Usage of proton pump inhibitors is associated with pancreatic cancer: a systematicreview and meta-analysis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

MAO Qingsong , FAN Hongdan ,  GONG Jianping

Department of Hepatobiliary Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing 400010, P. R. China;

Corresponding author：

GONG Jianping, Email: gongjianping11@126.com

Keywords：

proton pump inhibitor; pancreatic cancer; dose-response; time-effect; meta-analysis

DOI：

10.7507/1007-9424.202212045

Video：

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Objective To further evaluate the relation between usage of proton pump inhibitor (PPI) and the risk of pancreatic cancer. Method The observational studies were systematically searched in the databases of PubMed, Embase, Web of Science, Cochrane Library, ClinicalTrials.gov, CNKI, Wanfang, and VIP. The combined odds ratio (OR) and 95% confidence interval (CI) of pancreatic cancer risk were estimated by the corresponding effect model according to the heterogeneous results, and the subgroup analysis, meta-regression, and sensitivity analysis were performed. In addition, the relation between the defined daily dose (DDD) and usage time of PPI and the pancreatic cancer risk were studied by using restricted cubic spline. Results A total of 14 studies were included, including 1 601 430 subjects. The meta-analysis result showed that usage of PPI was positively correlated with the risk of pancreatic cancer [I²=98.9%, OR (95%CI)=1.60 (1.21, 2.11), P<0.001]. The subgroup analysis results showed that usage of PPI would increase the risk of pancreatic cancer in the subgroups of literature published before 2018 [OR (95%CI)=1.88 (1.05, 3.38), P=0.034], non-Asian regions [OR (95%CI)=1.37 (1.04, 1.82), P=0.028], case-control studies [OR (95%CI)=1.59 (1.16, 2.18), P=0.004], cohort studies [OR (95%CI)=1.65 (1.13, 2.39), P=0.009], and high-quality studies [OR (95%CI)=1.62 (1.19, 2.20), P=0.002]. The dose-response curve showed that there was a nonlinear relation between the usage of PPI and the risk of pancreatic cancer (χ²_linear=2.27, P=0.132; P_nonlinear=0.039). When the usage of PPI was 800 DDD or less, usage of PPI would increase the risk of pancreatic cancer, but there was no statistical significance when the usage of PPI was more than 800 DDD. The time-effect curve showed that there was a linear relation between the usage time of PPI and the risk of pancreatic cancer (χ²_linear=6.92, P=0.009), and the risk of pancreatic cancer would increase by 2.3% if the usage of PPI increased by one month [OR=1.02, 95%CI (1.01, 1.04), P=0.009]. The sensitivity analysis confirmed that the results were stable by gradually eliminating each study, the OR (95%CI) of the risk of pancreatic cancer was 1.37 (1.08, 1.74) to 1.66 (1.22, 2.27), and the publication bias was not found by Egger test (P=0.594).Conclusions From the results of this meta-analysis, usage of PPI will increase the risk of pancreatic cancer, and the dosage of PPI and usage time of PPI may be related to the risk of pancreatic cancer. The clinical usage of PPI should be strictly controlled, and the dosage and usage time should also be carefully considered.

Citation： MAO Qingsong, FAN Hongdan, GONG Jianping. Usage of proton pump inhibitors is associated with pancreatic cancer: a systematicreview and meta-analysis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(5): 587-594. doi: 10.7507/1007-9424.202212045 Copy

