Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants
Abstract Background Clostridium perfringens forms part of the human gut microbiota and has been associated with life-threatening necrotising enterocolitis (NEC) in premature infants. Whether specific toxigenic strains are responsible is unknown, as is the extent of diversity of strains in healthy pr...
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| Format: | Article |
| Language: | English |
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BMC
2020-02-01
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| Series: | BMC Pediatrics |
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| Online Access: | http://link.springer.com/article/10.1186/s12887-020-1976-7 |
| _version_ | 1819081339426570240 |
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| author | Alexander G. Shaw Emma Cornwell Kathleen Sim Hannah Thrower Hannah Scott Joseph C. S. Brown Ronald A. Dixon J. Simon Kroll |
| author_facet | Alexander G. Shaw Emma Cornwell Kathleen Sim Hannah Thrower Hannah Scott Joseph C. S. Brown Ronald A. Dixon J. Simon Kroll |
| author_sort | Alexander G. Shaw |
| collection | DOAJ |
| description | Abstract Background Clostridium perfringens forms part of the human gut microbiota and has been associated with life-threatening necrotising enterocolitis (NEC) in premature infants. Whether specific toxigenic strains are responsible is unknown, as is the extent of diversity of strains in healthy premature babies. We investigated the C. perfringens carrier status of premature infants in the neonatal intensive care unit, factors influence this status, and the toxic potential of the strains. Methods C. perfringens was isolated by culture from faecal samples from 333 infants and their toxin gene profiles analysed by PCR. A survival analysis was used to identify factors affecting probability of carriage. Competitive growth experiments were used to explore the results of the survival analysis. Results 29.4% of infants were colonized with C. perfringens before they left hospital. Three factors were inversely associated with probability of carriage: increased duration of maternal milk feeds, CPAP oxygen treatment and antibiotic treatment. C. perfringens grew poorly in breast milk and was significantly outperformed by Bifidobacterium infantis, whether grown together or separately. Toxin gene screening revealed that infants carried isolates positive for collagenase, perfringolysin O, beta 2, beta, becA/B, netB and enterotoxin toxin genes, yet none were observed to be associated with the development of NEC. Conclusions Approximately a third of preterm infants are colonised 3 weeks after birth with toxin gene-carrying C. perfringens. We speculate that increased maternal breast milk, oxygen and antibiotic treatment creates an environment in the gut hostile to growth of C. perfringens. Whilst potentially toxigenic C. perfringens isolates were frequent, no toxin type was associated with NEC. Trial registration clinicaltrials.gov NCT01102738, registered 13th April 2010. |
| first_indexed | 2024-12-21T19:59:12Z |
| format | Article |
| id | doaj.art-aca0493958fe48f681a0f72cf5854b71 |
| institution | Directory Open Access Journal |
| issn | 1471-2431 |
| language | English |
| last_indexed | 2024-12-21T19:59:12Z |
| publishDate | 2020-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Pediatrics |
| spelling | doaj.art-aca0493958fe48f681a0f72cf5854b712022-12-21T18:52:01ZengBMCBMC Pediatrics1471-24312020-02-0120111110.1186/s12887-020-1976-7Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infantsAlexander G. Shaw0Emma Cornwell1Kathleen Sim2Hannah Thrower3Hannah Scott4Joseph C. S. Brown5Ronald A. Dixon6J. Simon Kroll7Department of Infectious Disease Epidemiology, Imperial College LondonDepartment of Medicine, Section of Paediatrics, Imperial College LondonDepartment of Medicine, Section of Paediatrics, Imperial College LondonDepartment of Medicine, Section of Paediatrics, Imperial College LondonDepartment of Medicine, Section of Paediatrics, Imperial College LondonSchool of Life Sciences, University of LincolnSchool of Life Sciences, University of LincolnDepartment of Medicine, Section of Paediatrics, Imperial College LondonAbstract Background Clostridium perfringens forms part of the human gut microbiota and has been associated with life-threatening necrotising enterocolitis (NEC) in premature infants. Whether specific toxigenic strains are responsible is unknown, as is the extent of diversity of strains in healthy premature babies. We investigated the C. perfringens carrier status of premature infants in the neonatal intensive care unit, factors influence this status, and the toxic potential of the strains. Methods C. perfringens was isolated by culture from faecal samples from 333 infants and their toxin gene profiles analysed by PCR. A survival analysis was used to identify factors affecting probability of carriage. Competitive growth experiments were used to explore the results of the survival analysis. Results 29.4% of infants were colonized with C. perfringens before they left hospital. Three factors were inversely associated with probability of carriage: increased duration of maternal milk feeds, CPAP oxygen treatment and antibiotic treatment. C. perfringens grew poorly in breast milk and was significantly outperformed by Bifidobacterium infantis, whether grown together or separately. Toxin gene screening revealed that infants carried isolates positive for collagenase, perfringolysin O, beta 2, beta, becA/B, netB and enterotoxin toxin genes, yet none were observed to be associated with the development of NEC. Conclusions Approximately a third of preterm infants are colonised 3 weeks after birth with toxin gene-carrying C. perfringens. We speculate that increased maternal breast milk, oxygen and antibiotic treatment creates an environment in the gut hostile to growth of C. perfringens. Whilst potentially toxigenic C. perfringens isolates were frequent, no toxin type was associated with NEC. Trial registration clinicaltrials.gov NCT01102738, registered 13th April 2010.http://link.springer.com/article/10.1186/s12887-020-1976-7Clostridium perfringensBreast milkToxinsNecrotising enterocolitis |
| spellingShingle | Alexander G. Shaw Emma Cornwell Kathleen Sim Hannah Thrower Hannah Scott Joseph C. S. Brown Ronald A. Dixon J. Simon Kroll Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants BMC Pediatrics Clostridium perfringens Breast milk Toxins Necrotising enterocolitis |
| title | Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants |
| title_full | Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants |
| title_fullStr | Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants |
| title_full_unstemmed | Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants |
| title_short | Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants |
| title_sort | dynamics of toxigenic clostridium perfringens colonisation in a cohort of prematurely born neonatal infants |
| topic | Clostridium perfringens Breast milk Toxins Necrotising enterocolitis |
| url | http://link.springer.com/article/10.1186/s12887-020-1976-7 |
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