Helicobacter pylori Infection Associated with Type 2 Diabetes
A Case–Control Study
Abstract
Helicobacter pylori (Hp) is a spiral Gram-negative bacterium that causes gastritis and peptic ulcers. It has been identified as a risk factor for gastric cancer and has become a significant global health burden. This is further complicated by being associated with increasing the prevalence of Type 2 diabetes (T2D). The study aimed to evaluate the possible associations between Hp infection and T2D, as well as its impact on glycated hemoglobin. A 1:1 matching case–control study is conducted on 548 individuals with T2D as cases and 548 controls, and a 14C-urea breath test is used to determine the presence of Hp infection. All diabetic subjects are tested for glycated hemoglobin, and binary logistic regression analysis is used to evaluate the associations between Hp infection and T2D. The prevalence of Hp infection is higher among cases (58.94%) than control subjects (38.69%) (p < 0.001). A significant association is observed between Hp infection and T2D according to logistic regression analysis (OR = 2.275; 95% CI: 1.786-2.898; p < 0.001), and there is a significant association (p = 0.022) between glycated hemoglobin levels and Hp infection. Individuals infected with Hp had a higher-level glycated hemoglobin (7.84 ± 1.797) than Hp-negative individuals (p < 0.001). Hp infection is associated with elevated glycated hemoglobin levels. Type 2 diabetes is considered a risk factor for developing Hp infection.
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Alias, N.M., and Elkarsany, M.S.M., 2022. Effect of H. pylori among Diabetic Patients Living in Khartoum State, Sudan. International Blood Research and Reviews, 13, pp.1-8. DOI: https://doi.org/10.9734/ibrr/2022/v13i330175
Alzahrani, S., Nelson, J., Moss, S.F., Paulus, J.K., Knowler, W.C., and Pittas, A.G., 2017. H. pylori seroprevalence and risk of diabetes: An ancillary case-control study nested in the diabetes prevention program. Journal of Diabetes and Its Complications, 31, pp.1515-1520. DOI: https://doi.org/10.1016/j.jdiacomp.2017.05.015
Andrew, W., and Adrian, V., 2022. What is type 2 diabetes? Medicine, 50, pp.625-631. DOI: https://doi.org/10.1016/j.mpmed.2022.07.003
Bajaj, S., Rekwal, L., Misra, S.P., Misra, V., Yadav, R.K., and Srivastava, A., 2014. Association of Helicobacter pylori infection with type 2 diabetes. Indian Journal of Endocrinology and Metabolism, 18, pp.694-699. DOI: https://doi.org/10.4103/2230-8210.139235
Bener, A., Ağan, A.F., Al-Hamaq, A., Barisik, C.C., Öztürk, M., and Ömer, A., 2020. Prevalence of Helicobacter pylori infection among Type 2 diabetes mellitus. Advanced Biomedical Research, 9, p.27. DOI: https://doi.org/10.4103/abr.abr_248_19
Chávez-Reyes, J., Escárcega-González, C.E., Chavira-Suárez, E., León-Buitimea, A., Vázquez-León, P., Morones-Ramírez, J.R., Villalón, C.M., Quintanar-Stephano, A., and Marichal-Cancino, B.A., 2021. Susceptibility for some infectious diseases in patients with diabetes: The key role of glycemia. DOI: https://doi.org/10.3389/fpubh.2021.559595
Front Public Health, 9, p.559595.
