An update on the association of vitamin D deficiency with common infectious diseases1

Canadian Journal of Physiology and Pharmacology

Volumn 93, Issue 5, 2015, Pages 363-368

  Watkins, Richard R ^a,b   Lemonovich, Tracy L ^c,d   Salata, Robert A ^c,d  

^a Northeastern Ohio Medical University   (United States)

^b AKRON GENERAL MEDICAL CENTER   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

HIV; Immunity; MRSA; Pneumonia; Sepsis; Therapy; Vitamin D

Indexed keywords

VITAMIN D;

ADAPTIVE IMMUNITY; HEPATITIS C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION; INFLUENZA; INNATE IMMUNITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY TRACT INFECTION; REVIEW; SEPSIS; VITAMIN D DEFICIENCY; ANIMAL; COMMUNICABLE DISEASES; IMMUNOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; COMMUNICABLE DISEASES; HUMANS; IMMUNITY, INNATE; SEPSIS; VITAMIN D; VITAMIN D DEFICIENCY;

EID: 84928887251     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/cjpp-2014-0352     Document Type: Review

References (70)

1. Amrein, K., Zajic, P., Schnedl, C., Waltensdorfer, A., Fruhwald, S., Holl, A., et al. 2014. Vitamin D status and its association with season, hospital and sepsis mortality in critical illness. Crit. Care, 18(2): R47. doi:10.1186/cc13790. PMID: 24661739.
2. Ansemant, T., Mahy, S., Piroth, C., Ornetti, P., Ewing, S., Guilland, J.C., et al. 2013. Severe hypovitaminosis D correlates with increased inflammatory markers in HIV infected patients. BMC Infect. Dis. 13: 7. doi:10.1186/1471-2334-13-7. PMID:23295013.
3. Aziz, M., Livak, B., Burke-Miller, J., French, A.L., Glesby, M.J., Sharma, A., et al. 2013. Vitamin D insufficiency may impair CD4 recovery among Women’s Interagency HIV Study participants with advanced disease on HAART. AIDS, 27(4): 573–578. doi:10.1097/QAD.0b013e32835b9ba1. PMID:23095316.
4. Beard, J.A., Bearden, A., and Striker, R. 2012. Vitamin D and the anti-viral state. J. Clin. Virol. 50(3): 194–200. doi:10.1016/j.jcv.2010.12.006. PMID:21242105.
5. Bergman, P., Lindh, A.U., Björkhem-Bergman, L., and Lindh, J.D. 2013. Vitamin D and respiratory tract infections: a systematic review and meta-analysis of randomized controlled trials. PLoS One, 8(6): e65835. doi:10.1371/journal.pone.0065835. PMID:23840373.
6. Braun, A., Chang, D., Mahadevappa, K., Gibbons, F.K., Liu, Y., Giovannucci, E., et al. 2011. Association of low serum 25-hydroxyvitamin D levels and mortality in the critically ill. Crit. Care Med. 39(4): 671–677. doi:10.1097/CCM.0b013e318206ccdf. PMID:21242800.
7. Campbell, G.R., and Spector, S.A. 2012. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog. 8(5): e1002689. doi:10.1371/journal.ppat.1002689. PMID:22589721.
8. Cervero, M., Agud, J.L., Torres, R., García-Lacalle, C., Alcázar, V., Jusdado, J.J., et al. 2013. Higher vitamin D levels in HIV-infected out-patients on treatment with boosted protease inhibitor monotherapy. HIV Med. 14(9): 556–562. doi: 10.1111/hiv.12049. PMID:23738846.
9. Chen, S., Sims, G.P., Chen, X.X., Gu, Y.Y., Chen, S., and Lipsky, P.E. 2007. Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J. Immunol. 179(3): 1634–1647. doi:10.4049/jimmunol.179.3.1634. PMID: 17641030.
