OpenLB
Open Library of Bioscience

Pulmonary Delivery of Emerging Antibacterials for Bacterial Lung Infections Treatment.

Abstract

Keywords

References

1. GBD 2019 Risk Factors Collaborators. Global burden of 87 risk factors in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020;396(10258):1223–49.
2. Andrade F, Rafael D, Videira M, Ferreira D, Sosnik A, Sarmento B. Nanotechnology and pulmonary delivery to overcome resistance in infectious diseases. Adv Drug Deliv Rev. 2013;65(13–14):1816–27. [PMID: 23932923]
3. Velkov T, Abdul Rahim N, Zhou Q, Chan H-K, Li J. Inhaled anti-infective chemotherapy for respiratory tract infections: successes, challenges and the road ahead. Adv Drug Deliv Rev. 2015;85:65–82. [PMID: 25446140]
4. Misra A, Hickey AJ, Rossi C, Borchard G, Terada H, Makino K, et al. Inhaled drug therapy for treatment of tuberculosis. Tuberculosis (Edinb). 2011;91(1):71–81. [PMID: 20875771]
5. Taccetti G, Francalanci M, Pizzamiglio G, Messore B, Carnovale V, Cimino G, et al. Cystic fibrosis: recent insights into inhaled antibiotic treatment and future perspectives. Antibiotics (Basel). 2021;10(3):338. [PMID: 33810116]
6. World Health O. 2020 antibacterial agents in clinical and preclinical development: an overview and analysis. Geneva: World Health Organization; 2021.
7. León-Buitimea A, Garza-Cárdenas CR, Garza-Cervantes JA, Lerma-Escalera JA, Morones-Ramírez JR. The demand for new antibiotics: antimicrobial peptides, nanoparticles, and combinatorial therapies as future strategies in antibacterial agent design. Front Microbiol. 2020;11:1669. [PMID: 32793156]
8. Zharkova MS, Orlov DS, Golubeva OY, Chakchir OB, Eliseev IE, Grinchuk TM, et al. Application of antimicrobial peptides of the innate immune system in combination with conventional antibiotics-a novel way to combat antibiotic resistance? Front Cell Infect Microbiol. 2019;9:128. [PMID: 31114762]
9. Man DK, Chow MY, Casettari L, Gonzalez-Juarrero M, Lam JK. Potential and development of inhaled RNAi therapeutics for the treatment of pulmonary tuberculosis. Adv Drug Deliv Rev. 2016;102:21–32. [PMID: 27108702]
10. Düzgüneş N, Sessevmez M, Yildirim M. Bacteriophage therapy of bacterial infections: the rediscovered frontier. Pharmaceuticals (Basel). 2021;14(1):1–16. [DOI: 10.3390/ph14010034]
11. Huang Z, Kłodzińska SN, Wan F, Nielsen HM. Nanoparticle-mediated pulmonary drug delivery: state of the art towards efficient treatment of recalcitrant respiratory tract bacterial infections. Drug Deliv Transl Res. 2021;11(4):1634–54. [PMID: 33694082]
12. Kradin RL, Digumarthy S. The pathology of pulmonary bacterial infection. Semin Diagn Pathol. 2017;34(6):498–509. [PMID: 28655479]
13. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis. 2018;18(11):1191–210.
