Вплив інфекції Helicobacter pylori на компоненти метаболічного синдрому. Огляд літератури

О. Є. Гріднєв; С. В. Гріднєва

doi:10.30978/UTJ2024-1-77

Автор(и)

О. Є. Гріднєв ДУ «Національний інститут терапії імені Л. Т. Малої НАМН України», Харків, Україна https://orcid.org/0000-0003-4716-3520
С. В. Гріднєва ДУ «Національний інститут терапії імені Л. Т. Малої НАМН України», Харків; Харківський національний університет імені В. Н. Каразіна, Україна http://orcid.org/0000-0002-7498-9574

DOI:

https://doi.org/10.30978/UTJ2024-1-77

Ключові слова:

метаболічний синдром, Helicobacter pylori, антигелікобактерна терапія, дисліпідемії, гіперглікемія

Анотація

Наголошено на здатності Helicobacter pylori впливати на метаболічні процеси. Розглянуто можливі механізми такого впливу. Наведено дані, що інфікування H. pylori підвищує частоту метаболічного синдрому та його компонентів. Зазначено, що системні хронічні запальні процеси (одна з основних ланок патогенезу метаболічно‑асоційованих захворювань) можуть ініціюватися H. pylori за рахунок «класичних» механізмів, притаманних метаболічним захворюванням: активації прозапальних цитокінів (фактора некрозу пухлини α, інтерлейкінів‑1, ‑6,) і адипоцитарних гормонів. Насамперед це зумовлено здатністю H. pylori продукувати цитотоксини (CagА/VacA) і наявністю ліпополісахариду в їхній клітинній стінці (ендотоксину), що може як безпосередньо, так і опосередковано індукувати прозапальну відповідь, зокрема системну. Доказом цього є дані про те, що ерадикація H. pylori запобігає повторному стенозу коронарних артерій після встановлення стенту, поліпшує перебіг артеріальної гіпертензії, сприяє значному зниженню концентрації С‑реактивного білка. Крім того, вплив H. pylori на прозапальні цитокіни й адипоцитарні гормони може спричинити формування аномального проатерогенного ліпідного профілю. Про це свідчать дані щодо зменшення концентрації загального холестерину, тригліцеридів, холестерину ліпопротеїнів низької густини на тлі збільшення вмісту холестерину ліпопротеїнів високої густини після успішної ерадикації H. pylori. Зазначено, що інфекція H. pylori є чинником, що спричиняє інсулінорезистентність та хронічну гіперглікемію. Це також переважно пов’язано зі здатністю H. pylori продукувати цитотоксини. Деякі дослідники не встановили зв’язку між H. pylori та рівнем глікозильованого гемоглобіну, що можна пояснити використанням серологічних методів діагностики гелікобактерій. Відмінності в результатах досліджень можуть бути пов’язані з методологічними помилками, тому необхідно провести додаткові дослідження в цьому напрямі, що сприятиме розробці профілактичних і лікувальних стратегій.

Біографії авторів

О. Є. Гріднєв, ДУ «Національний інститут терапії імені Л. Т. Малої НАМН України», Харків

MD, Doctor of Medical Science, Senior Researcher, Leading Researcher of the Department of Study of Digestive System Diseases and their Comorbidity with Non-Communicable Diseases

С. В. Гріднєва, ДУ «Національний інститут терапії імені Л. Т. Малої НАМН України», Харків; Харківський національний університет імені В. Н. Каразіна

к. мед. н., доцент, доцент кафедри загальної практики — сімейної медицини, лікар-гастроентеролог

Посилання

Abd-El-Kareem YH, Alkabeer AMM, Nuser MM, Mohammed AS, Saleh MW. Study of the relation between glycemic control in Egyptian patients with type-2 diabetes mellitus and helicobacter pylori infection. Int J Multidiscip Res Dev. 2018;5(4):249-56. https://typeset.io/papers/study-of-the-relation-between-glycemic-control-in-egyptian-2ly7il5or6.

Aladhami AK, Unger CA, Ennis SL, et al. Macrophage tumor necrosis factor-alpha deletion does not protect against obesity-associated metabolic dysfunction. FASEB J. 2021;35:e21665. http://doi.org/10.1096/fj.202100543RR.

Anastasios R, Goritsas C, Papamihail C, Trigidou R, Garzonis P, Ferti A. Helicobacter pylori infection in diabetic patients: prevalence and endoscopic Findings Eur J Int. Med. 2002;13:376. http://doi.org/10.1016/s0953-6205(02)00094-8.

Asaka M, Kimura T, Kudo M, Takeda H, Mitani S, Miyazaki T, Miki K, Graham DY. Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology. 1992 Mar;102(3):760-6. http://doi.org/10.1016/0016-5085(92)90156-s. PMID: 1537513.

