Pulmonary drug delivery systems for tuberculosis treatment

International Journal of Pharmaceutics

Volumn 478, Issue 2, 2015, Pages 517-529

  Pham, Dinh Duy ^a,b,c   Fattal, Elias ^a   Tsapis, Nicolas ^a  

^a UNIV PARIS SUD   (France)

^b UNIVERSITY OF MEDICINE AND PHARMACY AT HO CHI MINH CITY   (Viet Nam)

^c TON DUC THANG UNIVERSITY   (Viet Nam)

Author keywords

Dry powders; Liposomes; Lung delivery; Nanoparticles; Tuberculosis

Indexed keywords

AMIKACIN; AMINOSALICYLIC ACID; BIOMATERIAL; CAPREOMYCIN; CYCLOSERINE; ETHAMBUTOL; ETHIONAMIDE; ISONIAZID; KANAMYCIN; LIPOSOME; MICROPARTICLE; NANOPARTICLE; PROTIONAMIDE; PYRAZINAMIDE; RIFAMPICIN; STREPTOMYCIN; TERIZIDONE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG; VIOMYCIN; POWDER;

CONTROLLED DRUG RELEASE; DRUG ADMINISTRATION ROUTE; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRY POWDER; HUMAN; LUNG ALVEOLUS MACROPHAGE; LUNG TUBERCULOSIS; MULTIDRUG RESISTANT TUBERCULOSIS; MYCOBACTERIUM; MYCOBACTERIUM AFRICANUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM CANETTI; MYCOBACTERIUM CAPRAE; MYCOBACTERIUM MICROTI; MYCOBACTERIUM MUNGI; MYCOBACTERIUM PINNIPEDII; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; REVIEW; ANIMAL; INHALATIONAL DRUG ADMINISTRATION; POWDER; TUBERCULOSIS, PULMONARY;

ADMINISTRATION, INHALATION; ANIMALS; ANTITUBERCULAR AGENTS; DRUG DELIVERY SYSTEMS; HUMANS; POWDERS; TUBERCULOSIS, PULMONARY;

EID: 84918500647     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2014.12.009     Document Type: Review

References (118)