1.	Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2.	Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin, 2020, 70(1): 7-30.
3.	Zheng RS, Zhang SW, Zeng HM, et al. Cancer incidence and mortality in China, 2016. J Natl Cancer Cent, 2022, 2(1): 1-9.
4.	Zhao C, Gao F, Li Q, et al. The distributional characteristic and growing trend of pancreatic cancer in China. Pancreas, 2019, 48(3): 309-314.
5.	Xu M, Jung X, Hines OJ, et al. Obesity and pancreatic cancer: overview of epidemiology and potential prevention by weight loss. Pancreas, 2018, 47(2): 158-162.
6.	Molina-Montes E, Van Hoogstraten L, Gomez-Rubio P, et al. Pancreatic cancer risk in relation to lifetime smoking patterns, tobacco type, and dose-response relationships. Cancer Epidemiol Biomarkers Prev, 2020, 29(5): 1009-1018.
7.	Rawla P, Sunkara T, Gaduputi V. Epidemiology of pancreatic cancer: global trends, etiology and risk factors. World J Oncol, 2019, 10(1): 10-27.
8.	Huang BZ, Pandol SJ, Jeon CY, et al. New-onset diabetes, longitudinal trends in metabolic markers, and risk of pancreatic cancer in a heterogeneous population. Clin Gastroenterol Hepatol, 2020, 18(8): 1812-1821.
9.	Tsai HJ, Chang JS. Environmental risk factors of pancreatic cancer. J Clin Med, 2019, 8(9): 1427. doi: 10.3390/jcm8091427.
10.	Best LM, Takwoingi Y, Siddique S, et al. Non-invasive diagnostic tests for Helicobacter pylori infection. Cochrane Database Syst Rev, 2018, 3(3): CD012080. doi: 10.1002/14651858.CD012080.pub2.
11.	Xu JH, Fu JJ, Wang XL, et al. Hepatitis B or C viral infection and risk of pancreatic cancer: a meta-analysis of observational studies. World J Gastroenterol, 2013, 19(26): 4234-4241.
12.	Rijkers AP, Bakker OJ, Ahmed Ali U, et al. Risk of pancreatic cancer after a primary episode of acute pancreatitis. Pancreas, 2017, 46(8): 1018-1022.
13.	Gong Y, Zhou Q, Zhou Y, et al. Gastrectomy and risk of pancreatic cancer: systematic review and meta-analysis of observational studies. Cancer Causes Control, 2012, 23(8): 1279-1288.
14.	Nassar Y, Richter S. Proton-pump inhibitor use and fracture risk: an updated systematic review and meta-analysis. J Bone Metab, 2018, 25(3): 141-151.
15.	Trifan A, Stanciu C, Girleanu I, et al. Proton pump inhibitors therapy and risk of Clostridium difficile infection: systematic review and meta-analysis. World J Gastroenterol, 2017, 23(35): 6500-6515.
16.	Shah NH, LePendu P, Bauer-Mehren A, et al. Proton pump inhibitor usage and the risk of myocardial infarction in the general population. PLoS One, 2015, 10(6): e0124653. doi: 10.1371/journal.pone.0124653.
17.	Maes ML, Fixen DR, Linnebur SA. Adverse effects of proton-pump inhibitor use in older adults: a review of the evidence. Ther Adv Drug Saf, 2017, 8(9): 273-297.
18.	Song HJ, Jiang X, Henry L, et al. Proton pump inhibitors and risk of liver cancer and mortality in patients with chronic liver disease: a systematic review and meta-analysis. Eur J Clin Pharmacol, 2020, 76(6): 851-866.
