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Rezaeian M, Hoveida L. Prevalence of carbapenem resistance genes in Enterobacteriaceae, Pseudomonas aeruginosa, and Acinetobacter baumannii from meat samples. mljgoums 2025; 19 (1) :36-41
URL: http://mlj.goums.ac.ir/article-1-1867-en.html
URL: http://mlj.goums.ac.ir/article-1-1867-en.html
1- Department of Microbiology, Fal.C., Islamic Azad University, Isfahan, Iran
2- Department of Microbiology, Fal.C., Islamic Azad University, Isfahan, Iran ,La.hoveida@iau.ac.ir
2- Department of Microbiology, Fal.C., Islamic Azad University, Isfahan, Iran ,
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Results
Studied population and bacterial isolates
Among 100 cultured samples, 70 were positive for bacterial infections. Following standard bacteriological tests, 30 isolates were identified as E. coli, 14 isolates as K. pneumoniae, 9 isolates as S. typhimurium, 11 as P. aeruginosa, and 6 isolates were identified as A. baumannii.
Antibiotic susceptibility test
The highest rates of antibiotic resistance were found in E. coli against tetracycline (100%) and streptomycin (93.33%), while K. pneumoniae also showed 100% resistance to tetracycline. S. typhimurium was resistant to tetracycline (100%) and trimethoprim (88.88%). P. aeruginosa exhibited 100% resistance to tetracycline, and A. baumannii showed complete resistance (100%) to meropenem and imipenem. Notably, P. aeruginosa showed the highest resistance to imipenem (Table 2, Figure 1).
Discussion
The emergence and spread of antibiotic resistance among bacterial pathogens pose significant challenges to public health worldwide. The increasing prevalence of carbapenem resistance genes in various bacterial species has raised concerns about the potential transmission of these resistance genes through the food chain (6,7). The expression of carbapenemase genes, which facilitates bacterial survival against carbapenems, raises concerns about the effectiveness of current treatment protocols and the need for novel therapeutic strategies. Strengthening surveillance and implementing targeted infection control measures are essential to mitigate the impact of these resistant strains on public health (27,28). In the current study, we investigated the frequency of carbapenem resistance genes in Enterobacteriaceae, P. aeruginosa, and A. baumannii isolated from meat. Among Enterobacteria, 42.8% of isolates were E. coli, 20% were K. pneumoniae, and 12.9% were S. typhimurium. The frequency of P. aeruginosa was 15.7%, and for A. baumannii was 8.6%.
Similarly, Dehkordi et al. reported a prevalence of 45.2% for E. coli isolated from raw chicken meat in Iran (29). Nazari Moghadam et al. demonstrated that 2% of chicken meat samples were positive for Salmonella, and all were S. typhimurium (30). It indicates that most antibiotics commonly utilized in the livestock and poultry industries are ineffective against a significant isolate of Salmonella, underscoring their importance in public health considerations. In a study by Mousse et al., about 20% of bacteria isolated from the food were K. pneumoniae (31). Atabay et al. observed that among 484 isolates, 78.92% were E. coli, followed by 7.64% Salmonella, 3.71% Proteus, 3.51% S. aureus, 1.85% Streptococcus, 1.44% P. aeruginosa, 1.23% Klebsiella, and 1.03% S. epidermidis (32). Rafei et al. reported different prevalences of A. baumannii isolated from meat, raw milk, drinking water, cheese, and domestic animal samples, respectively (33).
We observed that about 70% of selected samples contained Gram-negative bacteria from raw chicken meat with high antibiotic resistance to various antibiotics, including tetracycline, cotrimoxazole, gentamicin, trimethoprim, and streptomycin. This high contamination rate likely results from the overuse of antibiotics in poultry farming, where these substances are routinely prescribed to control and prevent bacterial infections, treat diseases, and promote growth (1,34). Such practices not only contribute to the development of resistant bacterial strains but also pose significant public health risks as these resistant pathogens can be transmitted to humans through the food chain. Moreover, the widespread resistance observed may compromise the effectiveness of treatment options for bacterial infections in humans, necessitating urgent interventions to regulate antibiotic use in livestock and improve food safety standards (35).
