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. 2025 Aug 7;104(11):105647. doi: 10.1016/j.psj.2025.105647

Whole genome sequencing of Salmonella in poultry from China reveals the presence of blaNDM-5 in different serotypes

Yi Zhou a, Ke Wu a, Heng Lin a, Yu-Lian Hu a, Wei Xu a, Jie Zhang a, Sheng Zhou b, Kai Yu b, Chun-Guo Liu b, Hong-Ning Wang a, Chang-Wei Lei a,⁎
PMCID: PMC12361821  PMID: 40803221

Abstract

Salmonella is a significant zoonotic pathogen, which carries diverse antibiotic resistance genes (ARGs) and utilizes poultry as a major reservoir. It spreads along the farm-to-table continuum, posing risks of human salmonellosis and clinical infections. In this study, 144 Salmonella strains were isolated from 741 poultry samples across 23 provinces in China. Whole genome sequencing (WGS) identified 16 serotypes and 18 sequence types (STs); the main serotypes are S. Enteritidis, S. Kentucky, S. Indiana and S. Typhimurium. SNP analysis of S. Enteritidis and S. Kentucky revealed potential transmission events (SNPs < 10), which were concentrated in close provinces. Antimicrobial susceptibility testing provides information on antimicrobial resistance phenotype, with over 50 % exhibiting multidrug resistance (MDR). Bioinformatics analysis revealed 67 ARGs in all strains, including 6 blaNDM-5-positive isolates. Nanopore sequencing revealed that blaNDM-5 genes in different isolates were located on IncHI2/ST3 plasmids or chromosomes. The ability of horizontal transfer was verified by inverse PCR and conjugation experiments. Notably, this is the first report of blaNDM-5-positive S. Idikan. This study revealed Salmonella's current prevalence status in poultry from China and emphasized the transmission of blaNDM-5 in poultry, which can help guide the rational use of antibiotics and the formulation of relevant rules in poultry breeding.

Keywords: Salmonella enterica, Poultry, Whole genome sequencing, blaNDM-5

Introduction

Non-typhoidal Salmonella (NTS), the predominant zoonotic bacteria, are primarily transmitted to humans through consumption of contaminated animal-derived foods — particularly poultry products (Abebe et al., 2020). Colonization by this pathogen typically manifests as self-limiting gastrointestinal syndromes, including food poisoning and acute diarrhea, while invasive infections may progress to life-threatening systemic complications such as bacteremia in immunocompromised hosts (Bresee, et al., 2012; Lu, et al., 2025). Given its substantial public health burden, Salmonella has been systematically monitored throughout poultry production chains, including breeding, slaughtering, and transportation processes (Adhikari, et al., 2025). Global surveillance data consistently demonstrate persistent Salmonella contamination in retail meat products (Chen, et al., 2024; Peng, et al., 2024). This contamination risk may originate from Salmonella colonization in poultry during breeding processes, which can subsequently facilitate cross-contamination throughout production chains (Meng, et al., 2025). Notably, the epidemiological patterns of Salmonella infection exhibit variations across poultry farming systems, with infection risks being modulated by heterogeneous factors including farm environments, feed formulations, avian species, and flock age distributions (Tang, et al., 2023; Wang, et al., 2024). In China, previous investigations have revealed Salmonella prevalence rates ranging from 10 % to 50 % across poultry production chains. Particularly, waterfowl species (ducks and geese) demonstrate significantly higher colonization rates compared to chickens (Chen, et al., 2025; Guan, et al., 2022; Wang, et al., 2020; Wu, et al., 2025). However, current surveillance data might be biased due to limited sample diversity in some studies, potentially leading to inaccurate estimations of both prevalence rates and serotype distributions. Therefore, a large-scale survey of Salmonella in different regions and species is needed to eliminate the possible influence of a single clone.

