Preview

Tuberculosis and Lung Diseases

Advanced search

100 Years of Vaccination against Tuberculosis – Lessons Learnt and Prospects

https://doi.org/10.58838/2075-1230-2024-102-2-6-19

Abstract

The article presents a literature review dedicated to the 100th anniversary of introduction of the BCG vaccine against tuberculosis; it analyzes of 83 publications by Russian and foreign authors. The results of the BCG vaccination used in various clinical studies and real clinical practice are assessed. The article presents data on development of new candidate vaccines and mechanisms of their effect on various parts of the immune system. Candidate vaccines are of particular interest, these candidate vaccines are used not only for prevention before infants are exposed to the infection for the first time, but also for therapy, the vaccines are aimed at therapeutic action against tuberculosis and latent tuberculosis infection.

About the Authors

E. M. Bogorodskaya
Moscow Research and Clinical Center for Tuberculosis Control of the Moscow Government Department of Health; Russian Medical Academy of On-going Professional Education, Russian Ministry of Health
Russian Federation

Elena M. Bogorodskaya, Doctor of Medical Sciences, Professor, Director, Head of Phthisiology Department

10 Stromynka St., Moscow, 107014

Phone: + 7 (499) 268-00-05



D. A. Kudlay
I.M. Sechenov First Moscow State Medical University (Sechenov University), Russian Ministry of Health; Lomonosov Moscow State University; Immunology Research Institute by the Russian Federal Medical Biological Agency
Russian Federation

Dmitry A. Kudlay, Correspondent Member of RAS, Doctor of Medical Sciences, Professor of Pharmacology Department of Pharmacy Institute, Professor of Department of Pharmacognosy and Industrial Pharmacy, Faculty of Fundamental Medicine; Leading Researcher of Laboratory of Personalized Medicine and Molecular Immunology

8 Bd. 2, Trubetskaya St., Russia Moscow, 119991

Phone: +7 (499) 248-05-53



L. V. Slogotskaya
Moscow Research and Clinical Center for Tuberculosis Control of the Moscow Government Department of Health; Russian Medical Academy of On-going Professional Education, Russian Ministry of Health
Russian Federation

Ludmila V. Slogotskaya, Doctor of Medical Sciences, Head of Research Clinical Department, Professor of Phthisiology Department

10 Stromynka St., Moscow, 107014

Phone: + 7 (499) 268-00-05



References

1. Averbakh A.A., Litvinov V.I. Immunologicheskie osnovy protivotuberkuleznoy vaktsinatsii. [Immunological basics of anti-tuberculosis vaccination]. Moscow, Meditsina Publ., 1970, 222 p.

2. Weisfeller Yu.K. The mechanism of immunity and allergies in case of tuberculosis. Problemy Tuberkuleza, 1946, no. 2, pp. 3-15. (In Russ.)

3. Lyubarsky V.A. On the issue of anti-tuberculosis vaccination. Voprosy Tuberkuleza, 1926, vol. 4, no. 3, pp. 14-15. (In Russ.)

4. Togunova A.I., Zhulina L.V., Khatenever M.L. About antigens and crude extracts of Mycobacterium tuberculosis. Problemy Tuberkuleza, 1962, no. 4, pp. 71-76. (In Russ.)

5. Togunova A.I. On the biology of the BCG strain. Borba s Tuberkulezom, 1932, no. 7, pp. 591-599. (In Russ.)

6. Togunova A.I. Materials for studying the BCG strain. Voprosy Tuberkuleza, no. 1926, vol. 4, no, 3, pp. 1–13. (In Russ.)

7. Togunova A.I., Khatenever M.L. Immunobiological properties of some so-called atypical mycobacteria. Problemy Tuberkuleza, 1965, no. 3, pp. 56-60. (In Russ.)

8. Abubakar I., Pimpin L., Ariti C., Beynon R., Mangtani P., Sterne J.A. Systematic review and metaanalysis of the current evidence on the duration of protection by bacillus Calmette-Guerin vaccination against tuberculosis. Health Technol. Assess., 2013, vol. 17, no. 37, pp. 1-372. https://doi.org/10.3310/hta17370

9. Andersen P., Scriba T.J. Moving tuberculosis vaccines from theory to practice. Nature Reviews, 2019, no. 19, pp. 550-562.

