Prevalence of JC polyomavirus among rheumatoid arthritis and systemic lupus erythematosus patients and its correlation with vitamin D levels
-
Golnaz Irani Mokhtari
,
Azarakhsh Azaran
,
Elham Rajahi
,
Saeed Hesam
,
Azam Dehghani Ghahfarokhi
,
Manoochehr Makvandi
Abstract
Background and Objectives: Vitamin D deficiency in viral infection associated with autoimmune diseases is well documented. This study assessed the prevalence of JC virus in patients with rheumatoid arthritis (RA) and systemic lupus erythematosus (SLE), and its correlation with vitamin D level.
Materials and Methods: Serum and urine samples were collected from 50 patients with RA and SLE. DNA was extracted and subjected to PCR test. Positive PCR products were sequenced, phylogenetic tree was constructed to determine the JC virus genotype. The patient’s vitamin D level was evaluated.
Results: Of 50 patients, 19 (38%) were diagnosed as RA, and 31 (62%) were identified as SLE. JC virus DNA was detected in 17 (34%) patients’ urine samples including 5 (26.3%) RA and 12 (38.7%) SLE cases. JC virus DNA was detected 2 (4%) in patients’ serum samples (one RA. and one SLE). JC virus genotype 3A was dominant. Interestingly, the SLE patients with positive JC virus showed lowered vitamin D compared to patients with negative JC virus (P<0.005).
Conclusion: Given the high rate of JC virus, DNA detection and susceptibility of patients for PML development, it is recommended that detection of JC virus DNA and vitamin D level should be implemented for patients with RA/SLE prior to treatment.
1. Cinque P, Koralnik IJ, Gerevini S, Miro JM, Price RW. Progressive multifocal leukoencephalopathy in HIV-1 infection. Lancet Infect Dis 2009; 9: 625-636.
2. Hildreth JE, Alcendor DJ. JC polyomavirus and transplantation: implications for virus reactivation after immunosuppression in transplant patients and the occurrence of PML disease. Transplantology 2021; 2: 37-48.
3. Major EO. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Annu Rev Med 2010; 61: 35-47.
4. Frohman EM, Monaco MC, Remington G, Ryschkewitsch C, Jensen PN, Johnson K, et al. JC virus in CD34+ and CD19+ cells in patients with multiple sclerosis treated with natalizumab. JAMA Neurol 2014; 71: 596-602.
5. Morris-Love J, Atwood WJ. Complexities of JC polyomavirus receptor-dependent and-independent mechanisms of infection. Viruses 2022; 14: 1130.
6. Makvandi M, Mombeini H, Haghighi SB, Dastoorpoor M, Khodadad N, Babaahmadi MK, et al. Molecular epidemiology of JC polyomavirus in HIV-infected patients and healthy individuals from Iran. Braz J Microbiol 2020; 51: 37-43.
7. Gorelik L, Reid C, Testa M, Brickelmaier M, Bossolasco S, Pazzi A, et al. Progressive multifocal leukoencephalopathy (PML) development is associated with mutations in JC virus capsid protein VP1 that change its receptor specificity. J Infect Dis 2011; 204: 103-114.
8. Reid CE, Li H, Sur G, Carmillo P, Bushnell S, Tizard R, et al. Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. J Infect Dis 2011; 204: 237-244.
9. Sunyaev SR, Lugovskoy A, Simon K, Gorelik L. Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML). PLoS Genet 2009; 5(2): e1000368.
10. Prezioso C, Zingaropoli MA, Iannetta M, Rodio DM, Altieri M, Conte A, et al. Which is the best PML risk stratification strategy in natalizumab-treated patients affected by multiple sclerosis? Mult Scler Relat Disord 2020; 41: 102008.
11. Mócsai A, Kovács L, Gergely P. What is the future of targeted therapy in rheumatology: biologics or small molecules? BMC Med 2014; 12: 43.
