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Impact of Active Helicobacter pylori Infection-related Metabolic Syndrome on Systemic Arterial Hypertension

Helicobacter pylori; Hypertension; Metabolic Syndrome; Atherosclerosis; Dyslipidemias

To the Editor,

In their meta-analysis, Huang et al.11. Huang M, Zhu L, Jin Y, Fang Z, Chen Y, Yao Y.Association between Helicobacter Pylori Infection and Systemic Arterial Hypertension: A Meta-Analysis[Article in English, Portuguese]. Arq Bras Cardiol. 2021;117(4):626-36. DOI: DOI: 10.36660/abc.20200186. concluded that Helicobacter pylori infection ( H. pylori infection) is positively associated with systemic arterial hypertension, particularly by introducing the diagnostic 13C-urea breath test, signifying current H. pylori infection.

In this regard, systemic arterial hypertension is one of the most significant parameters of the metabolic syndrome (MetS), and its pathogenesis may mostly comprise of a noxious interplay between vascular, renal, neural, and hormonal mechanisms, of which augmented activation of the sympathetic nervous system (SNS) and the renin-angiotensin-aldosterone system (RAAS) predominate.22. Gupta R, Alcantara R, Popli T, Tariq U, Sood A, Mahajan S, et al. Firibastat: A Novel Brain Aminopeptidase Inhibitor - A New Era of Antihypertensive therapy. Curr Probl Cardiol. 2021;100859. [PubMed] Augmented activity of SNS is a usual feature of resistant systemic arterial hypertension, accompanied by increased release of norepinephrine, signifying a neurogenic element that contributes to the development of systemic arterial hypertension; and overactivation of SNS is associated with morbidity and mortality of MetS-related cardiovascular disorders.33. Grassi G, Mark A, Esler M. The sympathetic nervous system alterations in human hypertension. Circ Res. 2015;116(6):976-90. DOI: 10.1161/CIRCRESAHA.116.303604. Moreover, RAAS dysregulation, including the systemic and brain RAAS, has been documented as one of the chief causes of several types of systemic arterial hypertension; and RAAS overactivation also contributes to MetS-associated obesity and cardiovascular morbidity and mortality.44. Vecchiola A, Fuentes CA, Solar I, Lagos CF, Opazo MC, Muñoz-Durango N, et al. Eplerenone Implantation Improved Adipose Dysfunction Averting RAAS Activation and Cell Division. Front Endocrinol (Lausanne). 2020;11:223. DOI: 10.3389/fendo.2020.00223.

Likewise, H. pylori infection is also associated with MetS-related systemic pathologies, especially cardio-cerebrovascular and neurodegenerative diseases, the endpoints of MetS.55. Franceschi F, Gasbarrini A, Polyzos SA, Kountouras J. Extragastric Diseases and Helicobacter pylori. Helicobacter. 2015:20 (Suppl 1): 40–46. DOI: 10.3389/fendo.2020.00223.
https://doi.org/10.3389/fendo.2020.00223...

6. Kountouras J, Polyzos SA, KatsinelosP, Zeglinas C, Artemaki F, Tivras D, et al. Cardio-cerebrovascular disease and Helicobacter pylori-related metabolic syndrome: We consider eradication therapy as a potential cardio-cerebrovascular prevention strategy. Int J Cardiol. 2017;229:17–8. doi: 10.1016/j.ijcard.2016.11.265.