Rezaloo et al. found that 9.16% of meat samples were P. aeruginosa. These isolates exhibited pronounced antibiotic resistance, particularly to ampicillin, penicillin, and tetracycline, and the lowest resistance was reported to imipenem and trimethoprim (36). Studies reported that K. pneumoniae and E. coli isolated from meat were more likely to be multidrug-resistant and resistant (37,38). K. pneumoniae isolated from meat was more resistant to tetracycline and gentamicin than those isolated from the gastrointestinal tract (37). Among detected E. coli, K. pneumoniae, S. typhimurium, and P. aeruginosa had the highest resistance to tetracycline. Yang et al. reported that among Salmonella isolated from meat, S. typhimurium isolates were more prevalent than others with the highest resistance to tetracycline (39). Consequently, the prescription of antibiotics and, inevitably, the emergence of antibiotic resistance in poultry farms, is exacerbated. The primary source of contamination in livestock and poultry stems from the transmission of antibiotic-resistant bacterial strains from humans to meat, leading to an escalation in the prevalence of strains isolated from livestock and poultry that are resistant to antibiotics used in human medicine (40,41).
Alhazmi et al.’s study on K. pneumoniae isolates showed a high frequency of blaOXA-48 and blaNDM carbapenemase genes. Among their isolates, only one isolate each harbored blaVIM and blaKPC genes, while no blaIMP-producing isolates were detected (42). In the current study, KPC was the most prevalent carbapenemase gene expression in K. pneumoniae, while OXA-48 had the lowest frequency. It should be considered that differences in geographical location and sample origin between studies may influence the variations of the genes. Bakhtiari et al. demonstrated that 24% of K. pneumoniae isolates were resistant to imipenem, 35.45% represented the blaKPC gene, and 16.36% expressed the blaVIM-1 gene (43). Amini et al. demonstrated that among K. pneumoniae isolates, expression of blaVIM and blaIMP were higher than other carbapenemase gene (44). Li et al. showed that among carbapenem-resistant A. baumannii, common carbapenemase-positive genes included blaOXA-51-like, blaOXA-23-like, blaNDM-1, and blaOXA-58 (45). The current study reported gene expressions of IMP, VIM, and OXA-48 genes in A. baumannii isolates. Another study by Ghaffoori Kanaan et al. demonstrated that the most common gene expression among carbapenem-resistant S. enteritidis isolates was blaIMP, blaOXA-48-like, and blaNDM. In contrast, the blaKPC and blaVIM genes were undetected (46). We detected S. typhimurium and E. coli from collected meat, with the highest frequency of NDM expression.
The differences observed in the levels of antibiotic resistance and the prevalence of specific genes across various studies are multifactorial. These include the indiscriminate use of antibiotics in different countries, variations in patterns of antibiotic administration, the emergence of novel resistance mechanisms, the site of infection acquisition, genetic variations among bacterial strains, and geographical conditions, among others (47,48). The emergence of antibiotic resistance poses a significant burden on healthcare systems globally, leading to substantial economic costs. Apart from inappropriate antibiotic usage, factors such as aggressive treatment approaches, immunocompromised patients, and non-compliance with hygiene protocols also contribute to the problem. In the agricultural sector, adherence to health regulations, proper animal nutrition, modern slaughtering practices, and maintaining the integrity of the cold chain during transportation play pivotal roles in infection control efforts.
This study has some limitations that should be acknowledged. First, the sample size was relatively small, which may affect the generalizability of our findings. Additionally, the geographical bias inherent in our sampling could limit the applicability of the results to broader contexts, as antibiotic resistance patterns may vary significantly across different regions due to variations in antibiotic usage and regulations. Finally, the potential for changes in resistance patterns over time, influenced by evolving antibiotic practices, cannot be ruled out. Future research with larger, more diverse samples is essential to provide a more comprehensive understanding of carbapenem resistance in these pathogens.