19.	Ahn JS, Eom CS, Jeon CY, et al. Acid suppressive drugs and gastric cancer: a meta-analysis of observational studies. World J Gastroenterol, 2013, 19(16): 2560-2568.
20.	Leucht S, Samara M, Heres S, et al. Dose equivalents for antipsychotic drugs: the DDD method. Schizophr Bull, 2016, 42 Suppl 1(Suppl 1): S90-S94. doi: 10.1093/schbul/sbv167.
21.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
22.	Wu Y, Qie R, Cheng M, et al. Air pollution and DNA methylation in adults: a systematic review and meta-analysis of observational studies. Environ Pollut, 2021, 284: 117152. doi: 10.1016/j.envpol.2021.117152.
23.	Orsini N, Li R, Wolk A, et al. Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol, 2012, 175(1): 66-73.
24.	Jayedi A, Gohari A, Shab-Bidar S. Daily step count and all-cause mortality: a dose-response meta-analysis of prospective cohort studies. Sports Med, 2022, 52(1): 89-99.
25.	Boursi B, Finkelman B, Giantonio BJ, et al. A clinical prediction model to assess risk for pancreatic cancer among patients with New-Onset diabetes. Gastroenterology, 2017, 152(4): 840-850.
26.	Hwang IC, Chang J, Park SM. Association between proton pump inhibitor use and the risk of pancreatic cancer: a Korean nationwide cohort study. PLoS One, 2018, 13(9): e0203918. doi: 10.1371/journal.pone.0203918.
27.	Risch HA, Yu H, Lu L, et al. Detectable symptomatology preceding the diagnosis of pancreatic cancer and absolute risk of pancreatic cancer diagnosis. Am J Epidemiol, 2015, 182(1): 26-34.
28.	Brusselaers N, Sadr-Azodi O, Engstrand L. Long-term proton pump inhibitor usage and the association with pancreatic cancer in Sweden. J Gastroenterol, 2020, 55(4): 453-461.
29.	Lee JK, Merchant SA, Schneider JL, et al. Proton pump inhibitor use and risk of gastric, colorectal, liver, and pancreatic cancers in a community-based population. Am J Gastroenterol, 2020, 115(5): 706-715.
30.	Peng YC, Lin CL, Hsu WY, et al. Proton pump inhibitor use is associated with risk of pancreatic cancer: a nested case-control study. Dose Response, 2018, 16(4): 1559325818803283. doi: 10.1177/1559325818803283.
31.	Bradley MC, Murray LJ, Cantwell MM, et al. Proton pump inhibitors and histamine-2-receptor antagonists and pancreatic cancer risk: a nested case-control study. Br J Cancer, 2012, 106(1): 233-239.
32.	Chien LN, Huang YJ, Shao YH, et al. Proton pump inhibitors and risk of periampullary cancers—a nested case-control study. Int J Cancer, 2016, 138(6): 1401-1409.
33.	Kearns MD, Boursi B, Yang YX. Proton pump inhibitors on pancreatic cancer risk and survival. Cancer Epidemiol, 2017, 46: 80-84.
34.	Valente R, Hayes AJ, Haugvik SP, et al. Risk and protective factors for the occurrence of sporadic pancreatic endocrine neoplasms. Endocr Relat Cancer, 2017, 24(8): 405-414.
35.	Bosetti C, Lucenteforte E, Bracci PM, et al. Ulcer, gastric surgery and pancreatic cancer risk: an analysis from the International Pancreatic Cancer Case-Control Consortium (PanC4). Ann Oncol, 2013, 24(11): 2903-2910.
