Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UFMG |
Texto Completo: | https://doi.org/10.1155/2022/1466011 http://hdl.handle.net/1843/61233 https://orcid.org/0000-0001-8402-1375 https://orcid.org/0000-0003-4511-3722 https://orcid.org/0000-0002-5753-624X https://orcid.org/0000-0002-7821-6392 https://orcid.org/0000-0002-8664-9753 https://orcid.org/0000-0002-6291-0515 https://orcid.org/0000-0002-0851-5610 https://orcid.org/0000-0002-1061-6445 https://orcid.org/0000-0002-1715-3834 https://orcid.org/0000-0002-5695-8256 |
Resumo: | Background. Asthma is a chronic pulmonary disease that affects about 300 million people worldwide. Previous studies have associated antimicrobial use with allergies, but the real impact of antibiotics on asthma is still elusive. We investigated the potential impact of amoxicillin (Amox), trimethoprim/sulfamethoxazole (TMP/SMX), and metronidazole (Metro) in a murine model of OVA-induced allergic airway inflammation. Methods. BALB/c mice received three cycles of 7 days of antibiotics in drinking water followed by 7 days washout and were sensitized i.p. with OVA/Alum at days 0 and 14. After the end of the last antibiotic washout, the mice were challenged with aerosolized OVA. Pulmonary parameters were evaluated, and serum, BAL, and feces were collected for analysis. Results. Amox- and TMP/SMX-treated animals displayed more severe allergic airway inflammation parameters with increased airway hyperresponsiveness, reduced lung alveolar volume, and increased levels in BAL of IL-4 and IL-6. In contrast, Metro-treated mice showed preserved FEV-50, decreased lung inflammation, and higher levels of butyrate and propionate in their feces. Metro treatment was associated with increased OVA-specific IgA in serum. BAL microbiota was abundant in allergic groups but not in nonallergic controls with the Amox-treated group displaying the increased frequency of Proteobacteria, while Metro and TMP/SMX showed increased levels of Firmicutes. In the gut, we observed the enrichment of Akkermansia muciniphila associated with reduced airway inflammation phenotype in the Metro group, even after the recovery period. Conclusion. Our data suggest that different antibiotic treatments may impact the course of experimental allergic airway inflammation in diverse ways by several mechanisms, including modulation of short-chain fat acids production by intestinal microbiota. |
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2023-11-21T21:15:45Z2023-11-21T21:15:45Z20222022https://doi.org/10.1155/2022/14660112314-7156http://hdl.handle.net/1843/61233https://orcid.org/0000-0001-8402-1375https://orcid.org/0000-0003-4511-3722https://orcid.org/0000-0002-5753-624Xhttps://orcid.org/0000-0002-7821-6392https://orcid.org/0000-0002-8664-9753https://orcid.org/0000-0002-6291-0515https://orcid.org/0000-0002-0851-5610https://orcid.org/0000-0002-1061-6445https://orcid.org/0000-0002-1715-3834https://orcid.org/0000-0002-5695-8256Background. Asthma is a chronic pulmonary disease that affects about 300 million people worldwide. Previous studies have associated antimicrobial use with allergies, but the real impact of antibiotics on asthma is still elusive. We investigated the potential impact of amoxicillin (Amox), trimethoprim/sulfamethoxazole (TMP/SMX), and metronidazole (Metro) in a murine model of OVA-induced allergic airway inflammation. Methods. BALB/c mice received three cycles of 7 days of antibiotics in drinking water followed by 7 days washout and were sensitized i.p. with OVA/Alum at days 0 and 14. After the end of the last antibiotic washout, the mice were challenged with aerosolized OVA. Pulmonary parameters were evaluated, and serum, BAL, and feces were collected for analysis. Results. Amox- and TMP/SMX-treated animals displayed more severe allergic airway inflammation parameters with increased airway hyperresponsiveness, reduced lung alveolar volume, and increased levels in BAL of IL-4 and IL-6. In contrast, Metro-treated mice showed preserved FEV-50, decreased lung inflammation, and higher levels of butyrate and propionate in their feces. Metro treatment was associated with increased OVA-specific IgA in serum. BAL microbiota was abundant in allergic groups but not in nonallergic controls with the Amox-treated group displaying the increased frequency of Proteobacteria, while Metro and TMP/SMX showed increased levels of Firmicutes. In the gut, we observed the enrichment of Akkermansia muciniphila associated with reduced airway inflammation phenotype in the Metro group, even after the recovery period. Conclusion. Our data suggest that different antibiotic treatments may impact the course of experimental allergic airway inflammation in diverse ways by several mechanisms, including modulation of short-chain fat acids production by intestinal microbiota.Fundo. A asma é uma doença pulmonar crônica que afeta cerca de 300 milhões de pessoas em todo o mundo. Estudos anteriores associaram o uso de antimicrobianos a alergias, mas o real impacto dos