Conclusion
The current study underscored multifaceted factors influencing antibiotic resistance disparities among studies, including varied antibiotic usage patterns, emergence of resistance mechanisms, and genetic diversity among bacterial strains. Antibiotic resistance poses a substantial global healthcare burden, exacerbated by inappropriate usage and other factors like aggressive treatments and agricultural practices. Addressing these complexities is critical for effective infection control.
Acknowledgement
Not applicable.
Funding sources
None.
Ethical statement
The study was approved by the Ethics Committee of the Falavarjan Branch, Islamic Azad University, Isfahan, Iran (IR.IAU.FALA.REC.1400.033).
Conflicts of interest
The authors declare that they have no competing interests.
Author contributions
All authors made significant contributions to the work reported. MR and LH participated in the research design and writing the first draft; MR and LH performed the research and analysis tools; MR and LH participated in data analysis. All authors reviewed and confirmed the final manuscript.
Data availability statement
All data generated or analyzed during this study are included in this published article.
Full-Text: (26 Views)
Introduction
As the global population expands, ensuring food security becomes increasingly pressing. It is necessary to assess whether food production systems can meet this demand while maintaining high quality and adhering to safety protocols. Animal-derived food products, such as meat, are an important part of the human diet, yet their safety and sustainability are threatened by various factors (1,2). Foodborne infections caused by Gram-positive and Gram-negative bacteria are becoming more widespread, raising concerns about treatment efficacy (3). The prevalence of antibiotic resistance in the food chain poses a significant threat to human health, as antibiotic-resistant bacteria can enter the food supply through various pathways, including the use of antibiotics in livestock for growth promotion and disease prevention (4,5). Among the diverse array of resistance mechanisms, the rise of carbapenem resistance in clinically relevant pathogens represents a pressing concern due to the limited treatment options available (6,7). The mechanisms of antibiotic resistance -such as the acquisition of resistance genes and the production of carbapenemase enzymes that render carbapenems ineffective- highlight the complexity of this issue, as these enzymes can spread among bacterial species, complicating treatment options (8,9).
Carbapenems, including imipenem and meropenem, constitute crucial medications renowned for their extensive and enduring spectrum of activity in contrast to beta-lactamases (10). Enterobacteriaceae, P. aeruginosa, and A. baumannii are notable bacterial species known for acquiring and disseminating resistance genes, including those conferring resistance to carbapenems (8,11-14). The most important carbapenems are commonly categorized into three classes: Class A (KPC), Class B: encompassing metallo β-lactamases such as IMP, VIM, and NDM, and Class D: represented by oxacillinase, notably OXA-48, of which OXA-48 has been reported frequently worldwide for its role in the rapid spread of infection (15,16).
Meatborne diseases caused by bacterial infections are more common in children (17). Numerous bacterial pathogens, including P. aeruginosa, A. baumannii, Klebsiella pneumoniae (K. pneumoniae), E. coli, Salmonella, Listeria monocytogenes, Yersinia enterocolitica, toxin-producing species like Staphylococcus aureus (S. aureus), and Bacillus cereus, contribute to meatborne diseases either through animal infection or contamination during meat processing or handling (18-20). Consuming contaminated meat poses a risk of contracting various diseases, categorized into gastrointestinal and extra-gastrointestinal infections (21). In the current study, we investigated the frequency of carbapenem resistance genes in Enterobacteriaceae, P. aeruginosa, and A. baumannii isolated from raw chicken meat in Isfahan, Iran.
