Chen JG , Zhang SW , 2011. Liver cancer epidemic in China: past, present and future. Semin Cancer Biol 21: 59–69.
Nishikawa H , Osaki Y , 2015. Liver cirrhosis: evaluation, nutritional status, and prognosis. Mediators Inflamm 2015: 872152.
Paik JM , Golabi P , Younossi Y , Srishord M , Mishra A , Younossi ZM , 2020. The growing burden of disability related to nonalcoholic fatty liver disease: data from the global burden of disease 2007–2017. Hepatol Commun 4: 1769–1780.
Deeb A , Attia S , Mahmoud S , Elhaj G , Elfatih A , 2018. Dyslipidemia and fatty liver disease in overweight and obese children. J Obes 2018: 8626818.
Farooq MO , Bataller R , 2016. Pathogenesis and management of alcoholic liver disease. Dig Dis 34: 347–355.
Nishikawa H , Yoh K , Enomoto H , Iwata Y , Nishimura T , Nishiguchi S , Iijima H , 2020. Frailty and sleep disorder in chronic liver diseases. Life (Basel) 10: 137.
Novo-Veleiro I , Alvela-Suarez L , Chamorro AJ , Gonzalez-Sarmiento R , Laso FJ , Marcos M , 2016. Alcoholic liver disease and hepatitis C virus infection. World J Gastroenterol 22: 1411–1420.
Seto W-K , Lo Y-R , Pawlotsky J-M , Yuen M-F , 2018. Chronic hepatitis B virus infection. Lancet 392: 2313–2324.
Go MF , 2002. Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther 16 (Suppl 1):3–15.
Leja M , Grinberga-Derica I , Bilgilier C , Steininger C , 2019. Review: epidemiology of Helicobacter pylori infection. Helicobacter 24 (Suppl 1 ):e12635.
Burucoa C , Axon A , 2017. Epidemiology of Helicobacter pylori infection. Helicobacter 22 (Suppl 1 ):e12403.
Correa P , Piazuelo MB , 2012. The gastric precancerous cascade. J Dig Dis 13: 2–9.
Goo MJ et al., 2009. Helicobacter pylori promotes hepatic fibrosis in the animal model. Lab Invest 89: 1291–1303.
Okushin K , Tsutsumi T , Ikeuchi K , Kado A , Enooku K , Fujinaga H , Moriya K , Yotsuyanagi H , Koike K , 2018. Helicobacter pylori infection and liver diseases: epidemiology and insights into pathogenesis. World J Gastroenterol 24: 3617–3625.
Tahashi Y , Matsuzaki K , Date M , Yoshida K , Furukawa F , Sugano Y , Matsushita M , Himeno Y , Inagaki Y , Inoue K , 2002. Differential regulation of TGF-beta signal in hepatic stellate cells between acute and chronic rat liver injury. Hepatology 35: 49–61.
Wang J , Chen RC , Zheng YX , Zhao SS , Li N , Zhou RR , Huang Y , Huang ZB , Fan XG , 2016. Helicobacter pylori infection may increase the risk of progression of chronic hepatitis B disease among the Chinese population: a meta-analysis. Int J Infect Dis 50: 30–37.
Baeg MK , Yoon SK , Ko SH , Noh YS , Lee IS , Choi MG , 2016. Helicobacter pylori infection is not associated with nonalcoholic fatty liver disease. World J Gastroenterol 22: 2592–2600.
Fan N , Peng L , Xia Z , Zhang L , Wang Y , Peng Y , 2018. Helicobacter pylori infection is not associated with non-alcoholic fatty liver disease: a cross-sectional study in China. Front Microbiol 9: 73.
Okushin K et al., 2015. Helicobacter pylori infection is not associated with fatty liver disease including non-alcoholic fatty liver disease: a large-scale cross-sectional study in Japan. BMC Gastroenterol 15: 25.
Wang MY , Yue JY , Zhang YX , Liu XD , Gao XZ , 2011. Helicobacter pylori infection in asymptomatic HBV carriers, alcohol users and normal adult population in Shandong Province, China. Clin Res Hepatol Gastroenterol 35: 560–562.
