Early Strains of Multidrug-Resistant Salmonella enterica Serovar Kentucky Sequence Type 198 from Southeast Asia Harbor Salmonella Genomic Island 1-J Variants with a Novel Insertion Sequence

Abstract

ABSTRACTSalmonellagenomic island 1 (SGI1) is a 43-kb integrative mobilizable element that harbors a great diversity of multidrug resistance gene clusters described in numerousSalmonella entericaserovars and also inProteus mirabilis. The majority of SGI1 variants contain an In104-derivative complex class 1 integron inserted between resolvase generesand open reading frame (ORF) S044 in SGI1. Recently, the international spread of ciprofloxacin-resistantS. entericaserovar Kentucky sequence type 198 (ST198) containing SGI1-K variants has been reported. A retrospective study was undertaken to characterize ST198S. Kentucky strains isolated before the spread of the epidemic ST198-SGI1-K population in Africa and the Middle East. Here, we characterized 12 ST198S. Kentucky strains isolated between 1969 and 1999, mainly from humans returning from Southeast Asia (n= 10 strains) or Israel (n= 1 strain) or from meat in Egypt (n= 1 strain). All these ST198S. Kentucky strains did not belong to the XbaI pulsotype X1 associated with the African epidemic clone but to pulsotype X2. SGI1-J subgroup variants containing different complex integrons with a partial transposition module and inserted within ORF S023 of SGI1 were detected in six strains. The SGI1-J4 variant containing a partially deleted class 1 integron and thus showing a narrow resistance phenotype to sulfonamides was identified in two epidemiologically unrelated strains from Indonesia. The four remaining strains harbored a novel SGI1-J variant, named SGI1-J6, which containedaadA2,floR2,tetR(G)-tetA(G), andsul1resistance genes within its complex integron. Moreover, in all theseS. Kentucky isolates, a novel insertion sequence related to the IS630family and named ISSen5was found inserted upstream of the SGI1 complex integron in ORF S023. Thus, two subpopulations ofS. Kentucky ST198 independently and exclusively acquired the SGI1 during the 1980s and 1990s. Unlike the ST198-X1 African epidemic subpopulation, the ST198-X2 subpopulation mainly from Asia harbors variants of the SGI1-J subgroup that are encountered mainly in the Far East, as previously described forS. entericaserovars Emek and Virchow.