Ethambutol partitioning in tuberculous pulmonary lesions explains its clinical efficacy

Antimicrobial Agents and Chemotherapy

Volumn 61, Issue 9, 2017, Pages

  Zimmerman, Matthew ^a   Lestner, Jodi ^a,b   Prideaux, Brendan ^a   O'Brien, Paul ^a   Dias Freedman, Isabela ^a   Chen, Chao ^a   Dietzold, Jillian ^c   Daudelin, Isaac ^a   Kaya, Firat ^a   Blanc, Landry ^a   Chen, Pei Yu ^a   Park, Steven ^a   Salgame, Padmini ^c   Sarathy, Jansy ^a   Dartois, Véronique ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Ethambutol; Lesion penetration; Mycobacterium tuberculosis; Pharmacokinetics

Indexed keywords

ETHAMBUTOL; TUBERCULOSTATIC AGENT;

ANIMAL; C57BL MOUSE; DRUG EFFECTS; FEMALE; HUMAN; LEPORIDAE; LIQUID CHROMATOGRAPHY; LUNG TUBERCULOSIS; MOUSE; MYCOBACTERIUM TUBERCULOSIS; PROCEDURES; TANDEM MASS SPECTROMETRY; TREATMENT OUTCOME;

ANIMALS; ANTITUBERCULAR AGENTS; CHROMATOGRAPHY, LIQUID; ETHAMBUTOL; FEMALE; HUMANS; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; RABBITS; TANDEM MASS SPECTROMETRY; TREATMENT OUTCOME; TUBERCULOSIS, PULMONARY;

EID: 85028360127     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00924-17     Document Type: Article

References (40)

