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. 2026 Jul 23;105(11):107483. doi: 10.1016/j.psj.2026.107483

Characterization of Campylobacter isolates from chicken farms and retail poultry meat

Xiaoyan Zhang a, Xiangyu Guo b, Mengjun Tang a, Qian Zhou a, Junxian Lu a, Xiujun Tang a, Dawei Chen a, Wanqiang Chen a, Yushi Gao a,⁎
PMCID: PMC13450189  PMID: 42531844

Abstract

Campylobacter is a major bacterial cause of gastroenteritis worldwide, and poultry meat is widely recognized as a principal reservoir for human Campylobacter infection. This study characterized the antimicrobial susceptibility profiles, genomic diversity, key antimicrobial-resistance determinants, and virulence genes of Campylobacter isolates collected from chicken farms and fresh retail poultry meat in ten regions of Jiangsu Province, China. The biofilm- forming capacity of selected strains was also evaluated. MLST identified CC-574 and CC-828 as the predominant clonal complexes of Campylobacter jejuni and Campylobacter coli, respectively. The isolates exhibited a broad range of sequence types (STs), including 21 previously documented STs in C. jejuni and 16 in C. coli, as well as six novel STs from C. jejuni and three novel STs from C. coli. Phylogenetic analysis revealed extensive genetic diversity among the Campylobacter isolates. Overall, 46.6 % of isolates were classified as MDR. The MDR proportion was significantly higher in C. coli (75.4 %) than in C. jejuni (17.5 %), and C. coli exhibited broader resistance across the ten antibiotics assessed. Among the detected resistance genes, the resistance-enhancing variant RE-CmeABC, which was primarily harbored by C. jejuni, had the highest prevalence (32.8 %), followed by tet(O) (31.3 %), the aminoglycoside resistance gene cluster aadEsat4-aphA-3 (21.9 %), and erm(B) (9.4 %). Virulence-gene profiling of the 128 Campylobacter isolates identified 10 virulence genes across five functional categories: adhesinon, invasion, immune modulation, motility, and toxin production. The wlaN gene, which is associated with Guillain–Barré syndrome, was detected in 7 (5.5 %) C. jejuni isolates. Among the 38 Campylobacter strains tested for biofilm formation, six C. coli isolates exhibited pronounce biofilm-forming capacity. These findings indicate that Campylobacter isolates from chicken farms and retail poultry meat pose potential public health risks, underscoring the need for targeted Campylobacter control strategies and providing a useful reference for future surveillance pograms.

Keywords: Campylobacter, Multidrug resistance, Genomic diversity, Biofilm, Potential risk

Introduction

Campylobacter is a leading pathogen responsible for bacterial foodborne diarrheal disease in humans, and poultry is one of its most important reservoirs (Blomvall et al., 2026). Campylobacter spreads horizontally in breeding environments, readily colonizes poultry, and is rapidly transmitted among birds within flocks (Taha-Abdelaziz et al., 2023). During slaughter, processing, and retail distribution, chicken carcasses and poultry products can be contaminated by intestinal contents from Campylobacter-positive birds, creating serious public health risks (Mota-Gutierrez et al., 2022; Newell et al., 2011). Approximately 56.5 % of human campylobacteriosis cases are linked to consumption and handling of contaminated poultry (EFSA, 2019; Wilson et al., 2008).

Campylobacter infection can cause fever, diarrhea, and abdominal pain, frequently accompanied by nausea and vomiting. In humans, campylobacteriosis may also be associated with sequelae such as reactive arthritis, Guillain–Barré syndrome (GBS), and irritable bowel syndrome (Kaakoush et al., 2015; Willison et al., 2016). Campylobacter outbreaks are reported worldwide (Yang et al., 2025). In China, foodborne outbreaks of Campylobacter have been reported in Lishui, Beijing, and other locations in southeastern China (Ge et al., 2026; Li et al., 2020; Zhang et al., 2024). In addition, antimicrobial resistance (AMR) in Campylobacter, particularly the emergence of multidrug resistance (MDR), has become a major public heath concern. The prevalence of Campylobacter strains resistant to clinically important antibiotics, such as fluoroquinolones, macrolides, and aminoglycosides, has increased markedly in recent years (Mourkas et al., 2019). In Beijing and Shanghai, China, Campylobacter isolates from patients with diarrhea showed resistance rates to ciprofloxacin, tetracycline, and nalidixic acid of more than 90 % (Gao et al., 2023; Zhang et al., 2020). In southern China, high resistance rates to ampicillin, sulfamethoxazole, and erythromycin were also observed among Campylobacter isolates from different retail meat products (Liu et al., 2026). Our previous studies have consistently highlighted the persistent presence of AMR in Campylobacter isolated from chicken slaughterhouses (Zhang et al., 2018, 2021).

