Skip to main content
Top
Published in: Cancer Causes & Control 1/2012

01-01-2012 | Original paper

Cholecystectomy and risk of pancreatic cancer: a meta-analysis of observational studies

Authors: Genlai Lin, Zhaochong Zeng, Xiaolin Wang, Zheng Wu, Jian Wang, Chenggang Wang, Qiao Sun, Yixing Chen, Hongbo Quan

Published in: Cancer Causes & Control | Issue 1/2012

Login to get access

Abstract

Objective

Data from epidemiological studies related to the association of cholecystectomy and pancreatic cancer (PaC) risk are inconsistent. We conducted a meta-analysis of observational studies to explore this relationship.

Methods

We identified studies by a literature search of Medline (from 1 January 1966) and EMBASE (from 1 January 1974), through 30 June 2011, and by searching the reference lists of pertinent articles. Summary relative risks with their 95% confidence intervals were calculated with a random-effects model. Between-study heterogeneity was assessed using Cochran’s Q statistic and the I 2.

Results

A total of 18 studies (10 case–control studies, eight cohort studies) were included in this meta-analysis. Analysis of these 18 studies found that cholecystectomy was associated with a 23% excess risk of PaC (SRR = 1.23, 95% CI = 1.12–1.35), with moderate heterogeneity among these studies (p heterogeneity = 0.006, I 2 = 51.0%). Sub-grouped analyses revealed that the increased risk of PaC was independent of geographic location, gender, study design and confounders. There was no publication bias in the current meta-analysis.

