Rapid drug tolerance and dramatic sterilizing effect of moxifloxacin monotherapy in a novel hollow-fiber model of intracellular mycobacterium kansasii disease

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 4, 2015, Pages 2273-2279

  Srivastava, Shashikant ^a   Pasipanodya, Jotam ^a   Sherman, Carleton M ^a   Meek, Claudia ^b   Leff, Richard ^b   Gumbo, Tawanda ^a,c  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ETHAMBUTOL; ISONIAZID; MOXIFLOXACIN; RESERPINE; RIFAMPICIN; ANTIINFECTIVE AGENT; QUINOLONE DERIVATIVE;

AREA UNDER THE CURVE; ARTICLE; ATYPICAL MYCOBACTERIOSIS; COLONY FORMING UNIT; CONTROLLED STUDY; DRUG EFFECT; DRUG EXPOSURE; DRUG HALF LIFE; DRUG TOLERANCE; HOLLOW FIBER SYSTEM MODEL; HUMAN; MAJOR CLINICAL STUDY; MONOTHERAPY; MYCOBACTERIUM KANSASII; NONBIOLOGICAL MODEL; OPTIMAL DRUG DOSE; PRIORITY JOURNAL; BACTERIAL COUNT; DOSE RESPONSE; DRUG EFFECTS; INSTRUMENT STERILIZATION; LUNG DISEASES; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS;

ANTI-BACTERIAL AGENTS; AREA UNDER CURVE; COLONY COUNT, MICROBIAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUOROQUINOLONES; LUNG DISEASES; MICROBIAL SENSITIVITY TESTS; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS; MYCOBACTERIUM KANSASII; RESERPINE; STERILIZATION;

EID: 84949115430     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.04441-14     Document Type: Article

References (42)

