Detection of the BK virus in urban wastewater inlets into the Karun River
-
Parvaneh Bahrami
,
Afshin Takdastan
,
Manoochehr Makvandi
,
Sahand Jorfi
,
Mohammad Karimi Baba Ahmadi
,
Abdolkazem Neisi
Abstract
Background and Objectives: The presence of the BK virus in wastewater indicates pollution, as it is shed in the urine of infected individuals. Over fifty percent of the human population remains asymptomatic for the BK virus. Reactivation of the BK virus in immunosuppressed individuals can lead to serious health issues, including cystic hemorrhagic, nephritis, and kidney graft rejection. The BK virus is associated with various cancers, such as head and neck, prostate, bladder, and colorectal cancers. The urban wastewater inlets into the Karun River cause the river contamination. This study focused on detecting the BK virus in wastewater inlet in Karun River, Ahvaz city, Iran.
Materials and Methods: Sixty raw wastewater samples were collected from diverse urban sources and concentrated using polyethylene glycol 6000 to isolate BK virus. The BK virus isolates were analyzed for genotypes and the non-coding control region (NCCR).
Results: The Nested PCR results indicated that thirty-two out of sixty samples (53.33%) were positive for the BK virus. The phylogenetic analysis revealed the dominance of BK virus genotype Ib2, followed by genotype 4. The BK virus non-coding control region (NCCR) analysis identified an archetype strain.
Conclusion: The sewage plant treatment should be implemented to remove pathogenic viruses specially BK virus and to curb the circulating of BK virus in human and environment.
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2. Rashed MK, El-Senousy WM, Sayed ETAE, AlKhazindar M. Infectious pepper mild mottle virus and human adenoviruses as viral indices in sewage and water samples. Food Environ Virol 2022; 14: 246-257.
3. Ambalathingal GR, Francis RS, Smyth MJ, Smith C, Khanna R. BK polyomavirus: clinical aspects, immune regulation, and emerging therapies. Clin Microbiol Rev 2017; 30: 503-528.
4. Alcendor DJ. BK polyomavirus virus glomerular tropism: implications for virus reactivation from latency and amplification during immunosuppression. J Clin Med 2019; 8: 1477.
5. Kotla SK, Kadambi PV, Hendricks AR, Rojas R. BK polyomavirus-pathogen, paradigm and puzzle. Nephrol Dial Transplant 2021; 36: 587-593.
6. Krajewski W, Kamińska D, Poterek A, Małkiewicz B, Kłak J, Zdrojowy R, et al. Pathogenicity of BK virus on the urinary system. Cent European J Urol 2020; 73: 94-103.
7. Morel V, Martin E, François C, Helle F, Faucher J, Mourez T, et al. A simple and reliable strategy for BK virus subtyping and subgrouping. J Clin Microbiol 2017; 55: 1177-1185.
8. Zhou X, Zhu C, Li H. BK polyomavirus: latency, reactivation, diseases and tumorigenesis. Front Cell Infect Microbiol 2023; 13: 1263983.
9. 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.
10. Sahragard I, Yaghobi R, Mohammadi A, Afshari A, Pakfetrat M, Karimi MH, et al. Impact of BK Polyomavirus NCCR variations in post kidney transplant outcomes. Gene 2024; 913: 148376.
11. Lu D, Huang Z, Luo J, Zhang X, Sha S. Primary concentration–the critical step in implementing the wastewater-based epidemiology for the COVID-19 pandemic: a mini-review. Sci Total Environ 2020; 747: 141245.
12. WHO. In: Guidelines for Environmental Surveillance of Poliovirus Circulation. Biologicals DoVa, editor. World Health Organization Switzerland 2003.
13. Amdiouni H, Faouzi A, Fariat N, Hassar M, Soukri A, Nourlil J. Nourlil. Detection and molecular identification of human adenoviruses and enteroviruses in wastewater from Morocco. Lett Appl Microbiol 2012; 54: 359-366.
14. 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.
15. Egli A, Infanti L, Dumoulin A, Buser A, Samaridis J, Stebler C, et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis 2009; 199: 837-846.
16. Carmo Dos Santos M, Cerqueira Silva AC, Dos Reis Teixeira C, Pinheiro Macedo Prazeres F, Fernandes Dos Santos R, de Araújo Rolo C, et al. Wastewater surveillance for viral pathogens: a tool for public health. Heliyon 2024; 10(13): e33873.
17. 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.
18. Machado DM, Fink MC, Pannuti CS, Succi RC, Machado AA, Carmo FB, et al. Human polyomaviruses JC and BK in the urine of Brazilian children and adolescents vertically infected by HIV. Mem Inst Oswaldo Cruz 2011; 106: 931-935.