14. Butler MS, Gigante V, Sati H, Paulin S, Al-Sulaiman L, Rex JH, et al. Analysis of the clinical pipeline of treatments for drug-resistant bacterial infections: despite progress, more action is needed. Antimicrob Agents Chemother. 2022;66(3):199–21. [DOI: 10.1128/aac.01991-21]
15. Kaufmann SHE, Dorhoi A, Hotchkiss RS, Bartenschlager R. Host-directed therapies for bacterial and viral infections. Nat Rev Drug Discov. 2018;17(1):35–56. [PMID: 28935918]
16. Eldholm V, Balloux F. Antimicrobial resistance in mycobacterium tuberculosis: the odd one out. Trends Microbiol. 2016;24(8):637–48. [PMID: 27068531]
17. Bloemberg GV, Keller PM, Stucki D, Trauner A, Borrell S, Latshang T, et al. Acquired resistance to Bedaquiline and Delamanid in therapy for tuberculosis. N Engl J Med. 2015;373(20):1986–8. [PMID: 26559594]
18. Reynolds JH, McDonald G, Alton H, Gordon SB. Pneumonia in the immunocompetent patient. Br J Radiol. 2010;83(996):998–1009. [PMID: 21088086]
19. Garg M, Prabhakar N, Gulati A, Agarwal R, Dhooria S. Spectrum of imaging findings in pulmonary infections. Part 1: bacterial and viral. Pol J Radiol. 2019;84:205–13. [DOI: 10.5114/pjr.2019.85812]
20. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, et al. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet. 2002;359(9308):753–9. [PMID: 11888586]
21. Niederman MS, Mandell LA, Anzueto A, Bass JB, Broughton WA, Campbell GD, et al. Guidelines for the management of adults with community-acquired pneumonia. Am J Respir Crit Care Med. 2001;163(7):1730–54. [PMID: 11401897]
22. Labiris NR, Dolovich MB. Pulmonary drug delivery. Part I: physiological factors affecting therapeutic effectiveness of aerosolized medications. Br J Clin Pharmacol. 2003;56(6):588–99. [PMID: 14616418]
23. Ladavière C, Gref R. Toward an optimized treatment of intracellular bacterial infections: input of nanoparticulate drug delivery systems. Nanomedicine (Lond). 2015;10(19):3033–55. [PMID: 26420270]
24. D'Anna SE, Maniscalco M, Cappello F, Carone M, Motta A, Balbi B, et al. Bacterial and viral infections and related inflammatory responses in chronic obstructive pulmonary disease. Ann Med. 2021;53(1):135–50. [PMID: 32997525]
25. Sethi S. Infection as a comorbidity of COPD. Eur Respir J. 2010;35(6):1209–15. [PMID: 20513910]
26. Sethi S, Murphy TF. Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin Microbiol Rev. 2001;14(2):336–63. [PMID: 11292642]
27. Singanayagam A, Glanville N, Cuthbertson L, Bartlett NW, Finney LJ, Turek E, et al. Inhaled corticosteroid suppression of cathelicidin drives dysbiosis and bacterial infection in chronic obstructive pulmonary disease. Sci Transl Med. 2019;11(507):38–79. [DOI: 10.1126/scitranslmed.aav3879]
28. Toews GB. Impact of bacterial infections on airway diseases. Eur Respir Rev. 2005;14(95):62–8. [DOI: 10.1183/09059180.05.00009504]
29. Taylor SL, Leong LEX, Choo JM, Wesselingh S, Yang IA, Upham JW, et al. Inflammatory phenotypes in patients with severe asthma are associated with distinct airway microbiology. J Allergy Clin Immunol. 2018;141(1):94 -103-15. [PMID: 28479329]
30. Teo SM, Mok D, Pham K, Kusel M, Serralha M, Troy N, et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe. 2015;17(5):704–15. [PMID: 25865368]
31. Huang YJ, Nariya S, Harris JM, Lynch SV, Choy DF, Arron JR, et al. The airway microbiome in patients with severe asthma: associations with disease features and severity. J Allergy Clin Immunol. 2015;136(4):874–84. [PMID: 26220531]
32. Martin RJ, Kraft M, Chu HW, Berns EA, Cassell GH. A link between chronic asthma and chronic infection. J Allergy Clin Immunol. 2001;107(4):595–601. [PMID: 11295645]
33. Chmiel JF, Aksamit TR, Chotirmall SH, Dasenbrook EC, Elborn JS, LiPuma JJ, et al. Antibiotic management of lung infections in cystic fibrosis. II. Nontuberculous mycobacteria, anaerobic bacteria, and fungi. Ann Am Thorac Soc. 2014;11(8):1298–306. [PMID: 25167882]
