Anti-Tuberculosis Bacteriophage D29 Delivery with a Vibrating Mesh Nebulizer, Jet Nebulizer, and Soft Mist Inhaler

Pharmaceutical Research

Volumn 34, Issue 10, 2017, Pages 2084-2096

  Carrigy, Nicholas B ^a   Chang, Rachel Y ^b   Leung, Sharon S Y ^b   Harrison, Melissa ^a   Petrova, Zaritza ^c   Pope, Welkin H ^c   Hatfull, Graham F ^c   Britton, Warwick J ^b   Chan, Hak Kim ^b   Sauvageau, Dominic ^a   Finlay, Warren H ^a   Vehring, Reinhard ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

aerosol; Mycobacterium tuberculosis; nebulization; phage therapy; titer reduction

Indexed keywords

BACTERIOPHAGE D29; SODIUM CHLORIDE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG;

AEROSOL; ARTICLE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; INHALATION; JET NEBULIZER; MYCOBACTERIUM SMEGMATIS; NEBULIZATION; NEBULIZER; NONHUMAN; PHAGE THERAPY; PRIORITY JOURNAL; SOFT MIST INHALER; VIBRATING MESH NEBULIZER; ANIMAL; BACTERIOPHAGE; CHEMISTRY; DEVICES; DRUG RELEASE; DRUG STABILITY; EQUIPMENT DESIGN; HUMAN; INHALATIONAL DRUG ADMINISTRATION; PROCEDURES; TUBERCULOSIS;

ADMINISTRATION, INHALATION; AEROSOLS; ANIMALS; BACTERIOPHAGES; DRUG LIBERATION; DRUG STABILITY; EQUIPMENT AND SUPPLIES; EQUIPMENT DESIGN; HUMANS; NEBULIZERS AND VAPORIZERS; PHAGE THERAPY; TUBERCULOSIS;

EID: 85021238425     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-017-2213-4     Document Type: Article

References (48)