Molecular typing of Campylobacter is essential for understanding the prevalence and potential cross-transmission of Campylobacter species among diverse hosts (O'Mahony et al., 2011). In China, several studies have examined the molecular characteristics of Campylobacter isolates from clinical and poultry sources (Yang et al., 2025; Zhang et al., 2020). However, the molecular epidemiology of Campylobacter in Jiangsu Province remains insufficiently characterized.

Biofilm formation on food-processing surfaces is a major food safety concern. Campylobacter can form biofilms on a range of abiotic materials, including stainless steel and plastics, which are commonly used in poultry-processing facilities (Laconi et al., 2023). Biofilm formation can protect Campylobacter cells from cleaning and disinfection and can contribute to persistent cross-contamination of food products, thereby increasing the risk of foodborne disease (Pokhrel et al., 2024). Previous studies have shown that Campylobacter can form biofilms under laboratory conditions, including microaerophilic conditions (Araújo et al., 2022; Bundurus et al., 2024).

Therefore, this study investigated the molecular typing and antimicrobial susceptibility profiles of Campylobacter isolates obtained from chicken farms and retail poultry meat in Jiangsu Province. The virulence potential and biofilm-forming abilities of these isolates were also assessed to further clarify their public health risks.

Materials and methods

Bacterial strains and culture conditions

A total of 128 Campylobacter isolates were obtained from different localities in Jiangsu Province, China, as part of our laboratory’s annual antimicrobial resistance surveillance programme. In total, strains were isolated from two sample matrices: chicken cloacal swabs and poultry meat. Specifically, 50 Campylobacter strains (35 C. jejuni, 15 C. coli) were obtained from farm chicken cloacal swabs (n = 130), 58 strains (18 C. jejuni, 40 C. coli) from retail chicken meat (n = 140), 14 strains (6 C. jejuni, 8 C. coli) from pigeon meat (n = 35), and 6 strains (4 C. jejuni, 2 C. coli) from duck meat (n = 21) (Table S1). Isolation and identification were performed according to the methodology described in a previous study (Zhang et al., 2018). Briefly, bacterial cultures were streaked onto modified charcoal-cefoperazone-deoxycholate agar (mCCDA) (Oxoid CM0739) and incubated at 42 °C for 36–42 h in a microaerophilic environment (5 % O2, 10 % CO2, and 85 % N2). Morphologically uniform colonies were selected and subcultured on Mueller–Hinton (MH) agar (Difco, MD) with blood, followed by incubation for 24–48 h at 42 °C under microaerobic conditions. All isolates were stored at −80 °C in brain-heart infusion (BD) broth containing 20 % (v/v) glycerol.

Antibiotic susceptibility testing

Antimicrobial susceptibility of Campylobacter isolates was tested using the Kirby−Bauer disk-diffusion method (Bauer et al., 1996) and interpreted according to Clinical Laboratory Standards Institute (CLSI., 2012) guidelines. The antibiotics (Oxoid) tested included macrolides: erythromycin (E, 15 µg) and azithromycin (AZM, 15 µg); quinolones and fluoroquinolones: ciprofloxacin (CIP, 5 µg); aminoglycosides: gentamicin (GEN, 10 µg) and tobramycin (TOB, 10 µg); tetracyclines: tetracycline (TE, 30 µg); β-lactams: ampicillin (AMP, 10 µg); chloramphenicol: florfenicol (FFC, 30 µg); sulfonamides: (SXT, 25 µg); and fosfomycin: (FOS, 50 µg). The reference strain C. jejuni ATCC 33560 was used for quality control in antimicrobial susceptibility testing. Isolates resistant to three or more antibiotic categories were defined as multidrug-resistant (MDR) isolates in this study. MARI (Multiple Antimicrobial Resistance Index) = a/b (a, the number of antibiotics to which the isolate was resistant; b, the total number of antibiotics to which the isolate was tested) (Krumperman, 1983).