34. Ciofu O, Tolker-Nielsen T, Jensen P, Wang H, Høiby N. Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Adv Drug Deliv Rev. 2015;85:7–23. [PMID: 25477303]
35. Carmody LA, Zhao J, Schloss PD, Petrosino JF, Murray S, Young VB, et al. Changes in cystic fibrosis airway microbiota at pulmonary exacerbation. Ann Am Thorac Soc. 2013;10(3):179–87. [PMID: 23802813]
36. Klinger-Strobel M, Lautenschläger C, Fischer D, Mainz JG, Bruns T, Tuchscherr L, et al. Aspects of pulmonary drug delivery strategies for infections in cystic fibrosis--where do we stand? Expert Opin Drug Deliv. 2015;12(8):1351–74. [PMID: 25642831]
37. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49. [PMID: 33538338]
38. Mao Q, Jiang F, Yin R, Wang J, Xia W, Dong G, et al. Interplay between the lung microbiome and lung cancer. Cancer Lett. 2018;415:40–8. [PMID: 29197615]
39. Ganzel C, Silverman B, Chemtob D, Ben Shoham A, Wiener-Well Y. The risk of tuberculosis in cancer patients is greatest in lymphoma and myelodysplastic syndrome/myeloproliferative neoplasm: a large population-based cohort study. Leuk Lymphoma. 2019;60(3):720–5. [PMID: 30188229]
40. Pilaniya V, Gera K, Kunal S, Shah A. Pulmonary tuberculosis masquerading as metastatic lung disease. Eur Respir Rev. 2016;25(139):97–8. [PMID: 26929427]
41. Akinosoglou KS, Karkoulias K, Marangos M. Infectious complications in patients with lung cancer. Eur Rev Med Pharmacol Sci. 2013;17(1):8–18. [PMID: 23329518]
42. Halley A, Leonetti A, Gregori A, Tiseo M, Deng DM, Giovannetti E, et al. The role of the microbiome in cancer and therapy efficacy: focus on lung cancer. Anticancer Res. 2020;40(9):4807–18. [PMID: 32878769]
43. Zhang M, Li M, Du L, Zeng J, Yao T, Jin Y. Paclitaxel-in-liposome-in-bacteria for inhalation treatment of primary lung cancer. Int J Pharm. 2020;578:119–27. [DOI: 10.1016/j.ijpharm.2020.119177]
44. Munita JM, Arias CA. Mechanisms of antibiotic resistance. Microbiol Spectr. 2016;4(2):1–37. [DOI: 10.1128/microbiolspec.VMBF-0016-2015]
45. Douafer H, Andrieu V, Brunel JM. Scope and limitations on aerosol drug delivery for the treatment of infectious respiratory diseases. J Control Release. 2020;325:276–92. [PMID: 32652109]
46. Chang RYK, Wallin M, Lin Y, Leung SSY, Wang H, Morales S, et al. Phage therapy for respiratory infections. Adv Drug Deliv Rev. 2018;133:76–86. [PMID: 30096336]
47. Mookherjee N, Anderson MA, Haagsman HP, Davidson DJ. Antimicrobial host defence peptides: functions and clinical potential. Nat Rev Drug Discov. 2020;19(5):311–32. [PMID: 32107480]
48. Divyashree M, Mani MK, Reddy D, Kumavath R, Ghosh P, Azevedo V, et al. Clinical applications of antimicrobial peptides (AMPs): where do we stand now? Protein Pept Lett. 2020;27(2):120–34. [PMID: 31553285]
49. Li W, Separovic F, O'Brien-Simpson NM, Wade JD. Chemically modified and conjugated antimicrobial peptides against superbugs. Chem Soc Rev. 2021;50(8):4932–73. [PMID: 33710195]
50. Fjell CD, Hiss JA, Hancock RE, Schneider G. Designing antimicrobial peptides: form follows function. Nat Rev Drug Discov. 2011;11(1):37–51. [PMID: 22173434]
51. Kumar P, Kizhakkedathu JN, Straus SK. Antimicrobial peptides: diversity, mechanism of action and strategies to improve the activity and biocompatibility in vivo. Biomolecules. 2018;8(1):1–24. [DOI: 10.3390/biom8010004]
52. Graf M, Mardirossian M, Nguyen F, Seefeldt AC, Guichard G, Scocchi M, et al. Proline-rich antimicrobial peptides targeting protein synthesis. Nat Prod Rep. 2017;34(7):702–11. [PMID: 28537612]
53. Van Eijk M, van Dijk A, van der Ent CK, Arets HGM, Breukink E, van Os N, et al. PepBiotics, novel cathelicidin-inspired antimicrobials to fight pulmonary bacterial infections. Biochim Biophys Acta Gen Subj. 1865;2021(9):1–11.