antibióticos na asma ainda é incerto. Nós investigamos o impacto potencial da amoxicilina (Amox), trimetoprim/sulfametoxazol (TMP/SMX) e metronidazol (Metro) em um modelo murino de inflamação alérgica das vias aéreas induzida por OVA. Métodos. Camundongos BALB/c receberam três ciclos de 7 dias de antibióticos em água potável seguidos de 7 dias de lavagem e foram sensibilizados i.p. com OVA/Alum nos dias 0 e 14. Após o final da última lavagem com antibiótico, os ratos foram desafiados com OVA em aerossol. Os parâmetros pulmonares foram avaliados e soro, LBA e fezes foram coletados para análise. Resultados. Os animais tratados com Amox e TMP / SMX apresentaram parâmetros de inflamação alérgica das vias aéreas mais graves, com aumento da hiperresponsividade das vias aéreas, redução do volume alveolar pulmonar e aumento dos níveis de IL-4 e IL-6 no LBA. Em contraste, os ratos tratados com Metro apresentaram FEV-50 preservado, diminuição da inflamação pulmonar e níveis mais elevados de butirato e propionato nas fezes. O tratamento com Metro foi associado ao aumento de IgA específica para OVA no soro. A microbiota BAL foi abundante em grupos alérgicos, mas não em controles não alérgicos, com o grupo tratado com Amox exibindo maior frequência de Proteobactérias, enquanto Metro e TMP/SMX mostraram níveis aumentados de Firmicutes. No intestino, observamos o enriquecimento de Akkermansia muciniphila associado à redução do fenótipo de inflamação das vias aéreas no grupo Metro, mesmo após o período de recuperação. Conclusão. Nossos dados sugerem que diferentes tratamentos com antibióticos podem impactar o curso da inflamação alérgica experimental das vias aéreas de diversas maneiras por vários mecanismos, incluindo a modulação da produção de ácidos graxos de cadeia curta pela microbiota intestinal.FAPEMIG - Fundação de Amparo à Pesquisa do Estado de Minas GeraisCAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível SuperiorengUniversidade Federal de Minas GeraisUFMGBrasilICB - DEPARTAMENTO DE BIOQUÍMICA E IMUNOLOGIAICB - DEPARTAMENTO DE FISIOLOGIA E BIOFÍSICAICB - DEPARTAMENTO DE MICROBIOLOGIAJournal of Immunology ResearchAsmaAntibióticosMicrobiotaAsthmaAntibioticsSymbiotic microbiotaTreatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiotaTratamento com classes distintas de antibióticos causa diferentes desfechos pulmonares na inflamação alérgica das vias aéreas associada à modulação da microbiota simbióticainfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://www.hindawi.com/journals/jir/2022/1466011/Gregório Grama CavalcanteAnna Gabriella GuimarãesCamila Pereira Queiroz-GlaussMarcela Helena Gonçalves PereiraAngélica Samer Lallo DiasLaila Sampaio HortaJamil Silvano de OliveiraSilvia Dantas CangussúPaula Prazeres MagalhãesRemo Castro RussoHelton da Costa Santiagoapplication/pdfinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFMGinstname:Universidade Federal de Minas Gerais (UFMG)instacron:UFMGLICENSELicense.txtLicense.txttext/plain; charset=utf-82042https://repositorio.ufmg.br/bitstream/1843/61233/1/License.txtfa505098d172de0bc8864fc1287ffe22MD51ORIGINALTreatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota.pdfTreatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota.pdfapplication/pdf11227803https://repositorio.ufmg.br/bitstream/1843/61233/2/Treatment%20with%20distinct%20antibiotic%20classes%20causes%20different%20pulmonary%20outcomes%20on%20allergic%20airway%20inflammation%20associated%20with%20modulation%20of%20symbiotic%20microbiota.pdf67a3247da8803b2e6bc3d9f136b144abMD521843/612332023-11-21 18:15:46.013oai:repositorio.ufmg.br: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Repositório de PublicaçõesPUBhttps://repositorio.ufmg.br/oaiopendoar:2023-11-21T21:15:46Repositório Institucional da UFMG - Universidade Federal de Minas Gerais (UFMG)false |
dc.title.pt_BR.fl_str_mv |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota |
dc.title.alternative.pt_BR.fl_str_mv |
Tratamento com classes distintas de antibióticos causa diferentes desfechos pulmonares na inflamação alérgica das vias aéreas associada à modulação da microbiota simbiótica |
title |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota |
spellingShingle |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota Gregório Grama Cavalcante Asthma Antibiotics Symbiotic microbiota Asma Antibióticos Microbiota |
title_short |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota |
title_full |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota |
title_fullStr |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota |
title_full_unstemmed |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota |
title_sort |
Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota |
author |
Gregório Grama Cavalcante |
author_facet |
Gregório Grama Cavalcante Anna Gabriella Guimarães Camila Pereira Queiroz-Glauss Marcela Helena Gonçalves Pereira Angélica Samer Lallo Dias Laila Sampaio Horta Jamil Silvano de Oliveira Silvia Dantas Cangussú Paula Prazeres Magalhães Remo Castro Russo Helton da Costa Santiago |