10. Arregui S., Sanz J., Marinova D., Martín C., Moreno Y. On the impact of masking and blocking hypotheses for measuring the efficacy of new tuberculosis vaccines. Peer J., 2016, no. 4, pp. e1513.

11. Barreto M.L., Pilger D., Pereira S.M., Genser B., Cruz A.A., Cunha S.S. Causes of variation in BCG vaccine efficacy: examining evidence from the BCG REVAC cluster randomized trial to explore the masking and the blocking hypotheses. Vaccine, 2014, vol. 32, no. 30, pp. 3759-3764. https://doi.org/10.1016/j.vaccine.2014.05.042

12. Bellini С., Horváti K. Recent Advances in the development of protein- and peptide-based subunit vaccines against tuberculosis. Cells, 2020, vol. 9, no. 12, pp. 2673. https://doi.org/10.3390/cells9122673

13. Bettencourt P., Müller J., Nicastri A., Cantillon D., Madhavan M., Charles P.D. et al. Identification of antigens presented by MHC for vaccines against tuberculosis. NPJ Vaccines, 2020, vol. 5, no. 1, pp. 2. https://doi.org/10.1038/s41541-019-0148-y

14. Bhatt K., Verma S., Ellner J.J., Salgame P. Quest for correlates of protection against tuberculosis. Clin. Vaccine Immunol., 2015, no. 22, pp. 258-266.

15. Brazier B., McShane H. Towards new TB vaccines. Semin. Immunopathol., 2020, no. 42, pp. 315-331. https://doi.org/10.1007/s00281-020-00794-0

16. Brennan M.J. The enigmatic PE/PPE multigene family of mycobacteria and tuberculosis vaccination. Infect. Immun., 2017, no. 85, pp. e00969-е01016. https://doi.org/10.1128/IAI.00969-16

17. Broset E., Saubi N., Guitart N., Aguilo N., Uranga S., Kilpeläinen A. et al. MTBVAC-Based TB-HIV vaccine is safe, elicits HIV-T cell responses, and protects against Mycobacterium tuberculosis in mice. Mol. Ther. Methods Clin. Dev., 2019, no. 13, pp. 253-264.

18. Cardona P.J. The progress of therapeutic vaccination with regard to tuberculosis. Front. Microbiol., 2016, no. 7, pp. 1536.

19. Chesson C.B., Huante M., Nusbaum R.J., Walker A.G., Clover T.M., Chinnaswamy J., Endsley J.J., Rudra J.S. Nanoscale peptide self-assemblies boost BCG-primed cellular immunity against Mycobacterium tuberculosis. Sci. Rep., 2018, no. 8, pp. 12519. https://doi.org/10.1038/s41598-018-31089-y

20. Darrah P.A., Zeppa J.J., Maiello P., Hackney J.A., Wadsworth M.H., Hughes T.K. et al. Prevention of tuberculosis in macaques after intravenous BCG immunization. Nature, 2020, no. 577, pp. 95-102.

21. de Martino M., Lodi L., Galli L., Chiappini E. Immune response to Mycobacterium tuberculosis: a narrative review. Front. Pediatr., 2019, no. 7, pp. 350. https://doi.org/10.3389/fped.2019.00350

22. Delogu G., Provvedi R., Sali M., Manganelli R. Mycobacterium tuberculosis virulence: insights and impact on vaccine development. Future Microbiol., 2015, no. 10, pp. 1177-1194. https://doi.org/10.2217/fmb.15.26

23. Dijkman K., Sombroek C.C., Vervenne R.A.W., Hofman S.O., Boot C., Remarque E.J. et al. Prevention of tuberculosis infection and disease by local BCG in repeatedly exposed rhesus macaques. Nature Med., 2019, no. 25, pp. 255-262.

24. Drain P.K., Bajema K.L., Dowdy D., Dheda K., Naidoo K., Schumacher S.G. et al. Incipient and subclinical tuberculosis: a clinical review of early stages and progression of infection. Clin. Microbiol. Rev., 2018, no. 31, pp. e00021-е00018. https://doi.org/10.1128/CMR.00021-18

25. Fatima S., Kumari A., Das G., Dwivedi V.P. Tuberculosis vaccine: a journey from BCG to present. Life Sci., 2020, no. 252, pp. 117594.