Multilocus sequence typing (MLST) for Campylobacter

DNA was extracted from selected strains using a commercial TIANamp Bacteria DNA kit (TiangenBiotech Inc., Beijing, China). MLST was performed by sequencing seven housekeeping genes (aspA, glnA, gltA, glyA, pgm, tkt, and uncA) using previously described primers for Campylobacter (http://pubmlst.org/Campylobacter) (Dingle et al., 2001). The nucleotide sequences of the amplicons were determined by GenScript, Inc. (Nanjing, China). Allele numbers, sequence types (STs), and clonal complexes (CCs) were assigned using the Campylobacter PubMLST database. STs not found in the database were defined as new STs. The dendrogram tree of housekeeping genes data was visualized and edited using Interactive Tree Of Life.

Identification of toxin and antimicrobial resistance genes

Campylobacter isolates in this study were tested for virulence genes and antimicrobial resistance genes (ARGs). The 10 selected virulence genes (cadF, virB11, iam, wlaN, flhA, flaA, ciaB, cdtA, cdtB, and cdtC) and 4 ARGs (RE-CmeABC, aadEsat4-aphA-3 cluster, tet(O), and erm(B)) were detected by PCR in all strains. Genomic DNA was isolated from the strains using a TIANamp Bacteria DNA purification kit (TiangenBiotech Inc., Beijing, China). The primers used for these genes and the annealing temperatures for the different target genes are listed in Table S2. Each 25 µL reaction mixture contained 12.5 µL of GoTaq green master mix (Promega, Madison, WI), 1 µL of each forward and reverse primer (10 µM), 1 µL of template DNA, and 9.5 µL of nuclease-free water. The PCR thermocycling conditions were as follows: initial denaturation at 95 °C for 1 min, followed by 30 cycles of 95 °C for 30 s, annealing at the primer-specific temperature for 1 min, 72 °C for 1 min, and a final extension at 72 °C for 10 min. The amplified products were analyzed by 1.0 % agarose gel electrophoresis and subsequently sent to Sangon Biotech Co., Ltd. (Shanghai, China) for sequencing. Sequence alignment was performed using the GenBank BLAST online tool to confirm the identity of each amplified gene. A gene was considered “positive” if its BLAST result showed ≥98 % identity with the corresponding reference sequence.

Assessment of biofilm formation

Thirty-eight strains were selected for assessment of biofilm formation. The assay was conducted following the procedure described previously by Araújo (Araújo et al., 2022), with slight modifications. Briefly, overnight cultures of Campylobacter strains were adjusted with culture medium to achieve the desired inoculum concentration (about 106 CFU/mL). Aliquots of 200 µL were taken from the prepared cell suspensions and added to 96-well polystyrene microplates. For the negative control, two wells in each plate were filled only with culture medium. Two replicates of each strain were inoculated on each plate. The plates were then incubated for 72 h under microaerobic conditions at 42 °C.

Finally, crystal violet staining was performed for biofilm quantification as described by Xiao (Xiao et al., 2025). Briefly, culture medium was removed, and each well was washed three times with 200 μL of sterile water to remove excess cells. Next, 200 μL of 0.1 % crystal violet was added to each well and incubated for 15 min at room temperature before removal. The plate was rinsed 3-4 times with water to remove residual crystal violet. Thereafter, the plate was dried at 37 °C for a few hours. Subsequently, 30 % v/v glacial acetic acid was added to each well for elution. The microtiter plate was incubated at room temperature for 10-15 min. The absorbance of the solubilizing buffer was measured at 590 nm.

Data analysis

The bar graphs for “Prevalence (%) of antibiotic resistance”, “Prevalence (%) of virulence genes”, and “Prevalence (%) of resistance genes” were created using GraphPad Prism software. The chi-square test was used to compare such proportions between groups (C. jejuni, C. coli).

For quantitative data of biofilm formation ability, the independent t-test was conducted to evaluate the statistical differences between isolates. P-value < 0.05 was considered statistically significant.

Results

Antimicrobial resistance

Overall, 96 Campylobacter isolates were resistant to at least one of the tested antibiotics. A total of 46.6 % of the tested strains were classified as MDR; among these, 1 C. jejuni strain and 14 C. coli strains were resistant to 8 tested antibiotics. The MDR rate of C. coli (75.4 %) was significantly higher than that of C. jejuni (17.5 %) (Fig. 1A). For each of the ten antibiotics, resistance rates were higher in C. coli isolates than in C. jejuni isolates (Fig. 1B).

