Biomarkers Associated with Death After Initiating Treatment for Tuberculosis and HIV in Patients with Very Low CD4 Cells

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Fred Richard Sattler
Daniel Chelliah
Xingye Wu
Alejandro Sanchez
Michelle A. Kendall
Evelyn Hogg
David Lagat
Umesh Lalloo
Valdilea Veloso
Diane V. Havlir
Alan Landay


Background: The risk of short-term death for treatment naive patients dually infected with Mycobacterium tuberculosis and HIV may be reduced by early anti-retroviral therapy. Of those dying, mechanisms responsible for fatal outcomes are unclear. We hypothesized that greater malnutrition and/or inflammation when initiating treatment are associated with an increased risk for death.

Methods: We utilized a retrospective case-cohort design among participants of the ACTG A5221 study who had baseline CD4 < 50 cells/mm3. The case-cohort sample consisted of 51 randomly selected participants, whose stored plasma was tested for C-reactive protein, cytokines, chemokines, and nutritional markers. Cox proportional hazards models were used to assess the association of nutritional, inflammatory, and immunomodulatory markers for survival.

Results: The case-cohort sample was similar to the 282 participants within the parent cohort with CD4 < 50 cells/mm3. In the case cohort, 7 (14%) had BMI < 16.5 (kg/m2) and 17 (33%) had BMI 16.5-18.5(kg/m2). Risk of death was increased per 1 IQR width higher of log10 transformed level of C-reactive protein (adjusted hazard ratio (aHR) = 3.42 [95% CI = 1.33-8.80],P = 0.011), interferon gamma (aHR = 2.46 [CI = 1.02-5.90], P = 0.044), MCP-3 (3.67 [CI = 1.08-12.42], P = 0.037), and with IL-15 (aHR = 2.75 [CI = 1.08-6.98], P = 0.033) and IL-17 (aHR = 3.99 [CI = -1.06-15.07], P = 0.041). BMI, albumin, hemoglobin, and leptin levels were not associated with risk of death.

Conclusions: Unlike patients only infected with M. tuberculosis for whom malnutrition and low BMI increase the risk of death, this relationship was not evident in our dually infected patients. Risk of death was associated with significant increases in markers of global inflammation along with soluble biomarkers of innate and adaptive immunity.


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Sattler FR, Chelliah D, Wu X, Sanchez A, Kendall MA, Hogg E, et al. Biomarkers Associated with Death After Initiating Treatment for Tuberculosis and HIV in Patients with Very Low CD4 Cells. PAI [Internet]. 2018 Apr. 26 [cited 2023 Sep. 23];3(1):46-62. Available from:
Author Biography

Fred Richard Sattler, Keck School of Medicine of the University of Southern California, Los Angeles, CA

Professor of Medicine

Chief of the Division of Infectious Diseases



1. Ford N, Shubber Z, Meintjes G, Grinsztejn B, Eholie S, Mills EJ, Davies MA, Vitoria M, Penazzato M, Nsanzimana S, Frigati L, O'Brien D, Ellman T, Ajose O, Calmy A, Doherty M. Causes of hospital admission among people living with HIV worldwide: a systematic review and meta-analysis. Lancet HIV. 2015;2(10):e438-44. PubMed PMID: 26423651. doi: 10.1016/S2352-3018(15)00137-X

2. Odone A, Amadasi S, White RG, Cohen T, Grant AD, Houben RM. The impact of antiretroviral therapy on mortality in HIV positive people during tuberculosis treatment: a systematic review and meta-analysis. PLoS One. 2014;9(11):e112017. PubMed PMID: 25391135. Pubmed Central PMCID: 4229142. doi: 10.1371/journal.pone.0112017

3. Havlir DV, Kendall MA, Ive P, Kumwenda J, Swindells S, Qasba SS, Luetkemeyer AF, Hogg E, Rooney JF, Wu X, Hosseinipour MC, Lalloo U, Veloso VG, Some FF, Kumarasamy N, Padayatchi N, Santos BR, Reid S, Hakim J, Mohapi L, Mugyenyi P, Sanchez J, Lama JR, Pape JW, Sanchez A, Asmelash A, Moko E, Sawe F, Andersen J, Sanne I, A ACTGS. Timing of antiretroviral therapy for HIV-1 infection and tuberculosis. N Engl J Med. 2011;365(16):1482-91. PubMed PMID: 22010914. Pubmed Central PMCID: 3327101. doi: 10.1056/NEJMoa1013607