54. Hancock RE, Haney EF, Gill EE. The immunology of host defence peptides: beyond antimicrobial activity. Nat Rev Immunol. 2016;16(5):321–34. [PMID: 27087664]
55. Beaumont PE, McHugh B, Gwyer Findlay E, Mackellar A, Mackenzie KJ, Gallo RL, et al. Cathelicidin host defence peptide augments clearance of pulmonary Pseudomonas aeruginosa infection by its influence on neutrophil function in vivo. PLoS One. 2014;9(6):1–12. [DOI: 10.1371/journal.pone.0099029]
56. Tewary P, de la Rosa G, Sharma N, Rodriguez LG, Tarasov SG, Howard OM, et al. β-Defensin 2 and 3 promote the uptake of self or CpG DNA, enhance IFN-α production by human plasmacytoid dendritic cells, and promote inflammation. J Immunol. 2013;191(2):865–74. [PMID: 23776172]
57. Severino P, Ariga SK, Barbeiro HV, de Lima TM, de Paula SE, Barbeiro DF, et al. Cathelicidin-deficient mice exhibit increased survival and upregulation of key inflammatory response genes following cecal ligation and puncture. J Mol Med (Berl). 2017;95(9):995–1003. [PMID: 28623379]
58. Coorens M, Schneider VAF, de Groot AM, van Dijk A, Meijerink M, Wells JM, et al. Cathelicidins inhibit Escherichia coli-induced TLR2 and TLR4 activation in a viability-dependent manner. J Immunol. 2017;199(4):1418–28. [PMID: 28710255]
59. Kahlenberg JM, Kaplan MJ. Little peptide, big effects: the role of LL-37 in inflammation and autoimmune disease. J Immunol (Baltimore, Md : 1950). 2013;191(10):4895–901.
60. Song X, Liu P, Liu X, Wang Y, Wei H, Zhang J, et al. Dealing with MDR bacteria and biofilm in the post-antibiotic era: application of antimicrobial peptides-based nano-formulation. Mater Sci Eng C Mater Biol Appl. 2021;128:112–318. [DOI: 10.1016/j.msec.2021.112318]
61. Silva JP, Gonçalves C, Costa C, Sousa J, Silva-Gomes R, Castro AG, et al. Delivery of LLKKK18 loaded into self-assembling hyaluronic acid nanogel for tuberculosis treatment. J Control Release. 2016;235:112–24. [PMID: 27261333]
62. Falciani C, Zevolini F, Brunetti J, Riolo G, Gracia R, Marradi M, et al. Antimicrobial peptide-loaded nanoparticles as inhalation therapy for Pseudomonas aeruginosa infections. Int J Nanomedicine. 2020;15:1117–28. [PMID: 32110011]
63. Yang L, Liu Y, Wang N, Wang H, Wang K, Luo XL, et al. Albumin-based LL37 peptide nanoparticles as a sustained release system against Pseudomonas aeruginosa lung infection. ACS Biomater Sci Eng. 2021;7(5):1817–26. [PMID: 33966375]
64. Song J, Cortez-Jugo C, Shirbin SJ, Lin Z, Pan S, Qiao GG, et al. Immobilization and intracellular delivery of structurally nanoengineered antimicrobial peptide polymers using polyphenol-based capsules. Adv Funct Mater. 2022;32(6):1–12. [DOI: 10.1002/adfm.202107341]
65. Water JJ, Smart S, Franzyk H, Foged C, Nielsen HM. Nanoparticle-mediated delivery of the antimicrobial peptide plectasin against Staphylococcus aureus in infected epithelial cells. Eur J Pharm Biopharm. 2015;92:65–73. [PMID: 25701808]
66. Kwok PC, Grabarek A, Chow MY, Lan Y, Li JC, Casettari L, et al. Inhalable spray-dried formulation of D-LAK antimicrobial peptides targeting tuberculosis. Int J Pharm. 2015;491(1–2):367–74. [PMID: 26151107]
67. Amariei G, Kokol V, Vivod V, Boltes K, Letón P, Rosal R. Biocompatible antimicrobial electrospun nanofibers functionalized with ε-poly-l-lysine. Int J Pharm. 2018;553(1–2):141–8. [PMID: 30336186]
68. Kandil R, Merkel OM. Pulmonary delivery of siRNA as a novel treatment for lung diseases. Ther Deliv. 2019;10(4):203–6. [PMID: 30991921]
69. Dyawanapelly S, Ghodke SB, Vishwanathan R, Dandekar P, Jain R. RNA interference-based therapeutics: molecular platforms for infectious diseases. J Biomed Nanotechnol. 2014;10(9):1998–2037. [PMID: 25992447]
70. Lam JK, Chow MY, Zhang Y, Leung SW. siRNA versus miRNA as therapeutics for gene silencing. Mol Ther Nucleic Acids. 2015;4(9):1–20.