Chen, J., Xing, Y., Zhao, L., and Ma, H., 2019b. The association between Helicobacter pylori infection and glycated hemoglobin A in diabetes: A meta-analysis. Journal of Diabetes Research, 2019, p.3705264. DOI: https://doi.org/10.1155/2019/3705264
Chen, Y., Yang, C., You, N., and Zhang, J., 2023. Relationship between Helicobacter pylori and glycated hemoglobin: A cohort study. Frontiers in Cellular and Infection Microbiology, 13, p.1196338. DOI: https://doi.org/10.3389/fcimb.2023.1196338
Chen, Y.Y., Fang, W.H., Wang, C.C., Kao, T.W., Chang, Y.W., Wu, C.J., Zhou, Y.C., Sun, Y.S., and Chen, W.L., 2019a. Helicobacter pylori infection increases risk of incident metabolic syndrome and diabetes: A cohort study. PLoS One, 14, p.e0208913. DOI: https://doi.org/10.1371/journal.pone.0208913
Cheng, K.P., Yang, Y.J., Hung, H.C., Lin, C.H., Wu, C.T., Hung, M.H., Sheu, B.S., and Ou, H.Y., 2019. Helicobacter pylori eradication improves glycemic control in type 2 diabetes patients with asymptomatic active Helicobacter pylori infection. Journal of Diabetes Investigation, 10, pp.1092-1101. DOI: https://doi.org/10.1111/jdi.12991
Chey, W.D., 2000. Accurate diagnosis of Helicobacter pylori: 14C-Urea Breath test. Gastroenterology Clinics of North America, 29, pp.895-902. DOI: https://doi.org/10.1016/S0889-8553(05)70157-6
Cooke, F.J., 2022. Infections in people with diabetes. Medicine, 50, pp.729-732. DOI: https://doi.org/10.1016/j.mpmed.2022.08.006
Costa, L.C.M.C., Das Graças Carvalho, M., La Guárdia Custódio Pereira, A.C., Teixeira Neto, R.G., Andrade Figueiredo, L.C., and Barros-Pinheiro, M., 2024. Diagnostic methods for Helicobacter pylori. Medical Principles and Practice, 33, pp.173-184. DOI: https://doi.org/10.1159/000538349
Daryabor, G., Atashzar, M.R., Kabelitz, D., Meri, S., and Kalantar, K., 2020. The effects of type 2 diabetes mellitus on organ metabolism and the immune system. Frontiers in Immunology, 11, p.1582. DOI: https://doi.org/10.3389/fimmu.2020.01582
Dore, M.P., and Graham, D.Y., 2022. Modern approach to the diagnosis of Helicobacter pylori infection. Alimentary Pharmacology and Therapeutics, 55, pp.S14-S21. DOI: https://doi.org/10.1111/apt.16566
Hooi, J.K., Lai, W.Y., Ng, W.K., Suen, M.M., Underwood, F.E., Tanyingoh, D., Malfertheiner, P., Graham, D.Y., Wong, V.W., and Wu, J.C., 2017. Global prevalence of Helicobacter pylori infection: Systematic review and meta-analysis. Gastroenterology, 153, pp.420-429. DOI: https://doi.org/10.1053/j.gastro.2017.04.022
Hosseininasab Nodoushan, S.A., and Nabavi, A., 2019. The interaction of Helicobacter pylori infection and type 2 diabetes mellitus. Advanced Biomedical Research, 8, p.15. DOI: https://doi.org/10.4103/abr.abr_37_18
Kouitcheu Mabeku, L.B., Noundjeu Ngamga, M.L., and Leundji, H., 2020. Helicobacter pylori infection, a risk factor for Type 2 diabetes mellitus: A hospital-based cross-sectional study among dyspeptic patients in Douala-Cameroon. Scientific Reports, 10, p.12141. DOI: https://doi.org/10.1038/s41598-020-69208-3
Li, Y., Choi, H., Leung, K., Jiang, F., Graham, D.Y., and Leung, W.K., 2023. Global prevalence of Helicobacter pylori infection between 1980 and 2022: A systematic review and meta-analysis. Lancet Gastroenterol Hepatol, 8, pp.553-564. DOI: https://doi.org/10.1016/S2468-1253(23)00070-5
