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ABSTRACT
In this study, a systematic review and meta‐analysis were conducted to consider antimicrobial resistance (AMR) rates of Campylobacter in Iran. A systematic search was conducted in the databases of PubMed, Scopus and Web of Science and reported according to the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses guidelines. Data analysis was done with R software. A number of 58 articles in the current study evaluated AMR in Campylobacter species in human, animal and food isolates. Our findings demonstrated that most of the Campylobacter spp. isolates in Iran have high resistance proportions to beta‐lactams (including cefixime (0.97), cephalothin (0.84), ceftriaxone (0.76), cephalexin (0.63), ceftazidime (0.53) and carbenicillin (0.38)), fluoroquinolones (including ofloxacin (0.79), nalidixic acid (0.51) and ciprofloxacin (0.52)), sulfonamides like trimethoprim‐sulfamethoxazole (0.68) (potentiated sulfonamides), florfenicol (0.62), tetracycline (0.57) and macrolides (including erythromycin (0.12) and azithromycin (0.17)). Conversely, Campylobacter spp. showed low resistance rates to aminoglycosides (including neomycin (0.08), amikacin (0.08), meropenem (0.06), spectinomycin (0.04), gentamicin (0.04) and imipenem (0.02)) and chloramphenicol (0.07). Regarding Campylobacter coli and Campylobacter jejuni isolates, resistance to erythromycin (0.18–0.09), and gentamycin (0.08–0.04) was higher in C. coli than C. jejuni isolates, respectively, whereas resistance to ciprofloxacin (0.56) and tetracycline (0.56) was higher in C. jejuni. The most prevalent antimicrobial resistance genes (ARGs) in Campylobacter spp. were tetO (0.73) and cmeB (0.48) and blaOXA61 (0.42). Therefore, the use of strict control systems and a restriction on the use of antibiotics in human, agricultural and animal farming are urgently required to reduce the development and spread of AMR.
- AMR
- antimicrobial resistance
- ARGs
- antimicrobial resistance genes
- AST
- antimicrobial susceptibility testing
- DD
- disk diffusion
- Fig
- figure
- MDR
- multidrug resistant
- MIC
- minimum inhibitory concentration
- PCR
- polymerase chain reaction
- PRISMA
- Preferred Reporting Items for Systematic Reviews and Meta-Analyses
- SID
- Scientific Information Database
Abbreviations
Introduction
Campylobacter genus are curved and S-shaped microaerophilic Gram-negative bacteria in the family Campylobacteraceae (Aminshahidi et al. 2017; Feizabadi et al. 2007; Rahimi et al. 2011). The Campylobacteraceae family comprises 18 species, 6 subspecies and 2 biovars. The most significant Campylobacter spp. attributed to human illness are thermophilic Campylobacters such as Campylobacter jejuni and Campylobacter coli (Hamidian et al. 2011; Rahimi et al. 2013a). More than 90% of the clinical cases are due to C. jejuni, whereas the incidence of C. coli is comparatively lesser (approximately 10%) (Azizian et al. 2019; Khoshbakht et al. 2016; Sharifi et al. 2021). The infective dose of this bacterium is exceptionally low; it has been assessed that 500 cells of C. jejuni can cause human disease (Ghane et al. 2011).
Campylobacter is a commensal of the intestinal tract of an extensive range of food animals, mammals and birds (Bakhshi et al. 2016). Poultry are considered to be the main potential reservoirs of these bacteria (Abbasi et al. 2019a; Khoshbakht et al. 2016; Maktabi et al. 2019). Utilization of contaminated water, unpasteurized milk, insufficiently cooked meat, cross-contamination of prepared foods and coordination of contact with animals are the most common causes of campylobacteriosis (Rahimi et al. 2013b; Samad et al. 2019). Large-scale epidemics of human campylobacteriosis are uncommon and are generally associated with the utilization of polluted water or raw milk. Campylobacteriosis is more frequently found in sporadic cases and due to consumption of undercooked chicken (Rahimi et al. 2017). They are one of the foremost common causes of acute diarrhoea, particularly in children under 3 years of age and older adults (Abbasi et al. 2019b). Campylobacter spp. strains are claimed to be the cause of 5.4%–10.8% of severe diarrhoea in Iran, which results in the death of 516 children under the age of 5 per year (Aminshahidi et al. 2017; Fani et al. 2019).
The clinical symptoms of campylobacteriosis range from asymptomatic and self-limiting gastroenteritis to severe inflammatory bloody diarrhoea, abdominal pain and fever (Hamidian et al. 2011). Furthermore, the acute phase of the disease can be attributed to other complications, such as meningitis, myocarditis attack, reactive arthritis, Guillain-Barre syndrome, Miller Fischer syndrome, inflammatory bowel syndrome and urinary tract infection (Fani et al. 2019; Maktabi et al. 2019; Sharifi et al. 2021). In immunocompromised patients, the elderly, infants and acute cases that require therapeutic interventions, macrolides (i.e., erythromycin and azithromycin) and fluoroquinolones (i.e., ciprofloxacin) are currently considered the preferred medications for treatment (Azizian et al. 2019; Fani et al. 2019; Khademi and Sahebkar 2020). Tetracyclines and gentamicin are alternative drugs (Khademi and Sahebkar 2020). Additionally, the incidence of human campylobacteriosis is on the rise globally due to the increase of antimicrobial resistance (AMR) in Campylobacter spp. (Jonaidi-Jafari et al. 2016; Rahimi et al. 2017). In 2019, an estimated 1.27 million deaths occurred worldwide that were directly attributed to antimicrobial-resistant bacteria. Multidrug-resistant (MDR) Campylobacter in livestock, broiler flocks, poultry and red meat (Abbasi et al. 2019b; Abdi-Hachesoo et al. 2014; Fani et al. 2019; Hamidian et al. 2011; Sharifi et al. 2021) has been reported to date in multiple Iranian studies. Antimicrobial-resistant microbial strains hold the potential to traverse the food chain, rendering them accessible to humans (Dallal et al. 2010; Fani et al. 2019; Maktabi et al. 2019; Ghane et al. 2011). Therefore, an improved understanding of the prevalence of the AMR in Campylobacter is a crucial step in creating efficient methods for reducing the occurrence and transmission of antimicrobial-resistant Campylobacter from food animal production and their immediate environment to humans.
