Frequency of BK virus genotypes in patients with colorectal cancer
-
Mahsa Javadi
,
Gholamabbas Kaydani
,
Roya Pirmoradi
,
Abdolhassan Talaiezadeh
,
Azadeh Haghi Navand
,
Mohammad Karimi Baba Ahmadi
,
Manoochehr Makvandi
Abstract
Background and Objectives: BK polyomavirus infection is prevalent and primarily asymptomatic, except for complications in kidney transplant recipients. Furthermore, its involvement in a tumorigenic family necessitates consideration in various malignancies such as urogenital tumors, prostate cancer, colorectal cancer (CRC), and brain cancer.
Materials and Methods: This investigation encompassed 50 specimens of colorectal adenocarcinoma tumors, 50 adjacent tissues, and 40 urine samples, with patients having a mean age of 61 years ± 12.4 years. The detection of BK virus DNA VP1 gene and genotyping were carried out through nested-PCR and sequencing techniques.
Results: Through the utilization of nested-PCR, BK virus DNA was identified in 15/50 (30%) colorectal tumor samples and 3/50 (6%) adjacent tissues (p-value = 0.008). Additionally, 6/40 (15%) urine samples exhibited positive results for BK virus DNA. Notably, among these findings, 9/15 BK virus positive tumor tissues (60%) and 3/6 BK virus positive urine samples (50%) were confirmed to be positive for BK virus subtype 4 (p-value < 0.001), whereas 2 tumor samples and 3 urine samples were attributed to BK virus type 1b2.
Conclusion: It is imperative to enhance one's understanding of the etiological and risk factors pertaining to cancers. The present findings offer substantiation of a potential correlation between BK virus infection and colorectal cancer. BK virus genotype 4 was found to be dominant among the CRC patients in this study.
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5. Marongiu L, Allgayer H. Viruses in colorectal cancer. Mol Oncol 2022; 16: 1423-1450.
6. Abend JR, Jiang M, Imperiale MJ. BK virus and human cancer: innocent until proven guilty. Semin Cancer Biol 2009; 19: 252-260.
7. Burger-Calderon R, Webster-Cyriaque J. Human BK Polyomavirus-The potential for head and neck malignancy and disease. Cancers (Basel) 2015; 7: 1244-1270.
8. Vaezjalali M, Azimi H, Hosseini SM, Taghavi A, Goudarzi H. Different strains of BK Polyomavirus: VP1 sequences in a group of iranian prostate cancer patients. Urol J 2018; 15: 44-48.
9. Moens U, Van Ghelue M, Ehlers B. Are human polyomaviruses co-factors for cancers induced by other oncoviruses? Rev Med Virol 2014; 24: 343-360.
10. Comar M, Bonifacio D, Zanconati F, Di Napoli M, Isidoro E, Martini F, et al. High prevalence of BK polyomavirus sequences in human papillomavirus-16-positive precancerous cervical lesions. J Med Virol 2011; 83: 1770-1776.
11. Jarzynski A, Zajac P, Zebrowski R, Boguszewska A, Polz-Dacewicz M. Occurrence of BK virus and human papilloma virus in colorectal cancer. Ann Agric Environ Med 2017; 24: 440-445.
12. Abolbashari S, Shakeri M, Hami M, Gholoobi A, Hooshyar Chechaklou A, Damavandi M, et al. Higher viral load of polyomavirus type BK but not JC among Renal transplant recipients in comparison to donors. Iran J Pathol 2022; 17: 8-14.
13. Kotla SK, Kadambi PV, Hendricks AR, Rojas R. BK polyomavirus-pathogen, paradigm and puzzle. Nephrol Dial Transplant 2021; 36: 587-593.
14. Krajewski W, Kaminska D, Poterek A, Malkiewicz B, Klak J, Zdrojowy R, et al. Pathogenicity of BK virus on the urinary system. Cent European J Urol 2020; 73: 94-103.