Conclusions

The results of this meta-analysis suggest that individuals with a history of cholecystectomy may have an increased risk of pancreatic cancer.
Literature
1.
go back to reference Nathan H, Pawlik TM, Wolfgang CL, Choti MA, Cameron JL, Schulick RD (2007) Trends in survival after surgery for cholangiocarcinoma: a 30-year population-based SEER database analysis. J Gastrointest Surg 11:1488–1496 (discussion 1496–1487)PubMedCrossRef Nathan H, Pawlik TM, Wolfgang CL, Choti MA, Cameron JL, Schulick RD (2007) Trends in survival after surgery for cholangiocarcinoma: a 30-year population-based SEER database analysis. J Gastrointest Surg 11:1488–1496 (discussion 1496–1487)PubMedCrossRef
2.
go back to reference Turrini O, Cano C, Legoffic A, Delpero JR, Dagorn JC, Iovanna J (2009) Genetic alterations in precancerous pancreatic lesions and their clinical implications. Gastroenterol Clin Biol 33(1028–1035):e1021–e1029 Turrini O, Cano C, Legoffic A, Delpero JR, Dagorn JC, Iovanna J (2009) Genetic alterations in precancerous pancreatic lesions and their clinical implications. Gastroenterol Clin Biol 33(1028–1035):e1021–e1029
3.
go back to reference Kuuselo R, Savinainen K, Azorsa DO et al (2007) Intersex-like (IXL) is a cell survival regulator in pancreatic cancer with 19q13 amplification. Cancer Res 67:1943–1949PubMedCrossRef Kuuselo R, Savinainen K, Azorsa DO et al (2007) Intersex-like (IXL) is a cell survival regulator in pancreatic cancer with 19q13 amplification. Cancer Res 67:1943–1949PubMedCrossRef
4.
go back to reference Bertuccio P, La Vecchia C, Silverman DT et al (2011) Cigar and pipe smoking, smokeless tobacco use and pancreatic cancer: an analysis from the international pancreatic cancer case–control consortium (PanC4). Ann Oncol 22:1420–1426PubMedCrossRef Bertuccio P, La Vecchia C, Silverman DT et al (2011) Cigar and pipe smoking, smokeless tobacco use and pancreatic cancer: an analysis from the international pancreatic cancer case–control consortium (PanC4). Ann Oncol 22:1420–1426PubMedCrossRef
5.
go back to reference Tang H, Dong X, Hassan M, Abbruzzese JL, Li D (2011) Body mass index and obesity- and diabetes-associated genotypes and risk for pancreatic cancer. Cancer Epidemiol Biomarkers Prev 20:779–792PubMedCrossRef Tang H, Dong X, Hassan M, Abbruzzese JL, Li D (2011) Body mass index and obesity- and diabetes-associated genotypes and risk for pancreatic cancer. Cancer Epidemiol Biomarkers Prev 20:779–792PubMedCrossRef
6.
go back to reference Ben Q, Cai Q, Li Z et al (2011) The relationship between new-onset diabetes mellitus and pancreatic cancer risk: a case–control study. Eur J Cancer 47:248–254PubMedCrossRef Ben Q, Cai Q, Li Z et al (2011) The relationship between new-onset diabetes mellitus and pancreatic cancer risk: a case–control study. Eur J Cancer 47:248–254PubMedCrossRef
7.
go back to reference Ben Q, Xu M, Ning X et al (2011) Diabetes mellitus and risk of pancreatic cancer: a meta-analysis of cohort studies. Eur J Cancer 48:1928–1937CrossRef Ben Q, Xu M, Ning X et al (2011) Diabetes mellitus and risk of pancreatic cancer: a meta-analysis of cohort studies. Eur J Cancer 48:1928–1937CrossRef
8.
go back to reference Shao T, Yang YX (2005) Cholecystectomy and the risk of colorectal cancer. Am J Gastroenterol 100:1813–1820PubMedCrossRef Shao T, Yang YX (2005) Cholecystectomy and the risk of colorectal cancer. Am J Gastroenterol 100:1813–1820PubMedCrossRef
9.
go back to reference Ekbom A, Yuen J, Karlsson BM, McLaughlin JK, Adami HO (1996) Risk of pancreatic and periampullar cancer following cholecystectomy: a population-based cohort study. Dig Dis Sci 41:387–391PubMedCrossRef Ekbom A, Yuen J, Karlsson BM, McLaughlin JK, Adami HO (1996) Risk of pancreatic and periampullar cancer following cholecystectomy: a population-based cohort study. Dig Dis Sci 41:387–391PubMedCrossRef
10.
go back to reference Chow WH, Johansen C, Gridley G, Mellemkjaer L, Olsen JH, Fraumeni JF Jr (1999) Gallstones, cholecystectomy and risk of cancers of the liver, biliary tract and pancreas. Br J Cancer 79:640–644PubMedCrossRef Chow WH, Johansen C, Gridley G, Mellemkjaer L, Olsen JH, Fraumeni JF Jr (1999) Gallstones, cholecystectomy and risk of cancers of the liver, biliary tract and pancreas. Br J Cancer 79:640–644PubMedCrossRef
11.
