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Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains

Helen L Brown, Georgie Metters, Matthew Hitchings Orcid Logo, Thomas Wilkinson Orcid Logo, Luis Sousa, Jenna Cooper, Harry Dance, Robert J. Atterbury, Rowena Jenkins Orcid Logo

Applied and Environmental Microbiology, Volume: 86, Issue: e01768-20

Swansea University Authors: Matthew Hitchings Orcid Logo, Thomas Wilkinson Orcid Logo, Rowena Jenkins Orcid Logo

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DOI (Published version): 10.1128/aem.01768-20

Abstract

Staphylococcus pseudintermedius causes opportunistic infections in dogs. It also has significant zoonotic potential, with the emergence of multidrug-resistance leading to difficulty treating both animal and human infections. Manuka honey has previously been reported to inhibit many bacterial pathoge...

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Published in: Applied and Environmental Microbiology
ISSN: 0099-2240 1098-5336
Published: American Society for Microbiology 2020
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URI: https://cronfa.swan.ac.uk/Record/cronfa54999
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It also has significant zoonotic potential, with the emergence of multidrug-resistance leading to difficulty treating both animal and human infections. Manuka honey has previously been reported to inhibit many bacterial pathogens including methicillin resistant Staphylococcus aureus and is successfully utilised in both clinical and veterinary practice. Here we evaluated the ability of manuka honey to inhibit strains of S. pseudintermedius growth alone and in combination with antibiotics, and its capacity to modulate virulence within multiple S. pseudintermedius. All 18 of the genetically diverse S. pseudintermedius strains sequenced and tested were inhibited by &#x2264; 12% (w/v) medical grade manuka honey, although tolerance to five clinically relevant antibiotics was observed. The susceptibility of the isolates to four of these antibiotics was significantly increased (p &#x2264;0.05) when combined with sub lethal concentrations of honey, although sensitivity to oxacillin was decreased. Virulence (DNase, protease and haemolysin) activity was also significantly reduced (p &#x2264; 0.05) in over half of isolates when cultured with sub lethal concentrations of honey (13, 9 and 10 isolates respectively). These findings highlight the potential for manuka honey to be utilised against S. pseudintermedius infections. Importance: Staphylococcus pseudintermedius is an important member of the skin microbial community in animals and can cause opportunistic infections in both pets and their owners. The high incidence of antimicrobial resistance in S. pseudintermedius highlights that this opportunistic zoonotic pathogen can cause infections which require prolonged and intensive treatment to resolve. Manuka honey has proven efficacy against many bacterial pathogens and is an accepted topical treatment for infections in both veterinary and clinical practice so is a particularly appropriate antimicrobial for use with zoonotic pathogens such as S. pseudintermedius. Here we demonstrate that manuka honey is not only highly potent against novel multi-drug resistant S. pseudintermedius isolates, but also acts synergistically with clinically relevant antibiotics. In addition, manuka honey modulates S. pseudintermedius virulence activity, even at subinhibitory concentrations. In a clinical setting these attributes may assist in controlling infection, allowing a more rapid resolution and reducing antibiotic use.</abstract><type>Journal Article</type><journal>Applied and Environmental Microbiology</journal><volume>86</volume><journalNumber>e01768-20</journalNumber><paginationStart/><paginationEnd/><publisher>American Society for Microbiology</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>0099-2240</issnPrint><issnElectronic>1098-5336</issnElectronic><keywords>manuka honey, antibiotic resistance, synergy, haemolysis, proteolysis, aggregation</keywords><publishedDay>1</publishedDay><publishedMonth>10</publishedMonth><publishedYear>2020</publishedYear><publishedDate>2020-10-01</publishedDate><doi>10.1128/aem.01768-20</doi><url/><notes/><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm/><lastEdited>2020-12-03T16:28:11.6593579</lastEdited><Created>2020-08-18T09:58:07.8988851</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Medicine</level></path><authors><author><firstname>Helen L</firstname><surname>Brown</surname><order>1</order></author><author><firstname>Georgie</firstname><surname>Metters</surname><order>2</order></author><author><firstname>Matthew</firstname><surname>Hitchings</surname><orcid>0000-0002-5527-4709</orcid><order>3</order></author><author><firstname>Thomas</firstname><surname>Wilkinson</surname><orcid>0000-0003-0397-6079</orcid><order>4</order></author><author><firstname>Luis</firstname><surname>Sousa</surname><order>5</order></author><author><firstname>Jenna</firstname><surname>Cooper</surname><order>6</order></author><author><firstname>Harry</firstname><surname>Dance</surname><order>7</order></author><author><firstname>Robert J.