15. Levican J, Acevedo M, Leon O, Gaggero A, Aguayo F. Role of BK human polyomavirus in cancer. Infect Agent Cancer 2018; 13: 12.
16. Villani S, Gagliano N, Procacci P, Sartori P, Comar M, Provenzano M, et al. Characterization of an in vitro model to study the possible role of polyomavirus BK in prostate cancer. J Cell Physiol 2019; 234: 11912-11922.
17. Saber Amoli S, Zebardast A, Keyvani H, Yahyapour Y, Ghodsi SM, Maniati M, et al. Prevalence and viral load determination of BK polyomavirus among Iranian patients with brain tumors. Caspian J Intern Med 2021; 12: 173-179.
18. Burger-Calderon R, Ramsey KJ, Dolittle-Hall JM, Seaman WT, Jeffers-Francis LK, Tesfu D, et al. Distinct BK polyomavirus non-coding control region (NCCR) variants in oral fluids of HIV- associated Salivary Gland Disease patients. Virology 2016; 493: 255-266.
19. Starrett GJ, Buck CB. The case for BK polyomavirus as a cause of bladder cancer. Curr Opin Virol 2019; 39: 8-15.
20. Javadi M, Jalilian S, Kanani M, Kia V, Talaiezadeh A, Angali KA, et al. Time to take HPV infection in colorectal cancer patients more seriously. Front Med (Lausanne) 2024; 11: 1418359.
21. Anzivino E, Bellizzi A, Mitterhofer AP, Tinti F, Barile M, Colosimo MT, et al. Early monitoring of the human polyomavirus BK replication and sequencing analysis in a cohort of adult kidney transplant patients treated with basiliximab. Virol J 2011; 8: 407.
22. Tarharoudi R, Sari S, Sakhaee F, Vaziri F, Rahimi Jamnani F, Siadat SD, et al. BK polyomavirus in Iranian patients with papillary thyroid cancer: Is it a major future challenge? J Med Virol 2022; 94: 6023-6027.
23. Delbue S, Matei DV, Carloni C, Pecchenini V, Carluccio S, Villani S, et al. Evidence supporting the association of polyomavirus BK genome with prostate cancer. Med Microbiol Immunol 2013; 202: 425-430.
24. Tseng CE, Yeh CM, Fang CY, Shay J, Chen PL, Lin MC, et al. Detection of human JCPyV and BKPyV in diffuse large B-cell lymphoma of the GI tract. Eur J Clin Microbiol Infect Dis 2014; 33: 665-672.
25. Casini B, Borgese L, Del Nonno F, Galati G, Izzo L, Caputo M, et al. Presence and incidence of DNA sequences of human polyomaviruses BKV and JCV in colorectal tumor tissues. Anticancer Res 2005; 25: 1079-1085.
26. Sarvari J, Mahmoudvand S, Pirbonyeh N, Safaei A, Hosseini SY. The very low frequency of Epstein-Barr JC and BK Viruses DNA in Colorectal cancer tissues in Shiraz, Southwest Iran. Pol J Microbiol 2018; 67: 73-79.
27. Khabaz MN, Nedjadi T, Gari MA, Al-Maghrabi JA, Atta HM, Basuni AA, et al. BK polyomavirus association with colorectal cancer development. Genet Mol Res 2016; 15: 10.4238/gmr.15027841.
28. Zheng HY, Nishimoto Y, Chen Q, Hasegawa M, Zhong S, Ikegaya H, et al. Relationships between BK virus lineages and human populations. Microbes Infect 2007; 9: 204-213.
29. Kaydani GA, Makvandi M, Samarbafzadeh A, Shahbazian H, Hamidi Fard M. Prevalence and distribution of BK virus subtypes in renal transplant recipients referred to Golestan hospital in Ahvaz, Iran. Jundishapur J Microbiol 2015; 8(3): e16738.
