A study of the association between <em>Helicobacter pylori</em> infection type and pancreatic cancer risk: A systematic review and meta‑analysis

Qin,Chao; Xu,Chonghe; Zhu,Zhongqi; Song,Xixi; Wang,Xin; Xu,Wei; Zhu,Mei

doi:10.3892/ol.2025.14920

A study of the association between Helicobacter pylori infection type and pancreatic cancer risk: A systematic review and meta‑analysis

Authors:
- Chao Qin
- Chonghe Xu
- Zhongqi Zhu
- Xixi Song
- Xin Wang
- Wei Xu
- Mei Zhu
View Affiliations

Affiliations: Department of Clinical Laboratory, The Affiliated Chaohu Hospital of Anhui Medical University, Chaohu, Anhui 238000, P.R. China, School of Basic Medical Sciences, Capital Medical University, Beijing 100069, P.R. China, Department of Blood Transfusion, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui 230022, P.R. China
Published online on: February 7, 2025 https://doi.org/10.3892/ol.2025.14920
Article Number: 174
Copyright: © Qin et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Pancreatic cancer is a highly invasive malignant tumor with a complex pathogenesis that makes early diagnosis challenging. The potential association between Helicobacter pylori infection and pancreatic cancer risk has been noted; however, the available results are still highly divergent. The aim of the present study was to systematically evaluate the association between different types of H. pylori infection and pancreatic cancer risk as well as to explore the possible causes. A systematic search was conducted using the PubMed, Embase and Cochrane Library databases up to August 2023. The literature quality was evaluated using the Newcastle‑Ottawa Scale. All studies that met the criteria were included in the overall meta‑analysis to calculate the odds ratios (ORs) and corresponding 95% confidence intervals (CIs). In addition, subgroup analyses were performed based on factors such as diagnostic criteria for H. pylori infection, study region, type of study design and CagA status. The effect of publication bias on the quantitative synthesis results was assessed using the trim‑and‑fill analysis, and sensitivity analyses were used to verify the robustness of the quantitative synthesis results. A total of 17 studies involving 67,910 participants, including 64,372 controls and 3,538 patients with pancreatic cancer, were included in the present study. The overall analysis showed that no significant association was observed between H. pylori infection and pancreatic cancer risk (OR, 1.15; 95% CI, 0.93‑1.41). Further subgroup analyses, which did not consider the effects of study quality, diagnostic criteria, geographical distribution and the type of study design, did not produce new findings that contradicted the results of the overall analysis. CagA⁺ H. pylori infection did not significantly affect the risk of pancreatic cancer (OR, 0.95; 95% CI, 0.78‑1.16), whereas CagA^‑ H. pylori infection may be a possible risk factor for pancreatic cancer (OR, 1.24; 95% CI, 1.004‑1.541). The H. pylori infection did not significantly increase the risk of pancreatic cancer. However, it is noteworthy that CagA^‑ H. pylori infection could be a potential factor that elevated the risk of pancreatic cancer.

View Figures

View References

1	Crowe SE: Helicobacter pylori infection. N Engl J Med. 380:1158–1165. 2019. View Article : Google Scholar : PubMed/NCBI
2	Marshall BJ and Warren JR: Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1:1311–1315. 1984. View Article : Google Scholar : PubMed/NCBI
3	Wang W, Cui Y, Wei X, Zang Y, Chen X, Cheng L and Wang X: CuCo₂O₄ nanoflowers with multiple enzyme activities for treating bacterium-infected wounds via cuproptosis-like death. ACS Nano. 18:15845–15863. 2024. View Article : Google Scholar : PubMed/NCBI
4	Xing J, Shan J, Xue H, Zhang H, Cheng L, Hao J and Wang X: Multifunctional adaptable injectable TiN-based hydrogels for antitumor and antidrug-resistant bacterial therapy. Adv Healthc Mater. 13:e24002972024. View Article : Google Scholar : PubMed/NCBI
