Severe Salmonella spp. or Campylobacter spp. Infection and the Risk of Biliary Tract Cancer: A Population-Based Study
Abstract
:Simple Summary
Abstract
1. Introduction
2. Results
2.1. Cohort Characteristics
2.2. Patients with Salmonella spp. Infection and BTC
2.3. Patients with Campylobacter spp. Infection and BTC
2.4. Risk of BTC After Salmonella spp. or Campylobacter spp. Infection
3. Discussion
4. Materials and Methods
4.1. Data Collection and Linkage
4.2. Patient Selection and Variable Definitions
4.3. Outcomes
4.4. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Surveillance EaERp. Biliary Tract Cancer, Survival by Stage 2018. Available online: https://www.cancer.org/cancer/bile-duct-cancer/detection-diagnosis-staging/survival-by-stage.html (accessed on 1 March 2020).
- Ries, L.A.G.; Reichman, M.E.; Lewis, D.R.; Hankey, B.F.; Edwards, B.K. Cancer Survival and Incidence from the Surveillance, Epidemiology, and End Results (SEER) Program. Oncologist 2003, 8, 541–552. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cronin, K.A.; Bs, A.J.L.; Scott, S.; Sherman, R.L.; Noone, A.-M.; Ms, N.H.; Henley, S.J.; Anderson, R.N.; Bs, A.U.F.; Ma, J.; et al. Annual Report to the Nation on the Status of Cancer, part I: National cancer statistics. Cancer 2018, 124, 2785–2800. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shroff, R.T.; Kennedy, E.B.; Bachini, M.; Bekaii-Saab, T.; Crane, C.; Edeline, J.; El-Khoueiry, A.; Feng, M.; Katz, M.H.; Primrose, J.; et al. Adjuvant Therapy for Resected Biliary Tract Cancer: ASCO Clinical Practice Guideline. J. Clin. Oncol. 2019, 37, 1015–1027. [Google Scholar] [CrossRef] [Green Version]
- Public Health Agency of Canada; Statistics Canada; Canadian Cancer Society. Release notice-Canadian Cancer Statistics 2019. Health Promot. Chronic Dis. Prev. Can. 2019, 39, 255. [Google Scholar] [CrossRef] [PubMed]
- Are, C.; Ahmad, H.; Ravipati, A.; Croo, D.; Clarey, D.; Smith, L.; Price, R.R.; Butte, J.M.; Gupta, S.; Chaturvedi, A.; et al. Global epidemiological trends and variations in the burden of gallbladder cancer. J. Surg. Oncol. 2017, 115, 580–590. [Google Scholar] [CrossRef]
- Lohman, E.D.S.; De Bitter, T.; Verhoeven, R.H.; Van Der Geest, L.; Hagendoorn, J.; Mohammad, N.H.; Daams, F.; Klümpen, H.-J.; Van Gulik, T.; Erdmann, J.I.; et al. Trends in Treatment and Survival of Gallbladder Cancer in the Netherlands; Identifying Gaps and Opportunities from a Nation-Wide Cohort. Cancers 2020, 12, 918. [Google Scholar] [CrossRef]
- Tyson, G.L.; El-Serag, H.B. Risk factors for cholangiocarcinoma. Hepatology 2011, 54, 173–184. [Google Scholar] [CrossRef]
- Gatto, M.; Bragazzi, M.C.; Semeraro, R.; Napoli, C.; Gentile, R.; Torrice, A.; Gaudio, E.; Alvaro, D. Cholangiocarcinoma: Update and future perspectives. Dig. Liver Dis. 2010, 42, 253–260. [Google Scholar] [CrossRef]
- Schottenfeld, D.; Beebe-Dimmer, J. The cancer burden attributable to biologic agents. Ann. Epidemiol. 2015, 25, 183–187. [Google Scholar] [CrossRef] [PubMed]
- Wardak, S. Human Papillomavirus (HPV) and cervical cancer. Medycyna Doswiadczalna i Mikrobiologia 2016, 68, 73–84. [Google Scholar]
- Balogh, J.; Victor, D.; Asham, E.H.; Burroughs, S.G.; Boktour, M.; Saharia, A.; Li, X.; Ghobrial, R.M.; Monsour, H.P. Hepatocellular carcinoma: A review. J. Hepatocell. Carcinoma 2016, 3, 41–53. [Google Scholar] [CrossRef] [Green Version]
- Aitken, C.A.; Van Agt, H.M.E.; Siebers, A.G.; Van Kemenade, F.J.; Niesters, H.G.M.; Melchers, W.J.G.; Vedder, J.E.M.; Schuurman, R.; Brule, A.J.C.V.D.; Van Der Linden, H.C.; et al. Introduction of primary screening using high-risk HPV DNA detection in the Dutch cervical cancer screening programme: A population-based cohort study. BMC Med. 2019, 17, 1–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gagnaire, A.; Nadel, B.; Raoult, D.; Neefjes, J.; Gorvel, A.G.B.N.J.-P. Collateral damage: Insights into bacterial mechanisms that predispose host cells to cancer. Nat. Rev. Genet. 2017, 15, 109–128. [Google Scholar] [CrossRef] [PubMed]