12. Ogdie A, Weiss P. The epidemiology of psoriatic arthritis. Rheum Dis Clin North Am 2015; 41: 545-568.
13. Gurevitz SL, Snyder JA, Wessel EK, Frey J, Williamson BA. Systemic lupus erythematosus: a review of the disease and treatment options. Consult Pharm 2013; 28: 110-121.
14. Belderbos ME, Houben ML, Wilbrink B, Lentjes E, Bloemen EM, Kimpen JL, et al. Cord blood vitamin D deficiency is associated with respiratory syncytial virus bronchiolitis. Pediatrics 2011; 127(6): e1513-e1520.
15. Loeb M, Dang AD, Thiem VD, Thanabalan V, Wang B, Nguyen NB, et al. Effect of vitamin D supplementation to reduce respiratory infections in children and adolescents in Vietnam: a randomized controlled trial. Influenza Other Respir Viruses 2019; 13: 176-183.
16. Warraich S, Sidhu A, Hou M, Alenezi O. The impact of middle eastern origin, HIV, HCV, and HIV/HCV co-infection in the development of hypovitaminosis D in adults. Mol Genet Genomic Med 2018; 6: 1010-1014.
17. Wang TT, Nestel FP, Bourdeau V, Nagai Y, Wang Q, Liao J, et al. Cutting edge: 1, 25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J Immunol 2004; 173: 2909-2912.
18. Ganguly D, Chamilos G, Lande R, Gregorio J, Meller S, Facchinetti V, et al. Self-RNA–antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med 2009; 206: 1983-1994.
19. Quiñones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, Rangel HR, et al. Human epithelial β-defensins 2 and 3 inhibit HIV-1 replication. AIDS 2003; 17: F39-F48.
20. Aguilar-Jimenez W, Zapata W, Caruz A, Rugeles MT. High transcript levels of vitamin D receptor are correlated with higher mRNA expression of human beta defensins and IL-10 in mucosa of HIV-1-exposed seronegative individuals. PLoS One 2013; 8(12): e82717.
21. Aguilar-Jimenez W, Zapata W, Rugeles MT. Antiviral molecules correlate with vitamin D pathway genes and are associated with natural resistance to HIV-1 infection. Microbes Infect 2016; 18: 510-516.
22. Howell MD, Jones JF, Kisich KO, Streib JE, Gallo RL, Leung DY. Selective killing of vaccinia virus by LL-37: implications for eczema vaccinatum. J Immunol 2004; 172: 1763-1767.
23. Bastian A, Schäfer H. Human alpha ‐defensin 1 (HNP‐1) inhibits adenoviral infection in vitro. Regul Pept 2001; 101: 157-161.
24. Proud D, Sanders SP, Wiehler S. Human rhinovirus infection induces airway epithelial cell production of human beta-defensin 2 both in vitro and in vivo. J Immunol 2004; 172: 4637-4645.
25. Leikina E, Delanoe-Ayari H, Melikov K, Cho MS, Chen A, Waring AJ, et al. Carbohydrate-binding molecules inhibit viral fusion and entry by crosslinking membrane glycoproteins. Nat Immunol 2005; 6: 995-1001.
26. Mao X, Hu B, Zhou Z, Xing X, Wu Y, Gao J, et al. Vitamin D levels correlate with lymphocyte subsets in elderly patients with age-related diseases. Sci Rep 2018; 8: 7708.
27. Pender MP. CD8+ T-cell deficiency, Epstein-Barr virus infection, vitamin D deficiency, and steps to autoimmunity: a unifying hypothesis. Autoimmune Dis 2012; 2012: 189096.
28. Yasin B, Pang M, Turner JS, Cho Y, Dinh NN, Waring AJ, et al. Evaluation of the inactivation of infectious herpes simplex virus by host-defense peptides. Eur J Clin Microbiol Infect Dis 2000; 19: 187-194.