5	Hu Z, Shan J, Jin X, Sun W, Cheng L, Chen XL and Wang X: Nanoarchitectonics of in situ antibiotic-releasing acicular nanozymes for targeting and inducing cuproptosis-like death to eliminate drug-resistant bacteria. ACS Nano. 18:24327–24349. 2024. View Article : Google Scholar : PubMed/NCBI
6	Peek RM Jr and Blaser MJ: Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2:28–37. 2002. View Article : Google Scholar : PubMed/NCBI
7	Malfertheiner P, Megraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, et al: Management of helicobacter pylori infection-the maastricht V/Florence consensus report. Gut. 66:6–30. 2017. View Article : Google Scholar : PubMed/NCBI
8	Zhang C, Chen Y, Long Y, Zheng H, Jing J and Pan W: Helicobacter pylori and gastrointestinal cancers: Recent advances and controversies. Clin Med Insights Oncol. 18:117955492412346372024. View Article : Google Scholar : PubMed/NCBI
9	Vincent A, Herman J, Schulick R, Hruban RH and Goggins M: Pancreatic cancer. Lancet. 378:607–620. 2011. View Article : Google Scholar : PubMed/NCBI
10	Stoffel EM, Brand RE and Goggins M: Pancreatic cancer: Changing epidemiology and new approaches to risk assessment, early detection, and prevention. Gastroenterology. 164:752–765. 2023. View Article : Google Scholar : PubMed/NCBI
11	Bray F, Laversanne M, Sung H, Ferlay J, Siegel RL, Soerjomataram I and Jemal A: Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 74:229–263. 2024. View Article : Google Scholar : PubMed/NCBI
12	Whitcomb DC, Shelton CA and Brand RE: Genetics and genetic testing in pancreatic cancer. Gastroenterology. 149:1252–1264.e4. 2015. View Article : Google Scholar : PubMed/NCBI
13	Klein AP: Pancreatic cancer epidemiology: Understanding the role of lifestyle and inherited risk factors. Nat Rev Gastroenterol Hepatol. 18:493–502. 2021. View Article : Google Scholar : PubMed/NCBI
14	Bosetti C, Lucenteforte E, Silverman DT, Petersen G, Bracci PM, Ji BT, Negri E, Li D, Risch HA, Olson SH, et al: Cigarette smoking and pancreatic cancer: An analysis from the international pancreatic cancer case-control consortium (Panc4). Ann Oncol. 23:1880–1888. 2012. View Article : Google Scholar : PubMed/NCBI
15	Franceschi F, Tortora A, Gasbarrini G and Gasbarrini A: Helicobacter pylori and extragastric diseases. Helicobacter. 19 (Suppl 10):S52–S58. 2014. View Article : Google Scholar
16	Huang J, Zagai U, Hallmans G, Nyrén O, Engstrand L, Stolzenberg-Solomon R, Duell EJ, Overvad K, Katzke VA, Kaaks R, et al: Helicobacter pylori infection, chronic corpus atrophic gastritis and pancreatic cancer risk in the European prospective investigation into cancer and nutrition (EPIC) cohort: A nested case-control study. Int J Cancer. 140:1727–1735. 2017. View Article : Google Scholar : PubMed/NCBI
17	Risch HA, Yu H, Lu L and Kidd MS: ABO blood group, Helicobacter pylori seropositivity, and risk of pancreatic cancer: A case-control study. J Natl Cancer Inst. 102:502–505. 2010. View Article : Google Scholar : PubMed/NCBI
18	Xiao M, Wang Y and Gao Y: Association between Helicobacter pylori infection and pancreatic cancer development: A meta-analysis. PLoS One. 8:e755592013. View Article : Google Scholar : PubMed/NCBI
19	Zhou BG, Mei YZ, Wang JS, Xia JL, Jiang X, Ju SY and Ding YB: Is Helicobacter pylori infection associated with pancreatic cancer? A systematic review and meta-analysis of observational studies. Ther Adv Chronic Dis. 14:204062232311551192023. View Article : Google Scholar : PubMed/NCBI
20	Schulte A, Pandeya N, Fawcett J, Fritschi L, Risch HA, Webb PM, Whiteman DC and Neale RE: Association between Helicobacter pylori and pancreatic cancer risk: A meta-analysis. Cancer Causes Control. 26:1027–1035. 2015. View Article : Google Scholar : PubMed/NCBI
