The liquid Kangfuxin (KFX) has efficient antifungal activity and can be used in the treatment of vulvovaginal candidiasis in mice

Vulvovaginal candidiasis (VVC) is an infectious disease caused mainly by Candida albicans. Kangfuxin (KFX) is a traditional Chinese medicine preparation made from Periplaneta americana extracts, which promotes wound healing and enhances body immunity and also acts as an antifungal agent. Here, we ev...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Letters in applied microbiology 2022-04, Vol.74 (4), p.564-576
Hauptverfasser: Ma, J., Yang, Y.‐C., Su, L.‐Q., Qin, D.‐M., Yuan, K., Zhang, Y., Wang, R.‐R.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 576
container_issue 4
container_start_page 564
container_title Letters in applied microbiology
container_volume 74
creator Ma, J.
Yang, Y.‐C.
Su, L.‐Q.
Qin, D.‐M.
Yuan, K.
Zhang, Y.
Wang, R.‐R.
description Vulvovaginal candidiasis (VVC) is an infectious disease caused mainly by Candida albicans. Kangfuxin (KFX) is a traditional Chinese medicine preparation made from Periplaneta americana extracts, which promotes wound healing and enhances body immunity and also acts as an antifungal agent. Here, we evaluated the effect of KFX in the treatment of VVC in vitro and in vivo. The minimum inhibitory concentration (MIC50) of KFX against C. albicans ranged from 7·65 to 20·57%. In addition, KFX was more efficient than fluconazole (FLC) in inhibiting the drug‐resistant C. albicans, and the effect was more intense after 8 h. The KFX treatment also exhibited good activity in vivo. It restored the body weight and reduced the vulvovaginal symptoms in mice induced with VVC. It downregulated the expression of the hyphae‐related gene, HWP1, thus inhibiting the growth and development of C. albicans hyphae. It also increased the number of neutrophils and promoted the secretion of interleukin‐17A (IL‐17A); however, the levels of interleukin‐8 (IL‐8) and interleukin‐1β (IL‐1β) decreased in mice with VVC. We deduce that KFX effectively treats vaginal candidiasis in two ways: by inhibiting the growth and development of mycelia to reduce colonization of C. albicans and by promoting the secretion and release of IL‐17A and neutrophils in high numbers to fight C. albicans infection. This study provides a theoretical basis for the use of KFX for the clinical treatment of VVC. Significance and Impact of the Study: Vulvovaginal candidiasis (VVC) is an infectious disease of the female external reproductive tract, caused by the ecological imbalance in the vagina due to the influence of various pathogenic factors, which brings harm to women's physical and mental health. However, the availability of drugs is limited and the frequency of drug‐resistant Candida isolates is increasing. It is urgent to find new drugs or effective treatment strategies. We found that Kangfuxin liquid (KFX) can be used to treat VVC by reducing mycelial growth and boosting immunity, which presents a new clinical alternative.
doi_str_mv 10.1111/lam.13641
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2615122743</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2639037936</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3531-ccaf470527a7119b6cd096c0fd7dbc3c954a02d967fd7bf5283161ff9bb759953</originalsourceid><addsrcrecordid>eNp10ctKAzEUBuAgitbLwheQgJu6mJrLJGmWUqyKFTcK3Q2ZXGpkLjqZVLv0zU2tuhDM5sDhOz-BH4BjjEY4vfNK1SNMeY63wADngmSCs_k2GCDCeTYmLN8D-yE8I4TGmMhdsEdzycYC0QH4eHiysPKv0Rt4q5qFi---gcPb6fwMPqkArXNee9v0UDW9d7FZqAoq3ful71dpZ6BWDSwtjMEamE77lNd3VvX1-qh1cBmrZbtUC9-ky4SNN14FH9a49toegh2nqmCPvucBeJxePkyus9n91c3kYpZpyijOtFYuF4gRoQTGsuTaIMk1ckaYUlMtWa4QMZKLtCkdI2OKOXZOlqVgUjJ6AIab3JeufY029EXtg7ZVpRrbxlAQjhkmROQ00dM_9LmNXfr_WlGJqJCUJ3W2UbprQ-isK146X6tuVWBUrHspUi_FVy_JnnwnxrK25lf-FJHA-Qa8-cqu_k8qZhd3m8hPqZiXLQ</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2639037936</pqid></control><display><type>article</type><title>The liquid Kangfuxin (KFX) has efficient antifungal activity and can be used in the treatment of vulvovaginal candidiasis in mice</title><source>Oxford University Press Journals All Titles (1996-Current)</source><source>MEDLINE</source><source>Wiley Online Library All Journals</source><creator>Ma, J. ; Yang, Y.