Bajaj S, Rekwal L, Misra SP, Misra V, Yadav RK, Srivastava A. Association of helicobacter pylori infection with type 2 diabetes. Indian J Endocrinol Metab. 2014 Sep;18(5):694-9. http://doi.org/10.4103/2230-8210.139235. PMID: 25285288; PMCID: PMC4171894.

Boziki M, Grigoriadis N, Doulberis M, Papaefthymiou A, Polyzos SA, Kountouras J. Potential impact of Helicobacter pylori-related galectin-3 on chronic kidney, cardiovascular and brain disorders in decompensated cirrhosis. Dig Liver Dis. 2019;52:121-3. http://doi.org/10.1016/j.dld.2019.09.001.

Candelli M, Rigante D, Schiavino A, Gabrielli M, Crea F, Minguell Del Lungo L, Pignataro G, Sacco E, Monaco S, Gentiloni Silveri N, Gasbarrini A. High reinfection rate of Helicobacter pylori in young type 1 diabetic patients: a three-year follow-up study. Eur Rev Med Pharmacol Sci. 2012 Oct;16(11):1468-72. PMID: 23111958.

Chen Y, Blaser MJ. Association between gastric Helicobacter pylori colonization and glycated hemoglobin levels. J Infect Dis. 2012;205:1195-202. http://doi.org/10.1093/infdis/jis106.

Cheng KP, Yang YJ, Hung HC, Lin CH, Wu CT, Hung MH, Sheu BS, Ou HY. Helicobacter pylori eradication improves glycemic control in type 2 diabetes patients with asymptomatic active Helicobacter pylori infection. J Diabetes Investig. 2019 Jul;10(4):1092-1101. http://doi.org/10.1111/jdi.12991. Epub 2019 Jan 22. PMID: 30556347; PMCID: PMC6626959.

Cohen E, Levi A, Vecht-Lifshitz SE, Goldberg E, Garty M, Krause I. Assessment of a possible link between hyperhomocysteinemia and hyperuricemia. J Investig Med. 2015;63:534-8. http://doi.org/10.1097/JIM.0000000000000152.

Consolazio A, Borgia MC, Ferro D, Iacopini F, Paoluzi OA, Crispino P, Nardi F, Rivera M, Paoluzi P. Increased thrombin generation and circulating levels of tumour necrosis factor-alpha in patients with chronic Helicobacter pylori-positive gastritis. Aliment Pharmacol Ther. 2004 Aug 1;20(3):289-94. http://doi.org/10.1111/j.1365-2036.2004.02074.x. PMID: 15274665.

Coskun S, Kasirga E, Yilmaz O, Bayindir P, Akil I, Yuksel H, Polat M, Sanlidag T. Is Helicobacter pylori related to endothelial dysfunction during childhood? Pediatr Int. 2008 Apr;50(2):150-3. http://doi.org/10.1111/j.1442-200X.2008.02542.x. PMID: 18353048.

Dahl LK. Possible role of salt intake in the development of essential hypertension. Int J Epidemiol. 2005;34:967-72. http://doi.org/10.1093/ije/dyh317.

Demir M, Gokturk HS, Ozturk NA, Kulaksizoglu M, Serin E, Yilmaz U. Helicobacter pylori prevalence in diabetes mellitus patients with dyspeptic symptoms and its relationship to glycemic control and late complications. Dig Dis Sci. 2008;53:2646-9. http://doi.org/10.1007/s10620-007-0185-7.

Devrajani BR, Shah SZA, Soomro AA, Devrajani T. Type 2 diabetes mellitus: a risk factor for Helicobacter pylori infection: a hospital based case-control study. Int J Diabetes Dev Ctries. 2010;30(1):22-6.

Diomedi M, Stanzione P, Sallustio F, Leone G, Renna A, Misaggi G, Fontana C, Pasqualetti P, Pietroiusti A. Cytotoxin-associated Gene-A-positive Helicobacter pylori strains infection increases the risk of recurrent atherosclerotic stroke. Helicobacter. 2008 Dec;13(6):525-31. http://doi.org/10.1111/j.1523-5378.2008.00627.x. PMID: 19166418.

Doheim MF, Altaweel AA, Elgendy MG, Elshanbary AA, Dibas M, Ali AAHA, Dahy TM, Sharaf AK, Hassan AE. Association between Helicobacter Pylori infection and stroke: a meta-analysis of 273,135 patients. J Neurol. 2021 Sep;268(9):3238-3248. http://doi.org/10.1007/s00415-020-09933-x. Epub 2020 May 23. PMID: 32447554.

Dongiovanni P, Stender S, Pietrelli A, et al. Causal relationship of hepatic fat with liver damage and insulin resistance in nonalcoholic fatty liver. J Intern Med. 2017;283:356-70. http://doi.org/10.1111/joim.12719.

