2014) · Gut Microbes · doi:10.4161/gmic.28682 · Cited by 225 · see citing works
Mind-altering with the gut: Modulation of the gut-brain axis with probiotics
Kim, N., Yun, M., Oh, Y. J., & Choi, H.-J. (2018) · Journal of Microbiology · doi:10.1007/s12275-018-8032-4 · Cited by 210 · see citing works
Untitled work
(2011) · PubMed · Cited by 207 · see citing works
Oral and nasal microbiota in Parkinson's disease
Pereira, P. A. B., Aho, V. T. E., Paulin, L. G., Pekkonen, E., Auvinen, P., & Scheperjans, F. (2017) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2017.02.026 · Cited by 207 · see citing works
The Gut-Brain Axis in Parkinson’s Disease: Possibilities for Food-Based Therapies
Perez-Pardo, P., Kliest, T., Dodiya, H. B., Broersen, L. M., Garssen, J., Keshavarzian, A., & Kraneveld, A. D. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.05.042 · Cited by 203 · see citing works
Association Between Parkinsonʼs Disease and Inflammatory Bowel Disease
Lin, J.-C., Lin, C., Hsu, C.-W., Lin, C., & Kao, C. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000735 · Cited by 203 · 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
Deleterious Effects of Minocycline in Animal Models of Parkinson’s Disease and Huntington’s Disease
Diguet, E., Fernagut, P., Wei, X., Du, Y., Rouland, R., Gross, C., Bezard, E., & Tison, F. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03372.x · Cited by 189 · see citing works
Smoking Cessation Alters Intestinal Microbiota: Insights from Quantitative Investigations on Human Fecal Samples Using FISH
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
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
Prevalence of small intestinal bacterial overgrowth in Parkinson’s disease
Gabrielli, M., Bonazzi, P., Scarpellini, E., Bendia, E., Lauritano, E. C., Fasano, A., Ceravolo, M. G., Capecci, M., Rita Bentivoglio, A., Provinciali, L., et al. (2011) · Movement Disorders · doi:10.1002/mds.23566 · Cited by 175 · see citing works
Inflammatory Bowel Disease and Parkinson’s Disease: A Nationwide Swedish Cohort Study
Weimers, P., Halfvarson, J., Sachs, M. C., Saunders-Pullman, R. J., Ludvigsson, J. F., Peter, I., Burisch, J. M., & Olén, O. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izy190 · Cited by 175 · see citing works
In vitro colonic metabolism of coffee and chlorogenic acid results in selective changes in human faecal microbiota growth
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
Starke Belege: Parkinson könnte im Verdauungstrakt beginnen
(2017) · Fortschritte der Neurologie · Psychiatrie · doi:10.1055/s-0043-113319 · Cited by 162 · see citing works
Changing the research criteria for the diagnosis of Parkinson's disease: obstacles and opportunities
Berg, D., Lang, A. E., Postuma, R. B., Maetzler, W., Deuschl, G., Gasser, T., Siderowf, A. D., Schapira, A. H. V., Oertel, W. H., Obeso, J. A., et al. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70047-4 · Cited by 158 · 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
Gut Microbiota Dysfunction as Reliable Non-invasive Early Diagnostic Biomarkers in the Pathophysiology of Parkinson's Disease: A Critical Review
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
More than constipation - Bowel symptoms in Parkinson's disease and their connection to gut microbiota
Mertsalmi, T. H., Aho, V. T. E., Pereira, P. A. B., Paulin, L., Pekkonen, E., Auvinen, P., & Scheperjans, F. (2017) · European Journal of Neurology · doi:10.1111/ene.13398 · Cited by 153 · cited 14× · see citing works
“Patients with PD and irritable bowel syndrome (IBS)-like symptoms have been shown to feature more NMS, as well as a lower faecal abundance of Prevotella bacteria than those without IBS-like symptoms [86].”
BackgroundInfluential
Neuroprotective effects of compounds with antioxidant and anti-inflammatory properties in a Drosophila model of Parkinson's disease
Faust, K., Gehrke, S., Yang, Y., Yang, L., Beal, M. F., & Lu, B. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-109 · Cited by 151 · see citing works
Fecal Microbiota Transplantation and Its Usage in Neuropsychiatric Disorders
Evrensel, A., & Ceylan, M. E. (2016) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2016.14.3.231 · Cited by 150 · 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
Helicobacter pylori infection is associated with worse severity of Parkinson's disease
Tan, A. H., Mahadeva, S., Marras, C., Thalha, A. M., Kiew, C. K., Yeat, C. M., Ng, S. W., Ang, S. P., Chow, S. K., Loke, M. F., et al. (2014) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2014.12.009 · Cited by 132 · see citing works
Self-citation
Parkinson’s disease and bacteriophages as its overlooked contributors
Tetz, G. V., Brown, S. M., Hao, Y., & Tetz, V. (2018) · Scientific Reports · doi:10.1038/s41598-018-29173-4 · Cited by 126 · 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
Dietary Fiber from Coffee Beverage: Degradation by Human Fecal Microbiota
Gniechwitz, D., Reichardt, N., Blaut, M., et al. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf070646b · Cited by 111 · see citing works
Does vagotomy reduce the risk of Parkinson's disease?
