Diet in Parkinson’s Disease: Critical Role for the Microbiome

Jackson, Aeja; Forsyth, Christopher B.; Shaikh, Maliha; Voigt, Robin M.; Engen, Phillip A.; Ramirez, Vivian; Keshavarzian, Ali

doi:10.3389/fneur.2019.01245

Cited by 145Gut microbiota and healthParkinson's Disease Mechanisms and TreatmentsNutritional Studies and Diet

Diet in Parkinson’s Disease: Critical Role for the Microbiome

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Jackson, Aeja, Forsyth, Christopher B., Shaikh, Maliha, Voigt, Robin M., Engen, Phillip A., Ramirez, Vivian, Keshavarzian, Ali·2019·Frontiers in Neurology

DOI 10.3389/fneur.2019.01245PMC PMC6915094

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Abstract

Background. Parkinson’s disease (PD) is the most common movement disorder affecting up to 1% of the population above the age of 60 and 4–5% of those above the age of 85. Little progress has been made on efforts to prevent disease development or halt disease progression. Diet has emerged as a potential factor that may prevent the development or slow the progression of PD. In this review, we discuss evidence for a role for the intestinal microbiome in PD and how diet-associated changes in the microbiome may be a viable approach to prevent or modify disease progression. Methods. We reviewed studies demonstrating that dietary components/foods were related to risk for PD. We reviewed evidence for the dysregulated intestinal microbiome in PD patients including abnormal shifts in the intestinal microbiota composition (i.e., dysbiosis) characterized by a loss of short chain fatty acid (SCFA) bacteria and increased lipopolysaccharide (LPS) bacteria. We also examined several candidate mechanisms by which the microbiota can influence PD including the NLRP3 inflammasome, insulin resistance, mitochondrial function, vagal nerve signaling. Results. The PD-associated microbiome is associated with decreased production of SCFA and increased LPS and it is believed that these changes may contribute to the development or exacerbation of PD. Diet robustly impacts the intestinal microbiome and the Western diet is associated with increased risk for PD whereas the Mediterranean diet (including high intake of dietary fiber) decreases PD risk. Mechanistically this may be the consequence of changes in the relative abundance of SCFA-producing or LPS-containing bacteria in the intestinal microbiome with effects on intestinal barrier function, endotoxemia (i.e., systemic LPS), NLRP3 inflammasome activation, insulin resistance, and mitochondrial dysfunction, and the production of factors such as glucagon like peptide 1 (GLP-1) and brain derived neurotrophic factor (BDNF) as well as intestinal gluconeogenesis. Conclusions. This review summarizes a model of microbiota-gut-brain-axis regulation of neuroinflammation in PD including several new mechanisms. We conclude with the need for clinical trials in PD patients to test this model for beneficial effects of Mediterranean based high fiber diets.

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A high-fat, low-fiber Western diet is associated with an increased risk of Parkinson's disease.
“The high-fat, low-fiber Western diet has been associated with an increased risk of Parkinson’s disease.”
From Mediterranean Diet as an Antioxidant: The Impact on Metabolic Health and Overall Wellbeing (2021) · cites this paper as [112]

