Meta‐analysis: Association of Helicobacter pylori infection with Parkinson's diseases

Shen, Xiaoli; Yang, Huazhen; Wu, Yili; Zhang, Dongfeng; Jiang, Hong

doi:10.1111/hel.12398

Cited by 114Helicobacter pylori-related gastroenterology studiesParkinson's Disease Mechanisms and TreatmentsGut microbiota and health

Meta‐analysis: Association of Helicobacter pylori infection with Parkinson's diseases

Shen, Xiaoli, Yang, Huazhen, Wu, Yili, Zhang, Dongfeng, Jiang, Hong·2017·Helicobacter

DOI 10.1111/hel.12398

Open this paper in CoChat — free account

Abstract

Background: The results from observational studies on the relationship between helicobacter pylori (H. pylori) infection and Parkinson's disease remain controversial. A meta‐analysis was conducted to evaluate the association between helicobacter pylori infection and Parkinson's disease. Methods: A comprehensive literature search was performed on relevant studies published from January 1983 to January 2017 in PubMed, Web of Science and EMBASE databases. The fixed or random effects model was used to pool the odds ratio with 95% confidence interval from individual studies. Publication bias was estimated by Egger's test and the funnel plot. Results: Eight eligible studies involving 33 125 participants were included in this meta‐analysis. Compared with the no helicobacter pylori infected person, the pooled odds ratio of Parkinson's disease in helicobacter pylori infected person was 1.59 (95% confidence interval: 1.37‐1.85). In subgroup analyzes, the combined odds ratios were 1.96 (1.23‐3.12) in Asia, 1.55 (1.32‐1.82) in Europe, 1.59 (1.35‐1.88) in case‐control studies, 1.56 (1.01‐2.39) in cross‐sectional studies, 1.56 (1.32‐1.85) in studies with confounders adjusted, and 1.71 (1.21‐2.43) in studies with no confounder adjusted, respectively. Conclusions: This meta‐analysis indicated that H. pylori infection might be associated with the risk of Parkinson's disease.

Integrity signals

Registry

Crossref · 10.1111/hel.12398

Cites

52 of 52 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?

Changing the endotoxin-producing bacterial species can affect Parkinson's disease in patients and mouse models.
“changing the endotoxin-producing bacterial species can affect the disease in patients and mouse models.”
From The endotoxin hypothesis of neurodegeneration (2019) · cites this paper as [96]
Gut colonisation with endotoxin-producing Helicobacter pylori is associated with Parkinson's disease, and eradication of H. pylori improved PD symptoms.
“Gut colonisation with endotoxin-producing Helicobacter pylori is associated with PD [96], and eradication of H. pylori improved PD symptoms [97, 98].”
From The endotoxin hypothesis of neurodegeneration (2019) · cites this paper as [96]

Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888 · see citing works
Epidemiology of Parkinson’s disease
Tysnes, O., & Storstein, A. M. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1686-y · Cited by 2,437 · see citing works
Parkinson's disease
Lees, A. J., Hardy, J., & Revesz, T. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60492-x · Cited by 1,956 · see citing works
Microglia in neurodegenerative disease
Perry, V. H., Nicoll, J. A. R., & Holmes, C. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.17 · Cited by 1,543 · see citing works
The clinical symptoms of Parkinson's disease.
Sveinbjornsdottir, S. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13691 · Cited by 1,410 · see citing works
Parkinson Disease in Twins
Tanner, C. M., Ottman, R., Goldman, S. M., Ellenberg, J., Chan, P., Mayeux, R. P., & Langston, J. W. (1999) · JAMA · doi:10.1001/jama.281.4.341 · Cited by 869 · see citing works
A Nurr1/CoREST Pathway in Microglia and Astrocytes Protects Dopaminergic Neurons from Inflammation-Induced Death
Saijo, K., Winner, B., Carson, C. T., Collier, J. G., Boyer, L., Rosenfeld, M. G., Gage, F. H., & Glass, C. K. (2009) · Cell · doi:10.1016/j.cell.2009.01.038 · Cited by 859 · see citing works
Analyses of the cag pathogenicity island of Helicobacter pylori
Akopyants, N. S., Clifton, S. W., Kersulyte, D., Crabtree, J. E., Youree, B. E., Reece, C. A., Bukanov, N. O., Drazek, E. S., Roe, B. A., & Berg, D. E. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00770.x · Cited by 716 · 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
Inflammation as a causative factor in the aetiology of Parkinson's disease
Whitton, P. S. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707167 · Cited by 625 · 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
Association of circulating TNF-α and IL-6 with ageing and parkinsonism
Dobbs, R. J., Charlett, A., Purkiss, A. G., Dobbs, S. M., Weller, C., & Peterson, D. W. (1999) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1999.tb00721.x · Cited by 324 · see citing works
A study on the association between infectious burden and A lzheimer's disease
Bu, X., Yao, X., Jiao, S. ‐., Zeng, F., Liu, Y. ‐., Xiang, Y., Liang, C. ‐., Wang, Q. ‐., Wang, X., Cao, H., et al. (2014) · European Journal of Neurology · doi:10.1111/ene.12477 · Cited by 273 · see citing works
Bias in meta-analysis detected by a simple, graphical test. Increase in studies of publication bias coincided with increasing use of meta-analysis.
Song, F., & Gilbody, S. M. (1998) · PubMed · Cited by 238 · see citing works
Inflammation and α-Synuclein’s Prion-like Behavior in Parkinson's Disease—Is There a Link?
Tomé, C. M. L., Tyson, T., Rey, N. L., Grathwohl, S. A., Britschgi, M., & Brundin, P. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8267-8 · Cited by 237 · see citing works
Helicobacter pylori eradication and l-dopa absorption in patients with PD and motor fluctuations
Pierantozzi, M., Pietroiusti, A., Brusa, L., Galati, S., Stefani, A., Lunardi, G., Fedele, E., Sancesario, G., Bernardi, G., Bergamaschi, A., et al. (2006) · Neurology · doi:10.1212/01.wnl.0000221672.01272.ba · Cited by 199 · see citing works
PREDISPOSITION TO FAMILIAL OSTEOARTHROSIS LINKED TO TYPE II COLLAGEN GENE
Palotie, A. V., Ott, J., Elima, K., et al. (1989) · The Lancet · doi:10.1016/s0140-6736(89)92507-5 · Cited by 184 · see citing works
Treatment for Helicobacter pylori infection and risk of parkinson’s disease in Denmark
Nielsen, H. H., Qiu, J., Friis, S., Wermuth, L., & Ritz, B. (2012) · European Journal of Neurology · doi:10.1111/j.1468-1331.2011.03643.x · Cited by 155 · see citing works
The association between infectious burden and Parkinson's disease: A case-control study.