Methods
One hundred raw chicken meat samples were collected from various farms to represent different production settings and potential contamination levels. The samples were obtained using sterile swabs to prevent any external contamination during collection. Each sample was cultured on Eosin Methylene Blue (EMB) medium, adhering to standard microbiological protocols to promote the growth of Gram-negative bacteria. Following the initial confirmation of Gram-negative bacilli, positive lactose colonies were further cultured on a Triple Sugar Iron Agar medium specifically designed for the isolation of Enterobacteriaceae. For the identification of Pseudomonas species, suspicious colonies were cultured on Pseudomonas Cetrimide Agar (PCA), while colonies suspected to be A. baumannii were cultured on blood agar. Phenotypic and biochemical tests were applied to identify the isolates as follows: for Enterobacteriaceae, indole, methyl red, Voges Proskauer, and citrate tests were utilized to differentiate diagnosis between E. coli, S. typhimurium, and K. pneumoniae; P. aeruginosa isolated were confirmed through lactose, citrate, indole, oxidase, DNase, and hemolysis tests; and A. baumannii isolates were confirmed by lactose, oxidase, catalase, pigmentation, urease, and IMVIC tests.
The antibiotic susceptibility of all isolates was determined by the Kirby-Bauer method. Applied antibiotics included tetracycline, ceftazidime, ciprofloxacin, trimethoprim-sulfamethoxazole, tobramycin, chloramphenicol, norfloxacin, amikacin, gentamicin, rifampin, cephalothin, streptomycin, trimethoprim, levofloxacin, imipenem, meropenem, azithromycin (22).
DNA extraction was conducted from pure bacterial cultures (23) and was assessed using NanoDrop (24). Polymerase chain reaction (PCR) to detect OXA-181, OXA-48, VIM, NDM, IMP and KPC genes expression was performed through the following steps: for E. coli (1 for 5 min cycle at 94 °C for initial denaturation; 33 cycles included 60 sec at 94 °C for denaturation, 45 sec at 58 °C for annealing, and 60 sec at 72 °C for extension; and 1 cycle for 7 min at 72 °C for final extension), for K. pneumoniae (1 for 5 min cycle at 94 °C for initial denaturation; 35 cycles included 30 sec at 95 °C for denaturation, 90 sec at 58 °C for annealing, and 90 sec at 72 °C for extension; and 1 cycle for 10 min at 72 °C for final extension), for S. typhimurium (1 for 4 min cycle at 95 °C for initial denaturation; 30 cycles included 45 sec at 94 °C for denaturation, 60 sec at 58 °C for annealing, and 40 sec at 72 °C for extension; and 1 cycle for 5 min at 72 °C for final extension), for P. aeruginosa (1 for 5 min cycle at 94°C for initial denaturation; 25 cycles included 35 sec at 94 °C for denaturation, 45 sec at 53 °C for annealing, and 60 sec at 72 °C for extension; and 1 cycle for 7 min at 72 °C for final extension), for A. baumannii (1 for 3 min cycle at 94 °C for initial denaturation; 30 cycles included 40 sec at 95 °C for denaturation, 55 sec at 59 °C for annealing, and 60 sec at 72 °C for extension; and 1 cycle for 6 min at 72 °C for final extension). Multiplex PCR was performed to evaluate the expression of gene coding for resistance to carbapenem compounds in isolates. Utilized primers have been presented in Table 1 (25). The quality of the product was evaluated using gel electrophoresis (26).
Statistical analysis
Numbers and percentages reported the frequency of data. All data was analyzed using SPSS version 21.
As the global population expands, ensuring food security becomes increasingly pressing. It is necessary to assess whether food production systems can meet this demand while maintaining high quality and adhering to safety protocols. Animal-derived food products, such as meat, are an important part of the human diet, yet their safety and sustainability are threatened by various factors (1,2). Foodborne infections caused by Gram-positive and Gram-negative bacteria are becoming more widespread, raising concerns about treatment efficacy (3). The prevalence of antibiotic resistance in the food chain poses a significant threat to human health, as antibiotic-resistant bacteria can enter the food supply through various pathways, including the use of antibiotics in livestock for growth promotion and disease prevention (4,5). Among the diverse array of resistance mechanisms, the rise of carbapenem resistance in clinically relevant pathogens represents a pressing concern due to the limited treatment options available (6,7). The mechanisms of antibiotic resistance -such as the acquisition of resistance genes and the production of carbapenemase enzymes that render carbapenems ineffective- highlight the complexity of this issue, as these enzymes can spread among bacterial species, complicating treatment options (8,9).