1. The Global Plan to Stop TB, 2011. Transforming the Fight towards Elimination of Tuberculosis. World Health Organization Press, Geneva, Switzerland.
2. Anonymous, 2000. Diagnostic standards and classification of tuberculosis in adults and children. Am. J. Respir. Crit. Care Med. 161, 1376-1395.
3. Anonymous, 2012. Pharmacokinetics. In: Michelle Clark, A., Richard Finkel, Jose Rey Karen Whalen, A. (Eds.), Lippincott's Illustrated Reviews: Pharmacology. Pharmacology.
4. Anonymous, 2013. Core Curriculum on Tuberculosis: What the Clinician Should Know, sixth ed. Division of Tuberculosis Elimination - Centers for Disease Control and Prevention.
5. Abu-Dahab, R.M., Schafer, U.F., Lehr, C.M., 2001. Lectin-functionalized liposomes for pulmonary drug delivery: effect of nebulization on stability and bioadhesion. Eur. J. Pharm. Sci. 14, 37-46.
6. Agrawal, S., Singh, I., Kaur, K.J., Bhade, S.R., Kaul, C.L., Panchagnula, R., 2004. Comparative bioavailability of rifampicin, isoniazid and pyrazinamide from a four drug fixed dose combination with separate formulations at the same dose levels. Int. J. Pharm. 276, 41-49.
7. Ahmad, Z., Sharma, S., Khuller, G.K., 2005. Inhalable alginate nanoparticles as antitubercular drug carriers against experimental tuberculosis. Int. J. Antimicrob. Agents 26, 298-303.
8. Al-Hallak, M.H., Sarfraz, M.K., Azarmi, S., Roa, W.H., Finlay, W.H., Lobenberg, R., 2011. Pulmonary delivery of inhalable nanoparticles: dry powder inhalers. Ther. Deliv. 2, 1313-1324.
9. Kundawala, J.A., Patel, A.V., Patel, V.H., Choudhary, D., 2011. Influence of formulation components on aerosolization properties of isoniazid loaded chitosan microspheres. Int. J. Pharm. Sci. Drug Res. 3, 297-302.
10. Kundawala, A.J., Patel, V.A., Patel, H.V., Choudhary, D., 2012. Treating tuberculosis with chitosan microparticles loaded with rifampicin as respirable powder for pulmonary delivery Indian. J. Novel Drug Deliv. 4, 57-65.
11. Andrade, F., Rafael, D., Videira, M., Ferreira, D., Sosnik, A., Sarmento, B., 2013. Nanotechnology and pulmonary delivery to overcome resistance in infectious diseases. Adv. Drug Deliv. Rev. 65, 1816-1827.
12. Ashford, D.A., Whitney, E., Raghunathan, P., Cosivi, O., 2001. Epidemiology of selected mycobacteria that infect humans and other animals. Rev. Sci. Tech. 20, 325-337.
13. Barrow, E.L., Winchester, G.A., Staas, J.K., Quenelle, D.C., Barrow, W.W., 1998. Use of microsphere technology for targeted delivery of rifampin to Mycobacterium tuberculosis-infected macrophages. Antimicrob. Agents Chemother. 42, 2682-2689.
14. Biggs, D.L., Lengsfeld, C.S., Hybertson, B.M., Ng, K.Y., Manning, M.C., Randolph, T.W., 2003. In vitro and in vivo evaluation of the effects of PLA microparticle crystallinity on cellular response. J. Controlled Release 92, 147-161.
15. Blomberg, B., Spinaci, S., Fourie, B., Laing, R., 2001. The rationale for recommending fixed-dose combination tablets for treatment of tuberculosis. Bull. World Health Organ. 79, 61-68.
16. Blumberg, H.M., Burman, W.J., Chaisson, R.E., Daley, C.L., Etkind, S.C., Friedman, L.N., Fujiwara, P., Grzemska, M., Hopewell, P.C., Iseman, M.D., Jasmer, R.M., Koppaka, V., Menzies, R.I., O'Brien, R.J., Reves, R.R., Reichman, L.B., Simone, P.M., Starke, J. R., Vernon, A.A., 2003. American Thoracic Society/Centers for Disease Control and Prevention/Infectious Diseases Society of America: treatment of tuberculosis. Am. J. Respir. Crit. Care Med. 167, 603-662.