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“Change in life style with PD that helps patients to cope with symptoms can affect microbiota-like lack of exercise and change in diet- these changes can explain worsening of dysbiosis in those with a long duration of PD but also in early onset PD (138).”
Background
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 · see citing works
Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
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Vagotomy and subsequent risk of <scp>P</scp> arkinson's disease
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Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation
Yan, Y., Jiang, W., Spinetti, T., Tardivel, A., Castillo, R., Bourquin, C., Guarda, G., Tian, Z., Tschopp, J., & Zhou, R. (2013) · Immunity · doi:10.1016/j.immuni.2013.05.015 · Cited by 784 · see citing works
Association of coffee and caffeine intake with the risk of Parkinson disease
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Colonic microbiome is altered in alcoholism
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Docosahexaenoic Acid, a Ligand for the Retinoid X Receptor in Mouse Brain
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Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson's disease mice: gut microbiota, glial reaction and TLR4/TNF-α signaling pathway
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Inflammasome is a central player in the induction of obesity and insulin resistance
Stienstra, R., van Diepen, J. A., Tack, C. J., Zaki, M. H., van de Veerdonk, F. L., Perera, D., Neale, G. A., Hooiveld, G. J., Hijmans, A., Vroegrijk, I., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100255108 · Cited by 727 · see citing works
Microbiome-wide association studies link dynamic microbial consortia to disease
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Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model
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Canonical Nlrp3 Inflammasome Links Systemic Low-Grade Inflammation to Functional Decline in Aging
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Intermittent Fasting Promotes White Adipose Browning and Decreases Obesity by Shaping the Gut Microbiota
Li, G., Xie, C., Lu, S., Nichols, R. G., Tian, Y., Li, L., Patel, D., Ma, Y., Brocker, C. N., Yan, T., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.08.019 · Cited by 667 · see citing works
Dietary Fiber and Bacterial SCFA Enhance Oral Tolerance and Protect against Food Allergy through Diverse Cellular Pathways
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Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naive Parkinson's disease patients
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Inflammasomes in the CNS
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“Inflammasomes are present in peripheral immune cells such as macrophages, as well as in the brain and especially in microglia (206, 210, 211).”
Background
Butyrate, neuroepigenetics and the gut microbiome: Can a high fiber diet improve brain health?
Bourassa, M. W., Alim, I., Bultman, S. J., & Ratan, R. R. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.02.009 · Cited by 636 · see citing works
Intermittent metabolic switching, neuroplasticity and brain health
Mattson, M. P., Moehl, K., Ghena, N., Schmaedick, M., & Cheng, A. (2018) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.156 · Cited by 624 · see citing works
Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila
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Neuroprotection by Caffeine and A 2A Adenosine Receptor Inactivation in a Model of Parkinson's Disease
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Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease
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Triggering of inflammasome by aggregated α-synuclein, an inflammatory response in synucleinopathies
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Brain-Gut-Microbiota Axis in Parkinson’s Disease
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The neuroprotective properties of calorie restriction, the ketogenic diet, and ketone bodies
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Shifts on Gut Microbiota Associated to Mediterranean Diet Adherence and Specific Dietary Intakes on General Adult Population
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The nasal and gut microbiome in Parkinson's disease and idiopathic rapid eye movement sleep behavior disorder
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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
Dietary Omega-3 Fatty Acids Normalize BDNF Levels, Reduce Oxidative Damage, and Counteract Learning Disability after Traumatic Brain Injury in Rats
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Reduced BDNF mRNA Expression in the Parkinson's Disease Substantia Nigra
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D-β-Hydroxybutyrate rescues mitochondrial respiration and mitigates features of Parkinson disease
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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
Microbiome–microglia connections via the gut–brain axis
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Alpha-synuclein in colonic submucosa in early untreated Parkinson’s disease
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NLRP3 inflammasome in neurological diseases, from functions to therapies
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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
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Type 2 Diabetes and the Risk of Parkinson's Disease
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Is alpha-synuclein in the colon a biomarker for premotor Parkinson’s disease? Evidence from 3 cases
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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 Gastrointestinal Microbiome: Alcohol Effects on the Composition of Intestinal Microbiota
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MPTP-driven NLRP3 inflammasome activation in microglia plays a central role in dopaminergic neurodegeneration
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Pesticide exposure and risk for Parkinson's disease
Ascherio, A., Chen, H.-L., Weisskopf, M., O'Reilly, É., McCullough, M. L., Calle, E. E., Schwarzschild, M., & Thun, M. (2006) · Annals of Neurology · doi:10.1002/ana.20904 · Cited by 429 · see citing works
Metagenome-wide association studies: fine-mining the microbiome
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The MPTP Story
Langston, J. W. (2017) · Journal of Parkinson s Disease · doi:10.3233/jpd-179006 · Cited by 424 · see citing works
Behavioral Deficits Associated with Dietary Induction of Decreased Brain Docosahexaenoic Acid Concentration
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Pathological α‐synuclein in gastrointestinal tissues from prodromal <scp>P</scp> arkinson disease patients
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
(Dis)Trust your gut: the gut microbiome in age-related inflammation, health, and disease
Buford, T. W. (2017) · Microbiome · doi:10.1186/s40168-017-0296-0 · Cited by 409 · 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
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Review: Sporadic Parkinson's disease: development and distribution ofα‐synuclein pathology
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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
Fast food fever: reviewing the impacts of the Western diet on immunity
