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Expanding clinical phage microbiology: simulating phage inhalation for respiratory tract infections

Shira Ben Porat, Daniel Gelman, Ortal Yerushalmy, Sivan Alkalay-Oren, Shunit Coppenhagen-Glazer, Malena Cohen-Cymberknoh, Eitan Kerem, Israel Amirav, Ran Nir-Paz, Ronen Hazan
ERJ Open Research 2021 7: 00367-2021; DOI: 10.1183/23120541.00367-2021
Shira Ben Porat
1Institute of Biomedical and Oral Research, Faculty of Dental Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
2Dept of Military Medicine, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
7These authors contributed equally
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Daniel Gelman
1Institute of Biomedical and Oral Research, Faculty of Dental Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
2Dept of Military Medicine, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
3Dept of Clinical Microbiology and Infectious Diseases, Hadassah-Hebrew University Medical Center, Jerusalem, Israel
7These authors contributed equally
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Ortal Yerushalmy
1Institute of Biomedical and Oral Research, Faculty of Dental Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
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  • ORCID record for Ortal Yerushalmy
Sivan Alkalay-Oren
1Institute of Biomedical and Oral Research, Faculty of Dental Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
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Shunit Coppenhagen-Glazer
1Institute of Biomedical and Oral Research, Faculty of Dental Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
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Malena Cohen-Cymberknoh
4Pediatric Pulmonology Unit and Cystic Fibrosis Center, Hadassah Medical Center, Jerusalem, Israel
5Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel
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Eitan Kerem
4Pediatric Pulmonology Unit and Cystic Fibrosis Center, Hadassah Medical Center, Jerusalem, Israel
5Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel
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Israel Amirav
6Pediatric Pulmonary Unit, Dana-Dwek Children's Hospital, Tel Aviv, Israel
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  • ORCID record for Israel Amirav
Ran Nir-Paz
3Dept of Clinical Microbiology and Infectious Diseases, Hadassah-Hebrew University Medical Center, Jerusalem, Israel
5Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel
8These authors contributed equally
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Ronen Hazan
1Institute of Biomedical and Oral Research, Faculty of Dental Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
8These authors contributed equally
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  • ORCID record for Ronen Hazan
  • For correspondence: ronenh@ekmd.huji.ac.il
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  • FIGURE 1
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    FIGURE 1

    Model for evaluation of phage nebulisation and delivery. a) Demonstration and schematic representation of phage nebulisation. Filter pads were placed at the output of the nebuliser to allow phage capture after each run of nebulisation. b) Anterior and lateral views of the 3D face and respiratory airways model. c) Demonstration and schematic representation of phage inhalation. Phages were nebulised and delivered by a face mask to the face and respiratory tract model, connected to a breathing simulator. Phages were captured by filter pads placed at the distal orifice of the airways model.

  • FIGURE 2
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    FIGURE 2

    Titre reduction of phages following nebulisation and inhalation to the airways model. For each phage, the initial phage titre inserted to the nebuliser, corrected according to the filter reduction fraction (Corrected Input), is compared to the phage titres retrieved from filters placed at the output of the nebuliser (Nebulisation) and at the tracheal level of the respiratory tract model (Inhalation). Three separate runs were made for each phage in every condition. Asterisks represent significant difference (p<0.05). PFU: plaque-forming units.

  • FIGURE 3
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    FIGURE 3

    Phage characterisation and its effect on inhalation fitness. Correlation plots representing phage inhalation efficacy, defined as the proportion between viable phages reaching the tracheal level and the corrected initial phage loads, according to a) tail length, b) capsid diameter, c) total phage length and d) phage genome size. e) Transmission electron microscopy images of the phages used in the study. Scale bar: 200 nm.

Tables

  • Figures
  • TABLE 1

    Characteristics of the phages used in the study

    PhageHostTaxonomyGenome size bpGenome structureGenBank accession
    BCSR5Burkholderia cepacia BCC378Myoviridae227 351CircularMW460245.1
    SAOMS1Staphylococcus aureus SAR1Herelleviridae140 135CircularMW460250.1
    BCSR129B. cepacia BCC197Myoviridae66 147CircularMW460247.1
    PASA16Pseudomonas aeruginosa PA14Myoviridae66 127CircularMT933737.1c
    Itty13P. aeruginosa PAR1Podoviridae61 818LinearMW460249.1
    Maco2Mycobacterium abscessus c107Siphoviridae48 239CircularMW460248.1
    Maco7M. abscessusx c107Siphoviridae47 836LinearMZ152914
    SeAlphiStaphylococcus epidermidis SE52Podoviridae18 368CircularMZ152915
  • TABLE 2

    Filter reduction fraction (Fr) of each phage

    PhageFr
    BCSR50.178
    SAOMS10.222
    BCSR1290.132
    PASA160.085
    Itty130.053
    Maco20.036
    Maco70.015
    SeAlphi0.58
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Vol 7 Issue 4 Table of Contents
ERJ Open Research: 7 (4)
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Expanding clinical phage microbiology: simulating phage inhalation for respiratory tract infections
Shira Ben Porat, Daniel Gelman, Ortal Yerushalmy, Sivan Alkalay-Oren, Shunit Coppenhagen-Glazer, Malena Cohen-Cymberknoh, Eitan Kerem, Israel Amirav, Ran Nir-Paz, Ronen Hazan
ERJ Open Research Oct 2021, 7 (4) 00367-2021; DOI: 10.1183/23120541.00367-2021

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Expanding clinical phage microbiology: simulating phage inhalation for respiratory tract infections
Shira Ben Porat, Daniel Gelman, Ortal Yerushalmy, Sivan Alkalay-Oren, Shunit Coppenhagen-Glazer, Malena Cohen-Cymberknoh, Eitan Kerem, Israel Amirav, Ran Nir-Paz, Ronen Hazan
ERJ Open Research Oct 2021, 7 (4) 00367-2021; DOI: 10.1183/23120541.00367-2021
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