Campylobacter is listed among the significant etiological agents associated with gastroenteritis in Iran (Rahimi et al. 2013b), but a comprehensive national report on the AMR patterns of Campylobacter spp. remains unavailable, primarily due to the absence of sustainable surveillance systems for foodborne zoonotic pathogens and their resistance to antimicrobials. To address this gap, the present systematic review and meta-analysis was undertaken to assess the prevalence of AMR in Campylobacter spp. isolated from humans, animals and food sources in Iran, as well as to examine the distribution of antibiotic resistance genes (ARGs) from an One Health perspective. Although this study shares certain thematic overlaps with the work of Khademi and Sahebkar (2020), it incorporates a broader range of investigations and thus provides a more extensive evidence base. The findings of this review are expected to generate critical data that can inform optimal antimicrobial therapy for infections caused by Campylobacter spp. Furthermore, the results will be instrumental in shaping national strategies for the prevention and control of Campylobacter infections, whereas simultaneously highlighting key research gaps that warrant future exploration.
Methods and Materials
Search Strategy
This study was performed as a systematic review of Campylobacter prevalence in Iran (Ansarifar et al. 2023). To identify the qualified investigations, scientific digital databases such as PubMed, Web of Science, Scopus, Google Scholar and Scientific Information Database (SID) were searched with the following keywords: C. coli or C. jejuni combined with the following terms: ‘Food’, ‘Animal’, ‘Chicken’, ‘Poultry’, ‘Meat’, ‘Beef’, ‘Lamb’, ‘Fish’, ‘Milk’, ‘Dairy’, ‘Egg’, ‘Sheep’, ‘Goat’, ‘Avian’, ‘Cow’, ‘Cattle’, ‘Human’, ‘Faeces’, ‘Diarrhoea’, ‘Gastroenteritis’ and ‘Iran’ and reported according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.
Criteria for Inclusion and Exclusion
The consideration standards included published or in-press original articles with a cross-sectional design that reported AMR in Campylobacter isolates and studies with a characterized test size. There was no restriction on the antimicrobial susceptibility testing (AST) method. To select eligible articles, the titles and abstracts of the acquired articles were reviewed. In some circumstances full texts were evaluated. The exclusion criteria were as follows: (1) duplicate articles from different databases, (2) articles that did not follow culture or molecular methods for Campylobacter isolation, (3) articles with unclear or incomprehensible text and analysis that did not show the accurate results of AMR in Campylobacter, (4) articles that did not report the specific sample size and number/percent of Campylobacter, (5) positive sample reviews; letters or editorial articles without original data and (6) articles did not report the AMR of Campylobacter spp.
Data Extraction
Data extraction was carried out in Microsoft Excel. Articles that met 6 of 10 criteria of the Joanna Briggs checklist (Munn et al. 2014) (i.e., 60% of the quality score) were included in the analysis. The following information was obtained: author's name, publication year, study year, study design, number of isolates and AMR of Campylobacter spp., C. jejuni, C. coli and AST method.
Risk of Bias Assessment
The quality evaluation of the eligible articles was performed in accordance with the risk of bias assessment table of the Joanna Briggs Institute (Munn et al. 2014).
Statistical Analysis
The analysis of the data was carried out using R 4.2 software with metafor packages to determine the pooled prevalence and 95% confidence interval of antibiotic resistance of Campylobacter species by random effects model. Statistical heterogeneity among studies was evaluated by computing I2, Cochran's Q. 25%, 50% and 75% of I2 values were classified as low, medium and high heterogeneity, respectively.
Results
A total number of 627 articles were searched and screened. A number of 58 articles in the current study from 2004 to 2025 evaluated AMR in Campylobacter species, including C. jejuni and C. coli. Reviews, case reports, abstracts, confused text/incomprehensible, duplicates and non-available full-text articles were excluded. All the studies that isolated Campylobacter from human, animals or foods and reported their AMR to some antibiotics were included. Most of the articles investigated AMR through the disk diffusion (DD) method. AMR data that were reported in two studies just one time extracted and inserted in the meta-analysis. Figure 1 shows the searched diagram of articles. Table 1 shows the characteristics of the included studies. A list of excluded articles can be available upon request.
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TABLE 1 Characteristics of the included studies.
| Reference | Study year | Sample source | Sample type | Campylobacter species (isolates number) | Antibiotics tested | Method | Quality assessment | |
| 1 | Abbasi et al. (2019a) | 2015 | Human | Diarrhoea | Campylobacter coli (5) | Ampicillin, ciprofloxacin, erythromycin, gentamicin, tetracycline | Disk diffusion test (DD) | 10 |
| 2 | Abbasi et al. (2019b) | 2015 | Human | Diarrhoea | Campylobacter jejuni (76) | Ampicillin, ciprofloxacin, erythromycin, gentamicin, tetracycline | DD, minimum inhibitory concentration (MIC) by antibiotic gradient testing, polymerase chain reaction (PCR) | 10 |
| 3 | Abdi-Hachesoo et al. (2014) | 2009 | Food | White meat | Campylobacter jejuni (43) and coli (40) | Tetracycline | PCR | 10 |
| 4 | Ahmadi et al. (2023) | 2022 | Food | Milk | Campylobacter jejuni (6) and coli (10) | Amoxicillin/Clavulanic acid, azithromycin, ceftriaxone, chloramphenicol doxycycline, erythromycin, nalidixic acid, tetracycline | DD | 10 |
| 5 | Aminshahidi et al. (2017) | 2014–2015 | Human | Diarrhoea | Campylobacter jejuni (7) | Ampicillin, azithromycin, ciprofloxacin, gentamicin, meropenem, nalidixic acid, tetracycline | DD | 9 |
| 6 | Ashrafganjooyi and Saeid-Adeli (2016) | 2008–2010 | Animal (poultry) | Cecal content | Campylobacter jejuni (190) | Ampicillin, tetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 7 | Azizian et al. (2019) | 2015–2016 | Animal (poultry) | Cecal content | Campylobacter jejuni (50) and coli (8) | Amoxicillin, ampicillin, ciprofloxacin, erythromycin, gentamicin, tetracycline, meropenem | DD and agar dilution method | 10 |