‐C. ; Su, L.‐Q. ; Qin, D.‐M. ; Yuan, K. ; Zhang, Y. ; Wang, R.‐R.</creator><creatorcontrib>Ma, J. ; Yang, Y.‐C. ; Su, L.‐Q. ; Qin, D.‐M. ; Yuan, K. ; Zhang, Y. ; Wang, R.‐R.</creatorcontrib><description>Vulvovaginal candidiasis (VVC) is an infectious disease caused mainly by Candida albicans. Kangfuxin (KFX) is a traditional Chinese medicine preparation made from Periplaneta americana extracts, which promotes wound healing and enhances body immunity and also acts as an antifungal agent. Here, we evaluated the effect of KFX in the treatment of VVC in vitro and in vivo. The minimum inhibitory concentration (MIC50) of KFX against C. albicans ranged from 7·65 to 20·57%. In addition, KFX was more efficient than fluconazole (FLC) in inhibiting the drug‐resistant C. albicans, and the effect was more intense after 8 h. The KFX treatment also exhibited good activity in vivo. It restored the body weight and reduced the vulvovaginal symptoms in mice induced with VVC. It downregulated the expression of the hyphae‐related gene, HWP1, thus inhibiting the growth and development of C. albicans hyphae. It also increased the number of neutrophils and promoted the secretion of interleukin‐17A (IL‐17A); however, the levels of interleukin‐8 (IL‐8) and interleukin‐1β (IL‐1β) decreased in mice with VVC. We deduce that KFX effectively treats vaginal candidiasis in two ways: by inhibiting the growth and development of mycelia to reduce colonization of C. albicans and by promoting the secretion and release of IL‐17A and neutrophils in high numbers to fight C. albicans infection. This study provides a theoretical basis for the use of KFX for the clinical treatment of VVC. Significance and Impact of the Study: Vulvovaginal candidiasis (VVC) is an infectious disease of the female external reproductive tract, caused by the ecological imbalance in the vagina due to the influence of various pathogenic factors, which brings harm to women's physical and mental health. However, the availability of drugs is limited and the frequency of drug‐resistant Candida isolates is increasing. It is urgent to find new drugs or effective treatment strategies. We found that Kangfuxin liquid (KFX) can be used to treat VVC by reducing mycelial growth and boosting immunity, which presents a new clinical alternative.</description><identifier>ISSN: 0266-8254</identifier><identifier>EISSN: 1472-765X</identifier><identifier>DOI: 10.1111/lam.13641</identifier><identifier>PMID: 34958703</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Animals ; antifungal ; Antifungal activity ; Antifungal Agents - pharmacology ; Antifungal Agents - therapeutic use ; Body weight ; Candida albicans ; Candidiasis ; Candidiasis, Vulvovaginal - drug therapy ; Candidiasis, Vulvovaginal - microbiology ; Colonization ; Cytokines ; Female ; Fluconazole ; Fluconazole - pharmacology ; Fluconazole - therapeutic use ; Fungicides ; Health services ; Herbal medicine ; Hyphae ; Infectious diseases ; Interleukins ; Kangfuxin liquid ; Leukocytes (neutrophilic) ; Materia Medica - pharmacology ; Materia Medica - therapeutic use ; Mice ; Minimum inhibitory concentration ; murine model ; Mycelia ; Neutrophils ; Signs and symptoms ; Traditional Chinese medicine ; vaginal candidiasis ; Weight reduction ; Wound healing</subject><ispartof>Letters in applied microbiology, 2022-04, Vol.74 (4), p.564-576</ispartof><rights>2021 The Society for Applied Microbiology</rights><rights>2021 The Society for Applied Microbiology.