71. Zhou X, Li X, Wu M. miRNAs reshape immunity and inflammatory responses in bacterial infection. Signal Transduct Target Ther. 2018;3:1–13.
72. Zhou X, Li X, Ye Y, Zhao K, Zhuang Y, Li Y, et al. MicroRNA-302b augments host defense to bacteria by regulating inflammatory responses via feedback to TLR/IRAK4 circuits. Nat Commun. 2014;5:1–13. [DOI: 10.1038/ncomms4619]
73. Vergadi E, Vaporidi K, Theodorakis EE, Doxaki C, Lagoudaki E, Ieronymaki E, et al. Akt2 deficiency protects from acute lung injury via alternative macrophage activation and miR-146a induction in mice. J Immunol. 2014;192(1):394–406. [PMID: 24277697]
74. Yanagihara K, Tashiro M, Fukuda Y, Ohno H, Higashiyama Y, Miyazaki Y, et al. Effects of short interfering RNA against methicillin-resistant Staphylococcus aureus coagulase in vitro and in vivo. J Antimicrob Chemother. 2006;57(1):122–6. [PMID: 16344286]
75. Gong FY, Zhang DY, Zhang JG, Wang LL, Zhan WL, Qi JY, et al. siRNA-mediated gene silencing of MexB from the MexA-MexB-OprM efflux pump in Pseudomonas aeruginosa. BMB Rep. 2014;47(4):203–8. [PMID: 24219865]
76. Rosas-Taraco AG, Higgins DM, Sánchez-Campillo J, Lee EJ, Orme IM, González-Juarrero M. Local pulmonary immunotherapy with siRNA targeting TGFβ1 enhances antimicrobial capacity in mycobacterium tuberculosis infected mice. Tuberculosis (Edinb). 2011;91(1):98–106. [PMID: 21195670]
77. Lam JK, Liang W, Chan HK. Pulmonary delivery of therapeutic siRNA. Adv Drug Deliv Rev. 2012;64(1):1–15. [PMID: 21356260]
78. Fujita Y, Takeshita F, Kuwano K, Ochiya T. RNAi therapeutic platforms for lung diseases. Pharmaceuticals (Basel). 2013;6(2):223–50. [PMID: 24275949]
79. Mottais A, Le Gall T, Sibiril Y, Ravel J, Laurent V, d'Arbonneau F, et al. Enhancement of lung gene delivery after aerosol: a new strategy using non-viral complexes with antibacterial properties. Biosci Rep. 2017;37(6):1–17. [DOI: 10.1042/BSR20160618]
80. Chow MYT, Qiu Y, Lam JKW. Inhaled RNA therapy: from promise to reality. Trends Pharmacol Sci. 2020;41(10):715–29. [PMID: 32893004]
81. Bardoliwala D, Patel V, Javia A, Ghosh S, Patel A, Misra A. Nanocarriers in effective pulmonary delivery of siRNA: current approaches and challenges. Ther Deliv. 2019;10(5):311–32. [PMID: 31116099]
82. Okuda T, Morishita M, Mizutani K, Shibayama A, Okazaki M, Okamoto H. Development of spray-freeze-dried siRNA/PEI powder for inhalation with high aerosol performance and strong pulmonary gene silencing activity. J Control Release. 2018;279:99–113. [PMID: 29627404]
83. Jensen DK, Jensen LB, Koocheki S, Bengtson L, Cun D, Nielsen HM, et al. Design of an inhalable dry powder formulation of DOTAP-modified PLGA nanoparticles loaded with siRNA. J Control Release. 2012;157(1):141–8. [PMID: 21864597]
84. Bielski E, Zhong Q, Mirza H, Brown M, Molla A, Carvajal T, et al. TPP-dendrimer nanocarriers for siRNA delivery to the pulmonary epithelium and their dry powder and metered-dose inhaler formulations. Int J Pharm. 2017;527(1–2):171–83. [PMID: 28549971]
85. Agnoletti M, Bohr A, Thanki K, Wan F, Zeng X, Boetker JP, et al. Inhalable siRNA-loaded nano-embedded microparticles engineered using microfluidics and spray drying. Eur J Pharm Biopharm. 2017;120:9–21. [PMID: 28780275]
86. Chow MYT, Qiu Y, Lo FFK, Lin HHS, Chan HK, Kwok PCL, et al. Inhaled powder formulation of naked siRNA using spray drying technology with l-leucine as dispersion enhancer. Int J Pharm. 2017;530(1–2):40–52. [PMID: 28720537]