Bu, X.-L., Wang, X., Xiang, Y., Shen, L.-L., Wang, Q.-H., Liu, Y.-H., Jiao, S.-S., Wang, Y.-R., Cao, H.-Y., Yi, X., et al. (2015) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2015.05.015 · Cited by 153 · see citing works
Molecular mimicry between Helicobacter pylori and the host
Appelmelk, B. J., Negrini, R., Moran, A. P., et al. (1997) · Trends in Microbiology · doi:10.1016/s0966-842x(96)10084-6 · Cited by 144 · see citing works
Eradication of Helicobacter pylori Infection Improves Levodopa Action, Clinical Symptoms and Quality of Life in Patients with Parkinson's Disease
Hashim, H., Azmin, S., Razlan, H., Yahya, N. W., Tan, H. J., Manaf, M. R. A., & Ibrahim, N. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112330 · Cited by 136 · 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
Molecular mimicry between Helicobacter pylori and the host
Appelmelk, B. J., Straver, S., Verboom, T., et al. (1998) · Springer eBooks · doi:10.1007/978-94-011-4882-5_5 · Cited by 126 · see citing works
DOPAMINE DISORDER IN DUODENAL ULCERATION
Szabó, S. (1979) · The Lancet · doi:10.1016/s0140-6736(79)92690-4 · Cited by 118 · see citing works
Helicobacter pyloriand neurological diseases: Married by the laws of inflammation
Álvarez‐Arellano, L. (2014) · World Journal of Gastrointestinal Pathophysiology · doi:10.4291/wjgp.v5.i4.400 · Cited by 111 · see citing works
Helicobacter pylori infection and motor fluctuations in patients with Parkinson's disease
Lee, W. Y., Yoon, W. T., Shin, H. Y., Jeon, S. H., & Rhee, P. (2008) · Movement Disorders · doi:10.1002/mds.22190 · Cited by 110 · see citing works
THE ASSOCIATION OF GASTRO‐DUODENAL ULCERATION AND PARKINSON'S DISEASE
Strang, R. R. (1965) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.1965.tb72277.x · Cited by 95 · 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
Parkinsonism: siblings share Helicobacter pylori seropositivity and facets of syndrome
Charlett, A., Dobbs, R. J., Dobbs, S. M., Weller, C., Brady, P., & Peterson, D. W. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1999.tb00654.x · Cited by 82 · see citing works
Parallel manifestations of neuropathologies in the enteric and central nervous systems
Natale, G., Pasquali, L., Paparelli, A., & Fornai, F. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01794.x · Cited by 69 · see citing works
Significantly higher frequency of H elicobacter suis in patients with idiopathic parkinsonism than in control patients
Blaecher, C., Smet, A., Flahou, B., et al. (2013) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12520 · Cited by 62 · see citing works
Link between Helicobacter pylori infection and idiopathic parkinsonism
Dobbs, S. M., Dobbs, R. J., Weller, C., & Charlett, A. (2000) · Medical Hypotheses · doi:10.1054/mehy.2000.1110 · Cited by 61 · see citing works
The relationship between Helicobacter pylori infection and Alzheimer’s disease in Japan
Shiota, S., Murakami, K., Yoshiiwa, A., Yamamoto, K., Ohno, S., Kuroda, A., Mizukami, K., Hanada, K., Okimoto, T., Kodama, M., et al. (2011) · Journal of Neurology · doi:10.1007/s00415-011-5957-5 · Cited by 61 · see citing works
Role of Chronic Infection and Inflammation in the Gastrointestinal Tract in the Etiology and Pathogenesis of Idiopathic Parkinsonism
Weller, C., Charlett, A., Oxlade, N. L., et al. (2005) · Helicobacter · doi:10.1111/j.1523-5378.2005.00329.x · Cited by 60 · see citing works
Small Intestinal Bacterial Overgrowth in Gastroparesis: Are There Any Predictors?
Reddymasu, S. C., & McCallum, R. W. (2010) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e3181aec746 · Cited by 56 · see citing works
Diagnostic values of Helicobacter pylori diagnostic tests: stool antigen test, urea breath test, rapid urease test, serology and histology.
Kazemi, S., Tavakkoli, H., Habizadeh, M. R., et al. (2011) · PubMed · Cited by 56 · see citing works