Fig. 1.

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Antimicrobial resistance of Campylobacter. (A) Numbers of MDR Campylobacter isolates; (B) Percentage of Campylobacter isolates resistant to various antibiotics.

Among C. coli isolates, resistance to tobramycin accounted for a large proportion (75.4 %), followed by resistance to azithromycin (70.8 %), erythromycin (69.2 %), ampicillin (69.2 %), tetracycline (67.7 %), gentamicin (63.1 %), and ciprofloxacin (58.5 %). Among C. jejuni isolates, resistance to ampicillin accounted for a large proportion (42.9 %), followed by resistance to tetracycline (23.8 %), tobramycin (17.5 %), and ciprofloxacin (17.5 %). Resistance to florfenicol and fosfomycin was detected in C. coli (16.9 % and 7.7 %) but not in C. jejuni isolates (Fig. 1B).

The MARI values of the tested C. coli and C. jejuni isolates are presented in Table 1, Table 2, respectively. A total of 37 antibiotic-resistance patterns, with MARI values ranging from 0 to 0.80, were observed among 65 C. coli isolates, whereas 16 antibiotic-resistance patterns, with MARI values ranging from 0 to 0.80, were observed among 63 C. jejuni isolates. The resistance spectra of C. coli were more diverse than those of C. jejuni.

Table 1.

Resistance spectra for 65 C.coli isolates to various antibiotic combinations.

MAR index No. of C. coli isolates
 Antibiotic resistance patterns
Farm Poultry meat
0 0 3 -
0.10 0 1 TOB
0.10 0 2 TE
0.20 1 2 E, AZM
0.20 1 0 CIP, TE
0.20 1 0 AMP, CIP
0.20 0 1 TOB, CIP
0.30 0 1 GEN, TOB, AMP
0.30 0 1 E, AZM, AMP
0.30 1 0 E, AZM, TOB
0.30 0 1 AMP, CIP, TE
0.30 0 1 AMP, TE, FFC
0.40 1 0 GEN, TOB, E, AZM
0.40 0 1 GEN, TOB, E, TE
0.50 0 2 GEN, TOB, AMP, CIP, TE
0.50 1 1 GEN, TOB, E, AZM, CIP
0.50 0 1 GEN, TOB, E, AZM, AMP
0.50 1 0 TOB, E, AZM, AMP, CIP
0.50 1 0 GEN, TOB, E, CIP, TE
0.50 0 1 SXT, E, AZM, AMP, CIP
0.50 0 1 E, AZM, AMP, CIP, TE
0.60 0 6 GEN, TOB, E, AZM, AMP, TE
0.60 0 2 TOB, E, AZM, AMP, CIP, TE
0.60 1 0 TOB, E, AZM, TE, FFC, FOS
0.60 0 1 E, AZM, AMP, TE, FFC, FOS
0.60 0 1 SXT, E, AZM, AMP, CIP, TE
0.60 0 1 GEN, TOB, E, AZM, CIP, TE
0.60 0 1 TOB, SXT, E, AZM, CIP, TE
0.60 0 1 GEN, TOB, E, AZM, AMP, CIP
0.70 0 1 GEN, TOB, SXT, E, AZM, AMP, TE
0.70 0 1 TOB, E, AZM, AMP, CIP, TE, FFC
0.70 3 3 GEN, TOB, E, AZM, AMP, CIP, TE
0.70 0 1 GEN, TOB, E, AZM, AMP, TE, FFC
0.80 2 3 GEN, TOB, SXT, E, AZM, AMP, CIP, TE
0.80 1 0 GEN, TOB, E, AZM, AMP, CIP, TE, FOS
0.80 0 7 GEN, TOB, E, AZM, AMP, CIP, TE, FFC
0.80 0 1 GEN, TOB, SXT, E, AZM, AMP, TE, FOS
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Table 2.

Resistance spectra for 63 C. jejuni isolates to various antibiotic combinations.