17. Bosquillon, C., Lombry, C., Preat, V., Vanbever, R., 2001. Influence of formulation excipients and physical characteristics of inhalation dry powders on their aerosolization performance. J. Controlled Release 70, 329-339.
18. Canonico, A.E., Plitman, J.D., Conary, J.T., Meyrick, B.O., Brigham, K.L., 1994. No lung toxicity after repeated aerosol or intravenous delivery of plasmid-cationic liposome complexes. J. Appl. Physiol. (1985) 77, 415-419.
19. Chaisson, R.E., Schecter, G.F., Theuer, C.P., Rutherford, G.W., Echenberg, D.F., Hopewell, P.C., 1987. Tuberculosis in patients with the acquired immunodeficiency syndrome. Clinical features response to therapy, and survival. Am. Rev. Respir. Dis. 136, 570-574.
20. Chan, J.G.Y., Chan, H.K., Prestidge, C.A., Denman, J.A., Young, P.M., Traini, D., 2013. A novel dry powder inhalable formulation incorporating three first-line antitubercular antibiotics. Eur. J. Pharm. Biopharm. 83, 285-292.
21. Changsan, N., Chan, H.K., Separovic, F., Srichana, T., 2009a. Physicochemical characterization and stability of rifampicin liposome dry powder formulations for inhalation. J. Pharm. Sci. 98, 628-639.
22. Changsan, N., Nilkaeo, A., Pungrassami, P., Srichana, T., 2009b. Monitoring safety of liposomes containing rifampicin on respiratory cell lines and in vitro efficacy against Mycobacterium bovis in alveolar macrophages. J. Drug Target. 17, 751-762.
23. Chimote, G., Banerjee, R., 2010. In vitro evaluation of inhalable isoniazid-loaded surfactant liposomes as an adjunct therapy in pulmonary tuberculosis. J. Biomed. Mater. Res. B Appl. Biomater. 94, 1-10.
24. Colombo, P., Traini, D., Buttini, F., 2013. Inhalation drug delivery. Wiley-Blackwell.
25. Condos, R., Rom, W.N., Schluger, N.W., 1997. Treatment of multidrug-resistant pulmonary tuberculosis with interferon-gamma via aerosol. Lancet 349, 1513-1515.
26. Conte Jr., J.E., Golden, J.A., McQuitty, M., Kipps, J., Duncan, S., McKenna, E., Zurlinden, E., 2002. Effects of gender, AIDS, and acetylator status on intrapulmonary concentrations of isoniazid. Antimicrob. Agents Chemother. 46, 2358-2364.
27. Coowanitwong, I., Arya, V., Kulvanich, P., Hochhaus, G., 2008. Slow release formulations of inhaled rifampin. AAPS J. 10, 342-348.
28. Cosgrove, B.D., Cheng, C., Pritchard, J.R., Stolz, D.B., Lauffenburger, D.A., Griffith, L. G., 2008. An inducible autocrine cascade regulates rat hepatocyte proliferation and apoptosis responses to tumor necrosis factor-alpha. Hepatology 48, 276-288.
29. Daniel, T.M., Bates, J.H., Downes, K.A., 1994. Tuberculosis: Pathogenesis, protection and control. In: Bloom, B.R. (Ed.), History of Tuberculosis. ASM Press, Washington, DC, pp. 13-24.
30. Daniher, D.I., Zhu, J., 2008. Dry powder platform for pulmonary drug delivery. Particuology 6, 225-238.
31. Dannenberg Jr., A.M., 1993. Immunopathogenesis of pulmonary tuberculosis. Hosp. Pract. (Off. Ed.) 28, 51-58.
32. Deol, P., Khuller, G.K., Joshi, K., 1997. Therapeutic efficacies of isoniazid and rifampin encapsulated in lung-specific stealth liposomes against Mycobacterium tuberculosis infection induced in mice. Antimicrob. Agents Chemother. 41, 1211-1214.
33. du Toit, L.C., Pillay, V., Danckwerts, M.P., 2006. Tuberculosis chemotherapy: current drug delivery approaches. Respir. Res. 7, 118.