Carbapenems, including imipenem and meropenem, constitute crucial medications renowned for their extensive and enduring spectrum of activity in contrast to beta-lactamases (10). Enterobacteriaceae, P. aeruginosa, and A. baumannii are notable bacterial species known for acquiring and disseminating resistance genes, including those conferring resistance to carbapenems (8,11-14). The most important carbapenems are commonly categorized into three classes: Class A (KPC), Class B: encompassing metallo β-lactamases such as IMP, VIM, and NDM, and Class D: represented by oxacillinase, notably OXA-48, of which OXA-48 has been reported frequently worldwide for its role in the rapid spread of infection (15,16).
Meatborne diseases caused by bacterial infections are more common in children (17). Numerous bacterial pathogens, including P. aeruginosa, A. baumannii, Klebsiella pneumoniae (K. pneumoniae), E. coli, Salmonella, Listeria monocytogenes, Yersinia enterocolitica, toxin-producing species like Staphylococcus aureus (S. aureus), and Bacillus cereus, contribute to meatborne diseases either through animal infection or contamination during meat processing or handling (18-20). Consuming contaminated meat poses a risk of contracting various diseases, categorized into gastrointestinal and extra-gastrointestinal infections (21). In the current study, we investigated the frequency of carbapenem resistance genes in Enterobacteriaceae, P. aeruginosa, and A. baumannii isolated from raw chicken meat in Isfahan, Iran.
Methods
One hundred raw chicken meat samples were collected from various farms to represent different production settings and potential contamination levels. The samples were obtained using sterile swabs to prevent any external contamination during collection. Each sample was cultured on Eosin Methylene Blue (EMB) medium, adhering to standard microbiological protocols to promote the growth of Gram-negative bacteria. Following the initial confirmation of Gram-negative bacilli, positive lactose colonies were further cultured on a Triple Sugar Iron Agar medium specifically designed for the isolation of Enterobacteriaceae. For the identification of Pseudomonas species, suspicious colonies were cultured on Pseudomonas Cetrimide Agar (PCA), while colonies suspected to be A. baumannii were cultured on blood agar. Phenotypic and biochemical tests were applied to identify the isolates as follows: for Enterobacteriaceae, indole, methyl red, Voges Proskauer, and citrate tests were utilized to differentiate diagnosis between E. coli, S. typhimurium, and K. pneumoniae; P. aeruginosa isolated were confirmed through lactose, citrate, indole, oxidase, DNase, and hemolysis tests; and A. baumannii isolates were confirmed by lactose, oxidase, catalase, pigmentation, urease, and IMVIC tests.
The antibiotic susceptibility of all isolates was determined by the Kirby-Bauer method. Applied antibiotics included tetracycline, ceftazidime, ciprofloxacin, trimethoprim-sulfamethoxazole, tobramycin, chloramphenicol, norfloxacin, amikacin, gentamicin, rifampin, cephalothin, streptomycin, trimethoprim, levofloxacin, imipenem, meropenem, azithromycin (22).