21	Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, et al: The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ. 372:n712021. View Article : Google Scholar : PubMed/NCBI
22	Stang A: Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 25:603–605. 2010. View Article : Google Scholar : PubMed/NCBI
23	Higgins JP and Thompson SG: Quantifying heterogeneity in a meta-analysis. Stat Med. 21:1539–1558. 2002. View Article : Google Scholar : PubMed/NCBI
24	Begg CB and Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics. 50:1088–1101. 1994. View Article : Google Scholar : PubMed/NCBI
25	Egger M, Smith GD, Schneider M and Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ. 315:629–634. 1997. View Article : Google Scholar : PubMed/NCBI
26	Duval S and Tweedie R: Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 56:455–463. 2000. View Article : Google Scholar : PubMed/NCBI
27	Stolzenberg-Solomon RZ, Blaser MJ, Limburg PJ, Perez-Perez G, Taylor PR, Virtamo J and Albanes D; ATBC Study, : Helicobacter pylori seropositivity as a risk factor for pancreatic cancer. J Natl Cancer Inst. 93:937–941. 2001. View Article : Google Scholar : PubMed/NCBI
28	Lee AA, Wang QL, Kim J, Babic A, Zhang X, Perez K, Ng K, Nowak J, Rifai N, Sesso HD, et al: Helicobacter pylori seropositivity, ABO blood type, and pancreatic cancer risk from 5 prospective cohorts. Clin Transl Gastroenterol. 14:e005732023. View Article : Google Scholar : PubMed/NCBI
29	Risch HA, Lu L, Kidd MS, Wang J, Zhang W, Ni Q, Gao YT and Yu H: Helicobacter pylori seropositivities and risk of pancreatic carcinoma. Cancer Epidemiol Biomarkers Prev. 23:172–178. 2014. View Article : Google Scholar : PubMed/NCBI
30	de Martel C, Llosa AE, Friedman GD, Vogelman JH, Orentreich N, Stolzenberg-Solomon RZ and Parsonnet J: Helicobacter pylori infection and development of pancreatic cancer. Cancer Epidemiol Biomarkers Prev. 17:1188–1194. 2008. View Article : Google Scholar : PubMed/NCBI
31	Permuth JB, Rahman S, Chen DT, Waterboer T and Giuliano AR: A case control study of the seroprevalence of helicobacter pylori proteins and their association with pancreatic cancer risk. J Pancreat Cancer. 7:57–64. 2021. View Article : Google Scholar : PubMed/NCBI
32	Hirabayashi M, Inoue M, Sawada N, Saito E, Abe SK, Hidaka A, Iwasaki M, Yamaji T, Shimazu T and Tsugane S: Helicobacter pylori infection, atrophic gastritis, and risk of pancreatic cancer: A population-based cohort study in a large Japanese population: The JPHC study. Sci Rep. 9:60992019. View Article : Google Scholar : PubMed/NCBI
33	Raderer M, Wrba F, Kornek G, Maca T, Koller DY, Weinlaender G, Hejna M and Scheithauer W: Association between Helicobacter pylori infection and pancreatic cancer. Oncology. 55:16–19. 1998. View Article : Google Scholar : PubMed/NCBI
34	Lindkvist B, Johansen D, Borgström A and Manjer J: A prospective study of Helicobacter pylori in relation to the risk for pancreatic cancer. BMC Cancer. 8:3212008. View Article : Google Scholar : PubMed/NCBI
35	Ai F, Hua X, Liu Y, Lin J and Feng Z: Preliminary study of pancreatic cancer associated with Helicobacter pylori infection. Cell Biochem Biophys. 71:397–400. 2015. View Article : Google Scholar : PubMed/NCBI
36	Hsu WY, Lin CH, Lin CC, Sung FC, Hsu CP and Kao CH: The relationship between Helicobacter pylori and cancer risk. Eur J Intern Med. 25:235–240. 2014. View Article : Google Scholar : PubMed/NCBI
37	Chen XZ, Schöttker B, Castro FA, Chen H, Zhang Y, Holleczek B and Brenner H: Association of helicobacter pylori infection and chronic atrophic gastritis with risk of colonic, pancreatic and gastric cancer: A ten-year follow-up of the ESTHER cohort study. Oncotarget. 7:17182–17193. 2016. View Article : Google Scholar : PubMed/NCBI
38	Shimoyama T, Takahashi R, Abe D, Mizuki I, Endo T and Fukuda S: Serological analysis of Helicobacter hepaticus infection in patients with biliary and pancreatic diseases. J Gastroenterol Hepatol. 25 (Suppl 1):S86–S89. 2010. View Article : Google Scholar : PubMed/NCBI