Dore MP, Bilotta M, Malaty HM, et al. Diabetes mellitus and Helicobacter pylori infection. Nutrition. 2000;16:407-10. http://doi.org/10.1016/s0899-9007(00)00267-7.

Doulberis M, Kotronis G, Gialamprinou D, Polyzos SA, Papaefthymiou A, Katsinelos P, Kountouras J. Alzheimer's disease and gastrointestinal microbiota; impact of Helicobacter pylori infection involvement. Int J Neurosci. 2021 Mar;131(3):289-301. http://doi.org/10.1080/00207454.2020.1738432. Epub 2020 Mar 13. PMID: 32125206.

Doulberis M, Papaefthymiou A, Polyzos SA, et al. Association between active Helicobacter pylori infection and glaucoma: a systematic review and meta-analysis. Microorganisms. 2020;8:894. http://doi.org/10.3390/microorganisms8060894.

Eshraghian A. The continuous story of Helicobacter pylori infection and insulin resistance: this time in Japan. Helicobacter. 2010 Apr;15(2):160; author reply 161. http://doi.org/10.1111/j.1523-5378.2009.00741.x. PMID: 20402819.

Fahed G, Aoun L, Bou Zerdan M, Allam S, Bou Zerdan M, Bouferraa Y, Assi HI. Metabolic Syndrome: Updates on Pathophysiology and Management in 2021. Int J Mol Sci. 2022 Jan 12;23(2):786. http://doi.org/10.3390/ijms23020786. PMID: 35054972; PMCID: PMC8775991.

Fernandini-Paredes GG, Mezones-Holguin E, Vargas-Gonzales R, Pozo-Briceño E, Rodriguez-Morales AJ. In patients with type 2 diabetes mellitus, are glycosylated hemoglobin levels higher for those with Helicobacter pylori infection than those without infection? Clin Infect Dis. 2008 Jul 1;47(1):144-6. http://doi.org/10.1086/588846. PMID: 18522510.

Ferrannini E, Buzzigoli G, Bonadonna R, Giorico MA, Oleggini M, Graziadei L, Pedrinelli R, Brandi L, Bevilacqua S. Insulin resistance in essential hypertension. N Engl J Med. 1987 Aug 6;317(6):350-7. http://doi.org/10.1056/NEJM198708063170605. PMID: 3299096.

Fox JG, Dangler CA, Taylor NS, King A, Koh TJ, Wang TC. High-salt diet induces gastric epithelial hyperplasia and parietal cell loss, and enhances Helicobacter pylori colonization in C57BL/6 mice. Cancer Res. 1999;59:4823-8.

Franceschi F, Sepulveda AR, Gasbarrini A, Pola P, Silveri NG, Gasbarrini G, Graham DY, Genta RM. Cross-reactivity of anti-CagA antibodies with vascular wall antigens: possible pathogenic link between Helicobacter pylori infection and atherosclerosis. Circulation. 2002 Jul 23;106(4):430-4. http://doi.org/10.1161/01.cir.0000024100.90140.19. PMID: 12135941.

Franceschi F, Gasbarrini A, Polyzos SA, Kountouras J. Extragastric diseases and Helicobacter pylori. Helicobacter. 2015;20:40-6. http://doi.org/10.1111/hel.12256.

Francois F, Roper J, Joseph N, Pei Z, Chhada A, Shak JR, de Perez AZ, Perez-Perez GI, Blaser MJ. The effect of H. pylori eradication on meal-associated changes in plasma ghrelin and leptin. BMC Gastroenterol. 2011 Apr 14;11:37. http://doi.org/10.1186/1471-230X-11-37. PMID: 21489301; PMCID: PMC3089783.

Gen R, Demir M, Ataseven H. Effect of Helicobacter pylori eradication on insulin resistance, serum lipids and low-grade inflammation. South Med J. 2010;103:190-6. doi: 10.1097/SMJ.0b013e3181cf373f.

Global Burden of Metabolic Risk Factors for Chronic Diseases Collaboration. Cardiovascular disease, chronic kidney disease, and diabetes mortality burden of cardiometabolic risk factors from 1980 to 2010: a comparative risk assessment. Lancet Diabetes Endocrinol. 2014 Aug;2(8):634-47. http://doi.org/10.1016/S2213-8587(14)70102-0. Epub 2014 May 16. PMID: 24842598; PMCID: PMC4572741.

Grebowska A, Rechciński T, Bak-Romaniszyn L, Czkwianianc E, Moran A, Druszczyńska M, Kowalewicz-Kulbat M, Owczarek A, Dziuba M, Krzemińska-Pakuła M, Płaneta-Małecka I, Rudnicka W, Chmiela M. Potential role of LPS in the outcome of Helicobacter pylori related diseases. Pol J Microbiol. 2006;55(1):25-30. PMID: 16878600.