Liu, J., Bai, R., Chai, Z., Cooper, M.E., Zimmet, P.Z., and Zhang, L., 2022. Low-and middle-income countries demonstrate rapid growth of type 2 diabetes: An analysis based on Global Burden of Disease 1990-2019 data. Diabetologia, 65, pp.1339-1352. DOI: https://doi.org/10.1007/s00125-022-05713-6
Lovic, D., Piperidou, A., Zografou, I., Grassos, H., Pittaras, A., and Manolis, A., 2020. The growing epidemic of diabetes mellitus. Current Vascular Pharmacology, 18, pp.104-109. DOI: https://doi.org/10.2174/1570161117666190405165911
Malfertheiner, P., Camargo, M.C., El-Omar, E., Liou, J.M., Peek, R., Schulz, C., Smith, S.I., and Suerbaum, S., 2023. Helicobacter pylori infection. Nature Reviews Disease Primers, 9, p.19. DOI: https://doi.org/10.1038/s41572-023-00431-8
Maluf, S., Salgado, J.V., Cysne, D.N., Camelo, D.M.F., Nascimento, J.R., Maluf, B.V.T., Silva, L.D.M., Belfort, M.R.C., Silva, L.A., and Guerra, R.N.M., 2020. Increased glycated hemoglobin levels in patients with Helicobacter pylori infection are associated with the grading of chronic gastritis. Frontiers in Immunology, 11, p.2121. DOI: https://doi.org/10.3389/fimmu.2020.02121
Man, S., Ma, Y., Jin, C., Lv, J., Tong, M., Wang, B., Li, L., and Ning, Y., 2020. Association between Helicobacter pylori infection and diabetes: A cross-sectional study in China. Journal of Diabetes Research, 2020, p.7201379. DOI: https://doi.org/10.1155/2020/7201379
Mansori, K., Moradi, Y., Naderpour, S., Rashti, R., Moghaddam, A.B., Saed, L., and Mohammadi, H. 2020. Helicobacter pylori infection as a risk factor for diabetes: A meta-analysis of case-control studies. BMC Gastroenterology, 20, p.77. DOI: https://doi.org/10.1186/s12876-020-01223-0
Martin-Nuñez, G.M., Cornejo-Pareja, I., Clemente-Postigo, M., and Tinahones, F.J., 2021. Gut microbiota: The missing link between Helicobacter pylori infection and metabolic disorders? Frontiers in Endocrinology, 12, p.639856. DOI: https://doi.org/10.3389/fendo.2021.639856
Pyo, J.H., Lee, H., Choi, S.C., Cho, S.J., Choi, Y.H., Min, Y.W., Min, B.H., Lee, J.H., Yoo, H., Kim, K., and Kim, J.J., 2019. Lack of association between past Helicobacter pylori infection and diabetes: A two-cohort study. Nutrients, 11, p.1874. DOI: https://doi.org/10.3390/nu11081874
Ren, S., Cai, P., Liu, Y., Wang, T., Zhang, Y., Li, Q., Gu, Y., Wei, L., Yan, C., and Jin, G., 2022. Prevalence of Helicobacter pylori infection in China: Asystematic review and meta‐analysis. Journal of Gastroenterology and Hepatology, 37, pp.464-470. DOI: https://doi.org/10.1111/jgh.15751
Sabbagh, P., Mohammadnia-Afrouzi, M., Javanian, M., Babazadeh, A., Koppolu, V., Vasigala, V.R., Nouri, H.R., and Ebrahimpour, S., 2019. Diagnostic methods for Helicobacter pylori infection: Ideals, options, and limitations. European Journal of Clinical Microbiology and Infectious Diseases, 38, pp.55-66. DOI: https://doi.org/10.1007/s10096-018-3414-4
Shah, S.C., Halvorson, A.E., Lee, D., Bustamante, R., McBay, B., Gupta, R., Denton, J., Dorn, C., Wilson, O., and Peek, R Jr., 2024. Helicobacter pylori burden in the United States according to individual demographics and geography: A nationwide analysis of the Veterans Healthcare System. Clinical DOI: https://doi.org/10.1016/j.cgh.2023.05.016
Gastroenterology and Hepatology, 22, pp.42-50, e26.