7. Kountouras J, Doulberis M, Polyzos SA, Katsinelos T, Vardaka E, Kountouras C, et al. Impact of Helicobacter pylori and/or Helicobacter pylori–related metabolic syndrome on incidence of all-cause and Alzheimer’s dementia. Alzheimer’s Dement. 2019;15(5):723–5. doi: 10.1016/j.jalz.2019.01.008.
- 88. Doulberis M, Kotronis G, Gialamprinou D, Polyzos SA, Papaefthymiou A, Katsinelow P, et al. Alzheimer’s disease and gastrointestinal microbiota; impact of Helicobacter pylori infection involvement. Int J Neurosci. 2021;131(3):289–doi: 10.1016/j.ijcard.2016.11.265301.
https://doi.org/10.1016/j.ijcard.2016.11...
Specifically, H. pylori infection seems to contribute to insulin resistance (IR), the chief underlying mechanism responsible for MetS,99. Kountouras J, Polyzos SA, Doulberis M, Zeglinas C, Artemaki F, Vardaka E, et al. Potential impact of Helicobacter pylori-related metabolic syndrome on upper and lower gastrointestinal tract oncogenesis. Metabolism. 2018;87:18–24. doi: 10.1016/j.metabol.2018.06.008 which also plays n critical role in the pathogenesis and progression of systemic arterial hypertension-triggered target organ injuries.1010. Mancusi C, Izzo R, di Gioia G, Losi AM, Barbaro E, Morisco C. Insulin Resistance the Hinge Between Hypertension and Type 2 Diabetes. High Blood Press Cardiovasc Prev. 2020;27(6):515-26. doi: 10.1007/s40292-020-00408-8. MetS contributes to an increased risk of developing atherosclerosis,1111. Xu J, Kitada M, Ogura Y, Koya D. Relationship Between Autophagy and Metabolic Syndrome Characteristics in the Pathogenesis of Atherosclerosis. Front Cell Dev Biol. 2021;9:641852. doi: 10.3389/fcell.2021.641852. doi: 10.3389/fcell.2021.641852.
https://doi.org/10.3389/fcell.2021.64185...
and in this respect, invasion of H. pylori into atheroma has been detected by introducing polymerase chain reaction (PCR).1212. Kowalski M. 2001. 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 atherosclerot. J Physiol Pharmacol. 2001;52 (1 Suppl1):3–31. PMID: 11795863 Direct H. pylori colonization in the arterial walls has been observed. H. pylori is associated with arterial stiffness, an early marker of systemic atherosclerosis correlated with systemic arterial hypertension and an independent predictor of cardiovascular complications and all-cause mortality. Thus, H. pylori have been associated with MetS-related atherosclerosis via a diversity of involved mechanisms, thereby potentially triggering systemic arterial hypertension. H. pylori infection might independently be involved in atherosclerosis and arterial hypertension through mechanisms distinct from the conventional causes of atherosclerosis, including the three non-conventional coronary artery disease risk factors homocysteine, fibrinogen and lipoprotein(a).66. Kountouras J, Polyzos SA, KatsinelosP, Zeglinas C, Artemaki F, Tivras D, et al. Cardio-cerebrovascular disease and Helicobacter pylori-related metabolic syndrome: We consider eradication therapy as a potential cardio-cerebrovascular prevention strategy. Int J Cardiol. 2017;229:17–8. doi: 10.1016/j.ijcard.2016.11.265. , 1313. Bostom AG, Shemin D, Lapane, KL, Sutherland P, Nadeau MR, Wilson PW, et al. Hyperhomocysteinemia, hyperfibrinogenemia, and lipoprotein (a) excess in maintenance dialysis patients: A matched case-control study. Atherosclerosis 1996;125(1): 91–10. , 1414. 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(3):805-7. DOI: 10.1093/ajcn/86.3.805.