29. Howell MD, Wollenberg A, Gallo RL, Flaig M, Streib JE, Wong C, et al. Cathelicidin deficiency predisposes to eczema herpeticum. J Allergy Clin Immunol 2006; 117: 836-841.
30. Barlow PG, Svoboda P, Mackellar A, Nash AA, York IA, Pohl J, et al. Antiviral activity and increased host defense against influenza infection elicited by the human cathelicidin LL-37. PLoS One 2011; 6(10): e25333.
31. Schögler A, Muster RJ, Kieninger E, Casaulta C, Tapparel C, Jung A, et al. Vitamin D represses rhinovirus replication in cystic fibrosis cells by inducing LL-37. Eur Respir J 2016; 47: 520-530.
32. Gal-Tanamy M, Bachmetov L, Ravid A, Koren R, Erman A, Tur-Kaspa R, et al. Vitamin D: an innate antiviral agent suppressing hepatitis C virus in human hepatocytes. Hepatology 2011; 54: 1570-1579.
33. Teymoori-Rad M, Shokri F, Salimi V, Marashi SM. The interplay between vitamin D and viral infections. Rev Med Virol 2019; 29(2): e2032.
34. Ray M, Curtis JR, Baddley JW. A case report of progressive multifocal leucoencephalopathy (PML) associated with adalimumab. Ann Rheum Dis 2014; 73: 1429-1430.
35. Simopoulou T, Tsimourtou V, Katsiari C, Vlychou M, Bogdanos DP, Sakkas LI. Progressive multifocal leukoencephalopathy in a patient with systemic sclerosis treated with methotrexate: A case report and literature review. J Scleroderma Relat Disord 2020; 5: NP1-NP6.
36. Molloy ES. PML and rheumatology: the contribution of disease and drugs. Cleve Clin J Med 2011; 78 Suppl 2: S28-S32.
37. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, et al. Guidelines for preventing and treating vitamin D deficiency and insufficiency revisited. J Clin Endocrinol Metab 2012; 97: 1153-1158.
38. Agostini HT, Deckhut A, Jobes DV, Girones R, Schlunck G, Prost MG, et al. Genotypes of JC virus in east, central and southwest Europe. J Gen Virol 2001; 82: 1221-1331.
39. Szekanecz Z, McInnes IB, Schett G, Szamosi S, Benkő S, Szűcs G. Autoinflammation and autoimmunity across rheumatic and musculoskeletal diseases. Nat Rev Rheumatol 2021; 17: 585-595.
40. Thanou A, Jupe E, Purushothaman M, Niewold TB, Munroe ME. Clinical disease activity and flare in SLE: Current concepts and novel biomarkers. J Autoimmun 2021; 119: 102615.
41. Connelly K, Morand EF. Systemic lupus erythematosus: a clinical update. Intern Med J 2021; 51: 1219-1228.
42. Lan T-Y, Chen Y-S, Cheng C-F, Huang S-T, Shen C-Y, Hsu P-N. Progressive multifocal leukoencephalopathy in systemic lupus erythematosus managed with pembrolizumab: A case report with literature review. Lupus 2021; 30: 1849-1855.
43. Kapoor T, Mahadeshwar P, Hui-Yuen J, Quinnies K, Tatonetti N, Gartshteyn Y, et al. Prevalence of prog ressive multifocal leukoencephalopathy (PML) in adults and children with systemic lupus erythematosus. Lupus Sci Med 2020; 7(1): e000388.
44. Cortese I, Reich DS, Nath A. Progressive multifocal leukoencephalopathy and the spectrum of JC virus-related disease. Nat Rev Neurol 2021; 17: 37-51.
45. Clifford DB, Ances B, Costello C, Rosen-Schmidt S, Andersson M, Parks D, et al. Rituximab-associated progressive multifocal leukoencephalopathy in rheumatoid arthritis. Arch Neurol 2011; 68: 1156-1164.