Tysnes, O., Kenborg, L., Herlofson, K., Steding‐Jessen, M., Horn, A., Olsen, J. H., & Reichmann, H. (2015) · Annals of Neurology · doi:10.1002/ana.24531 · Cited by 102 · see citing works
Serum Urate and the Risk of Parkinson's Disease: Results From a Meta-Analysis
Shen, C., Guo, Y. C., Luo, W. F., Chen, L., & Ding, M. (2013) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100012981 · Cited by 100 · see citing works
Influence of coffee (<i>Coffea arabica</i>) and galacto-oligosaccharide consumption on intestinal microbiota and the host responses
Nakayama, T., & Oishi, K. (2013) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12142 · Cited by 97 · see citing works
Fermented foods, neuroticism, and social anxiety: An interaction model
Hilimire, M. R., DeVylder, J., & Forestell, C. A. (2015) · Psychiatry Research · doi:10.1016/j.psychres.2015.04.023 · Cited by 95 · see citing works
Hospitalisation and comorbidities in Parkinson's disease: a large Australian retrospective study
Lubomski, M., Rushworth, R. L., & Tisch, S. H. (2014) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2014-307822 · Cited by 95 · see citing works
Self-citation
Gut microbiota and central nervous system development
Principi, N., & Esposito, S. (2016) · Journal of Infection · doi:10.1016/j.jinf.2016.09.010 · Cited by 92 · see citing works
Effect of diet on the intestinal microbiota and its activity
Zoetendal, E. G., & de Vos, W. M. (2014) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000048 · Cited by 90 · see citing works
Intestinal Permeability and Orocaecal Transit Time in Elderly Patients with Parkinson’s Disease
Davies, K. N., King, D., Billington, D., & Barrett, J. A. (1996) · Postgraduate Medical Journal · doi:10.1136/pgmj.72.845.164 · Cited by 88 · see citing works
The microbiota–gut–brain axis: learning from intestinal bacteria?
Bercik, P. (2011) · Gut · doi:10.1136/gut.2010.226779 · Cited by 87 · see citing works
Reduced L -dopa absorption and increased clinical fluctuations in Helicobacter pylori -infected Parkinson's disease patients
Pierantozzi, M., Pietroiusti, A., Sancesario, G., Lunardi, G., Fedele, E., Giacomini, P., Frasca, S., Galante, A., Marciani, M. G., & Stanzione, P. (2001) · Neurological Sciences · doi:10.1007/s100720170061 · Cited by 85 · see citing works
The Potential Role of Gut-Derived Inflammation in Multiple System Atrophy
Engen, P. A., Dodiya, H. B., Naqib, A. D., Forsyth, C. B., Green, S. J., Voigt, R. M., Kordower, J. H., Mutlu, E., Shannon, K. M., & Keshavarzian, A. (2017) · Journal of Parkinson s Disease · doi:10.3233/jpd-160991 · Cited by 84 · 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
Increased Intestinal Permeability and Parkinson Disease Patients: Chicken or Egg?
Salat-Foix, D., Tran, K., Ranawaya, R., Meddings, J., & Suchowersky, O. (2012) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100013202 · Cited by 80 · see citing works
Evidence that folic acid deficiency is a major determinant of hyperhomocysteinemia in Parkinson's disease
dos Santos, E. F., Busanello, E. N. B., Miglioranza, A., Zanatta, Â., Barchak, A. G., Vargas, C. R., Saute, J., Rosa, C., Carrion, M. J., Camargo, D., et al. (2009) · Metabolic Brain Disease · doi:10.1007/s11011-009-9139-4 · Cited by 76 · see citing works
In vivo models of alpha-synuclein transmission and propagation
Recasens, A., Ulusoy, A., Kahle, P. J., Monte, D. A. D., & Dehay, B. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2730-9 · Cited by 72 · see citing works
Treatment of Slow Transit Constipation With Fecal Microbiota Transplantation: A Pilot Study
Tian, H., Ding, C., Gong, J., Ge, X., Mcfarland, L. V., Gu, L.-L., Wei, Y., Chen, Q.-Y., Zhu, W.-M., Li, J.-S., et al. (2016) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000472 · Cited by 69 · see citing works
Gut microbiota, 1013 new pieces in the Parkinson's disease puzzle
Scheperjans, F. (2016) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000389 · Cited by 63 · see citing works
G ut F eelings Ab out α‐ S ynuclein in G astrointestinal B iopsies: B iomarker in the M aking?