87. Liang W, Chan AYL, Chow MYT, Lo FFK, Qiu Y, Kwok PCL, et al. Spray freeze drying of small nucleic acids as inhaled powder for pulmonary delivery. Asian J Pharm Sci. 2018;13(2):163–72. [PMID: 32104389]
88. Liang W, Chow MYT, Lau PN, Zhou QT, Kwok PCL, Leung GPH, et al. Inhalable dry powder formulations of siRNA and pH-responsive peptides with antiviral activity against H1N1 influenza virus. Mol Pharm. 2015;12(3):910–21. [PMID: 25599953]
89. Liang W, Chow MYT, Chow SF, Chan HK, Kwok PCL, Lam JKW. Using two-fluid nozzle for spray freeze drying to produce porous powder formulation of naked siRNA for inhalation. Int J Pharm. 2018;552(1–2):67–75. [PMID: 30244146]
90. Qiu Y, Lam JK, Leung SW, Liang W. Delivery of RNAi therapeutics to the airways-from bench to bedside. Molecules. 2016;21(9):1–32. [DOI: 10.3390/molecules21091249]
91. Kandil R, Merkel M. Therapeutic delivery of RNA effectors: diseases affecting the respiratory system. Pharmazie. 2016;71(1):21–6. [PMID: 26867349]
92. Li J, Cai C, Li J, Li J, Li J, Sun T, et al. Chitosan-based nanomaterials for drug delivery. Molecules. 2018;23(10):1–26. [DOI: 10.3390/molecules23102661]
93. Kannen V, Parry L, Martin FL. Phages enter the fight against colorectal cancer. Trends Cancer. 2019;5(10):577–9. [PMID: 31706504]
94. Manohar P, Loh B, Athira S, Nachimuthu R, Hua X, Welburn SC, et al. Secondary bacterial infections during pulmonary viral disease: phage therapeutics as alternatives to antibiotics? Front Microbiol. 2020;11:14–34. [DOI: 10.3389/fmicb.2020.01434]
95. Abedon ST, Kuhl SJ, Blasdel BG, Kutter EM. Phage treatment of human infections. Bacteriophage. 2011;1(2):66–85. [PMID: 22334863]
96. Cooper CJ, Denyer SP, Maillard JY. Stability and purity of a bacteriophage cocktail preparation for nebulizer delivery. Lett Appl Microbiol. 2014;58(2):118–22. [PMID: 24111661]
97. Carrigy NB, Larsen SE, Reese V, Pecor T, Harrison M, Kuehl PJ, et al. Prophylaxis of mycobacterium tuberculosis H37Rv infection in a preclinical mouse model via inhalation of nebulized bacteriophage D29. Antimicrob Agents Chemother. 2019;63(12):1–13. [DOI: 10.1128/AAC.00871-19]
98. Carrigy NB, Chang RY, Leung SSY, Harrison M, Petrova Z, Pope WH, et al. Anti-tuberculosis bacteriophage D29 delivery with a vibrating mesh nebulizer, jet nebulizer, and soft mist inhaler. Pharm Res. 2017;34(10):2084–96. [PMID: 28646325]
99. Leung SSY, Carrigy NB, Vehring R, Finlay WH, Morales S, Carter EA, et al. Jet nebulization of bacteriophages with different tail morphologies - structural effects. Int J Pharm. 2019;554:322–6. [PMID: 30445174]
100. Lebeaux D, Merabishvili M, Caudron E, Lannoy D, Van Simaey L, Duyvejonck H, et al. A case of phage therapy against Pandrug-resistant Achromobacter xylosoxidans in a 12-year-old lung-transplanted cystic fibrosis patient. Viruses. 2021;13(1):1–10. [DOI: 10.3390/v13010060]
101. Marqus S, Lee L, Istivan T, Kyung Chang RY, Dekiwadia C, Chan HK, et al. High frequency acoustic nebulization for pulmonary delivery of antibiotic alternatives against Staphylococcus aureus. Eur J Pharm Biopharm. 2020;151:181–8. [PMID: 32315699]
102. Jończyk E, Kłak M, Międzybrodzki R, Górski A. The influence of external factors on bacteriophages--review. Folia Microbiol (Praha). 2011;56(3):191–200. [PMID: 21625877]