Guirguis-Blake JM, Evans CV, Webber EM, Coppola EL, Perdue LA, Weyrich MS. Screening for hypertension in adults. JAMA. 2021;325:1657-69. http://doi.org/10.1001/jama.2020.21669.

Gulcelik NE, Kaya E, Demirbas B, Culha C, Koc G, Ozkaya M, Cakal E, Serter R, Aral Y. Helicobacter pylori prevalence in diabetic patients and its relationship with dyspepsia and autonomic neuropathy. J Endocrinol Invest. 2005 Mar;28(3):214-7. http://doi.org/10.1007/BF03345375. PMID: 15952404.

Gunji T, Matsuhashi N, Sato H, Fujibayashi K, Okumura M, Sasabe N, Urabe A. Helicobacter pylori infection significantly increases insulin resistance in the asymptomatic Japanese population. Helicobacter. 2009 Oct;14(5):144-50. http://doi.org/10.1111/j.1523-5378.2009.00705.x. PMID: 19751440.

Gupta R, Alcantara R, Popli T, Tariq U, Sood A, Mahajan S, Ayele H, Rajeswaran Y, Vyas AV. Firibastat: A Novel Brain Aminopeptidase Inhibitor - A New Era of Antihypertensive therapy. Curr Probl Cardiol. 2022 Sep;47(9):100859. http://doi.org/10.1016/j.cpcardiol.2021.100859. Epub 2021 Apr 3. PMID: 33994025.

Han X, Li Y, Wang J, Liu B, Hu H, Li X, Yang K, Yuan J, Yao P, Wei S, Wang Y, Liang Y, Miao X, Zhang X, Guo H, Yang H, Wu T, He M. Helicobacter pylori infection is associated with type 2 diabetes among a middle- and old-age Chinese population. Diabetes Metab Res Rev. 2016 Jan;32(1):95-101. http://doi.org/10.1002/dmrr.2677. Epub 2015 Aug 15. PMID: 26172433.

Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG, Ng SC. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017 Aug;153(2):420-429. http://doi.org/10.1053/j.gastro.2017.04.022. Epub 2017 Apr 27. PMID: 28456631.

Hsieh MC, Wang SS, Hsieh YT, Kuo FC, Soon MS, Wu DC. Helicobacter pylori infection associated with high HbA1c and type 2 diabetes. Eur J Clin Invest. 2013 Sep;43(9):949-56. http://doi.org/10.1111/eci.12124. Epub 2013 Jul 24. PMID: 23879740.

Intersalt Cooperative Research Group Intersalt: An international study of electrolyte excretion and blood pressure. Results for 24 hour urinary sodium and potassium excretion. BMJ. 1988;297:319-28. http://doi.org/10.1136/bmj.297.6644.319.

Jafarzadeh A, Hassanshahi GH, Nemati M. Serum levels of high-sensitivity C-reactive protein (hs-CRP) in Helicobacter pylori-infected peptic ulcer patients and its association with bacterial CagA virulence factor. Dig Dis Sci. 2009;54:2612-6. http://doi.org/10.1007/s10620-008-0686-z.

Jukic A, Bozic D, Kardum D, Becic T, Luksic B, Vrsalovic M, Ljubkovic M, Fabijanic D. Helicobacter pylori infection and severity of coronary atherosclerosis in patients with chronic coronary artery disease. Ther Clin Risk Manag. 2017 Jul 27;13:933-938. http://doi.org/10.2147/TCRM.S142193. PMID: 28794636; PMCID: PMC5538697.

Katsinelos T, Doulberis M, Polyzos SA, Papaefthymiou A, Katsinelos P, Kountouras J. Molecular links between Alzheimer’s disease and gastrointestinal microbiota: emphasis on Helicobacter pylori infection involvement. Curr Mol Med. 2019;20:3-12. http://doi.org/10.2174/1566524019666190917125917.

Kato S, Tsukamoto T, Mizoshita T, Tanaka H, Kumagai T, Ota H, Katsuyama T, Asaka M, Tatematsu M. High salt diets dose-dependently promote gastric chemical carcinogenesis in Helicobacter pylori-infected Mongolian gerbils associated with a shift in mucin production from glandular to surface mucous cells. Int J Cancer. 2006 Oct 1;119(7):1558-66. http://doi.org/10.1002/ijc.21810. PMID: 16646055.

Ko GT, Chan FK, Chan WB, Sung JJ, Tsoi CL, To KF, Lai CW, Cockram CS. Helicobacter pylori infection in Chinese subjects with type 2 diabetes. Endocr Res. 2001 Feb-May;27(1-2):171-7. http://doi.org/10.1081/erc-100107178. PMID: 11428708.