Besides, MetS-related dyslipidemia is linked with systemic arterial hypertension1515. Lillich FF, Iming JD, Proschak E. Multi-Target Approaches in Metabolic Syndrome. Front Pharmacol. 2021;11:554961. doi: 10.3389/fphar.2020.554961. and in this regard, chronic H. pylori infection can trigger abnormal lipid metabolism of the host, including, beyond the mentioned lipoprotein(a), low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), and total cholesterol (TC),1616. Papamichael KX, Papaioannou GG, Karga H, Roussos A, Mantzaris GJ Helicobacter pylori infection and endocrine disorders: Is there a link? World J. Gastroenterol. 2009;15:2701–2707. doi: 10.3748/wjg.15.2701. also mentioned by the authors;11. Huang M, Zhu L, Jin Y, Fang Z, Chen Y, Yao Y.Association between Helicobacter Pylori Infection and Systemic Arterial Hypertension: A Meta-Analysis[Article in English, Portuguese]. Arq Bras Cardiol. 2021;117(4):626-36. DOI: DOI: 10.36660/abc.20200186. H. pylori -related lower HDL-C appears to promote dyslipidemia.1717. Abdu A, Cheneke W, Adem M, Belete R, Getachew A. Dyslipidemia and Associated Factors Among Patients Suspected to Have Helicobacter pylori Infection at Jimma University Medical Center, Jimma, Ethiopia. Int J Gen Med. 2020 ;13:311-321. doi: 10.2147/IJGM.S243848. In contrast, H. pylori eradication significantly decreases the levels of TC, TG, LDL-C and fibrinogen, an independent risk factor for cardiovascular disease,66. Kountouras J, Polyzos SA, KatsinelosP, Zeglinas C, Artemaki F, Tivras D, et al. Cardio-cerebrovascular disease and Helicobacter pylori-related metabolic syndrome: We consider eradication therapy as a potential cardio-cerebrovascular prevention strategy. Int J Cardiol. 2017;229:17–8. doi: 10.1016/j.ijcard.2016.11.265. whereas increases HDL-C concentrations.1818. Majka J, Róg T, Konturek PC, Konturek SJ, Bielański W, Kowalsky M, et al. Influence of chronic Helicobacter pylori infection on ischemic cerebral stroke risk factors. Med Sci Monit. 2002;8(10):CR675-84. PMID:12388919. , 1919. Pellicano R, Oliaro E, Fagoonee S, Astegiano M, Berrutti M, Saracco G, et al. Clinical and biochemical parameters related to cardiovascular disease after Helicobacter pylori eradication. Int Angiol. 2009; 28(6): 469–73. PMID:20087284. Moreover, beyond dyslipidemia and systemic arterial hypertension, H. pylori eradication also improves other MetS-related parameters, including body mass index (BMI),2020. Jalalzadeh M, Ghadiani MH, Mousavinasab N. Association between helicobacter pylori infection and body mass index, before and after eradication of infection in hemodialysis batients. J Nephropathol. 2012;1(3):170–6. doi:10.5812/numonthly.25560.
https://doi.org/10.5812/numonthly.25560...
IR,2121. Gen R M. Demir M, Ataseven H. Effect of Helicobacter pylori Eradication on Insulin Resistance, Serum Lipids and Low-Grade Inflammation. South Med J. 2010;103(3):190–6. doi: 10.5812/numonthly.25560. and total oxidant status.2222. Nazligul Y, Aslan M, Horoz M, Celik Y, Dulger AC, Celik H, et al. The effect on serum myeloperoxidase activity and oxidative status of eradication treatment in patients Helicobacter pylori infected. Clin Biochem. 2011;44(8-9):647-9. doi: 10.1016/j.clinbiochem.2011.03.001. Therefore, eradication of H. pylori infection reduces the occurrence of MetS-related dyslipidemia and other parameters including systemic arterial hypertension,2323. Migneco A, Ojetti V, Specchia L, Franceschi F, Candelli M, Mettimano M, et al. Eradication of Helicobacter pylori Infection Improves Blood Pressure Values in Patients Affected by Hypertension. Helicobacter 2003;8(6): 585–9. doi: 10.1111/j.1523-5378.2003.00180.x. , 2424. Fang Y, Xie H, Fan C. Association of hypertension with helicobacter pylori: A systematic review and meta-analysis. PLoS One. 2022;17(5):e0268686. doi: 10.1371/journal.pone.0268686. thereby potentially preventing the occurrence of MetS-related cardiovascular disease accompanied by arterial hypertension.

Recent data indicate that MetS-related sarcopenia, H. pylori infection, dyslipidemia, systemic arterial hypertension, diabetes mellitus, smoking, alcohol consumption, and diet (salty and/or spicy diets) are linked with precancerous gastric mucosa lesions, including gastric atrophy, intestinal metaplasia, and dysplasia.2525. Kim YM, Kim JH, Baik SJ, Chun J, Youn YH. Sarcopenia and Sarcopenic Obesity as Novel Risk Factors for Gastric Carcinogenesis: A Health Checkup Cohort Study. Front Oncol. 2019;9:1249. doi: 10.3389/fonc.2019.01249 In this respect, interesting recent evidence also indicates that bariatric patients with H. pylori infection display baseline significantly high rates of the mentioned gastric pre-malignant lesions, including gastric atrophy and intestinal metaplasia accompanied with IR and arterial hypertension.2626. Doulberis M, Pierre NT, Manzini G, Papaefthymiou A, Kountouras J, Klukowska-Rotzlwer J, et al. Helicobacter pylori-Related Metabolic Parameters and Premalignant Gastric Mucosdoi: 10.3389/fonc.2019.01249a Histological Lesions in Swiss Bariatric Patients. Microorganisms. 2021;9(7):1361. doi: doi: 10.3390/microorganisms9071361. 10.3390/microorganisms9071361.