39	Laya GB, Anandhi A, Gurushankari B, Mandal J and Kate V: Association between helicobacter pylori and periampullary and pancreatic cancer: A case-control study. J Gastrointest Cancer. 53:902–907. 2022. View Article : Google Scholar : PubMed/NCBI
40	Osaki T, Lin Y, Sasahira N, Ueno M, Yonezawa H, Hojo F, Okuda M, Matsuyama M, Sasaki T, Kobayashi S, et al: Prevalence estimates of helicobacter species infection in pancreatic and biliary tract cancers. Helicobacter. 27:e128662022. View Article : Google Scholar : PubMed/NCBI
41	Yu G, Murphy G, Michel A, Weinstein SJ, Männistö S, Albanes D, Pawlita M and Stolzenberg-Solomon RZ: Seropositivity to Helicobacter pylori and risk of pancreatic cancer. Cancer Epidemiol Biomarkers Prev. 22:2416–2419. 2013. View Article : Google Scholar : PubMed/NCBI
42	Chen Sackett DL, Rosenberg WM, Gray JA, Haynes RB and Richardson WS: Evidence based medicine: What it is and what it isn't. BMJ. 312:71–72. 1996. View Article : Google Scholar : PubMed/NCBI
43	Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P and Schünemann HJ; GRADE Working Group, : GRADE: An emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 336:924–926. 2008. View Article : Google Scholar : PubMed/NCBI
44	Trikudanathan G, Philip A, Dasanu CA and Baker WL: Association between Helicobacter pylori infection and pancreatic cancer. A cumulative meta-analysis. JOP. 12:26–31. 2011.PubMed/NCBI
45	Liu H, Chen YT and Wang R XZ: Helicobacter pylori infection, atrophic gastritis, and pancreatic cancer risk: A meta-analysis of prospective epidemiologic studies. Medicine (Baltimore). 96:e781112017.
46	Cover TL and Blanke SR: Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol. 3:320–332. 2005. View Article : Google Scholar : PubMed/NCBI
47	Necchi V, Sommi P, Vanoli A, Fiocca R, Ricci V and Solcia E: Natural history of Helicobacter pylori VacA toxin in human gastric epithelium in vivo: Vacuoles and beyond. Sci Rep. 7:145262017. View Article : Google Scholar : PubMed/NCBI
48	Posselt G, Backert S and Wessler S: The functional interplay of Helicobacter pylori factors with gastric epithelial cells induces a multi-step process in pathogenesis. Cell Commun Signal. 11:772013. View Article : Google Scholar : PubMed/NCBI
49	Jiménez-Soto LF and Haas R: The CagA toxin of Helicobacter pylori: Abundant production but relatively low amount translocated. Sci Rep. 6:232272016. View Article : Google Scholar : PubMed/NCBI
50	Sierra JC, Piazuelo MB, Luis PB, Barry DP, Allaman MM, Asim M, Sebrell TA, Finley JL, Rose KL, Hill S, et al: Spermine oxidase mediates Helicobacter pylori-induced gastric inflammation, DNA damage, and carcinogenic signaling. Oncogene. 39:4465–4474. 2020. View Article : Google Scholar : PubMed/NCBI
51	Chaturvedi R, de Sablet T, Asim M, Piazuelo MB, Barry DP, Verriere TG, Sierra JC, Hardbower DM, Delgado AG, Schneider BG, et al: Increased Helicobacter pylori-associated gastric cancer risk in the Andean region of Colombia is mediated by spermine oxidase. Oncogene. 34:3429–3440. 2015. View Article : Google Scholar : PubMed/NCBI
52	Gobert AP, Al-Greene NT, Singh K, Coburn LA, Sierra JC, Verriere TG, Luis PB, Schneider C, Asim M, Allaman MM, et al: Distinct immunomodulatory effects of spermine oxidase in colitis induced by epithelial injury or infection. Front Immunol. 9:12422018. View Article : Google Scholar : PubMed/NCBI
53	Liu J, Xiao Q, Xiao J, Niu C, Li Y, Zhang X, Zhou Z, Shu G and Yin G: Wnt/β-catenin signalling: Function, biological mechanisms, and therapeutic opportunities. Signal Transduct Target Ther. 7:32022. View Article : Google Scholar : PubMed/NCBI
54	Yu F, Yu C, Li F, Zuo Y, Wang Y, Yao L, Wu C, Wang C and Ye L: Wnt/β-catenin signaling in cancers and targeted therapies. Signal Transduct Target Ther. 6:3072021. View Article : Google Scholar : PubMed/NCBI