Rasool S , Abid S , Jafri W , 2007. Validity and cost comparison of 14carbon urea breath test for diagnosis of H. pylori in dyspeptic patients. World J Gastroenterol 13: 925–929.
Ahmed Z , Ahmed U , Walayat S , Ren J , Martin DK , Moole H , Koppe S , Yong S , Dhillon S , 2018. Liver function tests in identifying patients with liver disease. Clin Exp Gastroenterol 11: 301–307.
Green RM , Flamm S , 2002. AGA technical review on the evaluation of liver chemistry tests. Gastroenterology 123: 1367–1384.
Andria B et al., 2013. Biliverdin protects against liver ischemia reperfusion injury in swine. PLoS One 8: e69972.
Hamoud AR , Weaver L , Stec DE , Hinds TD Jr. , 2018. Bilirubin in the liver-gut signaling axis. Trends Endocrinol Metab 29: 140–150.
Seeff LB , Koff RS , Gretch DR , Nolte FS , Lott JA , Dufour DR , 2000. Diagnosis and monitoring of hepatic injury. I. Performance characteristics of laboratory tests. Clin Chem 46: 2027–2049.
Sterling RK et al., 2006. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology 43: 1317–1325.
Li Y , Chen Y , Zhao Y , 2014. The diagnostic value of the FIB-4 index for staging hepatitis B-related fibrosis: a meta-analysis. PLoS One 9: e105728.
Xu R , Wang J , Huang X , Zhang Q , Xie Y , Pang L , Bai L , Zhou J , 2019. Clinical value of spectral CT imaging combined with AFP in identifying liver cancer and hepatic focal nodular hyperplasia. J BUON 24: 1429–1434.
Zhao B , Sheng QJ , Qin Y , Wang XL , Zhao H , Zhao N , 2021. Correlations of Helicobacter pylori with liver function, inflammatory factors and serum levels of FoxP3 and RORgammat in patients with hepatitis B cirrhosis. Eur Rev Med Pharmacol Sci 25: 459–465.
Hanafy AS , El Hawary AT , Hamed EF , Hassaneen AM , 2016. Impact of Helicobacter pylori eradication on refractory thrombocytopenia in patients with chronic HCV awaiting antiviral therapy. Eur J Clin Microbiol Infect Dis 35: 1171–1176.
Chen C , Zhang C , Wang X , Zhang F , Zhang Z , Ma P , Feng S , 2020. Helicobacter pylori infection may increase the severity of nonalcoholic fatty liver disease via promoting liver function damage, glycometabolism, lipid metabolism, inflammatory reaction and metabolic syndrome. Eur J Gastroenterol Hepatol 32: 857–866.
Liu Y , Li D , Liu Y , Shuai P , 2021. Association between Helicobacter pylori infection and non-alcoholic fatty liver disease, hepatic adipose deposition and stiffness in southwest China. Front Med (Lausanne) 8: 764472.
Huang J , Cui J , 2017. Evaluation of Helicobacter pylori infection in patients with chronic hepatic disease. Chin Med J (Engl) 130: 149–154.
Abo-Amer YE , Sabal A , Ahmed R , Hasan NFE , Refaie R , Mostafa SM , Mohamed AA , Khalil M , Elagawy W , Abd-Elsalam S , 2020. Relationship between Helicobacter pylori infection and nonalcoholic fatty liver disease (NAFLD) in a developing country: a cross-sectional study. Diabetes Metab Syndr Obes 13: 619–625.
Wei L , Ding HG , 2021. Relationship between Helicobacter pylori infection and nonalcoholic fatty liver disease: what should we expect from a meta-analysis? Medicine (Baltimore) 100: e26706.
Waluga M , Kukla M , Zorniak M , Bacik A , Kotulski R , 2015. From the stomach to other organs: Helicobacter pylori and the liver. World J Hepatol 7: 2136–2146.