34. Dye, C., Hosseini, M., Watt, C., 2007. Did we reach the 2005 targets for tuberculosis control? Bull. World Health Organ. 85, 364-369.
35. Edwards, D.A., Hanes, J., Caponetti, G., Hrkach, J., Ben-Jebria, A., Eskew, M.L., Mintzes, J., Deaver, D., Lotan, N., Langer, R., 1997. Large porous particles for pulmonary drug delivery. Science 276, 1868-1871.
36. Fiegel, J., Garcia-Contreras, L., Thomas, M., VerBerkmoes, J., Elbert, K., Hickey, A., Edwards, D., 2008. Preparation and in vivo evaluation of a dry powder for inhalation of capreomycin. Pharm. Res. 25, 805-811.
37. Frijlink, H.W., De Boer, A.H., 2004. Dry powder inhalers for pulmonary drug delivery. Expert Opin. Drug Deliv. 1, 67-86.
38. Garcia-Contreras, L., Fiegel, J., Telko, M.J., Elbert, K., Hawi, A., Thomas, M., VerBerkmoes, J., Germishuizen, W.A., Fourie, P.B., Hickey, A.J., Edwards, D., 2007a. Inhaled large porous particles of capreomycin for treatment of tuberculosis in a guinea pig model. Antimicrob. Agents Chemother. 51, 2830-2836.
39. Garcia-Contreras, L., Fiegel, J., Telko, M.J., Elbert, K., Hawi, A., Thomas, M., VerBerkmoes, J., Germishuizen, W.A., Fourie, P.B., Hickey, A.J., Edwards, D., 2007b. Inhaled large porous particles of capreomycin for treatment of tuberculosis in a guinea pig model. Antimicrob. Agents Chemother. 51, 2830-2836.
40. Garcia-Contreras, L., Sung, J.C., Muttil, P., Padilla, D., Telko, M., Verberkmoes, J.L., Elbert, K.J., Hickey, A.J., Edwards, D.A., 2010. Dry powder PA-824 aerosols for treatment of tuberculosis in guinea pigs. Antimicrob. Agents Chemother. 54, 1436-1442.
41. Grosset, J.H., Singer, T.G., Bishai, W.R., 2012. New drugs for the treatment of tuberculosis: hope and reality. Int. J. Tuberc. Lung Dis. 16, 1005-1014.
42. Hanif, S.N.M., Garcia-Contreras, L., 2012. Pharmaceutical Aerosols for the Treatment and Prevention of Tuberculosis. Frontiers in Cellular and Infection Microbiology 2.
43. Heyder, J., Gebhart, J., Rudolf, G., Schiller, C.F., Stahlhofen, W., 1986. Deposition of particles in the human respiratory tract in the size range 0.005-15 μm. J. Aerosol Sci. 17, 811-825.
44. Hinds, W.C., 1999. Aerosol Technology: Properties, Behavior, and Measurement of Airborne Particles, second ed. John Wiey & Sons, Inc., Canada.
45. Hirota, K., Hasegawa, T., Nakajima, T., Inagawa, H., Kohchi, C., Soma, G., Makino, K., Terada, H., 2010. Delivery of rifampicin-PLGA microspheres into alveolar macrophages is promising for treatment of tuberculosis. J. Controlled Release 142, 339-346.
46. Hopewell, P., 1994. Tuberculosis: pathogenesis, protection and control. In: Bloom, B. R. (Ed.), Overview of Clinical Tuberculosis. ASM Press, Washington, DC, pp. 25-46.
47. Inderlied, C.B., Salfinger, M., 1999. Antimycobacterial agents, susceptibility test methods, In: Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C., Yolken, R. (Eds.), Manual of Clinical Microbiology. tenth ed. ASM Press, Washington, DC, pp. 1601-1623.
48. Iseman, M.D., 1993. Treatment of multidrug-resistant tuberculosis. N. Engl. J. Med. 329, 784-791.
49. Justo, O.R., Moraes, A.M., 2003. Incorporation of antibiotics in liposomes designed for tuberculosis therapy by inhalation. Drug Deliv. 10, 201-207.
50. Kanchan, V., Panda, A.K., 2007. Interactions of antigen-loaded polylactide particles with macrophages and their correlation with the immune response. Biomaterials 28, 5344-5357.
