719
Views
41
CrossRef citations to date
0
Altmetric
Review

BCG and protection against inflammatory and auto-immune diseases

&
Pages 699-708 | Received 21 Feb 2017, Accepted 19 May 2017, Published online: 30 May 2017

References

  • Calmette A, Guérin C. Sur quelques propriétés du bacilli tuberculeux d’origine bovine, cultivé sur la bile de boeuf glycérinée. Compt Rend Acad Sci. 1909;149:716–718.
  • Calmette A, Guérin C, Nègre L, et al. Prémunition des nouveaux-nés contre la tuberculose par le vaccin BCG (1921 à 1926). Ann Inst Pasteur. 1926;40:89–133.
  • Monteiro-Maia R, De Pinho T. Oral bacillus Calmette-Guérin vaccine against tuberculosis: why not? Mem Inst Oswaldo Cruz. 2014;109:838–845.
  • World Health Organization. BCG vaccine. WHO position paper. Wkly Epidemiol Rec. 2004;79:27–38.
  • Colditz GA, Berkey CS, Mosteller F, et al. The efficacy of bacillus Calmette-Guérin vaccination of newborns and infants in the prevention of tuberculosis: meta-analysis of the published literature. Pediatrics. 1995;96:29–35.
  • Colditz GA, Brewer TF, Berkey CS, et al. Efficacy of BCG vaccine in the prevention of tuberculosis: meta-analysis of the published literature. Jama. 1994;271:698–702.
  • Parkash O. How to avoid the impact of environmental mycobacteria towards the efficacy of BCG vaccination against tuberculosis? Int J Mycobacteriol. 2014;3:1–4.
  • Soysal A, Millington KA, Bakir M, et al. Effect of BCG vaccination on risk of Mycobacterium tuberculosis infection in children with household tuberculosis contact: a prospective community-based study. Lancet. 2005;366:1443–1451.
  • Mascart F, Locht C. Integrating knowledge of Mycobacterium tuberculosis pathogenesis for the design of better vaccines. Expert Rev Vaccines. 2015;14:1573–1585.
  • Lewis KN, Liao R, Guinn KM, et al. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guérin attenuation. J Infect Dis. 2003;187:117–123.
  • Van Der Wel N, Hava D, Houben D, et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid. Cells Cell. 2007;129:1287–1298.
  • Pym AS, Brodin P, Majlessi L, et al. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med. 2003;9:533–539.
  • Brosch R, Gordon SV, Garnier T, et al. Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci USA. 2007;104:5596–5601.
  • Magdalena J, Supply P, Locht C. Specific differentiation between Mycobacterium bovis BC and virulent strains or the Mycobacterium tuberculosis complex. J Clin Microbiol. 1998;36:2471–2476.
  • Behr MA, Wilson MA, Gill WP, et al. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science. 1999;284:1520–1523.
  • Stanley SJ, Howland C, Stone MM, et al. BCG vaccination of children against leprosy in Uganda: final results. J Hyg Camb. 1981;87:233–248.
  • Orege PA, Fine PE, Lucas SB, et al. Case-control study of BCG vaccination as a risk factor for leprosy and tuberculosis in western Kenya. Int J Lepr Other Mycobact Dis. 1993;61:542–549.
  • Pönnighaus JM, Fine PE, Sterne JA, et al. Efficacy of BCG vaccine against leprosy and tuberculosis in northern Malawi. Lancet. 1992;339:636–639.
  • Setia MS, Steinmaus C, Ho CS, et al. The role of BCG in prevention of leprosy: a meta-analysis. Lancet Infect Dis. 2006;6:162–170.
  • Rodrigues LC, Pereira SM, Cunha SS, et al. Effect of BCG revaccination on incidence of tuberculosis in school-aged children in Brazil: the BCG-REVAC cluster-randomised trial. Lancet. 2005;366:1290–1295.
  • Cunha SS, Alexander N, Barreto ML, et al. BCG revaccination does not protect against leprosy in the Brazilian Amazon: a cluster randomised trial. Plos Negl Trop Dis. 2008;13:e167.
  • MacCallum P, Tolhurst JC, Buckle G, et al. A new mycobacterial infection in man. J Pathol Bacteriol. 1948;60:93–122.