19. Boukoum H, Nahdi I, Sahtout W, Skiri H, Segondy M, Aouni M. BK and JC virus infections in healthy patients compared to kidney transplant recipients in Tunisia. Microb Pathog 2016; 97: 204-208.
20. Laskin BL, Denburg MR, Furth SL, Moatz T, Altrich M, Kleiboeker S, et al. The natural history of BK polyomavirus and the host immune response after stem cell transplantation. Clin Infect Dis 2020; 71: 3044-3054.
21. Peras M, Bilić E, Mareković I. Recent Insights into the Pathogenesis, Diagnostics, and Treatment of BK Virus Infections in Children After Hematopoietic Stem Cell Transplantation. Pathogens 2025; 14: 236.
22. Mody MD, Rocco JW, Yom SS, Haddad RI, Saba NF. Head and neck cancer. Lancet 2021; 398: 2289-2299.
23. Javadi M, Kaydani G, Pirmoradi R, Talaiezadeh A, Navand AH, Ahmadi MKB, et al. Frequency of BK virus genotypes in patients with colorectal cancer. Iran J Microbiol 2025; 17: 137-143.
24. Nourie N, Boueri C, Tran Minh H, Divard G, Lefaucheur C, Salmona M, et al. BK Polyomavirus Infection in Kidney Transplantation: A Comprehensive Review of Current Challenges and Future Directions. Int J Mol Sci 2024; 25: 12801.
25. Ahmed NI, Elmahdy EM, Allayh AK, Mohamed El-CB, Loutfy SA, Barakat A, et al. Prevalence of human polyomavirus and papillomavirus in wastewater and in stool of Egyptian patients. Egypt J Aquat Biol Fish 2019; 23: 29-41.
26. 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.
27. Kumblathan T, Liu Y, Uppal GK, Hrudey SE, Li XF. Wastewater-Based Epidemiology for Community Monitoring of SARS-CoV-2: Progress and Challenges. ACS Environ Au 2021; 1: 18-31.
28. Sims N, Kasprzyk-Hordern B. Future perspectives of wastewater-based epidemiology: Monitoring infectious disease spread and resistance to the community level. Environ Int 2020; 139: 105689.
29. Yan L, Toohey-Kurth KL, Crossley BM, Bai J, Glaser AL, Tallmadge RL, et al. Inhibition monitoring in veterinary molecular testing. J Vet Diagn Invest 2020; 32: 758-766.
30. Schrader C, Schielke A, Ellerbroek L, Johne R. PCR inhibitors - occurrence, properties and removal. J Appl Microbiol 2012; 113: 1014-1026.
31. Bethge T, Ajuh E, Hirsch HH. Imperfect symmetry of Sp1 and core promoter sequences regulates early and late virus gene expression of the bidirectional BK polyomavirus noncoding control region. J Virol 2016; 90: 10083-10101.
32. Walder TA, Odegard EA, Meeds HL, Kleiboeker SB, Ziady A, Sabulski A, et al. Single-nucleotide polymorphisms within the BK polyomavirus non-coding control region are genotype-associated. Microbiol Spectr 2025; 13(8): e0049425.
33. Liang B, Tikhanovich I, Nasheuer HP, Folk WR. Stimulation of BK virus DNA replication by NFI family transcription factors. J Virol 2012; 86: 3264-3275.
34. Bethge T, Hachemi HA, Manzetti J, Gosert R, Schaffner W, Hirsch HH. Sp1 sites in the noncoding control region of BK polyomavirus are key regulators of bidirectional viral early and late gene expression. J Virol 2015; 89: 3396-3411.
35. Gosert R, Rinaldo CH, Funk GA, Egli A, Ramos E, Drachenberg CB, et al. Polyomavirus BK with rearranged noncoding control region emerge in vivo in renal transplant patients and increase viral replication and cytopathology. J Exp Med 2008; 205: 841-852.
36. Li YJ, Chen YH, Wang JW, Wu HH, Hsu HH, Ho DR, et al. Suppression of cisplatin induced ATF3 expression and apoptosis by BK polyomavirus and its encoded microRNA in bladder cancer cells. Biomed Pharmacother 2025; 186: 118032.
37. Galati L, Chiantore MV, Marinaro M, Di Bonito P. Human oncogenic viruses: characteristics and prevention Strategies—Lessons learned from human papillomaviruses. Viruses 2024; 16: 416.
38. Wang R, Xiao M, Furusho H, Kodera N, Hoek EM, Honda R. Enhancing Adsorptive Removal of Viruses and Extracellular Antimicrobial Resistance Genes in Microfiltration: Impacts of Membrane Materials and Solution Chemistry. ACS ES T Water 2025; 5: 5079-5087.
