Skip to main content
Download PDF

Campylobacter prevalence from food, animals, human and environmental samples in Iran: a systematic review and meta-analysis

BMC Microbiology volume 23, Article number: 126 (2023) Cite this article

Abstract

Background

Campylobacter regarded as a major cause of foodborne gastroenteritis in humans. The present study aimed to determine the prevalence of campylobacter in food, animal and human samples of Iran.

Results

Quantitative synthesis was performed from 119 articles. White meat had the highest pooled prevalence of Campylobacter spp. (43.9%). Pooled prevalence of 7.9% and 5.5% for Campylobacter, respectively, were determined for red meat and eggs from Iran. Campylobacter was seen in 14.9% of environmental samples and 8.4% of human samples. In most of the samples C. jejuni had higher frequency than C. coli. Most of the isolated Campylobacter harbored several of the known virulence related genes of this pathogen.

Conclusion

Chicken was identified as the Campylobacter reservoir. As such preventive strategies in all stages of poultry production until consumption are necessary to control foodborne human infection with Campylobacter in Iran.

Peer Review reports

Background

Campylobacter species are gram-negative bacteria with different morphologies (from spiral to curved, or rod-shaped) [1]. They have single polar flagellum, bipolar flagella, or no flagellum, depending on the species. It has been reported that at least 12 species of Campylobacter cause human disease, the most common of which are Campylobacter jejuni and Campylobacter coli [2].

Many countries around the world recognize C. jejuni (~ 90%) and C. coli (~ 10%) as the major causative agents of human campylobacteriosis whose symptoms include diarrhea that occasionally is bloody, abdominal pain, and fever [3]. Rarely, serious long-term complications occur such as peripheral neuropathies, reactive arthritis, and Miller Fisher syndrome. Infection caused by C. jejuni is the most common reason of neurological sequelae [3]. Campylobacter is a zoonotic pathogen and its most common source is poultry [4]. In addition, contaminated water and food products, such as unpasteurized milk and contaminated fresh produce, are also known as other sources of Campylobacter infections [5]. Campylobacter infection can also occur from direct contact with infected animals, which usually carry the bacteria asymptomatically [4, 6].

According to recent data, there has been a rise in the global incidence of campylobacteriosis in most countries, although there is incomplete data from Asia, and the Middle East [7]. There is no comprehensive data on the prevalence of Campylobacter at the national level. This systematic review was conducted to provide comprehensive evidence on the prevalence of Campylobacter in human, animal, and food in Iran by using a systematic review and meta-analysis based method. Results of this study will serve as data that can be used for the prevention and control of Campylobacter infections in the country as well as guide to identify the research gaps.

Results

Overall a total of 536 articles were identified through PubMed, Scopus, and Web of Science, and 72 additional articles were identified through Google scholar, SID, and hand-based searching for the prevalence of Campylobacter species. Figure 1 illustrates the method applied for selecting eligible studies. 582 articles remained after removing duplicates. Based on the eligibility criteria, 457 articles were excluded. A further 5 full-text articles were excluded due to the following reasons Review (1), Case report (1), Abstract (1), confused text/incomprehensible data and duplicate data (1), Non-available full-text (1). Finally, 119 articles were included in the quantitative synthesis. Table 1 presents the detailed characteristics of every included study.

Fig. 1
figure 1

Diagram of identification and selection of studies for inclusion in the review

Full size image
Table 1 Characteristics of the included study
Full size table

Prevalence/proportion of Campylobacter spp. in meat/animal products and environment of Iran

An overview showing the pooled Campylobacter spp. prevalence data generated from Iranian meat (92 studies), environment (6 studies), fecal (79 studies) and animal product sample (44 studies) categories generated using the random effects model is provided in Fig. 2. The highest prevalence of Campylobacter spp. has been observed in white meat (43.9%) from 55 studies among the meat and animal products that was reported in different studies from 0 to 90%. Campylobacter spp. prevalence in white meat was higher for chicken (48.6%) than other types of poultry meat (33.9%). Within the red meat category by 37 studies, Campylobacter spp. was detected at an overall pooled prevalence of 7.9% (Table 2), which was reported from 0 to 24% in the literature. Campylobacter contamination in this category was mostly prevalent in buffalo (13.5%), followed by goat and sheep (8.6%), cattle (8.4%) and camel (2.5%) meat. While among animal products eggs were found to have a 5.5% prevalence of Campylobacter spp. contamination, with a high rate of contamination prevalence being observed for chicken eggs (9.9%) in eight studies compared to eggs of other types of poultry (4.2%) from 24 studies. The prevalence of Campylobacter spp. contamination detected among environmental samples was 14.9%. Vegetables were constituted environmental samples that showed highest prevalence (19.4%) of Campylobacter contamination. Water and sewage samples had prevalence of 15.4% and 7.4%, respectively. As the I2 heterogeneity index was more than 50, there was heterogeneity in the included studies.

Fig. 2
figure 2

Forest plot of pooled prevalence/proportion of Campylobacter spp. in white and red meat, product of animal, feces and environmental samples of Iran

Full size image
Table 2 Pooled prevalence/proportion of Campylobacter spp. in samples
Full size table

Prevalence/proportion of Campylobacter spp. in fecal samples

Literature review of 79 studies that investigated the fecal samples in animal [60] and human [34] revealed that pooled proportion of Campylobacter spp. was 18.7% in fecal samples. Among food animals, poultry had the highest contamination of fecal samples (46.8%). Domestic and wild animal had 21% and 14.1% contamination of Campylobacter spp. (Table 2). A proportion of 8.4% of human samples were positive regarding Campylobacter spp.

Prevalence/proportion of Campylobacter spp. by place of sampling

Table 3 presents an overview from the meta-analysis of Campylobacter spp. prevalence from Iran based on sampling places. Poultry feces (61.9%) and white meat (47.2%) were determined to have the highest Campylobacter spp. prevalence at the slaughterhouse. This was followed by white meat at market (42.6%) and farm (40%) levels. The lowest pooled prevalence of Campylobacter spp. was observed for milk sampled at farm (1%) and market (3.3%) levels, eggs sampled at market (5.4%) and red meat sampled at slaughterhouse (6.2%) levels. Campylobacter spp. prevalence in white and red meat, and milk samples at markets (sampled from retails, supermarkets and butcher’s) was higher than at farms (Table 3). Considerable proportions of wild animal (prevalence of 25.4%) and dog and cat feces (prevalence of 20.4%), were found to be contaminated with Campylobacter spp..

Table 3 Pooled Prevalence/proportion of Campylobacter spp. by sampling place
Full size table

Prevalence/proportion of C. jejuni and C. coli

As the C. jejuni and C. coli are the main causative agents of human campylobacteriosis, the pooled prevalence of these two species was determined in Iran samples. Most of the studies reported the prevalence of C. jejuni and C. coli in their samples. C. jejuni had higher pooled prevalence/proportion than C. coli in all of the obtained samples except for those derived from vegetables. Sewage (100%) (one study), milk (86.6%) (7 studies), human feces (83.3%) (33 studies) and water (82.8%) (3 studies) samples had the most frequent contaminations with C. jejuni (Fig. 3). Pooled C. jejuni prevalence in white meat (54 studies), egg (28 studies), poultry feces (19 studies) and red meat (35 studies) was 68.7%, 65.5%, 65.2% and 62.7%, respectively. Vegetable (2 studies) samples had the least pooled prevalence of C. jejuni (28%). On the other hand the highest pooled prevalence of C. coli was reported in vegetable samples (72%) followed by egg (33%) and red meat (24.1%) samples. Pooled prevalence of C. coli was zero (95%CI: 0–84.2%) in sewage samples (Fig. 3).

Fig. 3
figure 3

Pooled prevalence/proportion of C. jejuni and C. coli from literature in Iran based on the different categories. Error bars show the 95% confidence interval

Full size image

Pooled proportion of virulence genes in Campylobacter spp.

Despite the high number of studies that reported the prevalence of Campylobacter spp., a limited number of them investigated the virulence genes required for pathogenesis. CdtA, cdtB, cdtC, cadF and pldA had the highest number of investigated studies. Figure 4 shows the proportion of virulence genes in Campylobacter spp. cadF (97%) had the highest pooled prevalence in Campylobacter spp. in 28 studies, followed by racR (93.8%) (3 studies) and flaA (91.3%) (17 studies). VirB11 had the least prevalence (0%) in the Campylobacter spp. in 11 investigated studies. A total of 31% of Campylobacter spp. contained wlaN in 7 studies. With the sensitivity analysis, it was found that one of the studies pulls the results towards itself. The virB11 gene has the greatest impact on heterogeneity.

Fig. 4
figure 4

Pooled proportion of virulence genes in Campylobacter spp. isolates in Iran

Full size image

Discussion

Campylobacter spp. are regarded as the commonest cause of bacterial human gastroenteritis around the world [121]. In the present study, we tried to determine the prevalence of Campylobacter spp. in the food, animal and human samples of Iran based on systematic review of studies published from the country. Our findings showed that in Iran, white meat including, chicken and poultry accounts for the highest pooled prevalence of Campylobacter spp. These results are consistent with high average Campylobacter contamination prevalence that has also been observed for broiler chicken (36.7%) and turkey (11.0%) meat in Europe as reported by the European Food Safety Authority [122]. Campylobacter spp. (33.3%) represented the second most prevalent bacterial contamination of poultry meat based on a systematic review of European surveys [123]. As much as 48.6% of chicken and 23% of other poultry meat samples in Europe were contaminated with Campylobacter spp. [123]. Frequency of Campylobacter spp. contamination in chicken was reported as 99.5% in Italy, 93.7% in Northern Ireland, 84% in Ireland, 82% in Switzerland, 56% in Turkey, 53% in Spain, 51% in Austria, 50% in Poland, 14.9% in Sweden, and 9.7% in Romania [123]. In Portugal 40.3% of fresh broiler meat samples were reported to be contaminated with Campylobacter spp. [124]. Our analysis in this review shows that about 76% of broiler flocks in Shiraz, Iran were positive for Campylobacter. C. jejuni accounted for 22% whereas C. coli for 32% of the Campylobacter positive chicken samples [2]. The current study revealed a higher prevalence of C. jejuni than C. coli in white meat of Iran. Poultry carcasses had 35.37% and 19.82% prevalence of C. jejuni and C. coli contaminations, respectively from the slaughterhouses of Jahrom-Iran [20]. Campylobacter was recovered from 49.2% of poultry liver, 42.8% of gizzard 33.3% of heart and 25.4% of meat from poultry slaughterhouses at West Azerbaijan, Iran [30]. The quail meat had the highest contamination (68.4%) with Campylobacter spp. followed by chicken (56.1%), turkey (27.4%) and ostrich meat (11.7%). The high contamination of quail meat could be due to handling in slaughtering and packaging procedure that leads to higher cross–contamination [4]. The total prevalence of Campylobacter spp. in poultry meat sampled from Isfahan was 47.1% [4]. Meanwhile about 55.4% of hen carcasses sampled in processing plant of Ahvaz, Iran, were contaminated with Campylobacter spp. [38]. Turkey samples had contamination with Campylobacter spp. (62.1%) [39]. Duck samples were more contaminated (39.2%) than goose samples (26.1%) [74]. Hen liver had the highest frequency of Campylobacter spp. (63.6%), then was turkey (40%) and ostrich liver (16.7%) [88]. Liver was more contaminated with Campylobacter spp. than meat [104]. Recovery of Campylobacter was more in chicken (63%) than beef (10%) [110]. Sheep meat (3.10%) was the most contaminated in the meat samples followed by chicken (2.40%), beef (1.80%), and buffalo meat (1.10%) from Khuzestan. 81.30% of the isolates were C. jejuni and 18.70% were C. coli [26]. Campylobacter was detected in 49.5% of chicken and 8% of beef samples [28]. Lamb meat had the highest prevalence (12%) of Campylobacter spp. followed by goat (9.4%), beef (2.4%) and camel meat (0.9%) [36] in Isfahan and Yazd, which was according to the present study. Higher contamination of lamb and goat meat revealed the effect of manual skinning, evisceration and processing in abattoir and inadequate hygiene in transport, storage and cutting of meat in local butcheries. Lower rate of contamination of camel milk may be related to high number of homogenic bacteria in rumen of camel and H2 accumulation that leads to destroying of campylobacter [118].

In a study that examined individual unpasteurized bovine and ovine milk samples from Zanjan, Iran, Haghi et al. [15] detected no Campylobacter contamination, which was in contrast to most of other studies covered in the current meta-analysis and it could be due to that other studies examined bulk milk, but Haghi et al. investigated individual milk. Campylobacter spp. isolated from 2.5% to 12.5% of milk samples in Mazandaran, Isfahan and Mashhad. C. jejuni was detected in 2.5% to 13.88% of these milk samples [5, 54, 77, 79]. Results of the current study showed 5.5% detection of Campylobacter spp. in eggs. Another study showed 7% contamination of eggshell of hen, 5% of duck’s eggshell, 3.3% of goose, 2.5% of ostrich, 4.2% of partridge, 5% of quail and 3.8% of turkey’s eggshell to Campylobacter spp. [22]. Prevalence of C. jejuni (6.3%) was more than C. coli (1.3%) in avian eggs which was according to present study. Safaei et al. [41] observed no C. jejuni in table eggs. 18.67% to 31.6% of eggshell were contaminated with Campylobacter spp. [83, 101].

Examination of cecal contents of poultry conducted in Kurdistan revealed that 55% of samples were contaminated with Campylobacter spp. that included C. jejuni (86.2%) and C. coli (13.7%) [13]. Similar prevalence levels have also been reported in Iran based on literature reviewed here that found C. jejuni is more frequent than C. coli in poultry feces. Khoshbakht et al. [23] reported 67.8% of Campylobacter spp. in cattle and sheep fecal samples of Shiraz, which was higher than current study. C. jejuni and C. coli were seen in 78.5% of the samples simultaneously. Moreover, 2.9% and 12.6% of the samples were positive for C. coli and C. jejuni, respectively [23]. Prevalence studies conducted in Isfahan detected Campylobacter spp. in 10%, 8%, 5.3% and 4% of sheep, goat, cattle and camel feces [34]. Salari et al. (2020) observed no C. jejuni in Crested lark [42]. About 33% of pet bird feces were contaminated with Campylobacter spp. [61]. C. jejuni was detected in 48.62% of bird feces [27]. 52.3% of Persian fallow deer fecal samples which were collected from Dasht-e-Arzhan located in southwest of Iran, were contaminated with Campylobacter spp. [80], which was higher than the present study. Most of the studies reported higher prevalence of C. jejuni than C. coli in the foodstuffs [4, 26, 28, 30, 31, 35, 36, 38, 39, 44, 51, 55, 56, 60, 83, 85, 93, 99, 101, 104] and fecal samples [13, 61, 64, 65, 70, 74, 75].

Among environmental samples examined from northern Iran, the prevalence of Campylobacter spp. was higher in river water (36.92%) than fecal samples of poultry (34.88%), cow (28.57%), horse (20%) and sheep (9%) origin. The lowest contaminated environmental samples were those of sewage (7.4%) origin [66]. A study that have examined Caspian Sea’s water reported a Campylobacter spp. contamination prevalence of 2.66% [67]. In the investigation of vegetable samples, 15% of mushrooms in Shahrekord had Campylobacter spp. contamination [105]. Campylobacter spp. was detected in 3.5% of leafy vegetables marketed in Tehran [115]. These different reported rate of contamination could be due to the difference of geographical location and season of sampling, type and number of the samples, method of isolation, and different sanitary situation on farms and slaughterhouses [49, 74].

Our current study found that human diarrheal samples examined from Iran had a pooled Campylobacter spp. prevalence of 8.4%. Studies from central Iran reported that 33% of infectious diarrheal samples were positive for C. jejuni [8]. Among acute diarrhea samples examined in Tehran, Campylobacter spp. were detected in 8.6% of the samples of which 69.5% were C. jejuni and 24.5% was C. coli [16]. Jafari et al., [6] studied the prevalence of Campylobacter spp. in children under five years of age with acute diarrhea in Tehran. They found campylobacter in 5.5% of patients, equal to 10.8% of all isolated bacteria. In Shiraz ~ 9.6% of acute diarrhea samples were positive for C. jejuni [17]. 4% of fecal samples were contaminated with Campylobacter spp. [46]. 9.8% of diarrheic children was positive for C. jejuni [63]. C. jejuni was the major species recovered from human samples [122].

Pathogenesis of Campylobacter was associated with some virulence genes. cadF, flaA, and ciaB genes are essential virulence factors for adhesion and colonization of Campylobacter to epithelial cells in human intestine [68]. Some studies observed 100% prevalence of cadF virulence gene in C. jejuni [14, 24, 62, 68, 76] and C. coli isolates [24, 68] which was agreed with the current study. The CDT toxin leads to cell cycle arrest and promotes DNA damage; so, its presence is related with the severity of the campylobacteriosis [68]. Prevalence of cdtA, cdtB, cdtC, pldA, and iamA genes were 97%, 97%, 96%, 72%, and 60%, respectively in the isolates [14], which was higher than the current study. Prevalence of cdtA, cdtB, cdtC, racR and pldA was observed 100% in some studies [24, 25, 62, 68, 69, 76]. VirB11 gene was not detected in any of the strains [5, 24] that was according to present study and could be related to the plasmid nature of this gene [5]. Guillain–Barre’ and Miller-Fischer syndromes are associated with wlaN, cgtB genes and waaC gene [125]. Prevalence of other genes including iamA, and wlaN, was reported as 81.11%, and 82.22%, respectively [24], which was higher than current meta-analysis. Frequency of cgtB genes was observed as 22.22% [24] that was lower than present study. Frequency of ciaB was reported in 76.92% of poultry, 55.56% of cow and 100% of sheep fecal samples [25]. pldA and cgtB were detected in raw chicken Campylobacter isolates in Shiraz as 65.4% and 15.4%, respectively [62]. Prevalence of dnaJ was from 11 to 100% in different samples [69]. WaaC was detected in 100% of food isolates of C. jejuni and 75.6% of C. coli [5]. Campylobacter food isolates carried most of the virulence genes essential for pathogenesis that shows the high risk of these isolates for human.

Prevalence of Campylobacter spp. contamination was higher at market than farm level in Iran as determined in the present study, which is similar to observations from previous studies conducted in other countries [123]. Gonçalves-Tenório et al. [123] reported higher prevalence of Campylobacter spp. (44.3%) contamination at retail level than at the end-processing (30.7%) stage in poultry meat. Campylobacter spp. are able to colonize and attach to tissues of poultry during processing [126]. Carcass processing in the slaughterhouse including, scalding, washing and cooling was found not to decrease the level of Campylobacter spp. contamination of poultry meat [127]. Freezing significantly decreased chicken contamination with Campylobacter spp. during processing of poultry carcasses from 80 to 30% [73]. Washing reduced the contamination of sheep carcass from 10% after hiding to 8% after washing [106]. Since farms are considered as the initial site of contamination with Campylobacter, most preventive strategies must therefore be implemented at farm level by increasing of biosecurity and enhancing monitoring [128]. The higher contamination observed at market level may be due to uncontrolled temperature during transport of meat [5].

Poultry are regarded as a major source of this organism due to their carriage of Campylobacter spp. in the intestinal tract [127]. Similarly we also found here that poultry samples in Iran including meat and feces are associated with higher Campylobacter spp. contamination. The handling and preparation of broiler meat led to cross-contamination of poultry meat and is considered as contributing cause for one-third of human campylobacter infection in Europe while the remaining cases are related to the self-contamination of chicken with Campylobacter as the reservoir of the organism [122]. Establishing if such a link also exists in Iran is rather difficult due to the fact that there is currently neither notification nor investigation of food vehicles of human campylobacteriosis.

Conclusion

In conclusion the current systematic review and meta-analysis of Campylobacter prevalence shows that chicken has great concern for Campylobacter carriage in Iran. This must be considered in preparation of undercooked poultry such as barbecue. Most of the isolated Campylobacter carried virulence associated genes that show their potential pathogenicity. Since our analysis showed that the gastrointestinal tract and slaughtering facilities are among the main sources of Campylobacter contamination for poultry meat in Iran, implementing preventive and corrective actions at several stages mainly at farm level is very vital. Implementing control strategies specifically for this pathogen will have a remarkable impact on its incidence and production of safer meat for consumers. Moreover, consumer education in hand hygiene, sanitation of surfaces prior to and after handling meat, separation of raw and cooked meat and checking the temperature of refrigerator is also needed to reduce contamination and infections with this pathogen.

Methods

Search strategy

A systematic search was performed in PubMed, Scopus, and Web of Science electronic databases in papers that were published from November of 2021 to the end of January 2022. The search keyword was “Campylobacter coli “ or “Campylobacter jejuni” combined with the following terms: “Food”, “Animal”, “Chicken”, “Poultry”, “Meat”, “Beef”, “Lamb”, “Fish”, “Milk”, “Dairy”, “Egg”, “Sheep”, “Goat”, “Avian”, “Cow”, “Cattle”, “Human”, “Feces”, “Diarrhea”, “Gastroenteritis “ and “Iran” (Supplementary file). Handmade search was performed in Google Scholar and scientific information database (SID). PRISMA guidelines were used to perform the systematic reviews.

Selection criteria and quality assessment

Selection of studies were performed by these inclusion criteria: research studies including original article either published or in press; studies with a cross-sectional design to detect Campylobacter on the samples based on culture or PCR; had a known sample size; and studies with available full-text. Title and abstracts of the searched papers were assessed to identify articles that matched with the inclusion criteria. In some circumstances full texts were evaluated. The exclusion criteria include articles that did not follow standard methods, duplicate articles and reports, studies with unclear or incomprehensible text and analysis, articles that did not report the exact sample size and number /percent of Campylobacter. Positive samples Reviews; letters or editorial articles without original data were also excluded. Quality assessment of the eligible studies were performed by Joanna Briggs Institute [129]. Articles which gained 6 score (from 10) were eligible for data extraction. When two reviewers (EA and TZ) were disagreed about an article, seek the opinion of third reviewer (PS). Duplicates articles were removed by help of Endnote reference manager and also some of them were found by manual check.

Data extraction

Data extraction forms were designed in Microsoft Excel. Articles that obtained more than 60% of quality score were eventually included in the analysis as they were meet 6 out of 10 criteria of Joanna Briggs checklist. Following information was collected from the included studies: the first author’s name, date of publication, study design, study location, number of samples, source of samples (animal, human and environment), sample group (meat, food product?, feces and environment) and type of samples (human, domestic animal, wild animal, poultry, white meat, red meat, milk, egg, water, sewage, vegetable), sample species (chicken, poultry white meat, cattle, goat, sheep, camel and other red meat, hen egg and poultry egg), place of sampling (hospital, pet clinic, slaughterhouse, farm, market and environment), diagnostic technique (Culture, PCR, culture and PCR), prevalence of Campylobacter spp., C. jejuni, C. coli, virulence factors and quality score.

Statistical analysis

In this study, the data analysis was done with STATA 14 software (STATA Corp., College Station, Texas) with metaprop command. A random effect model was applied to determine the pooled prevalence and 95% Confidence interval of Campylobacter spp.. A forest plot was used to calculate the pooled prevalence with 95% confidence intervals. Statistical heterogeneity among studies was evaluated by computing I2, Cochran’s Q. 25%, 50%, and 75% of I2 values are classified as low, medium, and high heterogeneity, respectively. A subgroup analysis, sensitivity analysis, and meta-regression were performed on the basis of publication year, and type of sampling to evaluate sources of heterogeneity.

Availability of data and materials

Data are available from the corresponding author on reasonable request.

Abbreviations

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

TZ:

Tayebeh Zeinali

SMR:

Seyed Mohamad Riahi

EA:

Elham Ansarifar

WHO:

World health organization

SD:

Standard deviation

PCR:

Polymerase chain reaction

Fig:

Figure

References

  1. Mobaien A, Moghaddam F, Talebi S, Karami A, Amirmoghaddami H, Ramazani A. Studying the prevalence of Campylobacter jejuni in adults with gastroenteritis from northwest of Iran. Asian Pacific J Trop Dis. 2016;6(12):957–60.

    Article  Google Scholar 

  2. Ansari-Lari M, Hosseinzadeh S, Shekarforoush SS, Abdollahi M, Berizi E. Prevalence and risk factors associated with campylobacter infections in broiler flocks in Shiraz, southern Iran. Int J Food Microbiol. 2011;144(3):475–9.

    Article  PubMed  Google Scholar 

  3. Rastyani S, Alikhani MY, Sedighi I, Kazemi S, Kohan HF, Arabestani MR. Campylobacter jejunia and Campylobacter coli in Children With Acute Diarrhea in Health Centers of Hamadan. Iran Avicenna J Clin Microb Infec. 2015;2(4): e29791.

    Article  Google Scholar 

  4. Rahimi E, Tajbakhsh E. Prevalence of campylobacter species in poultry meat in the esfahan city. Iran Bulgarian J Vet Med. 2008;11(4):257–62.

    Google Scholar 

  5. Raeisi M, Khoshbakht R, Ghaemi EA, Bayani M, Hashemi M, Seyedghasemi NS, et al. Antimicrobial Resistance and Virulence-Associated Genes ofCampylobacterspp. Isolated from Raw Milk, Fish, Poultry, and Red Meat. Microbial Drug Resist (Larchmont, NY). 2017;23(7):925–33.

  6. Jafari F, Garcia-Gil LJ, Salmanzadeh-Ahrabi S, Shokrzadeh L, Aslani MM, Pourhoseingholi MA, et al. Diagnosis and prevalence of enteropathogenic bacteria in children less than 5 years of age with acute diarrhea in Tehran children’s hospitals. J Infect. 2009;58(1):21–7.

    Article  CAS  PubMed  Google Scholar 

  7. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global Epidemiology of Campylobacter Infection. Clin Microbiol Rev. 2015;28(3):687–720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Abbasi E, van Belkum A, Ghaznavi-Rad E. Quinolone and Macrolide-Resistant Campylobacter jejuni in Pediatric Gastroenteritis Patients from Central Iran. Microb Drug Resist. 2019;25(7):1080–6.

    Article  CAS  PubMed  Google Scholar 

  9. Abdi-Hachesoo B, Khoshbakht R, Sharifiyazdi H, Tabatabaei M, Hosseinzadeh S, Asasi K. Tetracycline resistance genes in Campylobacter jejuni and C. coli isolated from poultry carcasses. Jundishapur J Microbiol. 2014;7(9):e1229.

  10. Abdollahpour N, Zendehbad B, Alipour A, Khayatzadeh J. Wild-bird feces as a source of Campylobacter jejuni infection in children’s playgrounds in Iran. Food Control. 2015;50:378–81.

    Article  Google Scholar 

  11. Akramzadeh N, Ramezani Z, Ferdousi R, Akbari-Adergani B, Mohammadi A, Karimian-Khosroshahi N, et al. Effect of chicken raw materials on physicochemical and microbiological properties of mechanically deboned chicken meat. Vet Res Forum. 2020;11(2):153–8.

    PubMed  PubMed Central  Google Scholar 

  12. Alborzi A, Aelami MH, Astaneh B, Pourabbas B, Farshad S, Kalani M, et al. Is Escherichia coli O157:H7 a common pathogen in children with bloody diarrhea in Shiraz, Iran? Gut Pathogens. 2008;50(4):349–53.

    Google Scholar 

  13. Azizian K, Hasani A, Shahsavandi S, Ahangarzadeh Rezaee M, Hosseinpour R, Alizadeh H. Campylobacter jejuni and Campylobacter coli in cecum. Trop Biomed. 2018;35(2):423–33.

    CAS  PubMed  Google Scholar 

  14. Divsalar G, Kaboosi H, Khoshbakht R, Shirzad-Aski H, Ghadikolaii FP. Molecular typing and virulence gene profiles of Campylobacter jejuni isolated from human, animals, and meat in northern Iran. Revue De Med Vet. 2019;170(7–9):129–35.

    CAS  Google Scholar 

  15. Haghi F, Zeighami H, Naderi G, Samei A, Roudashti S, Bahari S, et al. Detection of major food-borne pathogens in raw milk samples from dairy bovine and ovine herds in Iran. Small Rumin Res. 2015;131:136–40.

    Article  Google Scholar 

  16. Hamidian M, Sanaei M, Azimi-Rad M, Tajbakhsh M, Dabiri H, Zali MR. fla-typing, RAPD analysis, isolation rate and antimicrobial resistance profile of Campylobacter jejuni and Campylobacter coli of human origin collected from hospitals in Tehran. Iran Ann Microbiol. 2011;61(2):315–21.

    Article  CAS  Google Scholar 

  17. Hassanzadeh P, Motamedifar M. Occurrence of Campylobacter jejuni in Shiraz, Southwest Iran. J Cell Physiol. 2007;16(1):59–62.

    Google Scholar 

  18. Hoseinpour F, Foroughi A, Nomanpour B, Nasab RS. Identification and differentiation of Campylobacter species by high-resolution melting curve analysis. Microb Pathog. 2017;108:109–13.

    Article  PubMed  Google Scholar 

  19. Jafari F, Shokrzadeh L, Hamidian M, Salmanzadeh-Ahrabi S, Zali MR. Acute diarrhea due to enteropathogenic bacteria in patients at hospitals in Tehran. Jpn J Infect Dis. 2008;61(4):269–73.

    Article  PubMed  Google Scholar 

  20. Jahromi RR, Moradi F, Erfanian S, Faraji SZ, Zargar MF, Haghighi BR, et al. Molecular Analyses of the Prevalence of Campylobacter Detected from the Poultry Meat and its Byproducts. Ambient Science. 2019;6(2):7–10.

    Google Scholar 

  21. Jamshidi A, Bassami MR, Farkhondeh T. Isolation and identification of Campylobacter spp. and Campylobacter coli from poultry carcasses by conventional culture method and multiplex PCR in Mashhad, Iran. Iran J Vet Res. 2008;9(2):132–7.

  22. Jonaidi-Jafari N, Khamesipour F, Ranjbar R, Kheiri R. Prevalence and antimicrobial resistance of Campylobacter species isolated from the avian eggs. Food Control. 2016;70:35–40.

    Article  CAS  Google Scholar 

  23. Khoshbakht R, Tabatabaei M, Hoseinzadeh S, Raeisi M, Shirzad Aski H, Berizi E. Prevalence and antibiotic resistance profile of thermophilic Campylobacter spp. of slaughtered cattle and sheep in Shiraz, Iran. Vet Res Forum. 2016;7(3):241–6.

  24. Khoshbakht R, Tabatabaei M, Hosseinzadeh S, Shekarforoush SS, Aski HS. Distribution of nine virulence-associated genes in Campylobacter jejuni and C. coli isolated from broiler feces in Shiraz, Southern Iran. Foodborne Pathogens Dis. 2013;10(9):764–70.

  25. Mahmoodipour H, Baserisalehi M, Emami A. Molecular detection of virulence genes involved in adherence, colonization, invasion and cytotoxin production in campylobacter jejuni and campylobacter coli isolated from poultry, cow and sheep faeces. Acta Medica Mediterranea. 2017;33(5):763–8.

    Google Scholar 

  26. Maktabi S, Ghorbanpoor M, Hossaini M, Motavalibashi A. Detection of multi-antibiotic resistant Campylobacter coli and Campylobacter jejuni in beef, mutton, chicken and water buffalo meat in Ahvaz. Iran Vet Research Forum. 2019;10(1):37–42.

    Google Scholar 

  27. Malekian M, Shagholian J, Hosseinpour Z. Pathogen Presence in Wild Birds Inhabiting Landfills in Central Iran. EcoHealth. 2021;18(1):76–83.

    Article  PubMed  Google Scholar 

  28. Soltan Dallal MM, Doyle MP, Rezadehbashi M, Dabiri H, Sanaei M, Modarresi S, et al. Prevalence and antimicrobial resistance profiles ofSalmonellaserotypes, CampylobacterandYersiniaspp. isolated from retail chicken and beef, Tehran, Iran. Food Control. 2010;21:388–92.

  29. Sharifi S, Bakhshi B, Najar-Peerayeh S. Significant contribution of the CmeABC Efflux pump in high-level resistance to ciprofloxacin and tetracycline in Campylobacter jejuni and Campylobacter coli clinical isolates. Ann Clin Microbiol Antimicrob. 2021;144(3):475–9.

    Google Scholar 

  30. Nassiri D, Razavilar V, Motalebi A. Occurrence of Campylobacterin Poultry Meat and Edible Offal’s in the northwest of Iran. Int J Adv Biotechnol Res. 2016;7(1):351–7.

    Google Scholar 

  31. Nouri Gharajalar S, Hassanzadeh P, Hosseinali NN. Molecular detection of Campylobacter species and Cytolethal distending toxin isolated from chicken livers in Tabriz. Comp Immunol Microbiol Infect Dis. 2020;71: 101474.

    Article  PubMed  Google Scholar 

  32. Bakhshi B, Kalantar M, Rastegar-Lari A, Fallah F. PFGE genotyping and molecular characterization of Campylobacter spp. isolated from chicken meat. IJVR. 2016;17(3):177–83.

  33. Sarhangi M, Bakhshi B, Peeraeyeh SN. High prevalence of Campylobacter jejuni CC21 and CC257 clonal complexes in children with gastroenteritis in Tehran, Iran. BMC Infect Dis. 2021;21(1):108.

  34. Rahimi E, Alipoor-Amroabadi M, Khamesipour F. Investigation of prevalence of thermotolerant Campylobacter spp. in livestock feces. Canadian J Anim Sci. 2017;97(2):207–13.

  35. Rahimi E, Ameri M. Antimicrobial resistance patterns of Campylobacter spp. isolated from raw chicken, turkey, quail, partridge, and ostrich meat in Iran. Food Control. 2011;22(8):1165–70.

  36. Rahimi E, Ameri M, Kazemeini HR. Prevalence and Antimicrobial Resistance of Campylobacter Species Isolated from Raw Camel, Beef, Lamb, and Goat Meat in Iran. Foodborne Pathog Dis. 2010;7(4):443–7.

    Article  CAS  PubMed  Google Scholar 

  37. Rahimi E, Kazemeini HR, Safaei S, Allahbakhshi K, Momeni M, Riahi M, et al. Detection and identification of Campylobacter spp. from retail raw chicken, turkey, sheep and goat meat in Ahvaz, Iran. Afr J Microbiol Res. 2010;4(15):1620–3.

  38. Rahimi E, Momtaz H, Ameri M, Ghasemian-Safaei H, Ali-Kasemi M. Prevalence and antimicrobial resistance of Campylobacter species isolated from chicken carcasses during processing in Iran. Poult Sci. 2010;89(5):1015–20.

    Article  CAS  PubMed  Google Scholar 

  39. Rahimi E, Momtaz H, Bonyadian M. PCR detection of Campylobacter sp from turkey carcasses during processing plant in Iran. Food Control. 2010;21(5):692–4.

    Article  CAS  Google Scholar 

  40. Razei A, Sorouri R, Mousavi SL, Nazarian S, Amani J, Aghamollaei H. Presenting a rapid method for detection of Bacillus cereus, Listeria monocytogenes and Campylobacter jejuni in food samples. Iran J Basic Med Sci. 2017;20(9):1050–5.

    PubMed  PubMed Central  Google Scholar 

  41. Safaei HG, Jalali M, Hosseini A, Narimani T, Sharifzadeh A, Raheimi E. The prevalence of bacterial contamination of table eggs from retails markets by Salmonella spp., Listeria monocytogenes, Campylobacter jejuni and Escherichia coli in Shahrekord, Iran. Jundishapur J Microbiol. 2011;4(4):249–53.

  42. Salari S, Jahantigh M, Jahantigh M. Investigation of Campylobacter jejuni in microbiota of Galerida cristata, trapped in Southeast of Iran. Sistan J Wildlife Biodiversity. 2020;4(2):28–33.

    Google Scholar 

  43. Torkan S, Vazirian B, Khamesipour F, Dida GO. Prevalence of thermotolerant Campylobacter species in dogs and cats in Iran. Vet Med Sci. 2018;4:296–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Shafiei A, Rahimi E, Shakerian A. Prevalence, Virulence and Anti-Microbial Resistance in Campylobacter spp. from Routine Slaughtered Ruminants, as a Concern of Public Health (Case: Chaharmahal and Bakhtiari Province, Iran). J Complement Med Res. 2020;11(1):302–15.

  45. Ghane M, Eghbali M, Baserisalehi M, Bahador N. Antimicrobial Susceptibility of Thermophilic Campylobacter spp. Isolated from Environmental Samples in Tonekabon. Int J Mol Clin Microbiol. 2011;1:21–4.

  46. Ghorbanalizadgan M, Bakhshi B, Shams S, Najar-Peerayeh S. Pulsed-field gel electrophoresis fingerprinting of Campylobacter jejuni and Campylobacter coli strains isolated from clinical specimens. Iran Int Microbiol. 2019;22:391–8.

    Article  CAS  PubMed  Google Scholar 

  47. Tabar EA, Staji H, Mahdavi A. Comparative restriction enzyme mapping of Campylobacter jejuni isolates from turkeys and broilers based on flaA flagellar gene using HpyF3I endonuclease. Folia Microbiol. 2019;64(2):189–95.

    Article  CAS  Google Scholar 

  48. Zendehbad B, Arian AA, Alipour A. Identification and antimicrobial resistance of Campylobacter species isolated from poultry meat in Khorasan province. Iran Food Control. 2013;32(2):724–7.

    Article  CAS  Google Scholar 

  49. Zendehbad B, Khayatzadeh J, Alipour A. Prevalence, seasonality and antibiotic susceptibility of Campylobacter spp. isolates of retail broiler meat in Iran. Food Control. 2015;53:41–5.

  50. Amanpour Z, Kouhsari E, Pakzad I, Kenarkoohi A, Sadeghifard N. Simultaneous molecular detection of common bacterial Enteropathogens in children with diarrhea by multiplex-PCR assay. Clin Lab. 2021;67(6):1403–8.

  51. Shahrokhabadi R, Rahimi E, Mommtaz H, Poursahebi R. Prevalence of Campylobacter jejuni and coli in sheep carcasses by using cultural and PCR methods. Zahedan J Res Med Sci. 2013;15(12):28–31.

  52. Abbasi E, Khansarinejad B, Ghaznavi rad E. Dysentery caused by macrolide and fluoroquinolone resistant Campylobacter coli in central area of Iran. Tehran Univ Med J. 2019;76(11):736–41.

  53. Ashrafganjooyi S B, N. SA. Isolation and survey for drug resistance of Campylobacter jejuni in poultry feces in Kerman. Iran J Med Microbiol. 2016;9(4):95–8.

  54. Dabiri A, Rouhi S, Nouri B, Zaboli F. Assess the prevalence rate of Campylobacter genus and Campylobacter jejuni species in raw milk collected from the Amol City by Multiplex-Polymerase Chain Reaction. J Fasa Univ Med Sci. 2016;5(4):516–25.

    CAS  Google Scholar 

  55. Babaienajadbasiri F, Haghighi Khoshkhoo P, Akbariazad G. Prevalence and antibacterial susceptibility of thermophilic campylobacter spp. In broiler chickens. J Mazandaran Univ medical Sci. 2016;26(136):185–9.

  56. Bagherpour A, Ahmadi A, Soltanialvar M. Survey of Campylobacter contamination in poultry meat and by-products in Dezful province. WALIA J. 2014;30(1):115–8.

    Google Scholar 

  57. Barati M, Taghipour A, Bakhshi B, Shams S, Pirestani M. Prevalence of intestinal parasitic infections and Campylobacter spp. among children with gastrointestinal disorders in Tehran, Iran. Parasite Epidemiol Control. 2021;13:e00207.

  58. Berizi E, Shekarforoush S, Hosseinzadeh S, Abdollahi M. Study of the contamination of broiler-chicken flocks to Campylobacter jejuni and Campylobacter coli at the end of a rearing period. J Vet Microbiol. 2017;13(1):11–9.

    Google Scholar 

  59. Aminshahidi M, Arastehfar A, Pouladfar G, Arman E, Fani F. Diarrheagenic Escherichia coli and Shigella with high rate of extended-spectrum Beta-lactamase production: two predominant etiological agents of acute diarrhea in Shiraz. Iran Microbial Drug Resistance. 2017;23(8):1037–44.

    Article  CAS  PubMed  Google Scholar 

  60. Ebrahimi Lagha F, Zeynali F, Rezazadeh Bari M, Aliakbarlou J. Isolation of campylobacter from poultry gizzards in Urmia using pcr. J Food Res (University of Tabriz). 2015;25(4):577–84.

    Google Scholar 

  61. Ehsannejad F, Sheikholmolooki A, Hassanzadeh M, Shojaei Kavan R, Soltani M. Detection of cytolethal distending toxin (cdt) genes of Campylobacter Jejuni and Coli in fecal samples of pet birds in Iran. Iran J Vet Med. 2015;9(1):49–56.

    Google Scholar 

  62. Fani F, Aminshahidi M, Firoozian N, Rafaatpour N. Prevalence, antimicrobial resistance, and virulence-associated genes of Campylobacter isolates from raw chicken meat in Shiraz. Iran Iran J Vet Res. 2019;20(4):283–8.

    CAS  PubMed  Google Scholar 

  63. Jazayeri Moghadas A, Irajian G, Kalantari F, Monem M, Salehian A, Rahbar H, et al. Prevalence of Campylobacter jejuniin diarrheic children in Semnan (Iran) Journal of Semnan University of Medical Sciences. 2008;9(4):297–300.

  64. Feizabadi MM, Dolatabadi S, Zali MR. Isolation and drug-resistant patterns of Campylobacter strains cultured from diarrheic children in Tehran. Jpn J Infect Dis. 2007;60(4):217–9.

    CAS  PubMed  Google Scholar 

  65. Ghane M, Bahador N, Baserisalehi M, Eghbali M. A comparative study on antimicrobial susceptibility of campylobacter spp. Isolates from fecal samples of domestic animals and poultry in Tonekabon and Shiraz, Iran. J Paramed Sci. 2011;2(2):21–6.

  66. Ghane M, Bahador N, Baserisalehi M. Isolation, identification and characterization of Campylobacter spp. isolates from environmental samples in North Iran. Nature Environ Poll Technol. 2010;9(4):823–8.

  67. Ghane M, Moein FG, Massoudian S. The first isolation of Campylobacter jejuni. Adv Stud Biol. 2012;4(9):407–18.

    Google Scholar 

  68. Ghorbanalizadgan M, Bakhshi B, Kazemnejad Lili A, Najar-Peerayeh S, Nikmanesh B. A Molecular Survey of Campylobacter jejuni and Campylobacter Coli Virulence and Diversity Iranian biomedical journal. 2014;18(3):158–64.

    CAS  PubMed  Google Scholar 

  69. Hamidian M, Sanaei M, Bolfion M, Dabiri H, Zali MR, Walther-Rasmussen J. Prevalence of putative virulence markers in Campylobacter jejuni and Campylobacter coli isolated from hospitalized children, raw chicken, and raw beef in Tehran. Iran Canadian J Microbiol. 2011;57(2):143–8.

    Article  CAS  Google Scholar 

  70. Harzandi N, Jamshidi S, Dezfulian M, Bahonar A, Bakhtiari A, Banihashemi K. Molecular detection and speciation of Campylobacter species in children with gastroenteritis using polymerase chain reaction in Bahonar Hospital of Karaj City. Int J Enteric Pathog. 2015;3(2):1–4.

    Article  Google Scholar 

  71. Hosseinzadeh S, Mardani K, Aliakbarlu J, Ghorbanzadehghan M. Occurrence of Campylobacter in chicken wings marketed in the northwest of Iran. Int Food Res J. 2015;22(1):41–5.

  72. Irajian GR, Jazayeri Moghadas A, Beheshti AAS, Salehian A, Monem M, Ghods F. Prevalence of campylobacter jejuni samples from patients referred to semnan public health centers in 2007. Iran J Med Microbiol. 2008;1(4):35–9.

    Google Scholar 

  73. Irannejhad A, Rahimi E, Gholami Ahangaran M. Isolation of campylobacter in different processing stage and presentation of poultry carcasses. J Food Microbiol. 2015;2(1):59–67.

  74. Jamali H, Ghaderpour A, Radmehr B, Wei KSC, Chai LC, Ismail S. Prevalence and antimicrobial resistance of Campylobacter species isolates in ducks and geese. Food Control. 2015;50:328–30.

    Article  CAS  Google Scholar 

  75. Kafshdouzan K, Ashrafi Tamai I, Pouyan S. Detection of Faecal Contamination With Campylobacter jujuni and Campylobacter coli in Urban Ducks in the North of Iran. J Vet Res. 2019;74(2):283–9.

    Google Scholar 

  76. Kalantar M, Soltan Dallal M-M, Fallah F, Yektaie F. Monitoring the virulence genes in Campylobacter coli strains isolated from chicken meat in Tehran. Iran Infect Epidemiol Microbiol. 2017;3(1):12–5.

    CAS  Google Scholar 

  77. Kazemeini H, Valizade Y, Parsaei P, Nozarpour N, Rahimi E. Prevalence of Campylobacter species in raw bovine milk in Isfahan. Iran Middle-East J Sci Res. 2011;5:664–6.

    Google Scholar 

  78. Khalili M, Mansourinajand L. Frequency of Campylobacter jejuni in Cecal Content of Kerman Poultry Farms. Iran J Biol. 2010;22(4):730–3.

    Google Scholar 

  79. Khanzadi S, Jamshidi A, Soltaninejad V, Khajenasiri S. Isolation and identification of Campylobacter jejuni from bulk tank milk in Mashhad-Iran. World Appl Sci J. 2010;9(6):638–43.

    CAS  Google Scholar 

  80. Khoshbakht R, Tabatabaei M, Aski HS, Shayegh H. Distribution of Salmonella, Arcobacter, and thermophilic Campylobacter spp. among Persian fallow deer (Dama mesopotamica) population in Dasht-e-Arzhan Wildlife refuge, southern Iran. Comparative Clin Pathol. 2015;24(4):777–81.

  81. Khosravi AD, Mehdinejad M, Shamsizadeh A, Montazeri EA, Moghaddam M. Determination of antibiotic susceptibility pattern in Campylobacter jejuni and Campylobacter coli isolated from children with acute diarrhea. Asian Biomedicine. 2011;5(5):611–8.

    CAS  Google Scholar 

  82. Mahzounieh M, Ghorbani M, Zahraei Salehi T. Identification of campylobacter spp. In apparently healthy dog's and cat's stool by multiplex pcr. J Comparative Pathobiol Iran. 2014;10(4):1101–6.

  83. Modirrousta S, Shapouri R, Rezasoltani S, Molaabaszadeh H. Prevalence of Campylobacter spp. and their Common Serotypes in 330 Cases of Red-meat, Chicken-meat and Egg-shell in Zanjan City, Iran. Infect Epidemiol. 2016;2(1):8–10.

  84. Mohammadzadeh AAM, Hakimi Alni R, Sharifi A, Gorbami M. A survey of the genus campylobacter contamination in domestic dogs using pcr technique. J Large Animal Clin Sci Res (Journal of Veterinary Medicine). 2012;6(2):25–30.

    Google Scholar 

  85. Mokhtarian DH, Mohsenzadeh M, Ghahramani M, Moshki M, Fani M. Detection and identification of Campylobacter jejuni and Campylobacter coli from poultry carcasses slaughtered in Gonabad poultry slaughterhouse. Ofogh-e-danesh GMUHS J. 2009;15(3):30–6.

    Google Scholar 

  86. Mosallanejad B, Gharibi D, Avizeh R, Abbassi R. Isolation and characterization of Campylobacter spp. in feces of companion cats in Ahvaz district by culture and PCR methods. Sci-Res Iran Vet J. 2020;16(1):92–104.

  87. Negahdari B, Shirazi MH, Malekshahi ZV, Hajikhani S, Rahmati M. Identification of Campylobacter jejuni and Campylobacter coli from diarrheic samples using PCR. Int J Health Stud. 2016;2(2):1–3.

    Google Scholar 

  88. Rahimi E, Torki Baghbadorani Z. Prevalence of Campylobacter jejuni and C. coli in poultry liver in Isfahan. VetJof IslamicAzadUniv, Garmsar Branch. 2009;5(1):1–4.

  89. Rahimi E, Shakerian A, Kazemeini HR, Goudarzi MA. Antimicrobial resistance patterns of campylobacter spp. Isolated from raw chicken, turkey, quail, partridge, ostrich, beef, sheep, goat and camel meat marketed in shahrekord. J Food Technol Nutr. 2013;10(3 (39)):95–100.

  90. Rahimi E, Momtaz H, Hemmatzadeh F. The prevalence of Escherichia coli O157: H7, Listeria monocytogenes and Campylobacter spp. on bovine carcasses in Isfahan, Iran. Iran J Vet Res. 2008;9(4):365–70.

  91. Rahimi MK, Alambeigi P, Mousavi L, Adimi P, Tayyebi Z, Masoumi M, et al. Frequency of Campylobacter jejuni in stool samples of patients with bloody diarrhea. Med Sci J Islamic Azad Univ. 2009;19(3):212–5.

    Google Scholar 

  92. Rahimi E, Alian F, Alian F. Prevalence and characteristic of Campylobacter species isolated from raw duck and goose meat in Iran. IPCBEE. 2011;9:171–5.

    Google Scholar 

  93. Rahimi E, Ameri M, Alimoradi M, Chakeri A, Bahrami AR. Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from raw camel, beef, and water buffalo meat in Iran. Comp Clin Pathol. 2013;22(3):467–73.

    Article  CAS  Google Scholar 

  94. Rahimi E, Esfahani MS. Seasonal prevalence of Campylobacter jejuni and Campylobacter coli in raw chicken meat using PCR assay. Middle East J Sci Res. 2010;6(4):329–32.

    CAS  Google Scholar 

  95. Rahimi E. Campylobacter spp. Contamination of chicken meat and by-products in shahrekord, iran. Sci-Res Iran Vet J. 2013;9(1):30–6.

  96. Rashed T, Ghanaat J, Moshafi M. The prevalence of campylobacter jejuni induced gastroenteritis in patients with diarrhea referring to Mean Reza hospital in Mashhad. Iran J Kerman Univ Med Sci. 1994;1(3):114–9.

    Google Scholar 

  97. Ranjbar R, Babazadeh D. Contact with poultry and animals increases risk of Campylobacter infections in adults of Ardabil province. Iran Univ Med. 2017;36(1):59–67.

    Article  CAS  Google Scholar 

  98. Roshanjo k, Asadpour L, Shiri Shahsavar M, Hemmati A. Prevalence of cdt Gene in Campylobacter jejuni Strains Isolated from Surface Waters of Rasht, Iran. Med Lab J. 2017;11(2):36–40.

  99. Jahromi RR, Moradi F, Erfanian S, Pourahmadi M. Evaluation of the Contamination of Poultry Carcasses with Campylobacter jejuni and Campylobacter coli in Southern Iran: A Molecular Study. Jundishapur J Health Sci. 2021;13(3): e116991.

    Google Scholar 

  100. Saadatmand A, Alikhani MY, Habibipour R, Heshmati A. Antibiotic resistance and prevalence of Campylobacter jejuni and Campylobacter coli in poultry liver. Sci J Hamadan Univ Med Sci. 2017;24(3):253–8.

    Google Scholar 

  101. Sabzmeydani A, Rahimi E, Shakerian A. Incidence and Antimicrobial Resistance of Campylobacter Species Isolated from Poultry Eggshell Samples. Egypt J Vet Sci. 2020;51(3):329–35.

    Google Scholar 

  102. Sadeghi A, Owlia P, Ganji L, Besharati S, Ahmadi F, Fani F, et al. The Frequency of Infection with Campylobacter, Its Species Diversity, and Antimicrobial Resistance in Stool Samples of Patients with Community-Acquired Gastroenteritis in Tehran. Govaresh J. 2020;25(2):93–102.

    Google Scholar 

  103. Salehi M, Shafaei E, Bameri Z, Bokaeian M, Mirzaee B, Mirfakhraee S, et al. Prevalence and antimicrobial resistance of Campylobacter jejuni. Int J Infect. 2014;1(2):e19229.

  104. Shahrokhabad R, Rahimi E, Mommtaz H. Investigation of morbidity and antibacterial resistance of campylobacter spp. Sample isolation from broilers slaughter in Rafsanjan city using basic culture method. Vet Res Biol Products (pajouhesh-va-sazandegi). 2011;91:53–8.

  105. Shakerian A. Campylobacter spp. as a potential pathogen in the edible mushrum (Agaricus mushrooms). J Food Hygiene. 2016;3(1):63–72.

  106. Shakerian A, Rahimi E, Kazemi S. Prevalence and antibiotic resistant of Campylobacter spp. Isolated from different stages of sheep slaughterhouse. J Food Hygiene. 2012;1(4):63–9.

  107. Shams S, Ghorbanalizadgan M, Haj Mahmmodi S, Piccirillo A. Evaluation of a Multiplex PCR Assay for the Identification of Campylobacter jejuni and Campylobacter coli. Infect Epidemiol Microbiol. 2017;3(1):6–8.

    Article  CAS  Google Scholar 

  108. Shirazi M, Malekshahi V, Afshar D, Ranjbar R, Hajikhani S. Drug resistance among Campylobacter jejuni strain isolated from children with diarrhea. J Babol Univ Med Sci. 2013;15(1):79–83.

    Google Scholar 

  109. Soltan Dallal MM, Monzavipour MH, Masoumi Asl H, Shirazi MH, Hajikhani S, Rajabi Z. The study of campylobacter frequency in foodborne disease outbreaks in iran. Toloo-e-behdasht. 2017;16(2):9–19.

    Google Scholar 

  110. Taremi M, Mehdi Soltan Dallal M, Gachkar L, MoezArdalan S, Zolfagharian K, Reza Zali M. Prevalence and antimicrobial resistance of Campylobacter isolated from retail raw chicken and beef meat, Tehran, Iran. Int J Food Microbiol. 2006;108(3):401–3.

  111. Tavakoli Vaskas A, Karim G, Sharifi Soltani M, Nasiri D, Porjafar H. The study of seasonal incidence of Campylobacter jejuni and Campylobacter coli in raw milks of Amol town through using M. PCR method. Innovation Food Sci Technol. 2013;4(4):81–6.

  112. Zamani Moghaddam A, Tahmasby H, Mehrabian S, Barati S, Hashemi Babaheidari SH, Safarpour M. Molecular detection of Campylobacter in domestic pigeons from shahrekord, Iran. J Vet Microbiol. 2012;7(2 (23)):63–71.

  113. Zamani Moghadam A, Tahmasby H, Khosravi Farsani M, Ghasemi M, Kiani SA. Investigation of Campylobacter infection in lovebirds in shahrekord, iran by PCR. Jentashapir J Cell Mol Biology (jentashapir journal of health research). 2013;3(4):489–94.

    Google Scholar 

  114. Ziaei N, Amir Mozafari N, Kouhsari H, Moradi A, Tabarai A, Dadgar T, et al. Prevalence of Campylobacter jejuni in Diarrhea samples in Gorgan, East north of Iran. Med Lab J. 2008;2(2):36–42.

    Google Scholar 

  115. Azimirad M, Nadalian B, Alavifard H, Negahdar Panirani S, Mahdigholi Vand Bonab S, Azimirad F, et al. Microbiological survey and occurrence of bacterial foodborne pathogens in raw and ready-to-eat green leafy vegetables marketed in Tehran, Iran. Int J Hygiene Environ Health. 2021;237:113824.

  116. Rahimi E, Momtaz H, Nozarpour N. Prevalence of Listeria spp., Campylobacter spp. and Escherichia coli O157:H7 isolated from camel carcasses during processing. Bulgarian J Vet Med. 2010;13:179–85.

  117. Basirisaehi M, Bahador N, Kapandis BP. A comparison study on antimicrobial susceptibility of Campylobacter spp. isolates from fecal samples of Domestic Animals and Poultry in India and Iran. J Biol Sci. 2007;7(6):977–80.

  118. Baserisalehi M, Bahador N, Kapadnis BP. Isolation and characterization of Campylobacter spp. from domestic animals and poultry in south of Iran. Pakistan J Biol Sci. 2007;10(9):1519–24.

  119. Dabiri H, Aghamohammad S, Goudarzi H, Noori M, Ahmadi Hedayati M, Ghoreyshiamiri SM. Prevalence and antibiotic susceptibility of Campylobacter species isolated from chicken and beef meat. Int J Enteric Pathog. 2014;2(2): e17087.

    Article  Google Scholar 

  120. Mirzaee S, Hassanzadeh M, Bashashati M, Barrin A. Campylobacteroccurrence and antimicrobial resistance in samples from ceca of commercial turkeys and quails in Tehran. Iran Int Res J Microbiol. 2011;2(9):338–42.

    Google Scholar 

  121. Cody AJ, Maiden MC, Strachan NJ, ND. M. A systematic review of source attribution of human campylobacteriosis usingmultilocus sequence typing. Eurosurveillance. 2019;24(43):1800696.

  122. EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J. 2017;15:e0507.

  123. Gonçalves-Tenório A, Nunes Silva B, Rodrigues V, Cadavez V, Gonzales-Barron U. Prevalence of Pathogens in Poultry Meat: A Meta-Analysis of European Published Surveys. Foods. 2018;7(69):foods7050069.

  124. Xavier C, Gonzales-Barron U, Paula V, Estevinho L, Cadavez V. Meta-analysis of the incidence of foodborne pathogens in Portuguese meats and their products. Food Res Int. 2014;55:311–23.

    Article  Google Scholar 

  125. Linton D, Gilbert M, P.G. Hitchen, Dell A, Morris HR, Wakarchuk WW, et al. Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipooligosaccharide of Campylobacter jejuni. Mol Microbiol. 2000;37:501–14.

  126. Mead GC. Microbiological quality of poultry meat: A review. Rev Bras Cienc Avic. 2004;6:135–42.

    Article  Google Scholar 

  127. Humphrey T, O’Brien S, Madsen M. Campylobacters as zoonotic pathogens: A food production perspective. Int J Food Microbiol. 2007;117:237–57.

    Article  PubMed  Google Scholar 

  128. Skarp CPA, Hänninen ML, Rautelin HIK. Campylobacteriosis: The role of poultry meat. Clin Microbiol Infect. 2016;22:103–9.

    Article  CAS  PubMed  Google Scholar 

  129. Munn Z, Moola S, Riitano D, Lisy K. The development of a critical appraisal tool for use in systematic reviews addressing questions of prevalence. Int J Health Policy Manag. 2014;3:123.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the research and technology deputy of Birjand University of Medical Sciences for support of this study.

Funding

We have no financial sources to disclose for the study.

Author information

Authors and Affiliations

  1. Department of Public Health, School of Health, Social Determinants of Health Research Center, Birjand University of Medical Sciences, Birjand, Iran

    Elham Ansarifar & Tayebeh Zeinali

  2. Cardiovascular Diseases Research Center, Birjand University of Medical Sciences, Birjand, Iran

    Seyed Mohamad Riahi

  3. Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland

    Taurai Tasara

  4. Department of Environmental Health, Food Safety Division, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

    Parisa Sadighara

Authors
  1. Elham Ansarifar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Seyed Mohamad Riahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taurai Tasara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Parisa Sadighara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tayebeh Zeinali
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SMR, EA, TZ and T.T. designed research; PS and TZ conducted the systematic search; SMR conducted the meta-analysis; TZ and PS extracted the data; all authors drafted the manuscript and revised the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Tayebeh Zeinali.

Ethics declarations

Ethics approval and consent to participate

The study was approved by ethical committee of Birjand University of Medical Sciences (IR.BUMS.REC.1402.061).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ansarifar, E., Riahi, S.M., Tasara, T. et al. Campylobacter prevalence from food, animals, human and environmental samples in Iran: a systematic review and meta-analysis. BMC Microbiol 23, 126 (2023). https://doi.org/10.1186/s12866-023-02879-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12866-023-02879-w

Keywords

BMC Microbiology

ISSN: 1471-2180

Contact us