55	Yong X, Tang B, Xiao YF, Xie R, Qin Y, Luo G, Hu CJ, Dong H and Yang SM: Helicobacter pylori upregulates Nanog and Oct4 via Wnt/β-catenin signaling pathway to promote cancer stem cell-like properties in human gastric cancer. Cancer Lett. 374:292–303. 2016. View Article : Google Scholar : PubMed/NCBI
56	Peng R, Xu C, Zhang L, Liu X, Peng D, Chen X, Liu D and Li R: M2 macrophages participate in ILC2 activation induced by Helicobacter pylori infection. Gut Microbes. 16:23470252024. View Article : Google Scholar : PubMed/NCBI
57	Cassetta L and Pollard JW: Targeting macrophages: Therapeutic approaches in cancer. Nat Rev Drug Discov. 17:887–904. 2018. View Article : Google Scholar : PubMed/NCBI
58	Guo X, Zhao Y, Yan H, Yang Y, Shen S, Dai X, Ji X, Ji F, Gong XG, Li L, et al: Single tumor-initiating cells evade immune clearance by recruiting type II macrophages. Genes Dev. 31:247–259. 2017. View Article : Google Scholar : PubMed/NCBI
59	Doak GR, Schwertfeger KL and Wood DK: Distant relations: Macrophage functions in the metastatic niche. Trends Cancer. 4:445–459. 2018. View Article : Google Scholar : PubMed/NCBI
60	Hardbower DM, de Sablet T, Chaturvedi R and Wilson KT: Chronic inflammation and oxidative stress: The smoking gun for Helicobacter pylori-induced gastric cancer? Gut Microbes. 4:475–481. 2013. View Article : Google Scholar : PubMed/NCBI
61	Davies GR, Banatvala N, Collins CE, Sheaff MT, Abdi Y, Clements L and Rampton DS: Relationship between infective load of Helicobacter pylori and reactive oxygen metabolite production in antral mucosa. Scand J Gastroenterol. 29:419–424. 1994. View Article : Google Scholar : PubMed/NCBI
62	Bagchi D, Bhattacharya G and Stohs SJ: Production of reactive oxygen species by gastric cells in association with Helicobacter pylori. Free Radic Res. 24:439–450. 1996. View Article : Google Scholar : PubMed/NCBI
63	Granger DN and Kvietys PR: Reperfusion injury and reactive oxygen species: The evolution of a concept. Redox Biol. 6:524–551. 2015. View Article : Google Scholar : PubMed/NCBI
64	Franco R and Vargas MR: Redox biology in neurological function, dysfunction, and aging. Antioxid Redox Signal. 28:1583–1586. 2018. View Article : Google Scholar : PubMed/NCBI
65	Moloney JN and Cotter TG: ROS signalling in the biology of cancer. Semin Cell Dev Biol. 80:50–64. 2018. View Article : Google Scholar : PubMed/NCBI
66	Srinivas US, Tan BWQ, Vellayappan BA and Jeyasekharan AD: ROS and the DNA damage response in cancer. Redox Biol. 25:1010842019. View Article : Google Scholar : PubMed/NCBI
67	Karita M and Blaser MJ: Acid-tolerance response in Helicobacter pylori and differences between cagA+ and cagA- strains. J Infect Dis. 178:213–219. 1998. View Article : Google Scholar : PubMed/NCBI
68	Kunovsky L, Dite P, Jabandziev P, Dolina J, Vaculova J, Blaho M, Bojkova M, Dvorackova J, Uvirova M, Kala Z and Trna J: Helicobacter pylori infection and other bacteria in pancreatic cancer and autoimmune pancreatitis. World J Gastrointest Oncol. 13:835–844. 2021. View Article : Google Scholar : PubMed/NCBI
69	Risch HA: Etiology of pancreatic cancer, with a hypothesis concerning the role of N-nitroso compounds and excess gastric acidity. J Natl Cancer Inst. 95:948–960. 2003. View Article : Google Scholar : PubMed/NCBI
70	Storz P: Acinar cell plasticity and development of pancreatic ductal adenocarcinoma. Nat Rev Gastroenterol Hepatol. 14:296–304. 2017. View Article : Google Scholar : PubMed/NCBI
71	Marstrand-Daucé L, Lorenzo D, Chassac A, Nicole P, Couvelard A and Haumaitre C: Acinar-to-Ductal metaplasia (ADM): On the road to pancreatic intraepithelial neoplasia (PanIN) and pancreatic cancer. Int J Mol Sci. 24:99462023. View Article : Google Scholar : PubMed/NCBI