4. Blanc FX, Sok T, Laureillard D, Borand L, Rekacewicz C, Nerrienet E, Madec Y, Marcy O, Chan S, Prak N, Kim C, Lak KK, Hak C, Dim B, Sin CI, Sun S, Guillard B, Sar B, Vong S, Fernandez M, Fox L, Delfraissy JF, Goldfeld AE, Team CS. Earlier versus later start of antiretroviral therapy in HIV-infected adults with tuberculosis. N Engl J Med. 2011;365(16):1471-81. PubMed PMID: 22010913. Pubmed Central PMCID: 4879711. doi: 10.1056/NEJMoa1013911

5. Velasco M, Castilla V, Sanz J, Gaspar G, Condes E, Barros C, Cervero M, Torres R, Guijarro C, Cohort C. Effect of simultaneous use of highly active antiretroviral therapy on survival of HIV patients with tuberculosis. J Acquir Immune Defic Syndr. 2009;50(2):148-52. PubMed PMID: 19131895. doi: 10.1097/QAI.0b013e31819367e7

6. Van Lettow M, Kumwenda JJ, Harries AD, Whalen CC, Taha TE, Kumwenda N, Kang'ombe C, Semba RD. Malnutrition and the severity of lung disease in adults with pulmonary tuberculosis in Malawi. Int J Tuberc Lung Dis. 2004;8(2):211-7. PubMed PMID: 15139450.

7. Lonnroth K, Williams BG, Cegielski P, Dye C. A consistent log-linear relationship between tuberculosis incidence and body mass index. Int J Epidemiol. 2010;39(1):149-55. PubMed PMID: 19820104. doi: 10.1093/ije/dyp308

8. Mupere E, Parraga IM, Tisch DJ, Mayanja HK, Whalen CC. Low nutrient intake among adult women and patients with severe tuberculosis disease in Uganda: a cross-sectional study. BMC Public Health. 2012;12:1050. PubMed PMID: 23217171. Pubmed Central PMCID: PMC3537524. doi: 10.1186/1471-2458-12-1050

9. Zachariah R, Spielmann MP, Harries AD, Salaniponi FM. Moderate to severe malnutrition in patients with tuberculosis is a risk factor associated with early death. Trans R Soc Trop Med Hyg. 2002;96(3):291-4. PubMed PMID: 12174782.

10. Macallan DC, McNurlan MA, Kurpad AV, de Souza G, Shetty PS, Calder AG, Griffin GE. Whole body protein metabolism in human pulmonary tuberculosis and undernutrition: evidence for anabolic block in tuberculosis. Clin Sci (Lond). 1998;94(3):321-31. PubMed PMID: 9616267.

11. Mupere E, Malone L, Zalwango S, Chiunda A, Okwera A, Parraga I, Stein CM, Tisch DJ, Mugerwa R, Boom WH, Mayanja H, Whalen CC. Lean tissue mass wasting is associated with increased risk of mortality among women with pulmonary tuberculosis in urban Uganda. Ann Epidemiol. 2012;22(7):466-73. PubMed PMID: 22575813. Pubmed Central PMCID: 3377556. doi: 10.1016/j.annepidem.2012.04.007

12. Villamor E, Saathoff E, Mugusi F, Bosch RJ, Urassa W, Fawzi WW. Wasting and body composition of adults with pulmonary tuberculosis in relation to HIV-1 coinfection, socioeconomic status, and severity of tuberculosis. Eur J Clin Nutr. 2006;60(2):163-71. PubMed PMID: 16234841. doi: 10.1038/sj.ejcn.1602281

13. Lucas SB, De Cock KM, Hounnou A, Peacock C, Diomande M, Honde M, Beaumel A, Kestens L, Kadio A. Contribution of tuberculosis to slim disease in Africa. BMJ. 1994;308(6943):1531-3. PubMed PMID: 7912597. Pubmed Central PMCID: 2540503