Kountouras J, Gavalas E, Boziki M, Zavos C. Helicobacter pylori may be involved in cognitive impairment and dementia development through induction of atrophic gastritis, vitamin B-12–folate deficiency, and hyperhomocysteinemia sequence. Am J Clin Nutr. 2007;86:805-6. http://doi.org/10.1093/ajcn/86.3.805.

Kountouras J, Polyzos SA, Katsinelos P, Zeglinas C, Artemaki F, Tzivras D, Vardaka E, Gavalas E, Romiopoulos I, Simeonidou C, Grigoriadis N, Kountouras C, Dardiotis E, Deretzi G. Cardio-cerebrovascular disease and Helicobacter pylori-related metabolic syndrome: We consider eradication therapy as a potential cardio-cerebrovascular prevention strategy. Int J Cardiol. 2017 Feb 15;229:17-18. http://doi.org/10.1016/j.ijcard.2016.11.265. Epub 2016 Nov 19. PMID: 27887801.

Kountouras J, Boziki M, Polyzos S, et al. The emerging role of Helicobacter pylori-induced metabolic gastrointestinal dysmotility and neurodegeneration. Curr Mol Med. 2018;17:389-404.

doi: 10.2174/1566524018666171219094837.

Kountouras J, Polyzos SA, Doulberis M, et al. Potential impact of Helicobacter pylori-related metabolic syndrome on upper and lower gastrointestinal tract oncogenesis. Metabolism. 2018;87:18-24. http://doi.org/10.1016/j.metabol.2018.06.008.

Kountouras J, Doulberis M, Polyzos SA, Katsinelos T, Vardaka E, Kountouras C, Arapoglou S, Exadaktylos AK, Deretzi G, Tsolaki M, Boziki M, Katsinelos P. Impact of Helicobacter pylori and/or Helicobacter pylori-related metabolic syndrome on incidence of all-cause and Alzheimer's dementia. Alzheimers Dement. 2019 May;15(5):723-725. http://doi.org/10.1016/j.jalz.2019.01.008. Epub 2019 Mar 11. PMID: 30872115.

Kountouras J, Papaefthymiou A, Doulberis M, Polyzos SA. Influence of Helicobacter pylori-connected metabolic syndrome on non-alcoholic fatty liver disease and its related colorectal neoplasm high risk. Liver Int. 2019;40:475-6. http://doi.org/10.1111/liv.14264.

Kountouras J, Papaefthymiou A, Polyzos SA, et al. Impact of Helicobacter pylori-related metabolic syndrome parameters on arterial hypertension. Microorganisms. 2021 Nov;9(11): 2351. Published online 2021 Nov 14. http://doi.org/10.3390/microorganisms9112351.

Kowalski M. Helicobacter pylori (H. pylori) infection in coronary artery disease: influence of H. pylori eradication on coronary artery lumen after percutaneous transluminal coronary angioplasty. The detection of H. pylori specific DNA in human coronary atherosclerotic plaque. J Physiol Pharmacol. 2001 Aug;52(1 Suppl 1):3-31. PMID: 11795863.

Kucukazman M, Yavuz B, Sacikara M, et al. The relationship between updated Sydney System Score and LDL cholesterol levels in patients infected with Helicobacter pylori. Dig Dis Sci. 2008;54:604-7. http://doi.org/10.1007/s10620-008-0391-y.

Lee YH, Magkos F, Mantzoros CS, Kang ES. Effects of leptin and adiponectin on pancreatic β-cell function. Metabolism. 2011;60:1664-72. http://doi.org/10.1016/j.metabol.2011.04.008.

Lee YY, Ismail AW, Mustaffa N, et al. Sociocultural and dietary practices among Malay subjects in the North-Eastern Region of Peninsular Malaysia: A Region of low prevalence of Helicobacter pylori infection. Helicobacter. 2012;17:54-61. http://doi.org/10.1111/j.1523-5378.2011.00917.x.

Lejawa M, Osadnik K, Osadnik T, Pawlas N. Association of metabolically healthy and unhealthy obesity phenotypes with oxidative stress parameters and telomere length in healthy young adult men. Analysis of the MAGNETIC Study. Antioxidants. 2021;10:93. http://doi.org/10.3390/antiox10010093.

Lillich FF, Imig JD, Proschak E. Multi-target approaches in metabolic syndrome. Front. Pharmacol. 2021;11:554961. http://doi.org/10.3389/fphar.2020.554961.

Longo-Mbenza B, Mokondjimobe N, Mokolndjimobe E, et al. Helicobacter pylori infection is identified as a cardiovascular risk factor in Central Africans. Vasc. Health Risk Manag. 2012;6:455-61. http://doi.org/10.2147/VHRM.S28680.

Lutsey PL, Pankow JS, Bertoni AG, Szklo M, Folsom AR. Serological evidence of infections and type 2 diabetes: the MultiEthnic study of atherosclerosis. Diabet. Med. 2009;26:149-52 doi: 10.1111/j.1464-5491.2008.02632.x.