1. WHO. 2016. Global tuberculosis report 2016. World Health Organization, Geneva, Switzerland. http://apps.who.int/iris/bitstream/10665/250441/1/9789241565394-eng.pdf?ua1.
2. Fox W, Ellard GA, Mitchison DA. 1999. Studies on the treatment of tuberculosis undertaken by the British Medical Research Council tuberculosis units, 1946–1986, with relevant subsequent publications. Int J Tuberc Lung Dis 3:S231–S279.
3. Anonymous. 1981. Controlled trial of four thrice-weekly regimens and a daily regimen all given for 6 months for pulmonary tuberculosis. Lancet i:171–174.
4. Mitchison DA. 1985. The action of antituberculosis drugs in short-course chemotherapy. Tubercle 66:219 –225. https://doi.org/10.1016/0041-3879(85)90040-6.
5. Lakshminarayana SB, Huat TB, Ho PC, Manjunatha UH, Dartois V, Dick T, Rao SP. 2015. Comprehensive physicochemical, pharmacokinetic and activity profiling of anti-TB agents. J Antimicrob Chemother 70:857–867. https://doi.org/10.1093/jac/dku457.
6. Jindani A, Aber VR, Edwards EA, Mitchison DA. 1980. The early bactericidal activity of drugs in patients with pulmonary tuberculosis. Am Rev Respir Dis 121:939–949.
7. Clini V, Grassi C. 1970. The action of new antituberculous drugs on intracellular tubercle bacilli. Antibiot Chemother 16:20–26. https://doi.org/10.1159/000386799.
8. Hartkoorn RC, Chandler B, Owen A, Ward SA, Bertel Squire S, Back DJ, Khoo SH. 2007. Differential drug susceptibility of intracellular and extracellular tuberculosis, and the impact of P-glycoprotein. Tuberculosis (Edinb) 87:248–255. https://doi.org/10.1016/j.tube.2006.12.001.
9. Jia L, Tomaszewski JE, Hanrahan C, Coward L, Noker P, Gorman G, Nikonenko B, Protopopova M. 2005. Pharmacodynamics and pharmacokinetics of SQ109, a new diamine-based antitubercular drug. Br J Pharmacol 144:80–87. https://doi.org/10.1038/sj.bjp.0705984.
10. Denti P, Jeremiah K, Chigutsa E, Faurholt-Jepsen D, PrayGod G, Range N, Castel S, Wiesner L, Hagen CM, Christiansen M, Changalucha J, McIlleron H, Friis H, Andersen AB. 2015. Pharmacokinetics of isoniazid, pyrazinamide, and ethambutol in newly diagnosed pulmonary TB patients in Tanzania. PLoS One 10:e0141002. https://doi.org/10.1371/journal.pone.0141002.
11. Jonsson S, Davidse A, Wilkins J, Van der Walt JS, Simonsson US, Karlsson MO, Smith P, McIlleron H. 2011. Population pharmacokinetics of ethambutol in South African tuberculosis patients. Antimicrob Agents Chemother 55:4230–4237. https://doi.org/10.1128/AAC.00274-11.
12. Saktiawati AM, Sturkenboom MG, Stienstra Y, Subronto YW, Sumardi Kosterink JG, van der Werf TS, Alffenaar JW. 2016. Impact of food on the pharmacokinetics of first-line anti-TB drugs in treatment-naive TB patients: a randomized cross-over trial. J Antimicrob Chemother 71: 703–710. https://doi.org/10.1093/jac/dkv394.
13. Kelly RG, Kaleita E, Eisner HJ. 1981. Tissue distribution of [14C]ethambu-tol in mice. Am Rev Respir Dis 123:689–690.
14. Djurovic V, Decroix G, Daumet P. 1973. L’ethambutol chez l’homme. Etude comparative des taux seriques erythrocytaires et pulmonaires. Nouv Presse Med 2:2815–2816.
15. Liss RH, Letourneau RJ, Schepis JP. 1981. Distribution of ethambutol in primate tissues and cells. Am Rev Respir Dis 123:529–532.
16. Elliott AM, Berning SE, Iseman MD, Peloquin CA. 1995. Failure of drug penetration and acquisition of drug resistance in chronic tuberculous empyema. Tuber Lung Dis 76:463–467. https://doi.org/10.1016/0962-8479(95)90016-0.
17. Fatiguso G, Allegra S, Calcagno A, Baietto L, Motta I, Favata F, Cusato J, Bonora S, Perri GD, D’Avolio A. 2016. Ethambutol plasma and intracellular pharmacokinetics: a pharmacogenetic study. Int J Pharm 497: 287–292. https://doi.org/10.1016/j.ijpharm.2015.11.044.
18. Anonymous. 1982. Controlled trial of 4 three-times-weekly regimens and a daily regimen all given for 6 months for pulmonary tuberculosis. Second report: the results up to 24 months. Hong Kong Chest Service/ British Medical Research Council. Tubercle 63:89 –98.
19. Brown-Elliott BA, Nash KA, Wallace RJ, Jr. 2012. Antimicrobial susceptibility testing, drug resistance mechanisms, and therapy of infections with nontuberculous mycobacteria. Clin Microbiol Rev 25:545–582. https://doi.org/10.1128/CMR.05030-11.
20. Cowman S, Burns K, Benson S, Wilson R, Loebinger MR. 2016. The antimicrobial susceptibility of non-tuberculous mycobacteria. J Infect 72:324–331. https://doi.org/10.1016/j.jinf.2015.12.007.
21. Prideaux B, Via LE, Zimmerman MD, Eum S, Sarathy J, O’Brien P, Chen C, Kaya F, Weiner DM, Chen PY, Song T, Lee M, Shim TS, Cho JS, Kim W, Cho SN, Olivier KN, Barry CE, III, Dartois V. 2015. The association between sterilizing activity and drug distribution into tuberculosis lesions. Nat Med 21:1223–1227. https://doi.org/10.1038/nm.3937.
22. Sarathy JP, Zuccotto F, Hsinpin H, Sandberg L, Via LE, Marriner GA, Masquelin T, Wyatt P, Ray P, Dartois V. 2016. Prediction of drug penetration in tuberculosis lesions. ACS Infect Dis 2:552–563. https://doi.org/10.1021/acsinfecdis.6b00051.
