Associations between systemic inflammation, mycobacterial loads in sputum and radiological improvement after treatment initiation in pulmonary TB patients from Brazil: A prospective cohort study

BMC Infectious Diseases

Volumn 16, Issue 1, 2016, Pages

  Mesquita, Eliene D D ^a   Gil Santana, Leonardo ^b,c,d   Ramalho, Daniela ^e   Tonomura, Elise ^e   Silva, Elisangela C ^e,f   Oliveira, Martha M ^b   Andrade, Bruno B ^b,c,d   Kritski, Afrânio ^e  

^a Ary Parreiras Institute Rio de Janeiro State Secretary of Health   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Sponsoring Translational and Epidemiological Research (MONSTER) Initiative   (Brazil)

^d Faculdade de Tecnologia e Ciencias   (Brazil)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^f STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Acid fast bacilli; Anti tuberculous treatment; Biomarker; C reactive protein; Erythrocyte sedimentation rate; Inflammation; Radiographic evaluation; Tuberculosis

Indexed keywords

C REACTIVE PROTEIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; TUBERCULOSTATIC AGENT; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; TUMOR NECROSIS FACTOR;

ADULT; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; BRAZILIAN; COHORT ANALYSIS; CONTROLLED STUDY; ERYTHROCYTE SEDIMENTATION RATE; EXPLORATORY RESEARCH; FEMALE; HUMAN; INFLAMMATION; LUNG CAVITATION; LUNG TUBERCULOSIS; MAJOR CLINICAL STUDY; MALE; PROSPECTIVE STUDY; SPUTUM CULTURE; SPUTUM SMEAR; THORAX RADIOGRAPHY; BLOOD; BRAZIL; CASE CONTROL STUDY; COMPLICATION; IMMUNOLOGY; ISOLATION AND PURIFICATION; LONGITUDINAL STUDY; MICROBIOLOGY; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; SPUTUM; TUBERCULOSIS, PULMONARY;

ADULT; BACTERIAL LOAD; BRAZIL; C-REACTIVE PROTEIN; CASE-CONTROL STUDIES; COHORT STUDIES; CYTOKINES; FEMALE; HUMANS; INFLAMMATION; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; RADIOGRAPHY, THORACIC; SPUTUM; TUBERCULOSIS, PULMONARY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84982863844     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/s12879-016-1736-3     Document Type: Article

References (60)