103. Cooper CJ, Koonjan S, Nilsson AS. Enhancing whole phage therapy and their derived antimicrobial enzymes through complex formulation. Pharmaceuticals (Basel). 2018;11(2):1–25. [DOI: 10.3390/ph11020034]
104. Rios AC, Vila MMDC, Lima R, Del Fiol FS, Tubino M, Teixeira JA, et al. Structural and functional stabilization of bacteriophage particles within the aqueous core of a W/O/W multiple emulsion: a potential biotherapeutic system for the inhalational treatment of bacterial pneumonia. Process Biochem. 2018;64:177–92. [DOI: 10.1016/j.procbio.2017.09.022]
105. Lapenkova MB, Alyapkina YS, Vladimirsky MA. Bactericidal activity of liposomal form of lytic mycobacteriophage D29 in cell models of tuberculosis infection in vitro. Bull Exp Biol Med. 2020;169(3):361–4. [PMID: 32743783]
106. Wang X, Xie Z, Zhao J, Zhu Z, Yang C, Liu Y. Prospects of inhaled phage therapy for combatting pulmonary infections. Front Cell Infect Microbiol. 2021;11:1–20. [DOI: 10.3389/fcimb.2021.758392]
107. Malik DJ, Resch G. Editorial: manufacturing, formulation and delivery issues for phage therapy to become a reality. Front Microbiol. 2020;11:1–3. [DOI: 10.3389/fmicb.2020.584137]
108. Yan W, He R, Tang X, Tian B, Liu Y, Tong Y, et al. The influence of formulation components and environmental humidity on spray-dried phage powders for treatment of respiratory infections caused by Acinetobacter baumannii. Pharmaceutics. 2021;13(8):1–17. [DOI: 10.3390/pharmaceutics13081162]
109. Golshahi L, Lynch KH, Dennis JJ, Finlay WH. In vitro lung delivery of bacteriophages KS4-M and ΦKZ 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. [PMID: 20875034]
110. Leung SS, 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. [PMID: 26928668]
111. Leung SSY, Parumasivam T, Gao FG, Carter EA, Carrigy NB, Vehring R, et al. Effects of storage conditions on the stability of spray dried, inhalable bacteriophage powders. Int J Pharm. 2017;521(1–2):141–9. [PMID: 28163231]
112. Leung SSY, Parumasivam T, Nguyen A, Gengenbach T, Carter EA, Carrigy NB, et al. Effect of storage temperature on the stability of spray dried bacteriophage powders. Eur J Pharm Biopharm. 2018;127:213–22. [PMID: 29486303]
113. Chang RYK, Chen K, Wang J, Wallin M, Britton W, Morales S, et al. Proof-of-principle study in a murine lung infection model of antipseudomonal activity of phage PEV20 in a dry-powder formulation. Antimicrob Agents Chemother. 2018;62(2):1714–7. [DOI: 10.1128/AAC.01714-17]
114. Chang RY, Wong J, Mathai A, Morales S, Kutter E, Britton W, et al. Production of highly stable spray dried phage formulations for treatment of Pseudomonas aeruginosa lung infection. Eur J Pharm Biopharm. 2017;121:1–13. [PMID: 28890220]
115. Chang RYK, Wallin M, Kutter E, Morales S, Britton W, Li J, et al. Storage stability of inhalable phage powders containing lactose at ambient conditions. Int J Pharm. 2019;560:1–8. [DOI: 10.1016/j.ijpharm.2019.01.050]
116. Li M, Chang RYK, Lin Y, Morales S, Kutter E, Chan HK. Phage cocktail powder for Pseudomonas aeruginosa respiratory infections. Int J Pharm. 2021;596:1–8. [DOI: 10.1016/j.ijpharm.2021.120200]
117. Lin Y, Chang RYK, Britton WJ, Morales S, Kutter E, Li J, et al. Inhalable combination powder formulations of phage and ciprofloxacin for P. aeruginosa respiratory infections. Eur J Pharm Biopharm. 2019;142:543–52. [PMID: 31398437]