1. Corbett EL, Churchyard GJ, Hay M, Herselman P, Clayton T, Williams B, Hayes R, Mulder D, De Cock KM. 1999. The impact of HIV infection on Mycobacterium kansasii disease in South African gold miners. Am J Respir Crit Care Med 160:10-14. http://dx.doi.org/10.1164/ajrccm.160.1.9808052.
2. da Silva Telles MA, Chimara E, Ferrazoli L, Riley LW. 2005. Mycobacterium kansasii: antibiotic susceptibility and PCR-restriction analysis of clinical isolates. J Med Microbiol 54:975-979. http://dx.doi.org/10.1099/jmm.0.45965-0.
3. de Mello KG, Mello FC, Borga L, Rolla V, Duarte RS, Sampaio EP, Holland SM, Prevots DR, Dalcolmo MP. 2013. Clinical and therapeutic features of pulmonary nontuberculous mycobacterial disease, Brazil, 1993-2011. Emerg Infect Dis 19:393-399. http://dx.doi.org/10.3201/eid/1903.120735.
4. Griffith DE, Aksamit T, Brown-Elliott BA, Catanzaro A, Daley C, Gordin F, Holland SM, Horsburgh R, Huitt G, Iademarco MF, Iseman M, Olivier K, Ruoss S, von Reyn CF, Wallace RJ, Jr, Winthrop K. 2007. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 175: 367-416. http://dx.doi.org/10.1164/rccm.200604-571ST.
5. Horsburgh CR, Jr, Selik RM. 1989. The epidemiology of disseminated nontuberculous mycobacterial infection in the acquired immunodeficiency syndrome (AIDS). Am Rev Respir Dis 139:4-7. http://dx.doi.org/10.1164/ajrccm/139.1.4.
6. Shitrit D, Baum GL, Priess R, Lavy A, Shitrit AB, Raz M, Shlomi D, Daniele B, Kramer MR. 2006. Pulmonary Mycobacterium kansasii infection in Israel, 1999-2004: clinical features, drug susceptibility, and outcome. Chest 129:771-776. http://dx.doi.org/10.1378/chest.129.3.771.
7. Griffith DE. 2007. Therapy of nontuberculous mycobacterial disease. Curr Opin Infect Dis 20:198-203. http://dx.doi.org/10.1097/QCO.0b013e328055d9a2.
8. Guna R, Munoz C, Dominguez V, Garcia-Garcia A, Galvez J, de Julian-Ortiz JV, Borras R. 2005. In vitro activity of linezolid, clarithromycin and moxifloxacin against clinical isolates of Mycobacterium kansasii. J Antimicrob Chemother 55:950-953. http://dx.doi.org/10.1093/jac/dki111.
9. Pasipanodya J, Gumbo T. 2011. An oracle: antituberculosis pharmacokinetics-pharmacodynamics, clinical correlation, and clinical trial simulations to predict the future. Antimicrob Agents Chemother 55:24-34. http://dx.doi.org/10.1128/AAC.00749-10.
10. Smith MB, Molina CP, Schnadig VJ, Boyars MC, Aronson JF. 2003. Pathologic features of Mycobacterium kansasii infection in patients with acquired immunodeficiency syndrome. Arch Pathol Lab Med 127:554-560. http://dx.doi.org/10.1043/0003-9985(2003)127<0554:PFOMKI>2.0.CO;2.
11. Gumbo T, Louie A, Deziel MR, Parsons LM, Salfinger M, Drusano GL. 2004. Selection of a moxifloxacin dose that suppresses drug resistance in Mycobacterium tuberculosis, by use of an in vitro pharmacodynamic infection model and mathematical modeling. J Infect Dis 190:1642-1651. http://dx.doi.org/10.1086/424849.
12. Gumbo T, Louie A, Liu W, Brown D, Ambrose PG, Bhavnani SM, Drusano GL. 2007. Isoniazid bactericidal activity and resistance emergence: integrating pharmacodynamics and pharmacogenomics to predict efficacy in different ethnic populations. Antimicrob Agents Chemother 51:2329-2336. http://dx.doi.org/10.1128/AAC.00185-07.
13. Gumbo T, Louie A, Deziel MR, Liu W, Parsons LM, Salfinger M, Drusano GL. 2007. Concentration-dependent Mycobacterium tuberculosis killing and prevention of resistance by rifampin. Antimicrob Agents Chemother 51:3781-3788. http://dx.doi.org/10.1128/AAC.01533-06.
14. Gumbo T, Siyambalapitiyage Dona CS, Meek C, Leff R. 2009. Pharmacokinetics-pharmacodynamics of pyrazinamide in a novel in vitro model of tuberculosis for sterilizing effect: a paradigm for faster assessment of new antituberculosis drugs. Antimicrob Agents Chemother 53:3197-3204. http://dx.doi.org/10.1128/AAC.01681-08.