- Samaras, V.; Rafailidis, P.I.; Mourtzoukou, E.G.; Peppas, G.; Falagas, M.E. Chronic bacterial and parasitic infections and cancer: A review. J. Infect. Dev. Countries 2010, 4, 267–281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scanu, T.; Spaapen, R.M.; Bakker, J.M.; Pratap, C.B.; Wu, L.-E.; Hofland, I.; Broeks, A.; Shukla, V.K.; Kumar, M.; Janssen, H.; et al. Salmonella Manipulation of Host Signaling Pathways Provokes Cellular Transformation Associated with Gallbladder Carcinoma. Cell Host Microbe 2015, 17, 763–774. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mughini-Gras, L.; Schaapveld, M.; Kramers, J.; Mooij, S.; Neefjes-Borst, E.A.; Van Pelt, W.; Neefjes, J. Increased colon cancer risk after severe Salmonella infection. PLoS ONE 2018, 13, e0189721. [Google Scholar] [CrossRef] [Green Version]
- Brauner, A.; Brandt, L.; Frisan, T.; Thelestam, M.; Ekbom, A. Is there a risk of cancer development after Campylobacter infection? Scand. J. Gastroenterol. 2010, 45, 893–897. [Google Scholar] [CrossRef]
- Lara-Tejero, M. A Bacterial Toxin that Causes DNA Damage to Modulate Cellular Responses. Sci. World J. 2001, 1, 190–191. [Google Scholar] [CrossRef] [Green Version]
- He, Z.; Gharaibeh, R.Z.; Newsome, R.C.; Pope, J.L.; Dougherty, M.W.; Tomkovich, S.; Pons, B.; Mirey, G.; Vignard, J.; Hendrixson, D.R.; et al. Campylobacter jejuni promotes colorectal tumorigenesis through the action of cytolethal distending toxin. Gut 2018, 68, 289–300. [Google Scholar] [CrossRef] [Green Version]
- Wu, N.; Yang, X.; Zhang, R.; Li, J.; Xiao, X.; Hu, Y.; Chen, Y.; Yang, F.; Lu, N.; Wang, Z.; et al. Dysbiosis Signature of Fecal Microbiota in Colorectal Cancer Patients. Microb. Ecol. 2013, 66, 462–470. [Google Scholar] [CrossRef]
- Marcano-Bonilla, L.; Mohamed, E.A.; Mounajjed, T.; Roberts, L.R. Biliary tract cancers: Epidemiology, molecular pathogenesis and genetic risk associations. Chin. Clin. Oncol. 2016, 5, 61. [Google Scholar] [CrossRef] [PubMed]
- Caygill, C.; Hill, M.; Braddick, M.; Sharp, J. Cancer mortality in chronic typhoid and paratyphoid carriers. Lancet 1994, 343, 83–84. [Google Scholar] [CrossRef]
- Avilés-Jiménez, F.; Guitron, A.; Segura-López, F.; Méndez-Tenorio, A.; Iwai, S.; Hernández-Guerrero, A.; Torres, J. Microbiota studies in the bile duct strongly suggest a role for Helicobacter pylori in extrahepatic cholangiocarcinoma. Clin. Microbiol. Infect. 2016, 22, 178.e11–178.e22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Edwards, S.; Lilford, R.J.; Braunholtz, D.; Jackson, J. Why “underpowered” trials are not necessarily unethical. Lancet 1997, 350, 804–807. [Google Scholar] [CrossRef]
- Nagaraja, V.; Eslick, G.D. Systematic review with meta-analysis: The relationship between chronic Salmonella typhi carrier status and gall-bladder cancer. Aliment. Pharmacol. Ther. 2014, 39, 745–750. [Google Scholar] [CrossRef]
- Safaeian, M.; Gao, Y.-T.; Sakoda, L.C.; Quraishi, S.M.; Rashid, A.; Wang, B.-S.; Chen, J.; Pruckler, J.; Mintz, E.; Hsing, A.W. Chronic typhoid infection and the risk of biliary tract cancer and stones in Shanghai, China. Infect. Agents Cancer 2011, 6, 6. [Google Scholar] [CrossRef] [Green Version]
- Iyer, P.; Barreto, S.G.; Sahoo, B.; Chandrani, P.; Ramadwar, M.R.; Shrikhande, S.V.; Dutt, A. Non-typhoidal Salmonella DNA traces in gallbladder cancer. Infect. Agents Cancer 2016, 11, 1–4. [Google Scholar] [CrossRef] [Green Version]
- Egal-Mor, O.; Boyle, E.C.; Grassl, G.A. Same species, different diseases: How and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol. 2014, 5, 391. [Google Scholar] [CrossRef] [Green Version]
- Integraal Kankercentrum Nederland: Cijfers over Kanker. Available online: https://www.iknl.nl/nkr-cijfers (accessed on 1 March 2020).