39. Guerrero-Latorre L, Gonzales-Gustavson E, Hundesa A, Sommer R, Rosina G. UV disinfection and flocculation-chlorination sachets to reduce hepatitis E virus in drinking water. Int J Hyg Environ Health 2016; 219: 405-411.
40. Shi Q, Chen Z, Liu H, Lu Y, Li K, Shi Y, et al. Efficient synergistic disinfection by ozone, ultraviolet irradiation and chlorine in secondary effluents. Sci Total Environ 2021; 758: 143641.
2. Rashed MK, El-Senousy WM, Sayed ETAE, AlKhazindar M. Infectious pepper mild mottle virus and human adenoviruses as viral indices in sewage and water samples. Food Environ Virol 2022; 14: 246-257.
3. Ambalathingal GR, Francis RS, Smyth MJ, Smith C, Khanna R. BK polyomavirus: clinical aspects, immune regulation, and emerging therapies. Clin Microbiol Rev 2017; 30: 503-528.
4. Alcendor DJ. BK polyomavirus virus glomerular tropism: implications for virus reactivation from latency and amplification during immunosuppression. J Clin Med 2019; 8: 1477.
5. Kotla SK, Kadambi PV, Hendricks AR, Rojas R. BK polyomavirus-pathogen, paradigm and puzzle. Nephrol Dial Transplant 2021; 36: 587-593.
6. Krajewski W, Kamińska D, Poterek A, Małkiewicz B, Kłak J, Zdrojowy R, et al. Pathogenicity of BK virus on the urinary system. Cent European J Urol 2020; 73: 94-103.
7. Morel V, Martin E, François C, Helle F, Faucher J, Mourez T, et al. A simple and reliable strategy for BK virus subtyping and subgrouping. J Clin Microbiol 2017; 55: 1177-1185.
8. Zhou X, Zhu C, Li H. BK polyomavirus: latency, reactivation, diseases and tumorigenesis. Front Cell Infect Microbiol 2023; 13: 1263983.
9. 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.
10. Sahragard I, Yaghobi R, Mohammadi A, Afshari A, Pakfetrat M, Karimi MH, et al. Impact of BK Polyomavirus NCCR variations in post kidney transplant outcomes. Gene 2024; 913: 148376.
11. Lu D, Huang Z, Luo J, Zhang X, Sha S. Primary concentration–the critical step in implementing the wastewater-based epidemiology for the COVID-19 pandemic: a mini-review. Sci Total Environ 2020; 747: 141245.
12. WHO. In: Guidelines for Environmental Surveillance of Poliovirus Circulation. Biologicals DoVa, editor. World Health Organization Switzerland 2003.
13. Amdiouni H, Faouzi A, Fariat N, Hassar M, Soukri A, Nourlil J. Nourlil. Detection and molecular identification of human adenoviruses and enteroviruses in wastewater from Morocco. Lett Appl Microbiol 2012; 54: 359-366.
14. 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.
15. Egli A, Infanti L, Dumoulin A, Buser A, Samaridis J, Stebler C, et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis 2009; 199: 837-846.
16. Carmo Dos Santos M, Cerqueira Silva AC, Dos Reis Teixeira C, Pinheiro Macedo Prazeres F, Fernandes Dos Santos R, de Araújo Rolo C, et al. Wastewater surveillance for viral pathogens: a tool for public health. Heliyon 2024; 10(13): e33873.
17. 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.
18. Machado DM, Fink MC, Pannuti CS, Succi RC, Machado AA, Carmo FB, et al. Human polyomaviruses JC and BK in the urine of Brazilian children and adolescents vertically infected by HIV. Mem Inst Oswaldo Cruz 2011; 106: 931-935.
19. Boukoum H, Nahdi I, Sahtout W, Skiri H, Segondy M, Aouni M. BK and JC virus infections in healthy patients compared to kidney transplant recipients in Tunisia. Microb Pathog 2016; 97: 204-208.
20. Laskin BL, Denburg MR, Furth SL, Moatz T, Altrich M, Kleiboeker S, et al. The natural history of BK polyomavirus and the host immune response after stem cell transplantation. Clin Infect Dis 2020; 71: 3044-3054.
21. Peras M, Bilić E, Mareković I. Recent Insights into the Pathogenesis, Diagnostics, and Treatment of BK Virus Infections in Children After Hematopoietic Stem Cell Transplantation. Pathogens 2025; 14: 236.
22. Mody MD, Rocco JW, Yom SS, Haddad RI, Saba NF. Head and neck cancer. Lancet 2021; 398: 2289-2299.
23. Javadi M, Kaydani G, Pirmoradi R, Talaiezadeh A, Navand AH, Ahmadi MKB, et al. Frequency of BK virus genotypes in patients with colorectal cancer. Iran J Microbiol 2025; 17: 137-143.
