Neonatal intensive care units as a driver and reservoir of invasive infections: an example of the emerging Staphylococcus capitis multidrug-resistant NRCS-A clone

Abstract

Introduction: Healthcare environments have been identified as a significant source of multidrug-resistant bacterial infections, particularly, in vulnerable patients such as very-low-birth-weight preterm infants. Opportunistic pathogen Staphylococcus capitis is a common cause of late-onset sepsis in neonatal intensive care units (NICUs). NRCS-A, a healthcare-associated S. capitis clone frequently exhibiting multidrug resistance, has seen a rapid dispersion among NICUs since its first report in France in 2012, causing outbreaks worldwide with increasing detection in neonatal bacteraemia cases. In this pilot study, we set out to determine presence and patient-environment links of S. capitis in NICUs for improving cleaning guidance. Methods: S. capitis isolates were recovered from fomites and air in NICUs in four cities in the South West of England between 2021–2022 using surface swabs, agar contact plates, and settle plates. Three NICUs were each sampled once, and one was sampled twice. Each NICU was divided into four sampling zones: 1A, internal surfaces of infant incubators; 1B and 1C, wider cot space and bay, respectively; 2, the communal area shared by families and staff; and 3, staff-only areas. Comparator isolates were recovered from respiratory droplets of healthy adults in a distant non-healthcare setting. S. capitis isolates were identified using MALDI-TOF and subjected to Illumina whole-genome sequencing (WGS) at the UK Health Security Agency (UKHSA). WGS data of environmental isolates were compared with those of international clinical isolates previously published or newly sequenced by the UKHSA. Results: Fifty-four environmental isolates were obtained, including 47 from NICUs and seven from a non-NICU setting. The NRCS-A clone was more frequently detected in the NICU (40 out of 47 isolates, 85%) than it was in the non-healthcare, adult setting (one out of 7 isolates, 14%). Of the 40 environmental isolates from NICUs, 13 were recovered from Zone 1A, 22 from Zone 1B, three from Zone 1C, and one from Zones 2 and 3, respectively. Eight isolates were recovered from airborne particles (NICU: 1; adults: 7), including a sole NRCS-A isolate (from an adult). Detected antimicrobial resistance genes showed a predictable strong association between the NRCS-A clone and resistance to aminoglycosides, beta-lactams, fusidic acid, and nisin. Biofilm-related genes tarIJL were exclusively found in NRCS-A isolates. A comparison of these environmental isolates with 1167 clinical isolates identified 96 pairs of same-location, environment/infant isolates with at most 10 core-gene single nucleotide polymorphisms. Discussion: The S. capitis NRCS-A clone is associated with infant incubators in NICUs, with its detection decreasing as the distance from the incubator increases. Its transmission is likely through contaminated surfaces rather than air, and the known persistence within NICUs could be explained by biofilm formation and multidrug resistance. Conclusion: Continuous monitoring of bacterial populations in NICUs could inform control measures and reduce neonatal invasive infections.