Sharndama, H.C., and Mba, I.E., 2022. Helicobacter pylori: An up-to-date overview on the virulence and pathogenesis mechanisms. Brazilian Journal of Microbiology, 53, pp.33-50. DOI: https://doi.org/10.1007/s42770-021-00675-0
Shi, Y., Duan, J.Y., Liu, D.W., Qiao, Y.J., Han, Q.X., Pan, S.K., Tang, L., Cai, G.Y., Chen, X.M., Liu, Z.S., and Zhu, H.Y., 2018. Helicobacter pylori infection is associated with occurrence of proteinuria in type 2 diabetes patients: Asystemic review and meta-analysis. Chinese Medical Journal, 131, pp.2734-2740. DOI: https://doi.org/10.4103/0366-6999.245269
Singh, R., Zogg, H., Wei, L., Bartlett, A., Ghoshal, U.C., Rajender, S., and Ro, S., 2021. Gut microbial dysbiosis in the pathogenesis of gastrointestinal dysmotility and metabolic disorders. Journal of Neurogastroenterology and Motility, 27, p.19. DOI: https://doi.org/10.5056/jnm20149
Song, X., Cai, C., Jin, Q., Chen, X., and Yu, C., 2021. The efficacy of Helicobacter pylori eradication in diabetics and its effect on glycemic control: A systematic review and meta‐analysis. Helicobacter, 26, p.e12781. DOI: https://doi.org/10.1111/hel.12781
Talebi Bezmin Abadi, A., 2018. Diagnosis of Helicobacter pylori using invasive and noninvasive approaches. Journal of Pathogens, 2018, p.9064952. DOI: https://doi.org/10.1155/2018/9064952
Tamura, T., Morita, E., Kawai, S., Sasakabe, T., Sugimoto, Y., Fukuda, N., Suma, S., Nakagawa, H., Okada, R., and Hishida, A., 2015. No association between Helicobacter pylori infection and diabetes mellitus among a general Japanese population: A cross-sectional study. Springerplus, 4, pp.1-7. DOI: https://doi.org/10.1186/s40064-015-1371-2
Thrift, A.P., and El-Serag, H.B., 2020. Burden of gastric cancer. Clinical Gastroenterology and Hepatology, 18, pp.534-542. DOI: https://doi.org/10.1016/j.cgh.2019.07.045
Toniolo, A., Cassani, G., Puggioni, A., Rossi, A., Colombo, A., Onodera, T., and Ferrannini, E., 2019. The diabetes pandemic and associated infections: Suggestions for clinical microbiology. Reviews in Medical Microbiology, 30, p.1. DOI: https://doi.org/10.1097/MRM.0000000000000155
Uemura, N., Okamoto, S., Yamamoto, S., Matsumura, N., Yamaguchi, S., Yamakido, M., Taniyama, K., Sasaki, N., and Schlemper, R.J., 2001. Helicobacter pylori infection and the development of gastric cancer. New England Journal of Medicine, 345, pp.784-789. DOI: https://doi.org/10.1056/NEJMoa001999
Wada, Y., Hamamoto, Y., Kawasaki, Y., Honjo, S., Fujimoto, K., Tatsuoka, H., Matsuoka, A., Ikeda, H., Fujikawa, J., and Koshiyama, H., 2013. The eradication of Helicobacter pylori does not affect glycemic control in Japanese subjects with type 2 diabetes. Japanese Clinical Medicine, 4, p.41-43. DOI: https://doi.org/10.4137/JCM.S10828
Wan, Z., Song, L., Hu, L., Hu, M., Lei, X., Huang, Y., and Lv, Y., 2020. Helicobacter pylori infection is associated with diabetes among Chinese adults.Journal of Diabetes Investigation, 11, pp.199-205. DOI: https://doi.org/10.1111/jdi.13102
Xia, H.H., Talley, N.J., Kam, E.P., Young, L.J., Hammer, J., and Horowitz, M., 2001. Helicobacter pylori infection is not associated with diabetes mellitus, nor with upper gastrointestinal symptoms in diabetes mellitus. American Journal of Gastroenterology, 96, pp.1039-1046. DOI: https://doi.org/10.1111/j.1572-0241.2001.03604.x
Ye, J., Wu, Y., Yang, S., Zhu, D., Chen, F., Chen, J., Ji, X., and Hou, K., 2023. The global, regional and national burden of type 2 diabetes mellitus in the past, present and future: A systematic analysis of the global burden of disease study 2019. Frontiers in Endocrinology, 14, p.1192629. DOI: https://doi.org/10.3389/fendo.2023.1192629
Zang, H., Wang, J., Wang, H., Guo, J., Li, Y., Zhao, Y., Song, J., Liu, F., Liu, X., and Zhao, Y., 2023. Metabolic alterations in patients with Helicobacter pylori‐related gastritis: The H. pylori‐gut microbiota‐metabolism axis in progression of the chronic inflammation in the gastric mucosa. Helicobacter, p.e12984. DOI: https://doi.org/10.1111/hel.12984
Zhou, J., Wang, X., Liu, K., and Chen, K., 2022. Association between Helicobacter pylori infection and the risk of type 2 diabetes mellitus based on a middle-aged and elderly Chinese population. Endocrine Journal, 69, pp.839-846. DOI: https://doi.org/10.1507/endocrj.EJ21-0591
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