go back to reference Silverman DT, Schiffman M, Everhart J et al (1999) Diabetes mellitus, other medical conditions and familial history of cancer as risk factors for pancreatic cancer. Br J Cancer 80:1830–1837PubMedCrossRef Silverman DT, Schiffman M, Everhart J et al (1999) Diabetes mellitus, other medical conditions and familial history of cancer as risk factors for pancreatic cancer. Br J Cancer 80:1830–1837PubMedCrossRef
12.
go back to reference Ko AH, Wang F, Holly EA (2007) Pancreatic cancer and medical history in a population-based case–control study in the San Francisco Bay Area, California. Cancer Causes Control 18:809–819PubMedCrossRef Ko AH, Wang F, Holly EA (2007) Pancreatic cancer and medical history in a population-based case–control study in the San Francisco Bay Area, California. Cancer Causes Control 18:809–819PubMedCrossRef
13.
go back to reference Arnold LD, Patel AV, Yan Y et al (2009) Are racial disparities in pancreatic cancer explained by smoking and overweight/obesity? Cancer Epidemiol Biomarkers Prev 18:2397–2405PubMedCrossRef Arnold LD, Patel AV, Yan Y et al (2009) Are racial disparities in pancreatic cancer explained by smoking and overweight/obesity? Cancer Epidemiol Biomarkers Prev 18:2397–2405PubMedCrossRef
14.
go back to reference Gullo L, Pezzilli R, Morselli-Labate AM (1996) Risk of pancreatic cancer associated with cholelithiasis, cholecystectomy, or gastrectomy. Dig Dis Sci 41:1065–1068PubMedCrossRef Gullo L, Pezzilli R, Morselli-Labate AM (1996) Risk of pancreatic cancer associated with cholelithiasis, cholecystectomy, or gastrectomy. Dig Dis Sci 41:1065–1068PubMedCrossRef
15.
go back to reference Lee CT, Chang FY, Lee SD (1996) Risk factors for pancreatic cancer in orientals. J Gastroenterol Hepatol 11:491–495PubMedCrossRef Lee CT, Chang FY, Lee SD (1996) Risk factors for pancreatic cancer in orientals. J Gastroenterol Hepatol 11:491–495PubMedCrossRef
16.
go back to reference Ye W, Lagergren J, Nyren O, Ekbom A (2001) Risk of pancreatic cancer after cholecystectomy: a cohort study in Sweden. Gut 49:678–681PubMedCrossRef Ye W, Lagergren J, Nyren O, Ekbom A (2001) Risk of pancreatic cancer after cholecystectomy: a cohort study in Sweden. Gut 49:678–681PubMedCrossRef
17.
go back to reference Schernhammer ES, Michaud DS, Leitzmann MF, Giovannucci E, Colditz GA, Fuchs CS (2002) Gallstones, cholecystectomy, and the risk for developing pancreatic cancer. Br J Cancer 86:1081–1084PubMedCrossRef Schernhammer ES, Michaud DS, Leitzmann MF, Giovannucci E, Colditz GA, Fuchs CS (2002) Gallstones, cholecystectomy, and the risk for developing pancreatic cancer. Br J Cancer 86:1081–1084PubMedCrossRef
18.
go back to reference Goldacre MJ, Abisgold JD, Seagroatt V, Yeates D (2005) Cancer after cholecystectomy: record-linkage cohort study. Br J Cancer 92:1307–1309PubMedCrossRef Goldacre MJ, Abisgold JD, Seagroatt V, Yeates D (2005) Cancer after cholecystectomy: record-linkage cohort study. Br J Cancer 92:1307–1309PubMedCrossRef
19.
go back to reference McDonnell CO, Bailey I, Stumpf T, Walsh TN, Johnson CD (2002) The effect of cholecystectomy on plasma cholecystokinin. Am J Gastroenterol 97:2189–2192PubMedCrossRef McDonnell CO, Bailey I, Stumpf T, Walsh TN, Johnson CD (2002) The effect of cholecystectomy on plasma cholecystokinin. Am J Gastroenterol 97:2189–2192PubMedCrossRef
20.
go back to reference Matters GL, McGovern C, Harms JF et al (2011) Role of endogenous cholecystokinin on growth of human pancreatic cancer. Int J Oncol 38:593–601PubMed Matters GL, McGovern C, Harms JF et al (2011) Role of endogenous cholecystokinin on growth of human pancreatic cancer. Int J Oncol 38:593–601PubMed
21.
go back to reference Chu M, Rehfeld JF, Borch K (1997) Chronic endogenous hypercholecystokininemia promotes pancreatic carcinogenesis in the hamster. Carcinogenesis 18:315–320PubMedCrossRef Chu M, Rehfeld JF, Borch K (1997) Chronic endogenous hypercholecystokininemia promotes pancreatic carcinogenesis in the hamster. Carcinogenesis 18:315–320PubMedCrossRef
22.
go back to reference Narisawa T, Magadia NE, Weisburger JH, Wynder EL (1974) Promoting effect of bile acids on colon carcinogenesis after intrarectal instillation of N-methyl-N′-nitro-N-nitrosoguanidine in rats. J Natl Cancer Inst 53:1093–1097PubMed Narisawa T, Magadia NE, Weisburger JH, Wynder EL (1974) Promoting effect of bile acids on colon carcinogenesis after intrarectal instillation of N-methyl-N′-nitro-N-nitrosoguanidine in rats. J Natl Cancer Inst 53:1093–1097PubMed
