Identifying emerging trends in antimicrobial resistance using Salmonella surveillance data in poultry in Spain

Abstract

Despite of controls and preventive measures implemented along the food chain, infection with non-typhoidal Salmonella (NTS) remains one of the major causes of foodborne disease worldwide. Poultry is considered one of the major sources of NTS. This has led to the implementation of monitoring and control programmes in many countries (including Spain) to ensure that in poultry flocks infection is kept to a minimum and to allow the identification and monitoring of circulating NTS strains and their antimicrobial resistance (AMR) phenotypes. Here, we investigated the information from the monitoring programme for AMR in Salmonella from poultry in Spain in 2011-2017 to assess the diversity in phenotypic resistance and to evaluate the programme's ability to detect multi-resistance patterns and emerging strains in the animal reservoir. Data on serotype and AMR to nine antimicrobials obtained from 3,047 NTS isolates from laying hens (n = 1,060), broiler (n = 765) and turkey (n = 1,222) recovered during controls performed by the official veterinary services and food business operators were analysed using univariate and multivariate methods in order to describe host and serotype-specific profiles. Diversity and prevalence of phenotypic resistance to all but one of the antimicrobials (colistin) were higher in NTS from broiler and turkey compared with laying hen isolates. Certain combinations of serotype and AMR pattern (resistotype) were particularly linked with certain hosts (e.g. susceptible Enteritidis with laying hens, multi-drug resistant (MDR) Derby in turkey, MDR Kentucky in turkey and broiler). The widespread presence of certain serotype-resistotype combinations in certain hosts/years suggested the possible expansion of MDR strains in the animal reservoir. This study demonstrates the usefulness of the analysis of data from monitoring programmes at the isolate level to detect emerging threats and suggests aspects that should be subjected to further research to identify the forces driving the expansion/dominance of certain strains in the food chain.

Keywords: Non-typhoidal Salmonella; antimicrobial resistance; foodborne; monitoring; poultry; serotype Kentucky.

Figure 1

Venn diagram showing the degree of overlap of 94 resistotypes present in 3,047 Salmonella isolates retrieved from laying hen, broiler and turkey samples in 2011–2017 in Spain [Colour figure can be viewed at http://www.wileyonlinelibrary.com/]

Figure 2

Diversity in the distribution of resistotypes depending on the host of origin in 3,047 Salmonella isolates retrieved in 2011–2017 in Spain. Bars represent confidence intervals around the Simpson's diversity index estimated through 1,000 bootstrap replicates

Figure 3

Resistotype richness in 3,047 Salmonella isolates retrieved from laying hen, broiler and turkey samples in Spain in 2011–2017. Change in resistotype accumulation curves with increasing sample sizes for isolates recovered from samples of broiler, turkey and laying hen

Figure 4

Multiple correspondence analysis (MCA) of 3,047 Salmonella isolates retrieved in 2011–2017 in Spain (first two dimensions). (a) Distribution of the antimicrobial resistance, serotype and host variables included in the MCA. Antimicrobial resistance variables are indicated by the abbreviation followed by R_1 (resistance) or R_0 (susceptibility). (b) Distribution of observations into four clusters as determined by hierarchical clustering [Colour figure can be viewed at http://www.wileyonlinelibrary.com/]

Figure 5

Proportion of isolates recovered from laying hen, broiler and turkey samples belonging to the Salmonella Kentucky and Salmonella Derby (only turkey isolates) serotypes during 2011–2017. Bars represent confidence intervals around the proportions estimated using the Pearson‐Klopper method [Colour figure can be viewed at http://www.wileyonlinelibrary.com/]