Abstract
Background
We aimed to determine the genetic relatedness between Staphylococcus epidermidis colonizing breast milk (BM) and BM-fed neonates during the first month of life.
Methods
S. epidermidis was isolated from the stool and skin swabs of 20 healthy term and 49 preterm neonates hospitalized in the neonatal intensive care unit and from the BM of mothers once a week and typed by multilocus variable-number tandem-repeat analysis. Virulence-related genes were determined by PCR.
Results
The gut (95%) and skin (100%) of term neonates were colonized with strains genetically similar to those in BM and carrying mecA and IS256 at low rate (both <6.7%). In preterm neonates, colonization with strains genetically similar to those in BM was low on the skin (34.7%) and in the gut in the first week of life (14.3%), but the prevalence of mecA (>90.6%) and IS256 (>61.7%) was high. By the fourth week, in the gut of preterm neonates the prevalence of mecA (73.8%) and IS256 (18.4%) decreased, but colonization with strains genetically similar to those in BM increased (83.7%).
Conclusion
During early life, the skin and gut of preterm neonates is colonized with S. epidermidis that is distinct from strains found in BM, but gradually the gut is enriched with strains genetically similar to those in BM, as in term neonates.
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References
Hira V, Kornelisse RF, Sluijter M et al. Colonization dynamics of antibiotic-resistant coagulase-negative Staphylococci in neonates. J Clin Microbiol 2013;51:595–7.
Jiménez E, Delgado S, Maldonado A et al. Staphylococcus epidermidis: a differential trait of the fecal microbiota of breast-fed infants. BMC Microbiol 2008;8:143.
Soeorg H, Metsvaht T, Eelmäe I et al. Coagulase-negative staphylococci in breast milk of mothers of preterm compared with term neonates. J Hum Lact 2017;33:329–340.
Soeorg H, Huik K, Parm U et al. Genetic relatedness of coagulase-negative staphylococci from gastrointestinal tract and blood of preterm neonates with late-onset sepsis. Pediatr Infect Dis J 2013;32:389–93.
Martín V, Maldonado-Barragán A, Moles L et al. Sharing of bacterial strains between breast milk and infant feces. J Hum Lact 2012;28:36–44.
Vergnano S, Menson E, Kennea N et al. Neonatal infections in England: the NeonIN surveillance network. Arch Dis Child Fetal Neonatal Ed 2011;96:F9–14.
Hira V, Sluijter M, Estevão S et al. Clinical and molecular epidemiologic characteristics of coagulase-negative staphylococcal bloodstream infections in intensive care neonates. Pediatr Infect Dis J 2007;26:607–12.
Kayıran PG, Can F, Kayıran SM, Ergonul O, Gürakan B . Transmission of methicillin-sensitive Staphylococcus aureus to a preterm infant through breast milk. J Matern Fetal Neonatal Med 2014;27:527–9.
Zhang K, Sparling J, Chow BL et al. New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol 2004;42:4947–55.
Johansson A, Koskiniemi S, Gottfridsson P, Wiström J, Monsen T . Multiple-locus variable-number tandem repeat analysis for typing of Staphylococcus epidermidis. J Clin Microbiol 2006;44:260–5.
Cremniter J, Sivadon-Tardy V, Caulliez C et al. Genetic analysis of glycopeptide-resistant Staphylococcus epidermidis strains from bone and joint infections. J Clin Microbiol 2013;51:1014–9.
Thomas JC, Vargas MR, Miragaia M, Peacock SJ, Archer GL, Enright MC . Improved multilocus sequence typing scheme for Staphylococcus epidermidis. J Clin Microbiol 2007;45:616–9.
Kondo Y, Ito T, Ma XX et al. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother 2007;51:264–74.
Ziebuhr W, Krimmer V, Rachid S, Lössner I, Götz F, Hacker J . A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 1999;32:345–56.
Diep BA, Stone GG, Basuino L et al. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 2008;197:1523–30.
EstimateS: Statistical estimation of species richness and shared species from samples, Version 9. 2013. Available at http://purl.oclc.org/estimates. (accessed 26 July 2016).
Cong X, Xu W, Janton S et al. Gut microbiome developmental patterns in early life of preterm infants: impacts of feeding and gender. PLoS ONE 2016;11:e0152751.
Hira V, Sluijter M, Goessens WH et al. Coagulase-negative staphylococcal skin carriage among neonatal intensive care unit personnel: from population to infection. J Clin Microbiol 2010;48:3876–81.
Du X, Zhu Y, Song Y et al. Molecular analysis of Staphylococcus epidermidis strains isolated from community and hospital environments in China. PLoS ONE 2013;8:e62742.
Krediet TG, Jones ME, Janssen K, Gerards LJ, Fleer A . Prevalence of molecular types and mecA gene carriage of coagulase-negative Staphylococci in a neonatal intensive care unit: relation to nosocomial septicemia. J Clin Microbiol 2001;39:3376–78.
Klingenberg C, Embleton ND, Jacobs SE, O'Connell LA, Kuschel CA . Enteral feeding practices in very preterm infants: an international survey. Arch Dis Child Fetal Neonatal Ed 2012;97:F56–61.
Metsvaht T, Nellis G, Varendi H et al. High variability in the dosing of commonly used antibiotics revealed by a Europe-wide point prevalence study: implications for research and dissemination. BMC Pediatr 2015;15:41.
Dominguez-Bello MG, Costello EK, Contreras M et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 2010;107:11971–5.
Garten L, Maass E, Schmalisch G, Bührer C . O father, where art thou? Parental NICU visiting patterns during the first 28 days of life of very low-birth-weight infants. J Perinat Neonatal Nurs 2011;25:342–8.
Lamy Filho F, de Sousa SH, Freitas IJ et al. Effect of maternal skin-to-skin contact on decolonization of methicillin-oxacillin-resistant Staphylococcus in neonatal intensive care units: a randomized controlled trial. BMC Pregnancy Childbirth 2015;15:63.
Conceição T, Aires de Sousa M, Miragaia M et al. Staphylococcus aureus reservoirs and transmission routes in a Portuguese neonatal intensive care unit: a 30-month surveillance study. Microb Drug Resist 2012;18:116–24.
Boix-Amorós A, Collado MC, Mira A . Relationship between milk microbiota, bacterial load, macronutrients, and human cells during lactation. Front Microbiol 2016;7:492.
Acknowledgements
We thank the study nurses Eve Kaur, Marika Zuihhina, and Tuuli Tammekunn, laboratory assistants Dagmar Hoidmets, Tiiu Rööp, and Sandra Sokmann, undergraduate student Magda Karakai, and all study participants.
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This study was supported by Estonian Research Council (IUT34-24), European Regional Development Fund (Project SFOS WP1-NeuroAIDS), Archimedes Foundation (Project No. 3.2.1001.11-0032) and the European Society for Paediatric Infectious Diseases (ESPID Small Grant Award).
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Soeorg, H., Metsvaht, T., Eelmäe, I. et al. The role of breast milk in the colonization of neonatal gut and skin with coagulase-negative staphylococci. Pediatr Res 82, 759–767 (2017). https://doi.org/10.1038/pr.2017.150
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DOI: https://doi.org/10.1038/pr.2017.150
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