Association between Helicobacter pylori infection and Parkinson's disease: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

XIAO Huixia ¹ , YE Hui ^2,3 , HUANG Qiuyue ^2,3 , JIA Xiaofen ^2,3 , DENG Xin ¹ , ZHANG Chen ⁴ , LUO Ruixiang ⁵ , YE Suman ¹ , LI Chengcheng ¹ ,  ZHANG Xuezhi ^2,3

1. Dongzhimen Hospital, Beijing University of Chinese Medicine, Beijing 100700, P.R.China;
2. Peking University First Hospital, Beijing 100034, P.R.China;
3. Peking University Institute of Integrated Traditional Chinese and Western Medicine, Beijing 100034, P.R.China;
4. The Third Affiliated Hospital of Beijing University of Chinese Medicine, Beijing 100029, P.R.China;
5. Dongfang Hospital, Beijing University of Chinese Medicine, Beijing 100078, P.R.China;

Corresponding author：

ZHANG Xuezhi, Email: zhang.xuezhi@263.net

Keywords：

Helicobacter pylori infection; Parkinson's disease; Meta-analysis; Systematic review; Case-control study

DOI：

10.7507/1672-2531.202109102

Video：

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Objective To systematically review the association between Helicobacter pylori (HP) infection and Parkinson's disease (PD). Methods PubMed, EMbase, The Cochrane Library, CNKI, VIP and WanFang Data databases were electronically searched to collect case-control studies on the association between HP and PD from January 2000 to July 2021. Two reviewers independently screened literature, extracted data, and assessed the risk of bias of included studies. Meta-analysis was then performed using RevMan 5.3 software. Results A total of 16 case-control studies involving 2 790 subjects were included. The results of meta-analysis showed that the HP infection rate was higher in PD patients than that in healthy patients (OR=1.87, 95%CI 1.38 to 2.54, P<0.000 1). The results of subgroup analysis showed that the infection rate of HP in PD group in Asia and Africa region was significantly higher than that in control group, but not in Europe region. Breath tests and other detection methods were used to detect HP infection, and the HP infection rate in PD group was significantly higher than that in the healthy control group. However, there was no significant difference in HP infection between the two groups by ELISA. UPDRS Ⅲ score of PD patients with HP infection was significantly higher than that of PD patients without HP infection. Conclusions Current evidence shows that PD patients have a higher HP infection rate than the normal population, and the rates are affected by regions and HP detection methods. In addition, HP infection can aggravate the motor symptoms and motor complications of PD patients. Due to limited quality and quantity of included studies, more high-quality studies are required to verify the above conclusions.

Citation： XIAO Huixia, YE Hui, HUANG Qiuyue, JIA Xiaofen, DENG Xin, ZHANG Chen, LUO Ruixiang, YE Suman, LI Chengcheng, ZHANG Xuezhi. Association between Helicobacter pylori infection and Parkinson's disease: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2021, 21(12): 1391-1397. doi: 10.7507/1672-2531.202109102 Copy