14. van Lettow M, van der Meer JW, West CE, van Crevel R, Semba RD. Interleukin-6 and human immunodeficiency virus load, but not plasma leptin concentration, predict anorexia and wasting in adults with pulmonary tuberculosis in Malawi. J Clin Endocrinol Metab. 2005;90(8):4771-6. PubMed PMID: 15928249. doi: 10.1210/jc.2004-2539

15. Whalen CC, Nsubuga P, Okwera A, Johnson JL, Hom DL, Michael NL, Mugerwa RD, Ellner JJ. Impact of pulmonary tuberculosis on survival of HIV-infected adults: a prospective epidemiologic study in Uganda. AIDS. 2000;14(9):1219-28. PubMed PMID: 10894287. Pubmed Central PMCID: 2869086.

16. Toossi Z, Mayanja-Kizza H, Hirsch CS, Edmonds KL, Spahlinger T, Hom DL, Aung H, Mugyenyi P, Ellner JJ, Whalen CW. Impact of tuberculosis (TB) on HIV-1 activity in dually infected patients. Clin Exp Immunol. 2001;123(2):233-8. PubMed PMID: 11207653. Pubmed Central PMCID: 1905977.

17. Shah S, Whalen C, Kotler DP, Mayanja H, Namale A, Melikian G, Mugerwa R, Semba RD. Severity of human immunodeficiency virus infection is associated with decreased phase angle, fat mass and body cell mass in adults with pulmonary tuberculosis infection in Uganda. J Nutr. 2001;131(11):2843-7. PubMed PMID: 11694606. doi: 10.1093/jn/131.11.2843

18. Rivera S, Sattler FR, Boyd H, Auffenberg T, Nakao S, Moldawer LL. Urinary cytokines for assessing inflammation in HIV-associated wasting. Cytokine. 2001;13(5):305-13. PubMed PMID: 11243709. doi: 10.1006/cyto.2000.0830

19. Zackin RA, Clark RA, Currier JS, Mildvan D. Predictive markers of HIV-related weight loss and determination of differences between populations with weight loss stratified by opportunistic processes. J Acquir Immune Defic Syndr. 1999;22(2):189-93. PubMed PMID: 10843534.

20. Suttmann U, Ockenga J, Selberg O, Hoogestraat L, Deicher H, Muller MJ. Incidence and prognostic value of malnutrition and wasting in human immunodeficiency virus-infected outpatients. J Acquir Immune Defic Syndr Hum Retrovirol. 1995;8(3):239-46. PubMed PMID: 7859135.

21. Wheeler DA, Gibert CL, Launer CA, Muurahainen N, Elion RA, Abrams DI, Bartsch GE. Weight loss as a predictor of survival and disease progression in HIV infection. Terry Beirn Community Programs for Clinical Research on AIDS. J Acquir Immune Defic Syndr Hum Retrovirol. 1998;18(1):80-5. PubMed PMID: 9593462.

22. Lindan CP, Allen S, Serufilira A, Lifson AR, Van de Perre P, Chen-Rundle A, Batungwanayo J, Nsengumuremyi F, Bogaerts J, Hulley S. Predictors of mortality among HIV-infected women in Kigali, Rwanda. Ann Intern Med. 1992;116(4):320-8. PubMed PMID: 1733389.

23. van der Sande MA, Schim van der Loeff MF, Aveika AA, Sabally S, Togun T, Sarge-Njie R, Alabi AS, Jaye A, Corrah T, Whittle HC. Body mass index at time of HIV diagnosis: a strong and independent predictor of survival. J Acquir Immune Defic Syndr. 2004;37(2):1288-94. PubMed PMID: 15385737.

24. Kotler DP, Tierney AR, Wang J, Pierson RN, Jr. Magnitude of body-cell-mass depletion and the timing of death from wasting in AIDS. Am J Clin Nutr. 1989;50(3):444-7. PubMed PMID: 2773823. doi: 10.1093/ajcn/50.3.444

25. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340(6):448-54. PubMed PMID: 9971870. doi: 10.1056/NEJM199902113400607

26. Poli G, Bressler P, Kinter A, Duh E, Timmer WC, Rabson A, Justement JS, Stanley S, Fauci AS. Interleukin 6 induces human immunodeficiency virus expression in infected monocytic cells alone and in synergy with tumor necrosis factor alpha by transcriptional and post-transcriptional mechanisms. J Exp Med. 1990;172(1):151-8. PubMed PMID: 2193094. Pubmed Central PMCID: 2188185.