Finally, nonalcoholic fatty liver disease (NAFLD), recently renamed as metabolic dysfunction-associated fatty liver disease (MAFLD), is the hepatic component of MetS also associated with H. pylori infection, which appears to contribute to its development and progression;2727. Doulberis Mdoi: 10.1097/MD.0000000000026706., Srivastava S, Polyzos SA, Kountouras J, Papaefthymiou A, Klukowska-Rotzlwer J, et al. Active Helicobacter pylori Infection is Independently Associated with Nonalcoholic Steatohepatitis in Morbidly Obese Patients. J Clin Med. 2020;9(4):933.
https://doi.org/10.1097/MD.0000000000026...
NAFLD/MAFLD is associated with an about 1.6-fold augmented risk of developing systemic arterial hypertension; and MetS- related characteristics including high BMI, dyslipidemia, and type 2 diabetes mellitus in the setting of H. pylori infection exhibit a greater tendency for the development of NAFLD/MAFLD. In this regard, recent data indicate that H. pylori infection is connected with IR and augmented intestinal permeability, which could contribute to the development of NAFLD/MAFLD;2828. Wei L, Ding H-G. Relationship between Helicobacter pylori infection and nonalcoholic fatty liver disease. Medicine (Baltimore). 2021:100(31):e26706. doi: 10.1097/MD.0000000000026706. and active H. pylori infection is independently positively associated with the severity of nonalcoholic steatohepatitis and fibrosis, findings suggesting probable clinical implications.2727. Doulberis Mdoi: 10.1097/MD.0000000000026706., Srivastava S, Polyzos SA, Kountouras J, Papaefthymiou A, Klukowska-Rotzlwer J, et al. Active Helicobacter pylori Infection is Independently Associated with Nonalcoholic Steatohepatitis in Morbidly Obese Patients. J Clin Med. 2020;9(4):933.
https://doi.org/10.1097/MD.0000000000026...
Among patients with NAFLD/MAFLD, the prevalence of arterial hypertension varies from 40-70%, and relative studies have shown that NAFLD/MAFLD is strongly related to the augmented risk of systemic arterial prehypertension and hypertension.2929. Aneni EC, Oni ET, Martin SS, Blaha MJ, Agatston AS, Feldman T, et al. Blood pressure is associated with the presence and severity of nonalcoholic fatty liver disease across the spectrum of cardiometabolic risk. J Hypertens. 2015;33(6):1207–14. doi: 10.1097/HJH.0000000000000532. In contrast, beyond the reduction of the mentioned systemic arterial hypertension, H. pylori eradication particularly increases HDL-C and reduces LDL-C,3030. Adachi K, Mishiro T, Toda T, Kano N, Fujihara H, Mishima Y, et al. Effects of Helicobacter pylori eradication on serum lipid levels. J Clin Biochem Nutr. 2018;62(3):264-9. doi: 10.3164/jcbn.17-88 thus restoring the cardioprotective activity of the HDL-C/LDL-C ratio and diminishing the cardiovascular risk linked to MAFLD.3030. Adachi K, Mishiro T, Toda T, Kano N, Fujihara H, Mishima Y, et al. Effects of Helicobacter pylori eradication on serum lipid levels. J Clin Biochem Nutr. 2018;62(3):264-9. doi: 10.3164/jcbn.17-88

Viewing the aforementioned data, H. pylori infection seems to display pleiotropic effects beyond the gastrointestinal tract and rising evidence associates it with MetS, including systemic arterial hypertension. Further research is warranted, however, to clarify the potential impact of H. pylori related MetS on systemic arterial hypertension, which represents a serious public health problem with high global incidence and prevalence that continues to increase and may contribute to global high morbidity and mortality. Identifying H. pylori and MetS-related NAFLD/MAFLD and other relative disorders – as important risk factors for systemic arterial hypertension – may be helpful for improving the risk prediction, identifying primary preventive strategies, and selecting a therapeutic program for systemic arterial hypertension.