The misuse and inappropriate use of antibiotics will lead to the bacterial resistance (Islam, et al., 2024). With the cross-species transmission of pathogens and their antimicrobial resistance, the World Health Organization (WHO) has updated its ‘WHO Bacterial Priority Pathogens List 2024′ categorizing fluoroquinolone-resistant NTS as a high-priority pathogen and third-generation cephalosporin-resistant Enterobacterales as critical-priority pathogens (WHO, 2024). However, clinically isolated Salmonella strains frequently exhibit resistance to these commonly used antibiotics, resulting in treatment failures (Mkangara, 2023). Carbapenems, serving as last-resort β-lactam antibiotics, is one of the important treatment strategies in clinical practice. Carbapenem resistant Enterobacteriaceae (CRE) have been widely concerned, among which blaNDM-positive Salmonella is generally considered to be a relatively rare situation (Jean, et al., 2025; Wang, et al., 2025; Wu, et al., 2024). However, in recent years, the emergence of carbapenem resistant Salmonella enterica (CRSE) has been reported in many countries around the world (Wu, et al., 2023). Consequently, it is imperative to maintain ongoing surveillance of Salmonella and its antimicrobial resistance, particularly in food-producing animals.

In this study, we collected poultry samples from 23 provinces in China, investigating the prevalence and distribution of Salmonella. Whole genome sequencing was performed on all isolates, and a detailed genetic environment analysis was conducted for the blaNDM-5 genes, with their transmission ability assessed. This study provides a scientific basis for understanding the prevalence and spread of Salmonella and its antibiotic resistance in poultry, thus assisting in the development of relevant countermeasures.

Materials and methods

Sample collection

A total of 741 samples were collected from poultry farms in 23 provinces of China during 2024, including chickens (n = 552), ducks (n = 152) and geese (n = 37). All samples were viscera (liver, spleen, heart, gut) of dead poultry with symptoms. Samples were stratified into three age groups: 0-21 days (n = 193), 21-60 days (n = 383), and > 60 days (n = 165). After collecting the basic information (host, age and province), the samples were transferred to sterile sampling bags and transported to the laboratory using low-temperature preservation (foam box with coolant-packs) within 24 h. The samples were systematically processed within 4 h after receiving, including homogenization with PBS, and centrifugation at 3,000 × g for 10 min at 4°C to obtain the supernatant for subsequent use.

Salmonella isolation

The supernatant was initially enriched with buffered peptone water (BPW) (Hope Bio, Qingdao, China) and treated at 37 °C, 180 rpm for 12 h. Then it was inoculated into rappaport vassiliadis (RV) (Hope Bio, Qingdao, China) medium and treated at 42 °C, 180 rpm for 20 h. Cultures of each sample were inoculated on xylose lysine tergitol-4 (XLT-4) (Hope Bio, Qingdao, China) agar and incubated at 37 °C for 20 h. The suspicious single colony with transparent edge and black center was picked for PCR to verify whether it carried invA gene (Table S2) (Rahn, et al., 1992). All identified Salmonella were cultured with brain heart infusion (BHI) broth (Hope Bio, Qingdao, China), mixed with 50 % glycerol, and then stored at −80 °C.

Antimicrobial susceptibility testing

Antimicrobial susceptibility testing of 144 Salmonella strains was performed using the standard Kirby-Bauer disk diffusion method against 14 antimicrobial agents, including ampicillin/sulbactam (AMS, 20 μg), cefotaxime (CTX, 30 μg), cefoxitin (FOX, 30 μg), cefazolin (CFZ, 30 μg), imipenem (IMI, 10 μg), azithromycin (AZM, 15 μg), doxycycline (DXT, 30 μg), tigecycline (TGC, 15 μg), colistin sulfate (CS, 10 μg), ciprofloxacin (CIP, 5 μg), florfenicol (FFC, 30 μg), chloramphenicol (CHL, 30 μg), gentamicin (GEN, 10 μg), and trimethoprim-sulfamethoxazole (SXT, 25 μg). The results were determined according to the Clinical and Laboratory Standards Institute (CLSI) M100-Ed34. E. coli ATCC 25922 was used as the quality-control strain.