1.	Spatola M, Wider C. Genetics of Parkinson's disease: the yield. Parkinsonism Relat Disord, 2014, 20(Suppl 1): S35-38.
2.	Keshavarzian A, Green SJ, Engen PA, et al. Colonic bacterial composition in Parkinson's disease. Mov Disord, 2015, 30(10): 1351-1360.
3.	Khan AU, Akram M, Daniyal M, et al. Awareness and current knowledge of Parkinson's disease: a neurodegenerative disorder. Int J Neurosci, 2019, 129(1): 55-93.
4.	Qi S, Yin P, Wang L, et al. Prevalence of Parkinson’s disease: a community-based study in China. Mov Disord, 2021, online ahead of print.
5.	Davis RA, Epstein CH, Klepitskaya O, et al. Disambiguating the psychiatric sequelae of Parkinson’s disease, deep brain stimulation, and life events: case report and literature review. Am J Psychiatry, 2017, 174(1): 11-15.
6.	Martinez-Martin P. What is quality of life and how do we measure it. Relevance to Parkinson's disease and movement disorders. Mov Disord, 2017, 32(3): 382-392.
7.	La Cognata V, Morello G, D'Agata V, et al. Copy number variability in Parkinson's disease: assembling the puzzle through a systems biology approach. Hum Genet, 2017, 136(1): 13-37.
8.	Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther, 2018, 47(7): 868-876.
9.	Xia Y, Meng G, Zhang Q, et al. Dietary patterns are associated with helicobacter pylori infection in chinese adults: a cross-sectional study. Sci Rep, 2016, 6: 32334.
10.	Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med, 2002, 347(15): 1175-1186.
11.	Pellicano R, Ianiro G, Fagoonee S, et al. Review: Extragastric diseases and Helicobacter pylori. Helicobacter, 2020, 25(Suppl 1): e12741.
12.	Pierantozzi M, Pietroiusti A, Brusa L, et al. Helicobacter pylori eradication and l-dopa absorption in patients with PD and motor fluctuations. Neurology, 2006, 66(12): 1824-1829.
13.	Lee WY, Yoon WT, Shin HY, et al. Helicobacter pylori infection and motor fluctuations in patients with Parkinson's disease. Mov Disord, 2008, 23(12): 1696-1700.
14.	Nafisah WY, Najman Achok H, Hamizah R, et al. High prevalence of Helicobacter pylori infection in Malaysian Parkinson's disease patients. J Park Restless Legs Syndr, 2013, 3: 63-67.
15.	Hashim H, Azmin S, Razlan H, et al. Eradication of Helicobacter pylori infection improves levodopa action, clinical symptoms and quality of life in patients with Parkinson's disease. PLoS One, 2014, 9(11): e112330.
16.	Çamcı G, Oğuz S. Association between Parkinson's disease and Helicobacter pylori. J Clin Neurol, 2016, 12(2): 147-150.
17.	Alvarez-Arellano L, Maldonado-Bernal C. Helicobacter pylori and neurological diseases: Married by the laws of inflammation. World J Gastrointest Pathophysiol, 2014, 5(4): 400-404.
18.	Kato M, Ota H, Okuda M, et al. Guidelines for the management of Helicobacter pylori infection in Japan: 2016 Revised Edition. Helicobacter, 2019, 24(4): e12597.
19.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
20.	Dobbs RJ, Charlett A, Dobbs SM, et al. Parkinsonism: differential age-trend in Helicobacter pylori antibody. Aliment Pharmacol Ther, 2000, 14(9): 1199-1205.
21.	Blaecher C, Smet A, Flahou B, et al. Significantly higher frequency of Helicobacter suis in patients with idiopathic parkinsonism than in control patients. Aliment Pharmacol Ther, 2013, 38(11-12): 1347-1353.