Referências

  • 1
    Huang M, Zhu L, Jin Y, Fang Z, Chen Y, Yao Y.Association between Helicobacter Pylori Infection and Systemic Arterial Hypertension: A Meta-Analysis[Article in English, Portuguese]. Arq Bras Cardiol. 2021;117(4):626-36. DOI: DOI: 10.36660/abc.20200186.
  • 2
    Gupta R, Alcantara R, Popli T, Tariq U, Sood A, Mahajan S, et al. Firibastat: A Novel Brain Aminopeptidase Inhibitor - A New Era of Antihypertensive therapy. Curr Probl Cardiol. 2021;100859. [PubMed]
  • 3
    Grassi G, Mark A, Esler M. The sympathetic nervous system alterations in human hypertension. Circ Res. 2015;116(6):976-90. DOI: 10.1161/CIRCRESAHA.116.303604.
  • 4
    Vecchiola A, Fuentes CA, Solar I, Lagos CF, Opazo MC, Muñoz-Durango N, et al. Eplerenone Implantation Improved Adipose Dysfunction Averting RAAS Activation and Cell Division. Front Endocrinol (Lausanne). 2020;11:223. DOI: 10.3389/fendo.2020.00223.
  • 5
    Franceschi F, Gasbarrini A, Polyzos SA, Kountouras J. Extragastric Diseases and Helicobacter pylori. Helicobacter. 2015:20 (Suppl 1): 40–46. DOI: 10.3389/fendo.2020.00223.
    » https://doi.org/10.3389/fendo.2020.00223
  • 6
    Kountouras J, Polyzos SA, KatsinelosP, Zeglinas C, Artemaki F, Tivras D, et al. Cardio-cerebrovascular disease and Helicobacter pylori-related metabolic syndrome: We consider eradication therapy as a potential cardio-cerebrovascular prevention strategy. Int J Cardiol. 2017;229:17–8. doi: 10.1016/j.ijcard.2016.11.265.
  • 7
    Kountouras J, Doulberis M, Polyzos SA, Katsinelos T, Vardaka E, Kountouras C, et al. Impact of Helicobacter pylori and/or Helicobacter pylori–related metabolic syndrome on incidence of all-cause and Alzheimer’s dementia. Alzheimer’s Dement. 2019;15(5):723–5. doi: 10.1016/j.jalz.2019.01.008.
  • 8
    Doulberis M, Kotronis G, Gialamprinou D, Polyzos SA, Papaefthymiou A, Katsinelow P, et al. Alzheimer’s disease and gastrointestinal microbiota; impact of Helicobacter pylori infection involvement. Int J Neurosci. 2021;131(3):289–doi: 10.1016/j.ijcard.2016.11.265301.
    » https://doi.org/10.1016/j.ijcard.2016.11.265301
  • 9
    Kountouras J, Polyzos SA, Doulberis M, Zeglinas C, Artemaki F, Vardaka E, et al. Potential impact of Helicobacter pylori-related metabolic syndrome on upper and lower gastrointestinal tract oncogenesis. Metabolism. 2018;87:18–24. doi: 10.1016/j.metabol.2018.06.008
  • 10
    Mancusi C, Izzo R, di Gioia G, Losi AM, Barbaro E, Morisco C. Insulin Resistance the Hinge Between Hypertension and Type 2 Diabetes. High Blood Press Cardiovasc Prev. 2020;27(6):515-26. doi: 10.1007/s40292-020-00408-8.
  • 11
    Xu J, Kitada M, Ogura Y, Koya D. Relationship Between Autophagy and Metabolic Syndrome Characteristics in the Pathogenesis of Atherosclerosis. Front Cell Dev Biol. 2021;9:641852. doi: 10.3389/fcell.2021.641852. doi: 10.3389/fcell.2021.641852.
  • 12
    Kowalski M. 2001. 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 atherosclerot. J Physiol Pharmacol. 2001;52 (1 Suppl1):3–31. PMID: 11795863
  • 13
    Bostom AG, Shemin D, Lapane, KL, Sutherland P, Nadeau MR, Wilson PW, et al. Hyperhomocysteinemia, hyperfibrinogenemia, and lipoprotein (a) excess in maintenance dialysis patients: A matched case-control study. Atherosclerosis 1996;125(1): 91–10.
  • 14
    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(3):805-7. DOI: 10.1093/ajcn/86.3.805.
  • 15
    Lillich FF, Iming JD, Proschak E. Multi-Target Approaches in Metabolic Syndrome. Front Pharmacol. 2021;11:554961. doi: 10.3389/fphar.2020.554961.
  • 16
    Papamichael KX, Papaioannou GG, Karga H, Roussos A, Mantzaris GJ Helicobacter pylori infection and endocrine disorders: Is there a link? World J. Gastroenterol. 2009;15:2701–2707. doi: 10.3748/wjg.15.2701.
