Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contacts
ABSTRACT This study investigated the gut microbiome dynamics of index patients colonized with extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) (n = 5) or extended-spectrum beta-lactamase-producing Klebsiella pneumoniae (ESBL-Kp) (n = 3) and their household contacts (n = 9) up to...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01275-23 |
| _version_ | 1797393692942663680 |
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| author | Janetta Top Tess D. Verschuuren Marco C. Viveen M. Eugenia Riccio Stephan Harbarth Jan A. J. W. Kluytmans Rob J. L. Willems Fernanda L. Paganelli |
| author_facet | Janetta Top Tess D. Verschuuren Marco C. Viveen M. Eugenia Riccio Stephan Harbarth Jan A. J. W. Kluytmans Rob J. L. Willems Fernanda L. Paganelli |
| author_sort | Janetta Top |
| collection | DOAJ |
| description | ABSTRACT This study investigated the gut microbiome dynamics of index patients colonized with extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) (n = 5) or extended-spectrum beta-lactamase-producing Klebsiella pneumoniae (ESBL-Kp) (n = 3) and their household contacts (n = 9) up to 4 months after hospital discharge of the index patient using 16S rRNA amplicon gene sequencing. Samples were collected at the day of hospital discharge of the index patient, 1 week and 2 and 4 months after discharge. Compared to household contacts, we observed a significant lower alpha diversity (P < 0.001) among index patients and significant (P < 0.05) separation between the two groups for beta diversity. Principal component analysis of the samples from each household (i.e., index patient and respective household contact) showed a clear shift in microbiome composition, in 4/8 index patients, from dissimilar to more similar to the household contact group. This suggests recovery of the microbiome to a healthier status, which was also reflected by de novo colonization of (health-associated) taxa. In contrast, the four time-point samples of the household contacts clustered together indicating a stable microbiome composition over time irrespective of low-level ESBL-Ec (n = 3) or ESBL-Kp (n = 2) colonization. In conclusion, here we show that, at the day of hospital discharge, the microbiome composition of index patients is dissimilar from that of household contacts. Over time, signals of microbiome recovery were observed in half of the index patients. The stable microbiome composition in household contacts irrespective of low-level ESBL-Ec or ESBL-Kp colonization suggests that the gut microbiome in these healthy people provided colonization resistance against ESBL-PE outgrowth. IMPORTANCE Colonization with extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-PE) often precedes infections and is therefore considered as a great threat for public health. Here, we studied the gut microbiome dynamics in eight index patients colonized with ESBL-PE after hospital discharge and the impact of exposure to this index patient on the gut microbiome dynamics of their household contacts. We showed that the microbiome composition from index patients is different from their household contacts upon hospital discharge and that, in some of the index patients, their microbiome composition over time shifted toward the composition of their household contacts. In contrast, household contacts showed a stable microbiome composition over time irrespective of low-level extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) or extended-spectrum beta-lactamase-producing Klebsiella pneumoniae (ESBL-Kp) gut colonization, suggesting that, in healthy microbiomes, colonization resistance is able to prevent ESBL-PE expansion. |
| first_indexed | 2024-03-09T00:06:36Z |
| format | Article |
| id | doaj.art-be908a5af40a4cf08dd951b82cbb467d |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:36Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-be908a5af40a4cf08dd951b82cbb467d2023-12-12T13:17:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.01275-23Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contactsJanetta Top0Tess D. Verschuuren1Marco C. Viveen2M. Eugenia Riccio3Stephan Harbarth4Jan A. J. W. Kluytmans5Rob J. L. Willems6Fernanda L. Paganelli7Department of Medical Microbiology, University Medical Center Utrecht , Utrecht, the NetherlandsMahidol Oxford Tropical Medicine Research Unit (MORU) , Bangkok, ThailandDepartment of Medical Microbiology, University Medical Center Utrecht , Utrecht, the NetherlandsUniversity of Geneva Hospitals and Faculty of Medicine, Infection Control Program, WHO Collaborating Center , Geneva, SwitzerlandUniversity of Geneva Hospitals and Faculty of Medicine, Infection Control Program, WHO Collaborating Center , Geneva, SwitzerlandDepartment of Medical Microbiology, University Medical Center Utrecht , Utrecht, the NetherlandsDepartment of Medical Microbiology, University Medical Center Utrecht , Utrecht, the NetherlandsDepartment of Medical Microbiology, University Medical Center Utrecht , Utrecht, the NetherlandsABSTRACT This study investigated the gut microbiome dynamics of index patients colonized with extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) (n = 5) or extended-spectrum beta-lactamase-producing Klebsiella pneumoniae (ESBL-Kp) (n = 3) and their household contacts (n = 9) up to 4 months after hospital discharge of the index patient using 16S rRNA amplicon gene sequencing. Samples were collected at the day of hospital discharge of the index patient, 1 week and 2 and 4 months after discharge. Compared to household contacts, we observed a significant lower alpha diversity (P < 0.001) among index patients and significant (P < 0.05) separation between the two groups for beta diversity. Principal component analysis of the samples from each household (i.e., index patient and respective household contact) showed a clear shift in microbiome composition, in 4/8 index patients, from dissimilar to more similar to the household contact group. This suggests recovery of the microbiome to a healthier status, which was also reflected by de novo colonization of (health-associated) taxa. In contrast, the four time-point samples of the household contacts clustered together indicating a stable microbiome composition over time irrespective of low-level ESBL-Ec (n = 3) or ESBL-Kp (n = 2) colonization. In conclusion, here we show that, at the day of hospital discharge, the microbiome composition of index patients is dissimilar from that of household contacts. Over time, signals of microbiome recovery were observed in half of the index patients. The stable microbiome composition in household contacts irrespective of low-level ESBL-Ec or ESBL-Kp colonization suggests that the gut microbiome in these healthy people provided colonization resistance against ESBL-PE outgrowth. IMPORTANCE Colonization with extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-PE) often precedes infections and is therefore considered as a great threat for public health. Here, we studied the gut microbiome dynamics in eight index patients colonized with ESBL-PE after hospital discharge and the impact of exposure to this index patient on the gut microbiome dynamics of their household contacts. We showed that the microbiome composition from index patients is different from their household contacts upon hospital discharge and that, in some of the index patients, their microbiome composition over time shifted toward the composition of their household contacts. In contrast, household contacts showed a stable microbiome composition over time irrespective of low-level extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) or extended-spectrum beta-lactamase-producing Klebsiella pneumoniae (ESBL-Kp) gut colonization, suggesting that, in healthy microbiomes, colonization resistance is able to prevent ESBL-PE expansion.https://journals.asm.org/doi/10.1128/spectrum.01275-23ESBL-Enterobacteralesgut microbiome dynamicsindex patienthousehold contacts |
| spellingShingle | Janetta Top Tess D. Verschuuren Marco C. Viveen M. Eugenia Riccio Stephan Harbarth Jan A. J. W. Kluytmans Rob J. L. Willems Fernanda L. Paganelli Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contacts Microbiology Spectrum ESBL-Enterobacterales gut microbiome dynamics index patient household contacts |
| title | Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contacts |
| title_full | Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contacts |
| title_fullStr | Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contacts |
| title_full_unstemmed | Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contacts |
| title_short | Gut microbiome dynamics in index patients colonized with extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales after hospital discharge and their household contacts |
| title_sort | gut microbiome dynamics in index patients colonized with extended spectrum beta lactamase esbl producing enterobacterales after hospital discharge and their household contacts |
| topic | ESBL-Enterobacterales gut microbiome dynamics index patient household contacts |
| url | https://journals.asm.org/doi/10.1128/spectrum.01275-23 |
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