A meta‐analysis of coffee drinking, cigarette smoking, and the risk of Parkinson's disease
Abstract
We conducted a systematic review to summarize the epidemiological evidence on the association between cigarette smoking, coffee drinking, and the risk of Parkinson's disease. Case–control and cohort studies that reported the relative risk of physician‐confirmed Parkinson's disease by cigarette smoking or coffee drinking status were included. Study‐specific log relative risks were weighted by the inverse of their variances to obtain a pooled relative risk and its 95% confidence interval (CI). Results for smoking were based on 44 case–control and 4 cohort studies, and for coffee 8 case–control and 5 cohort studies. Compared with never smokers, the relative risk of Parkinson's disease was 0.59 (95% CI, 0.54–0.63) for ever smokers, 0.80 (95% CI, 0.69–0.93) for past smokers, and 0.39 (95% CI, 0.32–0.47) for current smokers. The relative risk per 10 additional pack‐years was 0.84 (95% CI, 0.81–0.88) in case–control studies and 0.78 (95% CI, 0.73–0.84) in cohort studies. Compared with non–coffee drinkers, relative risk of Parkinson's disease was 0.69 (95% CI, 0.59–0.80) for coffee drinkers. The relative risk per three additional cups of coffee per day was 0.75 (95% CI, 0.64–0.86) in case–control studies and 0.68 (95% CI, 0.46–1.00) in cohort studies. This meta‐analysis shows that there is strong epidemiological evidence that smokers and coffee drinkers have a lower risk of Parkinson's disease. Further research is required on the biological mechanisms underlying this potentially protective effect.
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The Parkinson disease risk reduction documented in the meta-analysis (OR = 0.67) was of a similar order of magnitude to risk reductions previously noted with caffeine consumption or smoking.
“To put this into perspective, the risk reduction documented in this meta-analysis (OR ϭ 0.67) was of a similar order of magnitude to the PD risk reductions previously noted with caffeine consumption or smoking, 8”
From Does vigorous exercise have a neuroprotective effect in Parkinson disease? (2011) · cites this paper as [8]
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“A recent meta-analysis (Hernán et al. 2002) showed that the overall risk of PD was 30% lower among coffee drinkers and 60% lower among smokers, suggesting that these factors are protective.”
MethodEnvironmental risk factors and Parkinson's disease: An umbrella review of meta-analyses
Bellou, V., Belbasis, L., Tzoulaki, I., Εvangelou, Ε., & Ioannidis, J. P. A. (2015) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2015.12.008 · Cited by 429 · see citing works
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
Inverse association between cancer and Alzheimer's disease: results from the Framingham Heart Study
Driver, J. A., Beiser, A., Au, R., Kreger, B. E., Splansky, G. L., Kurth, T., Kiel, D. P., Lu, K. P., Seshadri, S., & Wolf, P. A. (2012) · BMJ · doi:10.1136/bmj.e1442 · Cited by 425 · see citing works
Pooled analysis of tobacco use and risk of Parkinson disease.
Ritz, B., Ascherio, A., Checkoway, H., Marder, K., Nelson, L., Rocca, W., Ross, G., Strickland, D., den Eeden, S. K. V., & Gorell, J. (2007) · Archives of Neurology · doi:10.1001/archneur.64.7.990 · Cited by 366 · see citing works
“Our analyses confirmed prior reports of an inverse association between cigarette smoking and PD similar in size to those reported in a recent meta-analysis.(9) We also showed that associations did not differ by sex or educational status.”
ResultEarly Environmental Origins of Neurodegenerative Disease in Later Life
Landrigan, P. J., Sonawane, B., Butler, R. N., Trasande, L., Callan, R., & Droller, D. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7571 · Cited by 357 · see citing works
O’Keefe, J. H., Bhatti, S. K., Patil, H., DiNicolantonio, J. J., Lucan, S. C., & Lavie, C. J. (2013) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2013.06.035 · Cited by 353 · see citing works
“Other beneficial health effects of coffee may include reduced risks of Alzheimer’s dementia (52,53) and other diseases of the central nervous system including Parkinson’s disease (54-56).”
BackgroundOxidative damage to macromolecules in human Parkinson disease and the rotenone model
Sanders, L. H., & Greenamyre, J. T. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.01.003 · Cited by 347 · see citing works
“include smoking, well-water consumption, exercise, head trauma, and infectious agents [111–116].”