51. Koh, W.J., Kwon, O.J., Suh, G.Y., Chung, M.P., Kim, H., Lee, N.Y., Kim, T.S., Lee, K.S., 2004. Six-month therapy with aerosolized interferon-gamma for refractory multidrug-resistant pulmonary tuberculosis. J. Korean Med. Sci. 19, 167-171.
52. Kolyva, A.S., Karakousis, P.C., 2012. Old and new TB drugs: mechanisms of action and resistance. In: Cardona, D.P.-J. (Ed.), Understanding Tuberculosis-New Approaches to Fighting Against Drug Resistance. InTech, Baltimore, MD, U. S. A, pp. 209-232.
53. Kurunov Iu, N., Ursov, I.G., Krasnov, V.A., Petrenko, T.I., Iakovchenko, N.N., Svistelnik, A.V., Filimonov, P.A., 1995. Effectiveness of liposomal antibacterial drugs in the inhalation therapy of experimental tuberculosis. Probl. Tuberk. 38-40.
54. Lauzardo, M., Peloquin, C.A., 2012. Antituberculosis therapy for 2012 and beyond. Expert Opin. Pharmacother 13, 511-526.
55. Lienhardt, C., Vernon, A., Raviglione, M.C., 2010. New drugs and new regimens for the treatment of tuberculosis: review of the drug development pipeline and implications for national programmes. Curr. Opin. Pulm. Med. 16, 186-193.
56. Loira-Pastoriza, C., Todoroff, J., Vanbever, R., 2014. Delivery strategies for sustained drug release in the lungs. Adv. Drug Deliv. Rev. 75, 81-91.
57. Maherani, B., Arab-Tehrany, E., Mozafari, M.R., Gaiani, C., Linder, M., 2011. Liposomes: a review of manufacturing techniques and targeting strategies. Curr. Nanosci. 7, 436-452.
58. Makino, K., Nakajima, T., Shikamura, M., Ito, F., Ando, S., Kochi, C., Inagawa, H., Soma, G., Terada, H., 2004. Efficient intracellular delivery of rifampicin to alveolar macrophages using rifampicin-loaded PLGA microspheres: effects of molecular weight and composition of PLGA on release of rifampicin. Colloids Surf. B Biointerfaces 36, 35-42.
59. Mehanna, M.M., Mohyeldin, S.M., Elgindy, N.A., 2014. Respirable nanocarriers as a promising strategy for antitubercular drug delivery. J. Controlled Release 187, 183-197.
60. Misra, A., Jinturkar, K., Patel, D., Lalani, J., Chougule, M., 2009. Recent advances in liposomal dry powder formulations: preparation and evaluation. Expert Opin. Drug Deliv. 6, 71-89.
61. Muttil, P., Kaur, J., Kumar, K., Yadav, A.B., Sharma, R., Misra, A., 2007. Inhalable microparticles containing large payload of anti-tuberculosis drugs. Eur. J. Pharm. Sci. 32, 140-150.
62. Muttil, P., Wang, C., Hickey, A.J., 2009. Inhaled drug delivery for tuberculosis therapy. Pharm. Res. 26, 2401-2416.
63. Nardell, E.A., 1993. Lung Biology in Health and Disease. In: Reichman, L.B., Herschfield, E. (Eds.), Pathogenesis of tuberculosis. Marcel Dekker, New York, USA, pp. 103-123.
64. Niven, R.W., 1995. Delivery of biotherapeutics by inhalation aerosol. Crit. Rev. Ther. Drug Carrier Syst. 12, 151-231.
65. O'Hara, P., Hickey, A.J., 2000. Respirable PLGA microspheres containing rifampicin for the treatment of tuberculosis: manufacture and characterization. Pharm. Res. 17, 955-961.
66. Ohashi, K., Kabasawa, T., Ozeki, T., Okada, H., 2009. One-step preparation of rifampicin/poly(lactic-co-glycolic acid) nanoparticle-containing mannitol microspheres using a four-fluid nozzle spray drier for inhalation therapy of tuberculosis. J. Controlled Release 135, 19-24.
67. Panchal, R., Patel, H., Patel, V., Joshi, P., Parikh, A., 2012. Formulation and evalution of montelukast sodium - chitosan based spray dried microspheres for pulmonary drug delivery. J. Pharm. Bioall. Sci. 4, S110-111.
