Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland
BackgroundThe involvement of non-human-to-human transmission of extended-spectrum β-lactamase-producing Enterobacterales (ESBL-PE) remains elusive. Foodstuffs may serve as reservoirs for ESBL-PE and contribute to their spread.AimWe aimed to systematically investigate the presence and spatiotemporal...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1295037/full |
| _version_ | 1827662073686917120 |
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| author | Elena Gómez-Sanz Elena Gómez-Sanz Claudia Bagutti Ana B. García-Martín Ana B. García-Martín Jan A. Roth Monica Alt Hug Laura Maurer Pekerman Laura Maurer Pekerman Ruth Schindler Ruth Schindler Reto Furger Lucas Eichenberger Ingrid Steffen Philipp Hübner Tanja Stadler Lisandra Aguilar-Bultet Lisandra Aguilar-Bultet Sarah Tschudin-Sutter Sarah Tschudin-Sutter |
| author_facet | Elena Gómez-Sanz Elena Gómez-Sanz Claudia Bagutti Ana B. García-Martín Ana B. García-Martín Jan A. Roth Monica Alt Hug Laura Maurer Pekerman Laura Maurer Pekerman Ruth Schindler Ruth Schindler Reto Furger Lucas Eichenberger Ingrid Steffen Philipp Hübner Tanja Stadler Lisandra Aguilar-Bultet Lisandra Aguilar-Bultet Sarah Tschudin-Sutter Sarah Tschudin-Sutter |
| author_sort | Elena Gómez-Sanz |
| collection | DOAJ |
| description | BackgroundThe involvement of non-human-to-human transmission of extended-spectrum β-lactamase-producing Enterobacterales (ESBL-PE) remains elusive. Foodstuffs may serve as reservoirs for ESBL-PE and contribute to their spread.AimWe aimed to systematically investigate the presence and spatiotemporal distribution of ESBL-PE in diverse unprocessed foodstuffs of different origin purchased in a central European city.MethodsChicken and green (herbs, salad, sprouts, vegetables) samples were collected monthly for two consecutive years, from June 2017 to June 2019, from large supermarket chains and small local food retailers, representing all ten postcode areas of the City of Basel (Switzerland), and the kitchen of the University Hospital Basel (Basel, Switzerland). After enrichment, presumptive ESBL-PE were isolated by selective culture methods and identified by Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. ESBL production was confirmed by phenotypic testing.ResultsAmong 947 food samples, 14.8% were positive for ESBL-PE isolate/s belonging to eight different ESBL-producing bacterial species. Escherichia coli and Serratia fonticola were predominant across samples (9 and 2%, respectively). Higher ESBL-PE prevalence was observed in chicken (25.9%) than in green (3.8%) samples (p < 0.001). Among greens, ESBL-PE were most frequently isolated from sprouts (15.2%). High ESBL-PE species diversity was observed among chicken samples, with E. coli as predominant (17.6%). ESBL-producing Enterobacter cloacae was detected among different greens. Yet, ESBL-producing Klebsiella pneumoniae was predominant in sprouts (12.1%). In total, 20.5% of samples from organic farming and 14.2% of samples from conventionally raised animals harbored an ESBL-producing isolate. Detection of ESBL-PE across samples differed between organic and non-organic when stratified by food source (p < 0.001), particularly among greens (12.5% organic, 2.4% conventional). High proportion of organic chicken samples was positive for ESBL-E. coli (33.3%), while the detection of several species characterized the conventional chicken samples. No significant differences in ESBL-PE frequences were detected between national (13.4%) and international samples (8.0%) (p = 0.122). Instead, differences were observed between regions of food production and countries (p < 0.001). No significant differences were found when comparing the proportion of ESBL-PE positive samples across districts, shop sizes and the hospital kitchen. The percentage of ESBL-PE positive samples did not differ monthly across the two-year sampling period (p = 0.107).ConclusionOur findings indicate moderate dissemination of ESBL-PE in foodstuffs, especially between chicken products and sprouts. Chicken meat represents a source for several ESBL-producing Enterobacterales, especially E. coli, while greens are more prone to carry ESBL-K. pneumoniae and E. cloacae. We disclose the importance of food type, food production system and production origin when assessing the risk of contamination with different ESBL-PE species. |
| first_indexed | 2024-03-10T00:20:03Z |
| format | Article |
| id | doaj.art-9e6f8757ef9f446a99793809ffec0250 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-10T00:20:03Z |
| publishDate | 2023-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-9e6f8757ef9f446a99793809ffec02502023-11-23T15:44:52ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-11-011410.3389/fmicb.2023.12950371295037Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, SwitzerlandElena Gómez-Sanz0Elena Gómez-Sanz1Claudia Bagutti2Ana B. García-Martín3Ana B. García-Martín4Jan A. Roth5Monica Alt Hug6Laura Maurer Pekerman7Laura Maurer Pekerman8Ruth Schindler9Ruth Schindler10Reto Furger11Lucas Eichenberger12Ingrid Steffen13Philipp Hübner14Tanja Stadler15Lisandra Aguilar-Bultet16Lisandra Aguilar-Bultet17Sarah Tschudin-Sutter18Sarah Tschudin-Sutter19Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, University of Basel, Basel, SwitzerlandDepartment of Clinical Research, University Hospital Basel, Basel, SwitzerlandState Laboratory Basel-City, Basel, SwitzerlandDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, University of Basel, Basel, SwitzerlandDepartment of Clinical Research, University Hospital Basel, Basel, SwitzerlandDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, University of Basel, Basel, SwitzerlandState