24. Nourie N, Boueri C, Tran Minh H, Divard G, Lefaucheur C, Salmona M, et al. BK Polyomavirus Infection in Kidney Transplantation: A Comprehensive Review of Current Challenges and Future Directions. Int J Mol Sci 2024; 25: 12801.
25. Ahmed NI, Elmahdy EM, Allayh AK, Mohamed El-CB, Loutfy SA, Barakat A, et al. Prevalence of human polyomavirus and papillomavirus in wastewater and in stool of Egyptian patients. Egypt J Aquat Biol Fish 2019; 23: 29-41.
26. 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.
27. Kumblathan T, Liu Y, Uppal GK, Hrudey SE, Li XF. Wastewater-Based Epidemiology for Community Monitoring of SARS-CoV-2: Progress and Challenges. ACS Environ Au 2021; 1: 18-31.
28. Sims N, Kasprzyk-Hordern B. Future perspectives of wastewater-based epidemiology: Monitoring infectious disease spread and resistance to the community level. Environ Int 2020; 139: 105689.
29. Yan L, Toohey-Kurth KL, Crossley BM, Bai J, Glaser AL, Tallmadge RL, et al. Inhibition monitoring in veterinary molecular testing. J Vet Diagn Invest 2020; 32: 758-766.
30. Schrader C, Schielke A, Ellerbroek L, Johne R. PCR inhibitors - occurrence, properties and removal. J Appl Microbiol 2012; 113: 1014-1026.
31. Bethge T, Ajuh E, Hirsch HH. Imperfect symmetry of Sp1 and core promoter sequences regulates early and late virus gene expression of the bidirectional BK polyomavirus noncoding control region. J Virol 2016; 90: 10083-10101.
32. Walder TA, Odegard EA, Meeds HL, Kleiboeker SB, Ziady A, Sabulski A, et al. Single-nucleotide polymorphisms within the BK polyomavirus non-coding control region are genotype-associated. Microbiol Spectr 2025; 13(8): e0049425.
33. Liang B, Tikhanovich I, Nasheuer HP, Folk WR. Stimulation of BK virus DNA replication by NFI family transcription factors. J Virol 2012; 86: 3264-3275.
34. Bethge T, Hachemi HA, Manzetti J, Gosert R, Schaffner W, Hirsch HH. Sp1 sites in the noncoding control region of BK polyomavirus are key regulators of bidirectional viral early and late gene expression. J Virol 2015; 89: 3396-3411.
35. Gosert R, Rinaldo CH, Funk GA, Egli A, Ramos E, Drachenberg CB, et al. Polyomavirus BK with rearranged noncoding control region emerge in vivo in renal transplant patients and increase viral replication and cytopathology. J Exp Med 2008; 205: 841-852.
36. Li YJ, Chen YH, Wang JW, Wu HH, Hsu HH, Ho DR, et al. Suppression of cisplatin induced ATF3 expression and apoptosis by BK polyomavirus and its encoded microRNA in bladder cancer cells. Biomed Pharmacother 2025; 186: 118032.
37. Galati L, Chiantore MV, Marinaro M, Di Bonito P. Human oncogenic viruses: characteristics and prevention Strategies—Lessons learned from human papillomaviruses. Viruses 2024; 16: 416.
38. Wang R, Xiao M, Furusho H, Kodera N, Hoek EM, Honda R. Enhancing Adsorptive Removal of Viruses and Extracellular Antimicrobial Resistance Genes in Microfiltration: Impacts of Membrane Materials and Solution Chemistry. ACS ES T Water 2025; 5: 5079-5087.
39. Guerrero-Latorre L, Gonzales-Gustavson E, Hundesa A, Sommer R, Rosina G. UV disinfection and flocculation-chlorination sachets to reduce hepatitis E virus in drinking water. Int J Hyg Environ Health 2016; 219: 405-411.
40. Shi Q, Chen Z, Liu H, Lu Y, Li K, Shi Y, et al. Efficient synergistic disinfection by ozone, ultraviolet irradiation and chlorine in secondary effluents. Sci Total Environ 2021; 758: 143641.
| Files | ||
| Issue | Vol 17 No 6 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i6.20371 | |
| Keywords | ||
| Wastewater BK virus Genotype Non-coding control region (NCCR) | ||
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How to Cite
1.
Bahrami P, Takdastan A, Makvandi M, Jorfi S, Karimi Baba Ahmadi M, Neisi A. Detection of the BK virus in urban wastewater inlets into the Karun River. Iran J Microbiol. 2025;17(6):1023-1032.