| 8 | Basiri et al. (2016) | 2014–2015 | Animal (poultry) | Faeces | Campylobacter jejuni (78) and coli (20) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, neomycin, spectinomycin, streptomycin, tetracycline | DD | 10 |
| 9 | Bakhshi et al. (2016) | 2012 | Food | White meat | Campylobacter coli (39) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 10 | Basirisaehi et al. (2007) | 2006 | Animal (cows, horse, poultry) | Faeces | Campylobacter jejuni (15), coli (10) and lari (12) | Ampicillin, cefotaxime, cephalexin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, tetracycline, trimethoprim-sulfamethoxazole | DD, E-test | 8 |
| 11 | Dabiri et al. (2016) | 2011–2012 | Food | Red and white meat | Campylobacter jejuni (93) and coli (28) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, colistin, erythromycin, gentamicin, nalidixic acid, neomycin, spectinomycin, streptomycin, tetracycline | DD | 10 |
| 12 | Emami et al. (2023) | Food | Mushrooms | Campylobacter jejuni (32) and coli (11) | Amoxicillin + clavulanic acid, ampicillin azithromycin, chloramphenicol, ciprofloxacin, clindamycin, erythromycine, gentamicin, nalidixic acid, tetracycline | DD | 10 | |
| 13 | Fani et al. (2019) | 2016 | Food | White meat | Campylobacter jejuni (24) and coli (2) | Amikacin, ampicillin, azithromycin, cefepime, cefixime, ceftriaxone, cefuroxime, cephalotin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, meropenem, nalidixic acid, tetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 14 | Feizabadi et al. (2007) | 2004–2005 | Human | Diarrhoea | Campylobacter jejuni (29) and coli (5) | Ampicillin, carbenicillin, cefotaxime, ceftazidime, cephalexin, cephalotin, chloramphenicol, ciprofloxacin, colistin, erythromycin, gentamicin, imipenem, nalidixic acid, neomycin, ofloxacin, streptomycin, tetracycline | DD | 10 |
| 15 | Ghane et al. (2011) | 2010 | Animal (poultry and cattle) | Faeces | Campylobacter jejuni (27), coli (18) and lari (20) | Ampicillin, cefotaxime, cephalexin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, tetracycline | DD, E-test | 9 |
| 16 | Ghane et al. (2010) | 2010 | Animal (cow, horse, sheep, poultry), environment (sewage, and river) | Faeces | Campylobacter jejuni (16), coli (9) and lari (7) | Amikacin, amoxicillin, amoxicillin/clavulanic acid, ampicillin, ceftriaxone, cephalexin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, penicillin, tetracycline, tobramycin, vancomycin | DD, MIC | 10 |
| 17 | Ghorbanalizadgan et al. (2019) | 2018 | Human | Diarrhoea | Campylobacter jejuni (31) and coli (2) | Ampicillin, chloramphenicol, ciprofloxacin, colistin, erythromycin, gentamicin, nalidixic acid, tetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 18 | Gilani et al. (2023) | 2021–2022 | Animal | Faeces | Campylobacter jejuni (3) and coli (19) | Amoxicillin–clavulanic acid, ampicillin, ciprofloxacin, erythromycin, gentamicin, nalidixic acid, tetracycline | DD | 10 |
| 19 | Hadiyan, Momtaz and Shakerian (2022) | 2022 | Food | White meat | Campylobacter jejuni (54) and coli (26) | Amoxicillin, ampicillin, azithromycin, chloramphenicol, ciprofloxacin, clindamycin erythromycin, gentamicin, nalidixic acid, tetracycline | DD | 10 |
| 20 | Hamidian et al. (2011) | 2008–2009 | Human | Diarrhoea | Campylobacter jejuni (34) and coli (12) | Ampicillin, carbenicillin, cefotaxime, ceftazidime, chloramphenicol, ciprofloxacin, colistin, erythromycin, gentamicin, imipenem, nalidixic acid, neomycin, ofloxacin, streptomycin, tetracycline | DD | 9 |
| 21 | Irajian et al. (2008) | 2007 | Human | Diarrhoea | Campylobacter jejuni (38) | Ciprofloxacin, erythromycin, gentamicin, tetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 22 | Jamali et al. (2015) | 2008–2010 | Animal (poultry) | Cecal content | Campylobacter jejuni (138) and coli (23) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, colistin, erythromycin, gentamicin, nalidixic acid, neomycin, streptomycin, tetracycline | DD | 10 |
| 23 | Jazayeri Moghadas et al. (2008) | 2007 | Human | Diarrhoea | Campylobacter jejuni (27) | Ciprofloxacin, erythromycin, gentamicin, trimethoprim-sulfamethoxazole, tetracycline | DD | 10 |
| 24 | Jonaidi-Jafari et al. (2016) | 2014–2015 | Food | Eggshell and egg content | Campylobacter jejuni (28) and coli (6) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 25 | Khoshbakht et al. (2016) | 2011–2013 | Animal (cattle, sheep) | Faeces | Campylobacter jejuni (48) and coli (17) | Ampicillin, cefotaxime, cephalotin, chloramphenicol, ciprofloxacin, colistin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, neomycin, tetracycline, tylosin | DD | 10 |
| 26 | Khosravi et al. (2011) | 2007–2008 | Human | Diarrhoea | Campylobacter jejuni (9) and coli (5) | Ampicillin, cefotaxime, ceftazidime, cephalothin, ciprofloxacin, erythromycin, gentamycin, nalidixic acid, oxacillin, tetracycline, trimethoprim-sulfamethoxazole | DD, E-test | 10 |
| 27 | Maktabi et al. (2019) | 2016 | Food | Red and white meat | Campylobacter jejuni (26) and coli (6) | Ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, streptomycin, tetracycline | DD | 10 |
| 28 | Mirzaie et al. (2011) | 2010 | Animal (poultry) | Cecal content | Campylobacter jejuni (33) and coli (19) | Ampicillin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, neomycin, nalidixic acid, tetracycline | DD | 10 |
| 29 | Moradi and Baserisalehi (2022) | 2022 | Animal (poultry, cow) | Faeces | Campylobacter jejuni (9) and coli (1) | Ampicillin, cefotaxime, ceftriaxone, ciprofloxacin, erythromycin, gentamicin | DD | 10 |
| 30 | Mostafavi and Neyriz-Naghadehi (2023) | 2018 | Food | Milk | Campylobacter jejuni (11) and coli (2) | Ampicillin, ceftriaxone, chloramphenicol, ciprofloxacin, gentamicin, nitrofurantoin, tetracycline, trimethoprim-sulphamethoxazole | DD | 10 |
| 31 | Mousavinafchi et al. (2023) | 2020 | Food | White meat | Campylobacter jejuni (41) and coli (14) | Ciprofloxacin, erythromycin, gentamicin, nalidixic acid, tetracycline | MIC | 10 |