22.	Fasano A, Bove F, Gabrielli M, et al. The role of small intestinal bacterial overgrowth in Parkinson's disease. Mov Disord, 2013, 28(9): 1241-1249.
23.	Bu XL, Wang X, Xiang Y, et al. The association between infectious burden and Parkinson's disease: A case-control study. Parkinsonism Relat Disord, 2015, 21(8): 877-881.
24.	Efthymiou G, Dardiotis E, Liaskos C, et al. Immune responses against Helicobacter pylori-specific antigens differentiate relapsing remitting from secondary progressive multiple sclerosis. Sci Rep, 2017, 7(1): 7929.
25.	陈静. 幽门螺杆菌感染与帕金森病关系研究. 郑州: 郑州大学, 2020.
26.	李燃. 幽门螺旋杆菌、还原型谷胱甘肽, 尿酸与帕金森病相关性研究. 石家庄: 河北北方学院, 2018.
27.	罗晨, 肖波, 刘人恺, 等. 幽门螺旋杆菌感染对帕金森病患者血清氧化应激状态及血小板线粒体功能的影响. 中国神经免疫学和神经病学杂志, 2008, (5): 342-345,348.
28.	应小卫, 李灵晓, 汪立松, 等. 幽门螺旋杆菌感染对帕金森病患者运动症状及氧化应激状态的影响. 中华医院感染学杂志, 2018, 28(12): 1823-1826.
29.	辛华. 幽门螺旋杆菌与帕金森病患者运动症状严重程度的相关性研究. 青岛: 青岛大学, 2019.
30.	Mashaly M, Saudy N, Belal T, et al. Helicobacter pylori cytotoxin-associated gene A genotype in Egyptian patients with Parkinson’s disease: could eradication benefit. Comp Clin Path, 2017, 26(4): 893-900.
31.	范崇桂, 付国惠, 闪海霞. 帕金森病患者幽门螺杆菌感染对血清氧化应激状态及血小板线粒体功能的影响. 中华医院感染学杂志, 2014, 24(23): 5783-5785.
32.	苏晓敏, 蔡鸣, 刘晓春, 等. 幽门螺杆菌感染、同型半胱氨酸与帕金森病的相关性研究. 中国实用医药, 2019, 14(13): 50-52.
33.	Esmael A, El-Sherif M, Shabana HR, et al. Helicobacter pylori infection in Egyptians with Parkinson’s disease: Incidence and the effect on motor fluctuation and response to levodopa. Egypt. J. Neurol. Psychiatry Neurosurg, 2016, 53(2): 84-88.
34.	Roshan TB, Bihani A, Seyed RH, et al. The Association between Helicobacter Pylori Infection and Parkinson’s disease: a case-control study. J Clin Diagn Res, 2018, 12: 5-8.
35.	种红, 苏闻, 李淑华, 等. 中老年人帕金森病与幽门螺杆菌感染的相关性研究. 中华老年医学杂志, 2015, 34(11): 1223-1226.
36.	Smeyne RJ, Noyce AJ, Byrne M, et al. Infection and risk of Parkinson’s disease. J Parkinsons Dis, 2021, 11(1): 31-43.
37.	Nielsen HH, Qiu J, Friis S, et al. Treatment for Helicobacter pylori infection and risk of Parkinson's disease in Denmark. Eur J Neurol, 2012, 19(6): 864-869.
38.	Dobbs SM, Dobbs RJ, Weller C, et al. Link between Helicobacter pylori infection and idiopathic parkinsonism. Med Hypotheses, 2000, 55(2): 93-98.
39.	Kountouras J, Zavos C, Polyzos SA, et al. Helicobacter pylori infection and Parkinson's disease: apoptosis as an underlying common contributor. Eur J Neurol, 2012, 19(6): e56.
40.	Fernández-Espejo E. Microorganisms that are related with increased risk for Parkinson's disease. Neurologia (Engl Ed), 2020, online ahead of print.
41.	Shen X, Yang H, Wu Y, et al. Meta-analysis: Association of Helicobacter pylori infection with Parkinson's diseases. Helicobacter, 2017, 22(5): 10.
42.	李亚骐, 田锦勇, 瞿祥, 等. 幽门螺杆菌感染对帕金森患者运动能力及氧化应激的影响. 中华医院感染学杂志, 2020, 30(13): 2005-2008.
43.	王少颖, 王莉迪, 曹玉娇, 等. 根除幽门螺杆菌对帕金森病患者UPDRS评分和非运动症状的影响. 河北医药, 2021, 43(14): 2157-2160.
44.	曹羽. 青海地区幽门螺杆菌感染对帕金森病影响的研究. 西宁: 青海大学, 2020.
45.	刘欣, 刘娜, 娄凡, 等. 幽门螺杆菌感染对帕金森病临床症状的影响. 卒中与神经疾病, 2018, 25(2): 206-209.
46.	Goetz CG, Tilley BC, Shaftman SR, et al. Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord, 2008, 23(15): 2129-2170.
47.	王少颖, 王莉迪, 曹玉娇, 等. 幽门螺杆菌感染对帕金森病患者运动症状、便秘评分和生活质量的影响. 医学综述, 2021, 27(18): 3717-3721.
48.	Nyholm D, Hellström PM. Effects of Helicobacter pylori on levodopa pharmacokinetics. J Parkinsons Dis, 2021, 11(1): 61-69.