Whole-genome sequencing and bioinformatics analysis

Genomic DNA from different Salmonella isolates was extracted using TIANamp Bacteria DNA Kit (Tiangen, Beijing, China). WGS was performed on the Novaseq 6000 (Illumina, San Diego, USA) sequencer. The raw data was evaluated and filtered through Fastp (Chen, et al., 2018). The clean reads were assembled using Unicycler v0.5.0 (https://github.com/rrwick/Unicycler), and genomic quality of the assemblies was identified using checkM v.1.0.12 (Parks, et al., 2015). Antibiotic resistance genes (ARGs), virulence genes and plasmid replicon types were screened using ABRicate (https://github.com/tseemann/abricate) against ResFinder (Bortolaia, et al., 2020), VFDB (https://www.mgc.ac.cn/VFs/), and PlasmidFinder (Carattoli and Hasman, 2020). Salmonella Genomic Island 1 was screened using BLASTn. Multi-locus sequence typing (MLST) of the Salmonella isolates was performed using PubMLST (https://pubmlst.org/multilocus-sequence-typing) and serotyping was performed using SISTR (Yoshida, et al., 2016). A threshold of 90 % identity and 90 % coverage was applied to all sequence similarity analyses. Genome annotations of the isolates were performed using Rapid Annotation using Subsystem Technology (RAST) (https://rast.nmpdr.org/) and Prokka v1.14.5 (Seemann, 2014). Core genome alignment was generated using Snippy v4.6.0 (https://github.com/tseemann/snippy). Variant calling was performed by FreeBayes to identify single-nucleotide polymorphisms (SNPs), and a strict core genome alignment was extracted using snippy-core. The maximum likelihood trees of Salmonella isolates were constructed based on core-genome SNPs using FastTree v2.1 (Price, et al., 2009) and modified using iTOL (https://itol.embl.de/). Genomic DNA of Salmonella strains harboring blaNDM-5 was sequenced on the Oxford Nanopore platform by rapid barcoding sequencing (SQK-RBK004). Genome sequences were hybrid-assembled de novo using Unicycler v0.5.0 with integrated Illumina short-read and Nanopore MinION long-read data. Insertion sequences (ISs) were found using ISfinder (https://isfinder.biotoul.fr/about.php). Plasmid maps and genetic environments of blaNDM-5 were constructed using BRIG 0.95 (Alikhan, et al., 2011) and EasyFig 2.2.2 (https://mjsull.github.io/Easyfig/). All bioinformatic analyses were executed using default parameters unless otherwise specified.

Conjugation experiments and inverse PCR

Conjugation experiments using plasmid-borne blaNDM-5-positive strains as donors and E. coli J53 as recipient were performed to assess blaNDM-5 transmissibility. Both donors and recipients were separately incubated in LB broth at 37°C for 4 h; then mixed at a 1:1 ratio and subjected to static conjugation at 37°C overnight. After mating, 100 μL of the mixture was plated onto LB or eosin-methylene blue (EMB) (Hope Bio, Qingdao, China) agar plates containing imipenem (4 mg/L) and sodium azide (100 mg/L), and incubated for 18–24 h to select transconjugants. The blaNDM-5 genes located on chromosomes were evaluated for their transmission ability by verifying the formation of translocatable units (TUs) through inverse PCR (Table S2) (Zhao, et al., 2022).

Statistical analysis

SPSS version 27 was used for data analysis. The Chi-square test was used to assess differences between age groups. The Kruskal-Wallis test was used to determine whether there is a difference in ARGs and virulence genes of different serotypes, pairwise comparisons were conducted using Dunn's test and Bonferroni correction. The results were considered statistically significant at P < 0.05.