DNA extraction was conducted from pure bacterial cultures (23) and was assessed using NanoDrop (24). Polymerase chain reaction (PCR) to detect OXA-181, OXA-48, VIM, NDM, IMP and KPC genes expression was performed through the following steps: for E. coli (1 for 5 min cycle at 94 °C for initial denaturation; 33 cycles included 60 sec at 94 °C for denaturation, 45 sec at 58 °C for annealing, and 60 sec at 72 °C for extension; and 1 cycle for 7 min at 72 °C for final extension), for K. pneumoniae (1 for 5 min cycle at 94 °C for initial denaturation; 35 cycles included 30 sec at 95 °C for denaturation, 90 sec at 58 °C for annealing, and 90 sec at 72 °C for extension; and 1 cycle for 10 min at 72 °C for final extension), for S. typhimurium (1 for 4 min cycle at 95 °C for initial denaturation; 30 cycles included 45 sec at 94 °C for denaturation, 60 sec at 58 °C for annealing, and 40 sec at 72 °C for extension; and 1 cycle for 5 min at 72 °C for final extension), for P. aeruginosa (1 for 5 min cycle at 94°C for initial denaturation; 25 cycles included 35 sec at 94 °C for denaturation, 45 sec at 53 °C for annealing, and 60 sec at 72 °C for extension; and 1 cycle for 7 min at 72 °C for final extension), for A. baumannii (1 for 3 min cycle at 94 °C for initial denaturation; 30 cycles included 40 sec at 95 °C for denaturation, 55 sec at 59 °C for annealing, and 60 sec at 72 °C for extension; and 1 cycle for 6 min at 72 °C for final extension). Multiplex PCR was performed to evaluate the expression of gene coding for resistance to carbapenem compounds in isolates. Utilized primers have been presented in Table 1 (25). The quality of the product was evaluated using gel electrophoresis (26).
Statistical analysis
Numbers and percentages reported the frequency of data. All data was analyzed using SPSS version 21.
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Table 1. Forward and reverse primers
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Results
Studied population and bacterial isolates
Among 100 cultured samples, 70 were positive for bacterial infections. Following standard bacteriological tests, 30 isolates were identified as E. coli, 14 isolates as K. pneumoniae, 9 isolates as S. typhimurium, 11 as P. aeruginosa, and 6 isolates were identified as A. baumannii.
Antibiotic susceptibility test
The highest rates of antibiotic resistance were found in E. coli against tetracycline (100%) and streptomycin (93.33%), while K. pneumoniae also showed 100% resistance to tetracycline. S. typhimurium was resistant to tetracycline (100%) and trimethoprim (88.88%). P. aeruginosa exhibited 100% resistance to tetracycline, and A. baumannii showed complete resistance (100%) to meropenem and imipenem. Notably, P. aeruginosa showed the highest resistance to imipenem (Table 2, Figure 1).
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Table 2. Antibiotic susceptibility results
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Molecular detection of carbapenemase genes
The most frequently reported gene expression of E. coli, K. pneumoniae, and S. typhimurium was NDM (7.33%), KPC (71.43%), and NDM (66.67%), respectively, which were significantly higher than those of other genes (p <0.05). Among P. aeruginosa isolates, the frequency of VIM (100%) and IMP (90.91%) gene expression was significantly higher compared to others (p =0.018). In A. baumannii isolates, the gene expression of IMP, VIM, and OXA-48 was significantly higher than others (p =0.030). Notably, the presence of the NDM gene in S. typhimurium, which did not show carbapenem resistance, highlighted the complexity of antibiotic resistance gene distribution, suggesting that resistance genes should primarily be reported in the context of resistant strains to provide clearer implications for resistance mechanisms (Table 3, Figure 2).
The most frequently reported gene expression of E. coli, K. pneumoniae, and S. typhimurium was NDM (7.33%), KPC (71.43%), and NDM (66.67%), respectively, which were significantly higher than those of other genes (p <0.05). Among P. aeruginosa isolates, the frequency of VIM (100%) and IMP (90.91%) gene expression was significantly higher compared to others (p =0.018). In A. baumannii isolates, the gene expression of IMP, VIM, and OXA-48 was significantly higher than others (p =0.030). Notably, the presence of the NDM gene in S. typhimurium, which did not show carbapenem resistance, highlighted the complexity of antibiotic resistance gene distribution, suggesting that resistance genes should primarily be reported in the context of resistant strains to provide clearer implications for resistance mechanisms (Table 3, Figure 2).
