The key role of exudative lesions and their encapsulation: Lessons learned from the pathology of human pulmonary tuberculosis

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Cardona, Pere Joan ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Encapsulation; Exudative lesions; Interlobular septae; Liquefaction; Neutrophils; Proliferative lesions; Reinfection; Tuberculosis

Indexed keywords

CYTOKINE; MYELOPEROXIDASE;

AGE; BACTERIAL LOAD; BCG VACCINATION; CALCIFICATION; DISEASE COURSE; DISEASE MODEL; DISEASE TRANSMISSION; EPITHELIOID CELL; EXUDATIVE LESION; FIBROBLAST; GRANULOCYTE; GRANULOMA; HUMAN; IMMUNE DEFICIENCY; LIQUEFACTION; LUNG ALVEOLUS WALL; LUNG LAVAGE; LUNG LESION; LUNG LOBE; LUNG TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NECROSIS; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PH; REVIEW;

EID: 84936996779     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00612     Document Type: Review

References (80)

1. Adler, H. (1953). Phthisiogenetic considerations based on tomographic analysis of 320 consecutive cases of localized pulmonary tuberculosis in adults. Dis. Chest. 24, 191-204. doi: 10.1378/chest.24.2.191
2. Auerbach, O. (1944). Acute Generalized Miliary Tuberculosis. Am. J. Pathol. 20, 121-136.
3. Basaraba, R., Smith, E., Shanley, C., and Orme, I. (2006). Pulmonary lymphatics are primary sites of Mycobacterium tuberculosis infection in guinea pigs infected by aerosol. Infect. Immun. 74, 5397-5401. doi: 10.1128/IAI.00332-06
4. Berry, M. P., Graham, C. M., McNab, F. W., Xu, Z., Bloch, S. A., Oni, T., et al. (2010). An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466, 973-977. doi: 10.1038/nature09247
5. Bloom, C. I., Graham, C. M., Berry, M. P., Rozakeas, F., Redford, P. S., Wang, Y., et al. (2013). Transcriptional blood signatures distinguish pulmonary tuberculosis, pulmonary sarcoidosis, pneumonias and lung cancers. PLoS ONE 8:e70630. doi: 10.1371/journal.pone.0070630
6. Bru, A., and Cardona, P. (2010). Mathematical modeling of tuberculosis bacillary counts and cellular populations in the organs of infected mice. PLoS ONE 5:e12985. doi: 10.1371/journal.pone.0012985
7. Buddle, B. M., Skinner, M. A., Wedlock, D. N., de Lisle, G. W., Vordermeier, H. M., and Glyn Hewinson, R. (2005). Cattle as a model for development of vaccines against human tuberculosis. Tuberculosis 85, 19-24. doi: 10.1016/j.tube.2004.09.003
8. Byers, T. E., Vena, J. E., and Rzepka, T. F. (1984). Predilection of lung cancer for the upper lobes: an epidemiologic inquiry. J. Natl. Cancer Inst. 72, 1271-1275.
9. Bynum, H. (2012). Spitting Blood. The History of Tuberculosis. Oxford: Oxford University Press.
10. Cáceres, N., Tapia, G., Ojanguren, I., Altare, F., Gil, O., Pinto, S., et al. (2009). Evolution of foamy macrophages in the pulmonary granulomas of experimental tuberculosis models. Tuberculosis 89, 175-182. doi: 10.1016/j.tube.2008.11.001
11. Canetti, G. (1955). The Tubercle Bacillus in the Pulmonary Lesion of Man. Histobacteriology and its Bearing on the Therapy of Pulmonary Tuberculosis. New York, NY: Springer Publishing Company, Inc.