The two-century journey of Parkinson disease research
Przedborski, S. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.25 · Cited by 344 · see citing works
Pesticide Exposure and Self-reported Parkinson's Disease in the Agricultural Health Study
Kamel, F., Tanner, C. M., Umbach, D. M., Hoppin, J. A., Alavanja, M. C. R., Blair, A. E., Comyns, K., Goldman, S., Korell, M., Langston, J. W., et al. (2006) · American Journal of Epidemiology · doi:10.1093/aje/kwk024 · Cited by 339 · see citing works
“Consistent with previous reports (1, 46 ), we found an inverse association of cigarette smoking with PD. The association was stronger in prevalent cases than in incident cases.”
Exposure to pesticides or solvents and risk of Parkinson disease
Pezzoli, G., & Cereda, E. (2013) · Neurology · doi:10.1212/wnl.0b013e318294b3c8 · Cited by 327 · see citing works
Caffeine use in children: What we know, what we have left to learn, and why we should worry
Temple, J. L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.01.001 · Cited by 328 · see citing works
“Finally, there is some evidence of an inverse relationship between caffeine consumption and colorectal cancer (Giovannucci, 1998; Tavani and La Vecchia, 2004) and Parkinson’s disease (Hernan et al., 2002; Ross et al., 2000), but the mechanisms for this apparent protection remain unknown.”
The Role of Innate and Adaptive Immunity in Parkinson's Disease
Kannarkat, G. T., Boss, J. M., & Tansey, M. G. (2013) · Journal of Parkinson’s Disease · doi:10.3233/jpd-130250 · Cited by 324 · see citing works
“PD risk is increased by pesticide/ organophosphate exposure and head trauma while it is decreased by moderate amounts of cigarette use and caffeine consumption [13-15].”
BackgroundBiophysics 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
Larsson, S. C., & Burgess, S. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104154 · Cited by 319 · see citing works
Arendash, G. W., Mori, T., Cao, C., Mamcarz, M., Runfeldt, M., Dickson, A., Rezai-Zadeh, K., Tan, J., Citron, B. A., Lin, X., et al. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-1087 · Cited by 308 · see citing works
“More recently, several longitudinal studies have reported that daily caffeine intake, equivalent to 3 or more cups of coffee, reduces cognitive decline in “non-demented” elderly men and women [6, 7].”
Caffeine for treatment of Parkinson disease
Postuma, R. B., Lang, A. E., Munhoz, R. P., Charland, K., Pelletier, A., Moscovich, M., Filla, L., Zanatta, D., Romenets, S. R., Altman, R., et al. (2012) · Neurology · doi:10.1212/wnl.0b013e318263570d · Cited by 300 · see citing works
Incidence and remaining lifetime risk of Parkinson disease in advanced age
Driver, J. A., Logroscino, G., Gaziano, J. M., & Kurth, T. (2009) · Neurology · doi:10.1212/01.wnl.0000341769.50075.bb · Cited by 298 · see citing works
Identification of novel biomarkers for Parkinson's disease by metabolomic technologies
Hatano, T., Saiki, S., Okuzumi, A., Mohney, R., & Hattori, N. (2015) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2014-309676 · Cited by 257 · see citing works
Coffee and tea consumption and the risk of Parkinson's disease
Hu, G., Bidel, S., Jousilahti, P., Antikaínen, R., & Tuomilehto, J. O. (2007) · Movement Disorders · doi:10.1002/mds.21706 · Cited by 281 · see citing works
LRRK2 levels in immune cells are increased in Parkinson’s disease
Cook, D. A., Kannarkat, G. T., Cintron, A. F., Butkovich, L. M., Fraser, K. B., Chang, J., Grigoryan, N., Factor, S. A., West, A. B., Boss, J. M., et al. (2017) · npj Parkinson's Disease · doi:10.1038/s41531-017-0010-8 · Cited by 279 · see citing works
Association of Coffee Consumption With Total and Cause-Specific Mortality Among Nonwhite Populations
Park, S., Freedman, N. D., Haiman, C. A., Marchand, L. L., Wilkens, L. R., & Setiawan, V. W. (2017) · Annals of Internal Medicine · doi:10.7326/m16-2472 · Cited by 278 · see citing works
“Previous studies have indicated that coffee consumption is inversely associated with several types of cancer (2), diabetes (3, 4), liver disease (5), Parkinson disease (6, 7), and other chronic diseases (8).”