68. Pandey, R., Khuller, G.K., 2004. Polymer based drug delivery systems for mycobacterial infections. Curr. Drug Deliv. 1, 195-201.
69. Pandey, R., Khuller, G.K., 2005a. Antitubercular inhaled therapy: opportunities, progress and challenges. J. Antimicrob. Chemother. 55, 430-435.
70. Pandey, R., Khuller, G.K., 2005b. Solid lipid particle-based inhalable sustained drug delivery system against experimental tuberculosis. Tuberculosis 85, 227-234.
71. Pandey, R., Sharma, A., Zahoor, A., Sharma, S., Khuller, G.K., Prasad, B., 2003a. Poly (DL-lactide-co-glycolide) nanoparticle-based inhalable sustained drug delivery system for experimental tuberculosis. J. Antimicrob. Chemother. 52, 981-986.
72. Pandey, R., Sharma, S., Khuller, G.K., 2004. Nebulization of liposome encapsulated antitubercular drugs in guinea pigs. Int. J. Antimicrob. Agents 24, 93-94.
73. Pandey, R., Zahoor, A., Sharma, S., Khuller, G.K., 2003b. Nanoparticle encapsulated antitubercular drugs as a potential oral drug delivery system against murine tuberculosis. Tuberculosis (Edinb.) 83, 373-378.
74. Patomchaiviwat, V., Paeratakul, O., Kulvanich, P., 2008. Formation of inhalable rifampicin-poly(L-lactide) microparticles by supercritical anti-solvent process. AAPS PharmSciTech 9, 1119-1129.
75. Pham, D.D., Fattal, E., Ghermani, N., Guiblin, N., Tsapis, N., 2013. Formulation of pyrazinamide-loaded large porous particles for the pulmonary route: avoiding crystal growth using excipients. Int. J. Pharm. 454, 668-677.
76. Prabakaran, D., Singh, P., Jaganathan, K.S., Vyas, S.P., 2004. Osmotically regulated asymmetric capsular systems for simultaneous sustained delivery of antitubercular drugs. J. Controlled Release 95, 239-248.
77. Rojanarat, W., Changsan, N., Tawithong, E., Pinsuwan, S., Chan, H.K., Srichana, T., 2011. Isoniazid proliposome powders for inhalation-preparation, characterization and cell culture studies. Int. J. Mol. Sci. 12, 4414-4434.
78. Rojanarat, W., Nakpheng, T., Thawithong, E., Yanyium, N., Srichana, T., 2012a. Inhaled pyrazinamide proliposome for targeting alveolar macrophages. Drug Deliv. 19, 334-345.
79. Rojanarat, W., Nakpheng, T., Thawithong, E., Yanyium, N., Srichana, T., 2012b. Levofloxacin-proliposomes: opportunities for use in lung tuberculosis. Pharmaceutics 4, 385-412.
80. Rubinstein, E., Keynan, Y., 2013. Quinolones for mycobacterial infections. Int. J. Antimicrob. Agents 42, 1-4.
81. Saari, M., Vidgren, M.T., Koskinen, M.O., Turjanmaa, V.M., Nieminen, M.M., 1999. Pulmonary distribution and clearance of two beclomethasone liposome formulations in healthy volunteers. Int. J. Pharm. 181, 1-9.
82. Sacks, L.V., Pendle, S., Orlovic, D., Andre, M., Popara, M., Moore, G., Thonell, L., Hurwitz, S., 2001. Adjunctive salvage therapy with inhaled aminoglycosides for patients with persistent smear-positive pulmonary tuberculosis. Clin. Infect. Dis. 32, 44-49.
83. Schmitt, E., Meuret, G., Stix, L., 1977. Monocyte recruitment in tuberculosis and sarcoidosis. Br. J. Haematol. 35, 11-17.
84. Schoubben, A., Blasi, P., Marenzoni, M.L., Barberini, L., Giovagnoli, S., Cirotto, C., Ricci, M., 2013. Capreomycin supergenerics for pulmonary tuberculosis in vitro, and in vivo characterization. Eur. J. Pharm. Biopharm. 83, 388-395.
