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Review
. 2016 Oct 18:7:1599.
doi: 10.3389/fmicb.2016.01599. eCollection 2016.

Systematic Review on Global Epidemiology of Methicillin-Resistant Staphylococcus pseudintermedius: Inference of Population Structure from Multilocus Sequence Typing Data

Teresa Pires Dos Santos  1 , Peter Damborg  1 , Arshnee Moodley  1 , Luca Guardabassi  2
Affiliations
Review

Systematic Review on Global Epidemiology of Methicillin-Resistant Staphylococcus pseudintermedius: Inference of Population Structure from Multilocus Sequence Typing Data

Teresa Pires Dos Santos et al. Front Microbiol. .

Abstract

Background and rationale: Methicillin-resistant Staphylococcus pseudintermedius (MRSP) is a major cause of infections in dogs, also posing a zoonotic risk to humans. This systematic review aimed to determine the global epidemiology of MRSP and provide new insights into the population structure of this important veterinary pathogen. Methodology: Web of Science was searched systematically for articles reporting data on multilocus sequence typing (MLST) of S. pseudintermedius isolates from dogs or other animal or human patients and carriers. Data from the eligible studies were then integrated with data from the MLST database for this species. Analysis of MLST data was performed with eBURST and ClonalFrame, and the proportion of MRSP isolates resistant to selected antimicrobial drugs was determined for the most predominant clonal complexes. Results: Fifty-eight studies published over the last 10 years were included in the review. MRSP represented 76% of the 1428 isolates characterized by the current MLST scheme. The population of S. pseudintermedius was highly diverse and included five major MRSP clonal complexes (CCs). CC71, previously described as the epidemic European clone, is now widespread worldwide. In Europe, CC258, which is more frequently susceptible to enrofloxacin and aminoglycosides, and more frequently resistant to sulphonamides/trimethoprim than CC71, is increasingly reported in various countries. CC68, previously described as the epidemic North American clone, is frequently reported in this region but also in Europe, while CC45 (associated with chloramphenicol resistance) and CC112 are prevalent in Asia. It was estimated that clonal diversification in this species is primarily driven by homologous recombination (r/m = 7.52). Conclusion: This study provides evidence that S. pseudintermedius has an epidemic population structure, in which five successful MRSP lineages with specific traits regarding antimicrobial resistance, genetic diversity and geographical distribution have emerged upon a weakly clonal background through acquisition of SCCmec and other mobile genetic elements.

Keywords: MLST; MRSP; Staphylococcus pseudintermedius; antimicrobial resistance; companion animals; epidemiology; systematic review.

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Figures

Figure 1
Figure 1
Bar chart showing (i) the annual number of published articles retrieved when using the search word “Staphylococcus pseudintermedius” (dark gray); (ii) the annual number of published articles retrieved involving MRSP (intermediate gray); and (iii) the annual number of published articles retrieved employing MLST (light gray), since 2007–May 2016. A total of 58 studies reporting MLST data on MRSP and MSSP were included in this review.
Figure 2
Figure 2
eBURST population snapshot of Staphylococcus pseudintermedius. Clusters of linked isolates correspond to clonal complexes (CCs). Primary founders (blue) are positioned centrally in the clusters, and subgroup founders are shown in yellow. The diameter of the circles is directly proportional to the total number of isolates reported in the MLST database (http://pubmlst.org/spseudintermedius/) and in reviewed scientific papers given in Table S1. Names of various important STs associated with methicillin resistance are indicated within a large, “straggly” CC, CC258. Methicillin resistant S. pseudintermedius (MRSP) lineages are highlighted in pink.
Figure 3
Figure 3
Unrooted consensus tree displaying the relationship between the 144 STs of the S. pseudintermedius sample (96 MSSP, 46 MRSP, and 2 MSSP/MRSP) at seven concatenated loci (2944 nucleotides in total). The 144 STs represent major eBURST group/subgroup founders (with more than three SLV links) and singletons with no double locus variant (DLV) links to eBURST-assigned CCs. The phylogenetic tree was based on all trees sampled after 2,000,000 iterations, from which half were discarded as burn-in. The dendogram was constructed from the combination of two ClonalFrame runs with a cut-off value of 0.5 as a majority rule consensus. Scale is in coalescent units. There were no well-supported nodes (i.e., with a Bayesian posterior probability > 0.90) for clusters with > 3 STs). The main MRSP clones are shown in different colors. MRSP, black; MSSP, white; both MRSP and MSSP, gray.
Figure 4
Figure 4
Geographic variation in the reported frequency of major MRSP clonal complexes based on data from the MLST database (http://pubmlst.org/spseudintermedius/) and references given in Table S1. The numbers represent the percentage (%) of MRSP isolates from each lineage that was reported in each continent.
Figure 5
Figure 5
Proportion (%) of MRSP isolates resistant to selected antimicrobial drugs within three predominant clonal complexes (characterized by MLST-7). Antimicrobial susceptibility patterns were extracted from references given in Table S1. S, Susceptible; R, Resistance; TET, Tetracycline; SXT, Trimethoprim/Sulfamethoxazole; CHL, Chloramphenicol; CLI, Clindamycin; ERY, Erythromycin; ENRO, Enrofloxacin; AMK, Amikacin; GEN, Gentamicin.
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