10. Coussens, A.K., Wilkinson, R.J., Hanifa, Y., Nikolayevskyy, V., Elkington, P.T., Islam, K., et al. 2012. Vitamin D accelerates resolution of inflammatory responses during tuberculosis treatment. Proc. Natl. Acad. Sci. U.S.A. 109(38): 15449–15454. doi:10.1073/pnas.1200072109. PMID:22949664.
11. Danai, P.A., Sinha, S., Moss, M., Haber, M.J., and Martin, G.S. 2007. Seasonal variation in the epidemiology of sepsis. Crit. Care Med. 35(2): 410–415. doi: 10.1097/01.CCM.0000253405.17038.43. PMID:17167351.
12. Falleti, E., Bitetto, D., Fabris, C., Fattovich, G., Cussigh, A., Cmet, S., et al. 2012. Vitamin D binding protein gene polymorphisms and baseline vitamin D levels as predictors of antiviral response in chronic hepatitis C. Hepatology, 56(5): 1641–1650. doi:10.1002/hep.25848. PMID:22610885.
13. Ferreira, G.B., Kleijwegt, F.S., Waelkens, E., Lage, K., Nikolic, T., Hansen, D.A., et al. 2012. Differential protein pathways in 1,25-dihydroxyvitamin D(3) and dexamethasone modulated tolerogenic human dendritic cells. J. Proteome Res. 11(2): 941–971. doi:10.1021/pr200724e. PMID:22103328.
14. Grey, A., and Bolland, M. 2012. Vitamin D and tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 109(51): E3528. doi:10.1073/pnas.1216417109. PMID:23132936.
15. Griffin, A.T., and Arnold, F.W. 2012. Review of metabolic, immunologic, and virologic consequences of suboptimal vitamin D levels in HIV infection. AIDS Patient Care STDS, 26(9): 516–525. doi:10.1089/apc.2012.0145. PMID:22861070.
16. Gunther, G. 2014. Multidrug-resistant and extensively drug-resistant tuberculosis: a review of current concepts and future challenges. Clin Med. 14(3): 279–285. doi:10.7861/clinmedicine.14-3-279. PMID:24889573.
17. Guzmán-Fulgencio, M., García-Álvarez, M., Berenguer, J., Jiménez-Sousa, M.Á., Cosin, J., Pineda-Tenor, D., et al. 2014. Vitamin D deficiency is associated with severity of liver disease in HIV/HCV coinfected patients. J. Infect. 68(2): 176–184. doi:10.1016/j.jinf.2013.10.011. PMID:24184809.
18. Havers, F., Smeaton, L., Gupte, N., Detrick, B., Bollinger, R.C., Hakim, J., et al. 2014. 25-Hydroxyvitamin D insufficiency and deficiency is associated with HIV disease progression and virological failure post-antiretroviral therapy initiation in diverse multinational settings. J. Infect. Dis. 210(2): 244-253. doi:10.1093/infdis/jiu259. PMID:24799602.
19. Heine, G., Niesner, U., Chang, H.D., Steinmeyer, A., Zügel, U., Zuberbier, T., 2008. 1,25-Dihydroxyvitamin D(3) promotes IL-10 production in human B cells. Eur. J. Immunol. 38(8): 2210-2218. doi:10.1002/eji.200838216. PMID: 18651709.
20. Hewison, M. 2012a. Vitamin D and immune function: an overview. Proc. Nutr. Soc. 71(1): 50–61. doi:10.1017/S0029665111001650. PMID:21849106.
21. Hewison, M. 2012b. An update on vitamin D and human immunity. Clin. Endocrinol. (Oxf.), 76(3): 315–325. doi:10.1111/j.1365-2265.2011.04261.x. PMID: 21995874.
22. Holick, M.F. 2007. Vitamin D deficiency. N. Engl. J. Med. 357(3): 266–281. doi:10.1056/NEJMra070553. PMID:17634462.