118. Lin Y, Yoon Kyung Chang R, Britton WJ, Morales S, Kutter E, Li J, et al. Storage stability of phage-ciprofloxacin combination powders against Pseudomonas aeruginosa respiratory infections. Int J Pharm. 2020;591:1–7. [DOI: 10.1016/j.ijpharm.2020.119952]
119. Ly A, Carrigy NB, Wang H, Harrison M, Sauvageau D, Martin AR, et al. Atmospheric spray freeze drying of sugar solution with phage D29. Front Microbiol. 2019;10:1–11. [DOI: 10.3389/fmicb.2019.00488]
120. Carrigy NB, Liang L, Wang H, Kariuki S, Nagel TE, Connerton IF, et al. Trileucine and pullulan improve anti-Campylobacter bacteriophage stability in engineered spray-dried microparticles. Ann Biomed Eng. 2020;48(4):1169–80. [PMID: 31845128]
121. Carrigy NB, Liang L, Wang H, Kariuki S, Nagel TE, Connerton IF, et al. Spray-dried anti-Campylobacter bacteriophage CP30A powder suitable for global distribution without cold chain infrastructure. Int J Pharm. 2019;569:1–9. [DOI: 10.1016/j.ijpharm.2019.118601]
122. Ersoy SC, Heithoff DM, Barnes L, Tripp GK, House JK, Marth JD, et al. Correcting a fundamental flaw in the paradigm for antimicrobial susceptibility testing. EBioMedicine. 2017;20:173–81. [PMID: 28579300]
123. Meng N, Grimm D. Membrane-destabilizing ionizable phospholipids: novel components for organ-selective mRNA delivery and CRISPR-Cas gene editing. Signal Transduct Target Ther. 2021;6(1):1–3.
124. Depreter F, Pilcer G, Amighi K. Inhaled proteins: challenges and perspectives. Int J Pharm. 2013;447(1–2):251–80. [PMID: 23499756]
125. Elkins MR, Robinson P, Anderson SD, Perry CP, Daviskas E, Charlton B. Inspiratory flows and volumes in subjects with cystic fibrosis using a new dry powder inhaler device. Open Respir Med J. 2014;8:1–7. [PMID: 24570763]
126. Tiddens HA, Geller DE, Challoner P, Speirs RJ, Kesser KC, Overbeek SE, et al. Effect of dry powder inhaler resistance on the inspiratory flow rates and volumes of cystic fibrosis patients of six years and older. J Aerosol Med. 2006;19(4):456–65. [PMID: 17196074]
127. Silva AS, Tavares MT, Aguiar-Ricardo A. Sustainable strategies for nano-in-micro particle engineering for pulmonary delivery. J Nanopart Res. 2014;16(11):1–17. [DOI: 10.1007/s11051-014-2602-0]
128. Loira-Pastoriza C, Todoroff J, Vanbever R. Delivery strategies for sustained drug release in the lungs. Adv Drug Deliv Rev. 2014;75:81–91. [PMID: 24915637]
129. Li YZ, Sun X, Gong T, Liu J, Zuo J, Zhang ZR. Inhalable microparticles as carriers for pulmonary delivery of thymopentin-loaded solid lipid nanoparticles. Pharm Res. 2010;27(9):1977–86. [PMID: 20625801]
130. Łusiak-Szelachowska M, Międzybrodzki R, Fortuna W, Borysowski J, Górski A. Anti-phage serum antibody responses and the outcome of phage therapy. Folia Microbiol (Praha). 2021;66(1):127–31. [PMID: 33126265]
131. Popowski KD, Moatti A, Scull G, Silkstone D, Lutz H, López de Juan Abad B, et al. Inhalable dry powder mRNA vaccines based on extracellular vesicles. Matter. 2022;5:1–15. [DOI: 10.1016/j.matt.2022.06.012]
132. Roh EH, Fromen CA, Sullivan MO. Inhalable mRNA vaccines for respiratory diseases: a roadmap. Curr Opin Biotechnol. 2022;74:104–9. [PMID: 34894574]
133. Ndeupen S, Qin Z, Jacobsen S, Bouteau A, Estanbouli H, Igyártó BZ. The mRNA-LNP platform's lipid nanoparticle component used in preclinical vaccine studies is highly inflammatory. iScience. 2021;24(12):1–15. [DOI: 10.1016/j.isci.2021.103479]

Grants

1. 24300619/University Grants Committee

MeSH Term

Chemicals