Ruffmann, C., & Parkkinen, L. (2016) · Movement Disorders · doi:10.1002/mds.26480 · Cited by 58 · see citing works
Abnormal Lipopolysaccharide Binding Protein as Marker of Gastrointestinal Inflammation in Parkinson Disease
Pal, G. D., Shaikh, M., Forsyth, C. B., Ouyang, B., Keshavarzian, A., & Shannon, K. M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00306 · Cited by 57 · see citing works
Helicobacter pylori eradication for Parkinson's disease
Rees, K., Stowe, R., Patel, S., Ives, N., Breen, K., Clarke, C. E., & Ben-Shlomo, Y. (2011) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd008453.pub2 · Cited by 56 · see citing works
Integrating Patient Concerns into Parkinson’s Disease Management
Lim, S., Tan, A. H., Fox, S. H., Evans, A. H., & Low, S.-C. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0717-2 · Cited by 56 · see citing works
Self-citation
Faecal transplant eases symptoms of Parkinson's disease
Ananthaswamy, A. (2011) · The New Scientist · doi:10.1016/s0262-4079(11)60124-3 · Cited by 55 · see citing works
The use of nanopore analysis for discovering drugs which bind to α-synuclein for treatment of Parkinson's disease
Tavassoly, O., Kakish, J., Nokhrin, S. M., Dmitriev, O. Y., & Lee, J. S. (2014) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2014.07.090 · Cited by 53 · see citing works
The Gut and Nonmotor Symptoms in Parkinson's Disease
Klingelhoefer, L., & Reichmann, H. (2017) · International review of neurobiology · doi:10.1016/bs.irn.2017.05.027 · Cited by 53 · see citing works
Microbes Tickling Your Tummy: the Importance of the Gut-Brain Axis in Parkinson’s Disease
Perez‐Pardo, P., Hartog, M., Garssen, J., & Kraneveld, A. D. (2017) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-017-0129-2 · Cited by 52 · see citing works
A pilot, open‐label, 8‐week study evaluating the efficacy, safety and tolerability of adjunctive minocycline for the treatment of bipolar I/II depression
Soczynska, J. K., Kennedy, S. H., Alsuwaidan, M. T., Mansur, R. B., Li, M., McAndrews, M. P., Brietzke, E. M., Woldeyohannes, H. O., Taylor, V. H., & McIntyre, R. S. (2017) · Bipolar Disorders · doi:10.1111/bdi.12496 · Cited by 49 · see citing works
A controversy on the role of short-chain fatty acids in the pathogenesis of Parkinson's disease
Mulak, A. (2018) · Movement Disorders · doi:10.1002/mds.27304 · Cited by 45 · see citing works
Nortriptyline inhibits aggregation and neurotoxicity of alpha-synuclein by enhancing reconfiguration of the monomeric form
Collier, T. J., Srivastava, K. R., Justman, C. J., Grammatopoulous, T., Hutter‐Paier, B., Prokesch, M., Havas, D., Rochet, J., Liu, F., Jock, K., et al. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2017.07.007 · Cited by 41 · see citing works
Food for the Brain
Zuker, C. S. (2015) · Cell · doi:10.1016/j.cell.2015.03.016 · Cited by 40 · see citing works
Gut Feelings on Parkinson's and Depression.
Dinan, T. G., & Cryan, J. F. (2017) · PubMed Central · Cited by 27 · see citing works
The prodromal microbiome
Scheperjans, F. (2017) · Movement Disorders · doi:10.1002/mds.27197 · Cited by 21 · see citing works
Mini-review on initiatives to interfere with the propagation and clearance of alpha-synuclein in Parkinson’s disease
Chan, D. K. Y., Xu, Y. H., Chan, L. K. M., et al. (2017) · Translational Neurodegeneration · doi:10.1186/s40035-017-0104-6 · Cited by 13 · see citing works
[Correlation Between Emotional-Affective Disorders and Gut Microbiota Composition in Patients with Parkinson’s Disease].