26. Fekrvand S., Yazdani R., Olbrich P., Gennery A., Rosenzweig S.D., Condino-Neto A. et al. Primary immunodeficiency diseases and Bacillus Calmette-Guérin (BCG)-vaccine-derived complications: a systematic review. J. Allergy Clin. Immunol. Pract., 2020, no. 8, pp. 1371-1386.

27. Fine P.E. Variation in protection by BCG: implications of and for heterologous immunity. Lancet, 1995, no. 346, pp. 1339-1345.

28. Geckin B., Konstantin Föhse F., Domínguez-Andrés J., Netea M.G. Trained immunity: Implications for vaccination. Curr. Opin. Immunol., 2022, no. 77, pp. 102190.

29. Gong W., Liang Y., Wu X. The current status, challenges, and future developments of new tuberculosis vaccines. Hum. Vaccines Immunother., 2018, no. 14, pp. 1697-1716.

30. Gupta N., Garg S., Vedi S., Kunimoto D.Y., Kumar R., Agrawal B. Future path toward TB vaccine development: boosting BCG or re-educating by a new subunit vaccine. Front. Immunol., 2018, no. 9, pp. 2371.

31. Gupta N., Vedi S., Kunimoto D.Y., Agrawal B., Kumar R. Novel lipopeptides of ESAT-6 induce strong protective immunity against Mycobacterium tuberculosis: routes of immunization and TLR agonists critically impact vaccine’s efficacy. Vaccine, 2016, no. 34, pp. 5677-5688.

32. Heimbeck J. Incidence of tuberculosis in young adult women with special reference to employment. Br. J. Tuberculosis, 1938, no. 32, pp. 154-166.

33. Heimbeck J. Tuberculosis in hospital nurses. Tubercle Br. J. Tuberculosis, 1936, no. 18, pp. 97-99.

34. Hoft D.F., Xia M., Zhang G.L., Blazevic A., Tennant J., Kaplan C. et al. PO and ID BCG vaccination in humans induce distinct mucosal and systemic immune responses and CD4+ T cell transcriptomal molecular signatures. Mucosal Immunol., 2018, no. 11, pp. 486-495.

35. Hunter R., Actor J. The pathogenesis of post-primary tuberculosis. A game for vaccine development. Tuberculosis, 2019, no. 116S, pp. 114-117. https://doi.org/10.1016/j.tube.2019.04.018

36. Jeyanathan M., McCormick S., Lai R., Afkhami S., Shaler C.R., Horvath C.N. et al. Pulmonary M. tuberculosis infection delays Th1 immunity via immunoadaptor DAP12-regulated IRAK-M and IL-10 expression in antigenpresenting cells. Mucosal Immunol., 2014, no. 7, pp. 670-683. https://doi.org/10.1038/mi.2013.86

37. Jeyanathan M., Yao Y., Afkhami S., Smaill F., Xing Z. New tuberculosis vaccine strategies: taking aim at un-natural immunity. Trends Immunol., 2018, no. 39, pp. 419-433. https://doi.org/10.1016/j.it.2018.01.006

38. Kanno A.I., Boraschi D., Leite L.C.C., Rodriguez D. Recombinant BCG expressing the subunit 1 of pertussis toxin induces innate immune memory and confers protection against non-related pathogens. Vaccines, 2022, no. 10, pp. 234. https://doi.org/10.3390/vaccines10020234

39. Kaufmann S.H.E., Winau F. From bacteriology to immunology—the dualism of specificity. Nat. Immunol., 2005, no. 6, pp. 1063-1066.

40. Kilpeläinen A., Saubi N., Guitart N., Olvera A., Hanke T., Brander C., Joseph J. Recombinant BCG expressing HTI prime and recombinant ChAdOx1 boost is safe and elicits HIV-1-tpecific T-cell responses in BALB/c mice. Vaccines, 2019, no. 7, pp. 8.