Results

Prevalence and distribution of Salmonella in different poultry species

A total of 144 Salmonella strains (19.4 %) were isolated from 741 samples of dead poultry (Fig. 1a and 1c). The highest isolation rate was observed in duck samples (31.6 %, 48/152), followed by goose (24.3 %, 9/37) and chicken (15.8 %, 87/552). Among major poultry-producing provinces with larger sample sizes, the Salmonella infection rates were as follows: Shandong (25.9 %, 83/321), Liaoning (16.5 %, 14/85), Hebei (10.3 %, 8/78), and Henan (21.4 %, 15/70) (Fig. 1b). Age-related analysis revealed that Salmonella infections occurred more frequently in juvenile poultry (0-21 days, 25.4 %, 49/193) and immature poultry (21-60 days, 23.0 %, 88/383), while adult poultry (over 60 days) showed lower positivity rates than them (4.2 %, 7/165) (P < 0.001) (Table 1).

Fig. 1.

Fig 1

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Distribution of samples and Salmonella isolates in this study. (a) The number of samples from different provinces. (b) Prevalence of Salmonella in samples from different provinces, hosts and ages. (c) Distribution of Salmonella isolates according to province, serotype, age and host.

Table 1.

Isolation rates of Salmonella in different poultry and age groups.

Host Age (days) Number of samples Number of Salmonella Percentage of Salmonella in each age (%) Percentage of Salmonella in total samples (%)
Chicken 0-21 165 32 19.4 15.8
21-60 259 51 19.7
60- 128 4 3.1
Duck 0-21 26 16 61.5 31.6
21-60 112 32 28.6
60- 14 0 0
Goose 0-21 2 1 50.0 24.3
21-60 12 5 41.7
60- 23 3 13.0
Total 0-21 193 49 25.4 19.4
21-60 383 88 23.0
60- 165 7 4.2
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Susceptibility of Salmonella to antimicrobial agents

Antimicrobial susceptibility testing against 14 agents was conducted for all 144 Salmonella isolates (Fig. 2a). The highest resistance rate was observed to cefotaxime (71.5 %, 103/144). Resistance rates exceeding 55 % were detected for six antibiotics: gentamicin (64.6 %, 93/144), trimethoprim-sulfamethoxazole (59.0 %, 85/144), ciprofloxacin (56.9 %, 82/144), chloramphenicol (56.9 %, 82/144), florfenicol (56.2 %, 81/144), doxycycline (55.6 %, 80/144). Furthermore, over half of the isolates (61.1 %, 88/144) were classified as multidrug resistant (MDR) (Magiorakos, et al., 2012), demonstrating resistance to three or more antimicrobial categories (Fig. 2b).

Fig. 2.

Fig 2

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Antimicrobial resistance pattern of 144 strains of Salmonella. (a) Antibiotic susceptibility of the Salmonella isolates. (AMS: ampicillin/sulbactam, CTX: cefotaxime, FOX: efoxitin, CFZ: cefazolin, IMI: imipenem, AZM: azithromycin, DXT: doxycycline, TGC: tigecycline, CS: colistin sulfate, CIP: ciprofloxacin, FFC: florfenicol, CHL: chloramphenicol, GEN: gentamicin, SXT: rimethoprim-sulfamethoxazole) (b) MDR of the Salmonella isolates.

Molecular characteristics of Salmonella

WGS was performed on all 144 Salmonella isolates, revealing 16 distinct serotypes (Fig. 3). The dominant serotypes were S. Enteritidis (29.2 %, 42/144), S. Kentucky (27.8 %, 40/144), S. Indiana (15.3 %, 22/144) and S. Typhimurium (9.0 %, 13/144). MLST confirmed 18 distinct and serotype-specific sequence type (ST) associations: all S. Enteritidis isolates belonged to ST11, S. Kentucky to ST198, S. Indiana to ST17 with one ST2040 variant, S. Typhimurium to ST19 with two ST99, demonstrating serotype-specific ST clustering patterns among the sampled Salmonella populations.