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Discussion
The emergence and spread of antibiotic resistance among bacterial pathogens pose significant challenges to public health worldwide. The increasing prevalence of carbapenem resistance genes in various bacterial species has raised concerns about the potential transmission of these resistance genes through the food chain (6,7). The expression of carbapenemase genes, which facilitates bacterial survival against carbapenems, raises concerns about the effectiveness of current treatment protocols and the need for novel therapeutic strategies. Strengthening surveillance and implementing targeted infection control measures are essential to mitigate the impact of these resistant strains on public health (27,28). In the current study, we investigated the frequency of carbapenem resistance genes in Enterobacteriaceae, P. aeruginosa, and A. baumannii isolated from meat. Among Enterobacteria, 42.8% of isolates were E. coli, 20% were K. pneumoniae, and 12.9% were S. typhimurium. The frequency of P. aeruginosa was 15.7%, and for A. baumannii was 8.6%.
Similarly, Dehkordi et al. reported a prevalence of 45.2% for E. coli isolated from raw chicken meat in Iran (29). Nazari Moghadam et al. demonstrated that 2% of chicken meat samples were positive for Salmonella, and all were S. typhimurium (30). It indicates that most antibiotics commonly utilized in the livestock and poultry industries are ineffective against a significant isolate of Salmonella, underscoring their importance in public health considerations. In a study by Mousse et al., about 20% of bacteria isolated from the food were K. pneumoniae (31). Atabay et al. observed that among 484 isolates, 78.92% were E. coli, followed by 7.64% Salmonella, 3.71% Proteus, 3.51% S. aureus, 1.85% Streptococcus, 1.44% P. aeruginosa, 1.23% Klebsiella, and 1.03% S. epidermidis (32). Rafei et al. reported different prevalences of A. baumannii isolated from meat, raw milk, drinking water, cheese, and domestic animal samples, respectively (33).
We observed that about 70% of selected samples contained Gram-negative bacteria from raw chicken meat with high antibiotic resistance to various antibiotics, including tetracycline, cotrimoxazole, gentamicin, trimethoprim, and streptomycin. This high contamination rate likely results from the overuse of antibiotics in poultry farming, where these substances are routinely prescribed to control and prevent bacterial infections, treat diseases, and promote growth (1,34). Such practices not only contribute to the development of resistant bacterial strains but also pose significant public health risks as these resistant pathogens can be transmitted to humans through the food chain. Moreover, the widespread resistance observed may compromise the effectiveness of treatment options for bacterial infections in humans, necessitating urgent interventions to regulate antibiotic use in livestock and improve food safety standards (35).
Rezaloo et al. found that 9.16% of meat samples were P. aeruginosa. These isolates exhibited pronounced antibiotic resistance, particularly to ampicillin, penicillin, and tetracycline, and the lowest resistance was reported to imipenem and trimethoprim (36). Studies reported that K. pneumoniae and E. coli isolated from meat were more likely to be multidrug-resistant and resistant (37,38). K. pneumoniae isolated from meat was more resistant to tetracycline and gentamicin than those isolated from the gastrointestinal tract (37). Among detected E. coli, K. pneumoniae, S. typhimurium, and P. aeruginosa had the highest resistance to tetracycline. Yang et al. reported that among Salmonella isolated from meat, S. typhimurium isolates were more prevalent than others with the highest resistance to tetracycline (39). Consequently, the prescription of antibiotics and, inevitably, the emergence of antibiotic resistance in poultry farms, is exacerbated. The primary source of contamination in livestock and poultry stems from the transmission of antibiotic-resistant bacterial strains from humans to meat, leading to an escalation in the prevalence of strains isolated from livestock and poultry that are resistant to antibiotics used in human medicine (40,41).