author_role |
author |
author2 |
Anna Gabriella Guimarães Camila Pereira Queiroz-Glauss Marcela Helena Gonçalves Pereira Angélica Samer Lallo Dias Laila Sampaio Horta Jamil Silvano de Oliveira Silvia Dantas Cangussú Paula Prazeres Magalhães Remo Castro Russo Helton da Costa Santiago |
author2_role |
author author author author author author author author author author |
dc.contributor.author.fl_str_mv |
Gregório Grama Cavalcante Anna Gabriella Guimarães Camila Pereira Queiroz-Glauss Marcela Helena Gonçalves Pereira Angélica Samer Lallo Dias Laila Sampaio Horta Jamil Silvano de Oliveira Silvia Dantas Cangussú Paula Prazeres Magalhães Remo Castro Russo Helton da Costa Santiago |
dc.subject.por.fl_str_mv |
Asthma Antibiotics Symbiotic microbiota |
topic |
Asthma Antibiotics Symbiotic microbiota Asma Antibióticos Microbiota |
dc.subject.other.pt_BR.fl_str_mv |
Asma Antibióticos Microbiota |
description |
Background. Asthma is a chronic pulmonary disease that affects about 300 million people worldwide. Previous studies have associated antimicrobial use with allergies, but the real impact of antibiotics on asthma is still elusive. We investigated the potential impact of amoxicillin (Amox), trimethoprim/sulfamethoxazole (TMP/SMX), and metronidazole (Metro) in a murine model of OVA-induced allergic airway inflammation. Methods. BALB/c mice received three cycles of 7 days of antibiotics in drinking water followed by 7 days washout and were sensitized i.p. with OVA/Alum at days 0 and 14. After the end of the last antibiotic washout, the mice were challenged with aerosolized OVA. Pulmonary parameters were evaluated, and serum, BAL, and feces were collected for analysis. Results. Amox- and TMP/SMX-treated animals displayed more severe allergic airway inflammation parameters with increased airway hyperresponsiveness, reduced lung alveolar volume, and increased levels in BAL of IL-4 and IL-6. In contrast, Metro-treated mice showed preserved FEV-50, decreased lung inflammation, and higher levels of butyrate and propionate in their feces. Metro treatment was associated with increased OVA-specific IgA in serum. BAL microbiota was abundant in allergic groups but not in nonallergic controls with the Amox-treated group displaying the increased frequency of Proteobacteria, while Metro and TMP/SMX showed increased levels of Firmicutes. In the gut, we observed the enrichment of Akkermansia muciniphila associated with reduced airway inflammation phenotype in the Metro group, even after the recovery period. Conclusion. Our data suggest that different antibiotic treatments may impact the course of experimental allergic airway inflammation in diverse ways by several mechanisms, including modulation of short-chain fat acids production by intestinal microbiota. |
publishDate |
2022 |
dc.date.issued.fl_str_mv |
2022 |
dc.date.accessioned.fl_str_mv |
2023-11-21T21:15:45Z |
dc.date.available.fl_str_mv |
2023-11-21T21:15:45Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/1843/61233 |
dc.identifier.doi.pt_BR.fl_str_mv |
https://doi.org/10.1155/2022/1466011 |
dc.identifier.issn.pt_BR.fl_str_mv |
2314-7156 |
dc.identifier.orcid.pt_BR.fl_str_mv |
https://orcid.org/0000-0001-8402-1375 https://orcid.org/0000-0003-4511-3722 https://orcid.org/0000-0002-5753-624X https://orcid.org/0000-0002-7821-6392 https://orcid.org/0000-0002-8664-9753 https://orcid.org/0000-0002-6291-0515 https://orcid.org/0000-0002-0851-5610 https://orcid.org/0000-0002-1061-6445 https://orcid.org/0000-0002-1715-3834 https://orcid.org/0000-0002-5695-8256 |
url |
https://doi.org/10.1155/2022/1466011 http://hdl.handle.net/1843/61233 https://orcid.org/0000-0001-8402-1375 https://orcid.org/0000-0003-4511-3722 https://orcid.org/0000-0002-5753-624X https://orcid.org/0000-0002-7821-6392 https://orcid.org/0000-0002-8664-9753 https://orcid.org/0000-0002-6291-0515 https://orcid.org/0000-0002-0851-5610 https://orcid.org/0000-0002-1061-6445 https://orcid.org/0000-0002-1715-3834 https://orcid.org/0000-0002-5695-8256 |
identifier_str_mv |
2314-7156 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.ispartof.pt_BR.fl_str_mv |
Journal of Immunology Research |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
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openAccess |
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application/pdf |
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Universidade Federal de Minas Gerais |
dc.publisher.initials.fl_str_mv |
UFMG |
dc.publisher.country.fl_str_mv |
Brasil |
dc.publisher.department.fl_str_mv |
ICB - DEPARTAMENTO DE BIOQUÍMICA E IMUNOLOGIA ICB - DEPARTAMENTO DE FISIOLOGIA E BIOFÍSICA ICB - DEPARTAMENTO DE MICROBIOLOGIA |
publisher.none.fl_str_mv |
Universidade Federal de Minas Gerais |
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reponame:Repositório Institucional da UFMG instname:Universidade Federal de Minas Gerais (UFMG) instacron:UFMG |
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