15. Srivastava S, Pasipanodya JG, Meek C, Leff R, Gumbo T. 2011. Multidrug-resistant tuberculosis not due to noncompliance but to betweenpatient pharmacokinetic variability. J Infect Dis 204:1951-1959. http://dx.doi.org/10.1093/infdis/jir658.
16. Pasipanodya JG, McIlleron H, Burger A, Wash PA, Smith P, Gumbo T. 2013. Serum drug concentrations predictive of pulmonary tuberculosis outcomes. J Infect Dis 208:1464-1473. http://dx.doi.org/10.1093/infdis/jit352.
17. Critical Path Institute. 2013. Voluntary exploration data submission to the FDA. Hollow fiber system model of tuberculosis. Critical Path Institute, Tucson, AZ.
18. Gumbo T, Louie A, Liu W, Ambrose PG, Bhavnani SM, Brown D, Drusano GL. 2007. Isoniazid's bactericidal activity ceases because of the emergence of resistance, not depletion of Mycobacterium tuberculosis in the log phase of growth. J Infect Dis 195:194-201. http://dx.doi.org/10.1086/510247.
19. Srivastava S, Musuka S, Sherman C, Meek C, Leff R, Gumbo T. 2010. Efflux-pump-derived multiple drug resistance to ethambutol monotherapy in Mycobacterium tuberculosis and the pharmacokinetics and pharmacodynamics of ethambutol. J Infect Dis 201:1225-1231. http://dx.doi.org/10.1086/651377.
20. Schmalstieg AM, Srivastava S, Belkaya S, Deshpande D, Meek C, Leff R, van Oers NS, Gumbo T. 2012. The antibiotic resistance arrow of time: efflux pump induction is a general first step in the evolution of mycobacterial drug resistance. Antimicrob Agents Chemother 56:4806-4815. http://dx.doi.org/10.1128/AAC.05546-11.
21. Palomino JC, Martin A, Camacho M, Guerra H, Swings J, Portaels F. 2002. Resazurin microtiter assay plate: simple and inexpensive method for detection of drug resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 46:2720-2722. http://dx.doi.org/10.1128/AAC.46.8.2720-2722.2002.
22. Deshpande D, Srivastava S, Meek C, Leff R, Gumbo T. 2010. Ethambutol optimal clinical dose and susceptibility breakpoint identification by use of a novel pharmacokinetic-pharmacodynamic model of disseminated intracellular Mycobacterium avium. Antimicrob Agents Chemother 54:1728-1733. http://dx.doi.org/10.1128/AAC.01355-09.
23. Deshpande D, Srivastava S, Meek C, Leff R, Hall GS, Gumbo T. 2010. Moxifloxacin pharmacokinetics/pharmacodynamics and optimal dose and susceptibility breakpoint identification for treatment of disseminated Mycobacterium avium infection. Antimicrob Agents Chemother 54:2534-2539. http://dx.doi.org/10.1128/AAC.01761-09.
24. Srivastava S, Gumbo T. 2011. In vitro and in vivo modeling of anti-tuberculosis drugs and its impact on optimization of doses and regimens. Curr Pharm Des 17:2881-2888. http://dx.doi.org/10.2174/138161211797470192.
25. D'Argenio DZ, Schumitzky A. 1997. ADAPT II. A program for simulation, identification, and optimal experimental design. User manual. Biomedical Simulations Resource. University of Southern California, Los Angeles, CA.
26. Corbett EL, Hay M, Churchyard GJ, Herselman P, Clayton T, Williams BG, Hayes R, Mulder D, De Cock KM. 1999. Mycobacterium kansasii and M. scrofulaceum isolates from HIV-negative South African gold miners: incidence, clinical significance and radiology. Int J Tuberc Lung Dis 3:501-507.
27. Zvada SP, Denti P, Sirgel FA, Chigutsa E, Hatherill M, Charalambous S, Mungofa S, Wiesner L, Simonsson US, Jindani A, Harrison T, McIlleron HM. 2014. Moxifloxacin population pharmacokinetics and model-based comparison of efficacy between moxifloxacin and ofloxacin in African patients. Antimicrob Agents Chemother 58:503-510. http://dx.doi.org/10.1128/AAC.01478-13.
28. Simon N, Sampol E, Albanese J, Martin C, Arvis P, Urien S, Lacarelle B, Bruguerolle B. 2003. Population pharmacokinetics of moxifloxacin in plasma and bronchial secretions in patients with severe bronchopneumo-nia. Clin Pharmacol Ther 74:353-363. http://dx.doi.org/10.1016/S0009-9236(03)00201-7.