Figura N , 1996. Hypothesis: Helicobacter toxins and liver. Helicobacter 1: 187–189.
Tian XFFX , Fu CY , Huang Y , Zhu C , 2005. Experimental study on the pathological effect of Helicobacter pylori on liver tissues. Zhonghua Gan Zang Bing Za Zhi 13: 780–783.
Fukuda Y , Bamba H , Okui M , Tamura K , Tanida N , Satomi M , Shimoyama T , Nishigami T , 2001. Helicobacter pylori infection increases mucosal permeability of the stomach and intestine. Digestion 63 (Suppl 1 ):93–96.
Cai L , Zhang L , Liu A , Li S , Wang P , 2012. Prevalence, awareness, treatment, and control of dyslipidemia among adults in Beijing, China. J Atheroscler Thromb 19: 159–168.
Majka JRT , Konturek PC , Konturek SJ , Bielański W , Kowalsky M , Szczudlik A , 2002. Influence of chronic Helicobacter pylori infection on ischemic cerebral stroke risk factors. Med Sci Monit 8: CR675–CR684.
Alzahrani S , Nelson J , Moss SF , Paulus JK , Knowler WC , Pittas AG , Diabetes Prevention Program Research Group , 2017. H. pylori seroprevalence and risk of diabetes: an ancillary case-control study nested in the diabetes prevention program. J Diabetes Complications 31: 1515–1520.
Mostaza JM , Camino N , Gerique JG , Pena R , Baquero M , Lahoz C , 2005. C-reactive protein levels and prevalence of chronic infections in subjects with hypoalphalipoproteinemia. Metabolism 54: 33–37.
Gillum RF , 2004. Infection with Helicobacter pylori, coronary heart disease, cardiovascular risk factors, and systemic inflammation: the Third National Health and Nutrition Examination Survey. J Natl Med Assoc 96: 1470–1476.
Sotiropoulos A , Gikas A , Skourtis S , Merkouris P , Pentzeridis P , Polydorou A , Pappas S , 2006. Seropositivity to Chlamydia pneumoniae or Helicobacter pylori and coronary artery disease. Int J Cardiol 109: 420–421.
Woodward M , 2000. An investigation into factors associated with Helicobacter pylori infection. J Clin Epidemiol 53: 175–181.
Stahl EC , Haschak MJ , Popovic B , Brown BN , 2018. Macrophages in the aging liver and age-related liver disease. Front Immunol 9: 2795.
Lee J , Vali Y , Boursier J , Spijker R , Anstee QM , Bossuyt PM , Zafarmand MH , 2021. Prognostic accuracy of FIB-4, NAFLD fibrosis score and APRI for NAFLD-related events: a systematic review. Liver Int 41: 261–270.
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Abstract Views | 3855 | 2493 | 25 |
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Early prevention of liver injury by controlling risk factors deserves concern because of the heavy liver disease burden. Helicobacter pylori (HP) infection affects half of the world’s population and the relationship between it and early liver damage is unclear. This study focuses on assessing the correlation between them in the general population to provide clues to prevent liver disease. A total of 12,931 individuals underwent liver function and imaging tests as well as 13C/14C-urea breath tests. Results showed that the detection rate of HP was 35.9%, and the HP-positive group had a higher rate of liver injury (47.0% versus 44.5%, P = 0.007). Specifically, Fibrosis-4 (FIB-4) and alpha-fetoprotein levels in the HP-positive group were higher whereas the serum albumin level was lower. HP infection would raise the percentage of elevated aspartate aminotransferase (AST; 2.5% versus 1.7%, P = 0.006), elevated FIB-4 (20.2% versus 17.9%, P = 0.002), and abnormal liver imaging (31.0% versus 29.3%, P = 0.048). Most of these results remained stable after covariate adjustment but, for liver injury and liver imaging, the conclusions only held in young people (ORliver injury, odds ratio of liver injury, 1.127, P = 0.040; ORAST, 1.33, P = 0.034; ORFIB-4, 1.145, P = 0.032; ORimaging, 1.149, P = 0.043). Overall, HP infection might be associated with early liver injury, particularly in youth, suggesting that people with early liver injury should pay more attention to HP infection to prevent the occurrence of severe liver diseases.