27. Nakata K, Rom WN, Honda Y, Condos R, Kanegasaki S, Cao Y, Weiden M. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am J Respir Crit Care Med. 1997;155(3):996-1003. PubMed PMID: 9117038. doi: 10.1164/ajrccm.155.3.9117038

28. Wallis RS, Helfand MS, Whalen CC, Johnson JL, Mugerwa RD, Vjecha M, Okwera A, Ellner JJ. Immune activation, allergic drug toxicity and mortality in HIV-positive tuberculosis. Tuber Lung Dis. 1996;77(6):516-23. PubMed PMID: 9039444.

29. Rivera S, Briggs W, Qian D, Sattler FR. Levels of HIV RNA are quantitatively related to prior weight loss in HIV-associated wasting. J Acquir Immune Defic Syndr Hum Retrovirol. 1998;17(5):411-8. PubMed PMID: 9562043.

30. Paton NI, Chua YK, Earnest A, Chee CB. Randomized controlled trial of nutritional supplementation in patients with newly diagnosed tuberculosis and wasting. Am J Clin Nutr. 2004;80(2):460-5. PubMed PMID: 15277171. doi: 10.1093/ajcn/80.2.460

31. Grobler L, Nagpal S, Sudarsanam TD, Sinclair D. Nutritional supplements for people being treated for active tuberculosis. Cochrane Database Syst Rev. 2016 (6):CD006086. PubMed PMID: 27355911. Pubmed Central PMCID: 4981643. doi: 10.1002/14651858.CD006086.pub4

32. Vankayalapati R, Barnes PF. Innate and adaptive immune responses to human Mycobacterium tuberculosis infection. Tuberculosis (Edinb). 2009;89 Suppl 1:S77-80. PubMed PMID: 20006312. doi: 10.1016/S1472-9792(09)70018-6

33. Gregory SH, Jiang X, Wing EJ. Lymphokine-activated killer cells lyse Listeria-infected hepatocytes and produce elevated quantities of interferon-gamma. J Infect Dis. 1996;174(5):1073-9. PubMed PMID: 8896511.

34. Tay CH, Szomolanyi-Tsuda E, Welsh RM. Control of infections by NK cells. Curr Top Microbiol Immunol. 1998;230:193-220. PubMed PMID: 9586357.

35. Vankayalapati R, Wizel B, Weis SE, Safi H, Lakey DL, Mandelboim O, Samten B, Porgador A, Barnes PF. The NKp46 receptor contributes to NK cell lysis of mononuclear phagocytes infected with an intracellular bacterium. J Immunol. 2002;168(7):3451-7. PubMed PMID: 11907104.

36. Orange JS, Wang B, Terhorst C, Biron CA. Requirement for natural killer cell-produced interferon gamma in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J Exp Med. 1995;182(4):1045-56. PubMed PMID: 7561678. Pubmed Central PMCID: 2192290.

37. Lucey DR, Clerici M, Shearer GM. Type 1 and type 2 cytokine dysregulation in human infectious, neoplastic, and inflammatory diseases. Clin Microbiol Rev. 1996;9(4):532-62. PubMed PMID: 8894351. Pubmed Central PMCID: 172909.

38. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, Lowenstein CJ, Schreiber R, Mak TW, Bloom BR. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity. 1995;2(6):561-72. PubMed PMID: 7540941.

39. Chensue SW, Warmington KS, Ruth JH, Lincoln P, Kunkel SL. Cytokine function during mycobacterial and schistosomal antigen-induced pulmonary granuloma formation. Local and regional participation of IFN-gamma, IL-10, and TNF. J Immunol. 1995;154(11):5969-76. PubMed PMID: 7751640.

40. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med. 1993;178(6):2243-7. PubMed PMID: 8245795. Pubmed Central PMCID: 2191280.

41. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med. 1993;178(6):2249-54. PubMed PMID: 7504064. Pubmed Central PMCID: 2191274.

42. Vankayalapati R, Klucar P, Wizel B, Weis SE, Samten B, Safi H, Shams H, Barnes PF. NK cells regulate CD8+ T cell effector function in response to an intracellular pathogen. J Immunol. 2004;172(1):130-7. PubMed PMID: 14688318.