30. Karimi Dehcheshmeh L, Makvandi M, Timori A. Prevalence of human Polyomavirus JC and BK in normal population. Asian Pac J Cancer Prev 2020; 21: 2877-2882.
31. Muller DC, Ramo M, Naegele K, Ribi S, Wetterauer C, Perrina V, et al. Donor-derived, metastatic urothelial cancer after kidney transplantation associated with a potentially oncogenic BK polyomavirus. J Pathol 2018; 244: 265-270.
32. Iaconelli M, Petricca S, Libera SD, Di Bonito P, La Rosa G. First detection of human Papillomaviruses and human Polyomaviruses in river waters in Italy. Food Environ Virol 2015; 7: 309-315.
33. Ijaz R, Shahzad N, Farhan Ul Haque M. Detection of BK and JC polyomaviruses in sewage water of the urban areas of Lahore, Pakistan. Biologia (Bratisl) 2023; 1-8.
34. Comerlato J, Souza-Campos F, Souza-Arantes T, Roos-Kulmann MI, Trindade-Oliveira M, Rosado-Spilki F, et al. Distribution and genetic diversity of the human polyomaviruses JC and BK in surface water and sewage treatment plant during 2009 in Porto Alegre, Southern Brazil. Braz J Biol 2017; 77: 459-468.
35. Malla B, Ghaju Shrestha R, Tandukar S, Bhandari D, Thakali O, Sherchand JB, et al. Detection of Pathogenic Viruses, Pathogen indicators, and Fecal-Source markers within tanker water and their sources in the Kathmandu Valley, Nepal. Pathogens 2019; 8: 81.
36. Hewitt J, Greening GE, Leonard M, Lewis GD. Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Water Res 2013; 47: 6750-6761.
37. Ahmed W, Wan C, Goonetilleke A, Gardner T. Evaluating sewage-associated JCV and BKV polyomaviruses for sourcing human fecal pollution in a coastal river in Southeast Queensland, Australia. J Environ Qual 2010; 39: 1743-1750.
38. Kotton CN, Kamar N, Wojciechowski D, Eder M, Hopfer H, Randhawa P, et al. The Second international consensus guidelines on the management of BK Polyomavirus in Kidney transplantation. Transplantation 2024; 108: 1834-1866.
2. Observatory TGC. Iran, Islamic republic of. source: Globocan (2020). International agency for research on Cancer: World Health Organization; https://macsa.ir/fa/wp-content/uploads/2021/04/364-iran-islamic-republic-of-fact-sheets.pdf
3. Marmol I, Sanchez-de-Diego C, Pradilla Dieste A, Cerrada E, Rodriguez Yoldi MJ. Colorectal carcinoma: A general overview and future perspectives in Colorectal cancer. Int J Mol Sci 2017; 18: 197.
4. Johnson CM, Wei C, Ensor JE, Smolenski DJ, Amos CI, Levin B, et al. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control 2013; 24: 1207-1222.
5. Marongiu L, Allgayer H. Viruses in colorectal cancer. Mol Oncol 2022; 16: 1423-1450.
6. Abend JR, Jiang M, Imperiale MJ. BK virus and human cancer: innocent until proven guilty. Semin Cancer Biol 2009; 19: 252-260.
7. Burger-Calderon R, Webster-Cyriaque J. Human BK Polyomavirus-The potential for head and neck malignancy and disease. Cancers (Basel) 2015; 7: 1244-1270.
8. Vaezjalali M, Azimi H, Hosseini SM, Taghavi A, Goudarzi H. Different strains of BK Polyomavirus: VP1 sequences in a group of iranian prostate cancer patients. Urol J 2018; 15: 44-48.
9. Moens U, Van Ghelue M, Ehlers B. Are human polyomaviruses co-factors for cancers induced by other oncoviruses? Rev Med Virol 2014; 24: 343-360.