12. Canetti, G. (1950). Exogenous reinfection and pulmonary tuberculosis a study of the pathology. Tubercle 31, 224-33.
13. Cardona, P. J. (2009). A dynamic reinfection hypothesis of latent tuberculosis infection. Infection 37, 80-86. doi: 10.1007/s15010-008-8087-y
14. Cardona, P. J. (2010). Revisiting the natural history of tuberculosis. The inclusion of constant reinfection, host tolerance, and damage-response frameworks leads to a better understanding of latent infection and its evolution towards active disease. Arch. Immunol. Ther. Exp. 58, 7-14. doi: 10.1007/s00005-009-0062-5
15. Cardona, P. J. (2011). A spotlight on liquefaction: evidence from clinical settings and experimental models in tuberculosis. Clin. Dev. Immunol. 2011:868246. doi: 10.1155/2011/868246
16. Cardona, P. J., and Ivanyi, J. (2011). The secret trumps, impelling the pathogenicity of tubercle bacilli. Enferm. Infecc. Microbiol. Clin. 29(Suppl. 1), 14-19. doi: 10.1016/S0213-005X(11)70013-1
17. Cardona, P. J., and Vilaplana, C. (2014). Multiple consecutive infections might explain the lack of protection by BCG. PLoS ONE 9:e94736. doi: 10.1371/journal.pone.0094736
18. Cardona, P. J., Cooper, A., Luquin, M., Ariza, A., Filipo, F., Orme, I. M., et al. (1999). The intravenous model of murine tuberculosis is less pathogenic than the aerogenic model owing to a more rapid induction of systemic immunity. Scand. J. Immunol. 49, 362-366. doi: 10.1046/j.1365-3083.1999.00522.x
19. Cardona, P. J., Gordillo, S., Amat, I., Díaz, J., Lonca, J., Vilaplana, C., et al. (2003a). Catalase-peroxidase activity has no influence on virulence in a murine model of tuberculosis. Tuberculosis 83, 351-359. doi: 10.1016/S1472-9792(03)00056-8
20. Cardona, P. J., Gordillo, S., Díaz, J., Tapia, G., Amat, I., Pallarés, A., et al. (2003b). Widespread bronchogenic dissemination makes DBA/2 mice more susceptible than C57BL/6 mice to experimental aerosol infection with Mycobacterium tuberculosis. Infect. Immun. 71, 5845-5854. doi: 10.1128/IAI.71.10.5845-5854.2003
21. Dannenberg, A. M. J. (2006). Pathogenesis of Human Pulmonary Tuberculosis. Insights from the Rabbit Model. Washington, DC: ASM Press.
22. Dock, W. (1946). Apical localization of phthisis; its significance in treatment by prolonged rest in bed. Am. Rev. Tuberc. 53, 297-305.
23. Dock, W. (1954). Effect of posture in alveolar gas tension in tuberculosis: explanation for favored sites of chronic pulmonary lesions. AMA Arch. Intern. Med. 94, 700-708. doi: 10.1001/archinte.1954.00250050014003
24. Domingo, M., Gil, O., Serrano, E., Guirado, E., Nofrarias, M., Grassa, M., et al. (2009). Effectiveness and safety of a treatment regimen based on isoniazid plus vaccination with Mycobacterium tuberculosis cells' fragments: field-study with naturally Mycobacterium caprae-infected goats. Scand. J. Immunol. 69, 500-507. doi: 10.1111/j.1365-3083.2009.02251.x
25. Driver, E. R., Ryan, G. J., Hoff, D. R., Irwin, S. M., Basaraba, R. J., Kramnik, I., et al. (2012). Evaluation of a mouse model of necrotic granuloma formation using C3HeB/FeJ mice for testing of drugs against Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 56, 3181-3195. doi: 10.1128/AAC.00217-12
26. Dutta, N. K., Illei, P. B., Jain, S. K., and Karakousis, P. C. (2014). Characterization of a novel necrotic granuloma model of latent tuberculosis infection and reactivation in mice. Am. J. Pathol. 184, 2045-2055. doi: 10.1016/j.ajpath.2014.03.008
27. Eum, S. Y., Kong, J. H., Hong, M. S., Lee, Y. J., Kim, J. H., Hwang, S. H., et al. (2010). Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 137, 122-128. doi: 10.1378/chest.09-0903
28. Felson, B. (1952). Acute miliary diseases of the lung. Radiology 59, 32-48. doi: 10.1148/59.1.32
29. Flinn, J. W., and Flinn, R. S. (1930). A bird's-eye view of the histo-pathology of tuberculosis; and its refection in the differential blood count. Trans. Am. Climatol. Clin. Assoc. 46, 204-209.