1. Tiemersma EW, van der Werf MJ, Borgdorff MW, Williams BG, Nagelkerke NJ. Natural history of tuberculosis: duration and fatality of untreated pulmonary tuberculosis in HIV negative patients: a systematic review. PLoS One. 2011;6(4):e17601.
2. Cliff JM, Kaufmann SH, McShane H, van Helden P, O'Garra A. The human immune response to tuberculosis and its treatment: a view from the blood. Immunol Rev. 2015;264(1):88-102.
3. Jenum S, Dhanasekaran S, Lodha R, Mukherjee A, Kumar Saini D, Singh S, Singh V, Medigeshi G, Haks MC, Ottenhoff TH, et al. Approaching a diagnostic point-of-care test for pediatric tuberculosis through evaluation of immune biomarkers across the clinical disease spectrum. Sci Rep. 2016;6:18520.
4. Dorhoi A, Kaufmann SH. Pathology and immune reactivity: understanding multidimensionality in pulmonary tuberculosis. Semin Immunopathol. 2016;38(2):153-66.
5. Kassa D, de Jager W, Gebremichael G, Alemayehu Y, Ran L, Fransen J, Wolday D, Messele T, Tegbaru B, Ottenhoff TH, et al. The effect of HIV coinfection, HAART and TB treatment on cytokine/chemokine responses to Mycobacterium tuberculosis (Mtb) antigens in active TB patients and latently Mtb infected individuals. Tuberculosis (Edinb). 2016;96:131-40.
6. Lorenzetti R, Zullo A, Ridola L, Diamanti AP, Lagana B, Gatta L, Migliore A, Armuzzi A, Hassan C, Bruzzese V. Higher risk of tuberculosis reactivation when anti-TNF is combined with immunosuppressive agents: a systematic review of randomized controlled trials. Ann Med. 2014;46(7):547-54.
7. Denkinger CM, Kalantri Y, Schumacher SG, Michael JS, Shankar D, Saxena A, Sriram N, Balamugesh T, Luo R, Pollock NR, et al. Challenges in the development of an immunochromatographic interferon-gamma test for diagnosis of pleural tuberculosis. PLoS One. 2013;8(12):e85447.
8. Wallis RS, Kim P, Cole S, Hanna D, Andrade BB, Maeurer M, Schito M, Zumla A. Tuberculosis biomarkers discovery: developments, needs, and challenges. Lancet Infect Dis. 2013;13(4):362-72.
9. Andrade BB, Pavan Kumar N, Amaral EP, Riteau N, Mayer-Barber KD, Tosh KW, Maier N, Conceicao EL, Kubler A, Sridhar R, et al. Heme Oxygenase-1 Regulation of Matrix Metalloproteinase-1 Expression Underlies Distinct Disease Profiles in Tuberculosis. J Immunol. 2015;195(6):2763-73.
10. Mayer-Barber KD, Andrade BB, Oland SD, Amaral EP, Barber DL, Gonzales J, Derrick SC, Shi R, Kumar NP, Wei W, et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature. 2014;511(7507):99-103.
11. de Steenwinkel JE, de Knegt GJ, ten Kate MT, Verbrugh HA, Hernandez-Pando R, Leenen PJ, Bakker-Woudenberg IA. Relapse of tuberculosis versus primary tuberculosis; course, pathogenesis and therapy in mice. Tuberculosis (Edinb). 2013;93(2):213-21.
12. Dorhoi A, Kaufmann SH. Perspectives on host adaptation in response to Mycobacterium tuberculosis: modulation of inflammation. Semin Immunol. 2014;26(6):533-42.
13. Tuddenham WJ. Glossary of terms for thoracic radiology: recommendations of the Nomenclature Committee of the Fleischner Society. AJR Am J Roentgenol. 1984;143(3):509-17.
14. Andrade BB, Reis-Filho A, Souza-Neto SM, Clarencio J, Camargo LM, Barral A, Barral-Netto M. Severe Plasmodium vivax malaria exhibits marked inflammatory imbalance. Malar J. 2010;9:13.
15. Correia LC, Andrade BB, Borges VM, Clarencio J, Bittencourt AP, Freitas R, Souza AC, Almeida MC, Leal J, Esteves JP, et al. Prognostic value of cytokines and chemokines in addition to the GRACE Score in non-ST-elevation acute coronary syndromes. Clin Chim Acta. 2010;411(7-8):540-5.
16. Luz NF, Andrade BB, Feijo DF, Araujo-Santos T, Carvalho GQ, Andrade D, Abanades DR, Melo EV, Silva AM, Brodskyn CI, et al. Heme oxygenase-1 promotes the persistence of Leishmania chagasi infection. J Immunol. 2012;188(9):4460-7.