MAR index No. of C. jejuni isolates
 Antibiotic resistance patterns
Farm Poultry meat
0 14 18 -
0.10 3 6 AMP
0.10 0 1 TE
0.10 1 0 CIP
0.20 2 1 AMP, TE
0.20 1 1 GEN, AMP
0.20 2 0 AMP, CIP
0.20 1 0 TOB, AMP
0.30 2 0 AMP, CIP, TE
0.30 1 0 TOB, AMP, TE
0.30 1 0 TOB, E, AZM
0.40 3 0 TOB, AMP, CIP, TE
0.50 1 0 GEN, TOB, SXT, AMP, TE
0.50 1 0 GEN, TOB, AMP, CIP, TE
0.60 1 1 GEN, TOB, SXT, AMP, CIP, TE
0.80 1 0 GEN, TOB, SXT, E, AZM, AMP, CIP, TE
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MLST typing analysis

Fifty-two C. jejuni strains and 45 C. coli strains were selected for MLST molecular typing, and the results are presented in Table 3, Table 4. MLST analysis revealed a diverse range of sequence types (STs), including 21 previously reported STs for C. jejuni and 16 for C. coli, as well as six and three previously undescribed STs for the respective species. The most frequent CC in C. jejuni was CC-574 (26.9 %, 14/52), comprising ST6922, ST9617, ST9955, and ST8880, followed by CC-354 (9.6 %, 5/52), comprising ST653, ST2988, and ST5287. The remaining CCs included relatively few STs or a small number of isolates. Three C. jejuni STs (ST8880, ST4324, and ST14483) were detected in 2 districts. For C. coli, except for 2 unassigned STs (ST11899 and ST12337), all other STs were assigned to the same clonal complex, CC-828. Most C. coli STs (68.8 %, 11/16) were detected in two or more districts. A summary of allele numbers for the new Campylobacter STs identified in this study is presented in Table S3.

Table 3.

MLST typing results for C. jejuni.

CC ST (n) Source District
21 7419 (1) Poultry meat SQ
45 3456 (1) Poultry meat XZ
179 220 (3) Poultry meat HA
354 653 (1) Farm LYG
2988 (2) Poultry meat CZ
5287 (2) Farm CZ
460 9131 (1) Poultry meat LYG
464 7473 (1) Farm XZ
10335 (1) Farm CZ
574 6922 (1) Poultry meat CZ
9617 (1) Farm XZ
9955 (7) Farm CZ
8880 (5) Farm (3)+Poultry meat (2) XZ (4)+SQ (1)
607 10474 (2) Poultry meat HA
692 699 (1) Poultry meat XZ
4334 (1) Poultry meat SQ
UA 4324 (5) Poultry meat CZ (3)+LYG (2)
10629 (1) Poultry meat NJ
11903 (1) Poultry meat HA
12629 (1) Farm LYG
14483 (2) Farm XZ (1)+SQ (1)
NEW1 (2) Farm CZ
NEW2 (1) Farm CZ
NEW3 (1) Poultry meat HA
NEW4 (1) Poultry meat HA
NEW5 (1) Poultry meat HA
NEW6 (5) Farm SQ
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“UA” means unassigned.

Table 4.

MLST typing results for C. coli.

CC ST (n) Source District
828 825 (3) Poultry meat XZ (1)+HA (2)
829 (3) Poultry meat XZ (1)+YC (1)+SQ (1)
830 (3) Poultry meat XZ (2)+HA (1)
860 (3) Farm (2)+ Poultry meat (1) CZ (2)+SQ (1)
872 (2) Farm (1)+ Poultry meat (1) XZ (1)+HA (1)
899 (2) Poultry meat HA (2)
902 (1) Poultry meat HA (1)
1145 (2) Poultry meat YZ (1)+HA (1)
3236(2) Poultry meat YZ (1)+HA (1)
3753 (2) Poultry meat LYG (1)+HA (1)
5191(1) Farm XZ
7304 (1) Poultry meat YC
10339 (6) Farm (1)+Poultry meat (5) XZ (1)+SQ (5)
10344 (4) Farm CZ
UA 11899 (3) Poultry meat YZ (1)+HA (2)
12337 (4) Farm (1)+Poultry meat (3) YC (1)+LYG (3)
NEW1 (1) Poultry meat CZ
NEW2 (1) Poultry meat HA
NEW3 (1) Poultry meat SQ
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“UA” means unassigned.