Alhazmi et al.’s study on K. pneumoniae isolates showed a high frequency of blaOXA-48 and blaNDM carbapenemase genes. Among their isolates, only one isolate each harbored blaVIM and blaKPC genes, while no blaIMP-producing isolates were detected (42). In the current study, KPC was the most prevalent carbapenemase gene expression in K. pneumoniae, while OXA-48 had the lowest frequency. It should be considered that differences in geographical location and sample origin between studies may influence the variations of the genes. Bakhtiari et al. demonstrated that 24% of K. pneumoniae isolates were resistant to imipenem, 35.45% represented the blaKPC gene, and 16.36% expressed the blaVIM-1 gene (43). Amini et al. demonstrated that among K. pneumoniae isolates, expression of blaVIM and blaIMP were higher than other carbapenemase gene (44). Li et al. showed that among carbapenem-resistant A. baumannii, common carbapenemase-positive genes included blaOXA-51-like, blaOXA-23-like, blaNDM-1, and blaOXA-58 (45). The current study reported gene expressions of IMP, VIM, and OXA-48 genes in A. baumannii isolates. Another study by Ghaffoori Kanaan et al. demonstrated that the most common gene expression among carbapenem-resistant S. enteritidis isolates was blaIMP, blaOXA-48-like, and blaNDM. In contrast, the blaKPC and blaVIM genes were undetected (46). We detected S. typhimurium and E. coli from collected meat, with the highest frequency of NDM expression.
The differences observed in the levels of antibiotic resistance and the prevalence of specific genes across various studies are multifactorial. These include the indiscriminate use of antibiotics in different countries, variations in patterns of antibiotic administration, the emergence of novel resistance mechanisms, the site of infection acquisition, genetic variations among bacterial strains, and geographical conditions, among others (47,48). The emergence of antibiotic resistance poses a significant burden on healthcare systems globally, leading to substantial economic costs. Apart from inappropriate antibiotic usage, factors such as aggressive treatment approaches, immunocompromised patients, and non-compliance with hygiene protocols also contribute to the problem. In the agricultural sector, adherence to health regulations, proper animal nutrition, modern slaughtering practices, and maintaining the integrity of the cold chain during transportation play pivotal roles in infection control efforts.
This study has some limitations that should be acknowledged. First, the sample size was relatively small, which may affect the generalizability of our findings. Additionally, the geographical bias inherent in our sampling could limit the applicability of the results to broader contexts, as antibiotic resistance patterns may vary significantly across different regions due to variations in antibiotic usage and regulations. Finally, the potential for changes in resistance patterns over time, influenced by evolving antibiotic practices, cannot be ruled out. Future research with larger, more diverse samples is essential to provide a more comprehensive understanding of carbapenem resistance in these pathogens.
Conclusion
The current study underscored multifaceted factors influencing antibiotic resistance disparities among studies, including varied antibiotic usage patterns, emergence of resistance mechanisms, and genetic diversity among bacterial strains. Antibiotic resistance poses a substantial global healthcare burden, exacerbated by inappropriate usage and other factors like aggressive treatments and agricultural practices. Addressing these complexities is critical for effective infection control.
Acknowledgement
Not applicable.
Funding sources
None.
Ethical statement
The study was approved by the Ethics Committee of the Falavarjan Branch, Islamic Azad University, Isfahan, Iran (IR.IAU.FALA.REC.1400.033).
Conflicts of interest
The authors declare that they have no competing interests.
Author contributions
All authors made significant contributions to the work reported. MR and LH participated in the research design and writing the first draft; MR and LH performed the research and analysis tools; MR and LH participated in data analysis. All authors reviewed and confirmed the final manuscript.
Data availability statement
All data generated or analyzed during this study are included in this published article.
Research Article: Research Article |
Subject:
bacteriology
Received: 2024/09/10 | Accepted: 2024/12/29 | Published: 2025/02/22 | ePublished: 2025/02/22
Received: 2024/09/10 | Accepted: 2024/12/29 | Published: 2025/02/22 | ePublished: 2025/02/22
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