17. Andrade BB, Singh A, Narendran G, Schechter ME, Nayak K, Subramanian S, Anbalagan S, Jensen SM, Porter BO, Antonelli LR, et al. Mycobacterial antigen driven activation of CD14++CD16- monocytes is a predictor of tuberculosis-associated immune reconstitution inflammatory syndrome. PLoS Pathog. 2014;10(10):e1004433.
18. Mendonca VR, Andrade BB, Souza LC, Magalhaes BM, Mourao MP, Lacerda MV, Barral-Netto M. Unravelling the patterns of host immune responses in Plasmodium vivax malaria and dengue co-infection. Malar J. 2015;14:315.
19. Mendonca VR, Queiroz AT, Lopes FM, Andrade BB, Barral-Netto M. Networking the host immune response in Plasmodium vivax malaria. Malar J. 2013;12:69.
20. Musselwhite LW, Andrade BB, Ellenberg SS, Tierney A, Belaunzaran-Zamudio PF, Rupert A, Lederman MM, Sanne I, Sierra Madero JG, Sereti I. Vitamin D, d-dimer, Interferon gamma, and sCD14 Levels are Independently Associated with Immune Reconstitution Inflammatory Syndrome: A Prospective, International Study. EBioMedicine. 2016;4:115-23.
21. Andrade BB, Pavan Kumar N, Sridhar R, Banurekha VV, Jawahar MS, Nutman TB, Sher A, Babu S. Heightened plasma levels of Heme Oxygenase-1 and Tissue Inhibitor of Metalloproteinase-4 as well as elevated peripheral neutrophil counts are associated with tuberculosis-diabetes comorbidity. Chest. 2014;145(1):1244-54.
22. Golub JE, Bur S, Cronin WA, Gange S, Baruch N, Comstock GW, Chaisson RE. Delayed tuberculosis diagnosis and tuberculosis transmission. Int J Tuberc Lung Dis. 2006;10(1):24-30.
23. Kim HR, Hwang SS, Kim HJ, Lee SM, Yoo CG, Kim YW, Han SK, Shim YS, Yim JJ. Impact of extensive drug resistance on treatment outcomes in non-HIV-infected patients with multidrug-resistant tuberculosis. Clin Infect Dis. 2007;45(10):1290-5.
24. Visser ME, Stead MC, Walzl G, Warren R, Schomaker M, Grewal HM, Swart EC, Maartens G. Baseline predictors of sputum culture conversion in pulmonary tuberculosis: importance of cavities, smoking, time to detection and W-Beijing genotype. PLoS One. 2012;7(1):e29588.
25. Lee JJ, Chong PY, Lin CB, Hsu AH, Lee CC. High resolution chest CT in patients with pulmonary tuberculosis: characteristic findings before and after antituberculous therapy. Eur J Radiol. 2008;67(1):100-4.
26. Clifford V, He Y, Zufferey C, Connell T, Curtis N. Interferon gamma release assays for monitoring the response to treatment for tuberculosis: A systematic review. Tuberculosis (Edinb). 2015;95(6):639-50.
27. Azzurri A, Sow OY, Amedei A, Bah B, Diallo S, Peri G, Benagiano M, D'Elios MM, Mantovani A, Del Prete G. IFN-gamma-inducible protein 10 and pentraxin 3 plasma levels are tools for monitoring inflammation and disease activity in Mycobacterium tuberculosis infection. Microbes Infect. 2005;7(1):1-8.
28. Wang JY, Chang HC, Liu JL, Shu CC, Lee CH, Wang JT, Lee LN. Expression of toll-like receptor 2 and plasma level of interleukin-10 are associated with outcome in tuberculosis. Eur J Clin Microbiol Infect Dis. 2012;31(9):2327-33.
29. Horne DJ, Royce SE, Gooze L, Narita M, Hopewell PC, Nahid P, Steingart KR. Sputum monitoring during tuberculosis treatment for predicting outcome: systematic review and meta-analysis. Lancet Infect Dis. 2010;10(6):387-94.
30. Ameglio F, Casarini M, Capoluongo E, Mattia P, Puglisi G, Giosue S. Post-treatment changes of six cytokines in active pulmonary tuberculosis: differences between patients with stable or increased fibrosis. Int J Tuberc Lung Dis. 2005;9(1):98-104.
31. Bekker LG, Maartens G, Steyn L, Kaplan G. Selective increase in plasma tumor necrosis factor-alpha and concomitant clinical deterioration after initiating therapy in patients with severe tuberculosis. J Infect Dis. 1998;178(2):580-4.