Laboratory Basel-City, Basel, SwitzerlandDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, University of Basel, Basel, SwitzerlandDepartment of Clinical Research, University Hospital Basel, Basel, SwitzerlandDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, University of Basel, Basel, SwitzerlandDepartment of Clinical Research, University Hospital Basel, Basel, SwitzerlandState Laboratory Basel-City, Basel, SwitzerlandState Laboratory Basel-City, Basel, SwitzerlandRothen Laboratory, Basel, SwitzerlandState Laboratory Basel-City, Basel, SwitzerlandDepartment of Biosystems Science and Engineering, ETH Zurich, Zürich, SwitzerlandDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, University of Basel, Basel, SwitzerlandDepartment of Clinical Research, University Hospital Basel, Basel, SwitzerlandDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, University of Basel, Basel, SwitzerlandDepartment of Clinical Research, University Hospital Basel, Basel, SwitzerlandBackgroundThe involvement of non-human-to-human transmission of extended-spectrum β-lactamase-producing Enterobacterales (ESBL-PE) remains elusive. Foodstuffs may serve as reservoirs for ESBL-PE and contribute to their spread.AimWe aimed to systematically investigate the presence and spatiotemporal distribution of ESBL-PE in diverse unprocessed foodstuffs of different origin purchased in a central European city.MethodsChicken and green (herbs, salad, sprouts, vegetables) samples were collected monthly for two consecutive years, from June 2017 to June 2019, from large supermarket chains and small local food retailers, representing all ten postcode areas of the City of Basel (Switzerland), and the kitchen of the University Hospital Basel (Basel, Switzerland). After enrichment, presumptive ESBL-PE were isolated by selective culture methods and identified by Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. ESBL production was confirmed by phenotypic testing.ResultsAmong 947 food samples, 14.8% were positive for ESBL-PE isolate/s belonging to eight different ESBL-producing bacterial species. Escherichia coli and Serratia fonticola were predominant across samples (9 and 2%, respectively). Higher ESBL-PE prevalence was observed in chicken (25.9%) than in green (3.8%) samples (p < 0.001). Among greens, ESBL-PE were most frequently isolated from sprouts (15.2%). High ESBL-PE species diversity was observed among chicken samples, with E. coli as predominant (17.6%). ESBL-producing Enterobacter cloacae was detected among different greens. Yet, ESBL-producing Klebsiella pneumoniae was predominant in sprouts (12.1%). In total, 20.5% of samples from organic farming and 14.2% of samples from conventionally raised animals harbored an ESBL-producing isolate. Detection of ESBL-PE across samples differed between organic and non-organic when stratified by food source (p < 0.001), particularly among greens (12.5% organic, 2.4% conventional). High proportion of organic chicken samples was positive for ESBL-E. coli (33.3%), while the detection of several species characterized the conventional chicken samples. No significant differences in ESBL-PE frequences were detected between national (13.4%) and international samples (8.0%) (p = 0.122). Instead, differences were observed between regions of food production and countries (p < 0.001). No significant differences were found when comparing the proportion of ESBL-PE positive samples across districts, shop sizes and the hospital kitchen. The percentage of ESBL-PE positive samples did not differ monthly across the two-year sampling period (p = 0.107).ConclusionOur findings indicate moderate dissemination of ESBL-PE in foodstuffs, especially between chicken products and sprouts. Chicken meat represents a source for several ESBL-producing Enterobacterales, especially E. coli, while greens are more prone to carry ESBL-K. pneumoniae and E. cloacae. We disclose the importance of food type, food production system and production origin when assessing the risk of contamination with different ESBL-PE species.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1295037/fullESBL-producing Enterobacteralesfoodstuff, chicken, greensEscherichia coliKlebsiella pneumoniaespatiotemporal distribution |
| spellingShingle | Elena Gómez-Sanz Elena Gómez-Sanz Claudia Bagutti Ana B. García-Martín Ana B. García-Martín Jan A. Roth Monica Alt Hug Laura Maurer Pekerman Laura Maurer Pekerman Ruth Schindler Ruth Schindler Reto Furger Lucas Eichenberger Ingrid Steffen Philipp Hübner Tanja Stadler Lisandra Aguilar-Bultet Lisandra Aguilar-Bultet Sarah Tschudin-Sutter Sarah Tschudin-Sutter Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland Frontiers in Microbiology ESBL-producing Enterobacterales foodstuff, chicken, greens Escherichia coli Klebsiella pneumoniae spatiotemporal distribution |
| title | Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland |
| title_full | Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland |
| title_fullStr | Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland |
| title_full_unstemmed | Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland |
| title_short | Extended-spectrum β-lactamase-producing Enterobacterales in diverse foodstuffs: a prospective, longitudinal study in the city of Basel, Switzerland |
| title_sort | extended spectrum β lactamase producing enterobacterales in diverse foodstuffs a prospective longitudinal study in the city of basel switzerland |
| topic | ESBL-producing Enterobacterales foodstuff, chicken, greens Escherichia coli Klebsiella pneumoniae spatiotemporal distribution |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1295037/full |
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