These authors contributed equally to this work.
Authors’ addresses: Wenling Chang, Tingting Chen, Weigui Ni, and Zhihao Xie, Department of Epidemiology and Biostatistics, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, China, E-mails: whitneychang1201@outlook.com, tingtingchan@126.com, 2395711093@qq.com, and hlovml@163.com. Lin Cai and Juan Liao, Department of Gastroenterology, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, China, and Non-Communicable Diseases Research Center, West China-PUMC C. C. Chen Institute of Health, Sichuan University, Chengdu, China, E-mails: cloris58@126.com and juanliao@scu.edu.cn. Chunxia Yang, Department of Epidemiology and Biostatistics, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, China, and Non-Communicable Diseases Research Center, West China-Peking Union Medical College C. C. Chen Institute of Health, Sichuan University, Chengdu, China, E-mail: yangchunxia@scu.edu.cn.
Chen JG , Zhang SW , 2011. Liver cancer epidemic in China: past, present and future. Semin Cancer Biol 21: 59–69.
Nishikawa H , Osaki Y , 2015. Liver cirrhosis: evaluation, nutritional status, and prognosis. Mediators Inflamm 2015: 872152.
Paik JM , Golabi P , Younossi Y , Srishord M , Mishra A , Younossi ZM , 2020. The growing burden of disability related to nonalcoholic fatty liver disease: data from the global burden of disease 2007–2017. Hepatol Commun 4: 1769–1780.
Deeb A , Attia S , Mahmoud S , Elhaj G , Elfatih A , 2018. Dyslipidemia and fatty liver disease in overweight and obese children. J Obes 2018: 8626818.
Farooq MO , Bataller R , 2016. Pathogenesis and management of alcoholic liver disease. Dig Dis 34: 347–355.
Nishikawa H , Yoh K , Enomoto H , Iwata Y , Nishimura T , Nishiguchi S , Iijima H , 2020. Frailty and sleep disorder in chronic liver diseases. Life (Basel) 10: 137.
Novo-Veleiro I , Alvela-Suarez L , Chamorro AJ , Gonzalez-Sarmiento R , Laso FJ , Marcos M , 2016. Alcoholic liver disease and hepatitis C virus infection. World J Gastroenterol 22: 1411–1420.
Seto W-K , Lo Y-R , Pawlotsky J-M , Yuen M-F , 2018. Chronic hepatitis B virus infection. Lancet 392: 2313–2324.
Go MF , 2002. Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther 16 (Suppl 1):3–15.
Leja M , Grinberga-Derica I , Bilgilier C , Steininger C , 2019. Review: epidemiology of Helicobacter pylori infection. Helicobacter 24 (Suppl 1 ):e12635.
Burucoa C , Axon A , 2017. Epidemiology of Helicobacter pylori infection. Helicobacter 22 (Suppl 1 ):e12403.
Correa P , Piazuelo MB , 2012. The gastric precancerous cascade. J Dig Dis 13: 2–9.
Goo MJ et al., 2009. Helicobacter pylori promotes hepatic fibrosis in the animal model. Lab Invest 89: 1291–1303.
Okushin K , Tsutsumi T , Ikeuchi K , Kado A , Enooku K , Fujinaga H , Moriya K , Yotsuyanagi H , Koike K , 2018. Helicobacter pylori infection and liver diseases: epidemiology and insights into pathogenesis. World J Gastroenterol 24: 3617–3625.
Tahashi Y , Matsuzaki K , Date M , Yoshida K , Furukawa F , Sugano Y , Matsushita M , Himeno Y , Inagaki Y , Inoue K , 2002. Differential regulation of TGF-beta signal in hepatic stellate cells between acute and chronic rat liver injury. Hepatology 35: 49–61.