46. Nosaki Y, Ohyama K, Watanabe M, Yokoi T, Nakamichi K, Saijo M, et al. Simultaneous development of progressive multifocal leukoencephalopathy and cryptococcal meningitis during methotrexate and infliximab treatment. Intern Med 2019; 58: 2703-2709.
47. Rodio DM, Anzivino E, Mischitelli M, Bellizzi A, Scrivo R, Scribano D, et al. Increased prevalence of human polyomavirus JC viruria in chronic inflammatory rheumatic diseases patients in treatment with anti-TNF α: A 18 month follow-up study. Front Microbiol 2016; 7: 672.
48. Verheyen J, Maizus K, Feist E, Tolman Z, Knops E, Saech J, et al. Increased frequency of JC-polyomavirus detection in rheumatoid arthritis patients treated with multiple biologics. Med Microbiol Immunol 2015; 204: 613-618.
49. Comar M, Delbue S, Lepore L, Martelossi S, Radillo O, Ronfani L, et al. Latent viral infections in young patients with inflammatory diseases treated with biological agents: prevalence of JC virus genotype 2. J Med Virol 2013; 85: 716-722.
50. 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.
51. Hu C, Huang Y, Su J, Wang M, Zhou Q, Zhu B. Detection and analysis of variants of JC polyomavirus in urine samples from HIV-1-infected patients in China’s Zhejiang Province. J Int Med Res 2018; 46: 1024-1032.
52. Haghi Navand A, Jalilian S, Ahmadi Angali K, Karimi Babaahmadi M, Talaiezadeh A, Makvandi M. A new evaluation of the rearranged non-coding control region of JC virus in patients with colorectal cancer. BMC Cancer 2024; 24: 1001.
53. Atyabi SR, Bouzari M, Kardi MT. John cunningham (JC) virus genotypes in kidney transplant recipients, rheumatoid arthritis patients and healthy individuals in Isfahan, Iran. J Med Virol 2017; 89: 337-344.
54. Tanasescu R, Frakich N, Chou IJ, Filippini P, Podda G, Xin G, et al. Natalizumab treatment of relapsing remitting Multiple Sclerosis Has No Long-Term Effects on the proportion of circulating regulatory T cells. Neurol Ther 2023; 12: 2041-2052.
55. Honma T, Onda K, Masuyama K. Progressive multifocal leukoencephalopathy reports in rheumatoid arthritis concerning different treatment patterns-an exploratory assessment using the food and drug administration adverse event reporting system. Front Drug Saf Regul 2024; 4: 1334468.
56. Bellizzi A, Anzivino E, Ferrari F, Di Nardo G, Colosimo MT, Fioriti D, et al. Polyomavirus JC reactivation and noncoding control region sequence analysis in pediatric Crohn’s disease patients treated with infliximab. J Neurovirol 2011; 17: 303-313.
57. Campbell GR, Spector SA. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog 2012; 8(5): e1002689.
58. Saleh M, Welsch C, Cai C, Döring C, Gouttenoire J, Friedrich J, et al. Differential modulation of hepatitis C virus replication and innate immune pathways by synthetic calcitriol-analogs. J Steroid Biochem Mol Biol 2018; 183: 142-151.
59. Goncalves-Mendes N, Talvas J, Dualé C, Guttmann A, Corbin V, Marceau G, et al. Impact of vitamin D supplementation on influenza vaccine response and immune functions in deficient elderly persons: a randomized placebo-controlled trial. Front Immunol 2019; 10: 65.
60. Farnik H, Bojunga J, Berger A, Allwinn R, Waidmann O, Kronenberger B, et al. Low vitamin D serum concentration is associated with high levels of hepatitis B virus replication in chronically infected patients. Hepatology 2013; 58: 1270-1276.