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Anti–Tumor Necrosis Factor Therapy and Incidence of Parkinson Disease Among Patients With Inflammatory Bowel Disease
Peter, I., Dubinsky, M., Bressman, S., Park, A., Lu, C., Chen, N., & Wang, A. (2018) · JAMA Neurology · doi:10.1001/jamaneurol.2018.0605 · Cited by 386 · see citing works
Caloric restriction increases neurotrophic factor levels and attenuates neurochemical and behavioral deficits in a primate model of Parkinson's disease
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The glucagon-like peptide 1 (GLP) receptor as a therapeutic target in Parkinson's disease: mechanisms of action
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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
Secretory Products of the Human GI Tract Microbiome and Their Potential Impact on Alzheimer's Disease (AD): Detection of Lipopolysaccharide (LPS) in AD Hippocampus
Zhao, Y., Jaber, V., & Lukiw, W. J. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00318 · Cited by 379 · see citing works
Restructuring of the Gut Microbiome by Intermittent Fasting Prevents Retinopathy and Prolongs Survival in db/db Mice
Beli, E., Yan, Y., Moldovan, L., Vieira, C. P., Gao, R., Duan, Y., Prasad, R., Bhatwadekar, A. D., White, F. A., Townsend, S. D., et al. (2018) · Diabetes · doi:10.2337/db18-0158 · Cited by 372 · see citing works
A healthy gastrointestinal microbiome is dependent on dietary diversity
Heiman, M. L., & Greenway, F. L. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2016.02.005 · Cited by 370 · see citing works
β-hydroxybutyrate deactivates neutrophil NLRP3 inflammasome to relieve gout flares
Goldberg, E. L., Asher, J. L., Molony, R. D., Shaw, A. C., Zeiss, C. J., Wang, C., Morozova-Roche, L. A., Herzog, R. I., Iwasaki, A., & Dixit, V. D. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.004 · Cited by 370 · cited 1× · see citing works
“Indeed, BHB directly inhibits the NLRP3 inflammasome and attenuates NLRP3-mediated inflammatory disease (287, 290).”
Background
Gut microbiota in Parkinson's disease: Temporal stability and relations to disease progression
Aho, V. T. E., Pereira, P. A. B., Voutilainen, S., Paulin, L., Pekkonen, E., Auvinen, P., & Scheperjans, F. (2019) · eBioMedicine · doi:10.1016/j.ebiom.2019.05.064 · Cited by 361 · see citing works
Prospective study of dietary pattern and risk of Parkinson disease
Gao, X., Chen, H., Fung, T. T., Logroscino, G., Schwarzschild, M. A., Hu, F. B., & Ascherio, A. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.5.1486 · Cited by 340 · see citing works
Microbiome-Gut-Brain Axis and Toll-Like Receptors in Parkinson’s Disease
Caputi, V., & Giron, M. C. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19061689 · Cited by 338 · see citing works
Habitual intake of dietary flavonoids and risk of Parkinson disease
Gao, X., Cassidy, A., Schwarzschild, M. A., Rimm, E. B., & Ascherio, A. (2012) · Neurology · doi:10.1212/wnl.0b013e31824f7fc4 · Cited by 333 · see citing works
Insulin resistance and Parkinson’s disease: A new target for disease modification?
Athauda, D. S., & Foltynie, T. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.10.001 · Cited by 333 · see citing works
Gut to Brain Dysbiosis: Mechanisms Linking Western Diet Consumption, the Microbiome, and Cognitive Impairment
Noble, E. E., Hsu, T. M., & Kanoski, S. E. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00009 · Cited by 333 · see citing works
Colonic infusions of short-chain fatty acid mixtures promote energy metabolism in overweight/obese men: a randomized crossover trial
Canfora, E. E., van der Beek, C. M., Jocken, J. W. E., Goossens, G. H., Holst, J. J., Olde Damink, S. W. M., Lenaerts, K., Dejong, C. H. C., & Blaak, E. E. (2017) · Scientific Reports · doi:10.1038/s41598-017-02546-x · Cited by 331 · see citing works
Dietary Docosahexaenoic Acid and Docosapentaenoic Acid Ameliorate Amyloid-β and Tau Pathology via a Mechanism Involving Presenilin 1 Levels
Green, K. N., Martínez‐Coria, H., Khashwji, H., Hall, E. B., Yurko‐Mauro, K., Ellis, L., & LaFerla, F. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0055-07.2007 · Cited by 326 · see citing works
Biophysics of Parkinsons Disease: Structure and Aggregation of α- Synuclein
Uversky, V. N., & Eliezer, D. (2009) · Current Protein and Peptide Science · doi:10.2174/138920309789351921 · Cited by 320 · see citing works
A meta-analysis of Parkinson's disease and exposure to pesticides.
Priyadarshi, A., Khuder, S., Schaub, E. A., & Shrivastava, S. (2000) · PubMed · Cited by 319 · see citing works
Parkinson's disease and pesticides: a toxicological perspective
Hatcher, J. M., Pennell, K. D., & MILLER, G. (2008) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.03.007 · Cited by 319 · see citing works
Circulating endotoxin and systemic immune activation in sporadic amyotrophic lateral sclerosis (sALS)
Zhang, R., Miller, R. G., Gascon, R., Champion, S., Katz, J., Lancero, M., Narvaez, A., Honrada, R., Ruvalcaba, D., & McGrath, M. S. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.09.017 · Cited by 319 · 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
Fecal markers of intestinal inflammation and intestinal permeability are elevated in Parkinson's disease
Schwiertz, A., Spiegel, J., Dillmann, U., Grundmann, D., Bürmann, J., Faßbender, K., Schäfer, K.-H., & Unger, M. M. (2018) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2018.02.022 · 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
Environmental toxins and Parkinson's disease: what have we learned from pesticide-induced animal models?
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The pathogenic role of the inflammasome in neurodegenerative diseases
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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
Mitochondrial dysfunction and oxidative stress activate inflammasomes: impact on the aging process and age-related diseases
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Treatment of Parkinson disease with diet-induced hyperketonemia: A feasibility study
VanItallie, T. B., Nonas, C., Rocco, A. D., Boyar, K. L., Hyams, K., & Heymsfield, S. B. (2005) · Neurology · doi:10.1212/01.wnl.0000152046.11390.45 · Cited by 300 · see citing works
Gastrointestinal dysfunction in Parkinson's disease
Pfeiffer, R. F. (2011) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2010.08.003 · Cited by 298 · see citing works
History and Current Use of Antimicrobial Drugs in Veterinary Medicine
Prescott, J. F. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.arba-0002-2017 · Cited by 297 · see citing works
Central effects of GLP-1: new opportunities for treatments of neurodegenerative diseases
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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
Transporters and receptors for short-chain fatty acids as the molecular link between colonic bacteria and the host
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Ghrelin promotes and protects nigrostriatal dopamine function via a UCP2-dependent mitochondrial mechanism
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“Briefly these include PD subjects to exhibit: increased relative abundance of genera Akkermansia (7 studies) (98, 105, 108– 112), Bifidobacterium (5 studies) (103, 108, 110, 113, 114), and Lactobacillus (7 studies) (97, 103, 110, 111, 113, 115, 116); decreased abundance of genus Prevotella (7 studies) (97, 103, 104, 1…”
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[15]Anderson C Checkoway H Franklin GM Beresford S Smith-Weller T Swanson PD. Dietary factors in Parkinson's disease: the role of food groups and specific foods. Mov Disord. (1999) 14: 21– 7. 9918340