  • The Uganda Buruli Group. B.C.G. Vaccination against Mycobacterium ulcerans infection (Buruli ulcer). Lancet. 1969;1:111–115.
  • Portaels F, Aguiar J, Debacker M, et al. Prophylactic effect of Mycobacterium bovis BCG vaccination against osteomyelitis in children with Mycobacterium ulcerans disease (Buruli ulcer). Clin Diag Lab Immunol. 2002;9:1389–1391.
  • Raghunathan PL, Whitney EA, Asamoa K, et al. Risk factors for Buruli ulcer disease (Mycobacterium ulcerans infection): results from a case-control study in Ghana. Clin Infect Dis. 2005;40:1445–1453.
  • Nackers F, Dramaix M, Johnson RC, et al. BCG vaccine effectiveness against Buruli ulcer: a case-control study in Benin. Am J Trop Med Hyg. 2006;75:768–774.
  • Phillips RO, Phanzu DM, Beissner M, et al. Effectiveness of routine BCG vaccination on Buruli ulcer disease: a case-control study in the Democratic Republic of Congo, Ghana and Togo. Plos Negl Trop Dis. 2015;9:e3457.
  • Converse PJ, Almeida DV, Nuermberger EL, et al. BCG-mediated protection against Mycobacterium ulcerans infection in the mouse. Plos Negl Trop Dis. 2011;5:e985.
  • Pearl R. Cancer and tuberculosis. Am J Hyg. 1929;9:97–159.
  • Old LJ, Clarke DA, Benacerraf B. The effect of bacillus Calmette-Guérin infection on transplanted tumors in mice. Nature. 1959;184:291–292.
  • Silverstein MJ, DeKernion J, Morton DL. Malignant melanoma metastatic to the bladder. Regression following intratumor injection of BCG vaccine. Jama. 1974;229:688.
  • Herr HW, Morales A. History of bacillus Calmette-Guérin and bladder cancer: an immunotherapy success story. J Urol. 2008;179:53–56.
  • Kuroda K, Brown EJ, Telle WB, et al. Characterization of the internalization of bacillus Calmette-Guérin by human bladder tumor cells. J Clin Invest. 1993;91:69–76.
  • Ludwig AT, Moore JM, Luo Y, et al. Tumor necrosis factor-related apoptosis-inducing ligand: a novel mechanism for Bacillus Calmette-Guérin-induced antitumor activity. Cancer Res. 2004;64:3386–3390.
  • Kristensen I, Aaby P, Jensen H. Routine vaccinations and child survival; follow up study in Guinea-Bissau, West Africa. Bmj. 2000;321:1–8.
  • Naeslund C. Expérience de vaccination par le BCG dans la province du Norrbotten (Suède). Rev Tuberc. 1931;12:617–636.
  • Beiring-Sorensen S, Aaby P, Napirna BM, et al. Small randomized trial among low-birth-weight children receiving bacillus Calmette-Guérin vaccination at first health center contact. Pediatr Infect Dis J. 2012;31:306–308.
  • Hollm-Delgado MG, Stuart EA, Black RE. Acute lower respiratory infection among bacille Calmette-Guérin (BCG)-vaccinated children. Pediatrics. 2014;133:e73–e81.
  • Kleinnijenhuis J, Quintin J, Preijers F, et al. Bacille Calmette-Guérin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci USA. 2012;109:17537–17542.
  • Arts RJ, Carvalho A, LaRocca C, et al. Immunometabolic pathways in BCG-induced trained immunity. Cell Rep. 2016;17:2562–2571.
  • Johansson SG, Hourihane JO, Bousquet J, et al. EAACI (the European Academy of Allergology and Clinical Immunology) nomenclature task force – a revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy. 2001;56:813–824.
  • Akdis M. New treatments for allergen immunotherapy. World Allergy Org J. 2014;7:23.
  • Bantz SK, Zhu Z, Zheng T. The atopic march: progression from atopic dermatitis to allergic rhinitis and asthma. J Clin Cell Immunol. 2014;5:2.
  • Gould HJ, Ramadani F. IgE responses in mouse and man and the persistence of IgE memory. Trends Immunol. 2015;36:40–48.