29. Stass H, Dalhoff A, Kubitza D, Schuhly U. 1998. Pharmacokinetics, safety, and tolerability of ascending single doses of moxifloxacin, a new 8-methoxy quinolone, administered to healthy subjects. Antimicrob Agents Chemother 42:2060-2065.
30. Capitano B, Mattoes HM, Shore E, O'Brien A, Braman S, Sutherland C, Nicolau DP. 2004. Steady-state intrapulmonary concentrations of moxifloxacin, levofloxacin, and azithromycin in older adults. Chest 125:965-973. http://dx.doi.org/10.1378/chest.125.3.965.
31. Gumbo T. 2010. New susceptibility breakpoints for first-line antituberculosis drugs based on antimicrobial pharmacokinetic/pharmacodynamic science and population pharmacokinetic variability. Antimicrob Agents Chemother 54:1484-1491. http://dx.doi.org/10.1128/AAC.01474-09.
32. Pasipanodya JG, Gumbo T. 2011. A new evolutionary and pharmacokinetic-pharmacodynamic scenario for rapid emergence of resistance to single and multiple anti-tuberculosis drugs. Curr Opin Pharmacol 11:457-463. http://dx.doi.org/10.1016/j.coph.2011.07.001.
33. Ruslami R, Ganiem AR, Dian S, Apriani L, Achmad TH, van der Ven AJ, Borm G, Aarnoutse RE, van Crevel R. 2013. Intensified regimen containing rifampicin and moxifloxacin for tuberculous meningitis: an open-label, randomised controlled phase 2 trial. Lancet Infect Dis 13:27-35. http://dx.doi.org/10.1016/S1473-3099(12)70264-5.
34. Pranger AD, van Altena R, Aarnoutse RE, van Soolingen D, Uges DR, Kosterink JG, van der Werf TS, Alffenaar JW. 2011. Evaluation of moxifloxacin for the treatment of tuberculosis: 3 years of experience. Eur Respir J 38:888-894. http://dx.doi.org/10.1183/09031936.00176610.
35. Alffenaar JW, van Altena R, Bokkerink HJ, Luijckx GJ, van Soolingen D, Aarnoutse RE, van der Werf TS. 2009. Pharmacokinetics of moxifloxacin in cerebrospinal fluid and plasma in patients with tuberculous meningitis. Clin Infect Dis 49:1080-1082. http://dx.doi.org/10.1086/605576.
36. Williamson DA, Roberts SA, Bower JE, Vaughan R, Newton S, Lowe O, Lewis CA, Freeman JT. 2012. Clinical failures associated with rpoB mutations in phenotypically occult multidrug-resistant Mycobacterium tuberculosis. Int J Tuberc Lung Dis 16:216-220. http://dx.doi.org/10.5588/ijtld.11.0178.
37. van Ingen J, Aarnoutse R, de Vries G, Boeree MJ, van Soolingen D. 2011. Low-level rifampicin-resistant Mycobacterium tuberculosis strains raise a new therapeutic challenge. Int J Tuberc Lung Dis 15:990-992. http://dx.doi.org/10.5588/ijtld.10.0127.
38. Gumbo T, Chigutsa E, Pasipanodya J, Visser M, van Helden PD, Sirgel FA, McIlleron H. 2014. The pyrazinamide susceptibility breakpoint above which combination therapy fails. J Antimicrob Chemother 69: 2420-2425. http://dx.doi.org/10.1093/jac/dku136.
39. Gumbo T, Pasipanodya JG, Wash P, Burger A, McIlleron H. 2014. Redefining multidrug-resistant tuberculosis based on clinical response to combination therapy. Antimicrob Agents Chemother 58:6111-6115. http://dx.doi.org/10.1128/AAC.03549-14.
40. Ho J, Jelfs P, Sintchencko V. 2013. Phenotypically occult multidrugresistant Mycobacterium tuberculosis: dilemmas in diagnosis and treatment. J Antimicrob Chemother 68:2915-2920. http://dx.doi.org/10.1093/jac/dkt284.
41. Ocheretina O, Escuyer VE, Mabou MM, Royal-Mardi G, Collins S, Vilbrun SC, Pape JW, Fitzgerald DW. 2014. Correlation between genotypic and phenotypic testing for resistance to rifampin in Mycobacterium tuberculosis clinical isolates in Haiti: investigation of cases with discrepant susceptibility results. PLoS One 9:e90569. http://dx.doi.org/10.1371/journal.pone.0090569.
42. Christianson S, Voth D, Wolfe J, Sharma MK. 2014. Re-evaluation of the critical concentration for ethambutol antimicrobial sensitivity testing on the MGIT 960. PLoS One 9:e108911. http://dx.doi.org/10.1371/journal.pone.0108911.