For phylogenetic analysis, MLST data of Campylobacter isolates was used for genetic relationship analysis. The core housekeeping gene sequences required for MLST were aligned and trimmed, and a phylogenetic tree was subsequently constructed to preliminarily analyze the genetic clustering and evolutionary relatedness of isolates. As shown in Fig. 2A, isolates from different districts and different poultry meat sources (CZCM54, XZCM16, HADM31, and HAGM29) clustered on the same branch, indicating close genetic relatedness and a possible common origin. Moreover, isolates from the same district but different farms (CZ1801-CZ1805, CZ1901, and CZ1902) appeared on the same branch and had the same ST type. Notably, C. coli isolates from different districts or sources also tended to cluster with one another (Fig. 2B). Similar to some C. jejuni isolates, C. coli isolates from different districts and different poultry meat sources (SQBCM12, XZDM18, HACM46, and LYGGM18) clustered on the same branch. Three groups of strains from the same source but different districts were found on the same branch, and had the same ST type. These groups included 3 strains from pigeon meat (HAGM45, YZGM03, and HAGM43), 5 strains from chicken meat (XZBCM55, YCCM38, SQCM55, HACM42, and HACM20), and 10 strains from chicken meat (LYGCM11, YCCM44, LYGBCM25, HACM23, YZBCM37, HACM33, HACM41, HACM47, XZCM53, and XZCM51). Notably, MLST-based phylogenetic analysis could only provide preliminary genetic clustering information, which has limitations in resolving detailed clade classification.

Fig. 2.

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Phylogenetic tree based on seven housekeeping genes of Campylobacter from different sources and districts. (A) C. jejuni. (B) C. coli. Visualized in the interactive Tree Of Life tool.

Prevalence of virulence and resistance genes

In total, 10 virulence genes classified into five functional categories-adherence, invasion, immune modulation, motility, and toxin production were identified in 128 Campylobacter isolates (Fig. 3). The flagellar gene flhA and the toxin gene cdtB, had the highest prevalence (100 % for both), followed by the adherence factor gene cadF (96.1 %) and another flagellar gene, flaA (93.8 %). Detection rates for the virulence genes virB11, iam, cdtA, and cdtC ranged from 32.8 % to 64.8 %. The invasion-related gene ciaB was present in 11.7 % of isolates. The wlaN gene, which is associated with Guillain–Barré syndrome after Campylobacter infection, was detected in 7 (5.5 %) C. jejuni isolates. In contrast, wlaN was absent from all C. coli isolates.

Fig. 3.

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Prevalence of virulence genes for Campylobacter jejuni and Campylobacter coli.

The amplified resistance genes are presented in Fig. 4. This study examined the prevalence of the resistance-enhancing variant RE-CmeABC, which has high activity against multiple antibiotics, as well as other resistance genes associated with drugs commonly used in clinical treatment of bacterial infections. Overall, 32.8 % of isolates were positive for the RE-CmeABC variant, primarily among C. jejuni isolates (60.3 %). The carriage rate of the tetracycline resistance gene tet(O) was 31.3 %, and the aminoglycoside resistance gene cluster aadE-sat4-aphA-3 was detected in 21.9 % of isolates. The erythromycin resistance gene erm(B) was detected in 9.4 % of all tested isolates.

Fig. 4.

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Prevalence of antimicrobial resistance genes for Campylobacter jejuni and Campylobacter coli.

Biofilm formation in Campylobacter

Among the 38 strains selected for biofilm formation testing, 6 C. coli strains (LYGBCM25, LYGCM11, HACM36, XZDM18, CZ1501, and XZCM51) exhibited biofilm-forming behavior that differed significantly from that of the other Campylobacter strains. Fig. 5A shows a side view of the biofilm formed by Campylobacter. Campylobacter is motile, and the observed biofilm formed at the air-liquid interface. Motile microbes typically adhere to the walls of the well.

Fig. 5.

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A representative result for biofilm formation assays performed for Campylobacter. (A) Before elution. (B) After elution.

As shown in Fig. 6, the strains LYGCM11 and XZDM18 had the highest mean OD values (0.349 and 0.421, respectively). Another 4 strains (LYGBCM25, HACM36, CZ1501, and XZCM51) had OD values between 0.159 and 0.231, which were also significantly different (P < 0.05) from the OD values obtained for the other strains in the biofilm formation assay.

Fig. 6.

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Biofilm formation by Campylobacter strains.