  • Brooks C, Pearce N, Douwes J. The hygiene hypothesis in allergy and asthma: an update. Curr Opin Allergy Clin Immunol. 2013;13:70–77.
  • Braun-Fahrländer C, Gassner M, Grize L, et al. Prevalence of hay fever and allergic sensitization in farmer’s children and their peers living in the same rural community. Clin Exp Allergy. 1999;29:28–34.
  • Hogg C. T-helper polarization in atopic disease – how early does it occur? Clin Exp Allergy. 1997;27:1237–1239.
  • Rook GAW, Hamelmann E, Brunet LR. Mycobacteria and allergies. Immunobiology. 2007;212:461–473.
  • Erb KJ, Holloway JW, Sobeck A, et al. Infection of mice with Mycobacterium bovis bacillus Calmette-Guerin (BCG) suppresses allergen-induced airway eosinophilia. J Exp Med. 1998;187:561–569.
  • Hopfenspriger MT, Agrawal DK. Airway hyperresponsiveness, late allergic response, and eosinophilia are reversed with mycobacterial antigens in ovalbumin-presensitized mice. J Immunol. 2002;168:2516–2522.
  • Barlan I, Bahceciler NN, Akdis M, et al. Bacillus Calmette-Guérin, Mycobacterium bovis, as an immunomodulator in atopic diseases. Immunol Allergy Clin North Am. 2006;26:365–377.
  • Herz U, Gerhold K, Grüber C, et al. BCG infection suppresses allergic sensitization and development of increased airway reactivity in an animal model. J Allergy Clin Immunol. 1998;102:867–874.
  • Scanga CB, Le Gros G. Development of an asthma vaccine: research into BCG. Drugs. 2000;59:1217–1221.
  • Zuany-Amorim C, Sawicka E, Manlius C, et al. Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells. Nat Med. 2002;8:625–629.
  • Akdis M, Verhagen J, Taylor A, et al. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J Exp Med. 2004;199:1567–1575.
  • Ahrens B, Gruber C, Rha RD, et al. BCG priming of dendritic cells enhances T regulatory and Th1 function and suppresses allergen-induced Th2 function in vitro and in vivo. Int Arch Allergy Immunol. 2009;150:210–220.
  • Kim YJ, Kim HJ, Kang MJ, et al. Bacillus Calmette-Guérin suppresses asthmatic responses via CD4(+)CD25(+) regulatory T cells and dendritic cells. Allergy Asthma Immunol Res. 2014;6:201–207.
  • Qu SY, Ou-Yang HF, He YL, et al. Der p2 recombinant bacille Calmette-Guerin priming of bone marrow-derived dendritic cells suppresses Der p2-induced T helper17 function in a mouse model of asthma. Respirology. 2014;19:122–131.
  • Okamura HH, Tsutsi T, Komatsu M, et al. Cloning of a new cytokine that induces IFN gamma production by T cells. Nature. 1995;378:88–91.
  • Wawrocki S, Druszczynska M, Kowalewicz-Kulbat M, et al. Interleukin 18 (IL-18) as a target for immune intervention. Acta Biochim Pol. 2016;63:59–63.
  • Ming-Hui X, Feng-Lai Y, Shu-Jing W, et al. Association of interleukin-18 and asthma. Inflammation. 2017;40:324–327.
  • Kowalewicz-Kulbat M, Pestel J, Biet F, et al. Mycobacterium bovis BCG Mycobacteria – new application. Pol J Microb. 2006;15:13–17.
  • Biet F, Kremer L, Wolowczuk I, et al. Mycobacterium bovis BCG producing interleukin-18 increases antigen-specific gamma interferon production in mice. Infect Immun. 2002;60:6549–6557.
  • Biet F, Duez C, Kremer L, et al. Recombinant Mycobacterium bovis BCG producing IL-18 reduces IL-5 production and bronchoalveolar eosinophilia induced by an allergic reaction. Allergy. 2005;60:1065–1072.
  • Luo Y, Yamada H, Chen X, et al. Recombinant Mycobacterium bovis bacillus Calmette-Guérin (BCG) expressing mouse IL-18 augments Th1 immunity and macrophage cytotoxicity. Clin Exp Immunol. 2004;137:24–34.