23. Honda, J.R., Connick, E., MaWhinney, S., Chan, E.D., and Flores, S.C. 2014. Plasma LL-37 correlates with vitamin D and is reduced in human immunodeficiency virus-1 infected individuals not receiving antiretroviral therapy. J. Med. Microbiol. 63(7): 997–1003. doi:10.1099/jmm.0.070888-0. PMID: 24821067.
24. Iho, S., Takahashi, T., Kura, F., Sugiyama, H., and Hocino, T. 1986. The effect of 1,25-dihydroxyvitamin D3 on in vitro immunoglobulin production in human B cells. J. Immunol. 136(12): 4427–4431. PMID:3519769.
25. Jarvis, J.N., Bicanic, T., Loyse, A., Meintjes, G., Hogan, L., Roberts, C., et al. 2014. Very low levels of 25-hydroxyvitamin D are not associated with immunologic changes or clinical outcomes in South African patients with HIV-associated cryptococcal meningitis. Clin. Infect. Dis. 59(4): 493–500. doi:10.1093/cid/ciu349. PMID:24825871.
26. Jefferson, T., Jones, M.A., Doshi, P., Del Mar, C.B., Hama, R., Thompson, M.J., et al. 2014. Neuraminidase inhibitors for preventing and treating influenza in healthy adults and children. Cochrane Database Syst. Rev. 4: CD008965. doi:10.1002/14651858.CD008965.pub4. PMID:24718923.
27. Jeffery, L.E., Wood, A.M., Qureshi, O.S., Hou, T.Z., Gardner, D., Briggs, Z., et al. 2012. Availability of 25-hydroxyvitamin D(3) to APCs controls the balance between regulatory and inflammatory T cell responses. J. Immunol. 189(11): 5155–5164. doi:10.4049/jimmunol.1200786. PMID:23087405.
28. Jeng, L., Yamshchikov, A.V., Judd, S.E., Blumberg, H.M., Martin, G.S., Ziegler, T.R., et al. 2009. Alterations in vitamin D status and anti-microbial peptide levels in patients in the intensive care unit with sepsis. J. Transl. Med. 7: 28. doi:10.1186/1479-5876-7-28. PMID:19389235.
29. Jorde, R., Witham, M., Janssens, W., Rolighed, L., Borchhardt, K., de Boer, I.H., et al. 2012. Vitamin D supplementation did not prevent influenza-like illness as diagnosed retrospectively by questionnaires in subjects participating in randomized controlled trials. Scand. J. Infect. Dis. 44(2): 126–132. doi:10.3109/00365548.2011.621446. PMID:22026455.
30. Jovanovich, A.J., Ginde, A.A., Holmen, J., Jablonski, K., Allyn, R.L., Kendrick, J., et al. 2014. Vitamin D level and risk for community-acquired pneumonia and sepsis. Nutrients, 6(6): 2196–2205. doi:10.3390/nu6062196. PMID:24918697.
31. Kim, J.H., Park, J.S., Cho, Y.J., Yoon, H.I., Song, J.H., Lee, C.T., et al. 2014. Low serum 25-hydroxyvitamin D level: An independent risk factor for tuberculosis? Clin. Nutr. 33(6): 1081–1086. doi:10.1016/j.clnu.2013.11.014. PMID: 24332595.
32. Kitson, M.T., Dore, G.J., George, J., Button, P., McCaughan, G.W., Crawford, D.H., et al. 2013. Vitamin D status does not predict sustained virologic response or fibrosis stage in chronic hepatitis C genotype 1 infection. J. Hepatol. 58(3): 467–472. doi:10.1016/j.jhep.2012.11.017. PMID:23183524.
33. Kohchi, C., Inagawa, H., Nishizawa, T., and Soma, G. 2009. ROS and innate immunity. Anticancer Res. 29(3): 817–822. PMID:19414314.
34. Lake, J.E., and Adams, J.S. 2011. Vitamin D in HIV-Infected Patients. Curr. HIV/ AIDS Rep. 8(3): 133–141. doi:10.1007/s11904-011-0082-8. PMID:21647555.