61. Gibbons JB, Norton EC, McCullough JS, Meltzer DO, Lavigne J, Fiedler VC, et al. Gibbons RD. Association between vitamin D supplementation and COVID-19 infection and mortality. Sci Rep 2022; 12: 19397.
62. Megahed A, Gadalla H, Abdelhamid FM, Almehmadi SJ, Khan AA, Albukhari TA, et al. Vitamin D ameliorates the hepatic oxidative damage and fibrotic effect caused by thioacetamide in rats. Biomedicines 2023; 11: 424.
63. Czaja AJ, Montano-Loza AJ. Evolving role of vitamin D in immune-mediated disease and its implications in autoimmune hepatitis. Dig Dis Sci 2019; 64: 324-344.
2. Hildreth JE, Alcendor DJ. JC polyomavirus and transplantation: implications for virus reactivation after immunosuppression in transplant patients and the occurrence of PML disease. Transplantology 2021; 2: 37-48.
3. Major EO. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Annu Rev Med 2010; 61: 35-47.
4. Frohman EM, Monaco MC, Remington G, Ryschkewitsch C, Jensen PN, Johnson K, et al. JC virus in CD34+ and CD19+ cells in patients with multiple sclerosis treated with natalizumab. JAMA Neurol 2014; 71: 596-602.
5. Morris-Love J, Atwood WJ. Complexities of JC polyomavirus receptor-dependent and-independent mechanisms of infection. Viruses 2022; 14: 1130.
6. Makvandi M, Mombeini H, Haghighi SB, Dastoorpoor M, Khodadad N, Babaahmadi MK, et al. Molecular epidemiology of JC polyomavirus in HIV-infected patients and healthy individuals from Iran. Braz J Microbiol 2020; 51: 37-43.
7. Gorelik L, Reid C, Testa M, Brickelmaier M, Bossolasco S, Pazzi A, et al. Progressive multifocal leukoencephalopathy (PML) development is associated with mutations in JC virus capsid protein VP1 that change its receptor specificity. J Infect Dis 2011; 204: 103-114.
8. Reid CE, Li H, Sur G, Carmillo P, Bushnell S, Tizard R, et al. Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. J Infect Dis 2011; 204: 237-244.
9. Sunyaev SR, Lugovskoy A, Simon K, Gorelik L. Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML). PLoS Genet 2009; 5(2): e1000368.
10. Prezioso C, Zingaropoli MA, Iannetta M, Rodio DM, Altieri M, Conte A, et al. Which is the best PML risk stratification strategy in natalizumab-treated patients affected by multiple sclerosis? Mult Scler Relat Disord 2020; 41: 102008.
11. Mócsai A, Kovács L, Gergely P. What is the future of targeted therapy in rheumatology: biologics or small molecules? BMC Med 2014; 12: 43.
12. Ogdie A, Weiss P. The epidemiology of psoriatic arthritis. Rheum Dis Clin North Am 2015; 41: 545-568.
13. Gurevitz SL, Snyder JA, Wessel EK, Frey J, Williamson BA. Systemic lupus erythematosus: a review of the disease and treatment options. Consult Pharm 2013; 28: 110-121.
14. Belderbos ME, Houben ML, Wilbrink B, Lentjes E, Bloemen EM, Kimpen JL, et al. Cord blood vitamin D deficiency is associated with respiratory syncytial virus bronchiolitis. Pediatrics 2011; 127(6): e1513-e1520.
15. Loeb M, Dang AD, Thiem VD, Thanabalan V, Wang B, Nguyen NB, et al. Effect of vitamin D supplementation to reduce respiratory infections in children and adolescents in Vietnam: a randomized controlled trial. Influenza Other Respir Viruses 2019; 13: 176-183.
16. Warraich S, Sidhu A, Hou M, Alenezi O. The impact of middle eastern origin, HIV, HCV, and HIV/HCV co-infection in the development of hypovitaminosis D in adults. Mol Genet Genomic Med 2018; 6: 1010-1014.