</rights><rights>Copyright © 2022 The Society for Applied Microbiology</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3531-ccaf470527a7119b6cd096c0fd7dbc3c954a02d967fd7bf5283161ff9bb759953</citedby><cites>FETCH-LOGICAL-c3531-ccaf470527a7119b6cd096c0fd7dbc3c954a02d967fd7bf5283161ff9bb759953</cites><orcidid>0000-0003-3014-012X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Flam.13641$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Flam.13641$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34958703$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ma, J.</creatorcontrib><creatorcontrib>Yang, Y.‐C.</creatorcontrib><creatorcontrib>Su, L.‐Q.</creatorcontrib><creatorcontrib>Qin, D.‐M.</creatorcontrib><creatorcontrib>Yuan, K.</creatorcontrib><creatorcontrib>Zhang, Y.</creatorcontrib><creatorcontrib>Wang, R.‐R.</creatorcontrib><title>The liquid Kangfuxin (KFX) has efficient antifungal activity and can be used in the treatment of vulvovaginal candidiasis in mice</title><title>Letters in applied microbiology</title><addtitle>Lett Appl Microbiol</addtitle><description>Vulvovaginal candidiasis (VVC) is an infectious disease caused mainly by Candida albicans. Kangfuxin (KFX) is a traditional Chinese medicine preparation made from Periplaneta americana extracts, which promotes wound healing and enhances body immunity and also acts as an antifungal agent. Here, we evaluated the effect of KFX in the treatment of VVC in vitro and in vivo. The minimum inhibitory concentration (MIC50) of KFX against C. albicans ranged from 7·65 to 20·57%. In addition, KFX was more efficient than fluconazole (FLC) in inhibiting the drug‐resistant C. albicans, and the effect was more intense after 8 h. The KFX treatment also exhibited good activity in vivo. It restored the body weight and reduced the vulvovaginal symptoms in mice induced with VVC. It downregulated the expression of the hyphae‐related gene, HWP1, thus inhibiting the growth and development of C. albicans hyphae. It also increased the number of neutrophils and promoted the secretion of interleukin‐17A (IL‐17A); however, the levels of interleukin‐8 (IL‐8) and interleukin‐1β (IL‐1β) decreased in mice with VVC. We deduce that KFX effectively treats vaginal candidiasis in two ways: by inhibiting the growth and development of mycelia to reduce colonization of C. albicans and by promoting the secretion and release of IL‐17A and neutrophils in high numbers to fight C. albicans infection. This study provides a theoretical basis for the use of KFX for the clinical treatment of VVC. Significance and Impact of the Study: Vulvovaginal candidiasis (VVC) is an infectious disease of the female external reproductive tract, caused by the ecological imbalance in the vagina due to the influence of various pathogenic factors, which brings harm to women's physical and mental health. However, the availability of drugs is limited and the frequency of drug‐resistant Candida isolates is increasing. It is urgent to find new drugs or effective treatment strategies. We found that Kangfuxin liquid (KFX) can be used to treat VVC by reducing mycelial growth and boosting immunity, which presents a new clinical alternative.</description><subject>Animals</subject><subject>antifungal</subject><subject>Antifungal activity</subject><subject>Antifungal Agents - pharmacology</subject><subject>Antifungal Agents - therapeutic use</subject><subject>Body weight</subject><subject>Candida albicans</subject><subject>Candidiasis</subject><subject>Candidiasis, Vulvovaginal - drug therapy</subject><subject>Candidiasis, Vulvovaginal - microbiology</subject><subject>Colonization</subject><subject>Cytokines</subject><subject>Female</subject><subject>Fluconazole</subject><subject>Fluconazole - pharmacology</subject><subject>Fluconazole - therapeutic use</subject><subject>Fungicides</subject><subject>Health services</subject><subject>Herbal medicine</subject><subject>Hyphae</subject><subject>Infectious diseases</subject><subject>Interleukins</subject><subject>Kangfuxin liquid</subject><subject>Leukocytes (neutrophilic)</subject><subject>Materia Medica - pharmacology</subject><subject>Materia Medica - therapeutic use</subject><subject>Mice</subject><subject>Minimum