  • Szpakowski P, Biet F, Locht C, et al. Dendritic cell activity driven by recombinant Mycobacterium bovis BCG producing human IL-18, in healthy BCG vaccinated adults. J Immunol Res. 2015;2015:359153.
  • Shirakawa T, Enomoto T, Shimazu S, et al. The inverse association between tuberculin responses and atopic disorder. Science. 1999;275:77–79.
  • Aaby P, Shaheen SO, Heyes CB, et al. Early BCG vaccination and reduction in atopy in Guinea-Bissau. Clin Exp Allergy. 2000;30:644–650.
  • Marks GB, Ng K, Zhou J, et al. The effect of neonatal BCG vaccination on atopy and asthma at age 7 to 14 years: an historical cohort study in a community with a very low prevalence of tuberculosis infection and a high prevalence of atopic disease. J Allergy Clin Immunol. 2003;111:541–549.
  • Grüber C, Kulig M, Bergmann R. Delayed hypersensitivity to tuberculin total immunoglobulin E, specific sensitization, and atopic manifestation in longitudinally followed early bacille-Calmette-Guérin-vaccinated and nonvaccinated children. Pediatrics. 2001;107:E36.
  • Omenaas E, Jentoft HF, Vollmer WM, et al. Absence of relationship between tuberculin reactivity and atopy in BCG vaccinated young adults. Thorax. 2000;55:454–458.
  • Strannegard I, Larsson L, Wennergren G, et al. Prevalence of allergy in children in relation to prior BCG vaccination and infection with atypical mycobacteria. Allergy. 1998;53:249–254.
  • Alm J, Lilja G, Pershagen G, et al. Early BCG vaccination and the development of atopy. Lancet. 1997;350:400–403.
  • Linehan MF, Nurmatov U, Frank TL, et al. Does BCG vaccination protect against childhood asthma? Final results from the Manchester Community Asthma Study retrospective cohort study and updated systematic review and meta-analysis. J Allergy Clin Immunol. 2014;133:688–695.
  • Andersen E, Isager H, Hyllested K. Risk factors in multiple sclerosis tuberculin reactivity, age at measles infection, tonsillectomy and appendectomy. Acta Neurol Scandinav. 1981;63:131–135.
  • Ristori G, Buzzi M, Sabatini U, et al. Use of bacille Calmette-Guérin (BCG) in multiple sclerosis. Neurology. 1999;53:1588–1589.
  • Paolillo A, Buzzi MG, Giugni E, et al. The effect of bacille Calmette-Guérin on the evolution of new enhancing lesions to hypointense T1 lesions in relapsing remitting MS. J Neurol. 2003;250:247–248.
  • Ristori G, Romano S, Cannoni S, et al. Effects of bacille Calmette-Guérin after the first demyelinating event in the CNS. Neurology. 2014;82:41–48.
  • Sewell DL, Reinke EK, Co DO, et al. Infection with Mycobacterium bovis BCG diverts traffic of myelin oligodendroglial glycoprotein autoantigen-specific T cells away from the central nervous system and ameliorates experimental autoimmune encephalomyelitis. Clin Diag Lab Immunol. 2003;10:564–572.
  • Dalton DK, Haynes L, Chu CQ, et al. Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med. 2000;192:117–122.
  • O’Connor RA, Wittmer S, Dalton DK. Infection-induced apoptosis deletes bystander CD4+ T cells: a mechanism for suppression of autoimmunity during BCG infection. J Autoimmun. 2005;24:93–100.
  • Harrington LE, Hatton RD, Mangan PR, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 2005;6:1123–1132.
  • Komiyama Y, Nakae S, Matsuki T, et al. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol. 2006;177:566–573.
  • Lee JE, Reinke EK, Zozulya AL, et al. Mycobacterium bovis bacille Calmette-Guérin infection in the CNS suppresses experimental autoimmune encephalomyelitis and Th17 responses in an IFN-γ-independent manner. J Immunol. 2008;181:6201–6212.
  • Lampropoulou V, Hoehlig K, Roch T, et al. TLR-activated B cells suppress T cell-mediated autoimmunity. J Immunol. 2008;180:4763–4773.
  • Patterson C, Guariguata L, Dahlquist G, et al. Diabetes in the young – a global view and worldwide estimates of numbers of children with type 1 diabetes. Diabetes Res Clin Pract. 2014;103:161–175.