BackgroundDietary fatty acids and the risk of Parkinson disease
de Lau, L. M. L., Bornebroek, M., Witteman, J. C. M., Albert Hofman, D., Koudstaal, P. J., & Breteler, M. M. B. (2005) · Neurology · doi:10.1212/01.wnl.0000166038.67153.9f · Cited by 260 · see citing works
Neurodegeneration and neuroprotection in Parkinson disease
Fahn, S., & Sulzer, D. L. (2004) · Neurotherapeutics · doi:10.1602/neurorx.1.1.139 · Cited by 266 · see citing works
“Moreover, the pattern of neuronal loss in the SN in patients with PD and in the normal aging population differs, 18 again indicating that accelerated aging alone is not responsible for causing PD.”
BackgroundInfluentialNeuroprotective Effects of Coffee Bioactive Compounds: A Review
Socała, K., Szopa, A., Serefko, A., Poleszak, E., & Właź, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010107 · Cited by 263 · see citing works
Costa, J. N., Lunet, N., Santos, C. D., dos Santos, J. P., & Carneiro, A. V. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-091525 · Cited by 254 · see citing works
“The search date of the previous most recent systematic review on the risk of PD and caffeine exposure was 2001 [17].”
InfluentialParkinson’s disease and cancer risk: a systematic review and meta-analysis
Bajaj, A., Driver, J. A., & Schernhammer, E. S. (2010) · Cancer Causes & Control · doi:10.1007/s10552-009-9497-6 · Cited by 244 · see citing works
“Another common hypothesis for a decreased incidence of cancer in patients with PD is the well-known negative association between PD and smoking [55].”
BackgroundParkinson's Disease Therapeutics: New Developments and Challenges Since the Introduction of Levodopa
Smith, Y., Wichmann, T., Factor, S. A., & DeLong, M. R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.212 · Cited by 246 · see citing works
Breckenridge, C. B., Berry, C. L., Chang, E. T., Sielken, R. L., & Mandel, J. S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151841 · Cited by 239 · see citing works
“consistently inversely associated with PD [37, 39, 40], whereas positive associations have been reported PD between and rural living, well-water consumption, farming or pesticide use [28– 30, 36, 37].”
BackgroundResultThe lipopolysaccharide Parkinson’s disease animal model: mechanistic studies and drug discovery
Dutta, G., Zhang, P., & Liu, B. (2008) · Fundamental & Clinical Pharmacology · doi:10.1111/j.1472-8206.2008.00616.x · Cited by 235 · see citing works
Ascherio, A. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh312 · Cited by 232 · see citing works
Dórea, J. G., & da Costa, T. H. M. (2005) · British Journal Of Nutrition · doi:10.1079/bjn20051370 · Cited by 232 · see citing works
“The meta-analysis of Hernan et al. (2002) concluded that there was strong epidemiological evidence that coffee-drinkers have a lower risk of Parkinson’s disease.”
Hamza, T. H., Chen, H., Hill-Burns, E. M., Rhodes, S. L., Montimurro, J., Kay, D. M., Tenesa, A., Kusel, V. I., Sheehan, P., Eaaswarkhanth, M., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002237 · Cited by 218 · see citing works
A prescription for lifestyle change in patients with hyperuricemia and gout
Choi, H. K. (2010) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e328335ef38 · Cited by 219 · see citing works
Smoking duration, intensity, and risk of Parkinson disease
Chen, H., Huang, X., Guo, X., Mailman, R. B., Park, Y., Kamel, F., Umbach, D. M., Xu, Q., Hollenbeck, A. R., Schatzkin, A. G., et al. (2010) · Neurology · doi:10.1212/wnl.0b013e3181d55f38 · Cited by 222 · see citing works
Fardet, A., & Boirie, Y. (2014) · Nutrition Reviews · doi:10.1111/nure.12153 · Cited by 221 · see citing works
CYP2D6 polymorphism, pesticide exposure, and Parkinson's disease
Elbaz, A., Lévecque, C., Clavel, J., Vidal, J., Richard, F., Amouyel, P., Alpérovitch, A., Chartier‐Harlin, M., & Tzourio, C. (2004) · Annals of Neurology · doi:10.1002/ana.20051 · Cited by 212 · see citing works
Nørgaard, M., Ehrenstein, V., & Vandenbroucke, J. P. (2017) · Clinical Epidemiology · doi:10.2147/clep.s129879 · Cited by 211 · see citing works
“…smoking is associated with an increased risk of peptic ulcer (the underlying indication for vagotomy) 17 and, at the same time, may protect against Parkinson’s disease, 18 lack of data on smoking was of concern, as smoking, rather than vagotomy, could be behind the observed protective association.”