Wang J , Chen RC , Zheng YX , Zhao SS , Li N , Zhou RR , Huang Y , Huang ZB , Fan XG , 2016. Helicobacter pylori infection may increase the risk of progression of chronic hepatitis B disease among the Chinese population: a meta-analysis. Int J Infect Dis 50: 30–37.
Baeg MK , Yoon SK , Ko SH , Noh YS , Lee IS , Choi MG , 2016. Helicobacter pylori infection is not associated with nonalcoholic fatty liver disease. World J Gastroenterol 22: 2592–2600.
Fan N , Peng L , Xia Z , Zhang L , Wang Y , Peng Y , 2018. Helicobacter pylori infection is not associated with non-alcoholic fatty liver disease: a cross-sectional study in China. Front Microbiol 9: 73.
Okushin K et al., 2015. Helicobacter pylori infection is not associated with fatty liver disease including non-alcoholic fatty liver disease: a large-scale cross-sectional study in Japan. BMC Gastroenterol 15: 25.
Wang MY , Yue JY , Zhang YX , Liu XD , Gao XZ , 2011. Helicobacter pylori infection in asymptomatic HBV carriers, alcohol users and normal adult population in Shandong Province, China. Clin Res Hepatol Gastroenterol 35: 560–562.
Rasool S , Abid S , Jafri W , 2007. Validity and cost comparison of 14carbon urea breath test for diagnosis of H. pylori in dyspeptic patients. World J Gastroenterol 13: 925–929.
Ahmed Z , Ahmed U , Walayat S , Ren J , Martin DK , Moole H , Koppe S , Yong S , Dhillon S , 2018. Liver function tests in identifying patients with liver disease. Clin Exp Gastroenterol 11: 301–307.
Green RM , Flamm S , 2002. AGA technical review on the evaluation of liver chemistry tests. Gastroenterology 123: 1367–1384.
Andria B et al., 2013. Biliverdin protects against liver ischemia reperfusion injury in swine. PLoS One 8: e69972.
Hamoud AR , Weaver L , Stec DE , Hinds TD Jr. , 2018. Bilirubin in the liver-gut signaling axis. Trends Endocrinol Metab 29: 140–150.
Seeff LB , Koff RS , Gretch DR , Nolte FS , Lott JA , Dufour DR , 2000. Diagnosis and monitoring of hepatic injury. I. Performance characteristics of laboratory tests. Clin Chem 46: 2027–2049.
Sterling RK et al., 2006. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology 43: 1317–1325.
Li Y , Chen Y , Zhao Y , 2014. The diagnostic value of the FIB-4 index for staging hepatitis B-related fibrosis: a meta-analysis. PLoS One 9: e105728.
Xu R , Wang J , Huang X , Zhang Q , Xie Y , Pang L , Bai L , Zhou J , 2019. Clinical value of spectral CT imaging combined with AFP in identifying liver cancer and hepatic focal nodular hyperplasia. J BUON 24: 1429–1434.
Zhao B , Sheng QJ , Qin Y , Wang XL , Zhao H , Zhao N , 2021. Correlations of Helicobacter pylori with liver function, inflammatory factors and serum levels of FoxP3 and RORgammat in patients with hepatitis B cirrhosis. Eur Rev Med Pharmacol Sci 25: 459–465.
Hanafy AS , El Hawary AT , Hamed EF , Hassaneen AM , 2016. Impact of Helicobacter pylori eradication on refractory thrombocytopenia in patients with chronic HCV awaiting antiviral therapy. Eur J Clin Microbiol Infect Dis 35: 1171–1176.
Chen C , Zhang C , Wang X , Zhang F , Zhang Z , Ma P , Feng S , 2020. Helicobacter pylori infection may increase the severity of nonalcoholic fatty liver disease via promoting liver function damage, glycometabolism, lipid metabolism, inflammatory reaction and metabolic syndrome. Eur J Gastroenterol Hepatol 32: 857–866.