1. Ventola CL. The antibiotic resistance crisis. Part 1: causes and threats. PT. 2015;40(4):277–83.
2. World Health Organization. Multidrug-resistant tuberculosis (MDR-TB): 2016 Update. 2016 Available from: http://www.who.int/tb/challenges/mdr/mdr_tb_factsheet.pdf. Accessed 21 Feb 2017.
3. Udwadia ZF, Amale RA, Ajbani KK, Rodrigues C. Totally drug-resistant tuberculosis in India. Clin Infect Dis. 2012;54(4):579–81.
4. World Health Organization. Drug-resistant TB: Totally drug-resistant TB FAQ. 2017 Available from: http://www.who.int/tb/areas-of-work/drug-resistant-tb/totally-drug-resistant-tb-faq/en/. Accessed 21 Feb 2017.
5. Abedon ST, Kuhl SJ, Blasdel BG, Kutter EM. Phage treatment of human infections. Bacteriophage. 2011;1(2):66–85.
6. Kutateladze M, Adamia R. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol. 2010;28(12):591–5.
7. Verbeken G, Huys I, Pirnay J-P, Jennes S, Chanishvili N, Scheres J, et al. Taking bacteriophage therapy seriously: a moral argument. Biomed Res Int. 2014;2014:621316.
8. Hatfull GF, Vehring R. Respirable bacteriophage aerosols for the prevention and treatment of tuberculosis. In: Hickey AJ, Misra A, Fourie PB, editors. Drug delivery systems for tuberculosis prevention and treatment. Chichester: John Wiley & Sons, Ltd.; 2016. p. 277–92.
9. Loc-Carrillo C, Abedon ST. Pros and cons of phage therapy. Bacteriophage. 2011;1(2):111–4.
10. Kutter E, Sulakvelidze A. Bacteriophages: biology and applications. Boca Raton: CRC Press; 2005.
11. Hoe S, Semler DD, Goudie AD, Lynch KH, Matinkhoo S, Finlay WH, et al. Respirable bacteriophages for the treatment of bacterial lung infections. J Aerosol Med Pulm Drug Deliv. 2013;26(6):317–35.
12. Kutter E, de Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, et al. Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol. 2010;11(1):69–86.
13. Hoe S, Boraey MA, Ivey JW, Finlay WH, Vehring R. Manufacturing and device options for the delivery of biotherapeutics. J Aerosol Med Pulm Drug Deliv. 2014;27(5):315–28.
14. Golshahi L, Seed KD, Dennis JJ, Finlay WH. Toward modern inhalational bacteriophage therapy: nebulization of bacteriophages of Burkholderia cepacia complex. J Aerosol Med Pulm Drug Deliv. 2008;21(4):351–60.
15. Matinkhoo S, Lynch KH, Dennis JJ, Finlay WH, Vehring R. Spray-dried respirable powders containing bacteriophages for the treatment of pulmonary infections. J Pharm Sci. 2011;100(12):5197–205.
16. Leung SY, Parumasivam T, Gao FG, Carrigy NB, Vehring R, Finlay WH, et al. Production of inhalation phage powders using spray freeze drying and spray drying techniques for treatment of respiratory infections. Pharm Res. 2016;33(6):1486–96.
17. Golshahi L, Lynch KH, Dennis JJ, Finlay WH. In vitro lung delivery of bacteriophages KS4-M and ɸKZ using dry powder inhalers for treatment of Burkholderia cepacia complex and Pseudomonas Aeruginosa infections in cystic fibrosis. J Appl Microbiol. 2011;110(1):106–17.
18. Parracho HMRT, Burrowes BH, Enright MC, McConville ML, Harper DR. The role of regulated clinical trials in the development of bacteriophage therapeutics. J Mol Genet Med. 2012;6:279–86.
19. Verbeken G, Pirnay J-P, de Vos D, Jennes S, Zizi M, Lavigne R, et al. Optimizing the European regulatory framework for sustainable bacteriophage therapy in human medicine. Arch Immunol Ther Exp. 2012;60(3):161–72.
20. Abedon ST. Phage therapy of pulmonary infections. Bacteriophage. 2015;5(1):1–13.
21. Semler DD, Goudie AD, Finlay WH, Dennis JJ. Aerosol phage therapy efficacy in Burkholderia cepacia complex respiratory infections. Antimicrob Agents Chemother. 2014;58(7):4005–13.
22. Liu K-Y, Yang W-H, Dong X-K, Cong L-M, Li N, Li Y, et al. Inhalation study of mycobacteriophage D29 aerosol for mice by endotracheal route and nose-only exposure. J Aerosol Med Pulm Drug Deliv. 2016;29(5):393–405.
23. Cooper CJ, Denyer SP, Maillard J-Y. Stability and purity of a bacteriophage cocktail preparation for nebulizer delivery. Lett Appl Microbiol. 2013;58(2):118–22.
24. Sahota JS, Smith CM, Radhakrishnan P, Winstanley C, Goderdzishvili M, Chanishvili N, et al. Bacteriophage delivery by nebulization and efficacy against phenotypically diverse Pseudomonas Aeruginosa from cystic fibrosis patients. J Aerosol Med Pulm Drug Deliv. 2015;28(5):353–60.
