Isolation of Staphylococcus pseudintermedius in Immunocompromised Patients from a Single Center in Spain: A Zoonotic Pathogen from Companion Animals

Abstract

Staphylococcus pseudintermedius, a commensal opportunistic bacterium predominantly residing in the skin of companion animals, particularly dogs, has the potential to induce skin and soft tissue infections in pets, and zoonotic infections, including catheter-related complications. This study documents four cases of S. pseudintermedius infection or colonization in patients who had close contact with dogs or cats. Identification of the bacterial species was performed using MALDI-TOF mass spectrometry, and antibiotic susceptibility was determined using microdilution assay. DNA was sequenced using Nanopore technology followed by in silico analysis. Three isolates were multidrug resistant, including resistance to methicillin, with one belonging to the prevalent European lineage ST551, and the other two were attributed to a novel multilocus sequence type, ST2672. The remaining isolate was attributed to the novel multilocus sequence type ST2673 and was methicillin susceptible. All four isolates exhibited an array of virulence factors that contributed to colonization, damage to host immune cells, and biofilm formation. All the ST551 isolates included in the comparative analysis displayed clonality within the European continent. The importance of describing zoonotic infections associated with S. pseudintermedius resides in the scarcity of available scientific literature, further accentuated by its heightened resistance profile and potential complications, particularly in the context of catheter-related infections.

Keywords: MDR; MRSP; SSTI; ST551; Staphylococcus pseudintermedius; catheter-related infection; nanopore; one health; whole-genome sequencing; zoonosis.

Figure 1

Genomic context of the ARGs. (a) genomic context for aph(3′)-IIIa, sat4, ant(6)-Ia, erm(B), and dfrG. The first line corresponds to isolate 23-150, and the second to isolate 23-298; (b) genomic context for tet(K), tet(L), and tet(M) genes. The first two lines correspond to isolate 23-150 and the third one to isolate 23-298; (c) genomic context for aac(6′)-Ie-aph(2″)-Ia gene. This line corresponds to isolate 23-150, but ST2672 isolates present the same genomic context with the exception of the “group II intron reverse transcriptase/maturase”.

Figure 2

Genomic context of mecA. (a) SnapGene Viewer visualization of the genomic context of mecA in isolates 23-150 and 23-298. (b) EasyFig comparison of the genomic context of mecA in isolates 23-150 and 23-298 with SCCmec type V(5C2) from S. aureus JCSC3624(WIS) (GenBank: AB121219.1), ΨSCCmec₅₇₃₉₅ pseudocassette from S. pseudintermedius strain 57395 (GenBank: HE984157.2), mecA context from S. haemolyticus WCH1 (GenBank: JQ764731.1), and SCCmec type IX(1C2) from S. aureus JCSC6943 (GenBank: AB505628.1). In red, mecA gene; in orange, elements responsible for mobilization and reorganization of the cassette; in light blue, ∆mecR1; in green, gray, and teal, genes responsible for arsenic, cadmium, and copper resistance, respectively. Homology gradients range from green (100%) to yellow (85%), and violet to light blue (85%) for inverted regions.

Figure 3

Phylogenetic tree and ANI. We performed phylogenetic analysis with all the ST551 S. pseudintermedius genomes available at NCBI nucleotide database, and other S. pseudintermedius isolated from Homo sapiens. ANI results are expressed as percentages and displayed in a heat map, with green boxes indicating the highest identities and red boxes indicating the lowest identities. Information regarding host disease, isolation source, and sequencing technology used can be found in Supplementary Table S1. MLST, multilocus sequence type; UK, United Kingdom; USA, United States of America.