- Huai, J.-P.; Ding, J.; Ye, X.-H.; Chen, Y.-P. Inflammatory bowel disease and risk of cholangiocarcinoma: Evidence from a meta-analysis of population-based studies. Asian Pac. J. Cancer Prev. 2014, 15, 3477–3482. [Google Scholar] [CrossRef] [Green Version]
- Massa, A.; Varamo, C.; Vita, F.; Tavolari, S.; Peraldo-Neia, C.; Brandi, G.; Rizzo, A.; Cavalloni, G.; Aglietta, M. Evolution of the Experimental Models of Cholangiocarcinoma. Cancers 2020, 12, 2308. [Google Scholar] [CrossRef]
- Rizzo, A.; Ricci, A.D.; Tober, N.; Nigro, M.C.; Mosca, M.; Palloni, A.; Abbati, F.; Frega, G.; De Lorenzo, S.; Tavolari, S.; et al. Second-line Treatment in Advanced Biliary Tract Cancer: Today and Tomorrow. Anticancer Res. 2020, 40, 3013–3030. [Google Scholar] [CrossRef] [PubMed]
- Havelaar, A.H.; Ivarsson, S.; Löfdahl, M.; Nauta, M. Estimating the true incidence of campylobacteriosis and salmonellosis in the European Union, 2009. Epidemiol. Infect. 2012, 141, 293–302. [Google Scholar] [CrossRef] [PubMed]
- Friesema, I.; Koppeschaar, C.; Donker, G.; Dijkstra, F.; Van Noort, S.; Smallenburg, R.; Van Der Hoek, W.; Van Der Sande, M. Internet-based monitoring of influenza-like illness in the general population: Experience of five influenza seasons in the Netherlands. Vaccine 2009, 27, 6353–6357. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- A Iacobuzio-Donahue, C. Genetic evolution of pancreatic cancer: Lessons learnt from the pancreatic cancer genome sequencing project. Gut 2012, 61, 1085–1094. [Google Scholar] [CrossRef]
- Van Pelt, W.; De Wit, M.A.S.; Wannet, W.J.B.; Ligtvoet, E.J.J.; Widdowson, M.A.; Van Duynhoven, Y.T.H.P. Laboratory surveillance of bacterial gastroenteric pathogens in The Netherlands, 1991–2001. Epidemiol. Infect. 2003, 130, 431–441. [Google Scholar] [CrossRef] [Green Version]
- Casparie, M.; Tiebosch, A.T.M.G.; Burger, G.; Blauwgeers, H.; Van De Pol, A.; Van Krieken, J.H.J.M.; A Meijer, G. Pathology Databanking and Biobanking in The Netherlands, a Central Role for PALGA, the Nationwide Histopathology and Cytopathology Data Network and Archive. Cell. Oncol. 2007, 29, 19–24. [Google Scholar] [CrossRef]
- Van Der Willik, K.D.; Ruiter, R.; Van Rooij, F.J.; Heemst, J.V.; Hogewoning, S.J.; Timmermans, K.C.; Visser, O.; Schagen, S.B.; Ikram, M.A.; Stricker, B.H. Ascertainment of cancer in longitudinal research: The concordance between the Rotterdam Study and the Netherlands Cancer Registry. Int. J. Cancer 2019. [Google Scholar] [CrossRef] [Green Version]
Characteristic | N (%) | Type |
---|---|---|
Age | Salmonellosis | |
<40 | 6167 (38%) | |
40–49 | 2190 (13%) | |
50–59 | 2445 (15%) | |
60–69 | 2273 (14%) | |
70–79 | 2003 (12%) | |
80+ | 1172 (7%) | |
Sex | ||
Male | 7640 (47%) | |
Female | 8612 (53%) | |
Salmonella enterica serotype | ||
Typhimurium/monophasic var. | 4487 (28%) | |
Enteritidis | 5544 (34%) | |
(Para)Typhi | 318 (2%) | |
Other serotypes and S. spp. | 5903 (36%) | |
Type of infection | ||
Septicemic | 884 (5%) | |
Enteric | 13,864 (88%) | |
Other | 1066 (7%) | |
Age | Campylobacterosis | |
<40 | 10,125 (37%) | |
40–49 | 4499 (16%) | |
50–59 | 4985 (18%) | |
60–69 | 4153 (15%) | |
70–79 | 2703 (10%) | |
80+ | 1227 (4%) | |
Sex | ||
Male | 14,293 (52%) | |
Female | 13,399 (48%) | |
Campylobacter species | ||
C. jejuni | 23,647 (85%) | |
C. coli | 1910 (7%) | |
Other species | 2135 (8%) | |
Type of infection | ||
Septicemic | 1 | |
Enteric | 1 | |
Other | 1 |
Characteristic | N (%)/Median (95% CI) |
---|---|
Age | |
<40 | 99 (1%) |
40–49 | 326 (4%) |
50–59 | 993 (12%) |
60–69 | 2048 (24%) |
70–79 | 2851 (33%) |
80+ | 2189 (26%) |
Sex | |
Male | 3822 (45%) |
Female | 4684 (55%) |
Tumor location | |
Gallbladder | 2586 (30%) |
Bile ducts, NOS | 2421 (28%) |
Proximal bile ducts | 1846 (22%) |
Distal bile ducts | 1490 (18%) |
Other 1 | 163 (2%) |
Clinical stage | |
Non-metastatic | 4078 (48%) |
Metastatic | 4428 (52%) |
Treatment | |
Resection | 2479 (29%) |
Chemotherapy | 647 (8%) |
Survival (months) | 5.8 (5.5–6.0) |
Characteristic | N (%) |
---|---|
Sex (male) | 5 (56%) |
Age | |
<60 | 3 (33%) |
≥60 | 6 (66%) |
Serotype | |
Enteritidis | 4 (45%) |
Typhimurium/monophasic var. | 2 (22%) |
Other | 3 (33%) |
Interval | |
<60 months | 7 (78%) |
≥60 months | 2 (22%) |
Tumor location | |
Gallbladder/proximal bile ducts | 2 (22%) |
Distal bile ducts | 2 (22%) |
Extrahepatic bile ducts, NOS | 5 (56%) |
Base of diagnosis | |
Cytology/imaging | 6 (67%) |
Histology | 3 (33%) |
Characteristic | N (%) |
---|---|
Sex (male) | 3 (43%) |
Age | |
<60 | 2 (29%) |
≥60 | 5 (71%) |
Interval | |
<60 months | 3 (43%) |
≥60 months | 4 (57%) |
Tumor location | |
Gallbladder/proximal bile ducts | 1 |
Distal bile ducts | 1 |
Extrahepatic bile ducts, NOS | 0 (0%) |
Base of diagnosis | |
Cytology/imaging | 2 (29%) |
Histology | 5 (71%) |
Type | Observed Incidence | Expected Incidence | SIR | 95% CI | p-Value |
---|---|---|---|---|---|
Salmonella spp. | |||||
All patients | 9 | 5.875 | 1.53 | 0.70–2.91 | 0.280 |
20–60 | 3 | 1.740 | 1.72 | 0.36–5.04 | 0.507 |
Male | 5 | 2.665 | 1.88 | 0.61–4.38 | 0.264 |
Female | 4 | 3.289 | 1.22 | 0.33–3.11 | 0.835 |
Campylobacter spp. | |||||
All patients | 7 | 7.221 | 0.97 | 0.39–2.00 | 0.868 |
20–60 | 2 | 2.126 | 0.94 | 0.11–3.40 | 0.715 |
Male | 3 | 4.025 | 0.75 | 0.15–2.18 | 0.857 |
Female | 4 | 3.233 | 1.24 | 0.34–3.17 | 0.810 |
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de Savornin Lohman, E.; Duijster, J.; Groot Koerkamp, B.; van der Post, R.; Franz, E.; Mughini Gras, L.; de Reuver, P. Severe Salmonella spp. or Campylobacter spp. Infection and the Risk of Biliary Tract Cancer: A Population-Based Study. Cancers 2020, 12, 3348. https://doi.org/10.3390/cancers12113348
de Savornin Lohman E, Duijster J, Groot Koerkamp B, van der Post R, Franz E, Mughini Gras L, de Reuver P. Severe Salmonella spp. or Campylobacter spp. Infection and the Risk of Biliary Tract Cancer: A Population-Based Study. Cancers. 2020; 12(11):3348. https://doi.org/10.3390/cancers12113348
Chicago/Turabian Stylede Savornin Lohman, Elise, Janneke Duijster, Bas Groot Koerkamp, Rachel van der Post, Eelco Franz, Lapo Mughini Gras, and Philip de Reuver. 2020. "Severe Salmonella spp. or Campylobacter spp. Infection and the Risk of Biliary Tract Cancer: A Population-Based Study" Cancers 12, no. 11: 3348. https://doi.org/10.3390/cancers12113348