Atypical cancer pattern in patients with Parkinson's disease
Olsen, J. H., Friis, S., Frederiksen, K., McLaughlin, J. K., Mellemkjær, L., & Møller, H. (2004) · British Journal of Cancer · doi:10.1038/sj.bjc.6602279 · Cited by 210 · see citing works
“The risk reduction has been related to the relatively consistent observation that a high proportion of individuals who later develop Parkinson’s disease are lifelong nonsmokers, as compared with the general population (Hernan et al, 2002).”
BackgroundVisual symptoms in Parkinson's disease and Parkinson's disease dementia
Archibald, N. K., Clarke, M. P., Mosimann, U. P., & Burn, D. J. (2011) · Movement Disorders · doi:10.1002/mds.23891 · Cited by 207 · see citing works
Association of Cumulative Lead Exposure with Parkinson’s Disease
Weisskopf, M. G., Weuve, J., Nie, H., Saint‐Hilaire, M., Sudarsky, L. R., Simon, D. K., Hersh, B. P., Schwartz, J. D., Wright, R. O., & Hu, H. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1002339 · Cited by 207 · see citing works
“04), which is not as strong an inverse association as in other reports (Hernan et al. 2002), likely because smoking behaviors tend to be concordant among spouses, relatives, and friends (Di Castelnuovo et al.”
ResultInfluentialSerum Cholesterol Levels and the Risk of Parkinson's Disease
de Lau, L. M. L., Koudstaal, P. J., Albert Hofman, D., & Breteler, M. M. B. (2006) · American Journal of Epidemiology · doi:10.1093/aje/kwj283 · Cited by 205 · see citing works
“Additional adjustments were made for smoking habits, vitamin E intake, and coffee consumption, because all of these factors have been related to a decreased risk of Parkinson’s disease ( 11 , 12) and probably are associated with concentrations of total and high density lipoprotein cholesterol (13).”
BackgroundBody mass index and the risk of Parkinson disease
Hu, G., Jousilahti, P., Nissinen, A., Antikainen, R., Kivipelto, M., & Tuomilehto, J. (2006) · Neurology · doi:10.1212/01.wnl.0000247052.18422.e5 · Cited by 203 · see citing works
Caffeine and Coffee as Therapeutics Against Alzheimer's Disease
Arendash, G. W., & Cao, C. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-091249 · Cited by 202 · see citing works
Parkinson's disease: Evidence for environmental risk factors
Kieburtz, K. D., & Wunderle, K. B. (2012) · Movement Disorders · doi:10.1002/mds.25150 · Cited by 199 · see citing works
Caffeine Intake and Dementia: Systematic Review and Meta-Analysis
Santos, C. D., Costa, J. N., dos Santos, J. P., Carneiro, A. V., & Lunet, N. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-091387 · Cited by 193 · see citing works
“However, studies on the etiologic role of caffeine intake are less frequent than those focusing on the effects of tobacco, as shown in two meta-analyses addressing the association between coffee drinking, cigarette smoking and Parkinson’s disease, with 13 and 48 individual studies, respectively [33].”
Crippa, A., Discacciati, A., Larsson, S. C., Wolk, A., & Orsini, N. (2014) · American Journal of Epidemiology · doi:10.1093/aje/kwu194 · Cited by 191 · see citing works
Environment, lifestyle, and Parkinson's disease: Implications for prevention in the next decade
Marras, C., Canning, C. G., & Goldman, S. M. (2019) · Movement Disorders · doi:10.1002/mds.27720 · Cited by 192 · see citing works
“Despite these challenges, greater caffeine intake and higher levels of vitamin D have been shown in multiple studies and meta-analyses to be inversely associated with PD.(62,63) Longitudinal studies documenting reduced caffeine intake prior to the onset of PD have demonstrated an inverse association supporting its cla…”
BackgroundAssociation between cigarette smoking and Parkinson’s disease: A meta-analysis
Li, X., Li, W., Liu, G., Shen, X., & Tang, Y. (2015) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2015.08.004 · Cited by 190 · see citing works
“…factors might be linked to PD. Results from the present meta-analyses suggested a strong inverse association between active cigarette smoking and PD, which is in accordance with earlier studies (Hernán et al., 2002; Allam, Campbell, Castillo et al., 2004; Allam, Campbell, Hofman et al., 2004).”