Fig. 3.

Fig 3

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Core genome-derived phylogenetic tree of 144 Salmonella isolates, serotypes are represented by different colors.

ARG annotation identified 67 distinct genes spanning 11 antibiotic categories (Fig. 4a). High-prevalence ARGs included blaTEM-1 (50.0 %, 72/144), aph(3′)-Ia (48.6 %, 70/144), floR (47.9 %, 69/144), blaCTX-M-55 (41.0 %, 59/144), lnu(F) (38.2 %, 55/144), dfrA14 (36.1 %, 52/144), arr-2 (34.7 %, 50/144), and mph(A) (34.7 %, 50/144). Extended-spectrum β-lactamase (ESBL)-associated blaCTX-M variants were detected in 62.5 % (90/144) of isolates. All six imipenem-resistant Salmonella strains identified in prior antimicrobial susceptibility testing harbored blaNDM-5, corroborating phenotypic carbapenem resistance.

Fig. 4.

Fig 4

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Characteristics of Salmonella isolates. (a) Differences of ARGs in Salmonella from different species. (b) Differences in the number of ARGs in dominant serotypes. (c) Differences in the number of virulence genes in dominant serotypes.

Plasmid replicon analysis identified nine types, containing IncFIB (43.8 %, 63/144), IncFII (33.3 %, 48/144), IncHI2 (14.6 %, 21/144), Incl1 (7.6 %, 11/144), IncN (5.6 %, 8/144), IncQ (3.5 %, 5/144), IncX1 (13.9 %, 20/144), IncX4 (1.4 %, 2/144), and IncY (2.8 %, 4/144). BLASTn-based screening of the intSGI1 integrase identified 40 SGI1-positive strains. All SGI1-bearing isolates belonged to S. Kentucky, a serotype exhibiting minimal plasmid replicon carriage, suggesting chromosomal integration as the primary driver of its multidrug resistant phenotype.

The results of virulence gene annotation showed that a total of 139 specific virulence genes were identified, and the types of virulence genes carried by all isolates were: csg, fim (biofilm); ent, fep (iron uptake); inv, sop, ssa, ssc, sse, pip (T3SS); ompA (outer membrane protein). In addition, the ybt genes encoding yersiniabactin were specifically found in S. Infantis.

Overall, among the four dominant serotypes, S. Kentucky and S. Indiana carried the most ARGs (Fig. 4b), while S. Typhimurium and S. Enteritidis were more abundant in virulence genes (Fig. 4c). In addition, SNP analysis of the mainstream serotypes S. Enteritidis and S. Kentucky revealed potential transmission events (SNPs < 10), which were concentrated in adjacent or close provinces (Fig. 5). It is presumed that the transmission of bacteria may be caused by transportation or personnel flow between farms in different regions.

Fig. 5.

Fig 5

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SNP analysis of the mainstream serotypes S. Enteritidis and S. Kentucky revealed potential transmission events. (a) SNP distances in different S. Enteritidis isolates. (b) SNP distances in different S. Kentucky isolates.

Location and genetic environments of blaNDM-5

All blaNDM-5-positive strains (4.2 %, 6/144) were subjected to nanopore sequencing to determine blaNDM-5 gene location. These isolates were divided into three serotypes S. Kentucky (S026), S. Indiana (S029, S064, S094, S130), and S. Idikan (S135). Among them, S064, S130 and S135 were located on the IncHI2/ST3 plasmid; S026, S029 and S094 were located on the chromosome (Table 2). Phylogenetic relationship analysis results showed that there were 25 SNP differences between S064 and S130, 19 SNP differences between S029 and S094, indicating that blaNDM-5-positive S. Indiana belonged to different isolates.

Table 2.

Information about blaNDM-5 positive strains.