</firstname><surname>Atterbury</surname><order>8</order></author><author><firstname>Rowena</firstname><surname>Jenkins</surname><orcid>0000-0001-6664-6099</orcid><order>9</order></author></authors><documents><document><filename>54999__18797__46aa397dc87b45debd42658378aac4b4.pdf</filename><originalFilename>54999.VOR.pdf</originalFilename><uploaded>2020-12-02T17:33:26.1999758</uploaded><type>Output</type><contentLength>1152349</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.</documentNotes><copyrightCorrect>true</copyrightCorrect><language>eng</language><licence>https://creativecommons.org/licenses/by/4.0/</licence></document></documents><OutputDurs/></rfc1807>
spelling 2020-12-03T16:28:11.6593579 v2 54999 2020-08-18 Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains be98847c72c14a731c4a6b7bc02b3bcf 0000-0002-5527-4709 Matthew Hitchings Matthew Hitchings true false 86cca6bf31bfe8572de27c1b441420d8 0000-0003-0397-6079 Thomas Wilkinson Thomas Wilkinson true false caf58cd775a27bf8b9ee340079a29cc0 0000-0001-6664-6099 Rowena Jenkins Rowena Jenkins true false 2020-08-18 BMS Staphylococcus pseudintermedius causes opportunistic infections in dogs. It also has significant zoonotic potential, with the emergence of multidrug-resistance leading to difficulty treating both animal and human infections. Manuka honey has previously been reported to inhibit many bacterial pathogens including methicillin resistant Staphylococcus aureus and is successfully utilised in both clinical and veterinary practice. Here we evaluated the ability of manuka honey to inhibit strains of S. pseudintermedius growth alone and in combination with antibiotics, and its capacity to modulate virulence within multiple S. pseudintermedius. All 18 of the genetically diverse S. pseudintermedius strains sequenced and tested were inhibited by ≤ 12% (w/v) medical grade manuka honey, although tolerance to five clinically relevant antibiotics was observed. The susceptibility of the isolates to four of these antibiotics was significantly increased (p ≤0.05) when combined with sub lethal concentrations of honey, although sensitivity to oxacillin was decreased. Virulence (DNase, protease and haemolysin) activity was also significantly reduced (p ≤ 0.05) in over half of isolates when cultured with sub lethal concentrations of honey (13, 9 and 10 isolates respectively). These findings highlight the potential for manuka honey to be utilised against S. pseudintermedius infections. Importance: Staphylococcus pseudintermedius is an important member of the skin microbial community in animals and can cause opportunistic infections in both pets and their owners. The high incidence of antimicrobial resistance in S. pseudintermedius highlights that this opportunistic zoonotic pathogen can cause infections which require prolonged and intensive treatment to resolve. Manuka honey has proven efficacy against many bacterial pathogens and is an accepted topical treatment for infections in both veterinary and clinical practice so is a particularly appropriate antimicrobial for use with zoonotic pathogens such as S. pseudintermedius. Here we demonstrate that manuka honey is not only highly potent against novel multi-drug resistant S. pseudintermedius isolates, but also acts synergistically with clinically relevant antibiotics. In addition, manuka honey modulates S. pseudintermedius virulence activity, even at subinhibitory concentrations. In a clinical setting these attributes may assist in controlling infection, allowing a more rapid resolution and reducing antibiotic use. Journal Article Applied and Environmental Microbiology 86 e01768-20 American Society for Microbiology 0099-2240 1098-5336 manuka honey, antibiotic resistance, synergy, haemolysis, proteolysis, aggregation 1 10 2020 2020-10-01 10.1128/aem.01768-20 COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University 2020-12-03T16:28:11.6593579 2020-08-18T09:58:07.8988851 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Helen L Brown 1 Georgie Metters 2 Matthew Hitchings 0000-0002-5527-4709 3 Thomas Wilkinson 0000-0003-0397-6079 4 Luis Sousa 5 Jenna Cooper 6 Harry Dance 7 Robert J. Atterbury 8 Rowena Jenkins 0000-0001-6664-6099 9 54999__18797__46aa397dc87b45debd42658378aac4b4.pdf 54999.VOR.pdf 2020-12-02T17:33:26.1999758 Output 1152349 application/pdf Version of Record true This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. true eng https://creativecommons.org/licenses/by/4.0/
title Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains
spellingShingle Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains
Matthew Hitchings
Thomas Wilkinson
Rowena Jenkins
title_short Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains
title_full Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains
title_fullStr Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains
title_full_unstemmed Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains
title_sort Antibacterial and anti-virulence activity of manuka honey against genetically diverse Staphylococcus pseudintermedius strains
author_id_str_mv be98847c72c14a731c4a6b7bc02b3bcf
86cca6bf31bfe8572de27c1b441420d8
caf58cd775a27bf8b9ee340079a29cc0
author_id_fullname_str_mv be98847c72c14a731c4a6b7bc02b3bcf_***_Matthew Hitchings
86cca6bf31bfe8572de27c1b441420d8_***_Thomas Wilkinson
caf58cd775a27bf8b9ee340079a29cc0_***_Rowena Jenkins
author Matthew Hitchings
Thomas Wilkinson
Rowena Jenkins
author2 Helen L Brown
Georgie Metters
Matthew Hitchings
Thomas Wilkinson
Luis Sousa
Jenna Cooper
Harry Dance
Robert J. Atterbury
Rowena Jenkins
format Journal article
container_title Applied and Environmental Microbiology
container_volume 86
container_issue e01768-20
publishDate 2020
institution Swansea University
issn 0099-2240
1098-5336
doi_str_mv 10.1128/aem.01768-20
publisher American Society for Microbiology
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
document_store_str 1
active_str 0
description Staphylococcus pseudintermedius causes opportunistic infections in dogs. It also has significant zoonotic potential, with the emergence of multidrug-resistance leading to difficulty treating both animal and human infections. Manuka honey has previously been reported to inhibit many bacterial pathogens including methicillin resistant Staphylococcus aureus and is successfully utilised in both clinical and veterinary practice. Here we evaluated the ability of manuka honey to inhibit strains of S. pseudintermedius growth alone and in combination with antibiotics, and its capacity to modulate virulence within multiple S. pseudintermedius. All 18 of the genetically diverse S. pseudintermedius strains sequenced and tested were inhibited by ≤ 12% (w/v) medical grade manuka honey, although tolerance to five clinically relevant antibiotics was observed. The susceptibility of the isolates to four of these antibiotics was significantly increased (p ≤0.05) when combined with sub lethal concentrations of honey, although sensitivity to oxacillin was decreased. Virulence (DNase, protease and haemolysin) activity was also significantly reduced (p ≤ 0.05) in over half of isolates when cultured with sub lethal concentrations of honey (13, 9 and 10 isolates respectively). These findings highlight the potential for manuka honey to be utilised against S. pseudintermedius infections. Importance: Staphylococcus pseudintermedius is an important member of the skin microbial community in animals and can cause opportunistic infections in both pets and their owners. The high incidence of antimicrobial resistance in S. pseudintermedius highlights that this opportunistic zoonotic pathogen can cause infections which require prolonged and intensive treatment to resolve. Manuka honey has proven efficacy against many bacterial pathogens and is an accepted topical treatment for infections in both veterinary and clinical practice so is a particularly appropriate antimicrobial for use with zoonotic pathogens such as S. pseudintermedius. Here we demonstrate that manuka honey is not only highly potent against novel multi-drug resistant S. pseudintermedius isolates, but also acts synergistically with clinically relevant antibiotics. In addition, manuka honey modulates S. pseudintermedius virulence activity, even at subinhibitory concentrations. In a clinical setting these attributes may assist in controlling infection, allowing a more rapid resolution and reducing antibiotic use.
published_date 2020-10-01T04:08:55Z
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