41. Lahariya C. A brief history of vaccines & vaccination in India. Indian J. Med. Res., 2014, no. 139, pp. 491-511.

42. Lewinsohn D.A., Lewinsohn D.M., Scriba T.J. Polyfunctional CD4+ T cells as targets for tuberculosis vaccination. Front. Immunol., 2017, no. 8, pp. 1262. https://doi.org/10.3389/fimmu.2017.01262

43. Mangtani P., Abubakar I., Ariti C., Beynon R., Pimpin L., Fine P.E.M. et al. Protection by BCG vaccine against tuberculosis: a systematic review of randomized controlled trials. Nephrol. Dial. Transplant., 2014, no. 58, pp. 470-480.

44. Mazzola T.N., da Silva M.T., Abramczuk B.M., Moreno Y.M., Lima S.C., Zorzeto T.Q. et al. Impaired Bacillus Calmette-Guérin cellular immune response in HIV-exposed, uninfected infants. AIDS, 2011, no. 25, pp. 2079-2087.

45. Moguche A.O., Musvosvi M., Penn-Nicholson A., Plumlee C.R., Mearns H., Geldenhuys H. et al. Antigen availability shapes T cell differentiation and function during tuberculosis. Cell Host Microbe, 2017, no. 21, pp. 695-706.

46. Mustafa A.S. BCG pros and cons and new/improved vaccines for tuberculosis. In Text Book of Biochemistry, Biotechnology, Allied and Molecular Medicine. Talwar G.P., Hasnain S.E., Sarin S.K., Hasnain S., еds., PHI Learning Private Limited, India, 2016, no. 117, pp. 1347-1353.

47. Mustafa A.S. In silico analysis and experimental validation of Mycobacterium tuberculosis-specific proteins and peptides of Mycobacterium tuberculosis for immunological diagnosis and vaccine development. Med. Princ. Pract., 2013, no. 22, pp. 43-51.

48. Mustafa A.S. Plasmid DNA and mycobacteria as antigen delivery systems for Mycobacterium tuberculosis-specific antigens. (In Chapter in Molecular Medicine: Bench to Bedside and Beyond; Gupta S.K., Lohiya N.K., еds.). Indian Society for the Study of Reproduction and Fertility, University of Rajasthan, India, 2018, pp. 244-252.

49. Ndiaye B.P., Thienemann F., Ota M., Landry B.S., Camara M., Dièye S. et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet, 2015, no. 3, pp. 190-200.

50. Nemes E.H. Geldenhuys, Rozot V., Rutkowski K.T., Ratangee F. Bilek N. et al. Prevention of M. tuberculosis infection with H4:IC31 vaccine or BCG revaccination. N. Engl. J. Med., 2018, pp. 379, pp. 138-149. https://doi.org/10.1056/NEJMoa1714021

51. Nguipdop-Djomo P., Heldal E., Rodrigues L.C., Abubakar I. & Mangtani P. Duration of BCG protection against tuberculosis and change in effectiveness with time since vaccination in Norway: a retrospective population-based cohort study. Lancet Infect. Dis., 2016, no. 16, pp. 219-226.

52. Nieuwenhuizen N.E., Kulkarni P.S., Shaligram U., Cotton M.F., Rentsch C.A., Eisele B., Grode L., Kaufmann S.H.E. The recombinant Bacille Calmette-Guérin vaccine VPM1002: ready for clinical efficacy testing. Front Immunol., 2017, no. 8, pp. 1147.

53. Pennisi M., Russo G., Sgroi G., Bonaccorso A., Parasiliti Palumbo G.A., Fichera E. et al. Predicting the artificial immunity induced by RUTI® vaccine against tuberculosis using universal immune system simulator (UISS). BMC Bioinform., 2019, no. 20, pp. 504.

54. Pereira V.B., da Cunha V.P., Preisser T.M., Souza B.M., Turk M.Z., De Castro C.P. et al. Lactococcus lactis carrying a DNA vaccine coding for the ESAT-6 antigen increases IL-17 cytokine secretion and boosts the BCG vaccine immune response. J. Appl. Microbiol., 2017, no. 122, pp. 1657-1662.

55. Pérez I., Uranga S., Sayes F., Frigui W., Samper S., Arbués A. et al. Live attenuated TB vaccines representing the three modern Mycobacterium tuberculosis lineages reveal that the Euro-American genetic background confers optimal vaccine potential. EBioMedicine, 2020, no. 55, pp. 102761.