17. Wang TT, Nestel FP, Bourdeau V, Nagai Y, Wang Q, Liao J, et al. Cutting edge: 1, 25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J Immunol 2004; 173: 2909-2912.
18. Ganguly D, Chamilos G, Lande R, Gregorio J, Meller S, Facchinetti V, et al. Self-RNA–antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med 2009; 206: 1983-1994.
19. Quiñones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, Rangel HR, et al. Human epithelial β-defensins 2 and 3 inhibit HIV-1 replication. AIDS 2003; 17: F39-F48.
20. Aguilar-Jimenez W, Zapata W, Caruz A, Rugeles MT. High transcript levels of vitamin D receptor are correlated with higher mRNA expression of human beta defensins and IL-10 in mucosa of HIV-1-exposed seronegative individuals. PLoS One 2013; 8(12): e82717.
21. Aguilar-Jimenez W, Zapata W, Rugeles MT. Antiviral molecules correlate with vitamin D pathway genes and are associated with natural resistance to HIV-1 infection. Microbes Infect 2016; 18: 510-516.
22. Howell MD, Jones JF, Kisich KO, Streib JE, Gallo RL, Leung DY. Selective killing of vaccinia virus by LL-37: implications for eczema vaccinatum. J Immunol 2004; 172: 1763-1767.
23. Bastian A, Schäfer H. Human alpha ‐defensin 1 (HNP‐1) inhibits adenoviral infection in vitro. Regul Pept 2001; 101: 157-161.
24. Proud D, Sanders SP, Wiehler S. Human rhinovirus infection induces airway epithelial cell production of human beta-defensin 2 both in vitro and in vivo. J Immunol 2004; 172: 4637-4645.
25. Leikina E, Delanoe-Ayari H, Melikov K, Cho MS, Chen A, Waring AJ, et al. Carbohydrate-binding molecules inhibit viral fusion and entry by crosslinking membrane glycoproteins. Nat Immunol 2005; 6: 995-1001.
26. Mao X, Hu B, Zhou Z, Xing X, Wu Y, Gao J, et al. Vitamin D levels correlate with lymphocyte subsets in elderly patients with age-related diseases. Sci Rep 2018; 8: 7708.
27. Pender MP. CD8+ T-cell deficiency, Epstein-Barr virus infection, vitamin D deficiency, and steps to autoimmunity: a unifying hypothesis. Autoimmune Dis 2012; 2012: 189096.
28. Yasin B, Pang M, Turner JS, Cho Y, Dinh NN, Waring AJ, et al. Evaluation of the inactivation of infectious herpes simplex virus by host-defense peptides. Eur J Clin Microbiol Infect Dis 2000; 19: 187-194.
29. Howell MD, Wollenberg A, Gallo RL, Flaig M, Streib JE, Wong C, et al. Cathelicidin deficiency predisposes to eczema herpeticum. J Allergy Clin Immunol 2006; 117: 836-841.
30. Barlow PG, Svoboda P, Mackellar A, Nash AA, York IA, Pohl J, et al. Antiviral activity and increased host defense against influenza infection elicited by the human cathelicidin LL-37. PLoS One 2011; 6(10): e25333.
31. Schögler A, Muster RJ, Kieninger E, Casaulta C, Tapparel C, Jung A, et al. Vitamin D represses rhinovirus replication in cystic fibrosis cells by inducing LL-37. Eur Respir J 2016; 47: 520-530.
32. Gal-Tanamy M, Bachmetov L, Ravid A, Koren R, Erman A, Tur-Kaspa R, et al. Vitamin D: an innate antiviral agent suppressing hepatitis C virus in human hepatocytes. Hepatology 2011; 54: 1570-1579.
33. Teymoori-Rad M, Shokri F, Salimi V, Marashi SM. The interplay between vitamin D and viral infections. Rev Med Virol 2019; 29(2): e2032.