| 32 | Raeisi et al. (2017) | 2014–2015 | Food | Raw milk, white meat, red meat | Campylobacter jejuni (79) and coli (41) | Amikacin, amoxicillin, ampicillin, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 33 | Rahimi et al. (2010a) | 2008–2009 | Food | Red meat | Campylobacter jejuni (42) and coli (8) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 34 | Rahimi et al. (2010b) | 2007–2008 | Food | Poultry carcass | Campylobacter jejuni (177) and coli (21) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 35 | Rahimi and Ameri (2011) | 2009–2010 | Food | White meat | Campylobacter jejuni (172) and coli (15) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 36 | Rahimi et al. (2011) | 2009–2010 | Food | White meat | Campylobacter jejuni (46) and coli (6) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 37 | Rahimi et al. (2013a) | 2009–2010 | Food | Red meat | Campylobacter jejuni (24) and coli (7) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 38 | Rahimi et al. (2013b) | 2011 | Food | Red and white meat | Campylobacter jejuni (193) and coli (20) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 39 | Rahimi et al. (2017) | 2014–2015 | Animal (cattle, sheep, goat, camel) | Faeces | Campylobacter jejuni (22) and coli (6) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 40 | Rahimi et al. (2024) | 2020–2021 | Food | Red meat | Campylobacter jejuni (33) and coli (36) | Amoxicillin, ampicillin, azithromycin, chloramphenicol, ciprofloxacin, clindamycin erythromycin, gentamicin, nalidixic acid, tetracycline | DD | 10 |
| 41 | Rastyani et al. (2015) | 2013–2014 | Human | Diarrhoea | Campylobacter jejuni (6) and coli (3) | Amikacin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, meropenem, tetracycline | DD | 9 |
| 42 | Saadatmand et al. (2017) | 2016 | Food | Organ meat (poultry liver) | Campylobacter jejuni (53) and coli (19) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, colistin, erythromycin, gentamicin, streptomycin, tetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 43 | Sabzmeydani et al. (2020) | 2018–2019 | Food | Poultry eggshell | Campylobacter jejuni (45) and coli (39) | Amoxicillin, ampicillin, cephalothin, chloramphenicol, ciprofloxacin, colistin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, neomycin, streptomycin, tetracycline | DD | |
| 44 | Sadeghi et al. (2020) | 2019–2020 | Human | Diarrhoea | Campylobacter spp. (1), jejuni (24), coli (2) and lari (1) | Ampicillin, ciprofloxacin, clindamycin, erythromycin, gentamicin, nalidixic acid, tetracycline | Agar diffusion test, DD, E-test, PCR | 10 |
| 45 | Sadeghi et al. (2022) | Food | White meat | Campylobacter spp. (9), jejuni (23), coli (1) and lari (2) | Ampicillin, ciprofloxacin, clindamycin, erythromycin, gentamicin, nalidixic acid, tetracycline | Agar diffusion test, DD, E-test, PCR | 10 | |
| 46 | Salehi et al. (2014) | 2011–2013 | Human | Diarrhoea | Campylobacter jejuni (19) | Cephalotin, erythromycin, nalidixic acid | DD | 10 |
| 47 | Shafiei et al. (2020) | 2018–2019 | Food and animal (cattle, sheep, goat) | Meat, liver, kidney, heart and contents of rectum | Campylobacter jejuni (69) and coli (45) | Amikacin, amoxicillin, ampicillin, cefazolin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, imipenem, meropenem, nalidixic acid, norfloxacin, streptomycin, tetracycline | DD | 9 |
| 48 | Shahrokhabad et al. (2011) | 2010 | Food | White meat and organ meat | Campylobacter jejuni (19) and coli (12) | Ciprofloxacin, erythromycin, gentamicin, nalidixic acid, trimethoprim-sulfamethoxazole | DD | 10 |
| 49 | Shakerian et al. (2012) | 2006–2008 | Food | Red meat | Campylobacter jejuni (13) and coli (4) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 50 | Shakerian (2016) | 2014 | Food | Vegetable (mushroom) | Campylobacter jejuni (2) and coli (13) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 51 | Sharifi et al. (2021) | 2019–2020 | Human | Diarrhoea | Campylobacter jejuni (18) and coli (2) | Chloramphenicol, ciprofloxacin, erythromycin, gentamicin, minocycline, nalidixic acid, tetracycline | DD, MIC by broth microdilution method, PCR (tet O, gyrA) | 10 |
| 52 | Shirazi et al. (2013) | 2011 | Human | Diarrhoea | Campylobacter jejuni (9) | Ciprofloxacin, erythromycin, gentamicin, tetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 53 | Dallal et al. (2010) | 2006–2007 | Food | Red and white meat | Campylobacter jejuni (70) and coli (22) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, colistin, erythromycin, gentamicin, nalidixic acid, neomycin, spectinomycin, streptomycin, tetracycline | DD | 10 |
| 54 | Taremi et al. (2006) | 2004 | Food | Red and white meat | Campylobacter spp. (80) | Amoxicillin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, tetracycline | DD | 10 |
| 55 | Zamani Moghaddam et al. (2012) | 2010–2011 | Environment—pigeon | Faeces | Campylobacter jejuni (1) | Ampicillin, ciprofloxacin, doxycycline, enrofloxacin, erythromycin, florfenicol, oxytetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 56 | Zamani Moghadam et al. (2013) | 2011 | Environment—lovebird | Faeces | Campylobacter spp. (2) | Ampicillin, ciprofloxacin, doxycycline, enrofloxacin, erythromycin, florfenicol, oxytetracycline, trimethoprim-sulfamethoxazole | DD | 10 |
| 57 | Zendehbad et al. (2013) | 2012 | Food | White meat | Campylobacter jejuni (122) and coli (27) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, colistin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, neomycin, spectinomycin, streptomycin, tetracycline | DD | 10 |
| 58 | Zendehbad et al. (2015) | 2013 | Food | White meat | Campylobacter jejuni (200) and coli (27) | Amoxicillin, ampicillin, chloramphenicol, ciprofloxacin, enrofloxacin, erythromycin, gentamicin, nalidixic acid, neomycin, tetracycline | DD | 10 |
Pooled Prevalence of AMR in Campylobacter spp
Table 2 shows the AMR proportions among Campylobacter spp. in human, food and animal subgroups. A total of 58 studies reported the antibiotic resistance in human (faeces), animal faeces and food, including meat, milk, eggs or vegetables. As displayed, the most frequent resistance among Campylobacter spp. was to cefixime (0.97), cephalothin (0.84), ofloxacin (0.79), ceftriaxone (0.76), trimethoprim-sulfamethoxazole (0.68), cephalexin (0.63) and florfenicol (0.62). Resistance to tetracycline (0.57), doxycycline (0.54), ceftazidime (0.53), ciprofloxacin (0.52), nalidixic acid (0.51), amoxicillin–clavulanic acid (0.34), clindamycin (0.34), ampicillin (0.29), azithromycin (0.17) and erythromycin (0.12) was high. The lowest resistance frequency was detected for imipenem (0.02), spectinomycin (0.04), gentamicin (0.04), meropenem (0.06) and chloramphenicol (0.07). Campylobacter spp. isolates had different resistance proportions in different sectors (Table 2). In most of the investigated antibiotics (nine types), resistance was higher in human isolates than other ones. Food isolates had higher resistance to some antibiotics, including doxycycline, neomycin, imipenem, azithromycin, colistin, ciprofloxacin, trimethoprim-sulfamethoxazole and tetracycline.