10. Comar M, Bonifacio D, Zanconati F, Di Napoli M, Isidoro E, Martini F, et al. High prevalence of BK polyomavirus sequences in human papillomavirus-16-positive precancerous cervical lesions. J Med Virol 2011; 83: 1770-1776.
11. Jarzynski A, Zajac P, Zebrowski R, Boguszewska A, Polz-Dacewicz M. Occurrence of BK virus and human papilloma virus in colorectal cancer. Ann Agric Environ Med 2017; 24: 440-445.
12. Abolbashari S, Shakeri M, Hami M, Gholoobi A, Hooshyar Chechaklou A, Damavandi M, et al. Higher viral load of polyomavirus type BK but not JC among Renal transplant recipients in comparison to donors. Iran J Pathol 2022; 17: 8-14.
13. Kotla SK, Kadambi PV, Hendricks AR, Rojas R. BK polyomavirus-pathogen, paradigm and puzzle. Nephrol Dial Transplant 2021; 36: 587-593.
14. Krajewski W, Kaminska D, Poterek A, Malkiewicz B, Klak J, Zdrojowy R, et al. Pathogenicity of BK virus on the urinary system. Cent European J Urol 2020; 73: 94-103.
15. Levican J, Acevedo M, Leon O, Gaggero A, Aguayo F. Role of BK human polyomavirus in cancer. Infect Agent Cancer 2018; 13: 12.
16. Villani S, Gagliano N, Procacci P, Sartori P, Comar M, Provenzano M, et al. Characterization of an in vitro model to study the possible role of polyomavirus BK in prostate cancer. J Cell Physiol 2019; 234: 11912-11922.
17. Saber Amoli S, Zebardast A, Keyvani H, Yahyapour Y, Ghodsi SM, Maniati M, et al. Prevalence and viral load determination of BK polyomavirus among Iranian patients with brain tumors. Caspian J Intern Med 2021; 12: 173-179.
18. Burger-Calderon R, Ramsey KJ, Dolittle-Hall JM, Seaman WT, Jeffers-Francis LK, Tesfu D, et al. Distinct BK polyomavirus non-coding control region (NCCR) variants in oral fluids of HIV- associated Salivary Gland Disease patients. Virology 2016; 493: 255-266.
19. Starrett GJ, Buck CB. The case for BK polyomavirus as a cause of bladder cancer. Curr Opin Virol 2019; 39: 8-15.
20. Javadi M, Jalilian S, Kanani M, Kia V, Talaiezadeh A, Angali KA, et al. Time to take HPV infection in colorectal cancer patients more seriously. Front Med (Lausanne) 2024; 11: 1418359.
21. Anzivino E, Bellizzi A, Mitterhofer AP, Tinti F, Barile M, Colosimo MT, et al. Early monitoring of the human polyomavirus BK replication and sequencing analysis in a cohort of adult kidney transplant patients treated with basiliximab. Virol J 2011; 8: 407.
22. Tarharoudi R, Sari S, Sakhaee F, Vaziri F, Rahimi Jamnani F, Siadat SD, et al. BK polyomavirus in Iranian patients with papillary thyroid cancer: Is it a major future challenge? J Med Virol 2022; 94: 6023-6027.
23. Delbue S, Matei DV, Carloni C, Pecchenini V, Carluccio S, Villani S, et al. Evidence supporting the association of polyomavirus BK genome with prostate cancer. Med Microbiol Immunol 2013; 202: 425-430.
24. Tseng CE, Yeh CM, Fang CY, Shay J, Chen PL, Lin MC, et al. Detection of human JCPyV and BKPyV in diffuse large B-cell lymphoma of the GI tract. Eur J Clin Microbiol Infect Dis 2014; 33: 665-672.
25. Casini B, Borgese L, Del Nonno F, Galati G, Izzo L, Caputo M, et al. Presence and incidence of DNA sequences of human polyomaviruses BKV and JCV in colorectal tumor tissues. Anticancer Res 2005; 25: 1079-1085.