Isolates MLST Serotype Resistance genes Location Conjugation frequency
S026 198 Kentucky aac(3)-Iva, aadA2, aph(3′)-Ia, aph(4)-Ia, arr-2, blaCTX-M-55,blaNDM-5, blaTEM-1, bleMBL, dfrA14, floR, fosA3, mph(A), sul1 Chromosome ND
S029 17 Indiana aac(3)-Iva, aac(6′)-Ib-D181Y, aadA22, aph(3′)-Ia, aph(4)-Ia, aph(6)-Id, arr-3, blaCTX-M-55,blaNDM-5, blaOXA-1, bleMBL, bleO, catB3, lnu(F), mph(A), sul2 Chromosome ND
S064 17 Indiana aac(3)-Iva, aadA1, aadA2, aph(3′')-Ib, aph(3′)-Ia, aph(4)-Ia, aph(6)-Id, blaCTX-M-55,blaNDM-5, blaTEM-1, bleMBL, dfrA12, fosA3, lnu(F), mph(A), rmtB1, sul1 IncHI2/ST3 ND
S094 17 Indiana aac(3)-Iva, aac(6′)-Ib-D181Y, aadA22, aadA5, aph(3′)-Ia, aph(4)-Ia, aph(6)-Id, arr-3, blaCTX-M-55,blaNDM-5, blaOXA-1, bleMBL, bleO, catB3, dfrA17, lnu(F), mcr-1.1, mph(A), oqxA, oqxB, sul2 Chromosome ND
S130 17 Indiana aac(3)-Iva, aadA1, aadA2, aph(3′')-Ib, aph(3′)-Ia, aph(4)-Ia, aph(6)-Id, blaCTX-M-55,blaNDM-5, blaTEM-1, bleMBL, dfrA12, fosA3, lnu(F), mph(A), rmtB1, sul1 IncHI2/ST3 ND
S135 1561 Idikan aac(3)-Iva, aadA2, aph(3′')-Ib, aph(3′)-Ia, aph(4)-Ia, aph(6)-Id, arr-2, blaCTX-M-65, blaNDM-5, blaOXA-10,bleMBL, dfrA14, floR, fosA7.3, lnu(F), qnrS1, qnrS2, sul3 IncHI2/ST3 4.05×10−4
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Notes: ND, no data.

IncHI2 plasmids in this study were all around 230,000 bp in size (Fig. 6a), two of which (S064, S130) lack the essential T4CP and relaxase genes required for conjugative transfer (Li, et al., 2018), which explained the failure of the conjugation. The plasmid in S. Idikan (S135) could be successfully transferred to E. coli J53 by conjugation experiments. The genetic environment of blaNDM-5 on IncHI2 plasmids was similar to those previously reported (MN915010/MN915011, E. coli; CP104628, K. pneumoniae), which can form a circular structure Tn7051 (IS3000-ΔISAba125-IS5-ΔISAba125-blaNDM-5-bleMBL-trpF-dsbC-IS26-ΔumuD-∆ISKox3-IS3000), but some regions are missing or replaced (Fig. 6b).

Fig. 6.

Fig 6

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Location and genetic environments of blaNDM-5 in different Salmonella isolates. (a) Comparison of blaNDM-5-carrying plasmid IncHI2. (b) Genetic environment of blaNDM-5-carrying plasmid. (c) Comparison of chromosomal genetic environment between blaNDM-5-positive and blaNDM-5-negative isolates.

By comparing with the reference sequences of two serotypes (S. Kentucky: CP043664, CP092012, CP089794; S. Indiana: CP028131, CP033387, CP101340), we found that the blaNDM-5 located on the chromosome was the chromosomal integration of the multidrug resistance region (MDRR) mediated by IS26, and there were multiple copies of IS26 in MDRR (Fig. 6c). Here we verified that it can form TUs by inverse PCR, suggesting its transmission ability among bacterial individuals. The TUs were displayed in Fig. 6c.