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Diet and the microbiome in Parkinson's disease
Metcalfe‐Roach, A. (2025) · cIRcle (University of British Columbia) · doi:10.14288/1.0444180

Authors: Jackson, A., Forsyth, C. B., Shaikh, M., Voigt, R. M., Engen, P. A., Ramirez, V., & Keshavarzian, A.
Affiliations: Rush University Medical Center (US)
Corresponding author: Keshavarzian, Ali
ORCID: Jackson, Aeja
Forsyth, Christopher B.
Voigt, Robin M.
Engen, Phillip A.
Keshavarzian, Ali
Venue: Frontiers in Neurology
Publisher: Frontiers Media SA
Published: 2019-12-10
Volume: 10
Pages: 1245-1245
ISSN: 1664-2295 (ISSN-L)
DOI: 10.3389/fneur.2019.01245
PMC: PMC6915094
OpenAlex: W2995752611
Cited by: 145
References: 328
Citations by year: 2026: 16 · 2025: 22 · 2024: 21 · 2023: 17 · 2022: 35 · 2021: 18 · 2020: 13 · 2019: 1 · 2018: 1
FWCI: 1.48
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Frontiers in Neurology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: U.S. Department of Defense
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
Keywords: Parkinson's disease, diet, gut microbiota, dysbiosis, short-chain fatty acids, lipopolysaccharide, Western diet, Mediterranean diet, dietary fiber, NLRP3 inflammasome, insulin resistance, mitochondrial dysfunction, microbiota-gut-brain axis, neuroinflammation, endotoxemia, intestinal barrier function, glucagon-like peptide-1, brain-derived neurotrophic factor, intestinal gluconeogenesis

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Diet in Parkinson’s Disease: Critical Role for the Microbiome

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