26. Sarvari J, Mahmoudvand S, Pirbonyeh N, Safaei A, Hosseini SY. The very low frequency of Epstein-Barr JC and BK Viruses DNA in Colorectal cancer tissues in Shiraz, Southwest Iran. Pol J Microbiol 2018; 67: 73-79.
27. Khabaz MN, Nedjadi T, Gari MA, Al-Maghrabi JA, Atta HM, Basuni AA, et al. BK polyomavirus association with colorectal cancer development. Genet Mol Res 2016; 15: 10.4238/gmr.15027841.
28. Zheng HY, Nishimoto Y, Chen Q, Hasegawa M, Zhong S, Ikegaya H, et al. Relationships between BK virus lineages and human populations. Microbes Infect 2007; 9: 204-213.
29. Kaydani GA, Makvandi M, Samarbafzadeh A, Shahbazian H, Hamidi Fard M. Prevalence and distribution of BK virus subtypes in renal transplant recipients referred to Golestan hospital in Ahvaz, Iran. Jundishapur J Microbiol 2015; 8(3): e16738.
30. Karimi Dehcheshmeh L, Makvandi M, Timori A. Prevalence of human Polyomavirus JC and BK in normal population. Asian Pac J Cancer Prev 2020; 21: 2877-2882.
31. Muller DC, Ramo M, Naegele K, Ribi S, Wetterauer C, Perrina V, et al. Donor-derived, metastatic urothelial cancer after kidney transplantation associated with a potentially oncogenic BK polyomavirus. J Pathol 2018; 244: 265-270.
32. Iaconelli M, Petricca S, Libera SD, Di Bonito P, La Rosa G. First detection of human Papillomaviruses and human Polyomaviruses in river waters in Italy. Food Environ Virol 2015; 7: 309-315.
33. Ijaz R, Shahzad N, Farhan Ul Haque M. Detection of BK and JC polyomaviruses in sewage water of the urban areas of Lahore, Pakistan. Biologia (Bratisl) 2023; 1-8.
34. Comerlato J, Souza-Campos F, Souza-Arantes T, Roos-Kulmann MI, Trindade-Oliveira M, Rosado-Spilki F, et al. Distribution and genetic diversity of the human polyomaviruses JC and BK in surface water and sewage treatment plant during 2009 in Porto Alegre, Southern Brazil. Braz J Biol 2017; 77: 459-468.
35. Malla B, Ghaju Shrestha R, Tandukar S, Bhandari D, Thakali O, Sherchand JB, et al. Detection of Pathogenic Viruses, Pathogen indicators, and Fecal-Source markers within tanker water and their sources in the Kathmandu Valley, Nepal. Pathogens 2019; 8: 81.
36. Hewitt J, Greening GE, Leonard M, Lewis GD. Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Water Res 2013; 47: 6750-6761.
37. Ahmed W, Wan C, Goonetilleke A, Gardner T. Evaluating sewage-associated JCV and BKV polyomaviruses for sourcing human fecal pollution in a coastal river in Southeast Queensland, Australia. J Environ Qual 2010; 39: 1743-1750.
38. Kotton CN, Kamar N, Wojciechowski D, Eder M, Hopfer H, Randhawa P, et al. The Second international consensus guidelines on the management of BK Polyomavirus in Kidney transplantation. Transplantation 2024; 108: 1834-1866.
| Files | ||
| Issue | Vol 17 No 1 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i1.17811 | |
| Keywords | ||
| BK polyomavirus; Colorectal cancer; Urine; Genotypes | ||
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How to Cite
1.
Javadi M, Kaydani G, Pirmoradi R, Talaiezadeh A, Haghi Navand A, Karimi Baba Ahmadi M, Makvandi M. Frequency of BK virus genotypes in patients with colorectal cancer. Iran J Microbiol. 2025;17(1):137-143.