32. Day CL, Abrahams DA, Lerumo L, Janse van Rensburg E, Stone L, O'Rie T, Pienaar B, de Kock M, Kaplan G, Mahomed H, et al. Functional capacity of Mycobacterium tuberculosis-specific T cell responses in humans is associated with mycobacterial load. J Immunol. 2011;187(5):2222-32.
33. Djoba Siawaya JF, Beyers N, van Helden P, Walzl G. Differential cytokine secretion and early treatment response in patients with pulmonary tuberculosis. Clin Exp Immunol. 2009;156(1):69-77.
34. Pakasi TA, Karyadi E, Suratih NM, Salean M, Darmawidjaja N, Bor H, van der Velden K, Dolmans WM, van der Meer JW. Zinc and vitamin A supplementation fails to reduce sputum conversion time in severely malnourished pulmonary tuberculosis patients in Indonesia. Nutr J. 2010;9:41.
35. Peresi E, Silva SM, Calvi SA, Marcondes-Machado J. Cytokines and acute phase serum proteins as markers of inflammatory regression during the treatment of pulmonary tuberculosis. J Bras Pneumol. 2008;34(11):942-9.
36. Su WL, Perng WC, Huang CH, Yang CY, Wu CP, Chen JH. Association of reduced tumor necrosis factor alpha, gamma interferon, and interleukin-1beta (IL-1beta) but increased IL-10 expression with improved chest radiography in patients with pulmonary tuberculosis. Clin Vaccine Immunol. 2010;17(2):223-31.
37. Chowdhury IH, Ahmed AM, Choudhuri S, Sen A, Hazra A, Pal NK, Bhattacharya B, Bahar B. Alteration of serum inflammatory cytokines in active pulmonary tuberculosis following anti-tuberculosis drug therapy. Mol Immunol. 2014;62(1):159-68.
38. Lago PM, Boechat N, Migueis DP, Almeida AS, Lazzarini LC, Saldanha MM, Kritski AL, Ho JL, Lapa e Silva JR. Interleukin-10 and interferon-gamma patterns during tuberculosis treatment: possible association with recurrence. Int J Tuberc Lung Dis. 2012;16(5):656-9.
39. Mihret A, Abebe M, Bekele Y, Aseffa A, Walzl G, Howe R. Impact of HIV co-infection on plasma level of cytokines and chemokines of pulmonary tuberculosis patients. BMC Infect Dis. 2014;14:125.
40. Sahiratmadja E, Alisjahbana B, Buccheri S, Di Liberto D, de Boer T, Adnan I, van Crevel R, Klein MR, van Meijgaarden KE, Nelwan RH, et al. Plasma granulysin levels and cellular interferon-gamma production correlate with curative host responses in tuberculosis, while plasma interferon-gamma levels correlate with tuberculosis disease activity in adults. Tuberculosis (Edinb). 2007;87(4):312-21.
41. Belay M, Legesse M, Mihret A, Bekele Y, Ottenhoff TH, Franken KL, Bjune G, Abebe F. Pro- and anti-inflammatory cytokines against Rv2031 are elevated during latent tuberculosis: a study in cohorts of tuberculosis patients, household contacts and community controls in an endemic setting. PLoS One. 2015;10(4):e0124134.
42. Moura EP, Toledo VP, Oliveira MH, Spindola-de-Miranda S, Andrade HM, Guimaraes TM. Pulmonary tuberculosis: evaluation of interferon-gamma levels as an immunological healing marker based on the response to the Bacillus Calmette-Guerin. Mem Inst Oswaldo Cruz. 2004;99(3):283-7.
43. Ribeiro-Rodrigues R, Resende Co T, Johnson JL, Ribeiro F, Palaci M, Sa RT, Maciel EL, Pereira Lima FE, Dettoni V, Toossi Z, et al. Sputum cytokine levels in patients with pulmonary tuberculosis as early markers of mycobacterial clearance. Clin Diagn Lab Immunol. 2002;9(4):818-23.
44. Dorhoi A, Yeremeev V, Nouailles G, Weiner 3rd J, Jorg S, Heinemann E, Oberbeck-Muller D, Knaul JK, Vogelzang A, Reece ST, et al. Type I IFN signaling triggers immunopathology in tuberculosis-susceptible mice by modulating lung phagocyte dynamics. Eur J Immunol. 2014;44(8):2380-93.