Mabeku LBK, Ngamga MLN, Leundji H. Helicobacter pylori infection, a risk factor for Type 2 diabetes mellitus: a hospital-based cross-sectional study among dyspeptic patients in Douala-Cameroon. Sci Rep. 2020;10:12141. http://doi.org/10.1038/s41598-020-69208-3. PMID: 32699242; PMCID: PMC7376106.

Maciorkowska E. Soluble adhesion molecules ICAM-1, VCAM-1, P-selectin in children with Helicobacter pylori infection. World J Gastroenterol. 2005;11:6745. http://doi.org/10.3748/wjg.v11.i43.6745.

Madhur MS, Elijovich F, Alexander MR, et al. Hypertension. Circ. Res. 2021;128:908-33. http://doi.org/10.1161/CIRCRESAHA.121.318052.

Majka J, Róg T, Konturek PC, et al. Influence of chronic Helicobacter pylori infection on ischemic cerebral stroke risk factors. Med Sci Monit. 2002;8:CR675-CR684.

Mancusi C, Izzo R, di Gioia G, Losi MA, Barbato E, Morisco C. Insulin resistance the hinge between hypertension and type 2 diabetes and high blood press. Cardiovasc Prev. 2020;27:515-26. http://doi.org/10.1007/s40292-020-00408-8.

Martínez-Casales M, Hernanz R, Alonso MJ. Vascular and macrophage heme oxygenase-1 in hypertension: a mini-review. Front Physiol. 2021;12:643435. http://doi.org/10.3389/fphys.2021.643435.

Migneco A, Ojetti V, Specchia L, et al. Eradication of Helicobacter pylori infection improves blood pressure values in patients affected by hypertension. Helicobacter. 2003;8:585-9. http://doi.org/10.1111/j.1523-5378.2003.00180.x.

Murray LJ, Bamford KB, Kee F, et al. Infection with virulent strains of Helicobacter pylori is not associated with ischaemic heart disease: Evidence from a population-based case-control study of myocardial infarction. Atherosclerosis. 2000;149:379-85. http://doi.org/10.1016/S0021-9150(99)00325-1.

Nakagawa H, Tamura T, Mitsuda Y, et al. Significant association between serum interleukin-6 and Helicobacter pylori antibody levels among H. pylori-positive Japanese Adults. Mediat Inflamm. 2013:142358. http://doi.org/10.1155/2013/142358.

Nasrat SAM, Nasrat AM. An alternative approach for the rising challenge of hypertensive illness via Helicobacter pylori eradication. Cardiol Res. 2015;6:221-5. http://doi.org/10.14740/cr382e.

Nazligul Y, Aslan M, Horoz M, et al. The effect on serum myeloperoxidase activity and oxidative status of eradication treatment in patients Helicobacter pylori infected. Clin Biochem. 2011;44:647-9. http://doi.org/10.1016/j.clinbiochem.2011.03.001.

Newberry SJ, Chung M, Anderson CAM, Chen C, Fu Z, Tang A, Zhao N, Booth M, Marks J, Hollands S, Motala A, Larkin J, Shanman R, Hempel S. Sodium and Potassium Intake: Effects on Chronic Disease Outcomes and Risks [Internet]. Rockville (MD): Agency for Healthcare Research and Quality (US); 2018 Jun. Report No.: 18-EHC009-EF. PMID: 30125063.

Niccoli G, Franceschi F, Cosentino N, Giupponi B, De Marco G, Merra G, Conte M, Montone RA, Ferrante G, Bacà M, Gasbarrini A, Silveri NG, Crea F. Coronary atherosclerotic burden in patients with infection by CagA-positive strains of Helicobacter pylori. Coron Artery Dis. 2010 Jun;21(4):217-21. http://doi.org/10.1097/MCA.0b013e3283399f36. PMID: 20389238.

Papamichael KX, Papaioannou GG, Karga H, Roussos A, Mantzaris GJ. Helicobacter pylori infection and endocrine disorders: Is there a link? World J. Gastroenterol. 2009;15:2701-7. http://doi.org/10.3748/wjg.15.2701.

Patel PN, Shah RY, Ferguson JF, Reilly MP. Human experimental endotoxemia in modeling the pathophysiology, genomics, and therapeutics of innate immunity in complex cardiometabolic diseases. Arter Thromb Vasc Biol. 2015;35:525-34. http://doi.org/10.1161/ATVBAHA.114.304455.

Pellicano R, Oliaro E, Fagoonee S, Astegiano M, Berrutti M, Saracco G, Smedile A, Repici A, Leone N, Castelli A, Luigiano C, Fadda M, Rizzetto M. Clinical and biochemical parameters related to cardiovascular disease after Helicobacter pylori eradication. Int Angiol. 2009 Dec;28(6):469-73. PMID: 20087284.