  • 17
    Abdu A, Cheneke W, Adem M, Belete R, Getachew A. Dyslipidemia and Associated Factors Among Patients Suspected to Have Helicobacter pylori Infection at Jimma University Medical Center, Jimma, Ethiopia. Int J Gen Med. 2020 ;13:311-321. doi: 10.2147/IJGM.S243848.
  • 18
    Majka J, Róg T, Konturek PC, Konturek SJ, Bielański W, Kowalsky M, et al. Influence of chronic Helicobacter pylori infection on ischemic cerebral stroke risk factors. Med Sci Monit. 2002;8(10):CR675-84. PMID:12388919.
  • 19
    Pellicano R, Oliaro E, Fagoonee S, Astegiano M, Berrutti M, Saracco G, et al. Clinical and biochemical parameters related to cardiovascular disease after Helicobacter pylori eradication. Int Angiol. 2009; 28(6): 469–73. PMID:20087284.
  • 20
    Jalalzadeh M, Ghadiani MH, Mousavinasab N. Association between helicobacter pylori infection and body mass index, before and after eradication of infection in hemodialysis batients. J Nephropathol. 2012;1(3):170–6. doi:10.5812/numonthly.25560.
    » https://doi.org/10.5812/numonthly.25560
  • 21
    Gen R M. Demir M, Ataseven H. Effect of Helicobacter pylori Eradication on Insulin Resistance, Serum Lipids and Low-Grade Inflammation. South Med J. 2010;103(3):190–6. doi: 10.5812/numonthly.25560.
  • 22
    Nazligul Y, Aslan M, Horoz M, Celik Y, Dulger AC, Celik H, et al. The effect on serum myeloperoxidase activity and oxidative status of eradication treatment in patients Helicobacter pylori infected. Clin Biochem. 2011;44(8-9):647-9. doi: 10.1016/j.clinbiochem.2011.03.001.
  • 23
    Migneco A, Ojetti V, Specchia L, Franceschi F, Candelli M, Mettimano M, et al. Eradication of Helicobacter pylori Infection Improves Blood Pressure Values in Patients Affected by Hypertension. Helicobacter 2003;8(6): 585–9. doi: 10.1111/j.1523-5378.2003.00180.x.
  • 24
    Fang Y, Xie H, Fan C. Association of hypertension with helicobacter pylori: A systematic review and meta-analysis. PLoS One. 2022;17(5):e0268686. doi: 10.1371/journal.pone.0268686.
  • 25
    Kim YM, Kim JH, Baik SJ, Chun J, Youn YH. Sarcopenia and Sarcopenic Obesity as Novel Risk Factors for Gastric Carcinogenesis: A Health Checkup Cohort Study. Front Oncol. 2019;9:1249. doi: 10.3389/fonc.2019.01249
  • 26
    Doulberis M, Pierre NT, Manzini G, Papaefthymiou A, Kountouras J, Klukowska-Rotzlwer J, et al. Helicobacter pylori-Related Metabolic Parameters and Premalignant Gastric Mucosdoi: 10.3389/fonc.2019.01249a Histological Lesions in Swiss Bariatric Patients. Microorganisms. 2021;9(7):1361. doi: doi: 10.3390/microorganisms9071361. 10.3390/microorganisms9071361.
  • 27
    Doulberis Mdoi: 10.1097/MD.0000000000026706., Srivastava S, Polyzos SA, Kountouras J, Papaefthymiou A, Klukowska-Rotzlwer J, et al. Active Helicobacter pylori Infection is Independently Associated with Nonalcoholic Steatohepatitis in Morbidly Obese Patients. J Clin Med. 2020;9(4):933.
  • 28
    Wei L, Ding H-G. Relationship between Helicobacter pylori infection and nonalcoholic fatty liver disease. Medicine (Baltimore). 2021:100(31):e26706. doi: 10.1097/MD.0000000000026706.
  • 29
    Aneni EC, Oni ET, Martin SS, Blaha MJ, Agatston AS, Feldman T, et al. Blood pressure is associated with the presence and severity of nonalcoholic fatty liver disease across the spectrum of cardiometabolic risk. J Hypertens. 2015;33(6):1207–14. doi: 10.1097/HJH.0000000000000532.
  • 30
    Adachi K, Mishiro T, Toda T, Kano N, Fujihara H, Mishima Y, et al. Effects of Helicobacter pylori eradication on serum lipid levels. J Clin Biochem Nutr. 2018;62(3):264-9. doi: 10.3164/jcbn.17-88

Publication Dates

  • Publication in this collection
    05 Sept 2022
  • Date of issue
    Sept 2022
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