Antimicrobial Resistance and Genetic Diversity of Pseudomonas aeruginosa Strains Isolated from Equine and Other Veterinary Samples

Abstract

Pseudomonas aeruginosa is one of the leading causes of healthcare-associated infections in humans. This bacterium is less represented in veterinary medicine, despite causing difficult-to-treat infections due to its capacity to acquire antimicrobial resistance, produce biofilms, and persist in the environment, along with its limited number of veterinary antibiotic therapies. Here, we explored susceptibility profiles to antibiotics and to didecyldimethylammonium chloride (DDAC), a quaternary ammonium widely used as a disinfectant, in 168 P. aeruginosa strains isolated from animals, mainly Equidae. A genomic study was performed on 41 of these strains to determine their serotype, sequence type (ST), relatedness, and resistome. Overall, 7.7% of animal strains were resistant to carbapenems, 10.1% presented a multidrug-resistant (MDR) profile, and 11.3% showed decreased susceptibility (DS) to DDAC. Genomic analyses revealed that the study population was diverse, and 4.9% were ST235, which is considered the most relevant human high-risk clone worldwide. This study found P. aeruginosa populations with carbapenem resistance, multidrug resistance, and DS to DDAC in equine and canine isolates. These strains, which are not susceptible to antibiotics used in veterinary and human medicine, warrant close the setting up of a clone monitoring, based on that already in place in human medicine, in a one-health approach.

A 10-year microbiological study of Pseudomonas aeruginosa strains revealed the circulation of populations resistant to both carbapenems and quaternary ammonium compounds

“…The phenotype of DS to DDAC was also found in our veterinary study, a phenotype observed in 11.3% of the strains, mainly isolated from horses and associated with respiratory or genital type samples. In this veterinary study, the SD phenotype to DDAC was not associated with an MDR/XDR profile of the strains 25 . Interestingly, in another publication, Goodarzi et al 40 showed that out of 92 P. aeruginosa hospital strains isolated between 2019 and 2020 (Hamadan City Hospital, Iran), 32.6% had a DDAC MIC ranging from 64 to 128 mg/L as found in the present study.…”

“…However, no gene associated with the production of a carbapenemase was found to explain the resistance to carbapenems found in the animal strains. Finally, it is interesting to note that in this veterinary study, two strains were associated with ST235 25 , among the top 10 P. aeruginosa high-risk clones worldwide.…”

“…From our clinical data, we reveal that antipseudomonal prescriptions following species identification were present in only 60% of cases and did not correspond to the most active antibiotics such as colistin, amikacin, ceftolozane-tazobactam, aztreonam or meropenem. The antimicrobial resistance of the P. aeruginosa strain populations in this study can be compared with data from a similar study of veterinary strains isolated in Normandy between 1996 and 2020 (from horses, dogs, felins, and bovines) 25 . Among the antibiotics tested, ureidopenicillins, carboxypenicillins, carbapenems, 3rd and later generation cephalosporins, monobactams, levofloxacin and phosphonic acids were considered critically important antibiotic substances not authorized in veterinary medicine, in France since 2016, with exceptions 35 .…”

“…In addition, the overuse and misuse of disinfectants can also lead to decreased susceptibility to medically important antimicrobials due to cross-resistance and/or co-resistance mechanisms 23 . For example, in P. aeruginosa antibiotic resistances can be led by exposure to sodium hypochlorite, didecyldimethylammonium chloride (DDAC) 24 , 25 , or chlorhexidine 26 . These can occur by natural selection or by reinforcement of an acquired resistance mechanism that allows for adaptation to the new environment 24 .…”

“…In the European Union, there are approximately 250 different chemical compounds used, either alone or in combination, in disinfectant products including quaternary ammonium-based disinfectants 28 . DDAC is a compound used as a biocide in various applications such as agricultural, food, leisure, and medical equipment, both for private and professional use 25 , 29 . In health products, it is used for its detergent and disinfectant actions on floors, walls, accessories, examination tables, medicated equipment, and noninvasive medical devices 30 .…”