36.	Hicks B, Friis S, Pottegård A. Use of proton pump inhibitors and risk of pancreatic cancer. Pharmacoepidemiol Drug Saf, 2018, 27(8): 926-930.
37.	Lassalle M, Le Tri T, Afchain P, et al. Use of proton pump inhibitors and risk of pancreatic cancer: a nationwide case-control study based on the French National Health Data System (SNDS). Cancer Epidemiol Biomarkers Prev, 2022, 31(3): 662-669.
38.	Lai SW, Liao KF, Lai HC, et al. Use of proton pump inhibitors correlates with increased risk of colorectal cancer in Taiwan. Asia Pac J Clin Oncol, 2013, 9(2): 192-193.
39.	Alhazzani W, Alshamsi F, Belley-Cote E, et al. Efficacy and safety of stress ulcer prophylaxis in critically ill patients: a network meta-analysis of randomized trials. Intensive Care Med, 2018, 44(1): 1-11.
40.	Kinoshita Y, Ishimura N, Ishihara S. Advantages and disadvantages of long-term proton pump inhibitor use. J Neurogastroenterol Motil, 2018, 24(2): 182-196.
41.	Koyyada A. Long-term use of proton pump inhibitors as a risk factor for various adverse manifestations. Therapie, 2021, 76(1): 13-21.
42.	Abrahami D, McDonald EG, Schnitzer ME, et al. Proton pump inhibitors and risk of gastric cancer: population-based cohort study. Gut, 2022, 71(1): 16-24.
43.	Abrahami D, McDonald EG, Schnitzer ME, et al. Proton pump inhibitors and risk of colorectal cancer. Gut, 2022, 71(1): 111-118.
44.	Tran KT, McMenamin ÚC, Hicks B, et al. Proton pump inhibitor and histamine-2 receptor antagonist use and risk of liver cancer in two population-based studies. Aliment Pharmacol Ther, 2018, 48(1): 55-64.
45.	Cayrol C, Bertrand C, Kowalski-Chauvel A, et al. αⅤ integrin: a new gastrin target in human pancreatic cancer cells. World J Gastroenterol, 2011, 17(40): 4488-4495.
46.	Caplin M, Khan K, Grimes S, et al. Effect of gastrin and anti-gastrin antibodies on proliferation of hepatocyte cell lines. Dig Dis Sci, 2001, 46(7): 1356-1366.
47.	Hong HE, Kim AS, Kim MR, et al. Does the use of proton pump inhibitors increase the risk of pancreatic cancer? A systematic review and meta-analysis of epidemiologic studies. Cancers (Basel), 2020, 12(8): 2220. doi: 10.3390/cancers12082220.
48.	Alkhushaym N, Almutairi AR, Althagafi A, et al. Exposure to proton pump inhibitors and risk of pancreatic cancer: a meta-analysis. Expert Opin Drug Saf, 2020, 19(3): 327-334.
49.	Poly TN, Islam MM, Walther BA, et al. Proton pump inhibitors use and the risk of pancreatic cancer: evidence from eleven epidemiological studies, comprising 1.5 million individuals. Cancers (Basel), 2022, 14(21): 5357. doi: 10.3390/cancers14215357.
50.	Laoveeravat P, Thavaraputta S, Vutthikraivit W, et al. Proton pump inhibitors and histamine-2 receptor antagonists on the risk of pancreatic cancer: a systematic review and meta-analysis. QJM, 2020, 113(2): 100-107.
51.	李春杏, 王月, 任昭, 等. 基于《质子泵抑制剂临床应用指导原则(2020年版)》评价质子泵抑制剂的合理使用情况. 临床药物治疗杂志, 2022, 20(12): 71-75.
52.	Klein AP. Pancreatic cancer epidemiology: understanding the role of lifestyle and inherited risk factors. Nat Rev Gastroenterol Hepatol, 2021, 18(7): 493-502.

1. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin, 2020, 70(1): 7-30.
3. Zheng RS, Zhang SW, Zeng HM, et al. Cancer incidence and mortality in China, 2016. J Natl Cancer Cent, 2022, 2(1): 1-9.
4. Zhao C, Gao F, Li Q, et al. The distributional characteristic and growing trend of pancreatic cancer in China. Pancreas, 2019, 48(3): 309-314.
5. Xu M, Jung X, Hines OJ, et al. Obesity and pancreatic cancer: overview of epidemiology and potential prevention by weight loss. Pancreas, 2018, 47(2): 158-162.
6. Molina-Montes E, Van Hoogstraten L, Gomez-Rubio P, et al. Pancreatic cancer risk in relation to lifetime smoking patterns, tobacco type, and dose-response relationships. Cancer Epidemiol Biomarkers Prev, 2020, 29(5): 1009-1018.
7. Rawla P, Sunkara T, Gaduputi V. Epidemiology of pancreatic cancer: global trends, etiology and risk factors. World J Oncol, 2019, 10(1): 10-27.
8. Huang BZ, Pandol SJ, Jeon CY, et al. New-onset diabetes, longitudinal trends in metabolic markers, and risk of pancreatic cancer in a heterogeneous population. Clin Gastroenterol Hepatol, 2020, 18(8): 1812-1821.
9. Tsai HJ, Chang JS. Environmental risk factors of pancreatic cancer. J Clin Med, 2019, 8(9): 1427. doi: 10.3390/jcm8091427.
10. Best LM, Takwoingi Y, Siddique S, et al. Non-invasive diagnostic tests for Helicobacter pylori infection. Cochrane Database Syst Rev, 2018, 3(3): CD012080. doi: 10.1002/14651858.CD012080.pub2.
11. Xu JH, Fu JJ, Wang XL, et al. Hepatitis B or C viral infection and risk of pancreatic cancer: a meta-analysis of observational studies. World J Gastroenterol, 2013, 19(26): 4234-4241.
12. Rijkers AP, Bakker OJ, Ahmed Ali U, et al. Risk of pancreatic cancer after a primary episode of acute pancreatitis. Pancreas, 2017, 46(8): 1018-1022.
13. Gong Y, Zhou Q, Zhou Y, et al. Gastrectomy and risk of pancreatic cancer: systematic review and meta-analysis of observational studies. Cancer Causes Control, 2012, 23(8): 1279-1288.
14. Nassar Y, Richter S. Proton-pump inhibitor use and fracture risk: an updated systematic review and meta-analysis. J Bone Metab, 2018, 25(3): 141-151.
15. Trifan A, Stanciu C, Girleanu I, et al. Proton pump inhibitors therapy and risk of Clostridium difficile infection: systematic review and meta-analysis. World J Gastroenterol, 2017, 23(35): 6500-6515.
16. Shah NH, LePendu P, Bauer-Mehren A, et al. Proton pump inhibitor usage and the risk of myocardial infarction in the general population. PLoS One, 2015, 10(6): e0124653. doi: 10.1371/journal.pone.0124653.
17. Maes ML, Fixen DR, Linnebur SA. Adverse effects of proton-pump inhibitor use in older adults: a review of the evidence. Ther Adv Drug Saf, 2017, 8(9): 273-297.
18. Song HJ, Jiang X, Henry L, et al. Proton pump inhibitors and risk of liver cancer and mortality in patients with chronic liver disease: a systematic review and meta-analysis. Eur J Clin Pharmacol, 2020, 76(6): 851-866.
19. Ahn JS, Eom CS, Jeon CY, et al. Acid suppressive drugs and gastric cancer: a meta-analysis of observational studies. World J Gastroenterol, 2013, 19(16): 2560-2568.
20. Leucht S, Samara M, Heres S, et al. Dose equivalents for antipsychotic drugs: the DDD method. Schizophr Bull, 2016, 42 Suppl 1(Suppl 1): S90-S94. doi: 10.1093/schbul/sbv167.
21. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
22. Wu Y, Qie R, Cheng M, et al. Air pollution and DNA methylation in adults: a systematic review and meta-analysis of observational studies. Environ Pollut, 2021, 284: 117152. doi: 10.1016/j.envpol.2021.117152.
23. Orsini N, Li R, Wolk A, et al. Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol, 2012, 175(1): 66-73.
24. Jayedi A, Gohari A, Shab-Bidar S. Daily step count and all-cause mortality: a dose-response meta-analysis of prospective cohort studies. Sports Med, 2022, 52(1): 89-99.
25. Boursi B, Finkelman B, Giantonio BJ, et al. A clinical prediction model to assess risk for pancreatic cancer among patients with New-Onset diabetes. Gastroenterology, 2017, 152(4): 840-850.
26. Hwang IC, Chang J, Park SM. Association between proton pump inhibitor use and the risk of pancreatic cancer: a Korean nationwide cohort study. PLoS One, 2018, 13(9): e0203918. doi: 10.1371/journal.pone.0203918.
27. Risch HA, Yu H, Lu L, et al. Detectable symptomatology preceding the diagnosis of pancreatic cancer and absolute risk of pancreatic cancer diagnosis. Am J Epidemiol, 2015, 182(1): 26-34.
28. Brusselaers N, Sadr-Azodi O, Engstrand L. Long-term proton pump inhibitor usage and the association with pancreatic cancer in Sweden. J Gastroenterol, 2020, 55(4): 453-461.