Alifirova, V. M., Zhukova, N., Zhukova, I. A., et al. (2017) · Annals of the Russian academy of medical sciences · doi:10.15690/vramn734 · Cited by 6 · see citing works
[Gut microbiota research: highlights and commentary].
Yang, Y. (2015) · PubMed · Cited by 3 · see citing works

Flagged first, then by citations

Sorted by citations

Tryptophan metabolism and gut-brain homeostasis
Roth, W., Zadeh, K., Vekariya, R., Ge, Y., & Mohamadzadeh, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22062973 · Cited by 519 · see citing works
The microbiome–gut–brain axis in Parkinson disease — from basic research to the clinic
Tan, A. H., Lim, S. Y., & Lang, A. E. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00681-2 · Cited by 392 · see citing works
Self-citation
Probiotics for Constipation in Parkinson Disease: A Randomized Placebo-Controlled Study
Tan, A. H., Lim, S.-Y., Chong, K. K., A Manap, M. A. A., Hor, J. W., Lim, J. L., Low, S. C., Chong, C. W., Mahadeva, S., & Lang, A. E. (2021) · Neurology · doi:10.1212/wnl.0000000000010998 · Cited by 226 · see citing works
Self-citation
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Gut Microbial Ecosystem in Parkinson Disease: New Clinicobiological Insights from Multi‐Omics
Tan, A. H., Chong, C. W., Lim, S., Yap, I. K. S., Teh, C. S. J., Loke, M. F., Song, S., Tan, J. Y., Ang, B. H., Tan, Y. Q., et al. (2021) · Annals of Neurology · doi:10.1002/ana.25982 · Cited by 196 · see citing works
Self-citation
Lactobacillus Plantarum PS128 Alleviates Neurodegenerative Progression in 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine-Induced Mouse Models of Parkinson’s Disease
Liao, J.-F., Cheng, Y.-F., You, S.-T., Kuo, W.-C., Huang, C.-W., Chiou, J.-J., Hsu, C.-C., Hsieh-Li, H.-M., Wang, S., & Tsai, Y.-C. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.07.036 · Cited by 159 · see citing works
Diet in Parkinson’s Disease: Critical Role for the Microbiome
Jackson, A., Forsyth, C. B., Shaikh, M., Voigt, R. M., Engen, P. A., Ramirez, V., & Keshavarzian, A. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.01245 · Cited by 145 · see citing works
The Gut-Brain Axis in Inflammatory Bowel Disease—Current and Future Perspectives
Günther, C., Rothhammer, V., Karow, M., Neurath, M., & Winner, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168870 · Cited by 123 · see citing works
An open label, non-randomized study assessing a prebiotic fiber intervention in a small cohort of Parkinson’s disease participants
Hall, 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
Neuroprotective Effects of Bifidobacterium breve CCFM1067 in MPTP-Induced Mouse Models of Parkinson’s Disease
Li, T., Chu, C., Yu, L., Zhai, Q., Wang, S., Zhao, J., Zhang, H., Chen, W., & Tian, F. (2022) · Nutrients · doi:10.3390/nu14214678 · Cited by 76 · see citing works
Interplay of good bacteria and central nervous system: cognitive aspects and mechanistic considerations
Salami, M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.613120 · Cited by 67 · see citing works
The Gut Microbiome in Parkinson’s Disease: A Longitudinal Study of the Impacts on Disease Progression and the Use of Device-Assisted Therapies
Lubomski, M., Xu, X., Holmes, A. J., Muller, S., Yang, J. Y. H., Davis, R. L., & Sue, C. M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.875261 · Cited by 59 · see citing works
Self-citation
Twice Subacute MPTP Administrations Induced Time-Dependent Dopaminergic Neurodegeneration and Inflammation in Midbrain and Ileum, as Well as Gut Microbiota Disorders in PD Mice
Xie, W., Gao, J., Jiang, R., Liu, X., Lai, F., Tang, Y., Xiao, H., Jia, Y., & Bai, Q. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2019.11.009 · Cited by 40 · see citing works
Changes in Gastrointestinal Microbiome Composition in PD: A Pivotal Role of Covariates
Cosma-Grigorov, A., Meixner, H., Mrochen, A., Wirtz, S., Winkler, J., & Marxreiter, F. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.01041 · Cited by 38 · see citing works