23.
go back to reference Cameron RG, Imaida K, Tsuda H, Ito N (1982) Promotive effects of steroids and bile acids on hepatocarcinogenesis initiated by diethylnitrosamine. Cancer Res 42:2426–2428PubMed Cameron RG, Imaida K, Tsuda H, Ito N (1982) Promotive effects of steroids and bile acids on hepatocarcinogenesis initiated by diethylnitrosamine. Cancer Res 42:2426–2428PubMed
24.
go back to reference Ura H, Makino T, Ito S et al (1986) Combined effects of cholecystectomy and lithocholic acid on pancreatic carcinogenesis of N-nitrosobis(2-hydroxypropyl)amine in Syrian golden hamsters. Cancer Res 46:4782–4786PubMed Ura H, Makino T, Ito S et al (1986) Combined effects of cholecystectomy and lithocholic acid on pancreatic carcinogenesis of N-nitrosobis(2-hydroxypropyl)amine in Syrian golden hamsters. Cancer Res 46:4782–4786PubMed
25.
go back to reference Stroup DF, Berlin JA, Morton SC et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. Jama 283:2008–2012PubMedCrossRef Stroup DF, Berlin JA, Morton SC et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. Jama 283:2008–2012PubMedCrossRef
26.
go back to reference Bueno de Mesquita HB, Maisonneuve P, Moerman CJ, Walker AM (1992) Aspects of medical history and exocrine carcinoma of the pancreas: a population-based case–control study in the Netherlands. Int J Cancer 52:17–23PubMedCrossRef Bueno de Mesquita HB, Maisonneuve P, Moerman CJ, Walker AM (1992) Aspects of medical history and exocrine carcinoma of the pancreas: a population-based case–control study in the Netherlands. Int J Cancer 52:17–23PubMedCrossRef
27.
go back to reference Shibata A, Mack TM, Paganini-Hill A, Ross RK, Henderson BE (1994) A prospective study of pancreatic cancer in the elderly. Int J Cancer 58:46–49PubMedCrossRef Shibata A, Mack TM, Paganini-Hill A, Ross RK, Henderson BE (1994) A prospective study of pancreatic cancer in the elderly. Int J Cancer 58:46–49PubMedCrossRef
28.
29.
go back to reference Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558PubMedCrossRef Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558PubMedCrossRef
30.
go back to reference Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560PubMedCrossRef Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560PubMedCrossRef
31.
go back to reference Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101PubMedCrossRef Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101PubMedCrossRef
32.
go back to reference Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634PubMedCrossRef Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634PubMedCrossRef
33.
go back to reference Ichimiya H, Kono S, Ikeda M, Tokudome S, Nakayama F, Kuratsune M (1986) Cancer mortality among patients undergoing cholecystectomy for benign biliary diseases. Jpn J Cancer Res 77:579–583PubMed Ichimiya H, Kono S, Ikeda M, Tokudome S, Nakayama F, Kuratsune M (1986) Cancer mortality among patients undergoing cholecystectomy for benign biliary diseases. Jpn J Cancer Res 77:579–583PubMed
34.
go back to reference Wynder EL, Mabuchi K, Maruchi N, Fortner JG (1973) A case control study of cancer of the pancreas. Cancer 31:641–648PubMedCrossRef Wynder EL, Mabuchi K, Maruchi N, Fortner JG (1973) A case control study of cancer of the pancreas. Cancer 31:641–648PubMedCrossRef
35.
go back to reference Haines AP, Moss AR, Whittemore A, Quivey J (1982) A case–control study of pancreatic carcinoma. J Cancer Res Clin Oncol 103:93–97PubMedCrossRef Haines AP, Moss AR, Whittemore A, Quivey J (1982) A case–control study of pancreatic carcinoma. J Cancer Res Clin Oncol 103:93–97PubMedCrossRef
36.
go back to reference Mack TM, Yu MC, Hanisch R, Henderson BE (1986) Pancreas cancer and smoking, beverage consumption, and past medical history. J Natl Cancer Inst 76:49–60PubMed Mack TM, Yu MC, Hanisch R, Henderson BE (1986) Pancreas cancer and smoking, beverage consumption, and past medical history. J Natl Cancer Inst 76:49–60PubMed
37.
go back to reference Cuzick J, Babiker AG (1989) Pancreatic cancer, alcohol, diabetes mellitus and gall-bladder disease. Int J Cancer 43:415–421PubMedCrossRef Cuzick J, Babiker AG (1989) Pancreatic cancer, alcohol, diabetes mellitus and gall-bladder disease. Int J Cancer 43:415–421PubMedCrossRef