34. Ray M, Curtis JR, Baddley JW. A case report of progressive multifocal leucoencephalopathy (PML) associated with adalimumab. Ann Rheum Dis 2014; 73: 1429-1430.
35. Simopoulou T, Tsimourtou V, Katsiari C, Vlychou M, Bogdanos DP, Sakkas LI. Progressive multifocal leukoencephalopathy in a patient with systemic sclerosis treated with methotrexate: A case report and literature review. J Scleroderma Relat Disord 2020; 5: NP1-NP6.
36. Molloy ES. PML and rheumatology: the contribution of disease and drugs. Cleve Clin J Med 2011; 78 Suppl 2: S28-S32.
37. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, et al. Guidelines for preventing and treating vitamin D deficiency and insufficiency revisited. J Clin Endocrinol Metab 2012; 97: 1153-1158.
38. Agostini HT, Deckhut A, Jobes DV, Girones R, Schlunck G, Prost MG, et al. Genotypes of JC virus in east, central and southwest Europe. J Gen Virol 2001; 82: 1221-1331.
39. Szekanecz Z, McInnes IB, Schett G, Szamosi S, Benkő S, Szűcs G. Autoinflammation and autoimmunity across rheumatic and musculoskeletal diseases. Nat Rev Rheumatol 2021; 17: 585-595.
40. Thanou A, Jupe E, Purushothaman M, Niewold TB, Munroe ME. Clinical disease activity and flare in SLE: Current concepts and novel biomarkers. J Autoimmun 2021; 119: 102615.
41. Connelly K, Morand EF. Systemic lupus erythematosus: a clinical update. Intern Med J 2021; 51: 1219-1228.
42. Lan T-Y, Chen Y-S, Cheng C-F, Huang S-T, Shen C-Y, Hsu P-N. Progressive multifocal leukoencephalopathy in systemic lupus erythematosus managed with pembrolizumab: A case report with literature review. Lupus 2021; 30: 1849-1855.
43. Kapoor T, Mahadeshwar P, Hui-Yuen J, Quinnies K, Tatonetti N, Gartshteyn Y, et al. Prevalence of prog ressive multifocal leukoencephalopathy (PML) in adults and children with systemic lupus erythematosus. Lupus Sci Med 2020; 7(1): e000388.
44. Cortese I, Reich DS, Nath A. Progressive multifocal leukoencephalopathy and the spectrum of JC virus-related disease. Nat Rev Neurol 2021; 17: 37-51.
45. Clifford DB, Ances B, Costello C, Rosen-Schmidt S, Andersson M, Parks D, et al. Rituximab-associated progressive multifocal leukoencephalopathy in rheumatoid arthritis. Arch Neurol 2011; 68: 1156-1164.
46. Nosaki Y, Ohyama K, Watanabe M, Yokoi T, Nakamichi K, Saijo M, et al. Simultaneous development of progressive multifocal leukoencephalopathy and cryptococcal meningitis during methotrexate and infliximab treatment. Intern Med 2019; 58: 2703-2709.
47. Rodio DM, Anzivino E, Mischitelli M, Bellizzi A, Scrivo R, Scribano D, et al. Increased prevalence of human polyomavirus JC viruria in chronic inflammatory rheumatic diseases patients in treatment with anti-TNF α: A 18 month follow-up study. Front Microbiol 2016; 7: 672.
48. Verheyen J, Maizus K, Feist E, Tolman Z, Knops E, Saech J, et al. Increased frequency of JC-polyomavirus detection in rheumatoid arthritis patients treated with multiple biologics. Med Microbiol Immunol 2015; 204: 613-618.
49. Comar M, Delbue S, Lepore L, Martelossi S, Radillo O, Ronfani L, et al. Latent viral infections in young patients with inflammatory diseases treated with biological agents: prevalence of JC virus genotype 2. J Med Virol 2013; 85: 716-722.
50. 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.