30. Flynn, J. L., Gideon, H. P., Mattila, J. T., and Lin, P. L. (2015). Immunology studies in non-human primate models of tuberculosis. Immunol. Rev. 264, 60-73. doi: 10.1111/imr.12258
31. Fox, G. J., Barry, S. E., Britton, W. J., and Marks, G. B. (2013). Contact investigation for tuberculosis: a systematic review and meta-analysis. Eur Respir. J. 41, 140-156. doi: 10.1183/09031936.00070812
32. Gadkowski, L. B., and Stout, J. E. (2008). Cavitary pulmonary disease. Clin. Microbiol. Rev. 21, 305-333, doi: 10.1128/CMR.00060-07
33. Gan, H., Lee, J., Ren, F., Chen, M., Kornfeld, H., and Remold, H. (2008). Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat. Immunol. 9, 1189-1197. doi: 10.1038/ni.1654
34. Geng, E., Kreiswirth, B., Burzynski, J., and Schluger, N. W. (2005). Clinical and radiographic correlates of primary and reactivation tuberculosis: a molecular epidemiology study. JAMA 293, 2740-2745. doi: 10.1001/jama.293.22.2740
35. Gil, O., Díaz, I., Vilaplana, C., Tapia, G., Díaz, J., Fort, M., et al. (2010). Granuloma encapsulation is a key factor for containing tuberculosis infection in minipigs. PLoS ONE 5:e10030. doi: 10.1371/journal.pone.0010030
36. Gil, O., Guirado, E., Gordillo, S., Díaz, J., Tapia, G., Vilaplana, C., et al. (2006). Intragranulomatous necrosis in lungs of mice infected by aerosol with Mycobacterium tuberculosis is related to bacterial load rather than to any one cytokine or T cell type. Microbes Infect. 8, 628-636. doi: 10.1016/j.micinf.2005.08.014
37. Glenny, R. W., and Robertson, H. T. (2011). Spatial distribution of ventilation and perfusion: mechanisms and regulation. Compr. Physiol. 1, 375-395. doi: 10.1002/cphy.c100002
38. Guirado, E., Gil, O., Cáceres, N., Singh, M., Vilaplana, C., and Cardona, P. (2008). Induction of a specific strong polyantigenic cellular immune response after short-term chemotherapy controls bacillary reactivation in murine and guinea pig experimental models of tuberculosis. Clin. Vaccine Immunol. 15, 1229-1237. doi: 10.1128/CVI.00094-08
39. Guo, B., Xu, X. G., and Shi, C. (2011). Real time 4D IMRT treatment planning based on a dynamic virtual patient model: proof of concept. Med. Phys. 38, 2639-2650. doi: 10.1118/1.3578927
40. Gurney, J. W., and Schroeder, B. A. (1988). Upper lobe lung disease: physiologic correlates. Rev. Radiol. 167, 359-366. doi: 10.1148/radiology.167.2.3282257
41. Harper, J., Skerry, C., Davis, S. L., Tasneen, R., Weir, M., Kramnik, I., et al. (2012). Mouse model of necrotic tuberculosis granulomas develops hypoxic lesions. J. Infect. Dis. 205, 595-602. doi: 10.1093/infdis/jir786
42. Henningham, A., Dohrmann, S., Nizet, V., and Cole, J. N. (2015). Mechanisms of group A Streptococcus resistance to reactive oxygen species. FEMS Microbiol. Rev. doi: 10.1093/femsre/fuu009. [Epub ahead of print].
43. Hernandez-Pando, R., Jeyanathan, M., Mengistu, G., Aguilar, D., Orozco, H., Harboe, M., et al. (2000). Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet 356, 2133-2138. doi: 10.1016/S0140-6736(00)03493-0
44. Kayne, G. P. W., and O'Shaughnessy, L. (1948). Pulmonary Tuberculosis. Pathology, Diagnosis, Management and Prevention, 2nd Edn. London: Oxford University Press.