29. Lee JK, Merchant SA, Schneider JL, et al. Proton pump inhibitor use and risk of gastric, colorectal, liver, and pancreatic cancers in a community-based population. Am J Gastroenterol, 2020, 115(5): 706-715.
30. Peng YC, Lin CL, Hsu WY, et al. Proton pump inhibitor use is associated with risk of pancreatic cancer: a nested case-control study. Dose Response, 2018, 16(4): 1559325818803283. doi: 10.1177/1559325818803283.
31. Bradley MC, Murray LJ, Cantwell MM, et al. Proton pump inhibitors and histamine-2-receptor antagonists and pancreatic cancer risk: a nested case-control study. Br J Cancer, 2012, 106(1): 233-239.
32. Chien LN, Huang YJ, Shao YH, et al. Proton pump inhibitors and risk of periampullary cancers—a nested case-control study. Int J Cancer, 2016, 138(6): 1401-1409.
33. Kearns MD, Boursi B, Yang YX. Proton pump inhibitors on pancreatic cancer risk and survival. Cancer Epidemiol, 2017, 46: 80-84.
34. Valente R, Hayes AJ, Haugvik SP, et al. Risk and protective factors for the occurrence of sporadic pancreatic endocrine neoplasms. Endocr Relat Cancer, 2017, 24(8): 405-414.
35. Bosetti C, Lucenteforte E, Bracci PM, et al. Ulcer, gastric surgery and pancreatic cancer risk: an analysis from the International Pancreatic Cancer Case-Control Consortium (PanC4). Ann Oncol, 2013, 24(11): 2903-2910.
36. Hicks B, Friis S, Pottegård A. Use of proton pump inhibitors and risk of pancreatic cancer. Pharmacoepidemiol Drug Saf, 2018, 27(8): 926-930.
37. Lassalle M, Le Tri T, Afchain P, et al. Use of proton pump inhibitors and risk of pancreatic cancer: a nationwide case-control study based on the French National Health Data System (SNDS). Cancer Epidemiol Biomarkers Prev, 2022, 31(3): 662-669.
38. Lai SW, Liao KF, Lai HC, et al. Use of proton pump inhibitors correlates with increased risk of colorectal cancer in Taiwan. Asia Pac J Clin Oncol, 2013, 9(2): 192-193.
39. Alhazzani W, Alshamsi F, Belley-Cote E, et al. Efficacy and safety of stress ulcer prophylaxis in critically ill patients: a network meta-analysis of randomized trials. Intensive Care Med, 2018, 44(1): 1-11.
40. Kinoshita Y, Ishimura N, Ishihara S. Advantages and disadvantages of long-term proton pump inhibitor use. J Neurogastroenterol Motil, 2018, 24(2): 182-196.
41. Koyyada A. Long-term use of proton pump inhibitors as a risk factor for various adverse manifestations. Therapie, 2021, 76(1): 13-21.
42. Abrahami D, McDonald EG, Schnitzer ME, et al. Proton pump inhibitors and risk of gastric cancer: population-based cohort study. Gut, 2022, 71(1): 16-24.
43. Abrahami D, McDonald EG, Schnitzer ME, et al. Proton pump inhibitors and risk of colorectal cancer. Gut, 2022, 71(1): 111-118.
44. Tran KT, McMenamin ÚC, Hicks B, et al. Proton pump inhibitor and histamine-2 receptor antagonist use and risk of liver cancer in two population-based studies. Aliment Pharmacol Ther, 2018, 48(1): 55-64.
45. Cayrol C, Bertrand C, Kowalski-Chauvel A, et al. αⅤ integrin: a new gastrin target in human pancreatic cancer cells. World J Gastroenterol, 2011, 17(40): 4488-4495.
46. Caplin M, Khan K, Grimes S, et al. Effect of gastrin and anti-gastrin antibodies on proliferation of hepatocyte cell lines. Dig Dis Sci, 2001, 46(7): 1356-1366.
47. Hong HE, Kim AS, Kim MR, et al. Does the use of proton pump inhibitors increase the risk of pancreatic cancer? A systematic review and meta-analysis of epidemiologic studies. Cancers (Basel), 2020, 12(8): 2220. doi: 10.3390/cancers12082220.
48. Alkhushaym N, Almutairi AR, Althagafi A, et al. Exposure to proton pump inhibitors and risk of pancreatic cancer: a meta-analysis. Expert Opin Drug Saf, 2020, 19(3): 327-334.
49. Poly TN, Islam MM, Walther BA, et al. Proton pump inhibitors use and the risk of pancreatic cancer: evidence from eleven epidemiological studies, comprising 1.5 million individuals. Cancers (Basel), 2022, 14(21): 5357. doi: 10.3390/cancers14215357.
50. Laoveeravat P, Thavaraputta S, Vutthikraivit W, et al. Proton pump inhibitors and histamine-2 receptor antagonists on the risk of pancreatic cancer: a systematic review and meta-analysis. QJM, 2020, 113(2): 100-107.
51. 李春杏, 王月, 任昭, 等. 基于《质子泵抑制剂临床应用指导原则(2020年版)》评价质子泵抑制剂的合理使用情况. 临床药物治疗杂志, 2022, 20(12): 71-75.
52. Klein AP. Pancreatic cancer epidemiology: understanding the role of lifestyle and inherited risk factors. Nat Rev Gastroenterol Hepatol, 2021, 18(7): 493-502.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Usage of proton pump inhibitors is associated with pancreatic cancer: a systematicreview and meta-analysis

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