85. Sethuraman, V.V., Hickey, A.J., 2002. Powder properties and their influence on dry powder inhaler delivery of an antitubercular drug. AAPS PharmSciTech 3, E28.
86. Shah, S.P., Misra, A., 2004. Liposomal amikacin dry powder inhaler: effect of fines on in vitro performance. AAPS PharmSciTech 5, e65.
87. Sharma, A., Sharma, S., Khuller, G.K., 2004. Lectin-functionalized poly(lactide-co-glycolide) nanoparticles as oral/aerosolized antitubercular drug carriers for treatment of tuberculosis. J. Antimicrob. Chemother. 54, 761-766.
88. Sharma, R., Muttil, P., Yadav, A.B., Rath, S.K., Bajpai, V.K., Mani, U., Misra, A., 2007. Uptake of inhalable microparticles affects defence responses of macrophages infected with Mycobacterium tuberculosis H37Ra. J. Antimicrob. Chemother. 59, 499-506.
89. Sharma, R., Saxena, D., Dwivedi, A.K., Misra, A., 2001. Inhalable microparticles containing drug combinations to target alveolar macrophages for treatment of pulmonary tuberculosis. Pharm. Res. 18, 1405-1410.
90. Sawatdee, S., Worakul, N., Srichana, T., 2006. Preparation of isoniazid as dry powder formulations for inhalation by physical mixing and spray drying. Malays. J. Pharm. Sci. 4, 43-63.
91. Somoskovi, A., Wade, M.M., Sun, Z., Zhang, Y., 2004. Iron enhances the antituberculous activity of pyrazinamide. J. Antimicrob. Chemother. 53, 192-196.
92. Suarez, S., O'Hara, P., Kazantseva, M., Newcomer, C.E., Hopfer, R., McMurray, D.N., Hickey, A.J., 2001a. Airways delivery of rifampicin microparticles for the treatment of tuberculosis. J. Antimicrob. Chemother. 48, 431-434.
93. Suarez, S., O'Hara, P., Kazantseva, M., Newcomer, C.E., Hopfer, R., McMurray, D.N., Hickey, A.J., 2001b. Respirable PLGA microspheres containing rifampicin for the treatment of tuberculosis: screening in an infectious disease model. Pharm. Res. 18, 1315-1319.
94. Sung, J.C., Garcia-Contreras, L., VerBerkmoes, J.L., Peloquin, C.A., Elbert, K.J., Hickey, A.J., Edwards, D.A., 2009a. Dry powder nitroimidazopyran antibiotic PA-824 aerosol for inhalation. Antimicrob. Agents Chemother. 53, 1338-1343.
95. Sung, J.C., Padilla, D.J., Garcia-Contreras, L., Verberkmoes, J.L., Durbin, D., Peloquin, C. A., Elbert, K.J., Hickey, A.J., Edwards, D.A., 2009b. Formulation and pharmacokinetics of self-assembled rifampicin nanoparticle systems for pulmonary delivery. Pharm. Res. 26, 1847-1855.
96. Sung, J.C., Pulliam, B.L., Edwards, D.A., 2007. Nanoparticles for drug delivery to the lungs. Trends Biotechnol. 25, 563-570.
97. Taylor, K.M.G., Fan, S.J., 1993. Liposomes for drug delivery to the respiratory tract. Drug Dev. Ind. Pharm. 19, 123-142.
98. Thomas, D.A., Myers, M.A., Wichert, B., Schreier, H., Gonzalez-Rothi, R.J., 1991. Acute effects of liposome aerosol inhalation on pulmonary function in healthy human volunteers. Chest 99, 1268-1270.
99. Tomoda, K., Makino, K., 2007. Effects of lung surfactants on rifampicin release rate from monodisperse rifampicin-loaded PLGA microspheres. Colloids Surf. B Biointerfaces 55, 115-124.
100. Tsapis, N., Bennett, D., Jackson, B., Weitz, D.A., Edwards, D.A., 2002. Trojan particles: large porous carriers of nanoparticles for drug delivery. Proc. Natl. Acad. Sci. U. S. A. 99, 12001-12005.
101. Tsapis, N., Bennett, D., O'Driscoll, K., Shea, K., Lipp, M.M., Fu, K., Clarke, R.W., Deaver, D., Yamins, D., Wright, J., Peloquin, C.A., Weitz, D.A., Edwards, D.A., 2003. Direct lung delivery of para-aminosalicylic acid by aerosol particles. Tuberculosis (Edinb.) 83, 379-385.