TABLE 2 The subgroup analysis of antimicrobial resistance (AMR) rates among Campylobacter spp.
| World Health Organization's categorization of antibiotics (WHO 2024) | Antibiotic | Study number | Resistance proportions | Lower bound | Upper bound | I2 | Sample's type | No. study | Resistance proportions | Lower bound | Upper bound | I2 |
| Authorized for use in humans only | Carbenicillin | 2 | 0.38 | 0.28 | 0.49 | 0 | Human | 2 | 0.38 | 0.28 | 0.49 | 0 |
| Imipenem | 3 | 0.02 | 0.01 | 0.05 | 0 | Human | 2 | 0.01 | 0.00 | 0.08 | 0 | |
| Food | 1 | 0.02 | 0.00 | 0.07 | — | |||||||
| Meropenem | 6 | 0.06 | 0.01 | 0.25 | 76 | Animal | 1 | 0 | 0 | 0.05 | — | |
| Human | 3 | 0.11 | 0.01 | 0.68 | 82 | |||||||
| Food | 2 | 0.07 | 0.02 | 0.22 | 28 | |||||||
| Highest priority critically important antimicrobial | Cefixime | 2 | 0.97 | 0.82 | 1 | 0 | Animal | 1 | 1 | 0.69 | 1 | — |
| Food | 1 | 1 | 0.87 | 1 | — | |||||||
| Cefotaxime | 6 | 0.32 | 0.16 | 0.5 | 92 | Animal | 3 | 0.25 | 0.08 | 0.56 | 95 | |
| Human | 3 | 0.4 | 0.15 | 0.73 | 85 | |||||||
| Ceftazidime | 3 | 0.53 | 0.43 | 0.63 | 22 | Human | 3 | 0.53 | 0.43 | 0.63 | 22 | |
| Ceftriaxone | 5 | 0.76 | 0.53 | 0.90 | 67 | Animal | 2 | 0.83 | 0.48 | 0.96 | 40 | |
| Food | 3 | 0.72 | 0.36 | 0.92 | 79 | |||||||
| Ciprofloxacin | 53 | 0.52 | 0.45 | 0.59 | 85.6 | Animal | 13 | 0.43 | 0.19 | 0.71 | 92 | |
| Human | 13 | 0.45 | 0.28 | 0.63 | 82 | |||||||
| Food | 27 | 0.51 | 0.40 | 0.61 | 93 | |||||||
| Enrofloxacin | 18 | 0.23 | 0.18 | 0.29 | 84. 3 | Animal | 4 | 0.31 | 0.14 | 0.54 | 75.1 | |
| Food | 14 | 0.21 | 0.15 | 0.29 | 90 | |||||||
| Nalidixic acid | 39 | 0.51 | 0.43 | 0.59 | 87.9 | Animal | 6 | 0.54 | 0.36 | 0.72 | 92 | |
| Human | 8 | 0.53 | 0.35 | 0.70 | 78 | |||||||
| Food | 25 | 0.48 | 0.34 | 0.62 | 93 | |||||||
| Ofloxacin | 2 | 0.79 | 0.68 | 0.86 | 0 | Human | 2 | 0.79 | 0.68 | 0.86 | 0 | |
| Colistin | 11 | 0.23 | 0.1 | 0.45 | 92 | Animal | 2 | 0.03 | 0 | 0.81 | 92 | |
| Human | 3 | 0.21 | 0.01 | 0.87 | 95 | |||||||
| Food | 6 | 0.31 | 0.16 | 0.50 | 93 | |||||||
| Critically important antimicrobials | Amikacin | 3 | 0.08 | 0.03 | 0.18 | 73 | Animal | 3 | 0.08 | 0.03 | 0.18 | 73 |
| Gentamicin | 50 | 0.04 | 0.03 | 0.07 | 79.5 | Animal | 10 | 0.05 | 0.02 | 0.11 | 75 | |
| Human | 13 | 0.09 | 0.04 | 0.18 | 67 | |||||||
| Food | 27 | 0.03 | 0.01 | 0.06 | 85 | |||||||
| Neomycin | 12 | 0.08 | 0.05 | 0.14 | 86 | Animal | 4 | 0.06 | 0.01 | 0.35 | 92 | |
| Human | 2 | 0.07 | 0.02 | 0.20 | 31 | |||||||
| Food | 6 | 0.08 | 0.05 | 0.14 | 84 | |||||||
| Azithromycin | 5 | 0.17 | 0.09 | 0.29 | 50 | Human | 1 | 0 | 0 | 0.41 | — | |
| Food | 4 | 0.18 | 0.10 | 0.31 | 57 | |||||||
| Erythromycin | 52 | 0.12 | 0.07 | 0.16 | 89.5 | Animal | 12 | 0.14 | 0.06 | 0.31 | 88 | |
| Human | 13 | 0.23 | 0.11 | 0.43 | 80 | |||||||
| Food | 27 | 0.07 | 0.03 | 0.15 | 92 | |||||||
| Highly important antimicrobials | Chloramphenicol | 34 | 0.07 | 0.04 | 0.11 | 86.9 | Animal | 6 | 0.08 | 0.05 | 0.14 | 65.3 |
| Human | 5 | 0.07 | 0.04 | 0.13 | 0 | |||||||
| Food | 23 | 0.07 | 0.03 | 0.14 | 91 | |||||||
| Florfenicol | 2 | 0.62 | 0.16 | 0.93 | 0 | Animal | 2 | 0.62 | 0.16 | 0.93 | 0 | |
| Cephalexin | 4 | 0.63 | 0.32 | 0.86 | 88 | Animal | 3 | 0.50 | 0.28 | 0.71 | 81 | |
| Human | 1 | 0.91 | 0.77 | 0.98 | — | |||||||
| Cephalotin | 5 | 0.84 | 0.47 | 0.97 | 95 | Animal | 1 | 0.26 | 0.20 | 0.33 | — | |
| Human | 2 | 0.95 | 0.84 | 0.99 | 0 | |||||||
| Food | 2 | 0.87 | 0.42 | 0.98 | 78 | |||||||
| Clindamycin | 5 | 0.34 | 0.25 | 0.43 | 52 | Human | 2 | 0.49 | 0.25 | 0.74 | 49 | |
| Food | 3 | 0.29 | 0.23 | 0.35 | 23 | |||||||
| Amoxicillin | 26 | 0.16 | 0.11 | 0.23 | 89.8 | Animal | 5 | 0.31 | 0.14 | 0.56 | 88.8 | |
| Human | 1 | 0 | 0 | 0.07 | — | |||||||
| Food | 20 | 0.13 | 0.08 | 0.22 | 91 | |||||||