38.
go back to reference Farrow DC, Davis S (1990) Risk of pancreatic cancer in relation to medical history and the use of tobacco, alcohol and coffee. Int J Cancer 45:816–820PubMedCrossRef Farrow DC, Davis S (1990) Risk of pancreatic cancer in relation to medical history and the use of tobacco, alcohol and coffee. Int J Cancer 45:816–820PubMedCrossRef
39.
go back to reference Shaffer EA (2005) Epidemiology and risk factors for gallstone disease: has the paradigm changed in the 21st century? Curr Gastroenterol Rep 7:132–140PubMedCrossRef Shaffer EA (2005) Epidemiology and risk factors for gallstone disease: has the paradigm changed in the 21st century? Curr Gastroenterol Rep 7:132–140PubMedCrossRef
40.
go back to reference Borch K, Jonsson KA, Zdolsek JM, Halldestam I, Kullman E (1998) Prevalence of gallstone disease in a Swedish population sample. Relations to occupation, childbirth, health status, life style, medications, and blood lipids. Scand J Gastroenterol 33:1219–1225PubMedCrossRef Borch K, Jonsson KA, Zdolsek JM, Halldestam I, Kullman E (1998) Prevalence of gallstone disease in a Swedish population sample. Relations to occupation, childbirth, health status, life style, medications, and blood lipids. Scand J Gastroenterol 33:1219–1225PubMedCrossRef
41.
go back to reference Reid FD, Mercer PM, Harrison M, Bates T (1996) Cholecystectomy as a risk factor for colorectal cancer: a meta-analysis. Scand J Gastroenterol 31:160–169PubMedCrossRef Reid FD, Mercer PM, Harrison M, Bates T (1996) Cholecystectomy as a risk factor for colorectal cancer: a meta-analysis. Scand J Gastroenterol 31:160–169PubMedCrossRef
42.
go back to reference Rosenberg L, Duguid WP, Brown RA (1984) Cholecystectomy stimulates hypertrophy and hyperplasia in the hamster pancreas. J Surg Res 37:108–111PubMedCrossRef Rosenberg L, Duguid WP, Brown RA (1984) Cholecystectomy stimulates hypertrophy and hyperplasia in the hamster pancreas. J Surg Res 37:108–111PubMedCrossRef
43.
go back to reference Hyvarinen H, Partanen S (1987) Association of cholecystectomy with abdominal cancers. Hepatogastroenterology 34:280–284PubMed Hyvarinen H, Partanen S (1987) Association of cholecystectomy with abdominal cancers. Hepatogastroenterology 34:280–284PubMed
44.
go back to reference De Santis A, Attili AF, Corradini SG et al (1997) Gallstones and diabetes: a case–control study in a free-living population sample. Hepatology 25:787–790PubMedCrossRef De Santis A, Attili AF, Corradini SG et al (1997) Gallstones and diabetes: a case–control study in a free-living population sample. Hepatology 25:787–790PubMedCrossRef
45.
go back to reference Liu B, Balkwill A, Roddam A, Brown A, Beral V (2009) Separate and joint effects of alcohol and smoking on the risks of cirrhosis and gallbladder disease in middle-aged women. Am J Epidemiol 169:153–160PubMedCrossRef Liu B, Balkwill A, Roddam A, Brown A, Beral V (2009) Separate and joint effects of alcohol and smoking on the risks of cirrhosis and gallbladder disease in middle-aged women. Am J Epidemiol 169:153–160PubMedCrossRef
46.
go back to reference Iodice S, Gandini S, Maisonneuve P, Lowenfels AB (2008) Tobacco and the risk of pancreatic cancer: a review and meta-analysis. Langenbecks Arch Surg 393:535–545PubMedCrossRef Iodice S, Gandini S, Maisonneuve P, Lowenfels AB (2008) Tobacco and the risk of pancreatic cancer: a review and meta-analysis. Langenbecks Arch Surg 393:535–545PubMedCrossRef
47.
go back to reference Jorgensen T (1987) Prevalence of gallstones in a Danish population. Am J Epidemiol 126:912–921PubMed Jorgensen T (1987) Prevalence of gallstones in a Danish population. Am J Epidemiol 126:912–921PubMed
Metadata
Title
Cholecystectomy and risk of pancreatic cancer: a meta-analysis of observational studies
Authors
Genlai Lin
Zhaochong Zeng
Xiaolin Wang
Zheng Wu
Jian Wang
Chenggang Wang
Qiao Sun
Yixing Chen
Hongbo Quan
Publication date
01-01-2012
Publisher
Springer Netherlands
Published in
Cancer Causes & Control / Issue 1/2012
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-011-9856-y

Other articles of this Issue 1/2012

Cancer Causes & Control 1/2012 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine