Impact of Ascending HPV Infection on Colorectal Cancer Risk: Evidence from a Nationwide Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Database Sources
2.2. Study Population
2.3. Urbanization Classification
2.4. Comorbidities
2.5. Statistical Analysis
3. Results
3.1. Baseline Characteristics
3.2. Risk Relationship between HPV and Cumulative Incidence of CRC
3.3. Cox Regression
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Charde, S.H.; Warbhe, R.A. Human Papillomavirus Prevention by Vaccination: A Review Article. Cureus 2022, 14, e30037. [Google Scholar] [CrossRef] [PubMed]
- Hsu, C.H.; Lin, Y.J.; Chen, Y.C.; Liu, I.L.; You, S.L.; Hu, J.M.; Lin, T.C.; Chang, P.K.; Chen, C.Y.; Chou, Y.C.; et al. Human Papillomavirus and Risk of Colorectal Cancer: An Analysis of Nationwide Claims Data. Medicina 2022, 58, 1461. [Google Scholar] [CrossRef] [PubMed]
- Ibragimova, M.K.; Tsyganov, M.M.; Litviakov, N.V. Human papillomavirus and colorectal cancer. Med. Oncol. 2018, 35, 140. [Google Scholar] [CrossRef] [PubMed]
- Morgan, E.; Arnold, M.; Gini, A.; Lorenzoni, V.; Cabasag, C.J.; Laversanne, M.; Vignat, J.; Ferlay, J.; Murphy, N.; Bray, F. Global burden of colorectal cancer in 2020 and 2040: Incidence and mortality estimates from GLOBOCAN. Gut 2023, 72, 338–344. [Google Scholar] [CrossRef] [PubMed]
- Balkhi, B.; Alghamdi, A.; Alqahtani, S.; Al Najjar, M.; Al Harbi, A.; Bin Traiki, T. Colorectal cancer-related resource utilization and healthcare costs in Saudi Arabia. Saudi Pharm. J. 2023, 31, 101822. [Google Scholar] [CrossRef]
- Bernabe-Dones, R.D.; Gonzalez-Pons, M.; Villar-Prados, A.; Lacourt-Ventura, M.; Rodriguez-Arroyo, H.; Fonseca-Williams, S.; Velazquez, F.E.; Diaz-Algorri, Y.; Lopez-Diaz, S.M.; Rodriguez, N.; et al. High Prevalence of Human Papillomavirus in Colorectal Cancer in Hispanics: A Case-Control Study. Gastroenterol. Res. Pract. 2016, 2016, 7896716. [Google Scholar] [CrossRef]
- Liu, B.; Taioli, E. Associations between human papillomavirus and history of cancer among U.S. adults in the National Health and Nutrition Examination Survey (2003–2010). Br. J. Cancer 2014, 111, 1448–1453. [Google Scholar] [CrossRef]
- Buitrago-Perez, A.; Garaulet, G.; Vazquez-Carballo, A.; Paramio, J.M.; Garcia-Escudero, R. Molecular Signature of HPV-Induced Carcinogenesis: pRb, p53 and Gene Expression Profiling. Curr. Genom. 2009, 10, 26–34. [Google Scholar] [CrossRef]
- Damin, D.C.; Ziegelmann, P.K.; Damin, A.P. Human papillomavirus infection and colorectal cancer risk: A meta-analysis. Colorectal Dis. 2013, 15, e420–e428. [Google Scholar] [CrossRef]
- Lima, S.F.J.; Tavares, M.M.; Macedo, J.L.; Oliveira, R.S.; Heraclio, S.A.; Maia, M.M.; Souza, P.R.; Moura, R.; Crovella, S. Influence of IL-6, IL-8, and TGF-beta1 gene polymorphisms on the risk of human papillomavirus-infection in women from Pernambuco, Brazil. Mem. Inst. Oswaldo Cruz 2016, 111, 663–669. [Google Scholar] [CrossRef]
- Vahedpour, Z.; Abedzadeh-Kalahroudi, M.; Sehat, M.; Piroozmand, A.; Memar, M. Comparison of Cervical Levels of Interleukins-6 and -8 in Patients with and without Cervical Intraepithelial Neoplasia. Asian Pac. J. Cancer Prev. 2021, 22, 1225–1230. [Google Scholar] [CrossRef] [PubMed]
- Das, C.R.; Tiwari, D.; Dongre, A.; Khan, M.A.; Husain, S.A.; Sarma, A.; Bose, S.; Bose, P.D. Deregulated TNF-Alpha Levels Along with HPV Genotype 16 Infection Are Associated with Pathogenesis of Cervical Neoplasia in Northeast Indian Patients. Viral Immunol. 2018, 31, 282–291. [Google Scholar] [CrossRef]
- Hong, H.S.; Akhavan, J.; Lee, S.H.; Kim, R.H.; Kang, M.K.; Park, N.H.; Shin, K.H. Proinflammatory cytokine TNFalpha promotes HPV-associated oral carcinogenesis by increasing cancer stemness. Int. J. Oral. Sci. 2020, 12, 3. [Google Scholar] [CrossRef] [PubMed]
- Alotaibi, A.G.; Li, J.V.; Gooderham, N.J. Tumour necrosis factor-alpha (TNF-alpha) enhances dietary carcinogen-induced DNA damage in colorectal cancer epithelial cells through activation of JNK signaling pathway. Toxicology 2021, 457, 152806. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.T.; Li, W.; Liu, Q.; Guan, X.; Hu, J. Dendritic cells treated with HPV16mE7 in a three-dimensional model promote the secretion of IL-12p70 and IFN-gamma. Exp. Mol. Pathol. 2011, 91, 325–330. [Google Scholar] [CrossRef] [PubMed]
- Engel, M.A.; Neurath, M.F. Anticancer properties of the IL-12 family—Focus on colorectal cancer. Curr. Med. Chem. 2010, 17, 3303–3308. [Google Scholar] [CrossRef]
- Lorenzon, L.; Ferri, M.; Pilozzi, E.; Torrisi, M.R.; Ziparo, V.; French, D. Human papillomavirus and colorectal cancer: Evidences and pitfalls of published literature. Int. J. Colorectal Dis. 2011, 26, 135–142. [Google Scholar] [CrossRef]
- Ranjbar, R.; Saberfar, E.; Shamsaie, A.; Ghasemian, E. The aetiological role of human papillomavirus in colorectal carcinoma: An Iranian population- based case control study. Asian Pac. J. Cancer Prev. 2014, 15, 1521–1525. [Google Scholar] [CrossRef]
- Chesson, H.W.; Laprise, J.F.; Brisson, M.; Martin, D.; Ekwueme, D.U.; Markowitz, L.E. The Estimated Lifetime Medical Cost of Diseases Attributable to Human Papillomavirus Infections Acquired in 2018. Sex. Transm. Dis. 2021, 48, 278–284. [Google Scholar] [CrossRef]
- Goldsbury, D.E.; Feletto, E.; Weber, M.F.; Haywood, P.; Pearce, A.; Lew, J.B.; Worthington, J.; He, E.; Steinberg, J.; O’Connell, D.L.; et al. Health system costs and days in hospital for colorectal cancer patients in New South Wales, Australia. PLoS ONE 2021, 16, e0260088. [Google Scholar] [CrossRef]
- Chae, Y.K.; Valsecchi, M.E.; Kim, J.; Bianchi, A.L.; Khemasuwan, D.; Desai, A.; Tester, W. Reduced risk of breast cancer recurrence in patients using ACE inhibitors, ARBs, and/or statins. Cancer Investig. 2011, 29, 585–593. [Google Scholar] [CrossRef] [PubMed]
- Giovannucci, E.; Harlan, D.M.; Archer, M.C.; Bergenstal, R.M.; Gapstur, S.M.; Habel, L.A.; Pollak, M.; Regensteiner, J.G.; Yee, D. Diabetes and cancer: A consensus report. Diabetes Care 2010, 33, 1674–1685. [Google Scholar] [CrossRef] [PubMed]
- Renehan, A.G.; Tyson, M.; Egger, M.; Heller, R.F.; Zwahlen, M. Body-mass index and incidence of cancer: A systematic review and meta-analysis of prospective observational studies. Lancet 2008, 371, 569–578. [Google Scholar] [CrossRef]
- Lin, L.Y.; Warren-Gash, C.; Smeeth, L.; Chen, P.C. Data resource profile: The National Health Insurance Research Database (NHIRD). Epidemiol. Health 2018, 40, e2018062. [Google Scholar] [CrossRef] [PubMed]
- Lin, H.Y.; Ho, C.H.; Lin, Y.S.; Kuo, S.C.; Chen, Y.C.; Cheng, Y.J. Retinoblastoma Incidence in Taiwan Over a Recent 20-Year Period: A Comprehensive Nationwide Study. Int. J. Gen. Med. 2024, 17, 909–917. [Google Scholar] [CrossRef]
- Kao, S.S.; Li, C.J.; Wei, J.C.; Lin, C.L.; Chang, R.; Hung, Y.M. Human Papillomavirus Infection Is Associated with Decreased Risk of Hepatocellular Carcinoma in Chronic Hepatitis C Patients: Taiwan Nationwide Matched Cohort Study. Cancers 2022, 14, 1289. [Google Scholar] [CrossRef]
- Huang, J.Y.; Lin, C.; Tsai, S.C.; Lin, F.C. Human Papillomavirus Is Associated With Adenocarcinoma of Lung: A Population-Based Cohort Study. Front. Med. 2022, 9, 932196. [Google Scholar] [CrossRef]
- Brenne, S.S.; Ness-Jensen, E.; Edna, T.H.; Lydersen, S.; Laugsand, E.A. Risk factors for right colon, left colon and rectal cancers differ between men and women: The population-based HUNT study in Norway. Colorectal Dis. 2023, 25, 44–55. [Google Scholar] [CrossRef]
- Decker, K.M.; Lambert, P.; Nugent, Z.; Biswanger, N.; Samadder, J.; Singh, H. Time Trends in the Diagnosis of Colorectal Cancer with Obstruction, Perforation, and Emergency Admission after the Introduction of Population-Based Organized Screening. JAMA Netw. Open 2020, 3, e205741. [Google Scholar] [CrossRef]
- Lu, P.J.; Liu, J.Y.; Ma, H.; Chen, T.J.; Chou, L.F.; Hwang, S.J. Characteristics of Clinics without National Health Insurance Contracts: A Nationwide Survey in Taiwan. Int. J. Environ. Res. Public Health 2022, 19, 1517. [Google Scholar] [CrossRef]
- De Marco, M.F.; Janssen-Heijnen, M.L.; van der Heijden, L.H.; Coebergh, J.W. Comorbidity and colorectal cancer according to subsite and stage: A population-based study. Eur. J. Cancer 2000, 36, 95–99. [Google Scholar] [CrossRef]
- Qiu, H.; Wang, L.; Zhou, L.; Wang, X. Comorbidity Patterns in Patients Newly Diagnosed With Colorectal Cancer: Network-Based Study. JMIR Public Health Surveill. 2023, 9, e41999. [Google Scholar] [CrossRef] [PubMed]
- Parkin, D.M. 11. Cancers attributable to infection in the UK in 2010. Br. J. Cancer 2011, 105 (Suppl. S2), S49–S56. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.Y.; Wu, P.H.; Lu, P.L.; Liang, F.W. Different Trends of Distinct Time Points of AIDS Events Following HIV Diagnosis in Various At-risk Populations: A Retrospective Nationwide Cohort Study in Taiwan. Infect. Dis. Ther. 2021, 10, 1715–1732. [Google Scholar] [CrossRef] [PubMed]
- Kaneko, H.; Yano, Y.; Itoh, H.; Morita, K.; Kiriyama, H.; Kamon, T.; Fujiu, K.; Michihata, N.; Jo, T.; Takeda, N.; et al. Untreated Hypertension and Subsequent Incidence of Colorectal Cancer: Analysis of a Nationwide Epidemiological Database. J. Am. Heart Assoc. 2021, 10, e022479. [Google Scholar] [CrossRef]
- Xuan, K.; Zhao, T.; Sun, C.; Patel, A.S.; Liu, H.; Chen, X.; Qu, G.; Sun, Y. The association between hypertension and colorectal cancer: A meta-analysis of observational studies. Eur. J. Cancer Prev. 2021, 30, 84–96. [Google Scholar] [CrossRef]
- Yu, G.H.; Li, S.F.; Wei, R.; Jiang, Z. Diabetes and Colorectal Cancer Risk: Clinical and Therapeutic Implications. J. Diabetes Res. 2022, 2022, 1747326. [Google Scholar] [CrossRef]
- Boccardo, E.; Lepique, A.P.; Villa, L.L. The role of inflammation in HPV carcinogenesis. Carcinogenesis 2010, 31, 1905–1912. [Google Scholar] [CrossRef]
- Liu, X.; Ma, X.; Lei, Z.; Feng, H.; Wang, S.; Cen, X.; Gao, S.; Jiang, Y.; Jiang, J.; Chen, Q.; et al. Chronic Inflammation-Related HPV: A Driving Force Speeds Oropharyngeal Carcinogenesis. PLoS ONE 2015, 10, e0133681. [Google Scholar] [CrossRef]
- Moody, C.A.; Laimins, L.A. Human papillomavirus oncoproteins: Pathways to transformation. Nat. Rev. Cancer 2010, 10, 550–560. [Google Scholar] [CrossRef]
- Ghabreau, L.; Segal, E.; Yasmeen, A.; Kassab, A.; Akil, N.; Moustafa, A.-E.A. High-risk human papillomavirus infections in colorectal cancer in the Syrian population and their association with Fascin, Id-1 and P-cadherin expressions: A tissue microarray study. Clin. Cancer Investig. J. 2012, 1, 26–30. [Google Scholar] [CrossRef]
- Bodaghi, S.; Yamanegi, K.; Xiao, S.Y.; Da Costa, M.; Palefsky, J.M.; Zheng, Z.M. Colorectal papillomavirus infection in patients with colorectal cancer. Clin. Cancer Res. 2005, 11, 2862–2867. [Google Scholar] [CrossRef] [PubMed]
- Sunthamala, N.; Pang, C.L.; Thierry, F.; Teissier, S.; Pientong, C.; Ekalaksananan, T. Genome-wide analysis of high risk human papillomavirus E2 proteins in human primary keratinocytes. Genom. Data 2014, 2, 147–149. [Google Scholar] [CrossRef] [PubMed]
- Goto, N.; Westcott, P.M.K.; Goto, S.; Imada, S.; Taylor, M.S.; Eng, G.; Braverman, J.; Deshpande, V.; Jacks, T.; Agudo, J.; et al. SOX17 enables immune evasion of early colorectal adenomas and cancers. Nature 2024, 627, 636–645. [Google Scholar] [CrossRef]
- Elshikh, M.; Moawad, A.W.; Salem, U.; Klimkowski, S.P.; Hassan, T.; Rao Korivi, B.; Jensen, C.T.; Javadi, S.; Elsayes, K.M. Oncologic Imaging of the Lymphatic System: Current Perspective with Multi-Modality Imaging and New Horizon. Cancers 2021, 13, 4554. [Google Scholar] [CrossRef]
- Yamagata, K.; Kumagai, K.; Shimizu, K.; Masuo, K.; Nishida, Y.; Yasui, A. Gastrointestinal cancer metastasis and lymphogenous spread: Viewpoint of animal models of lymphatic obstruction. Jpn. J. Clin. Oncol. 1998, 28, 104–106. [Google Scholar] [CrossRef]
- Damin, D.C.; Caetano, M.B.; Rosito, M.A.; Schwartsmann, G.; Damin, A.S.; Frazzon, A.P.; Ruppenthal, R.D.; Alexandre, C.O. Evidence for an association of human papillomavirus infection and colorectal cancer. Eur. J. Surg. Oncol. 2007, 33, 569–574. [Google Scholar] [CrossRef] [PubMed]
- Perez, L.O.; Abba, M.C.; Laguens, R.M.; Golijow, C.D. Analysis of adenocarcinoma of the colon and rectum: Detection of human papillomavirus (HPV) DNA by polymerase chain reaction. Colorectal Dis. 2005, 7, 492–495. [Google Scholar] [CrossRef] [PubMed]
- Chang, Y.F.; Yan, G.J.; Liu, G.C.; Hong, Y.; Chen, H.L.; Jiang, S.; Zhong, Y.; Xiyang, Y.B.; Hu, T. HPV16 E6 Promotes the Progression of HPV Infection-Associated Cervical Cancer by Upregulating Glucose-6-Phosphate Dehydrogenase Expression. Front. Oncol. 2021, 11, 718781. [Google Scholar] [CrossRef]
- Khan, S.F.; Burmeister, C.A.; Scott, D.J.; Sinkala, M.; Ramburan, A.; Wu, H.T.; Schafer, G.; Katz, A.A.; Prince, S. TBX3 Promotes Cervical Cancer Proliferation and Migration via HPV E6 and E7 Signaling. Mol. Cancer Res. 2023, 21, 345–358. [Google Scholar] [CrossRef]
- Bonin-Jacob, C.M.; Almeida-Lugo, L.Z.; Puga, M.A.M.; Machado, A.P.; Padovani, C.T.J.; Noceti, M.C.; Ferreira, A.M.T.; Fernandes, C.; Resende, J.C.P.; Bovo, A.C.; et al. IL-6 and IL-10 in the serum and exfoliated cervical cells of patients infected with high-risk human papillomavirus. PLoS ONE 2021, 16, e0248639. [Google Scholar] [CrossRef] [PubMed]
- Morgan, E.L.; Macdonald, A. Autocrine STAT3 activation in HPV positive cervical cancer through a virus-driven Rac1-NFkappaB-IL-6 signalling axis. PLoS Pathog. 2019, 15, e1007835. [Google Scholar] [CrossRef] [PubMed]
- Amador-Molina, A.; Hernandez-Valencia, J.F.; Lamoyi, E.; Contreras-Paredes, A.; Lizano, M. Role of innate immunity against human papillomavirus (HPV) infections and effect of adjuvants in promoting specific immune response. Viruses 2013, 5, 2624–2642. [Google Scholar] [CrossRef] [PubMed]
- Gravitt, P.E. Evidence and impact of human papillomavirus latency. Open Virol. J. 2012, 6, 198–203. [Google Scholar] [CrossRef]
- Darwanto, A.; Hein, A.M.; Strauss, S.; Kong, Y.; Sheridan, A.; Richards, D.; Lader, E.; Ngowe, M.; Pelletier, T.; Adams, D.; et al. Use of the QIAGEN GeneReader NGS system for detection of KRAS mutations, validated by the QIAGEN Therascreen PCR kit and alternative NGS platform. BMC Cancer 2017, 17, 358. [Google Scholar] [CrossRef]
- Leung, E.; Han, K.; Zou, J.; Zhao, Z.; Zheng, Y.; Wang, T.T.; Rostami, A.; Siu, L.L.; Pugh, T.J.; Bratman, S.V. HPV Sequencing Facilitates Ultrasensitive Detection of HPV Circulating Tumor DNA. Clin. Cancer Res. 2021, 27, 5857–5868. [Google Scholar] [CrossRef]
- Phelps, R.A.; Broadbent, T.J.; Stafforini, D.M.; Jones, D.A. New perspectives on APC control of cell fate and proliferation in colorectal cancer. Cell Cycle 2009, 8, 2549–2556. [Google Scholar] [CrossRef]
- Rosenberg, D.W.; Giardina, C.; Tanaka, T. Mouse models for the study of colon carcinogenesis. Carcinogenesis 2009, 30, 183–196. [Google Scholar] [CrossRef]
- Yuan, Y.; Liu, L.; Chen, H.; Wang, Y.; Xu, Y.; Mao, H.; Li, J.; Mills, G.B.; Shu, Y.; Li, L.; et al. Comprehensive Characterization of Molecular Differences in Cancer between Male and Female Patients. Cancer Cell 2016, 29, 711–722. [Google Scholar] [CrossRef]
- Hasakova, K.; Bezakova, J.; Vician, M.; Reis, R.; Zeman, M.; Herichova, I. Gender-dependent expression of leading and passenger strand of miR-21 and miR-16 in human colorectal cancer and adjacent colonic tissues. Physiol. Res. 2017, 66, S575–S582. [Google Scholar] [CrossRef]
- Jung, J. Role of G Protein-Coupled Estrogen Receptor in Cancer Progression. Toxicol. Res. 2019, 35, 209–214. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Zhang, M.; Wu, J.; Tang, R.; Hu, L. Oncologic Outcome and Efficacy of Chemotherapy in Colorectal Cancer Patients Aged 80 Years or Older. Front. Med. 2020, 7, 525421. [Google Scholar] [CrossRef] [PubMed]
- Giefing-Kroll, C.; Berger, P.; Lepperdinger, G.; Grubeck-Loebenstein, B. How sex and age affect immune responses, susceptibility to infections, and response to vaccination. Aging Cell 2015, 14, 309–321. [Google Scholar] [CrossRef] [PubMed]
- Marquez, E.J.; Chung, C.H.; Marches, R.; Rossi, R.J.; Nehar-Belaid, D.; Eroglu, A.; Mellert, D.J.; Kuchel, G.A.; Banchereau, J.; Ucar, D. Sexual-dimorphism in human immune system aging. Nat. Commun. 2020, 11, 751. [Google Scholar] [CrossRef] [PubMed]
- Enayatrad, M.; Yavari, P.; Vahedi, H.; Mahdavi, S.; Etemad, K.; Khodakarim, S. Urbanization Levels and Its Association with Prevalence of Risk Factors and Colorectal Cancer Incidence. Iran. J. Public Health 2021, 50, 2317–2325. [Google Scholar] [CrossRef]
- Norgaard, M.; Iversen, L.H.; Sorensen, H.T. Colorectal cancer. Incidence and risk factors. Ugeskr. Laeger 2005, 167, 4157–4159. [Google Scholar]
- Coughlin, S.S.; Richards, T.B.; Thompson, T.; Miller, B.A.; VanEenwyk, J.; Goodman, M.T.; Sherman, R.L. Rural/nonrural differences in colorectal cancer incidence in the United States, 1998–2001. Cancer 2006, 107, 1181–1188. [Google Scholar] [CrossRef]
- Giovannucci, E. Modifiable risk factors for colon cancer. Gastroenterol. Clin. N. Am. 2002, 31, 925–943. [Google Scholar] [CrossRef]
- Amirsasan, R.; Akbarzadeh, M.; Akbarzadeh, S. Exercise and colorectal cancer: Prevention and molecular mechanisms. Cancer Cell Int. 2022, 22, 247. [Google Scholar] [CrossRef]
- Mohan, V.; Mathur, P.; Deepa, R.; Deepa, M.; Shukla, D.K.; Menon, G.R.; Anand, K.; Desai, N.G.; Joshi, P.P.; Mahanta, J.; et al. Urban rural differences in prevalence of self-reported diabetes in India—The WHO-ICMR Indian NCD risk factor surveillance. Diabetes Res. Clin. Pract. 2008, 80, 159–168. [Google Scholar] [CrossRef]
- Nagata, N.; Watanabe, K.; Nishijima, T.; Tadokoro, K.; Watanabe, K.; Shimbo, T.; Niikura, R.; Sekine, K.; Akiyama, J.; Teruya, K.; et al. Prevalence of Anal Human Papillomavirus Infection and Risk Factors among HIV-positive Patients in Tokyo, Japan. PLoS ONE 2015, 10, e0137434. [Google Scholar] [CrossRef]
- Hsu, Y.C. The History and Cultural Research of Taiwan Cuisine. Master’s Thesis, Tamkang University, New Taipei City, Taiwan, 2013. [Google Scholar]
- Chou, L.N.; Chen, M.L. Influencing Factors of the Body Mass Index of Elementary Students in Southern Taiwan. Int. J. Environ. Res. Public Health 2017, 14, 220. [Google Scholar] [CrossRef]
- Lin, S.F.; Kuo, T.T.; Pan, W.H.; Bai, C.H. Effects of socioeconomic status on the control of hypertension in patients <65 and >/=65 years of age in Taiwan: A nationwide cross-sectional study. BMJ Open 2022, 12, e050041. [Google Scholar] [CrossRef]
- Lu, F.H.; Tang, S.J.; Wu, J.S.; Yang, Y.C.; Chang, C.J. Hypertension in elderly persons: Its prevalence and associated cardiovascular risk factors in Tainan City, southern Taiwan. J. Gerontol. A Biol. Sci. Med. Sci. 2000, 55, M463–M468. [Google Scholar] [CrossRef] [PubMed]
- Neo, J.H.; Malcontenti-Wilson, C.; Muralidharan, V.; Christophi, C. Effect of ACE inhibitors and angiotensin II receptor antagonists in a mouse model of colorectal cancer liver metastases. J. Gastroenterol. Hepatol. 2007, 22, 577–584. [Google Scholar] [CrossRef] [PubMed]
- Dekker, E.; Tanis, P.J.; Vleugels, J.L.A.; Kasi, P.M.; Wallace, M.B. Colorectal cancer. Lancet 2019, 394, 1467–1480. [Google Scholar] [CrossRef] [PubMed]
- Lv, Y.; Lin, S.; Liu, M.; Wang, L.; Wang, X.; Cui, L.; Xu, J. Impacts of pre-existing diabetes mellitus on colorectal cancer in a mice model. Cancer Med. 2023, 12, 11641–11650. [Google Scholar] [CrossRef]
- Won, E.J.; Ju, J.K.; Cho, Y.N.; Jin, H.M.; Park, K.J.; Kim, T.J.; Kwon, Y.S.; Kee, H.J.; Kim, J.C.; Kee, S.J.; et al. Clinical relevance of circulating mucosal-associated invariant T cell levels and their anti-cancer activity in patients with mucosal-associated cancer. Oncotarget 2016, 7, 76274–76290. [Google Scholar] [CrossRef]
- Shuwen, H.; Xi, Y.; Quan, Q.; Yuefen, P.; Miao, D.; Qing, Z. Relationship between intestinal microorganisms and T lymphocytes in colorectal cancer. Future Oncol. 2019, 15, 1655–1666. [Google Scholar] [CrossRef]
- He, M.M.; Fang, Z.; Hang, D.; Wang, F.; Polychronidis, G.; Wang, L.; Lo, C.H.; Wang, K.; Zhong, R.; Knudsen, M.D.; et al. Circulating liver function markers and colorectal cancer risk: A prospective cohort study in the UK Biobank. Int. J. Cancer 2021, 148, 1867–1878. [Google Scholar] [CrossRef]
- Engstrand, J.; Nilsson, H.; Stromberg, C.; Jonas, E.; Freedman, J. Colorectal cancer liver metastases—A population-based study on incidence, management and survival. BMC Cancer 2018, 18, 78. [Google Scholar] [CrossRef] [PubMed]
- Hamoud, A.R.; Weaver, L.; Stec, D.E.; Hinds, T.D., Jr. Bilirubin in the Liver-Gut Signaling Axis. Trends Endocrinol. Metab. 2018, 29, 140–150. [Google Scholar] [CrossRef] [PubMed]
- Jia, W.; Xie, G.; Jia, W. Bile acid-microbiota crosstalk in gastrointestinal inflammation and carcinogenesis. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 111–128. [Google Scholar] [CrossRef] [PubMed]
Non-HPV | HPV | p | |
---|---|---|---|
Sex | 1.0000 | ||
Male | 934,908 (49.74%) | 467,454 (49.74%) | |
Female | 944,840 (50.26%) | 472,420 (50.26%) | |
Age | 1.0000 | ||
0–19 years | 513,000 (27.29%) | 256,500 (27.29%) | |
20–39 years | 669,372 (35.61%) | 334,686 (35.61%) | |
40–59 years | 469,150 (24.96%) | 234,575 (24.96%) | |
60–79 years | 191,510 (10.19%) | 95,755 (10.19%) | |
80+ years | 36,716 (1.95%) | 18,358 (1.95%) | |
Urbanization | <0.0001 | ||
1 (Highest level) | 542,433 (28.86%) | 319,694 (34.01%) | |
2 (Very high level) | 587,017 (31.23%) | 290,511 (30.91%) | |
3 (High level) | 340,505 (18.11%) | 162,859 (17.33%) | |
4 (Moderately high level) | 246,844 (13.13%) | 109,824 (11.68%) | |
5 (Moderate level) | 36,687 (1.95%) | 13,197 (1.40%) | |
6 (Low level) | 70,850 (3.77%) | 23,620 (2.51%) | |
7 (Lowest level) | 55,412 (2.95%) | 20,169 (2.15%) | |
Area | <0.0001 | ||
Taipei | 671,431 (35.72%) | 395,713 (42.10%) | |
Central | 347,664 (18.50%) | 180,479 (19.20%) | |
Northern | 279,894 (14.89%) | 124,964 (13.30%) | |
Kaohsiung, Pingtung | 276,130 (14.69%) | 115,919 (12.33%) | |
Southern | 261,434 (13.91%) | 107,447 (11.43%) | |
Eastern | 43,195 (2.30%) | 15,352 (1.63%) | |
Insurance coverage | <0.0001 | ||
Labor insurance | 1,183,084 (62.59%) | 618,250 (65.62%) | |
Unemployment | 294,431 (15.66%) | 122,189 (13.00%) | |
Agricultural, irrigation, and fishery associations | 91,295 (12.65%) | 94,204 (10.00%) | |
Low-income | 73,295 (11.11%) | 79,978 (8.84%) | |
Public insurance | 111,243 (9.39%) | 79,000 (8.41%) | |
Other | 25,492 (1.79%) | 17,858 (1.88%) | |
Co-morbidity | |||
Hypertension | 205,015 (10.91%) | 112,709 (11.99%) | <0.0001 |
Hyperlipidemia | 133,790 (7.12%) | 83,114 (8.84%) | <0.0001 |
Peptic ulcer | 122,250 (6.50%) | 74,302 (7.91%) | <0.0001 |
Diabetes mellitus | 96,584 (5.14%) | 46,782 (4.98%) | <0.0001 |
Abnormal liver function | 91,126 (4.85%) | 45,661 (4.86%) | 0.7009 |
Ischemic heart disease | 63,872 (3.40%) | 39,334 (4.19%) | <0.0001 |
Gout | 49,184 (2.62%) | 28,685 (3.05%) | <0.0001 |
Stroke | 40,087 (2.13%) | 20,246 (2.15%) | 0.2386 |
COPD | 32,326 (1.72%) | 18,607 (1.98%) | <0.0001 |
Chronic kidney diseases | 25,740 (1.37%) | 14,747 (1.57%) | <0.0001 |
Renal failure | 15,200 (0.81%) | 8191 (0.87%) | <0.0001 |
GI bleeding | 10,826 (0.58%) | 5723 (0.61%) | 0.0006 |
Adjusted HR | 95% CI | p | |
---|---|---|---|
HPV | 1.73 | 1.63–1.83 | <0.0001 |
Sex | |||
Male | 1.49 | 1.40–1.58 | <0.0001 |
Female | Reference | ||
Age | |||
0–19 years | 0.04 | 0.02–0.08 | <0.0001 |
20–39 years | Reference | ||
40–59 years | 6.81 | 6.00–7.72 | <0.0001 |
60–79 years | 21.26 | 18.67–24.20 | <0.0001 |
80+ years | 34.69 | 29.78–40.40 | <0.0001 |
Urbanization | |||
1 (Highest level) | Reference | ||
2 (Very high level) | 0.94 | 0.86–1.02 | 0.1157 |
3 (High level) | 0.98 | 0.89–1.09 | 0.7578 |
4 (Moderately high level) | 0.92 | 0.83–1.03 | 0.17 |
5 (Moderate level) | 0.87 | 0.70–1.08 | 0.2077 |
6 (Low level) | 0.71 | 0.58–0.85 | 0.0003 |
7 (Lowest level) | 0.93 | 0.77–1.13 | 0.4672 |
Area | |||
Taipei | Reference | ||
Northern | 0.95 | 0.85–1.06 | 0.3231 |
Central | 1.03 | 0.94–1.13 | 0.5037 |
Southern | 1.20 | 1.09–1.33 | 0.0004 |
Kaohsiung-Pingtung | 1.03 | 0.93–1.13 | 0.6043 |
Eastern | 0.98 | 0.78–1.22 | 0.833 |
Insurance coverage | |||
Public insurance | 0.96 | 0.85–1.08 | 0.4893 |
Labor insurance | Reference | ||
Agricultural, Irrigation, Fishery Associations | 1.09 | 0.99–1.20 | 0.0917 |
Low-income | 1.19 | 0.85–1.67 | 0.3165 |
Unemployment | 1.02 | 0.94–1.11 | 0.596 |
Other | 0.97 | 0.75–1.26 | 0.8318 |
Co-morbidity | |||
Ischemic heart disease | 0.99 | 0.91–1.08 | 0.8113 |
Hypertension | 1.22 | 1.13–1.31 | <0.0001 |
Stroke | 1.06 | 0.95–1.18 | 0.3014 |
Diabetes mellitus | 1.32 | 1.22–1.43 | <0.0001 |
Abnormal liver function | 1.18 | 1.07–1.30 | 0.001 |
Renal failure | 1.13 | 0.88–1.45 | 0.3416 |
Gastrointestinal bleed | 1.20 | 0.95–1.52 | 0.1367 |
Hyperlipidemia | 1.07 | 0.99–1.16 | 0.0921 |
Chronic kidney diseases | 1.22 | 1.00–1.50 | 0.0508 |
COPD | 1.09 | 0.97–1.23 | 0.1389 |
Peptic ulcer | 0.99 | 0.91–1.07 | 0.7521 |
Gout | 1.01 | 0.91–1.13 | 0.827 |
Subtypes | Non-HPV | HPV | ||||
---|---|---|---|---|---|---|
Event | Incidence Rate † | Event | Incidence Rate † | Crude HR | Adjusted HR | |
Colorectal cancer | 2409 | 2.70 (2.60–2.81) | 2083 | 4.70 (4.50–4.90) | 1.739 (1.640–1.844) | 1.727 (1.627–1.833) |
Colon (C18, C19) | 1694 | 1.90 (1.81–1.99) | 1487 | 3.35 (3.19–3.53) | 1.765 (1.646–1.892) | 1.739 (1.621–1.867) |
Rectum (C20) | 703 | 0.79 (0.73–0.85) | 567 | 1.28 (1.18–1.39) | 1.622 (1.452–1.811) | 1.644 (1.470–1.839) |
Anus (C21) | 12 | 0.01 (0.01–0.02) | 29 | 0.07 (0.05–0.09) | 4.856 (2.478–9.516) | 4.721 (2.394–9.310) |
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© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pan, P.-H.; Luo, C.-W.; Ting, W.-C.; Shiu, B.-H.; Huang, J.-Y.; Tsai, S.C.-S.; Lin, F.C.-F. Impact of Ascending HPV Infection on Colorectal Cancer Risk: Evidence from a Nationwide Study. Microorganisms 2024, 12, 1746. https://doi.org/10.3390/microorganisms12091746
Pan P-H, Luo C-W, Ting W-C, Shiu B-H, Huang J-Y, Tsai SC-S, Lin FC-F. Impact of Ascending HPV Infection on Colorectal Cancer Risk: Evidence from a Nationwide Study. Microorganisms. 2024; 12(9):1746. https://doi.org/10.3390/microorganisms12091746
Chicago/Turabian StylePan, Pin-Ho, Ci-Wen Luo, Wen-Chien Ting, Bei-Hao Shiu, Jing-Yang Huang, Stella Chin-Shaw Tsai, and Frank Cheau-Feng Lin. 2024. "Impact of Ascending HPV Infection on Colorectal Cancer Risk: Evidence from a Nationwide Study" Microorganisms 12, no. 9: 1746. https://doi.org/10.3390/microorganisms12091746