Discussion

Poultry is a major source of Campylobacter contamination in the human food chain. During poultry farming, birds infected with Campylobacter may show no clinical symptoms but can continuously shed the bacteria into the environment and carry the organism throughout life. One study reported that poultry remains the primary reservoir for C. jejuni in China, with chickens and chicken meat being the most severely contaminated sources, although other poultry sources, such as ducks and geese, should not be overlooked (Li et al., 2025). China has high poultry meat consumption. A meta-analysis of major foodborne pathogens in Chinese food commodities found that Campylobacter was the second most prevalent pathogen, with an overall average prevalence of 10.8 % between 2006 and 2016 (Paudyal et al., 2018). Surveillance studies in 2021 of diarrheal pathogens from patients across Huzhou local region of China found that Campylobacter had become the most frequently identified pathogen, ahead of Salmonella, Vibrio parahaemolyticus, and diarrheagenic Escherichia coli (Wu et al., 2024, 2021). Infections caused by antimicrobial-resistant Campylobacter strains pose a serious threat to successful treatment in humans. Because the antibiotic resistance and virulence status of Campylobacter isolates can vary by antibiotic use pattern, investigation period, and region, it is necessary to assess the antibiotic-resistance and virulence profiles of Campylobacter isolated from poultry sources. In this study, we focused on antimicrobial resistance, genetic diversity, and biofilm formation in Campylobacter from chicken farms and retail poultry meat and analyzed their potential risks to human health.

The observed high AMR, particularly 46.6 % MDR among 128 Campylobacter isolates-with C. coli exhibiting significantly higher resistance (75.4 %) than C. jejuni-likely reflects excessive antibiotic use in poultry farming (Bai et al., 2024; Bort et al., 2022; Dramé et al., 2020; Huong et al., 2024). MDR Campylobacter in the livestock production chain poses a food safety risk, as contaminated meat can enter the food chain and cause human infections (Varga, 2026; Bundurus et al., 2023; Mohan et al., 2025). Given that C. coli can horizontally transfer resistance genes, the identification of 14 isolates resistant to eight antibiotics underscores the urgent need for enhanced AMR surveillance (Zhang et al., 2021).

The RE-CmeABC variant, a globally recognized determinant of multidrug resistance in Campylobacter jejuni since 2014, was detected in 60.3 % of our C. jejuni isolates, consistent with a recent systematic review in China (Li et al., 2025). This high carriage rate is of particular concern, as RE-CmeABC confers resistance to multiple clinically important drug classes, including macrolides, fluoroquinolones, and β-lactams, which are mainstays of Campylobacter infection treatment (Dai et al., 2024; Yao et al., 2016). The aminoglycoside resistance gene cluster aadE-sat4-aphA-3 was present in 21.9 % of isolates, and among these, 70.6 % were phenotypically resistant to gentamicin, aligning with our previous observations (Zhang et al., 2021). Furthermore, all 12 erm(B)-positive C. coli strains in this study were resistant to erythromycin, providing direct genotypic evidence for the established role of erm(B) in macrolide resistance (Chang et al., 2017; Jehanne et al., 2021; Qin et al., 2014). These findings collectively demonstrate a correlation between the presence of specific resistance determinants and phenotypic resistance profiles, underscoring the utility of genotypic surveillance for predicting clinical resistance patterns in Campylobacter.

Expression of virulence genes plays a key role in Campylobacter colonization and pathogenicity. The detection of 10 virulence genes across five functional classes in all 128 isolates provides important insights into their pathogenic potential. Notably, cdtB and flhA were present in all strains (100 %), highlighting their essential roles in toxin production and motility. Similarly, high prevalence of cadF (96.1 %) and flaA (93.8 %) supports the importance of adherence and motility, consistent with broiler farm and chicken meat studies (Abu-Madi et al., 2016; Yang et al., 2023). The low prevalence (5.5 %) of wlaN in C. jejuni isolates is comparable to that in a study of Brazilian broiler isolates, in which wlaN was detected in 10.7 % of C. jejuni strains (Sierra-Arguello et al., 2021). Although only 5 wlaN-positive strains from chicken meat pose a risk of post-infection GBS, the potential risk to human health should not be ignored.