45. Goldberg MF, Saini NK, Porcelli SA. Evasion of Innate and Adaptive Immunity by Mycobacterium tuberculosis. Microbiol Spectr. 2014;2(5):MGM2-0005-2013. doi: 10.1128/microbiolspec.MGM2-0005-2013.
46. Sahiratmadja E, Alisjahbana B, de Boer T, Adnan I, Maya A, Danusantoso H, Nelwan RH, Marzuki S, van der Meer JW, van Crevel R, et al. Dynamic changes in pro- and anti-inflammatory cytokine profiles and gamma interferon receptor signaling integrity correlate with tuberculosis disease activity and response to curative treatment. Infect Immun. 2007;75(2):820-9.
47. Adekambi T, Ibegbu CC, Cagle S, Kalokhe AS, Wang YF, Hu Y, Day CL, Ray SM, Rengarajan J. Biomarkers on patient T cells diagnose active tuberculosis and monitor treatment response. J Clin Invest. 2015;125(5):1827-38.
48. Hur YG, Kang YA, Jang SH, Hong JY, Kim A, Lee SA, Kim Y, Cho SN. Adjunctive biomarkers for improving diagnosis of tuberculosis and monitoring therapeutic effects. J Infect. 2015;70(4):346-55.
49. Lee MR, Tsai CJ, Wang WJ, Chuang TY, Yang CM, Chang LY, Lin CK, Wang JY, Shu CC, Lee LN, et al. Plasma Biomarkers Can Predict Treatment Response in Tuberculosis Patients: A Prospective Observational Study. Medicine (Baltimore). 2015;94(39):e1628.
50. Kubler A, Larsson C, Luna B, Andrade BB, Amaral EP, Urbanowski M, Orandle M, Bock K, Ammerman NC, Cheung LS, et al. Cathepsin K Contributes to Cavitation and Collagen Turnover in Pulmonary Tuberculosis. J Infect Dis. 2016;213(4):618-27.
51. Kubler A, Luna B, Larsson C, Ammerman NC, Andrade BB, Orandle M, Bock KW, Xu Z, Bagci U, Mollura DJ, et al. Mycobacterium tuberculosis dysregulates MMP/TIMP balance to drive rapid cavitation and unrestrained bacterial proliferation. J Pathol. 2015;235(3):431-44.
52. Chen CJ, Cheng FC, Su HL, Sheu ML, Lu ZH, Chiang CY, Yang DY, Sheehan J, Pan HC. Improved neurological outcome by intramuscular injection of human amniotic fluid derived stem cells in a muscle denervation model. PLoS One. 2015;10(5):e0124624.
53. Ansar W, Ghosh S. C-reactive protein and the biology of disease. Immunol Res. 2013;56(1):131-42.
54. Nikitina IY, Kondratuk NA, Kosmiadi GA, Amansahedov RB, Vasilyeva IA, Ganusov VV, Lyadova IV. Mtb-specific CD27low CD4 T cells as markers of lung tissue destruction during pulmonary tuberculosis in humans. PLoS One. 2012;7(8):e43733.
55. Andrade BB, Pavan Kumar N, Mayer-Barber KD, Barber DL, Sridhar R, Rekha VV, Jawahar MS, Nutman TB, Sher A, Babu S. Plasma heme oxygenase-1 levels distinguish latent or successfully treated human tuberculosis from active disease. PLoS One. 2013;8(5):e62618.
56. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, Wilkinson KA, Banchereau R, Skinner J, Wilkinson RJ, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature. 2010;466(7309):973-7.
57. Bloom CI, Graham CM, Berry MP, Rozakeas F, Redford PS, Wang Y, Xu Z, Wilkinson KA, Wilkinson RJ, Kendrick Y, et al. Transcriptional blood signatures distinguish pulmonary tuberculosis, pulmonary sarcoidosis, pneumonias and lung cancers. PLoS One. 2013;8(8):e70630.
58. Koruk M, Taysi S, Savas MC, Yilmaz O, Akcay F, Karakok M. Serum levels of acute phase proteins in patients with nonalcoholic steatohepatitis. Turk J Gastroenterol. 2003;14(1):12-7.
59. Han ZQ, Huang T, Deng YZ, Zhu GZ. Expression profile and kinetics of cytokines and chemokines in patients with chronic hepatitis C. Int J Clin Exp Med. 2015;8(10):17995-8003.
60. Tientcheu LD, Maertzdorf J, Weiner J, Adetifa IM, Mollenkopf HJ, Sutherland JS, Donkor S, Kampmann B, Kaufmann SH, Dockrell HM, et al. Differential transcriptomic and metabolic profiles of M. africanum- and M. tuberculosis-infected patients after, but not before, drug treatment. Genes Immun. 2015;16(5):347-55.