35. Lange, C.M., Bojunga, J., Ramos-Lopez, E., von Wagner, M., Hassler, A., Vermehren, J., et al. 2011. Vitamin D deficiency and a CYP27B1-1260 promoter polymorphism are associated with chronic hepatitis C and poor response to interferon-alfa based therapy. J. Hepatol. 54(5): 887–893. doi:10.1016/j.jhep.2010.08.036. PMID:21145801.
36. Leow, L., Simpson, T., Cursons, R., Karalus, N., and Hancox, R.J. 2011. Vitamin D, innate immunity and outcomes in community acquired pneumonia. Respirology, 16(4): 611–616. doi:10.1111/j.1440-1843.2011.01924.x. PMID:21244571.
37. Levine, B., Mizushima, N., and Virgin, H.W. 2011. Autophagy in immunity and inflammation. Nature, 469(7330): 323–335. doi:10.1038/nature09782. PMID: 21248839.
38. Li-Ng, M., Aloia, J.F., Pollack, S., Cunha, B.A., Mikhail, M., Yeh, J., and Berbari, N. 2009. A randomized controlled trial of vitamin D3 supplementation for the prevention of symptomatic upper respiratory tract infections. Epidemiol. Infect. 37(10): 1396–404. doi:10.1017/S0950268809002404. PMID:19296870.
39. Liu, P.T., Stenger, S., Li, H., Wenzel, L., Tan, B.H., Krutzik, S.R., et al. 2006. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science, 311(5768): 1770–1773. doi:10.1126/science.1123933. PMID: 16497887.
40. Macaraig, M., Burzynski, J., and Varma, JK. 2014. Tuberculosis control in New York City: a changing landscape. N. Engl. J. Med. 370(25): 2362–2365. doi:10.1056/NEJMp1402147. PMID:24941176.
41. Mandorfer, M., Payer, B.A., Schwabl, P., Steiner, S., Ferlitsch, A., Aichelburg, M.C., et al. 2014. Revisiting liver disease progression in HIV/HCVcoinfected patients: the influence of vitamin D, insulin resistance, immune status, IL28B and PNPLA3. Liver Int. In press. doi:10.1111/liv.12615. PMID: 24905495.
42. Marra, A., Leoncini, G., Mussap, M., Bovio, M., Nazzari, E., Giusti, M., et al. 2014. Severe vitamin D deficiency is associated with frequently observed diseases in medical inpatients. Int. J. Clin. Pract. 68(5): 647–652. doi:10.1111/ijcp.12323. PMID:24499046.
43. Martineau, A.R., Timms, P.M., Bothamley, G.H., Hanifa, Y., Islam, K., Claxton, A.P., et al. 2011. High-dose vitamin D(3) during intensive-phase antimicrobial treatment of pulmonary tuberculosis: a double-blind randomised controlled trial. Lancet, 377(9761): 242–250. doi:10.1016/S0140-6736(10)61889-2. PMID:21215445.
44. Matheson, E.M., Mainous, A.G., Hueston, W.J., Diaz, V.A., and Everett, C.J. 2010. Vitamin D and methicillin-resistant Staphylococcus aureus nasal carriage. Scand. J. Infect. Dis. 42(6–7): 455–460. doi:10.3109/00365541003602049. PMID:20210515.
45. Mora, J.R., Iwata, M., and von Andrian, U.H. 2008. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat. Rev. Immunol. 8(9): 685–698. doi:10.1038/nri2378. PMID:19172691.
46. Moromizato, T., Litonjua, A.A., Braun, A.B., Gibbons, F.K., Giovannucci, E., and Christopher, K.B. 2014. Association of low serum 25-hydroxyvitamin D levels and sepsis in the critically ill. Crit. Care Med. 42(1): 97–107.oi:10.1097/CCM.0b013e31829eb7af. PMID:23982028.
47. Nguyen, H.B., Eshete, B., Lau, K.H., Sai, A., Villarin, M., and Baylink, D. 2013. Serum 1,25-dihydroxyvitamin D: an outcome prognosticator in human sepsis. PLoS One, 8(5): e64348. doi:10.1371/journal.pone.0064348. PMID:23741318.