25. Froman S, Will DW, Bogen E. Bacteriophage active against virulent mycobacterium tuberculosis I. Isolation and activity. Am J Public Health Nations Health. 1954;44(10):1326–33.
26. phagesDB.org. Phage hunting procedure & protocols. 2016 December 2. Available from: phagesdb.org/workflow/.
27. Engel M, Heinrichs S. Use of tiotropium salts in the treatment of moderate persistent asthma. 2015. Patent US 20150224090 A1.
28. Dalby R, Spallek M, Voshaar T. A review of the development of Respimat soft mist inhaler. Int J Pharm. 2004;283(1–2):1–9.
29. Dalby R, Eicher J, Zierenberg B. Development of Respimat® Soft Mist™ Inhaler and its clinical utility in respiratory disorders. Med Devices (Auckl). 2011;4:145–55.
30. Finlay WH. The mechanics of inhaled pharmaceutical aerosols: an introduction. San Diego: Academic Press; 2001.
31. Fink JB. New technology offers new opportunities: continuous bronchodilator therapy during mechanical ventilation. Available from: https://www.aerogen.com/uploads/Publications/Continuous%20Bronchodilator%20Therapy%20During%20Mechanical%20Ventilation%20Jim%20Fink.pdf. Accessed 22 Feb 2017.
32. May KR. The collison nebulizer: description, performance and application. J Aerosol Sci. 1973;4(3):235–43.
33. Lentz YK, Worden LR, Anchordoquy TJ, Lengsfeld CS. Effect of jet nebulization on DNA: identifying the dominant degradation mechanism and mitigation methods. J Aerosol Sci. 2005;36(8):973–90.
34. Liu K, Wen Z, Yang W, Wang J, Hu L, Dong X, et al. Impact of relative humidity and collection media on mycobacteriophage D29 aerosol. Appl Environ Microbiol. 2012;78(5):1466–72.
35. Arulmuthu ER, Williams DJ, Baldascini H, Versteeg HK, Hoare M. Studies on aerosol delivery of plasmid DNA using a mesh nebulizer. Biotechnol Bioeng. 2007;98(5):939–55.
36. Sidler-Moix A-L, Di Paolo ER, Dolci U, Berger-Gryllaki M, Cotting J, Pannatier A. Physicochemical aspects and efficiency of albuterol nebulization: comparison of three aerosol types in an in vitro pediatric model. Respir Care. 2015;60(1):38–46.
37. Fédération Antadir Commission Medico-Technique & Sociale. Fiche de synthese du dispositif: Pari Boy SX / Pari LC® Sprint SP. 2007 Available from: http://www.antadir.com/uploads/product/95/pdf/synthese-pari-lc-sprint-v4-inter.pdf. Accessed 12 May 2017.
38. Wachtel H, Ziegler J. Improved assessment of inhaler device performance using laser diffraction. Respiratory Drug Deliv VIII. 2002;2:379–81.
39. Carrigy NB, Martin AR, Finlay WH. Use of extrathoracic deposition models for patient-specific dose estimation during inhaler design. Curr Pharm Des. 2015;21(27):3984–92.
40. Vandal OH, Nathan CF, Ehrt S. Acid resistance in mycobacterium tuberculosis. J Bacteriol. 2009;191(15):4714–21.
41. Xiong X, Zhang HM, Wu TT, Xu L, Gan YL, Jiang LS, et al. Titer dynamic analysis of D29 within MTB-infected macrophages and effect on immune function of macrophages. Exp Lung Res. 2014;40(2):86–98.
42. Basra SK. The isolation and characterization of phages with lytic activity against Mycobacterium avium subspecies paratuberculosis, and their application using Bioluminescent assay in real-time Loop-mediated isothermal amplification assay for rapid detection. Master of Science Thesis. Department of Food Science, University of Guelph. 2013. Guelph, ON, Canada.
43. Darch SE, Kragh KN, Abbott EA, Bjarnsholt T, Bull JJ, Whiteley M. Phage inhibiting pathogen dissemination by targeting bacterial migrants in a chronic infected model. mBio. 2017;8(2):e00240–17.
44. Abedon ST. Bacteriophages and biofilms: ecology, phage therapy, plaques. New York: Nova Science Publishers, Inc.; 2011.
45. Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B, Delattre A-S, Lavigne R. Learning from bacteriophages – advantages and limitations of phage and phage-encoded protein applications. Curr Protein Pept Sci. 2012;13(8):699–722.
46. Lu TK, Collins JJ. Dispersing biofilms with engineered enzymatic bacteriophage. PNAS. 2007;104(27):11197–202.
47. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R. D-amino acids trigger biofilm disassembly. Science. 2010;328(5978):627–9.
48. Nadithe V, Rahamatalla M, Finlay WH, Mercer JR, Samuel J. Evaluation of nose-only aerosol inhalation chamber and comparison of experimental results with mathematical simulation of aerosol deposition in mouse lungs. J Pharm Sci. 2003;92(5):1066–76.