Since it has been established that ampicillin and trimethoprim/sulfamethoxazole have become obsolete in salmonellosis therapy, high non-susceptibility rates to these antimicrobials were expected. In many countries, aminopenicillins, which include ampicillin, trimethoprim, sulfamethoxazole, and trimethoprim/sulfonamide combinations are among the most frequently used antimicrobials in livestock production [12, 26]. These antimicrobials are generally administered in all phases of hog production [26]. In this study, non-susceptibilities to ampicillin and trimethoprim/sulfamethoxazole were observed in 71.9% and 70.8% of S. enterica, respectively. Phongaran et al. [13] reported that 69.0% of Salmonella isolated from hogs in Thailand were resistant to ampicillin. However, in this study, only 35.7% were resistant to trimethoprim/sulfamethoxazole. One study conducted among hogs in Vietnam reported that 36.7% of Salmonella isolates were resistant to trimethoprim/sulfamethoxazole and only 41.3% to ampicillin [27]. On the other hand, low rates of resistance (< 5%) to ESC and ciprofloxacin were reported in both studies [13, 27], while this present study reported rates which were slightly higher (< 10%).
In this study, multidrug resistance was observed in 13.5% of S. enterica isolates. Reports of (multidrug-resistant) MDR Salmonella isolated from hogs in other Southeast Asian countries are higher (30–40%) (13,27). In other countries, even higher rates (70–80%) of MDR Salmonella isolated from pork and the pork production chain were observed [15, 28]. Out of 24 MDR S. enterica isolates in the present study, 15 and 8 were non-susceptible to ESC and fluoroquinolones, respectively, the current drug options in treating salmonellosis. Multidrug resistance is a challenge as it narrows down the options for antimicrobial therapy.
Majority of studies on bla genes and livestock animals in Southeast Asian countries are focused on E. coli in which blaTEM and blaCTX−M are the most frequently identified bla genes [12]. In Salmonella, blaTEM appears to be the most common. In India, Lalruatdiki et al. [14] observed that 30% of Salmonella isolated from a pig population were carrying blaTEM, and 10% were carrying blaCTX−M. Co-carriage of blaCTX−M and blaTEM has also been observed in extended-spectrum ß-lactamase (ESBL)-producing Salmonella from pigs [14, 29]. In the present study, co-carriage of blaTEM and blaCTX−M was found in seven (3.9%) isolates. However, none of these isolates were ESBL-producing which could suggest that these are only carrier of silent bla genes. The only ESBL-producing Salmonella in this study was carrying only blaTEM. While most blaTEM in the study possibly confer only broad-spectrum ß-lactam resistance considering the high rates of non-susceptibility to ampicillin, its presence in combination with other resistance determinants could render an isolate multidrug-resistant.
We report in this study that 71.3% of S. enterica isolates harbored PMQR. The genes qnrA, qnrB, and qnrS were observed in 12.9%, 39.3%, and 61.2% of the isolates, respectively. While Qnr proteins offer only low resistance against quinolones, the high incidence of PMQR may be a cause for concern since it has been shown to broaden the mutant selection window in bacteria [7]. Lin et al. [16] demonstrated that ciprofloxacin resistance conferred by PMQR is even comparable to that of quinolone target mutations. Prevalence rates of qnr genes appear to vary among samples and geographical locations. Cameron-Veas et al. [15] reported that 15% of S. enterica isolated from a pork production chain in Brazil were carrying qnrB, and none were carrying qnrA and qnrS. A separate study in China reported the prevalence of qnrA (0%), qnrB (16%), and qnrS (66%) [16] in foodborne Salmonella. In Thailand and in Laos, Sinwat et al. [17] found only 1–8% of S. enterica isolated from pork to be carrying the same qnr genes. This highlights the importance of a national surveillance of ARG since it appears individual countries seem to have different prevalence rates.
Several studies have also reported the association of qnr genes with bla genes. One MDR Salmonella isolated from a piglet in Spain was carrying both qnrB and blaCTX−M. Moawad et al. [8] found that 33% of Salmonella from poultry and beef in Egypt were carrying qnr genes and either blaCTX−M, blaTEM, or both. Whether qnr and bla genes reside within the same plasmid was not confirmed in either of the studies. However, Penha Filho et al. [9] recently isolated Salmonella from poultry in Brazil which carried both blaCTX−M−2 and qnrB in the same plasmid. In clinical isolates of S. enterica, E. coli, and K. pneumoniae, qnr genes have also been found within the same plasmid as that of blaTEM or blaCTX−M [10, 11]. In the present study, 81 blaTEM-carrying isolates and all 9 blaCTX−M-carrying isolates were harboring one to three qnr subtypes.