48. Olliver, M., Spelmink, L., Hiew, J., Meyer-Hoffert, U., Henriques-Normark, B., and Bergman, P. 2013. Immunomodulatory effects of vitamin D on innate and adaptive immune responses to Streptococcus pneumoniae. J. Infect. Dis. 208(9): 1474–1481. doi:10.1093/infdis/jit355. PMID:23922371.
49. Ooi, J.H., McDaniel, K.L., Weaver, V., and Cantorna, M.T. 2014. Murine CD8+ T cells but not macrophages express the vitamin D 1 alpha-hydroxylase. J. Nutr. Biochem. 25(1): 58–65. doi:10.1016/j.jnutbio.2013.09.003. PMID:24314866.
50. Pinzone, M.R., Di Rosa, M., Malaguarnera, M., Madeddu, G., Foca, E., Ceccarelli, G., et al. 2013. Vitamin D deficiency in HIV infection: an underestimated and undertreated epidemic. Eur. Rev. Med. Pharmacol. Sci. 17(9): 1218–1232. PMID:23690192.
51. Pletz, M.W., Terkamp, C., Schumacher, U., Rohde, G., Schütte, H., Welte, T., et al. 2014. Vitamin D deficiency in community-acquired pneumonia: low levels of 1,25(OH)2 D are associated with disease severity. Respir. Res. 15: 53. doi:10.1186/1465-9921-15-53. PMID:24766747.
52. Rathored, J., Sharma, S.K., Singh, B., Banavaliker, J.N., Sreenivas, V., Srivastava, A.K., et al. 2012. Risk and outcome of multidrug-resistant tuberculosis: vitamin D receptor polymorphisms and serum 25(OH)D. Int. J. Tuberc. Lung Dis. 16(11): 1522–1528. doi:10.5588/ijtld.12.0122. PMID:22990231.
53. Ross, A.C., Manson, J.E., Abrams, S.A., Aloia, J.F., Brannon, P.M., Clinton, S.K., et al. 2011. The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J. Clin. Endocrinol. Metab. 96(1): 53–58. doi:10.1210/jc.2010-2704. PMID: 21118827.
54. Salamon, H., Bruiners, N., Lakehal, K., Shi, L., Ravi, J., Yamaguchi, K.D., et al. 2014. Cutting edge: vitamin D regulates lipid metabolism in Mycobacterium tuberculosis infection. J. Immunol. 193(1): 30–34. doi:10.4049/jimmunol.1400736. PMID:24899504.
55. Shepherd, L., Souberbielle, J.C., Bastard, J.P., Fellahi, S., Capeau, J., Reekie, J., et al. 2014. Prognostic value of vitamin D level for all-cause mortality, and association with inflammatory markers, in HIV-infected persons. J. Infect. Dis. 210(2): 234–243. doi:10.1093/infdis/jiu074. PMID:24493824.
56. Shin, D.M., Yuk, J.M., Lee, H.M., Lee, S.H., Son, J.W., Harding, C.V., et al. 2010. Mycobacterial lipoprotein activates autophagy via TLR2/1/CD14 and a functional vitamin D receptor signaling. Cell. Microbiol. 12(11): 1648–1665. doi:10.1111/j.1462-5822.2010.01497.x. PMID:20560977.
57. Sundaram, M.E., Talbot, H.K., Zhu, Y., Griffin, M.R., Spencer, S., Shay, D.K., et al. 2013. Vitamin D is not associated with serologic response to influenza vaccine in adults over 50 years old. Vaccine, 31(16): 2057–2061. doi:10.1016/j.vaccine.2013.02.028. PMID:23453766.
58. Torres, C., Sánchez de la Torre, M., García-Moruja, C., Carrero, A.J., Trujillo Mdel, M., Fibla, J., et al. 2010. Immunophenotype of vitamin D receptor polymorphism associated to risk of HIV-1 infection and rate of disease progression. Curr. HIV Res. 8(6): 487–492. doi:10.2174/157016210793499330. PMID:20642435.