Heart Matters: Cardiac Dysfunction and Other Autonomic Changes in Parkinson’s Disease
Gonçalves, V. C., Cuenca-Bermejo, L., Fernandez-Villalba, E., Martin-Balbuena, S., da Silva Fernandes, M. J., Scorza, C. A., & Herrero, M.-T. (2022) · The Neuroscientist · doi:10.1177/1073858421990000 · Cited by 37 · see citing works
Gut Microbiota Relieves Inflammation in the Substantia Nigra of Chronic Parkinson’s Disease by Protecting the Function of Dopamine Neurons
Zhang, T., Wang, T., Chen, X., Zhao, Z., & Chen, Z. (2021) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2021.10974 · Cited by 34 · see citing works
Evidence for immune system alterations in peripheral biological fluids in Parkinson’s disease
Bartl, M., Xylaki, M., Bähr, M., Weber, S., Trenkwalder, C., & Mollenhauer, B. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105744 · Cited by 33 · see citing works
Deep Nasal Sinus Cavity Microbiota Dysbiosis in Parkinson’s Disease
Pal, G., Ramirez, V., Engen, P. A., Naqib, A., Forsyth, C. B., Green, S. J., Mahdavinia, M., Batra, P. S., Tajudeen, B. A., & Keshavarzian, A. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00254-y · Cited by 28 · see citing works
Exploring the connection between the gut microbiome and parkinson's disease symptom progression and pathology: implications for supplementary treatment options
Chan, D. G., Ventura, K., Villeneuve, A., Du Bois, P., & Holahan, M. R. (2022) · Journal of Parkinson's Disease · doi:10.3233/jpd-223461 · Cited by 24 · see citing works

BMC322- A RATIONALLY-DESIGNED LIVE BACTERIAL CONSORTIUM BASED ON MICROBIOME FUNCTIONAL GENOMIC ANALYSIS FOR TREATMENT OF IBD
Polonsky, O., Meshner, S., Eshar, S., et al. (2021) · Gastroenterology · doi:10.1053/j.gastro.2021.01.140 · Cited by 1 · see citing works
The Microbiome in HIV-Infected Children
Green, R. J. (2020) · Springer eBooks · doi:10.1007/978-3-030-35433-6_21 · Cited by 1 · see citing works
Sa1911 – Analysis of the Small Intestinal Microbiome Reveals Marked Differences from Stool Microbiome in a Large Scale Human Cohort: Redefining the “Gut Microbiome”
Leite, G., Weitsman, S. R., Celly, S., et al. (2019) · Gastroenterology · doi:10.1016/s0016-5085(19)37977-6 · Cited by 5 · see citing works
[Vaginal microbiome: community characteristics and disease intervention].
Liu, H., Xu, X., Ling, K., et al. (2021) · PubMed · doi:10.13345/j.cjb.210204 · Cited by 1 · see citing works
The Gut Microbiome of Children during the COVID-19 Pandemic
Bacorn, M., Romero-Soto, H. N., Levy, S., Chen, Q., & Hourigan, S. K. (2022) · Microorganisms · doi:10.3390/microorganisms10122460 · Cited by 12 · see citing works

Authors: Lubomski, M., Tan, A. H., Lim, S.-Y., Holmes, A. J., Davis, R. L., & Sue, C. M.
Affiliations: The University of Sydney (AU)
University of Malaya (MY)
Corresponding author: Lubomski, Michal
ORCID: Lubomski, Michal
Tan, Ai Huey
Lim, Shen-Yang
Holmes, Andrew J.
Davis, Ryan L.
Sue, Carolyn M.
Venue: Journal of Neurology
Publisher: Springer Science and Business Media LLC
Published: 2019-04-30
Volume: 267
Issue: 9
Pages: 2507-2523
ISSN: 0012-1037 (ISSN-L)
0340-5354
1432-1459
DOI: 10.1007/s00415-019-09320-1
OpenAlex: W2942596495
Cited by: 172
References: 165
Citations by year: 2026: 13 · 2025: 13 · 2024: 25 · 2023: 30 · 2022: 32 · 2021: 29 · 2020: 19 · 2019: 11
FWCI: 3.05
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Journal of Neurology (publishedVersion)
PubMed (publishedVersion)
ResearchOnline@ND (The University of Notre Dame) (submittedVersion)
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, gastrointestinal microbiome, gut-brain axis, alpha-synuclein aggregation, neurodegeneration, intestinal inflammation, enteric nervous system, non-motor symptoms, probiotics, fecal microbiota transplantation, diet, aging, gut dysbiosis
MeSH terms: Gastrointestinal Microbiome, Humans, Inflammation, Parkinson Disease, Enteric Nervous System, alpha-Synuclein

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Parkinson’s Disease and the Gastrointestinal Microbiome

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks