Abstract
Campylobacter is a major public health problem, leading to foodborne diarrhea in the world. The current study aimed to isolate Campylobacter in different sources of poultry and determine antimicrobial susceptibility. A total of 150 fecal and 29 cloacal swabs were obtained from poultry farms (84 cloacal swabs) and live bird markets (LBMs), respectively, and 37 cecal swabs were also acquired from a local slaughterhouse located in the middle Euphrates region. Campylobacter Species (spp.) was first isolated and characterized by conventional bacteriological methods. Secondly, the antimicrobial susceptibility of isolates was investigated by disc diffusion method. The overall prevalence of Campylobacter spp. isolated from fecal cloacal and cecal poultry samples was 24% (36 out of 150). All strains were resistant to Nalidixic acid and Ciprofloxacin (100%), with high resistance to Tetracycline (88.8%), Ampicillin (83.3%), Sulpha/Trimethoprim (80.5%), Erythromycin (50%), and Ceftriaxone (50%), but less resistant to Gentamicin (30.5%), Amoxi-Clav (27.7%), and Chloramphenicol (22.2%). The majority of isolates (97.2%) scored a multiple antibiotic resistance (MAR) index of 0.3 or more, and 35 (97.2%) isolates were resistant to three or more antibiotic classes. Particularly, 61.1% of the isolates were multidrug resistance (MDR), 36.1% of the isolates were extensively drug resistant, and 2.8% of the isolates were Pan drug resistant. Moreover, the current study detected 24 multiple resistance patterns from 36 isolates of Campylobacter spp., and most of the isolates (27 out of 36) displayed an important route of resistance to Nalidixic acid, Ciprofloxacin, and Tetracycline. Based on the results, increased resistance rates to commonly used antibiotics in Campylobacter were recovered from poultry farms, LBMs, and local slaughterhouses. The majority of strains were MDR to commonly used antimicrobials with elevated MAR indices, requiring implementation of a national strategy to improve husbandry practice and the effective use of antibacterial agents, alternatives, and vaccines.
Keywords: Antimicrobial resistance, Campylobacter, LBMs, MAR index, Poultry farms, Slaughterhouse
1. Introduction
Campylobacter is a major public health problem, leading to food-borne diarrhea and the most prevalent bacterial cause of gastroenteritis in humans and Campylobacteriosis in the world. However, the course of this disease is usually self-limited, characterized by fever, abdominal pain, and diarrhea. The infections can be deadly in young children, immunocompromised people, and old age. Individuals immunocompromised with underlying chronic conditions and the elderly may develop a systemic spread of infection and septicemia ( 1 ).
Campylobacter is a zoonotic and thermophilic organism with an optimum growth temperature of about 42°C that is similar to avian body temperature, and poultry serves as a reservoir for these bacteria ( 2 ). Poultry and poultry products are considered the main source of pathogenic Campylobacter, resulting in transmitting these bacteria to humans. The treatment of the domestic animals with antimicrobials to improve the overall health and produce higher-quality products could result in developing resistance bacteria to these antibiotics and suppressing sensitive bacteria. Therefore, human consumption of such contaminated food from animal origin may lead to adverse and unwanted health consequences ( 3 ).
More recently, literature has reported an increased frequency of antimicrobial-resistant and multidrug resistance (MDR) Campylobacter strains, particularly macrolides, fluoroquinolones, and tetracyclines ( 4 ). The valuable surveillance strategies to control campylobacteriosis should focus not only on tracing bacteria in humans, but also on the significant sources of Campylobacter species (spp.), mainly poultry production chain, endorsed under the “One World-One Health” approach that represents collective efforts of ministries of health and agriculture, workers in medical and veterinary sectors, researchers, and politicians ( 5 ).
In Iraq, few studies have been conducted on the prevalence and antimicrobial resistance in Campylobacter isolated from poultry farms, live bird markets (LBMs), and slaughterhouses.
Therefore, the current study was conducted to isolate Campylobacter from poultry farms, LBMs, and a local slaughterhouse in the middle Euphrates region and determine the susceptibility of the isolates to commonly used antimicrobial agents.
2. Materials and Methods
2.1. Sample Collection
In this cross-sectional study, 150 fecal and 29 cloacal swabs were obtained from poultry farms (84 cloacal swabs) and LBMs, respectively; moreover, 37 cecal swabs were acquired from a local slaughterhouse located in Al-Najaf and Al-Qadisiyah Governorates in the middle Euphrates region from December 2020 to the end of March 2021. Sterile cotton swabs were used for fecal sample collection, immediately inoculated on C&S Modified Cary Blair Transport media (Hardy diagnostics/USA), and delivered by cold box to Public Health Laboratory of milk and meat hygiene, Department of Public Health, Faculty of Veterinary Medicine, University of Kufa, Kufa, Iraq.
2.2. Bacteriological Isolation of Campylobacter
According to the guidelines of OIE (2017) for the isolation of Campylobacter spp., each swab from the transport medium was streaked onto Campylobacter Agar Base (CRITERION, Hardy Diagnostic), enriched with 5%-10% (vol/vol) human blood and Campylobacter selective supplement (Karmali, Oxoid) with Sodium pyruvate 50 mg, Vancomycin 10 mg, Cefoperazone 16 mg, and Cycloheximide 50 mg. Subsequently, the streaked plates were incubated at 42°C under microaerophilic conditions (5% O2, 10% CO2, 85% N2), generated by CampyGenTM (Oxoid CN0035) for 48 h in the anaerobic jar (Oxoid, UK).
2.3. Identification of Campylobacter Isolates
Colonies with a small, not hemolytic, mucoid, grayish, and flat appearance, as well as irregular edges after 48 h from the incubation or those that were convex, round, entire, and glistening with 1-2 mm in diameter were presumptively identified as Campylobacter spp. ( 6 ) and subjected for further identification with Gram stain, oxidase, catalase, and indoxyl hydrolysis tests ( 7 ). All suspected isolates were subjected for agglutination with Microgen® Bioproducts Campylobacter Latex kit (Hardy diagnostics/USA) according to the manufacturer’s instructions.
2.4. Disk Diffusion Antibacterial Susceptibility Testing
The antimicrobial susceptibility test for all confirmed isolates was conducted using the disc diffusion method on Mueller-Hinton/blood agar plates in accordance with Gblossi Bernadette and Eric Essoh ( 8 ). Moreover, the susceptibility of strains was evaluated against 10 antimicrobial agents, including Erythromycin (15 μg), Tetracycline (30 μg), Ciprofloxacin (5 μg), Chloramphenicol (30 μg), Gentamicin (10 μg), Sulph/Trimethoprim (25 μg), Amoxi/Clav (30 μg), Ampicillin (10 μg), Ceftriaxone (30 μg), and Nalidixic acid (30 μg). The recorded results were interpreted according to the Clinical Laboratory Standards Institute (CLSI) guidelines for fastidious bacteria (CLSI, 2018) and CLSI criteria for Enterobacteriaceae (CLSI, 2019).
The multiple antibiotic resistance (MAR) index was estimated as the total number of medicines for each isolate and obtained as follows:
MAR=R/E ( 9 )
where R and E are resistant and the number of antibiotics examined for each isolate, respectively.
This study utilized the concepts of resistance patterns, defined by Magiorakos and Srinivasan ( 10 ) who defined MDR strains that are resistant to at least one drug in three antimicrobial medication classes. Extensively drug-resistant (XDR) refers to strains that are resistant to all drugs, except for two classes of medications, and pan drug resistance (PDR) also refers to an ability of strain to withstand all antimicrobial agents in all classes examined.
2.5. Statistics
The Chi-square and Fisher’s Exact tests were used to compare significance between two percentages, and a P-value less than 0.05 was considered statistically significant.
3. Results and Discussion
3.1. Prevalence of Campylobacter Species in Poultry
The overall prevalence of Campylobacter spp. isolated from fecal cloacal and cecal poultry samples confirmed by standard bacteriological methods was 36 (24%) isolates out of 150 samples. In reviewing the literature, the prevalence of Campylobacter spp. was very dynamic and varied according to geographic area, season, sampling, and culturing methods, as well as other confounding factors. The findings of the current study are consistent with the results of studies conducted by Karikari and Obiri-Danso ( 11 ) who found a prevalence rate of 22.5% after examining the broiler and layer fecal samples. However, a systemic review and meta-analysis study reported a high mean prevalence (40.2%) in cecal/fecal poultry samples among 14 African countries ( 12 ), and the prevalence varied from 2% to 100% among 28 European.
countries ( 13 ). Furthermore, the sampling season substantially affected the prevalence of Campylobacter due to the high temperature of summer ( 14 ). Therefore, all samples were collected in the winter, leading to a low prevalence rate of colonization in the current study.
3.2. Antibacterial Susceptibility Testing
All Campylobacter spp. isolates (100%) were resistant to Ciprofloxacin and Nalidixic acid emphasized in table 1. Moreover, high resistance frequency was recorded to Tetracycline (88.8%), Ampicillin (83.3%), Sulpha/Trimethoprim (80.5%), Erythromycin (50%), and Ceftriaxone (50%) with less resistant to Gentamicin (30.5%), Amoxi-Clav (27.7%), and Chloramphenicol (22.2%).
Table 1.
Antibiotic susceptibility testing of 36 Campylobacter spp. recovered from different poultry sources
| Antibiotic class | Agent | Interpretation | |
|---|---|---|---|
| Susceptible (%) | Resistant (%) | ||
| Macrolides | Erythromycin | 18 (50) | 18 (50) |
| Tetracyclines | Tetracycline | 4 (11.1) | 32 (88.8) |
| Fluoroquinolones | Ciprofloxacin | 0 (0) | 36 (100) |
| Phenicols | Chloramphenicol | 26 (72.2) | 10 (27.7) |
| Aminoglycosides | Gentamicin | 25 (69.4) | 11 (30.5) |
| Folate pathway inhibitor | Sulpha / Trimeth | 7 (19.4) | 29 (80.5) |
| Penicillin | Amoxi-Clav | 26 (72.2) | 10 (27.7) |
| Penicillin | Ampicillin | 7 (19.4) | 29 (80.5) |
| Cephalosporin | Ceftriaxone | 18 (50) | 18 (50) |
| Quinolones | Nalidixic acid | 0 (0) | 36 (100) |
Fluoroquinolones, Macrolides, and Tetracyclines are used to treat clinical cases of campylobacteriosis ( 15 ). However, antibiotic resistance, such as fluoroquinolones resistant Campylobacter among bacteria recovered from foods of animal origin is known as the main concern during the past two decades ( 16 , 17 ).
In the present study, ultimate resistance to Nalidixic acid and Ciprofloxacin and high resistance to Tetracycline and Erythromycin was observed, reflecting the great risk of current isolates on public health. A previous study conducted on Campylobacter from chicken meat in Baghdad reported a high level of resistance to Tetracycline (86.7%), Erythromycin (86.7%), and Norfloxacin (56.7%), but not to Nalidixic acid and Ciprofloxacin (23.3% and 13.3%, respectively) ( 18 ). In Algeria, Campylobacter recovered from broilers at farms and slaughterhouses was resistant to Nalidixic acid with a high frequency of resistance to Tetracycline, Ciprofloxacin, and Ampicillin ( 19 ). Some studies have documented increased levels of resistance to many classes of antimicrobials, including Fluoroquinolones and Tetracyclines in Campylobacter isolated from fecal samples in poultry ( 20 - 22 ). The misuse and heavy use of quinolones in poultry production may result in emerging and spreading quinolone and fluoroquinolone resistance in the bacterial population.
The data on the prevalence of resistance is an important milestone to assess the risk connected with antimicrobial resistance in Campylobacter surveillance programs ( 23 ). The use of Tetracycline in the food of poultry to prevent infection in breeding fields can lead to higher rates of resistance to it (88.8%), resulting in emerging and spreading antimicrobial resistance. These results are consistent with those of a study conducted in Canada in which resistance to Tetracycline was due to its overuse in the food of small poultry flocks ( 21 ).
In the current study, Ampicillin resistance was 83.3% that is in agreement with that in some previous studies ( 24 , 25 ). Out of 36 isolates, only 7 (19.4%) isloates showed susceptibility to Sulpha/Trimethoprim, showing that the less susceptible Campylobacter isolates to Sulpha/Trimethoprim seem increasing which is in line with the results of other studies ( 11 , 26 ). Furthermore, the antimicrobial susceptibility testing of the current study documented significant Erythromycin resistance (50%) among Campylobacter isolates, and a similar resistance rate (54.5%) was observed in Campylobacter isolated from chicken cloacal swabs in Egypt ( 27 ). However, a study in Tunisia determined Erythromycin resistance in all Campylobacter isolated from broilers ( 28 ). The increased Erythromycin resistance causes its less use as a first-line treatment option for human campylobacteriosis.
The resistance ratio of the current poultry isolates to Ceftriaxone was 50%. Moreover, high Ceftriaxone resistance was recorded in Campylobacter strains reported in broiler chicken products in Lithuania ( 20 ). However, the results of other studies are not in line with the findings of a study conducted by Rashid and Azeem ( 29 ) in Pakistan. They found very low Ceftriaxone resistance. Ceftriaxone is frequently recommended as an empirical treatment for individuals admitted to the hospital with stomach pain and fever.
On the contrary, very low resistance frequencies were reported in Campylobacter spp. recovered from poultry in countries that implemented Fluoroquinolone ban and/or restricted antibiotics usage by poultry farms, such as Australia and Scandinavian countries ( 30 ). Therefore, revising the Iraqi guidelines seems necessary to regulate the distribution and the use of these antimicrobial agents as growth promotors and prophylactic for therapeutic purposes in poultry production.
Although the current results showed the low resistance of Campylobacter to Gentamicin (30.5%), Amoxi-Clav (27.7%), and Chloramphenicol (22.2%), they are close to those recorded in Campylobacter isolated from different sources of poultry from different parts of the world ( 31 , 32 ). On the other hand, in eastern Algeria, a study was conducted on ultimate resistance to Amoxi-Clave and a moderate level of Chloramphenicol resistance (52.6%), all Campylobacter isolates were sensitive to Gentamycin ( 7 ), utilized rarely in Iraq for both preventive and therapeutic reasons, leading to the low prevalence of resistance.
3.3. Multiple Antibiotic Resistance Index and Multidrug Resistance
As presented in table 2, the MAR indices of the current isolates ranged between 0.2 and 0.7, and 35 out of 36 (97.2%) isolates were scored a MAR index of 0.3 or more.
Table 2.
Multiple antibiotic resistance indices of Campylobacter spp. isolated from the poultry sample
| MAR index | No. of antimicrobials to which the isolates were resistant (10) | No of Isolates (%) |
|---|---|---|
| 0.2 | 3 | 1 (2.77) |
| 0.3 | 4 | 2 (5.55) |
| 0.3 | 6 | 1 (2.77) |
| 0.4 | 5 | 12 (33.33) |
| 0.4 | 6 | 5 (13.88) |
| 0.4 | 7 | 1 (2.77) |
| 0.5 | 6 | 2 (5.55) |
| 0.5 | 8 | 4 (11.11) |
| 0.6 | 8 | 4 (11.11) |
| 0.6 | 9 | 1 (2.77) |
| 0.7 | 7 | 1 (2.77) |
| 0.7 | 9 | 1 (2.77) |
| 0.7 | 10 | 1 (2.77) |
MAR=multiple drug resistance
MAR index is used to measure how bacteria are affected by antibiotic usage, used as a tool to differentiate between animal isolates with high risk (MAR index over than 0.2) and low risk (MAR index less than 0.2). Furthermore, a MAR index of greater than 0.3 indicates that bacteria had already developed in an area in which antibiotics were often administered ( 33 ).
In the present study, however, the MAR index of 0.3 and more were recorded for the majority (97.2%) of Campylobacter spp. isolates were considered the most interesting finding. One isolate showed a 0.2 MAR index, indicating certainly the link to heavy and uncontrolled use of antibiotics which might create a high antibiotic selective pressure in the poultry production chain. Therefore, the current isolates represent a high public health risk.
Emerging and spreading MDR Campylobacter spp. is a vital and challenging issue that may compromise the effective treatment options for human campylobacteriosis. Therefore, the present data revealed that all isolates, except for one, were resistant to at least three of the most widely used antibiotics. However, similar studies in Iraq, South Korea, and Additionally, the findings of the current study are consistent with those of previous studies conducted on Campylobacter spp. isolated from frozen chicken meat in Iraq ( 9 ). Moreover, similar results were reported in many countries overusing antimicrobial agents in the poultry field ( 34 , 35 ). In India, a MAR index between 0.11 and 0.78 in Campylobacter isolated from broilers and slaughterhouse background was reported ( 36 ).
Furthermore, 35 (97.2%) isolates were resistant to three or more antibiotic classes, and 22 (61.1%) isolates were particularly MDR, showing resistance to 3-4 different antimicrobial classes. In addition, our findings revealed the presence of 11 (30.55%) XDR isolates (resistant to 5-7 different antimicrobial classes) with 1 (2.77%) PDR (resistant to all examined antimicrobials) as shown in table 3.
Table 3.
Prevalence of MDR, XDR, and PDR Campylobacter spp. isolated from poultry samples
| Character of resistant strains | No. (%) of Campylobacter spp. isolates | No. of antibiotics to which the isolates were resistant | No. of antibiotic classes (n=7) |
|---|---|---|---|
| MDR (22=61.1%) | 2 | 4 | 3 |
| 1 | 6 | 3 | |
| 12 | 5 | 4 | |
| 5 | 6 | 4 | |
| 1 | 7 | 4 | |
| XDR (11=30.55%) | 4 | 8 | 5 |
| 2 | 6 | 5 | |
| 1 | 9 | 6 | |
| 4 | 8 | 6 | |
| 1 | 7 | 7 | |
| 1 | 9 | 7 | |
| PDR (1=2.77%) | 1 | 10 | 7 |
MDR= Multidrug resistance
XDR= Extensively drug-resistant
PDR= Pan drug resistance
China have reported that the majority of Campylobacter isolates from poultry were MDR ( 9 , 35 , 37 ), and lower prevalence (54.4%) was demonstrated in Campylobacter isolates from broilers and slaughterhouse background swabs in India ( 36 ); moreover, a very lower prevalence of MDR was recorded among poultry isolates in Brazil ( 34 ).
Additionally, XDR and PDR were characterized in the present isolates, requiring more efforts toward controlling Campylobacter in the food chain in Iraq. The current results are apparently consistent with those of the other research conducted on an increased prevalence of MDR, XDR, and PDR Campylobacter strains of poultry in Egypt ( 38 ). Such categories of resistant bacteria may lead to antibiotic treatment failure both in veterinary and medical practices.
Table 4 tabulates 24 different resistant patterns in that the most frequent patterns include:
Table 4.
Diverse resistance patterns among poultry-derived Campylobacter isolates
| Resistance category | Resistance patterns | Code of isolates | No. of isolates |
|---|---|---|---|
| 2 class | CIP, NA, SXT | B56 | 1 |
| 3 class | CIP, NA, SXT, Te | L73 | 1 |
| 3 class | CIP, NA, SXT, GM | B55 | 1 |
| 3 class | CIP, NA, SXT, AM, CRO, AmC | F123 | 1 |
| 4 class | CIP, NA, SXT, Te, AM | L81, L84, L85 | 9 |
| F109, F110, F111, F113, F114, F115 | |||
| 4 class | CIP, NA, SXT, Te, AM, CRO | F106, F107 | 2 |
| 4 class | CIP, NA, Te, AM, CRO, E | B7, C1 | 2 |
| 4 class | CIP, NA, Te, GM, E | B62 | 1 |
| 4 class | CIP, NA, AM, E, C | B66 | 1 |
| 4 class | CIP, NA, Te, AM, CRO, E, AMC | C20 | 1 |
| 4 class | CIP, NA, Te, AM, CRO, GM | F117 | 1 |
| 4 class | CIP, NA, SXT, CRO, E | F126 | 1 |
| 5 class | CIP, NA, SXT, Te, AM, E | F108 | 1 |
| 5 class | CIP, NA, SXT, Te, AM, CRO, E, AmC | F119, B64, C2 | 3 |
| 5 class | CIP, NA, SXT, Te, E, C | B65 | 1 |
| 5 class | CIP, NA, SXT, Te, AM, CRO, GM, AMC | F124 | 1 |
| 6 class | CIP, NA, SXT, Te, AM, CRO, E, C | B11 | 1 |
| 6 class | CIP, NA, SXT, Te, AM, E, C, CRO | B44 | 1 |
| 6 class | CIP, NA, SXT, Te, AM, CRO, GM, E, AmC | B67 | 1 |
| 6 class | CIP, NA, SXT, Te, AM, GM, E, AmC | C3 | 1 |
| 6 class | CIP, NA, Te, AM, CRO, GM, E, C | C4 | 1 |
| 7 class | CIP, NA, SXT, Te, AM, CRO, GM, E, C | F93 | 1 |
| 7 class | CIP, NA, SXT, Te, AM, CRO, GM, E, C, AmC | F112 | 1 |
| 7 class | CIP, NA, SXT, Te, GM, E, C, AmC | H22 | 1 |
*Resistant to antimicrobials at normal dosages (μg): Erythromycin (E,15μg), Tetracycline (Te, 30μg), Ciprofloxacin (CIP, 5μg), Chloramphenicol (C, 30μg), Gentamycin (GM, 10μg), Sulpha-trieth (SXT, 25μg), Amoxicillin/Clav.Acid (AmC, 30μg), Ampicillin (AM, 10μg), Ceftriaxone (CRO 30μg), and Nalidixic acid (NA, 30μg).
-CIP + NA / SXT / Te / AM (9 isolates)
-CIP + NA / SXT / Te / AM + CRO + AmC / E (3 isolates)
-CIP + NA / SXT / Te / AM + CRO (2 isolates)
-CIP + NA / Te / AM + CRO / E (2 isolates)
Other patterns were in each isolate that most of isolates (27 out of 36) displayed an important route of resistance to Nalidixic acid, Ciprofloxacin, and Tetracycline.
In this study, the high prevalence of MDR strains among Campylobacter spp. isolates from poultry was an important finding in resistance pattern including NA/CIP/Te, detected previously in 90% of Salmonella Ohio isolated from poultry farms in Al-Najaf and Al-Muthana provinces ( 39 ) (i.e., the resistance traits could be circulating between pathogenic commensal bacteria colonizing the gut of birds may be via transmissible genetic elements).
To the best of our knowledge, this was the first survey study on isolation and antimicrobial susceptibility of Campylobacter in the middle Euphrates region that also found a significant prevalence of Campylobacter in poultry, regardless of its type and source with a very high prevalence of MDR strains. Therefore, the high levels of MAR index were in different poultry samples, showing a worrisome food safety situation in the middle Euphrates region.
Authors' Contribution
Study concept and design: Z. M. S.
Acquisition of data: A. O. A.
Analysis and interpretation of data: T. I. K.
Drafting of the manuscript: H. M. A.
Critical revision of the manuscript for important intellectual content: Z. M. S.
Statistical analysis: Z. M. S.
Administrative, technical, and material support: Z. M. S.
Ethics
Since this study used fecal samples from cloacal and cecal from slaughtered chicken, no ethical approval was needed.
Conflict of Interest
The authors declare that they have no conflict of interest.
References
- 1.Masila NM, Ross KE, Gardner MG, Whiley H. Zoonotic and Public Health Implications of Campylobacter Species and Squamates (Lizards, Snakes and Amphisbaenians) Pathogens. 2020;9(10):799. doi: 10.3390/pathogens9100799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.El-Wadawe NR, Omran EA, Hazzah WA, Bakr WM. Detection of Campylobacter in Chicken Parts by Conventional Methods and Polymerase Chain Reaction with Identification of Antibiotic Resistance Profile. J High Inst Public Health. 2019;49(2):73–81. [Google Scholar]
- 3.Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther. 2015;40(4):277. [PMC free article] [PubMed] [Google Scholar]
- 4.Igwaran A, Okoh AI. Human campylobacteriosis: A public health concern of global importance. Heliyon. 2019;5(11):02814. doi: 10.1016/j.heliyon.2019.e02814. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.WHO. Campylobacter. 2020. Available from: https://www.who.int/news-room/fact-sheets/detail/campylobacter .
- 6.Markey B, Leonard F, Archambault M, Cullinane A, Maguire D. Clinical veterinary microbiology e-book: Elsevier Health Sciences; 2013 [Google Scholar]
- 7.Baali M, Lounis M, Al Amir HL, Ayachi A, Hakem A, Kassah-Laouar A. Prevalence, seasonality, and antimicrobial resistance of thermotolerant Campylobacter isolated from broiler farms and slaughterhouses in East Algeria. Vet World. 2020;13(6):1221. doi: 10.14202/vetworld.2020.1221-1228. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Gblossi Bernadette G, Eric Essoh A, Solange E, Natalie G, Souleymane B, Lamine Sébastien N, et al. Prevalence and antimicrobial resistance of thermophilic Campylobacter isolated from chicken in Côte d’Ivoire. Int J Microbiol. 2012;2012 doi: 10.1155/2012/150612. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Kanaan MHG, Abdulwahid MT. Prevalence Rate, Antibiotic Resistance and Biotyping of Thermotolerant Campylobacter Isolated from Poultry Products Vended in Wasit Markets. Curr Res Nutr Food Sci. 2019;7(3):905–17. [Google Scholar]
- 10.Magiorakos A-P, Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81. doi: 10.1111/j.1469-0691.2011.03570.x. [DOI] [PubMed] [Google Scholar]
- 11.Karikari AB, Obiri-Danso K, Frimpong EH, Krogfelt KA. Multidrug resistant Campylobacter in faecal and carcasses of commercially produced poultry. Afr J Microbiol Res. 2017;11(7):271–7. [Google Scholar]
- 12.Thomas KM, de Glanville WA, Barker GC, Benschop J, Buza JJ, Cleaveland S, et al. Prevalence of Campylobacter and Salmonella in African food animals and meat: A systematic review and meta-analysis. Int J Food Microbiol. 2020;315:108382. doi: 10.1016/j.ijfoodmicro.2019.108382. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Hazards EPoB. Scientific opinion on quantification of the risk posed by broiler meat to human campylobacteriosis in the EU. EFSA J. 2010;8(1):1437. [Google Scholar]
- 14.Ibrahim JN, Eghnatios E, El Roz A, Fardoun T, Ghssein G. Prevalence, antimicrobial resistance and risk factors for campylobacteriosis in Lebanon. J Infect Dev Ctries. 2019;13(01):11–20. doi: 10.3855/jidc.10729. [DOI] [PubMed] [Google Scholar]
- 15.Wieczorek K, Osek J. Antimicrobial resistance mechanisms among Campylobacter. BioMed Res Int. 2013;2013 doi: 10.1155/2013/340605. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.WHO I. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. WHO. 2017;7 [Google Scholar]
- 17.Bonomo RA, Hooper DC, Kaye KS, Johnson JR, Clancy CJ, Thaden JT, et al. Gram-negative bacterial infections: research priorities, accomplishments, and future directions of the Antibacterial Resistance Leadership Group. Clin Infect Dis. 2017;64(1):30–5. doi: 10.1093/cid/ciw829. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Kanaan M, Khashan HT. Prevalence of multidrug resistant thermotolerant species of Campylobacter in Retail Frozen Chicken meat in Baghdad Province. Curr Res Microbiol Biotechnol. 2018;6(1):1431–40. [Google Scholar]
- 19.Messad S, Hamdi T-M, Bouhamed R, Ramdani-Bouguessa N, Tazir M. Frequency of contamination and antimicrobial resistance of thermotolerant Campylobacter isolated from some broiler farms and slaughterhouses in the region of Algiers. Food Control. 2014;40:324–8. [Google Scholar]
- 20.Aksomaitiene J, Ramonaite S, Tamuleviciene E, Novoslavskij A, Alter T, Malakauskas M. Overlap of antibiotic resistant Campylobacter jejuni MLST genotypes isolated from humans, broiler products, dairy cattle and wild birds in Lithuania. Front Microbiol. 2019;10:1377. doi: 10.3389/fmicb.2019.01377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Varga C, Guerin MT, Brash ML, Slavic D, Boerlin P, Susta L. Antimicrobial resistance in Campylobacter jejuni and Campylobacter coli isolated from small poultry flocks in Ontario, Canada: A two-year surveillance study. PLoS One. 2019;14(8):e0221429. doi: 10.1371/journal.pone.0221429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Gharbi M, Béjaoui A, Ben Hamda C, Jouini A, Ghedira K, Zrelli C, et al. Prevalence and antibiotic resistance patterns of Campylobacter spp. isolated from broiler chickens in the North of Tunisia. BioMed Res Int. 2018;2018 doi: 10.1155/2018/7943786. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Organization WH. Tackling antibiotic resistance from a food safety perspective in Europe: World Health Organization. REU: 2011. [Google Scholar]
- 24.Kouglenou SD, Agbankpe AJ, Dougnon V, Djeuda AD, Deguenon E, Hidjo M, et al. Prevalence and susceptibility to antibiotics from Campylobacter jejuni and Campylobacter coli isolated from chicken meat in southern Benin, West Africa. BMC Res Notes. 2020;13(1):1–6. doi: 10.1186/s13104-020-05150-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Proietti PC, Guelfi G, Bellucci S, De Luca S, Di Gregorio S, Pieramati C, et al. Beta-lactam resistance in Campylobacter coli and Campylobacter jejuni chicken isolates and the association between blaOXA-61 gene expression and the action of β-lactamase inhibitors. Vet Microbiol. 2020;241:108553. doi: 10.1016/j.vetmic.2019.108553. [DOI] [PubMed] [Google Scholar]
- 26.Aksomaitiene J, Novoslavskij A, Kudirkiene E, Gabinaitiene A, Malakauskas M. Whole Genome Sequence-Based Prediction of Resistance Determinants in High-Level Multidrug-Resistant Campylobacter jejuni Isolates in Lithuania. Microorganisms. 2021;9(1):66. doi: 10.3390/microorganisms9010066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Ghoneim NH, Sabry MA, Ahmed ZS, Elshafiee EA. Campylobacter Species Isolated from Chickens in Egypt: Molecular Epidemiology and Antimicrobial Resistance. Pak J Zool. 2020;52(3):917. [Google Scholar]
- 28.Gharbi M, Béjaoui A, Hamda CB, Ghedira K, Ghram A, Maaroufi A. Distribution of virulence and antibiotic resistance genes in Campylobacter jejuni and Campylobacter coli isolated from broiler chickens in Tunisia. J Microbiol Immunol Infect. 2021 doi: 10.1016/j.jmii.2021.07.001. [DOI] [PubMed] [Google Scholar]
- 29.Rashid S, Azeem M, Khan SA, Shah MM, Ahmad R. Characterization and synergistic antibacterial potential of green synthesized silver nanoparticles using aqueous root extracts of important medicinal plants of Pakistan. Colloids Surf B. 2019;179:317–25. doi: 10.1016/j.colsurfb.2019.04.016. [DOI] [PubMed] [Google Scholar]
- 30.Mattheus W, Botteldoorn N, Heylen K, Pochet B, Dierick K. Trend analysis of antimicrobial resistance in Campylobacter jejuni and Campylobacter coli isolated from Belgian pork and poultry meat products using surveillance data of 2004–2009. Foodborne Pathog Dis. 2012;9(5):465–72. doi: 10.1089/fpd.2011.1042. [DOI] [PubMed] [Google Scholar]
- 31.Hull DM, Harrell E, van Vliet AH, Correa M, Thakur S. Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019. PloS One. 2021;16(2):e0246571. doi: 10.1371/journal.pone.0246571. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Lazo-Láscarez S, Zumbado Gutiérrez L, Duarte-Martínez F, Romero Zúñiga JJ, Arias Echandi ML, Muñoz-Vargas L. Antimicrobial resistance and genetic diversity of Campylobacter spp. isolated from broiler chicken at three levels of the poultry production chain in Costa Rica. Antimicrobial resistance of Campylobacter isolated from poultry chain. J Food Prot. 2021 doi: 10.4315/JFP-21-111. [DOI] [PubMed] [Google Scholar]
- 33.Tripathi P, Banerjee G, Saxena S, Gupta MK, Ramteke P. Antibiotic resistance pattern of Pseudomonas aeruginosa isolated from patients of lower respiratory tract infection. Afr J Microbiol Res. 2011;5(19):2955–9. [Google Scholar]
- 34.Paravisi M, Laviniki V, Bassani J, Kunert H, Carvalho D, Wilsmann DE, et al. Antimicrobial Resistance in Campylobacter jejuni Isolated from Brazilian Poultry Slaughterhouses. Braz J Poult Sci. 2020;22 [Google Scholar]
- 35.Zhang X, Tang M, Zhou Q, Zhang J, Yang X, Gao Y. Prevalence and characteristics of Campylobacter throughout the slaughter process of different broiler batches. Front Microbiol. 2018;9:2092. doi: 10.3389/fmicb.2018.02092. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Suman Kumar M, Ramees T, Dhanze H, Gupta S, Dubal Z, Kumar A. Occurrence and antimicrobial resistance of Campylobacter isolates from broiler chicken and slaughter house environment in India. Anim Biotechnol. 2021:1–9. doi: 10.1080/10495398.2021.1953514. [DOI] [PubMed] [Google Scholar]
- 37.Wei B, Cha S-Y, Yoon R-H, Kang M, Roh J-H, Seo H-S, et al. Prevalence and antimicrobial resistance of Campylobacter spp. isolated from retail chicken and duck meat in South Korea. Food Control. 2016;62:63–8. [Google Scholar]
- 38.El-Naenaeey E-s, Abd El-Hamid M, Khalifa E. Prevalence and Antibiotic Resistanc Patterns of Campylobacter Species Isolated from Different Sources in Eygpt. J Microbiol Biotechnol. 2021;10(6):3723. [Google Scholar]
- 39.Mansour AO, Al-Jbouri SA, Mansour H. Antimicrobial resistance pattern and RAPD profile of Salmonella Ohio isolated from broiler farms in Al-Najaf and Al-Muthana provinces. Kufa J Vet Med Scien. 2013;4(2):18–30. [Google Scholar]