1. Spatola M, Wider C. Genetics of Parkinson's disease: the yield. Parkinsonism Relat Disord, 2014, 20(Suppl 1): S35-38.
2. Keshavarzian A, Green SJ, Engen PA, et al. Colonic bacterial composition in Parkinson's disease. Mov Disord, 2015, 30(10): 1351-1360.
3. Khan AU, Akram M, Daniyal M, et al. Awareness and current knowledge of Parkinson's disease: a neurodegenerative disorder. Int J Neurosci, 2019, 129(1): 55-93.
4. Qi S, Yin P, Wang L, et al. Prevalence of Parkinson’s disease: a community-based study in China. Mov Disord, 2021, online ahead of print.
5. Davis RA, Epstein CH, Klepitskaya O, et al. Disambiguating the psychiatric sequelae of Parkinson’s disease, deep brain stimulation, and life events: case report and literature review. Am J Psychiatry, 2017, 174(1): 11-15.
6. Martinez-Martin P. What is quality of life and how do we measure it. Relevance to Parkinson's disease and movement disorders. Mov Disord, 2017, 32(3): 382-392.
7. La Cognata V, Morello G, D'Agata V, et al. Copy number variability in Parkinson's disease: assembling the puzzle through a systems biology approach. Hum Genet, 2017, 136(1): 13-37.
8. Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther, 2018, 47(7): 868-876.
9. Xia Y, Meng G, Zhang Q, et al. Dietary patterns are associated with helicobacter pylori infection in chinese adults: a cross-sectional study. Sci Rep, 2016, 6: 32334.
10. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med, 2002, 347(15): 1175-1186.
11. Pellicano R, Ianiro G, Fagoonee S, et al. Review: Extragastric diseases and Helicobacter pylori. Helicobacter, 2020, 25(Suppl 1): e12741.
12. Pierantozzi M, Pietroiusti A, Brusa L, et al. Helicobacter pylori eradication and l-dopa absorption in patients with PD and motor fluctuations. Neurology, 2006, 66(12): 1824-1829.
13. Lee WY, Yoon WT, Shin HY, et al. Helicobacter pylori infection and motor fluctuations in patients with Parkinson's disease. Mov Disord, 2008, 23(12): 1696-1700.
14. Nafisah WY, Najman Achok H, Hamizah R, et al. High prevalence of Helicobacter pylori infection in Malaysian Parkinson's disease patients. J Park Restless Legs Syndr, 2013, 3: 63-67.
15. Hashim H, Azmin S, Razlan H, et al. Eradication of Helicobacter pylori infection improves levodopa action, clinical symptoms and quality of life in patients with Parkinson's disease. PLoS One, 2014, 9(11): e112330.
16. Çamcı G, Oğuz S. Association between Parkinson's disease and Helicobacter pylori. J Clin Neurol, 2016, 12(2): 147-150.
17. Alvarez-Arellano L, Maldonado-Bernal C. Helicobacter pylori and neurological diseases: Married by the laws of inflammation. World J Gastrointest Pathophysiol, 2014, 5(4): 400-404.
18. Kato M, Ota H, Okuda M, et al. Guidelines for the management of Helicobacter pylori infection in Japan: 2016 Revised Edition. Helicobacter, 2019, 24(4): e12597.
19. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
20. Dobbs RJ, Charlett A, Dobbs SM, et al. Parkinsonism: differential age-trend in Helicobacter pylori antibody. Aliment Pharmacol Ther, 2000, 14(9): 1199-1205.
21. Blaecher C, Smet A, Flahou B, et al. Significantly higher frequency of Helicobacter suis in patients with idiopathic parkinsonism than in control patients. Aliment Pharmacol Ther, 2013, 38(11-12): 1347-1353.
22. Fasano A, Bove F, Gabrielli M, et al. The role of small intestinal bacterial overgrowth in Parkinson's disease. Mov Disord, 2013, 28(9): 1241-1249.