Genetics, drugs and environmental factors in Parkinson's disease: a case-control study
Werneck, A. L. D. S., & Alvarenga, H. (1999) · Arquivos de Neuro-Psiquiatria · doi:10.1590/s0004-282x1999000300001 · Cited by 49 · see citing works
Parkinsonism: differential age‐trend in Helicobacter pylori antibody
Dobbs, S. M., Charlett, Dobbs, S. M., Weller, & Peterson, P. (2000) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2000.00815.x · Cited by 47 · see citing works
Cobalamin, Folate, Methylmalonic Acid, Homocysteine, and Gastritis Markers in Dementia
Nägga, K., Rajani, R., Mårdh, E., Borch, K., Mårdh, S., & Marcusson, J. O. (2003) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000072812 · Cited by 40 · see citing works
Helicobacter pylori infection and Parkinson’s disease: apoptosis as an underlying common contributor
Kountouras, J., Zavos, C., Pοlyzos, S. A., et al. (2012) · European Journal of Neurology · doi:10.1111/j.1468-1331.2012.03695.x · Cited by 39 · see citing works
Helicobacter pylori infection, dementia and primary open-angle glaucoma: are they connected?
Tsolaki-Tagaraki, F., Kountouras, J., Topouzis, F., & Tsolaki, M. (2015) · BMC Ophthalmology · doi:10.1186/s12886-015-0006-2 · Cited by 38 · see citing works
Helicobacter pylori may be involved in cognitive impairment and dementia development through induction of atrophic gastritis, vitamin B-12–folate deficiency, and hyperhomocysteinemia sequence
Kountouras, J., Gavalas, E., Boziki, M. K., et al. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.3.805 · Cited by 33 · see citing works
Dopamine and gastroprotection
Glavin, G. B. (1991) · Digestive Diseases and Sciences · doi:10.1007/bf01296607 · Cited by 32 · see citing works
Experimental basis for a role for sulfhydryls and dopamine in ulcerogenesis: a primer for cytoprotection--organoprotection.
Szabo, S. (1986) · PubMed · Cited by 30 · see citing works
Non-motor Parkinsonism
Pfeiffer, R. F. (2007) · Parkinsonism & Related Disorders · doi:10.1016/s1353-8020(08)70004-x · Cited by 29 · see citing works
Blood profile holds clues to role of infection in a premonitory state for idiopathic parkinsonism and of gastrointestinal infection in established disease
Charlett, A., Dobbs, R. J., Dobbs, S. M., Weller, C., Ibrahim, M. A. A., Dew, T. K., Sherwood, R. A., Oxlade, N. L., Plant, J., Bowthorpe, J., et al. (2009) · Gut Pathogens · doi:10.1186/1757-4749-1-20 · Cited by 29 · see citing works
MPTP-LIKE MOLECULES AND PARKINSON'S DISEASE
Fellman, J. H., & Nutt, J. N. (1985) · The Lancet · doi:10.1016/s0140-6736(85)91692-7 · Cited by 18 · see citing works
Immunocytochemical characterization of rat brainstem neurons with vagal afferent input from the stomach challenged by acid or ammonia
Danzer, M., Samberger, C., Schicho, R., et al. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03109.x · Cited by 17 · see citing works
Helicobacter pylori eradication and l-dopa absorption in patients with PD and motor fluctuations
Fiddian-Green, R. G. (2007) · Neurology · doi:10.1212/01.wnl.0000260440.07107.99 · Cited by 17 · see citing works
Prevalence of Helicobacter pylori Infection in Samples of Gastric Biopsies
Trindade, L. M. D. F., Menezes, L. B. D. O., Neta, A., et al. (2017) · Gastroenterology Research · doi:10.14740/gr785w · Cited by 14 · see citing works
Protective effect of vagotomy suggests source organ for P arkinson disease
Gray, M. T., Muñoz, D. G., Schlossmacher, M. G., Gray, D. A., & Woulfe, J. (2015) · Annals of Neurology · doi:10.1002/ana.24501 · Cited by 12 · see citing works
Syndrome de Munchausen par procuration, Niveau de responsabilité maternelle et prise en charge
Berthier, M., & Oriot, D. (1996) · Archives de Pédiatrie · doi:10.1016/0929-693x(96)81735-0 · Cited by 3 · see citing works

