Are animals a source of Stenotrophomonas maltophilia in human infections? Contributions of a nationwide molecular study

Abstract

Stenotrophomonas maltophilia (Sm) is an archetypal environmental opportunistic bacterium responsible for health care-associated infections. The role of animals in human Sm infections is unknown. This study aims to reveal the genetic and phylogenetic relationships between pathogenic strains of Sm, both animal and human, and identify a putative role for animals as a reservoir in human infection. We phenotypically and genotypically characterized 61 Sm strains responsible for animal infections (mainly respiratory tract infections in horses) from a French nationwide veterinary laboratory network. We tested antimicrobial susceptibility and performed MLST and genogrouping using the concatenation of the seven housekeeping genes from the original MLST scheme. Excluding the eight untypeable strains owing to the lack of gene amplification, only 10 out of the 53 strains yielded a known ST (ST5, ST39, ST162, ST8, ST27, ST126, ST131). The genogroup distribution highlighted not only genogroups (genogroups 5 and 9) comprised exclusively of animal strains but also genogroups shared by human and animal strains. Interestingly, these shared genogroups were primarily groups 2 and 6, which have previously been identified as the two most frequent genogroups among human-pathogenic Sm strains, especially among respiratory pathogens. The antimicrobial susceptibility testing underlined the presence of acquired resistance: 18.8 and 7.5% of the tested isolates were resistant to the sulfonamide-trimethoprim combination and ciprofloxacin, respectively. Animal strains of Sm shared phylogenetic traits with some of the most successful human strains. The exact relationships between the human and animal strains, and the genetic support of these common traits, need to be determined.

Population Structure, Molecular Epidemiology, and β-Lactamase Diversity among Stenotrophomonas maltophilia Isolates in the United States

“…These findings were not only confirmed but also expanded by the MLST scheme proposed by Kaiser et al (20). Since then, several other studies employed the genomic group determination based on the concatenation and alignment of the sequences corresponding to the seven housekeeping genes included in the S. maltophilia MLST scheme as an efficient approach to study the population structure of this pathogen (32)(33)(34). In line with other studies, we also report the predominance of genomic groups 6, 1, and C among our clinical samples, all of which have previously been associated with human sources (20,31).…”

Antimicrobial resistance and multilocus sequence types of Stenotrophomonas maltophilia isolated from dogs and cats in Japan

“…On the other hand, a total of seven isolates were categorized into genogroups 1, 2, 3, or 7 (one or two isolates per genogroup). These findings were different from those of Jayol et al [19], which stated that animal-origin isolates in France were distributed into the main genogroups 2, 5, 6, and 9. Thus, genogroup distribution was likely different across districts and/or animal species.…”

“…ST501-518 and ST525-529) (Table 1). Such expansive molecular diversity of S. maltophilia was observed in previous studies on animal and human isolates [16,19,20]. Different STs were detected among neighbouring prefectures, except Tokyo and Saitama prefectures (i.e.…”

“…Sm2, Sm3, Sm6, Sm14, Sm18, Sm20, Sm25, Sm29, Sm30, Sm31, Sm37, Sm38, and Sm39) were categorized into genogroup 6, which was more prevalent compared to isolates from French animals (mainly equines) [16,19]. This genogroup was also identified as a major genogroup among humans in France [19] and the United States [20]. Thus, the high prevalence of genogroup 6 in our collections might imply that companion animals can acquire S. maltophilia isolates from humans in Japan, possibly due to close contact with each other in the household.…”

Comparative Whole-Genome Phylogeny of Animal, Environmental, and Human Strains Confirms the Genogroup Organization and Diversity of the Stenotrophomonas maltophilia Complex

“…Additional studies based on whole-genome sequencing of an increasing number of strains confirmed this phylogenic organization (4)(5)(6). We recently reported the disproportionate representation of some genogroups, not only among human but also among animal infectious strains (7,8). From an epidemiological point of view, animals could be a reservoir for human diseases; while from a phylogenic point of view, animals could constitute an intermediate step for the adaptation of environmental strains to humans.…”