  • Cabrera SM, Rigby MR, Mirmira RG. Targeting regulatory T cells in the treatment of type 1 diabetes mellitus. Curr Mol Med. 2012;12:1261–1272.
  • Stankov K, Benc D, Draskovic D. Genetic and epigenetic factors in etiology of diabetes mellitus type 1. Pediatrics. 2013;132:1112–1122.
  • Kleinnijenhuis J, Quintin J, Preijers F, et al. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. J Innate Immun. 2014;6:152–158.
  • Sadelain MW, Quin HY, Lauzon J, et al. Prevention of type 1 diabetes in NOD mice by adjuvant immunotherapy. Diabetes. 1990;39:583–589.
  • Shehadeh N, Calcinaro F, Bradley BJ, et al. Effect of adjuvant therapy on development of diabetes in mouse and man. Lancet. 1994;343:706–707. Erratum in: Lancet. 2006;367:1240. Bruchlim, I [corrected to Bruchim, I].
  • Allen HF, Klingensmith GJ, Jensen P, et al. Effect of bacillus Calmette-Guerin vaccination on new-onset type 1 diabetes: a randomized clinical study. Diabetes Care. 1999;22:1703–1707.
  • Khan M, Aydin M. Effect of BCG vaccine in the prevention of type 1 diabetes mellitus. Contemp J Med. 2012;2:1–8.
  • Faustman DL, Wang L, Okubo Y, et al. Proof-of-concept, randomized, controlled clinical trial of bacillus-Calmette-Guerin for treatment of long-term type 1 diabetes. Plos One. 2012;7:e41756.
  • Elliott JF, Marlin KL, Couch RM. Effect of bacille Calmette-Guérin vaccination on C-peptide secretion in children newly diagnosed with IDDM. Diabetes Care. 1998;21:1691–1693.
  • Sanjeevi CB, Das AK, Shtauvere-Brameus A. BCG vaccination and GAD65 and IA-2 autoantibodies in autoimmune diabetes in southern India. Ann N Y Acad Sci. 2002;958:293–296.
  • EURODIAB Substudy 2 Study Group. Infections and vaccinations as risk factors for childhood type I (insulin-dependent) diabetes mellitus: a multicentre case-control investigation. Diabetologia. 2000;43:47–53.
  • Parent ME, Siemiatycki J, Menziez R, et al. Bacille Calmette-Guerin vaccination and incidence of IDDM in Montreal, Canada. Diabetes Care. 1997;20:767–772.
  • Dahlquist G, Gothefors L. The cumulative incidence of childhood diabetes mellitus in Sweden unaffected by BCG-vaccination (Letter). Diabetologia. 1995;38:873–874.
  • Huppmann M, Baumgarten A, Ziegler AG, et al. Neonatal bacille Calmette-Guerin vaccination and type 1 diabetes. Diabetes Care. 2005;28:1204–1206.
  • Rousseau MC, El-Zein M, Conus F, et al. Bacillus Calmette-Guérin (BCG) vaccination in infancy and risk of childhood diabetes. Paediatr Perinat Epidemiol. 2016;30:141–148.
  • Kodama S, Kühtreiber W, Fujimura S, et al. Islet regeneration during the reversal of autoimmune diabetes in NOD mice. Science. 2003;302:1223–1227.
  • Makino S, Kunimoto M, Muraoka Y, et al. Breeding of a non-obese, diabetic strain of mice. Exp Anim. 1980;29:1–13.
  • Yagi H, Matsumoto M, Suzuki S, et al. Possible mechanism of the preventive effect of BCG against diabetes mellitus in NOD mouse. Cell Immunol. 1991;138:130–141.
  • Da Rosa LC, Chiuso-Minicucci F, Zorzella-Pezavento SF, et al. Bacille Calmette-Guerin/DNAhsp65 prime-boost is protective against diabetes in non-obese diabetic mice but not in the streptozotocin model of type 1 diabetes. Clin Exp Immunol. 2013;173:430–437.
  • Huda MN, Lewis Z, Kalanetra KM, et al. Stool microbiota and vaccine responses in infants. Pediatrics. 2014;134:e362–e372.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.