45. Khandpur, R., Carmona-Rivera, C., Vivekanandan-Giri, A., Gizinski, A., Yalavarthi, S., Knight, J. S., et al. (2013). NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci. Transl. Med. 5:178ra40. doi: 10.1126/scitranslmed.3005580
46. Laennec, R. T. H. (1826). De l'Auscultation Médiate ou Traité du Diagnostic des Maladies des Poumons et du Coeur, 2nd Edn. Paris: Brosson & Chaude.
47. Lee, J., Remold, H., Ieong, M., and Kornfeld, H. (2006). Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway. J. Immunol. 176, 4267-4274. doi: 10.4049/jimmunol.176.7.4267
48. Lindgren, I. (1961). Anatomical and roentgenologic studies of tuberculous infections in BCG-vaccinated and non-vaccinated subjects with biophysical investigations of calcified foci. Acta Radiol. Suppl. 209, 1-101. doi: 10.3109/00016926109173811
49. Lowe, D. M., Redford, P. S., Wilkinson, R. J., O'Garra, A., and Martineau, A. R. (2012). Neutrophils in tuberculosis: friend or foe? Trends Immunol. 33, 14-25. doi: 10.1016/j.it.2011.10.003
50. Marzo, E., Vilaplana, C., Tapia, G., Diaz, J., Garcia, V., and Cardona, P. J. (2014). Damaging role of neutrophilic infiltration in a mouse model of progressive tuberculosis. Tuberculosis 94, 55-64. doi: 10.1016/j.tube.2013.09.004
51. Medlar, E. M. (1947a). Primary and reinfection tuberculosis as the cause of death in adults; an analysis of 100 consecutive necropsies. Am. Rev. Tuberc. 55, 517-528.
52. Medlar, E. M. (1947b). Incidence of tuberculous pulmonary cavities in unexpected deaths investigated at necropsy. Arch. Intern. Med. (Chic.) 80, 403-410.
53. Medlar, E. M. (1947c). The incidence of pathologically significant tuberculosis in routine necropsies in private and public general hospitals. N.Y. State J. Med. 47, 582-587.
54. Medlar, E. M. (1947d). Apical scars; their etiological relationship to tuberculous infection. Am. Rev. Tuberc. 55, 511-516.
55. Medlar, E. M. (1948). The pathogenesis of minimal pulmonary tuberculosis; a study of 1,225 necropsies in cases of sudden and unexpected death. Am. Rev. Tuberc. 58, 583-611.
56. Medlar, E. M. (1955). The behavior of pulmonary tuberculous lesions. A pathological study. Am. Rev. Tuberc. 71(Suppl. 1), 1-244.
57. Mestas, J., and Hughes, C. C. (2004). Of mice and not men: differences between mouse and human immunology. J. Immunol. 172, 2731-2738. doi: 10.4049/jimmunol.172.5.2731
58. Meunier, H. (1898). Bacilloscopie des crachats extraits de l'estomac pour le diagnostic de la tuberculose pulmonaire de l'enfant. Presse Med. 2, 81.
59. Nemec, S. F., Bankier, A. A., and Eisenberg, R. L. (2013). Upper lobe-predominant diseases of the lung. AJR Am. J. Roentgenol. 200, W222-W237. doi: 10.2214/AJR.12.9253
60. Opie, E. L., and Aronson, J. D. (1927). Tubercle bacilli in latent tuberculous lesions and in lung tissue without tuberculous lesions. Arch. Pathol. Lab. Med. 4, 460-461.
61. Ordway, D., Palanisamy, G., Henao-Tamayo, M., Smith, E. E., Shanley, C., Orme, I. M., et al. (2007). The cellular immune response to Mycobacterium tuberculosis infection in the guinea pig. J. Immunol. 179, 2532-2541. doi: 10.4049/jimmunol.179.4.2532
62. Osborne, D. R., Effmann, E. L., and Hedlund, L. W. (1983). Postnatal growth and size of the pulmonary acinus and secondary lobule in man. AJR Am. J. Roentgenol. 140, 449-454. doi: 10.2214/ajr.140.3.449
63. Pagel, W., and Toussaint, C. H. (1948). Pathology of reinfection; some sources of diagnostic errors. Am. Rev. Tuberc. 58, 85-97.