InfluentialTan, E., Tan, C. I. C., Fook-Chong, S. M. C., Lum, S. Y., Chai, A., Chung, H., Shen, H., Zhao, Y., Teoh, M. L., Yih, Y., et al. (2003) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2003.07.006 · Cited by 186 · see citing works
“A recent meta-analysis demonstrates smoking and coffee to reduce the risk of PD by 60% and 30% [5].”
BackgroundMethodEvans, A. H. (2005) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2005.065417 · Cited by 184 · see citing works
Coffee consumption and disease correlations
Gökcen, B. B., & Şanlıer, N. (2017) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2017.1369391 · Cited by 188 · see citing works
Tan, L. C. S., Koh, W., Yuan, J., Wang, R., Au, W., Tan, J.-H., Tan, E., & Yu, M. C. (2007) · American Journal of Epidemiology · doi:10.1093/aje/kwm338 · Cited by 183 · see citing works
“A metaanalysis involving eight case-control and four cohort studies showed that daily coffee drinkers, compared with nondrinkers, have a lower risk of Parkinson’s disease (relative risk ¼ 0.69, 95 percent confidence interval: 0.59, 0.80) ( 3 ).”
BackgroundResultInfluentialProspective study of coffee consumption and risk of Parkinson’s disease
Sääksjärvi, K., Knekt, P., Rissanen, H., Laaksonen, M. A., Reunanen, A., & Männistö, S. (2008) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602788 · Cited by 182 · see citing works
“Among dietary factors, coffee consumption has been considered to reduce the risk of Parkinson’s disease (Hernan et al., 2002).”
Driver, J. A. (2014) · Biogerontology · doi:10.1007/s10522-014-9523-2 · Cited by 182 · see citing works
“One is the fact that people who develop PD tend to be lifelong non-smokers (Hernan et al. 2002).”
BackgroundConsumers’ Perceptions of Coffee Health Benefits and Motives for Coffee Consumption and Purchasing
Samoggia, A., & Riedel, B. (2019) · Nutrients · doi:10.3390/nu11030653 · Cited by 179 · see citing works
Neural Systems Governed by Nicotinic Acetylcholine Receptors: Emerging Hypotheses
Miwa, J. M., Freedman, R., & Lester, H. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.014 · Cited by 205 · see citing works
“The most common example of such a desensitizing response to nicotine occurs at the presynaptic terminals of nigrostriatal dopaminergic neurons (Xiao et al., 2009). two—when one considers that it derives from retrospective epidemiological studies (Hernán et al., 2002).”
Cancer and Neurodegeneration: Between the Devil and the Deep Blue Sea
Plun‐Favreau, H., Lewis, P. A., Hardy, J., Martins, L. M., & Wood, N. W. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001257 · Cited by 173 · see citing works
Serum Iron Levels and the Risk of Parkinson Disease: A Mendelian Randomization Study
Pichler, I., Del Greco M., F., Gögele, M., Lill, C. M., Bertram, L., Do, C. B., Eriksson, N., Foroud, T., Myers, R. H., PD GWAS Consortium, et al. (2013) · PLoS Medicine · doi:10.1371/journal.pmed.1001462 · Cited by 173 · see citing works
Parkinson’s Disease and the Gastrointestinal Microbiome
Lubomski, M., Tan, A. H., Lim, S.-Y., Holmes, A. J., Davis, R. L., & Sue, C. M. (2020) · Journal of Neurology · doi:10.1007/s00415-019-09320-1 · Cited by 172 · see citing works
“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].”
BackgroundRisk factors for dementia with Lewy bodies
Boot, B. P., Orr, C., Ahlskog, J. E., Ferman, T. J., Roberts, R. O., Pankratz, V. S., Dickson, D. W., Parisi, J. E., Aakre, J. A., Geda, Y. E., et al. (2013) · Neurology · doi:10.1212/wnl.0b013e3182a2cbd1 · Cited by 174 · see citing works
Caffeine Intake, Smoking, and Risk of Parkinson Disease in Men and Women
Liu, R., Guo, X., Park, Y., Huang, X., Sinha, R. R., Freedman, N. D., Hollenbeck, A. R., Blair, A. E., & Chen, H. (2012) · American Journal of Epidemiology · doi:10.1093/aje/kwr451 · Cited by 171 · see citing works
Malignant Melanoma and Other Types of Cancer Preceding Parkinson Disease
Olsen, J. H., Friis, S. R., & Frederiksen, K. (2006) · Epidemiology · doi:10.1097/01.ede.0000229445.90471.5e · Cited by 171 · see citing works
“These findings are in accord with the findings of large prospective studies, which have all shown that the incidence of Parkinson disease is approximately 60% lower among current smokers and 40% lower among past smokers than among those who have never smoked and that the risk reduction diminishes with time after quitt…”
BackgroundResultProjection of the prevalence of Parkinson's disease in the coming decades: Revisited
Rossi, A., Berger, K., Chen, H., LESLIE, D. L., Mailman, R. B., & Huang, X. (2017) · Movement Disorders · doi:10.1002/mds.27063 · Cited by 170 · see citing works
“This also holds true for the degree of risk modification due to smoking that is used in the model, which also varies in the literature.(9,15) A recent study by Savica and colleagues(32) demonstrated that the incidence of PD might have increased during the 30-year time period from 1976 to 2005.”