inhibitory concentration</subject><subject>murine model</subject><subject>Mycelia</subject><subject>Neutrophils</subject><subject>Signs and symptoms</subject><subject>Traditional Chinese medicine</subject><subject>vaginal candidiasis</subject><subject>Weight reduction</subject><subject>Wound healing</subject><issn>0266-8254</issn><issn>1472-765X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10ctKAzEUBuAgitbLwheQgJu6mJrLJGmWUqyKFTcK3Q2ZXGpkLjqZVLv0zU2tuhDM5sDhOz-BH4BjjEY4vfNK1SNMeY63wADngmSCs_k2GCDCeTYmLN8D-yE8I4TGmMhdsEdzycYC0QH4eHiysPKv0Rt4q5qFi---gcPb6fwMPqkArXNee9v0UDW9d7FZqAoq3ful71dpZ6BWDSwtjMEamE77lNd3VvX1-qh1cBmrZbtUC9-ky4SNN14FH9a49toegh2nqmCPvucBeJxePkyus9n91c3kYpZpyijOtFYuF4gRoQTGsuTaIMk1ckaYUlMtWa4QMZKLtCkdI2OKOXZOlqVgUjJ6AIab3JeufY029EXtg7ZVpRrbxlAQjhkmROQ00dM_9LmNXfr_WlGJqJCUJ3W2UbprQ-isK146X6tuVWBUrHspUi_FVy_JnnwnxrK25lf-FJHA-Qa8-cqu_k8qZhd3m8hPqZiXLQ</recordid><startdate>202204</startdate><enddate>202204</enddate><creator>Ma, J.</creator><creator>Yang, Y.‐C.</creator><creator>Su, L.‐Q.</creator><creator>Qin, D.‐M.</creator><creator>Yuan, K.</creator><creator>Zhang, Y.</creator><creator>Wang, R.‐R.</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3014-012X</orcidid></search><sort><creationdate>202204</creationdate><title>The liquid Kangfuxin (KFX) has efficient antifungal activity and can be used in the treatment of vulvovaginal candidiasis in mice</title><author>Ma, J. ; Yang, Y.‐C. ; Su, L.‐Q. ; Qin, D.‐M. ; Yuan, K. ; Zhang, Y. ; Wang, R.‐R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3531-ccaf470527a7119b6cd096c0fd7dbc3c954a02d967fd7bf5283161ff9bb759953</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>antifungal</topic><topic>Antifungal activity</topic><topic>Antifungal Agents - pharmacology</topic><topic>Antifungal Agents - therapeutic use</topic><topic>Body weight</topic><topic>Candida albicans</topic><topic>Candidiasis</topic><topic>Candidiasis, Vulvovaginal - drug therapy</topic><topic>Candidiasis, Vulvovaginal - microbiology</topic><topic>Colonization</topic><topic>Cytokines</topic><topic>Female</topic><topic>Fluconazole</topic><topic>Fluconazole - pharmacology</topic><topic>Fluconazole - therapeutic use</topic><topic>Fungicides</topic><topic>Health services</topic><topic>Herbal medicine</topic><topic>Hyphae</topic><topic>Infectious diseases</topic><topic>Interleukins</topic><topic>Kangfuxin liquid</topic><topic>Leukocytes (neutrophilic)</topic><topic>Materia Medica - pharmacology</topic><topic>Materia Medica - therapeutic use</topic><topic>Mice</topic><topic>Minimum inhibitory concentration</topic><topic>murine model</topic><topic>Mycelia</topic><topic>Neutrophils</topic><topic>Signs and symptoms</topic><topic>Traditional Chinese medicine</topic><topic>vaginal candidiasis</topic><topic>Weight reduction</topic><topic>Wound healing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ma, J.</creatorcontrib><creatorcontrib>Yang, Y.‐C.</creatorcontrib><creatorcontrib>Su, L.‐Q.</creatorcontrib><creatorcontrib>Qin, D.‐M.</creatorcontrib><creatorcontrib>Yuan, K.</creatorcontrib><creatorcontrib>Zhang, Y.</creatorcontrib><creatorcontrib>Wang, R.‐R.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Letters in applied microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ma, J.</au><au>Yang, Y.‐C.</au><au>Su, L.‐Q.</au><au>Qin, D.‐M.</au><au>Yuan, K.</au><au>Zhang, Y.</au><au>Wang, R.