| Ampicillin | 46 | 0.29 | 0.22 | 0.37 | 91 | Animal | 14 | 0.32 | 0.17 | 0.51 | 94 | |
| Human | 8 | 0.51 | 0.23 | 0.78 | 89 | |||||||
| Food | 24 | 0.21 | 0.13 | 0.31 | 92 | |||||||
| Amoxicillin–clavulanic acid | 3 | 0.34 | 0.19 | 0.52 | 68 | Animal | 1 | 0.52 | 0.32 | 0.71 | — | |
| Food | 2 | 0.26 | 0.18 | 0.35 | 0 | |||||||
| Trimethoprim-sulfamethoxazole | 14 | 0.68 | 0.51 | 0.82 | 87 | Animal | 5 | 0.62 | 0.21 | 0.91 | 93 | |
| Human | 4 | 0.49 | 0.39 | 0.58 | 0 | |||||||
| Food | 5 | 0.81 | 0.74 | 0.86 | 0 | |||||||
| Doxycycline | 3 | 0.54 | 0.32 | 0.74 | 0 | Animal | 2 | 0.42 | 0.05 | 0.91 | 31 | |
| Food | 1 | 0.56 | 0.30 | 0.80 | — | |||||||
| Tetracycline | 53 | 0.57 | 0.05 | 0.64 | 89.5 | Animal | 13 | 0.45 | 0.25 | 0.67 | 94 | |
| Human | 12 | 0.51 | 0.36 | 0.65 | 75 | |||||||
| Food | 28 | 0.59 | 0.46 | 0.70 | 94 | |||||||
| Important antimicrobials | Spectinomycin | 5 | 0.04 | 0.02 | 0.06 | 6 | Animal | 1 | 0.05 | 0.02 | 0.12 | — |
| Food | 4 | 0.03 | 0.01 | 0.06 | 11 |
Pooled Prevalence of Ampicillin, Ciprofloxacin, Erythromycin, Gentamycin and Tetracycline Resistance Proportions in Campylobacter coli and jejuni Isolates
Ampicillin, ciprofloxacin, erythromycin, gentamycin and tetracycline were among the commonly used antibiotics in the studies, so resistance of C. jejuni and C. coli to these agents was investigated separately. Ampicillin resistance in C. coli isolates (0.3, 95% CI: 0.2–0.42; I2: 78.9%) was the same as C. jejuni isolates (0.3, 95% CI: 0.21–0.4; I2: 89.7%). Ciprofloxacin resistance was higher in C. jejuni isolates (0.56, 95% CI: 0.46–0.66; I2: 90.1%) than C. coli isolates (0.53, 95% CI: 0.43–0.62; I2: 71.6%). C. coli isolates (0.18, 95% CI: 0.11–0.28; I2: 78.5%) had twice the resistance to erythromycin than C. jejuni isolates (0.09, 95% CI: 0.06–0.14; I2: 85.4%). Moreover, gentamycin resistance in C. jejuni (0.04, 95% CI: 0.03–0.07; I2: 75.5%) was half of C. coli isolates (0.08, 95% CI: 0.05–0.11; I2: 22.8%). The resistance rates to tetracycline in C. jejuni (0.56, 95% CI: 0.47–0.65; I2: 91.1%) were more than in C. coli isolates (0.53, 95% CI: 0.43–0.62; I2: 71.6%). Figure 2 shows the forest plot of these antimicrobials in C. coli and C. jejuni isolates.
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Pooled Prevalence of ARG in Campylobacter spp. in Human
The most prevalent ARG in Campylobacter spp. was tetO (0.73; 95% CI: 0.46–0.90; I2: 90%; seven studies) and cmeB (0.48; 95% CI: 0.32–0.63; I2:78; four studies) and blaOXA61 (0.42; 95% CI: 0.06–0.9; I2: 91%; six studies). The prevalence of gyrA6 (0.32; 95% CI: 0.22–0.44), qnrs (0.31; 95% CI: 0.20–0.43), A23srRNA (0.3; 95% CI: 0.19–0.41), gyrA4 (0.29; 95% CI: 0.19–0.40) and gyrA5 (0.18; 95% CI: 0.09–0.28) genes was investigated in one study and was considerably high, whereas the lowest prevalence was observed for aphA (0.2; 95% CI: 0–0.7; one study), tetA (0.06; 95% CI: 0.03–0.10; two studies) and tetB and tetS (0.0%; 95% CI: 0.0–0.1; two studies).
Discussion
Foodborne campylobacteriosis was reported in 2 out of 102 reported outbreaks in Iran (Soltan Dallal et al. 2017). The emergence of antimicrobial-resistant pathogens is an ongoing global concern in both human and veterinary medicine. The indiscriminate and excessive utilization of the antimicrobial in veterinary medication, especially in food animals and agricultural sectors, exacerbates the issue as they can be transmitted to humans through the food chain (Bennani et al. 2020). In this respect, the development of AMR in Campylobacter spp. has become a serious threat to public health (Asuming-Bediako et al. 2019; Jamali et al. 2015; Khademi and Sahebkar 2020). Campylobacter spp. is one of the most commonly involved pathogens in human gastroenteritis around the world (Asuming-Bediako et al. 2019; Azizian et al. 2019; Modirrousta et al. 2016).
In the ongoing review, we present the AMR proportions in Campylobacter spp. in Iran, based on a systematic review of published articles from the country. Our findings demonstrated that the majority of Campylobacter spp. isolates from Iran showed high resistance rates to fluoroquinolones (including ofloxacin, nalidixic acid and ciprofloxacin), beta-lactams (including cephalothin, cephalexin, ceftazidime and carbenicillin), sulfonamides (including potentiated sulfonamide trimethoprim-sulfamethoxazole), florfenicol and tetracycline, which are among the critically and highly important antimicrobials for treatment of human infections. A recent study in intensive care units of a hospital in Iran showed that AMR against trimethoprim-sulfamethoxazole (61.7%), ciprofloxacin (51.3%), imipenem (50.0%) and ampicillin (49.6%) was the most common observed finding (Salarvand et al. 2023). Our results from Iran were practically identical to those recently reported from different countries (Abdallah et al. 2022; de Vries et al. 2018; Hakkinen et al. 2007; Igwaran and Okoh 2020; Little et al. 2008; Rangaraju et al. 2022; Sadeghi et al. 2022). Similar to our results, rising resistance proportions of Campylobacter isolates to fluoroquinolones have also been documented in the United States and the United Kingdom, where a steadily increasing trend has been observed (Luangtongkum et al. 2006; Tang et al. 2017; Veltcheva et al. 2022). Additionally, in Southern Europe, the prevalence of fluoroquinolone-resistant Campylobacter expanded altogether from 1997 to 2001. Erythromycin resistance has remained low and consistent (2%) (Gupta et al. 2004), which was lower than the present study (Gao et al. 2023).
Chatre et al. (2010) documented the AMR of Campylobacter isolated from cattle between 2002 and 2006 in France. They discovered that while ampicillin, erythromycin and gentamicin showed low (<1%) resistance, most isolates (>50%) had high tetracycline and nalidixic acid resistance. Resistance to fluoroquinolone increased from 29.7% to 70.4% between 2002 and 2006. Moreover, Chen et al. (2010) revealed that 98% of Campylobacter isolates in poultry from China were also resistant to quinolones (nalidixic acid, ciprofloxacin and enrofloxacin) and tetracyclines (tetracycline and doxycycline). On the other hand, our results established that Campylobacter spp. were vulnerable or appeared to have low resistance proportions to aminoglycosides (including spectinomycin (0.04), gentamicin (0.04), neomycin (0.08) and amikacin (0.08)). Similar findings have been detailed in previous studies conducted in other nations (Chatre et al. 2010; Gupta et al. 2004). Similar to our observations from Iran, resistance to macrolides (including azithromycin (0.17) and erythromycin (0.12)), Rangaraju et al. (2022) observed that the resistance rate to macrolides (61.53%) in poultry settings in India was among the highest AMR rates. More than 90% of Campylobacter strains (761 C. jejuni and 130 C. coli) had resistance to ciprofloxacin, nalidixic acid and tetracycline (Gao et al. 2023). Furthermore, Chen et al. (2010) reported the isolation rate and AMR profile of Campylobacter isolated from broilers in China. They stated that Campylobacter isolates exhibited a moderate-to-high (>5%–50%) rate of resistance to macrolides and gentamicin, which is similar to our findings. Fluoroquinolones are a medication of choice for treating Campylobacter infection. These results reflect that the fluoroquinolone resistance prevalence rates of Campylobacter from Iran are similar to those reported from Asia and Africa (>80%), the United States and Canada (19%–47%) and European countries (17%–99%) (Luangtongkum et al. 2009). This is consistent with the World Health Organization report on fluoroquinolone resistance in Campylobacter species worldwide (Luangtongkum et al. 2009). Different mechanisms are attributed to the occurrence of chromosomally mediated quinolone resistance in Campylobacter species, such as CmeABC, efflux pumps and single-point mutations in DNA gyrase A (GyrA), such as the C257 T mutation, which is the most common mutation (Luangtongkum et al. 2009). The cases of fluoroquinolone-resistant Campylobacter in consumers of poultry meat were reported by the FDA (Dafale et al. 2020).
Macrolides are another drug of choice used in Campylobacter infection therapy. Our results showed resistance in Campylobacter species to macrolides (erythromycin 12% and azithromycin 17%). The prevalence of erythromycin resistance in Iran (0.12) was higher than that in Canada (Narvaez-Bravo et al. 2017), the Czech Republic (Bardon et al. 2009), Australia (Miflin et al. 2007), and Turkey (Ozbey and Tasdemir 2014), and lower than that in China (Han et al. 2016), Malaysia (Premarathne et al. 2017) and South Africa (Shobo et al. 2016). Three important mechanisms related to macrolide resistance in Campylobacter species include target modifications of gyrA and 23S rRNA chromosomal genes through point mutations, ribosomal proteins (i.e., L4 and L22) and the CmeABC efflux pump (Luangtongkum et al. 2009; Sharifi et al. 2021). Alternative antibiotics for the treatment of campylobacteriosis are tetracyclines and gentamicin. The mode of action attributed to tetracycline resistance in Campylobacter species is the modification of ribosomal protection proteins (tetO and tetS), efflux protein genes (tetA and tetB) and the CmeABC efflux pump (Abdi-Hachesoo et al. 2014; Luangtongkum et al. 2009; Sharifi et al. 2021). Moreover, aminoglycoside-modifying enzymes play a critical role in aminoglycoside resistance in Campylobacter species (Luangtongkum et al. 2009). On the basis of our findings, tetracycline antibiotic resistance in Campylobacter was higher than gentamicin. Similar outcomes were reported in studies previously conducted in Turkey (Ozbey and Tasdemir 2014), South Korea (Ozbey and Tasdemir 2014), Poland (Maćkiw et al. 2012), Italy (Pezzotti et al. 2003) and Africa (de Vries et al. 2018). Similar to our findings, studies conducted in Turkey have reported notable levels of resistance (>50%) to tetracycline (Ozbey and Tasdemir 2014), China (Han et al. 2016), Malaysia (Premarathne et al. 2017), Italy (Pezzotti et al. 2003), Poland (Maćkiw et al. 2012), Canada (Narvaez-Bravo et al. 2017), South Africa (Shobo et al. 2016) and South Korea (Wei et al. 2014). Our study also showed that antibiotic resistance proportions to beta-lactam antibiotics, including cefixime, cephalothin, ceftriaxone, cephalexin and ceftazidime, were high. However, the resistance proportions to imipenem and meropenem were low. The production of beta-lactamase enzymes and intrinsic resistance are the two main mechanisms by which Campylobacter species are resistant to alkaline antibiotics (Aminshahidi et al. 2017; Luangtongkum et al. 2009).
In most of the antibiotics, a higher resistance was seen in human isolates than others. Food isolates had higher resistance to doxycycline, neomycin, imipenem, azithromycin, colistin, ciprofloxacin, trimethoprim-sulfamethoxazole and tetracycline. It was reported 30%–90% of administered antibiotics in animals are defecated unchanged, which, when applied as fertilizer, creates a major reservoir of antibiotic residues, antibiotic-resistant bacteria and ARGs (Enshaie et al. 2025). These residues are able to pollute soil and water via run-off or discharge, promoting the persistence and proliferation of antibiotic-resistant bacteria and ARGs, which can be transferred across species, including to humans. Soil bacteria can remain as long-term reservoirs of ARGs, which can be transmitted to pathogens, creating a cycle from the environment to humans via crops or water (Enshaie et al. 2025). Humans can take up the resistant bacteria via direct contact with animals, consumption of contaminated animal products such as meat or milk, and environmental sources like water contaminated with animal waste (Al-Nasser et al. 2020).
According to the findings of the present investigation, the proportion of erythromycin and gentamycin resistance was higher in C. coli than C. jejuni, whereas the resistance to ciprofloxacin and tetracycline was higher in C. jejuni than C. coli isolates. Erythromycin resistance of C. coli (59.23%) was higher than C. jejuni (2.50%) in clinical isolates in Shanghai, China (Gao et al. 2023). The authors who investigated the prevalence and antibiotic resistance rates of Campylobacter in United States dairy cattle concluded that C. coli strains showed higher resistance to antimicrobials than C. jejuni (Englen et al. 2007). Moreover, C. coli isolates had higher resistance to antimicrobials than C. jejuni from diarrhoeal patients and chickens in Botswana (de Vries et al. 2018). Eryildiz et al. (2020) reported the higher resistance to antimicrobials in C. jejuni (Eryildiz et al. 2020). C. jejuni and C. coli were resistant to ciprofloxacin, tetracycline, florfenicol and nalidixic acid (5.39%), and azithromycin, ciprofloxacin, erythromycin, gentamicin, tetracycline, clindamycin and nalidixic acid (28.46%), respectively (Gao et al. 2023).
AMR is increasingly conceptualized as a critical environmental concern, transcending its conventional association with clinical and veterinary domains. The natural environment operates as a fundamental reservoir, conduit and catalyst in the emergence, genetic evolution and dissemination of antimicrobial-resistant bacteria and ARGs. Within the framework of the One Health paradigm—which underscores the intrinsic interdependence of human, animal and environmental health—the environmental dimension is now regarded as indispensable to understanding the complex epidemiological and ecological dynamics underpinning AMR (Andersson and Hughes 2014).
On the basis of our findings, the most prevalent ARG in Campylobacter spp. was tetO, followed by cmeB, OXA61, gyrA6, qnrs, A23srRNA, gyrA4 and gyrA5 genes. The least prevalent AMR genes were tetB and tetS, aphA and total tetA. Resistance mechanisms observed in Campylobacter include horizontal gene transfer between different Campylobacter species, such as that observed with tetracycline (tetO, A, B, S), erythromycin (aphA), chloramphenicol, neomycin, kanamycin and streptomycin genes, as well as obtaining the resistance genes from other bacterial species, such as the kanamycin (aphA-3), streptomycin (aadA) and streptomycin/spectinomycin (aadE) resistance genes obtained from Gram-positive cocci (Aarestrup and Wegener 1999). The tet(O) and 23SrRNA genes were recorded in 54.55% and 50% of tetracycline- and macrolide-resistant isolates, respectively (Rangaraju et al. 2022). Analysis of environmental samples, including sewage, seawater, sediment and aerosol, documented widespread ARGs and also identified the overlapping of ARGs (Berendonk et al. 2015). Regarding the One Health approach, none of the studies in Iran used this approach to interlink these sectors in the assessment of AMR in Campylobacter. ARGs just have been studied in a few studies in human and food samples.
Limitations
One of the limitations of this study is the report of different antimicrobial agents in different samples, and also different food samples were studied in different research studies. Moreover, other limitations were the wide timeframe of included studies and lack of recent studies and also the low number of studies reporting ARGs. In addition, the findings of the current study must be interpreted cautiously due to high heterogeneity. Results of this study showed that, as the antibiotic resistance rates were different in different sectors and some of them had no considerable difference, control of AMR must be considered in all sectors.
Conclusion
Our meta-analysis results showed that Campylobacter species isolated from humans, animals and food in Iran have a high proportion of resistance to different antibiotics. To reduce the resistance rate of pathogens, different strategies such as frequent drug resistance monitoring, reduced and optimized use of antimicrobials in all sectors, education and raising awareness towards AMR have been suggested. Moreover, good agricultural and manufacturing practices and hazard analysis of critical control points at every stage of the food chain are recommended to decrease the risk of development and spread of antibiotic resistance. In addition, the investigation of ARGs in different sections, especially environmental sources, is suggested.
Author Contributions
Fatemeh Salmani, Sara Mohamadi, Parisa Sadighara and Tayebeh Zeinali conceptualized the study. Tayebeh Zeinali and Parisa Sadighara performed the search and extract the data. Sara Mohamadi and Tayebeh Zeinali evaluate the studies. Fatemeh Salmani performed the analysis. Taurai Tasara critically revised the article. All authors coorporate in the writing of the draft. All authors read and approved the final manuscript.
Acknowledgements
The authors acknowledge the research and technology deputy of Birjand University of Medical Sciences for support of this study.
Funding
The authors have nothing to report.
Ethics Statement
The study was approved by ethical committee of Birjand University of Medical Sciences.
Conflicts of Interest
The authors declare no conflicts of interest.
Data Availability Statement
Data are available from the corresponding author on reasonable request.
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