64. Parent, R. A. (2015). Comparative Biology of the Normal Lung, 2nd Edn. San Diego, CA: Academic Press.
65. Plopper, C. G., and Harkema, J. R. (2005). "The respiratory system and its use in research," in The Laboratory Primate, ed S. Wolfe-Coote (San Diego, CA: Elsevier B.V. Academic Press), 503-526. doi: 10.1016/B978-012080261-6/50030-1
66. Poppius, H., and Thomander, K. (1957). Segmentary distribution of cavities; a radiologic study of 500 consecutive cases of cavernous pulmonary tuberculosis. Ann. Med. Intern. Fenn. 46, 113-119.
67. Pottenger, F. M. (1934). Tuberculosis in the Child and the Adult. St. Louis, MO: The C.V. Mosby Company.
68. Redford, P. S., Boonstra, A., Read, S., Pitt, J., Graham, C., Stavropoulos, E., et al. (2010). Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur. J. Immunol. 40, 2200-2210. doi: 10.1002/eji.201040433
69. Rich, A. R. (1944). The Pathogenesis of Tuberculosis. Springfield, IL: Charles C Thomas.
70. Ryu, J. H., and Swensen, S. J. (2003). Cystic and cavitary lung diseases: focal and diffuse. Mayo Clin. Proc. 78, 744-752. doi: 10.4065/78.6.744
71. Stadnichenko, A., Cohen, S., and Sweany, H. C. (1940). Stomach lavage in the diagnosis and control of treatment of tuberculosis. JAMA 114, 634-639. doi: 10.1001/jama.1940.02810080006002
72. Stead, W. W. (1967). Pathogenesis of a first episode of chronic pulmonary tuberculosis in man: recrudescence of residuals of the primary infection or exogenous reinfection? Am. Rev. Respir. Dis. 95, 729-745.
73. Suki, B., Sato, S., Parameswaran, H., Szabari, M. V., Takahashi, A., and Bartolak-Suki, E. (2013). Emphysema and mechanical stress-induced lung remodeling. Physiology 28, 404-413. doi: 10.1152/physiol.00041.2013
74. Sutherland, I., and Lindgren, I. (1979). The protective effect of BCG vaccination as indicated by autopsy studies. Tubercle 60, 225-231. doi: 10.1016/0041-3879(79)90003-5
75. Vilaplana, C., and Cardona, P. J. (2014). The lack of a big picture in tuberculosis: the clinical point of view, the problems of experimental modeling and immunomodulation. The factors we should consider when designing novel treatment strategies. Front. Microbiol. 5:55. doi: 10.3389/fmicb.2014.00055
76. Vilaplana, C., Marzo, E., Tapia, G., Diaz, J., Garcia, V., and Cardona, P. J. (2013). Ibuprofen therapy resulted in significantly decreased tissue bacillary loads and increased survival in a new murine experimental model of active tuberculosis. J. Infect. Dis. 208, 199-202. doi: 10.1093/infdis/jit152
77. Wallgren, A. (1948). The time-table of tuberculosis. Tubercle 29, 245-251. doi: 10.1016/S0041-3879(48)80033-4
78. Wang, C. Y. (1916). An experimental study of latent tuberculosis. Lancet 2, 417-419. doi: 10.1016/S0140-6736(00)58936-3
79. Webb, W. R. (2006). Thin-section CT of the secondary pulmonary lobule: anatomy and the image-the 2004 Fleischner lecture. Radiology 239, 322-338. doi: 10.1148/radiol.2392041968
80. Yanar, M., Abel, F., Haalck, T., Klutmann, S., and Schumacher, U. (2014). The microenvironment in the human lung partly determines the site of the first metastasis. Anticancer Res. 34, 3845-3849.