43. Krutzik SR, Hewison M, Liu PT, Robles JA, Stenger S, Adams JS, Modlin RL. IL-15 links TLR2/1-induced macrophage differentiation to the vitamin D-dependent antimicrobial pathway. J Immunol. 2008;181(10):7115-20. PubMed PMID: 18981132. Pubmed Central PMCID: 2678236.

44. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198(12):1875-86. PubMed PMID: 14676299. Pubmed Central PMCID: 2194145. doi: 10.1084/jem.20030152

45. Khader SA, Cooper AM. IL-23 and IL-17 in tuberculosis. Cytokine. 2008;41(2):79-83. PubMed PMID: 18218322. Pubmed Central PMCID: 2266085. doi: 10.1016/j.cyto.2007.11.022

46. Khader SA, Pearl JE, Sakamoto K, Gilmartin L, Bell GK, Jelley-Gibbs DM, Ghilardi N, deSauvage F, Cooper AM. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J Immunol. 2005;175(2):788-95. PubMed PMID: 16002675.

47. Barnes PF, Lu S, Abrams JS, Wang E, Yamamura M, Modlin RL. Cytokine production at the site of disease in human tuberculosis. Infect Immun. 1993;61(8):3482-9. PubMed PMID: 8335379. Pubmed Central PMCID: 281026.

48. Cruz A, Khader SA, Torrado E, Fraga A, Pearl JE, Pedrosa J, Cooper AM, Castro AG. Cutting edge: IFN-gamma regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection. J Immunol. 2006;177(3):1416-20. PubMed PMID: 16849446.

49. Jones CE, Chan K. Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-alpha, and granulocyte-colony-stimulating factor by human airway epithelial cells. Am J Respir Cell Mol Biol. 2002;26(6):748-53. PubMed PMID: 12034575.

50. Sergejeva S, Ivanov S, Lotvall J, Linden A. Interleukin-17 as a recruitment and survival factor for airway macrophages in allergic airway inflammation. Am J Respir Cell Mol Biol. 2005;33(3):248-53. PubMed PMID: 15901616. doi: 10.1165/rcmb.2004-0213OC

51. Umemura M, Yahagi A, Hamada S, Begum MD, Watanabe H, Kawakami K, Suda T, Sudo K, Nakae S, Iwakura Y, Matsuzaki G. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol. 2007;178(6):3786-96. PubMed PMID: 17339477.

52. Lockhart E, Green AM, Flynn JL. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol. 2006;177(7):4662-9. PubMed PMID: 16982905.

53. Meraviglia S, El Daker S, Dieli F, Martini F, Martino A. gammadelta T cells cross-link innate and adaptive immunity in Mycobacterium tuberculosis infection. Clin Dev Immunol. 2011;2011:587315. PubMed PMID: 21253470. Pubmed Central PMCID: 3022180. doi: 10.1155/2011/587315

54. Poquet Y, Halary F, Champagne E, Davodeau F, Gougeon ML, Bonneville M, Fournie JJ. Human gamma delta T cells in tuberculosis. Res Immunol. 1996;147(8-9):542-9. PubMed PMID: 9127886.

55. Szereday L, Baliko Z, Szekeres-Bartho J. The role of Vdelta2+T-cells in patients with active Mycobacterium tuberculosis infection and tuberculin anergy. Int J Tuberc Lung Dis. 2008;12(3):262-8. PubMed PMID: 18284830.

56. Kabelitz D, Bender A, Prospero T, Wesselborg S, Janssen O, Pechhold K. The primary response of human gamma/delta + T cells to Mycobacterium tuberculosis is restricted to V gamma 9-bearing cells. J Exp Med. 1991;173(6):1331-8. PubMed PMID: 1827825. Pubmed Central PMCID: 2190845.

57. Havlir DV, Ellner JJ, Chervenak KA, Boom WH. Selective expansion of human gamma delta T cells by monocytes infected with live Mycobacterium tuberculosis. J Clin Invest. 1991;87(2):729-33. PubMed PMID: 1899430. Pubmed Central PMCID: 296366. doi: 10.1172/JCI115053

58. Zhang X, Sun S, Hwang I, Tough DF, Sprent J. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity. 1998;8(5):591-9. PubMed PMID: 9620680.