‐R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The liquid Kangfuxin (KFX) has efficient antifungal activity and can be used in the treatment of vulvovaginal candidiasis in mice</atitle><jtitle>Letters in applied microbiology</jtitle><addtitle>Lett Appl Microbiol</addtitle><date>2022-04</date><risdate>2022</risdate><volume>74</volume><issue>4</issue><spage>564</spage><epage>576</epage><pages>564-576</pages><issn>0266-8254</issn><eissn>1472-765X</eissn><abstract>Vulvovaginal candidiasis (VVC) is an infectious disease caused mainly by Candida albicans. Kangfuxin (KFX) is a traditional Chinese medicine preparation made from Periplaneta americana extracts, which promotes wound healing and enhances body immunity and also acts as an antifungal agent. Here, we evaluated the effect of KFX in the treatment of VVC in vitro and in vivo. The minimum inhibitory concentration (MIC50) of KFX against C. albicans ranged from 7·65 to 20·57%. In addition, KFX was more efficient than fluconazole (FLC) in inhibiting the drug‐resistant C. albicans, and the effect was more intense after 8 h. The KFX treatment also exhibited good activity in vivo. It restored the body weight and reduced the vulvovaginal symptoms in mice induced with VVC. It downregulated the expression of the hyphae‐related gene, HWP1, thus inhibiting the growth and development of C. albicans hyphae. It also increased the number of neutrophils and promoted the secretion of interleukin‐17A (IL‐17A); however, the levels of interleukin‐8 (IL‐8) and interleukin‐1β (IL‐1β) decreased in mice with VVC. We deduce that KFX effectively treats vaginal candidiasis in two ways: by inhibiting the growth and development of mycelia to reduce colonization of C. albicans and by promoting the secretion and release of IL‐17A and neutrophils in high numbers to fight C. albicans infection. This study provides a theoretical basis for the use of KFX for the clinical treatment of VVC. Significance and Impact of the Study: Vulvovaginal candidiasis (VVC) is an infectious disease of the female external reproductive tract, caused by the ecological imbalance in the vagina due to the influence of various pathogenic factors, which brings harm to women's physical and mental health. However, the availability of drugs is limited and the frequency of drug‐resistant Candida isolates is increasing. It is urgent to find new drugs or effective treatment strategies. We found that Kangfuxin liquid (KFX) can be used to treat VVC by reducing mycelial growth and boosting immunity, which presents a new clinical alternative.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>34958703</pmid><doi>10.1111/lam.13641</doi><tpages>576</tpages><orcidid>https://orcid.org/0000-0003-3014-012X</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 0266-8254
ispartof Letters in applied microbiology, 2022-04, Vol.74 (4), p.564-576
issn 0266-8254
1472-765X
language eng
recordid cdi_proquest_miscellaneous_2615122743
source Oxford University Press Journals All Titles (1996-Current); MEDLINE; Wiley Online Library All Journals
subjects Animals
antifungal
Antifungal activity
Antifungal Agents - pharmacology
Antifungal Agents - therapeutic use
Body weight
Candida albicans
Candidiasis
Candidiasis, Vulvovaginal - drug therapy
Candidiasis, Vulvovaginal - microbiology
Colonization
Cytokines
Female
Fluconazole
Fluconazole - pharmacology
Fluconazole - therapeutic use
Fungicides
Health services
Herbal medicine
Hyphae
Infectious diseases
Interleukins
Kangfuxin liquid
Leukocytes (neutrophilic)
Materia Medica - pharmacology
Materia Medica - therapeutic use
Mice
Minimum inhibitory concentration
murine model
Mycelia
Neutrophils
Signs and symptoms
Traditional Chinese medicine
vaginal candidiasis
Weight reduction
Wound healing
title The liquid Kangfuxin (KFX) has efficient antifungal activity and can be used in the treatment of vulvovaginal candidiasis in mice
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T04%3A39%3A32IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20liquid%20Kangfuxin%20(KFX)%20has%20efficient%20antifungal%20activity%20and%20can%20be%20used%20in%20the%20treatment%20of%20vulvovaginal%20candidiasis%20in%20mice&rft.jtitle=Letters%20in%20applied%20microbiology&rft.au=Ma,%20J.&rft.date=2022-04&rft.volume=74&rft.issue=4&rft.spage=564&rft.epage=576&rft.pages=564-576&rft.issn=0266-8254&rft.eissn=1472-765X&rft_id=info:doi/10.1111/lam.13641&rft_dat=%3Cproquest_cross%3E2639037936%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2639037936&rft_id=info:pmid/34958703&rfr_iscdi=true