56. Pipeline of Vaccines. Available: https://www.tbvi.eu/what-we-do/pipeline-of-vaccines/ Accessed August 16, 2022

57. Platteel A.C.M., Nieuwenhuizen N.E., Domaszewska T., Schürer S., Zedler U., Brinkmann V., Sijts A., Kaufmann S.H.E. Efficacy Testing of H56 cDNA tattoo immunization against tuberculosis in a mouse model. Front. Immunol., 2017, no. 8, pp. 1744.

58. Portal-Celhay C., Tufariello J., Srivastava S., Zahra A., Klevorn T., Grace P.S. et al. Mycobacterium tuberculosis EsxH inhibits ESCRT-dependent CD4+ T cell activation. Nat. Microbiol., 2016, no. 2, pp. 16232.

59. Pym A.S., Brodin P., Majlessi L., Brosch R., Demangel C., Williams A., Griffiths K.E., Marchal G., Leclerc C., Cole S.T. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nature Med., 2003, no. 9, pp. 533-539.

60. Ragonnet R., Trauer J.M., Geard N., Scott N., McBryde E.S. Profiling Mycobacterium tuberculosis transmission and the resulting disease burden in the five highest tuberculosis burden countries. BMC Med., 2019, no. 17, pp. 208.

61. Recombinant Vaccine. 2020. Available: https://www.nature.com/subjects/recombinant-vaccine Accessed July 01, 2022

62. Rentsch C.A., Thalmann G.N., Lucca I., Kwiatkowski M., Wirth G.J., Strebel R.T. et al. A phase 1/2 single-arm clinical trial of recombinant Bacillus Calmette-Guérin (BCG)VPM1002BC immunotherapy in non–muscle-invasive bladder cancer recurrence after conventional BCG therapy: SAKK 06/14. Eur. Urol. Oncol., 2022, no. 5, pp. 195-202. https://doi.org/10.1016/j.euo.2021.12.006

63. Reyn C.F.V. BCG, latitude, and environmental mycobacteria. Clin. Infect. Dis., vol. 59, no. 4, 2014, pp. 607-608.

64. Roy P., Vekemans J., Clark A., Sanderson C., Harris R.C., White R.G. Potential effect of age of BCG vaccination on global paediatric tuberculosis mortality: a modelling study. Lancet Glob. Health, 2019, no. 7, pp. e1655-e1663.

65. Safar H.A., Mustafa A.S., Amoudy H.A., El-Hashim A. The effect of adjuvants and delivery systems on Th1, Th2, Th17 and Treg cytokine responses in mice immunized with Mycobacterium tuberculosis-specific proteins. PLoS ONE, 2020, no. 15, pp. e0228381.

66. Schrager L.K., Harris R.C., Vekemans J. Research and development of new tuberculosis vaccines: A review. F1000 Research, 2019, no. 7, pp. 1732. https://doi.org/10.12688/f1000research.16521.2

67. Schrager L.K., Vekemens J., Drager N., Lewinsohn D.M., Olesen O.F. The status of tuberculosis vaccine development. Lancet Infect., 2020, no. 20, pp. e28-e37. https://doi.org/10.1016/S1473-3099(19)30625-5

68. Stockdale L., Fletcher H. The future of vaccines for tuberculosis. Clin. Chest Med., 2019, no. 40, pp. 849-856.

69. Suliman S., Luabeya A., Geldenhuys H., Tameris M., Hoff S. T., Shi Z. et al. Dose optimization of H56:IC31 vaccine for TB endemic populations: a double-blind, placebo-controlled, dose-selection trial. Am. J. Respir. Crit. Care Med., 2018, no. 199, pp. 220-231.

70. Tagliabue A., Boraschi D., Leite L.C.C., Kaufmann S.H.E. 100 years of BCG immunization: past, present and future. Vaccines, 2022, no. 10, pp. 1743. https://doi.org/10.3390/vaccines10101743

71. Tait D.R., Hatherill M., Van Der Meeren O., Ginsberg A.M., Van Brakel E., Salaun B. et al. Final analysis of a trial of M72/AS01 vaccine to prevent tuberculosis. N. Engl. J. Med., 2019, no. 381, pp. 2429-2439.