MLST analysis revealed high genetic diversity among poultry-derived Campylobacter isolates in this study, with novel STs identified in both C. jejuni and C. coli, indicative of ongoing bacterial genetic variation and adaptive evolution under poultry farming selective pressure (Sheppard and Maiden, 2015; Joseph et al., 2020). The dominant clonal complexes identified in C. jejuni (CC-574, CC-354) and C. coli (CC-828) are globally prevalent poultry- and human-associated lineages, confirming the zoonotic potential of chicken-borne Campylobacter in the investigated region (Kim et al., 2024; Yang et al., 2025). CC-21 was also detected in this study; although it was not the dominant CC, its presence indicates potential risks to human health (Zhang et al., 2020). Furthermore, the emergence of STs shared across multiple districts (68.8 % of C. coli STs detected in two or more districts) suggest ongoing potential regional transmission along poultry supply chains, underscoring retail chicken meat as a reservoir of genetically diverse Campylobacter of public health concern.

A notable finding was that C. jejuni isolates from different districts and different types of poultry meat (CZCM54, XZCM16, HADM31, and HAGM29) clustered on the same branch, suggesting close genetic relatedness and a common origin among these isolates. This pattern suggests that cross-regional circulation of these isolates may be related to long-distance transport of poultry products or dissemination of contaminated breeding materials, which could promote the spread of the same Campylobacter lineage across different geographic regions and poultry species. Notably, C. coli isolates from different districts or sources tended to cluster in the same clades, consistent with a previous report (Li et al., 2023). This pattern may be related to the strong adaptability of C. coli to different hosts and environments and to the extensive circulation of contaminated poultry products in the market.

Campylobacter species are known to form biofilms. Biofilm establishment and growth are important factors in the survival and spread of Campylobacter. During the production, processing, and transportation of poultry products, biofilm-derived Campylobacter can withstand routine cleaning and disinfection measures, leading to continuous food contamination and increasing the likelihood of human exposure to the pathogen through the food chain. In this study, 6 of the 38 tested Campylobacter strains exhibited distinct biofilm-forming behavior. These strains may readily adhere to the surfaces of food-processing equipment, poultry meat, and packaging materials, forming persistent biofilm contamination, and posing a higher risk to human health. Some of these biofilm-forming C. coli strains (LYGBCM25, LYGCM11, XZDM18, and XZCM51) were previously identified in the phylogenetic analysis as cross-regional isolates clustered with strains from different districts and poultry meat sources. This overlap suggests that high-risk biofilm-forming C. coli strains have the potential for cross-regional dissemination through poultry products, expanding the scope of human exposure risk.

Conclusions

In conclusion, this study characterized Campylobacter isolates from chicken farms and retail poultry meat and confirmed their potential public health risks. The extensive genetic diversity of the tested isolates, including dominant clonal complexes (CC-574 for C. jejuni and CC-828 for C. coli) and novel sequence types, may enhance their adaptability and transmission potential. A critical public health concern is the high multidrug-resistant (MDR) rate (46.6 %) among isolates, with C. coli showing a substantially higher MDR proportion (75.4 %) and broader antibiotic resistance than C. jejuni (17.5 %). Key resistance genes and 10 virulence genes were detected. Notably, detection of the wlaN gene (linked to Guillain–Barré syndrome) in 5.5 % of C. jejuni isolates indicates a severe, long-term neurological risk beyond acute gastrointestinal symptoms. Additionally, six C. coli isolates exhibited strong biofilm-forming capacity, which may facilitate their survival in the poultry production and retail chain and further increase the likelihood of human exposure through contaminated poultry products. Collectively, these findings indicate that Campylobacter from local poultry sources is a significant public health threat and highlight the urgent need for targeted control strategies in the poultry industry to reduce transmission and protect public health.

Author contribution

X. Z. participated in the study design, carried out all data analysis, and prepared the manuscript. Y. G. supervised and assisted in the manuscript preparation. X. G., M. T. and Q. Z. provided data and revised the manuscript. J. L., X. T., and D. C., participated in the study design and provided data. W. C. conceived the study and revised the manuscript. All authors contributed to the article and approved the submitted version.

Disclosures

The authors declare that they have no conflict of interest. All authors have read and agreed to the published version of the manuscript.

Acknowledgements

This work was supported by National Natural Science Foundation of China grant (32473117) and Yangzhou social development project (grant numbers YZ2025074).

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.psj.2026.107483.

Contributor Information

Xiaoyan Zhang, Email: xiaoyanpanda@163.com.

Yushi Gao, Email: 38625296@qq.com.

Appendix. Supplementary materials

mmc1.docx (12.2KB, docx)

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