72	Sozzi M, Valentini M, Figura N, De Paoli P, Tedeschi RM, Gloghini A, Serraino D, Poletti M and Carbone A: Atrophic gastritis and intestinal metaplasia in Helicobacter pylori infection: The role of CagA status. Am J Gastroenterol. 93:375–379. 1998. View Article : Google Scholar : PubMed/NCBI
73	Sharndama HC and Mba IE: Helicobacter pylori: An up-to-date overview on the virulence and pathogenesis mechanisms. Braz J Microbiol. 53:33–50. 2022. View Article : Google Scholar : PubMed/NCBI
74	Kusters JG, van Vliet AH and Kuipers EJ: Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev. 19:449–490. 2006. View Article : Google Scholar : PubMed/NCBI
75	Yamaoka Y: Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol. 7:629–641. 2010. View Article : Google Scholar : PubMed/NCBI
76	Lynch SM, Vrieling A, Lubin JH, Kraft P, Mendelsohn JB, Hartge P, Canzian F, Steplowski E, Arslan AA, Gross M, et al: Cigarette smoking and pancreatic cancer: A pooled analysis from the pancreatic cancer cohort consortium. Am J Epidemiol. 170:403–413. 2009. View Article : Google Scholar : PubMed/NCBI
77	Bosetti C, Rosato V, Li D, Silverman D, Petersen GM, Bracci PM, Neale RE, Muscat J, Anderson K, Gallinger S, et al: Diabetes, antidiabetic medications, and pancreatic cancer risk: An analysis from the international pancreatic cancer case-control consortium. Ann Oncol. 25:2065–2072. 2014. View Article : Google Scholar : PubMed/NCBI
78	Chari ST, Leibson CL, Rabe KG, Ransom J, de Andrade M and Petersen GM: Probability of pancreatic cancer following diabetes: A population-based study. Gastroenterology. 129:504–511. 2005. View Article : Google Scholar : PubMed/NCBI
79	Hu C, Hart SN, Polley EC, Gnanaolivu R, Shimelis H, Lee KY, Lilyquist J, Na J, Moore R, Antwi SO, et al: Association between inherited germline mutations in cancer predisposition genes and risk of pancreatic cancer. JAMA. 319:2401–2409. 2018. View Article : Google Scholar : PubMed/NCBI
80	Zhen DB, Rabe KG, Gallinger S, Syngal S, Schwartz AG, Goggins MG, Hruban RH, Cote ML, McWilliams RR, Roberts NJ, et al: BRCA1, BRCA2, PALB2, and CDKN2A mutations in familial pancreatic cancer: A PACGENE study. Genet Med. 17:569–577. 2015. View Article : Google Scholar : PubMed/NCBI
81	Patel SK, Pratap CB, Jain AK, Gulati AK and Nath G: Diagnosis of Helicobacter pylori: What should be the gold standard? World J Gastroenterol. 20:12847–12859. 2014. View Article : Google Scholar : PubMed/NCBI
82	Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VWS, Wu JCY, et al: Global prevalence of helicobacter pylori infection: Systematic review and meta-analysis. Gastroenterology. 153:420–429. 2017. View Article : Google Scholar : PubMed/NCBI
83	Li Y, Choi H, Leung K, Jiang F, Graham DY and Leung WK: Global prevalence of Helicobacter pylori infection between 1980 and 2022: A systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 8:553–564. 2023. View Article : Google Scholar : PubMed/NCBI
84	Mitchell H and Katelaris P: Epidemiology, clinical impacts and current clinical management of Helicobacter pylori infection. Med J Aust. 204:376–380. 2016. View Article : Google Scholar : PubMed/NCBI
85	Shah SC, Halvorson AE, Lee D, Bustamante R, McBay B, Gupta R, Denton J, Dorn C, Wilson O, Peek R Jr, et al: Helicobacter pylori Burden in the United States according to individual demographics and geography: A nationwide analysis of the veterans healthcare system. Clin Gastroenterol Hepatol. 22:42–50.e26. 2024. View Article : Google Scholar : PubMed/NCBI
86	Kist M, Strobel S, Kirchner T and Dammann HG: Impact of ELISA and immunoblot as diagnostic tools one year after eradication of Helicobacter pylori in a multicentre treatment study. FEMS Immunol Med Microbiol. 24:239–242. 1999. View Article : Google Scholar : PubMed/NCBI
87	Lu CY, Kuo CH, Lo YC, Chuang HY, Yang YC, Wu IC, Yu FJ, Lee YC, Jan CM, Wang WM and Wu DC: The best method of detecting prior Helicobacter pylori infection. World J Gastroenterol. 11:5672–5676. 2005. View Article : Google Scholar : PubMed/NCBI