Parkinson’s disease is associated with DNA methylation levels in human blood and saliva
Chuang, Y., Paul, K. C., Bronstein, J. M., Bordelon, Y. M., Horvath, S., & Ritz, B. R. (2017) · Genome Medicine · doi:10.1186/s13073-017-0466-5 · Cited by 168 · see citing works
Gout and risk of Parkinson disease
Alonso, Á., Rodríguez, L. A. G., Logroscino, G., & Hernán, M. Á. (2007) · Neurology · doi:10.1212/01.wnl.0000279518.10072.df · Cited by 166 · see citing works
Self-citationGene–environment interactions: Key to unraveling the mystery of Parkinson's disease
Gao, H., & Hong, J. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.03.005 · Cited by 164 · see citing works
Postural Instability in Parkinson’s Disease: A Review
Palakurthi, B., & Burugupally, S. P. (2019) · Brain Sciences · doi:10.3390/brainsci9090239 · Cited by 165 · see citing works
“Caffeine, a nonselective antagonist of adenosine receptors, has been known to decrease the risk of PD [74], with a greater reduction of the PIGD subtype risk when compared to the TD subtype [12,75,76].”
ResultA Prospective Cohort Study of Cancer Incidence Following the Diagnosis of Parkinson's Disease
Driver, J. A., Logroscino, G., Buring, J. E., Gaziano, J. M., & Kurth, T. (2007) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-07-0038 · Cited by 164 · see citing works
Parkinson disease and smoking revisited
Ritz, B. R., Lee, P., Lassen, C. F., & Arah, O. A. (2014) · Neurology · doi:10.1212/wnl.0000000000000879 · Cited by 161 · see citing works
Preventing Parkinson’s Disease: An Environmental Agenda
Miranda, B. R. D., Goldman, S. M., Miller, G. W., Greenamyre, J. T., & Dorsey, E. R. (2021) · Journal of Parkinson s Disease · doi:10.3233/jpd-212922 · Cited by 161 · see citing works
“Because the553 pathological elevation in LRRK2 kinase activity554 induced by environmental toxicants is similar to555 LRRK2 gain-of-function mutations, pharmaceuti-556 cal inhibiton of LRRK2 by small molecule kinase557 inhibitors currently under clinical review [107],558 could be appropriate for individuals following…”
BackgroundInfluentialNeurologic Manifestations of Chronic Methamphetamine Abuse
Rusyniak, D. E. (2013) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2013.02.005 · Cited by 162 · see citing works
- Authors
- Hernán, M. A., Takkouche, B., Caamaño‐Isorna, F., & Gestal‐Otero, J. J.
- Affiliations
- Universidade de Santiago de Compostela (ES)
- Venue
- Annals of Neurology
- Publisher
- Wiley
- Published
- 2002-05-29
- Volume
- 52
- Issue
- 3
- Pages
- 276-284
- ISSN
- 0364-5134 (ISSN-L)
- 1531-8249
- OpenAlex
- W2053969387
- Cited by
- 818
- References
- 62
- Citations by year
- 2026: 21 · 2025: 28 · 2024: 24 · 2023: 35 · 2022: 28 · 2021: 48 · 2020: 41 · 2019: 36 · 2018: 31 · 2017: 43 · 2016: 36 · 2015: 44 · 2014: 43 · 2013: 40 · 2012: 35
- FWCI
- 3.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Pharmacology › Coffee research and impacts
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Keywords
- Parkinson's disease, coffee consumption, cigarette smoking, pack-years, disease risk, protective factors, neurodegeneration
- MeSH terms
- Coffee, Humans, Parkinson Disease, Risk Factors, Smoking, Cohort Studies, Case-Control Studies
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