Pellicano R, Ianiro G, Fagoonee S, Settanni CR, Gasbarrini A. Review: Extragastric diseases and Helicobacter pylori. Helicobacter. 2020;25:e12741. http://doi.org/10.1111/hel.12741.

Penna C, Femminò S, Alloatti G, Brizzi M, Angelone T, Pagliaro P. Extracellular vesicles in comorbidities associated with ischaemic heart disease: focus on sex, an overlooked factor. J Clin Med. 2021;10:327. http://doi.org/10.3390/jcm10020327.

Piazzolla G, Candigliota M, Fanelli M, Castrovilli A, Berardi E, Antonica G, Battaglia S, Solfrizzi V, Sabbà C, Tortorella C. Hyperhomocysteinemia is an independent risk factor of atherosclerosis in patients with metabolic syndrome. Diabetol Metab Syndr. 2019 Oct 26;11:87. http://doi.org/10.1186/s13098-019-0484-0. PMID: 31673296; PMCID: PMC6815401.

Polyzos SA, Kountouras J. Helicobacter pylori infection and nonalcoholic fatty liver disease: Time for large clinical trials evaluating eradication therapy. Helicobacter. 2019;24:e12588. http://doi.org/10.1111/hel.12588.

Queiroz T, Lakkappa N, Lazartigues E. ADAM17-mediated shedding of inflammatory cytokines in hypertension. Front. Pharmacol. 2020;11:1154. http://doi.org/10.3389/fphar.2020.01154.

Ramji DP, Davies TS. Cytokines in atherosclerosis: Key players in all stages of disease and promising therapeutic targets. Cytokine Growth Factor Rev. 2015;26:673-85. http://doi.org/10.1016/j.cytogfr.2015.04.003.

Russo F, Jirillo E, Clemente C, Messa C, Chiloiro M, Riezzo G, Amati L, Caradonna L, Di Leo A. Circulating cytokines and gastrin levels in asymptomatic subjects infected by Helicobacter pylori (H. pylori). Immunopharmacol Immunotoxicol. 2001 Feb;23(1):13-24. http://doi.org/10.1081/iph-100102563. PMID: 11322645.

Saklayen MG. The global epidemic of the metabolic syndrome. Curr Hypertens Rep. 2018;20:12. http://doi.org/10.1007/s11906-018-0812-z.

Senmaru T, Fukui M, Kuroda M, Tanaka M, Ushigome E, Sakabe K, Nakanishi N, Mineoka Y, Asano M, Yamazaki M, Hasegawa G, Nakamura N. Serum pepsinogen I/II ratio is correlated with albuminuria in patients with type 2 diabetes. Endocr J. 2013;60(2):161-6. http://doi.org/10.1507/endocrj.ej12-0244. Epub 2012 Oct 5. PMID: 23047493.

Shin DW, Kwon HT, Kang JM, Park JH, Choi HC, Park MS, Park SM, Son KY, Cho B. Association between metabolic syndrome and Helicobacter pylori infection diagnosed by histologic status and serological status. J Clin Gastroenterol. 2012 Nov-Dec;46(10):840-5. http://doi.org/10.1097/MCG.0b013e3182522477. PMID: 23064216.

Shmuely H, Wattad M, Solodky A, Yahav J, Samra Z, Zafrir N. Association of Helicobacter pylori with coronary artery disease and myocardial infarction assessed by myocardial perfusion imaging. Isr Med Assoc J. IMAJ. 2014;16:341-6.

Slomiany BL, Slomiany A. Involvement of p38 MAPK-dependent activator protein (AP-1) activation in modulation of gastric mucosal inflammatory responses to Helicobacter pylori by ghrelin. Inflammopharmacology. 2013;21:67-78. http://doi.org/10.1007/s10787-012-0141-9.

Slomiany BL, Slomiany A. Induction in gastric mucosal prostaglandin and nitric oxide by Helicobacter pylori is dependent on MAPK/ERK-mediated activation of IKK-β and cPLA2: Modulatory effect of ghrelin. Inflammopharmacology. 2013;21:241-51. http://doi.org/10.1007/s10787-013-0169-5.

Risk Factor Collaborators. Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018 Nov 10;392(10159):1923-1994. http://doi.org/10.1016/S0140-6736(18)32225-6. Epub 2018 Nov 8. Erratum in: Lancet. 2019 Jan 12;393(10167):132. Erratum in: Lancet. 2019 Jun 22;393(10190):e44. PMID: 30496105; PMCID: PMC6227755.

Stanciu OG, Trifan A, Sfarti C, Cojocariu C, Stanciu C. Helicobacter pylori infection in patients with diabetes mellitus. Rev Med Chir Soc Med Nat Iasi. 2003 Jan-Mar;107(1):59-65. PMID: 14755971.