Discussion

Overdependence and improper use of antibiotics in poultry farming can result in the development of severe antibiotic resistance in bacteria, which can spread through the production chain from farm to table. In addition, if the bacteria carry some of the ARGs that are critical in the clinic, it may result in no drugs being available for treating human infections. China faces severe challenges from antibiotic misuse and environmental contamination by residual antibiotics, largely attributable to historically unregulated antimicrobial use in livestock production – a primary driver of escalating residue levels in food and ecosystems (Hanna, et al., 2018). A 2013 survey reported total antibiotic production of 248,000 tons in China, with 52 % used in livestock husbandry (Ying, et al., 2017). Since 2017, the Chinese government (https://english.moa.gov.cn/) has implemented a series of measures to regulate antibiotic usage in food animal production (Shao, et al., 2021). Nevertheless, translating these regulatory measures into standardized on-farm practices necessitates sustained collaboration between policymakers, enforcement agencies, and livestock producers.

Poultry, as an important and huge reservoir of Salmonella, serves as a key part of the spread of Salmonella from the perspective of ‘One Health’. Salmonella prevalence exhibits significant differences among poultry species. From recent studies, the prevalence of Salmonella in waterfowl may be higher than that in chickens. Isolation rates of Salmonella in dead duck embryos across Shandong were as high as 40 %, with associated environmental and duck feces approaching 20 % (Song, et al., 2024). In addition, Salmonella can be detected in different parts of the duck production chain (Kang, et al., 2022). We hypothesize that higher prevalence rates of Salmonella in waterfowl are related to waterfowl husbandry practices. Compared with large-scale cage chicken farms, the water environment provides a broader enrichment space for bacteria. Due to cross-contamination risks during slaughtering and processing stages, bacterial accumulation in animal-derived food may occur when it reaches retail markets. For example, the previously reported isolation rate of Salmonella in poultry meat in Sichuan and Guangdong retail markets is close to 50 % (Chen, et al., 2021; Zeng, et al., 2025), indicating that purification treatments during slaughter and processing require strengthening to minimize pathogen contamination.

Salmonella isolated in this study were categorized into 16 different serotypes and S. Kentucky has a high prevalence and high antibiotic resistance. Fluoroquinolones and third-generation cephalosporins are the most commonly used antibiotics in the clinical treatment of Salmonella infection, but since the 2000s, the resistance to these antibiotics has been observed in S. Kentucky, and this serotype has a trend of spreading worldwide, becoming the mainstream serotype of Salmonella from poultry (Le Hello, et al., 2013, 2011). Its main ST is ST198, which is the most common ST causing human infection the same as type of S. Kentucky isolated in this study (Hawkey, et al., 2019). A study of S. Kentucky by Beijing Centers for Disease Control and Prevention from 2016 to 2023 showed that 49 human and 5 chicken S. Kentucky isolates were resistant to fluoroquinolones and tetracyclines, with 60 % of them being resistant to more than 9 antibiotics (Qu, et al., 2024). The four-year monitoring results of Salmonella in a scale layer farm in Jiangsu showed that S. Kentucky ST198 gradually replaced the dominant position of S. Enteritidis, and was detected in many areas of the farm environment (Liu, et al., 2024). In this study, more than half of Salmonella isolates carried diverse ESBL genes, with the majority observed in S. Kentucky, demonstrating its concerning antimicrobial resistance profile.