Liu Y , Li D , Liu Y , Shuai P , 2021. Association between Helicobacter pylori infection and non-alcoholic fatty liver disease, hepatic adipose deposition and stiffness in southwest China. Front Med (Lausanne) 8: 764472.
Huang J , Cui J , 2017. Evaluation of Helicobacter pylori infection in patients with chronic hepatic disease. Chin Med J (Engl) 130: 149–154.
Abo-Amer YE , Sabal A , Ahmed R , Hasan NFE , Refaie R , Mostafa SM , Mohamed AA , Khalil M , Elagawy W , Abd-Elsalam S , 2020. Relationship between Helicobacter pylori infection and nonalcoholic fatty liver disease (NAFLD) in a developing country: a cross-sectional study. Diabetes Metab Syndr Obes 13: 619–625.
Wei L , Ding HG , 2021. Relationship between Helicobacter pylori infection and nonalcoholic fatty liver disease: what should we expect from a meta-analysis? Medicine (Baltimore) 100: e26706.
Waluga M , Kukla M , Zorniak M , Bacik A , Kotulski R , 2015. From the stomach to other organs: Helicobacter pylori and the liver. World J Hepatol 7: 2136–2146.
Figura N , 1996. Hypothesis: Helicobacter toxins and liver. Helicobacter 1: 187–189.
Tian XFFX , Fu CY , Huang Y , Zhu C , 2005. Experimental study on the pathological effect of Helicobacter pylori on liver tissues. Zhonghua Gan Zang Bing Za Zhi 13: 780–783.
Fukuda Y , Bamba H , Okui M , Tamura K , Tanida N , Satomi M , Shimoyama T , Nishigami T , 2001. Helicobacter pylori infection increases mucosal permeability of the stomach and intestine. Digestion 63 (Suppl 1 ):93–96.
Cai L , Zhang L , Liu A , Li S , Wang P , 2012. Prevalence, awareness, treatment, and control of dyslipidemia among adults in Beijing, China. J Atheroscler Thromb 19: 159–168.
Majka JRT , Konturek PC , Konturek SJ , Bielański W , Kowalsky M , Szczudlik A , 2002. Influence of chronic Helicobacter pylori infection on ischemic cerebral stroke risk factors. Med Sci Monit 8: CR675–CR684.
Alzahrani S , Nelson J , Moss SF , Paulus JK , Knowler WC , Pittas AG , Diabetes Prevention Program Research Group , 2017. H. pylori seroprevalence and risk of diabetes: an ancillary case-control study nested in the diabetes prevention program. J Diabetes Complications 31: 1515–1520.
Mostaza JM , Camino N , Gerique JG , Pena R , Baquero M , Lahoz C , 2005. C-reactive protein levels and prevalence of chronic infections in subjects with hypoalphalipoproteinemia. Metabolism 54: 33–37.
Gillum RF , 2004. Infection with Helicobacter pylori, coronary heart disease, cardiovascular risk factors, and systemic inflammation: the Third National Health and Nutrition Examination Survey. J Natl Med Assoc 96: 1470–1476.
Sotiropoulos A , Gikas A , Skourtis S , Merkouris P , Pentzeridis P , Polydorou A , Pappas S , 2006. Seropositivity to Chlamydia pneumoniae or Helicobacter pylori and coronary artery disease. Int J Cardiol 109: 420–421.
Woodward M , 2000. An investigation into factors associated with Helicobacter pylori infection. J Clin Epidemiol 53: 175–181.
Stahl EC , Haschak MJ , Popovic B , Brown BN , 2018. Macrophages in the aging liver and age-related liver disease. Front Immunol 9: 2795.
Lee J , Vali Y , Boursier J , Spijker R , Anstee QM , Bossuyt PM , Zafarmand MH , 2021. Prognostic accuracy of FIB-4, NAFLD fibrosis score and APRI for NAFLD-related events: a systematic review. Liver Int 41: 261–270.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 3855 | 2493 | 25 |
Full Text Views | 1060 | 55 | 0 |
PDF Downloads | 295 | 25 | 0 |