72. Tameris M.D., Hatherill M., Landry B.S., Scriba T.J., Snowden M.A., Lockhart S. et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: A randomised, placebo-controlled phase 2b trial. Lancet, 2013, no. 81, pp. 1021-1028. https://doi.org/10.1016/S0140-6736(13)60177-4

73. Thakur A., Pinto F.E., Hansen H.S., Andersen P., Christensen D., Janfelt C., Foged C. Intrapulmonary (i. pulmon.) pull immunization with the tuberculosis subunit vaccine candidate h56/caf01 after intramuscular (i. m.) priming elicits a distinct innate myeloid response and activation of antigen-presenting cells than i. m. or i. pulmon. Prime Immunization Alone. Front. Immunol., 2020, no. 11, pp. 803.

74. Tkachuk A.P., Bykonia E.N., Popova L.I., Kleymenov D.A, Semashko M.A., Chulanov V.P. et al. Safety and Immunogenicity of the GamTBvac, the recombinant subunit tuberculosis vaccine candidate: a phase ii, multi-center, double-blind, randomized, placebo-controlled study. Vaccines, 2020, vol. 8, no. 4, pp. 652. https://doi.org/10.3390/vaccines8040652

75. Vasina D.V., Kleymenov D.A., Manuylov V.A., Mazunina E.P., Koptev E.Y., Tukhovskaya E.A. et al. First-in-human trials of GamTBvac, a recombinant subunit tuberculosis vaccine candidate: safety and immunogenicity assessment. Vaccines (Basel), 2019, vol. 7, no. 4, pp. 166. https://doi.org/10.3390/vaccines7040166

76. Vetter V., Denizer G., Friedland L.R., Krishnan J., Shapiro M. Understanding modern-day vaccines: what you need to know. Ann. Med., 2018, no. 50, pp. 110-120.

77. Wang C., Lu J., Du W., Wang G., Li X., Shen X., Su C., Yang L., Chen B., Wang J. et al. Ag85b/ESAT6-CFP10 adjuvanted with aluminum/poly-IC effectively protects guinea pigs from latent Mycobacterium tuberculosis infection. Vaccine, 2019, no. 37, pp. 4477-4484.

78. Whitlow E., Mustafa A.S. , Hanif S.N.M. An overview of the development of new vaccines for tuberculosis. Vaccines, 2020, vol. 8, no. 4, pp. 586.

79. Woodworth J.S., Andersen P. Reprogramming the T cell response to tuberculosis. Trends Immunol., 2016, no. 37, pp. 81-83.

80. Yadav J., Verma S., Chaudhary D., Jaiwal P. K., Jaiwal R. Tuberculosis: current status, diagnosis, treatment and development of novel vaccines. Curr. Pharm. Biotechnol., 2019, no. 20, pp. 446-458.

81. Yan Y.H., Li M.C., Liu H.C., Xiao T.Y., Li N., Lou Y.L., Wan K.L. Cellular immunity evaluation of five Mycobacterium tuberculosis recombinant proteins and their compositions. Zhonghua Yu Fang Yi Xue Za Zhi, 2020, no. 54, pp. 539-545. https://doi.org/10.3760/cma.j.cn112150-20191119-00872

82. Zhang L. Multi-epitope vaccines: A promising strategy against tumors and viral infections. Cell. Mol. Immunol., 2018, no. 15, pp. 182-184. https://doi.org/10.1038/cmi.2017.92

83. Zhu B., Dockrell H.M., Ottenhoff T.H.M., Evans T.G., Zhang Y. Tuberculosis vaccines: Opportunities and challenges. Respirology, 2018, no. 23, pp. 359-368.


Review

For citations:


Bogorodskaya E.M., Kudlay D.A., Slogotskaya L.V. 100 Years of Vaccination against Tuberculosis – Lessons Learnt and Prospects. Tuberculosis and Lung Diseases. 2024;102(2):6-19. (In Russ.) https://doi.org/10.58838/2075-1230-2024-102-2-6-19

Views: 822


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2075-1230 (Print)
ISSN 2542-1506 (Online)