In China, the main serotypes of CRSE are S. Typhimurium and S. Indiana, from human or chicken (Huang, et al., 2025; Ke, et al., 2024; Sun, et al., 2023; Wang, et al., 2017). The blaNDM genes are mainly carried by IncX3 or IncHI2 plasmids (He, et al., 2023). Tn7051 is considered to be a new compound transposon carrying blaNDM-5 and exists on the IncHI2/ST3 plasmid. The first report of Tn7051-positive isolate is E. coli from ducks in Guangdong, and gradually appeared in K. pneumoniae in Anhui, as well as Salmonella in Guangdong (Deng, et al., 2024). The blaNDM-5-positive Salmonella isolates from Shandong in this study demonstrate that the IncHI2/ST3 plasmid has been detected in additional provinces of China—with one isolate (S135) successfully transferred to E. coli J53 via conjugation—suggesting its potential to disseminate as a new vector of blaNDM-5. In addition, IS26 plays a critical role in facilitating the acquisition and transmission of bacterial ARGs (Harmer, et al., 2014). Through homologous recombination (HR) between two similar copies of IS26 in the MDRR of bacterial chromosome, a circular translocatable unit (TU) is formed, enabling dissemination between different individuals (Partridge, et al., 2018). In this study, specific primers were designed for Salmonella isolates with blaNDM-5 located on their chromosome, to verify the ability of forming TUs between IS26 copies. Collectively, we demonstrated the horizontal transferability of the blaNDM-5 gene carried by Salmonella in both plasmid-borne and chromosomal contexts.

Conclusion

In conclusion, we characterized 144 Salmonella isolates collected from 741 poultry samples in 23 provinces of China. Through WGS and bioinformatics analysis, we found 16 distinct serotypes and revealed four prevalent serotypes: S. Enteritidis, S. Kentucky, S. Indiana and S. Typhimurium. The antimicrobial resistance profiles showed that the MDR rate of Salmonella was 61.1 %. Six strains carried clinically important ARG blaNDM-5 and their genetic environments has been resolved. Notably, this study is the first report of blaNDM-5-positive S. Idikan in China, signaling the emergence of CRSE across diverse Salmonella serotypes. We speculate that blaNDM-5 carried by IncHI2/ST3 plasmids is spreading to more regions. In addition, the formation of TUs mediated by IS26 also promotes the spread of blaNDM-5 among different bacterial individuals as well as between chromosomes and plasmids. Our findings show the Salmonella’s current prevalence status in poultry of China and fill the data gap of CRSE. Based on the perspective of ‘One Health’, implementing comprehensive surveillance throughout the animal-derived food is crucial to ensure products safety and public health.

Data availability

The whole genome of Salmonella isolates in this study was submitted to the GenBank database under the BioProject number: PRJNA1267742.

CRediT authorship contribution statement

Yi Zhou: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Visualization, Writing – original draft, Writing – review & editing. Ke Wu: Methodology, Software. Heng Lin: Resources, Visualization. Yu-Lian Hu: Investigation, Resources. Wei Xu: Investigation, Resources. Jie Zhang: Investigation, Resources. Sheng Zhou: Investigation, Resources. Kai Yu: Data curation, Investigation, Resources. Chun-Guo Liu: Investigation, Resources. Hong-Ning Wang: Funding acquisition, Writing – review & editing. Chang-Wei Lei: Conceptualization, Funding acquisition, Resources, Writing – review & editing.

Disclosures

The authors have no competing interests to declare.

Acknowledgments

This work was supported by the National Key Research and Development Program of China (Grant numbers 2022YFD1800400 and 2022YFC2303900), the Natural Science Foundation of Sichuan Province (grant number 2025ZNSFSC0209), and the earmarked fund for China Agriculture Research System (CARS-40-K14).

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.psj.2025.105647.

Appendix. Supplementary materials

Table S1. Information of Salmonella isolates in this study.

mmc1.xlsx (83.8KB, xlsx)

Table S2. The primers used in this study.

mmc2.docx (16.7KB, docx)

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Table S1. Information of Salmonella isolates in this study.

mmc1.xlsx (83.8KB, xlsx)

Table S2. The primers used in this study.

mmc2.docx (16.7KB, docx)

Data Availability Statement

The whole genome of Salmonella isolates in this study was submitted to the GenBank database under the BioProject number: PRJNA1267742.

Articles from Poultry Science are provided here courtesy of Elsevier

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