59. Uberti, F., Lattuada, D., Morsanuto, V., Nava, U., Bolis, G., Vacca, G., et al. 2014. Vitamin D protects human endothelial cells from oxidative stress through the autophagic and survival pathways. J. Clin. Endocrinol. Metab. 99(4): 1367–1374. doi:10.1210/jc.2013-2103. PMID:24285680.
60. Vergne, I., Chua, J., Singh, S.B., and Deretic, V. 2004. Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20: 367–394. doi:10.1146/annurev.cellbio.20.010403.114015. PMID:15473845.
61. Verway, M., Bouttier, M., Wang, T.T., Carrier, M., Calderon, M., An, B.S., et al. 2013. Vitamin D induces interleukin-1_ expression: paracrine macrophage epithelial signaling controls M. tuberculosis infection. PLoS Pathog. 9(6): e1003407. doi:10.1371/journal.ppat.1003407. PMID:23762029.
62. Villar, L.M., Del Campo, J.A., Ranchal, I., Lampe, E., and Romero-Gomez, M. 2013. Association between vitamin D and hepatitis C virus infection: a metaanalysis. World J. Gastroenterol. 19(35): 5917–5924. doi:10.3748/wjg.v19.i35.5917. PMID:24124339.
63. Wang, H.E., Shapiro, N.I., Angus, D.C., and Yealy, D.M. 2007. National estimates of severe sepsis in the United States emergency departments. Crit. Care Med. 35(8): 1928–1936. doi:10.1097/01.CCM.0000277043.85378.C1. PMID:17581480.
64. Wang, J., Lian, H., Zhao, Y., Kauss, M.A., and Spindel, S. 2008. Vitamin D3 induces autophagy of human myeloid leukemia cells. J. Biol. Chem. 283(37): 25596–25605. doi:10.1074/jbc.M801716200. PMID:18628207.
65. Watkins, R.R. 2012. Investigating the association between vitamin D deficiency and sepsis: challenges and future prospects. Expert Rev. Anti Infect. Ther. 10(7): 723–725. doi:10.1586/eri.12.61. PMID:22943393.
66. Watkins, R.R., Yamshchikov, A.V., Lemonovich, T.L., and Salata, R.A. 2011. The role of vitamin D deficiency in sepsis and potential therapeutic implications. J. Infect. 63(5): 321–326. doi:10.1016/j.jinf.2011.07.002. PMID:21777617.
67. Wejse, C., Gomes, V.F., Rabna, P., Gustafson, P., Aaby, P., Lisse, I.M., et al. 2009. Vitamin D as supplementary treatment for tuberculosis: a double-blind, randomized, placebo-controlled trial. Am. J. Respir. Crit. Care Med. 179(9): 843–850. doi:10.1164/rccm.200804-567OC. PMID:19179490.
68. Wohl, D.A., Orkin, C., Doroana, M., Pilotto, J.H., Sungkanuparph, S., Yeni, P., et al. 2014. Change in vitamin D levels and risk of severe vitamin D deficiency over 48 weeks among HIV-1-infected, treatment-naive adults receiving rilpivirine or efavirenz in a Phase III trial (ECHO). Antivir. Ther. 19(2): 191–200. doi:10.3851/IMP2721. PMID:24430534.
69. Xia, J., Shi, L., Zhao, L., and Xu, F. 2014. Impact of vitamin D supplementation on the outcome of tuberculosis treatment: a systematic review and metaanalysis of randomized controlled trials. Chin. Med. J. (Engl.), 127(17): 3127–3134. PMID:25189958.
70. Youssef, D., Bailey, B., El-Abbassi, A., Vannoy, M., Manning, T., Moorman, J.P., et al. 2012. Healthcare costs of methicillin resistant Staphylococcus aureus and Pseudomonas aeruginosa infections in veterans: role of vitamin D deficiency.Eur. J. Clin. Microbiol. Infect. Dis. 31(3): 281–286. doi:10.1007/s10096-011-1308-9. PMID:21695580.