102. Turner, P.V., Brabb, T., Pekow, C., Vasbinder, M.A., 2011. Administration of substances to laboratory animals: routes of administration and factors to consider. J. Am. Assoc. Lab. Anim. Sci. 50, 600-613.
103. Ulrichs, T., Kaufmann, S.H., 2006. New insights into the function of granulomas in human tuberculosis. J. Pathol. 208, 261-269.
104. Vadakkan, M.V., Annapoorna, K., Sivakumar, K.C., Mundayoor, S., Kumar, G.S., 2013. Dry powder cationic lipopolymeric nanomicelle inhalation for targeted delivery of antitubercular drug to alveolar macrophage. Int. J. Nanomed. 8, 2871-2885.
105. Vanbever, R., Ben-Jebria, A., Mintzes, J.D., Langer, R., Edwards, D.A., 1999a. Sustained release of insulin from insoluble inhaled particles. Drug Dev. Res. 48, 178-185.
106. Vanbever, R., Mintzes, J.D., Wang, J., Nice, J., Chen, D.H., Batycky, R., Langer, R., Edwards, D.A., 1999b. Formulation and physical characterization of large porous particles for inhalation. Pharm. Res.-Dordr. 16, 1735-1742.
107. Verma, R.K., Kaur, J., Kumar, K., Yadav, A.B., Misra, A., 2008. Intracellular time course, pharmacokinetics, and biodistribution of isoniazid and rifabutin following pulmonary delivery of inhalable microparticles to mice. Antimicrob. Agents Chemother. 52, 3195-3201.
108. Vyas, S.P., Kannan, M.E., Jain, S., Mishra, V., Singh, P., 2004. Design of liposomal aerosols for improved delivery of rifampicin to alveolar macrophages. Int. J. Pharm. 269, 37-49.
109. Weers, J., Tarara, T., Tzannis, S., 2005. Lipid formulations for spontaneous drug encapsulation. Google Patents.
110. WHO, 2011. Global Tuberculosis Control.
111. WHO, 2012. Global tuberculosis control: WHO report. Aust. N. Z. J. Public Health 36, 497-498.
112. WHO, 2013. Global Tuberculosis Report 2013. Geneva, Switzerland.
113. Wijagkanalan, W., Higuchi, Y., Kawakami, S., Teshima, M., Sasaki, H., Hashida, M., 2008. Enhanced anti-inflammation of inhaled dexamethasone palmitate using mannosylated liposomes in an endotoxin-induced lung inflammation model. Mol. Pharmacol. 74, 1183-1192.
114. Willis, L., Hayes Jr., D., Mansour, H.M., 2012. Therapeutic liposomal dry powder inhalation aerosols for targeted lung delivery. Lung 190, 251-262.
115. Yadav, A.B., Sharma, R., Muttil, P., Singh, A.K., Verma, R.K., Mohan, M., Patel, S.K., Misra, A., 2009. Inhalable microparticles containing isoniazid and rifabutin target macrophages and 'stimulate the phagocyte' to achieve high efficacy. Indian J. Exp. Biol. 47, 469-474.
116. Yoshida, A., Matumoto, M., Hshizume, H., Oba, Y., Tomishige, T., Inagawa, H., Kohchi, C., Hino, M., Ito, F., Tomoda, K., Nakajima, T., Makino, K., Terada, H., Hori, H., Soma, G., 2006. Selective delivery of rifampicin incorporated into poly(DL-lactic-co-glycolic) acid microspheres after phagocytotic uptake by alveolar macrophages, and the killing effect against intracellular Mycobacterium bovis Calmette-Guerin. Microbes Infect. 8, 2484-2491.
117. Zhang, L., Pornpattananangku, D., Hu, C.M., Huang, C.M., 2010. Development of nanoparticles for antimicrobial drug delivery. Curr. Med. Chem. 17, 585-594.
118. Zhou, H., Zhang, Y., Biggs, D.L., Manning, M.C., Randolph, T.W., Christians, U., Hybertson, B.M., Ng, K.Y., 2005. Microparticle-based lung delivery of INH decreases INH metabolism and targets alveolar macrophages. J. Controlled Release 107, 288-299.