Strachan DP. Non-gastrointestinal consequences of Helicobacter pylori infection. Br Med Bull. 1998;54:87-93. http://doi.org/10.1093/oxfordjournals.bmb.a011684.

Taher M, Mashayekhi M, Hashemi M, Bahrani V. Helicobacter pylori in diabetic and non-diabetic patients with dyspepsia. Acta Medica Iranica. 2012;50(5):315-8.

Tang BW, Wang XM, Wu J. [Progress in research on the relationship between Helicobacter pylori infection and cardiovascular diseases and its risk factors]. Zhonghua Yu Fang Yi Xue Za Zhi. 2020 Mar 6;54(3):327-31. Chinese. http://doi.org/10.3760/cma.j.issn.0253-9624.2020.03.016.

Tanriverdi O. Association of Helicobacter pylori infection with microalbuminuria in type 2 diabetic patients. Turk J Gastroenterol. 2011;22:569-74. doi: 10.4318/tjg.2011.0252.

The EUROGAST Study Group An international association between Helicobacter pylori infection and gastric cancer. Lancet. 1993;341:1359-62. http://doi.org/10.1016/0140-6736(93)90938-D.

Vafaeimanesh J, Parham M, Bagherzadeh M. Helicobacter pylori infection prevalence: is it different in diabetics and nondiabetics? Indian J Endocrinol Metab. 2015;19(3):364-8 doi: 10.4103/2230-8210.152773.

Vafaeimanesh J, Bagherzadeh M, Mirzaei A, Parham M, Norouzinia M, Vafaee R. Effect of Helicobacter pylori on metabolic syndrome parameters in diabetic patients. Gastroenterol Hepatol Bed Bench. 2016 Dec;9(Suppl1):S36-S41. PMID: 28224026; PMCID: PMC5310798.

Vallianou NG, Geladari E, Kounatidis D. Microbiome and hypertension. J Cardiovasc Med. 2020;21:83-8. http://doi.org/10.2459/JCM.0000000000000900.

Vijayvergiya R, Vadivelu R. Role of Helicobacter pylori infection in pathogenesis of atherosclerosis. World J Cardiol. 2015;7:134-43. http://doi.org/10.4330/wjc.v7.i3.134.

Wan Z, Hu L, Hu M, Lei X, Huang Y, Lv Y. Helicobacter pylori infection and prevalence of high blood pressure among Chinese adults. J Hum Hypertens. 2018 Feb;32(2):158-164. http://doi.org/10.1038/s41371-017-0028-8. Epub 2017 Dec 30. PMID: 29289960.

Wang C, Guan Y, Yang J. Cytokines in the progression of pancreatic β-cell dysfunction. Int J Endocrinol. 2010;2010:515136.

Wang J, Du J, Fan R. Exploration of the risk factors of essential hypertension with hyperhomocysteinemia: A hospital-based study and nomogram analysis. Clinics. 2021;76:e2233. http://doi.org/10.6061/clinics/2021/e2233.

Xia HH, Talley NJ, Kam EP, Young LJ, Hammer J, Horowitz M. Helicobacter pylori infection is not associated with diabetes mellitus, nor with upper gastrointestinal symptoms in diabetes mellitus. Am J Gastroenterol. 2001;96:1039-46. http://doi.org/10.1111/j.1572-0241.2001.03604.x.

Xiong X, Chen J, He M, Wu T, Yang H. Helicobacter pylori infection and the prevalence of hypertension in Chinese adults: The Dongfeng-Tongji cohort. J Clin Hypertens. 2020;22:1389-395. http://doi.org/10.1111/jch.13928.

Yang W, Xuan C. Influence of Helicobacter pylori infection on metabolic syndrome in old Chinese people. Gastroenterol Res Pract 2016;2016:6951264. doi: 10.1155/2016/6951264.

Ye P, Chen HWL. Diagnosis and treatment of dyslipidemia. 2nd ed. People’s Military Medical Press; Beijing, China; 2013.

Zelenkova J, Souckova A, Kvapil M, Soucek A, Vejvalka J, Segethova J. Helicobacter pylori and diabetes mellitus. Cas Lek Cesk. 2002;141:575-7.

Zhu J, Katz RJ, Quyyumi AA, Canos DA, Rott D, Csako G, Zalles-Ganley A, Ogunmakinwa J, Wasserman AG, Epstein SE. Association of serum antibodies to heat-shock protein 65 with coronary calcification levels: suggestion of pathogen-triggered autoimmunity in early atherosclerosis. Circulation. 2004 Jan 6;109(1):36-41. http://doi.org/10.1161/01.CIR.0000105513.37677.B3. Epub 2003 Dec 8. PMID: 14662717.