23. Bu XL, Wang X, Xiang Y, et al. The association between infectious burden and Parkinson's disease: A case-control study. Parkinsonism Relat Disord, 2015, 21(8): 877-881.
24. Efthymiou G, Dardiotis E, Liaskos C, et al. Immune responses against Helicobacter pylori-specific antigens differentiate relapsing remitting from secondary progressive multiple sclerosis. Sci Rep, 2017, 7(1): 7929.
25. 陈静. 幽门螺杆菌感染与帕金森病关系研究. 郑州: 郑州大学, 2020.
26. 李燃. 幽门螺旋杆菌、还原型谷胱甘肽, 尿酸与帕金森病相关性研究. 石家庄: 河北北方学院, 2018.
27. 罗晨, 肖波, 刘人恺, 等. 幽门螺旋杆菌感染对帕金森病患者血清氧化应激状态及血小板线粒体功能的影响. 中国神经免疫学和神经病学杂志, 2008, (5): 342-345,348.
28. 应小卫, 李灵晓, 汪立松, 等. 幽门螺旋杆菌感染对帕金森病患者运动症状及氧化应激状态的影响. 中华医院感染学杂志, 2018, 28(12): 1823-1826.
29. 辛华. 幽门螺旋杆菌与帕金森病患者运动症状严重程度的相关性研究. 青岛: 青岛大学, 2019.
30. Mashaly M, Saudy N, Belal T, et al. Helicobacter pylori cytotoxin-associated gene A genotype in Egyptian patients with Parkinson’s disease: could eradication benefit. Comp Clin Path, 2017, 26(4): 893-900.
31. 范崇桂, 付国惠, 闪海霞. 帕金森病患者幽门螺杆菌感染对血清氧化应激状态及血小板线粒体功能的影响. 中华医院感染学杂志, 2014, 24(23): 5783-5785.
32. 苏晓敏, 蔡鸣, 刘晓春, 等. 幽门螺杆菌感染、同型半胱氨酸与帕金森病的相关性研究. 中国实用医药, 2019, 14(13): 50-52.
33. Esmael A, El-Sherif M, Shabana HR, et al. Helicobacter pylori infection in Egyptians with Parkinson’s disease: Incidence and the effect on motor fluctuation and response to levodopa. Egypt. J. Neurol. Psychiatry Neurosurg, 2016, 53(2): 84-88.
34. Roshan TB, Bihani A, Seyed RH, et al. The Association between Helicobacter Pylori Infection and Parkinson’s disease: a case-control study. J Clin Diagn Res, 2018, 12: 5-8.
35. 种红, 苏闻, 李淑华, 等. 中老年人帕金森病与幽门螺杆菌感染的相关性研究. 中华老年医学杂志, 2015, 34(11): 1223-1226.
36. Smeyne RJ, Noyce AJ, Byrne M, et al. Infection and risk of Parkinson’s disease. J Parkinsons Dis, 2021, 11(1): 31-43.
37. Nielsen HH, Qiu J, Friis S, et al. Treatment for Helicobacter pylori infection and risk of Parkinson's disease in Denmark. Eur J Neurol, 2012, 19(6): 864-869.
38. Dobbs SM, Dobbs RJ, Weller C, et al. Link between Helicobacter pylori infection and idiopathic parkinsonism. Med Hypotheses, 2000, 55(2): 93-98.
39. Kountouras J, Zavos C, Polyzos SA, et al. Helicobacter pylori infection and Parkinson's disease: apoptosis as an underlying common contributor. Eur J Neurol, 2012, 19(6): e56.
40. Fernández-Espejo E. Microorganisms that are related with increased risk for Parkinson's disease. Neurologia (Engl Ed), 2020, online ahead of print.
41. Shen X, Yang H, Wu Y, et al. Meta-analysis: Association of Helicobacter pylori infection with Parkinson's diseases. Helicobacter, 2017, 22(5): 10.
42. 李亚骐, 田锦勇, 瞿祥, 等. 幽门螺杆菌感染对帕金森患者运动能力及氧化应激的影响. 中华医院感染学杂志, 2020, 30(13): 2005-2008.
43. 王少颖, 王莉迪, 曹玉娇, 等. 根除幽门螺杆菌对帕金森病患者UPDRS评分和非运动症状的影响. 河北医药, 2021, 43(14): 2157-2160.
44. 曹羽. 青海地区幽门螺杆菌感染对帕金森病影响的研究. 西宁: 青海大学, 2020.
45. 刘欣, 刘娜, 娄凡, 等. 幽门螺杆菌感染对帕金森病临床症状的影响. 卒中与神经疾病, 2018, 25(2): 206-209.
46. Goetz CG, Tilley BC, Shaftman SR, et al. Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord, 2008, 23(15): 2129-2170.
47. 王少颖, 王莉迪, 曹玉娇, 等. 幽门螺杆菌感染对帕金森病患者运动症状、便秘评分和生活质量的影响. 医学综述, 2021, 27(18): 3717-3721.
48. Nyholm D, Hellström PM. Effects of Helicobacter pylori on levodopa pharmacokinetics. J Parkinsons Dis, 2021, 11(1): 61-69.

Chinese Journal of Evidence-Based Medicine

Association between Helicobacter pylori infection and Parkinson's disease: a meta-analysis

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