59. Casetti R, Martino A. The plasticity of gamma delta T cells: innate immunity, antigen presentation and new immunotherapy. Cell Mol Immunol. 2008;5(3):161-70. PubMed PMID: 18582397. Pubmed Central PMCID: 4651290. doi: 10.1038/cmi.2008.20

60. Daley CL, Small PM, Schecter GF, Schoolnik GK, McAdam RA, Jacobs WR, Jr., Hopewell PC. An outbreak of tuberculosis with accelerated progression among persons infected with the human immunodeficiency virus. An analysis using restriction-fragment-length polymorphisms. N Engl J Med. 1992;326(4):231-5. PubMed PMID: 1345800. doi: 10.1056/NEJM199201233260404

61. Giovanni D, Chiara Danzi M, De Checchi G, Pizzighella S, Solbiati M, Cruciani M, Luzzati R, Malena M, Mazzi R, Concia E, Bassetti D. Nosocomial Epidemic of Active Tuberculosis Among HIV-Infected Patients. The Lancet.334(8678):1502-4. doi: 10.1016/S0140-6736(89)92942-5

62. Whalen C, Horsburgh CR, Hom D, Lahart C, Simberkoff M, Ellner J. Accelerated course of human immunodeficiency virus infection after tuberculosis. Am J Respir Crit Care Med. 1995;151(1):129-35. PubMed PMID: 7812542. doi: 10.1164/ajrccm.151.1.7812542

63. Pape JW, Jean SS, Ho JL, Hafner A, Johnson WD, Jr. Effect of isoniazid prophylaxis on incidence of active tuberculosis and progression of HIV infection. Lancet. 1993;342(8866):268-72. PubMed PMID: 8101302.

64. Eriki PP, Okwera A, Aisu T, Morrissey AB, Ellner JJ, Daniel TM. The influence of human immunodeficiency virus infection on tuberculosis in Kampala, Uganda. Am Rev Respir Dis. 1991;143(1):185-7. PubMed PMID: 1986677. doi: 10.1164/ajrccm/143.1.185

65. Goletti D, Weissman D, Jackson RW, Graham NM, Vlahov D, Klein RS, Munsiff SS, Ortona L, Cauda R, Fauci AS. Effect of Mycobacterium tuberculosis on HIV replication. Role of immune activation. J Immunol. 1996;157(3):1271-8. PubMed PMID: 8757635.

66. Janssen S, Schutz C, Ward A, Nemes E, Wilkinson KA, Scriven J, Huson MA, Aben N, Maartens G, Burton R, Wilkinson RJ, Grobusch MP, Van der Poll T, Meintjes G. Mortality in Severe Human Immunodeficiency Virus-Tuberculosis Associates With Innate Immune Activation and Dysfunction of Monocytes. Clin Infect Dis. 2017;65(1):73-82. PubMed PMID: 28369200. Pubmed Central PMCID: 5849097. doi: 10.1093/cid/cix254

67. Jones SP, Franco NF, Varney B, Sundaram G, Brown DA, de Bie J, Lim CK, Guillemin GJ, Brew BJ. Expression of the Kynurenine Pathway in Human Peripheral Blood Mononuclear Cells: Implications for Inflammatory and Neurodegenerative Disease. PLoS One. 2015;10(6):e0131389. PubMed PMID: 26114426. Pubmed Central PMCID: 4482723. doi: 10.1371/journal.pone.0131389

68. Adu-Gyamfi CG, Snyman T, Hoffmann CJ, Martinson NA, Chaisson RE, George JA, Suchard MS. Plasma Indoleamine 2, 3-Dioxygenase, a Biomarker for Tuberculosis in Human Immunodeficiency Virus-Infected Patients. Clin Infect Dis. 2017;65(8):1356-8. PubMed PMID: 29017244. Pubmed Central PMCID: 5848309. doi: 10.1093/cid/cix550

69. Mandi Y, Vecsei L. The kynurenine system and immunoregulation. J Neural Transm (Vienna). 2012;119(2):197-209. PubMed PMID: 21744051. doi: 10.1007/s00702-011-0681-y

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