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This study aims to characterise novel class 1 integron (Int1) structures containing <jats:italic>bla<\/jats:italic><jats:sub>VIM\u20102<\/jats:sub> and <jats:italic>bla<\/jats:italic><jats:sub>IMP\u20101<\/jats:sub> in high\u2010risk CP\u2010<jats:italic>Pa<\/jats:italic> sequence type (ST) 235 and ST654 strains from dogs and cats and illustrate the genetic relatedness between CP\u2010<jats:italic>Pa<\/jats:italic> strains from animal and human origins.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods and Results<\/jats:title><jats:p>Of the four CP\u2010<jats:italic>Pa<\/jats:italic> strains, whole\u2010genome sequencing and analysis revealed that three strains belonged to ST235\/O11\/<jats:italic>exoU+<\/jats:italic>\/<jats:italic>exoS\u2010<\/jats:italic>, with two strains harbouring <jats:italic>bla<\/jats:italic><jats:sub>VIM\u20102<\/jats:sub>, and one strain harbouring <jats:italic>bla<\/jats:italic><jats:sub>IMP\u20101<\/jats:sub>. The remaining strain was characterised as ST654\/O4\/<jats:italic>exoU\u2010<\/jats:italic>\/<jats:italic>exoS+<\/jats:italic> and harboured <jats:italic>bla<\/jats:italic><jats:sub>VIM\u20102<\/jats:sub>. Core\u2010genome single nucleotide polymorphism\u2010based phylogeny illustrated genetic relationships between animal and human high\u2010risk CP\u2010<jats:italic>Pa<\/jats:italic> ST235\/O11 and ST654\/O4 strains within the same STs. Three novel Int1 gene cassette arrays were identified in the canine and feline CP\u2010<jats:italic>Pa<\/jats:italic> strains in this study. The novel ~6.2\u2010kb <jats:italic>bla<\/jats:italic><jats:sub>VIM\u20102<\/jats:sub>\u2010containing Int1[Pae\u2010CUVET21\u2010397] and Int1[Pae\u2010CUVET23\u2010830] (<jats:italic>intI1<\/jats:italic>\u2010<jats:italic>aadB<\/jats:italic>\u2010<jats:italic>bla<\/jats:italic><jats:sub>VIM\u20102<\/jats:sub>\u2010<jats:italic>aadB<\/jats:italic>\u2010<jats:italic>cmlA6<\/jats:italic>\u2010<jats:italic>qacE<\/jats:italic>\u2206<jats:italic>1<\/jats:italic>\u2010<jats:italic>folP<\/jats:italic>) formed a complex Int1 located in an integrative and conjugative element of two feline CP\u2010<jats:italic>Pa<\/jats:italic> ST235 strains. The canine CP\u2010<jats:italic>Pa<\/jats:italic> ST235 strain CUVET20\u2010956 contained a novel ~5.8\u2010kb <jats:italic>bla<\/jats:italic><jats:sub>IMP\u20101<\/jats:sub>\u2010containing Int1[Pae\u2010CUVET20\u2010956] (<jats:italic>intI1<\/jats:italic>\u2010<jats:italic>bla<\/jats:italic><jats:sub>IMP\u20101<\/jats:sub>\u2010<jats:italic>aacA4<\/jats:italic>\u2010<jats:italic>aacA4<\/jats:italic>\u2010IS<jats:italic>1595<\/jats:italic>\u2010<jats:italic>qacE<\/jats:italic>\u2206<jats:italic>1<\/jats:italic>\u2010<jats:italic>sul1<\/jats:italic>). The CP\u2010<jats:italic>Pa<\/jats:italic> ST654 strain CUVET18\u2010860 contained In<jats:italic>1206<\/jats:italic> encoding <jats:italic>bla<\/jats:italic><jats:sub>VIM\u20102<\/jats:sub> and a novel ~5.9\u2010kb Int1[Pae\u2010CUVET18\u2010860] (\u2206<jats:italic>intI1<\/jats:italic>\u2010<jats:italic>bla<\/jats:italic><jats:sub>VEB\u20101<\/jats:sub>\u2010<jats:italic>aadB<\/jats:italic>\u2010<jats:italic>qnrVC1<\/jats:italic>\u2010<jats:italic>aacA4<\/jats:italic>\u2010<jats:italic>bla<\/jats:italic><jats:sub>OXA\u201010<\/jats:sub>\u2010<jats:italic>aadA1<\/jats:italic>\u2010<jats:italic>dfrA14<\/jats:italic>) encoding multidrug resistance (MDR). Additionally, In<jats:italic>51<\/jats:italic>\u2010containing Tn<jats:italic>6162<\/jats:italic> inserted in genomic island 1 was identified in all CP\u2010<jats:italic>Pa<\/jats:italic> ST235 strains.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>The novel Int1s encoding metallo\u2010\u03b2\u2010lactamases and MDR in canine and feline CP\u2010<jats:italic>Pa<\/jats:italic> play a crucial role in the development of resistance to multiple antimicrobials and last\u2010resort carbapenems in <jats:styled-content style=\"fixed-case\"><jats:italic>P. aeruginosa<\/jats:italic><\/jats:styled-content> ST235 and ST654 strains of veterinary and public health importance, posing possible zoonotic and anthroponotic transmission of the high\u2010risk CP\u2010<jats:italic>Pa<\/jats:italic> clones between companion animals and 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