51. Hu C, Huang Y, Su J, Wang M, Zhou Q, Zhu B. Detection and analysis of variants of JC polyomavirus in urine samples from HIV-1-infected patients in China’s Zhejiang Province. J Int Med Res 2018; 46: 1024-1032.
52. Haghi Navand A, Jalilian S, Ahmadi Angali K, Karimi Babaahmadi M, Talaiezadeh A, Makvandi M. A new evaluation of the rearranged non-coding control region of JC virus in patients with colorectal cancer. BMC Cancer 2024; 24: 1001.
53. Atyabi SR, Bouzari M, Kardi MT. John cunningham (JC) virus genotypes in kidney transplant recipients, rheumatoid arthritis patients and healthy individuals in Isfahan, Iran. J Med Virol 2017; 89: 337-344.
54. Tanasescu R, Frakich N, Chou IJ, Filippini P, Podda G, Xin G, et al. Natalizumab treatment of relapsing remitting Multiple Sclerosis Has No Long-Term Effects on the proportion of circulating regulatory T cells. Neurol Ther 2023; 12: 2041-2052.
55. Honma T, Onda K, Masuyama K. Progressive multifocal leukoencephalopathy reports in rheumatoid arthritis concerning different treatment patterns-an exploratory assessment using the food and drug administration adverse event reporting system. Front Drug Saf Regul 2024; 4: 1334468.
56. Bellizzi A, Anzivino E, Ferrari F, Di Nardo G, Colosimo MT, Fioriti D, et al. Polyomavirus JC reactivation and noncoding control region sequence analysis in pediatric Crohn’s disease patients treated with infliximab. J Neurovirol 2011; 17: 303-313.
57. Campbell GR, Spector SA. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog 2012; 8(5): e1002689.
58. Saleh M, Welsch C, Cai C, Döring C, Gouttenoire J, Friedrich J, et al. Differential modulation of hepatitis C virus replication and innate immune pathways by synthetic calcitriol-analogs. J Steroid Biochem Mol Biol 2018; 183: 142-151.
59. Goncalves-Mendes N, Talvas J, Dualé C, Guttmann A, Corbin V, Marceau G, et al. Impact of vitamin D supplementation on influenza vaccine response and immune functions in deficient elderly persons: a randomized placebo-controlled trial. Front Immunol 2019; 10: 65.
60. Farnik H, Bojunga J, Berger A, Allwinn R, Waidmann O, Kronenberger B, et al. Low vitamin D serum concentration is associated with high levels of hepatitis B virus replication in chronically infected patients. Hepatology 2013; 58: 1270-1276.
61. Gibbons JB, Norton EC, McCullough JS, Meltzer DO, Lavigne J, Fiedler VC, et al. Gibbons RD. Association between vitamin D supplementation and COVID-19 infection and mortality. Sci Rep 2022; 12: 19397.
62. Megahed A, Gadalla H, Abdelhamid FM, Almehmadi SJ, Khan AA, Albukhari TA, et al. Vitamin D ameliorates the hepatic oxidative damage and fibrotic effect caused by thioacetamide in rats. Biomedicines 2023; 11: 424.
63. Czaja AJ, Montano-Loza AJ. Evolving role of vitamin D in immune-mediated disease and its implications in autoimmune hepatitis. Dig Dis Sci 2019; 64: 324-344.
| Files | ||
| Issue | Vol 16 No 5 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i5.16803 | |
| Keywords | ||
| JC virus; Arthritis; Rheumatoid; Lupus erythematosus; Polymerase chain reaction | ||
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Irani Mokhtari G, Azaran A, Rajahi E, Hesam S, Dehghani Ghahfarokhi A, Makvandi M. Prevalence of JC polyomavirus among rheumatoid arthritis and systemic lupus erythematosus patients and its correlation with vitamin D levels. Iran J Microbiol. 2024;16(5):676-683.