23. van Oosterhout JJ, Dzinjalamala FK, Dimba A, Waterhouse D, Davies G, Zijlstra EE, Molyneux ME, Molyneux EM, Ward S. 2015. Pharmacokinetics of antituberculosis drugs in HIV-positive and HIV-negative adults in Malawi. Antimicrob Agents Chemother 59:6175–6180. https://doi.org/10.1128/AAC.01193-15.
24. Srivastava S, Musuka S, Sherman C, Meek C, Leff R, Gumbo T. 2010. Efflux-pump-derived multiple drug resistance to ethambutol mono-therapy in Mycobacterium tuberculosis and the pharmacokinetics and pharmacodynamics of ethambutol. J Infect Dis 201:1225–1231. https://doi.org/10.1086/651377.
25. Gillespie SH, Crook AM, McHugh TD, Mendel CM, Meredith SK, Murray SR, Pappas F, Phillips PP, Nunn AJ, REMoxTB Consortium. 2014. Four-month moxifloxacin-based regimens for drug-sensitive tuberculosis. N Engl J Med 371:1577–1587. https://doi.org/10.1056/NEJMoa1407426.
26. Merle CS, Fielding K, Sow OB, Gninafon M, Lo MB, Mthiyane T, Odhiambo J, Amukoye E, Bah B, Kassa F, N'Diaye A, Rustomjee R, de Jong BC, Horton J, Perronne C, Sismanidis C, Lapujade O, Olliaro PL, Lienhardt C, Project OFGfT. 2014. A four-month gatifloxacin-containing regimen for treating tuberculosis. N Engl J Med 371:1588 –1598. https://doi.org/10.1056/NEJMoa1315817.
27. Prideaux B, Dartois V, Staab D, Weiner DM, Goh A, Via LE, Barry CE, III, Stoeckli M. 2011. High-sensitivity MALDI-MRM-MS imaging of moxifloxacin distribution in tuberculosis-infected rabbit lungs and granulomatous lesions. Anal Chem 83:2112–2118. https://doi.org/10.1021/ac1029049.
28. Irwin SM, Prideaux B, Lyon ER, Zimmerman MD, Brooks EJ, Schrupp CA, Chao C, Reichlen MJ, Asay BC, Voskuil MI, Nuermberger EL, Andries K, Lyons MA, Dartois V, Lenaerts AJ. 2016. Bedaquiline and pyrazinamide treatment responses are affected by the heterogeneity in pulmonary lesions in Mycobacterium tuberculosis infected C3HeB/FeJ mice. ACS Infect Dis 2:251–267. https://doi.org/10.1021/acsinfecdis.5b00127.
29. Banerjee DK, Patel BR. 1993. Evaluation of the activity of a number of antimicrobial agents against mycobacteria within mouse macrophages by a radiometric method. J Antimicrob Chemother 31:289–302. https://doi.org/10.1093/jac/31.2.289.
30. Rey-Jurado E, Tudo G, Soy D, Gonzalez-Martin J. 2013. Activity and interactions of levofloxacin, linezolid, ethambutol and amikacin in three-drug combinations against Mycobacterium tuberculosis isolates in a human macrophage model. Int J Antimicrob Agents 42:524 –530. https://doi.org/10.1016/j.ijantimicag.2013.07.014.
31. Rastogi N, Labrousse V, Goh KS. 1996. In vitro activities of fourteen antimicrobial agents against drug susceptible and resistant clinical isolates of Mycobacterium tuberculosis and comparative intracellular activities against the virulent H37Rv strain in human macrophages. Curr Microbiol 33:167–175. https://doi.org/10.1007/s002849900095.
32. Shu CC, Lee CH, Hsu CL, Wang JT, Wang JY, Yu CJ, Lee LN, TAMI Group. 2011. Clinical characteristics and prognosis of nontuberculous mycobacterial lung disease with different radiographic patterns. Lung 189:467–474. https://doi.org/10.1007/s00408-011-9321-4.
33. Strollo SE, Adjemian J, Adjemian MK, Prevots DR. 2015. The burden of pulmonary nontuberculous mycobacterial disease in the United States. Ann Am Thorac Soc 12:1458–1464. https://doi.org/10.1513/AnnalsATS.201503-173OC.
34. Kalvass JC, Maurer TS. 2002. Influence of nonspecific brain and plasma binding on CNS exposure: implications for rational drug discovery. Biopharm Drug Dispos 23:327–338. https://doi.org/10.1002/bdd.325.
35. Di L, Umland JP, Trapa PE, Maurer TS. 2012. Impact of recovery on fraction unbound using equilibrium dialysis. J Pharm Sci 101:1327–1335. https://doi.org/10.1002/jps.23013.
36. Subbian S, Tsenova L, Yang G, O’Brien P, Parsons S, Peixoto B, Taylor L, Fallows D, Kaplan G. 2011. Chronic pulmonary cavitary tuberculosis in rabbits: a failed host immune response. Open Biol 1:110016. https://doi.org/10.1098/rsob.110016.
37. Savic RM, Ruslami R, Hibma JE, Hesseling A, Ramachandran G, Ganiem AR, Swaminathan S, McIlleron H, Gupta A, Thakur K, van Crevel R, Aarnoutse R, Dooley KE. 2015. Pediatric tuberculous meningitis: model-based approach to determining optimal doses of the anti-tuberculosis drugs rifampin and levofloxacin for children. Clin Pharmacol Ther 98:622–629. https://doi.org/10.1002/cpt.202.
38. Sheiner LB, Stanski DR, Vozeh S, Miller RD, Ham J. 1979. Simultaneous modeling of pharmacokinetics and pharmacodynamics: application to D-tubocurarine. Clin Pharmacol Ther 25:358–371. https://doi.org/10.1002/cpt1979253358.
39. Schon T, Jureen P, Giske CG, Chryssanthou E, Sturegard E, Werngren J, Kahlmeter G, Hoffner SE, Angeby KA. 2009. Evaluation of wild-type MIC distributions as a tool for determination of clinical breakpoints for Mycobacterium tuberculosis. J Antimicrob Chemother 64:786–793. https://doi.org/10.1093/jac/dkp262.
40. Kaniga K, Cirillo DM, Hoffner S, Ismail NA, Kaur D, Lounis N, Metchock B, Pfyffer GE, Venter A. 2016. A multi-laboratory, multi-country study to determine MIC quality control ranges for phenotypic drug-susceptibility testing of selected first-line anti-TB drugs, second-line injectables, fluoroquinolones, clofazimine and linezolid. J Clin Microbiol 54:2963–2968. https://doi.org/10.1128/JCM.01138-16.