Flagged first, then by citations

Sorted by citations

Microbiota-Brain-Gut Axis and Neurodegenerative Diseases
Quigley, E. M. M. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0802-6 · Cited by 804 · see citing works
The endotoxin hypothesis of neurodegeneration
Brown, G. C. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1564-7 · Cited by 457 · see citing works
Microbiota-Gut-Brain Axis: New Therapeutic Opportunities
Long-Smith, C., O'Riordan, K. J., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2020) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010919-023628 · Cited by 419 · see citing works
The Association Between the Gut Microbiota and Parkinson’s Disease, a Meta-Analysis
Shen, T., Yue, Y., He, T., Huang, C., Qu, B., Lv, W., & Lai, H.-Y. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.636545 · Cited by 219 · see citing works
Potential roles of gut microbiota and microbial metabolites in Parkinson’s disease
Zheng, S.-Y., Li, H.-X., Xu, R.-C., Miao, W.-T., Dai, M.-Y., Ding, S.-T., & Liu, H.-D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101347 · Cited by 101 · see citing works
The gut-brain axis and Parkinson disease: Clinical and pathogenetic relevance
Menozzi, E., Macnaughtan, J., & Schapira, A. H. V. (2021) · Annals of Medicine · doi:10.1080/07853890.2021.1890330 · Cited by 81 · 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

In an empirical evaluation of the funnel plot, researchers could not visually identify publication bias
Terrin, N. C., Schmid, C. H., & Lau, J. (2005) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2005.01.006 · Cited by 493 · see citing works
Meta-Analyses with Binary Outcomes: How Many Studies Need to be Omitted to Detect a Publication Bias?
Saveleva, E., & Selinski, S. (2008) · Journal of Toxicology and Environmental Health · doi:10.1080/15287390801985844 · Cited by 10 · see citing works
In response
Frass, M., Schuster, E., Muchitsch, I., et al. (2005) · EXPLORE · doi:10.1016/j.explore.2005.10.003 · Cited by 1 · see citing works
The Perils of Misinterpreting and Misusing “Publication Bias” in Meta-analyses: An Education Review on Funnel Plot-Based Methods
Afonso, J., Ramirez-Campillo, R., Clemente, F., Büttner, F., & Andrade, R. (2023) · Sports Medicine · doi:10.1007/s40279-023-01927-9 · Cited by 193 · see citing works
Helicobacter pylori infection and pancreatic cancer risk: A meta-analysis
Wu, J., Guo, Y., & Liu, W. (2016) · Journal of Cancer Research and Therapeutics · doi:10.4103/0973-1482.200744 · Cited by 61 · see citing works

Authors: Shen, X., Yang, H., Wu, Y., Zhang, D., & Jiang, H.
Affiliations: Qingdao University (CN)
Sichuan University (CN)
Corresponding author: Shen, Xiaoli
ORCID: Shen, Xiaoli
Yang, Huazhen
Wu, Yili
Zhang, Dongfeng
Jiang, Hong
Venue: Helicobacter
Publisher: Wiley
Published: 2017-06-09
Volume: 22
Issue: 5
ISSN: 1083-4389 (ISSN-L)
1523-5378
DOI: 10.1111/hel.12398
OpenAlex: W2975368988
Semantic Scholar: 4fd382c8a22b6d25057b78092be7c45350c0fd8e
Cited by: 114
References: 52
Citations by year: 2026: 9 · 2025: 10 · 2024: 14 · 2023: 11 · 2022: 16 · 2021: 22 · 2020: 16 · 2019: 7 · 2018: 6 · 2017: 3
FWCI: 1.86
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Helicobacter (publishedVersion)
PubMed (publishedVersion)
Funders: Natural Science Foundation of Shandong Province, China (ZR2016HM11)
Project Funded by China Postdoctoral Science Foundation, China (2016M592145)
Topics: Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords: Helicobacter pylori infection, Parkinson's disease, neurodegenerative disease risk, case-control study, cross-sectional study
MeSH terms: Asia, Cross-Sectional Studies, Europe, Humans, Parkinson Disease, Helicobacter Infections, Risk Assessment

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

Meta‐analysis: Association of Helicobacter pylori infection with Parkinson's diseases

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks