Campylobacter infections in Middle Eastern children: Review article

Materials and Method

This review searched English publications over the past 14 years on Campylobacter in children across Middle Eastern countries. Using Google Scholar and PubMed, the key terms “Campylobacter” or “Campylobacter jejuni” with “Children”, “Infant”, “Pediatric”, and the name of Middle Eastern Countries were combined with various keywords such as “Prevalence”, “Incidence”, “Burden”, “Epidemiology”, “Colonization”, and “Diarrhea”, “Antibiotic Resistance”, “Antimicrobial susceptibility”.

Our inclusive criteria included research conducted during the period from 2010 to 2023, prioritizing studies that focus on children or at least 50% of their samples are children or mention the age group prevalence ([Figure 1]). According to these criteria, the search produced a total of 170 publications related to Campylobacter spp in the Middle Eastern regions. One hundred forty-three were excluded as they either focused on animals, animal products, food, or humans with a children sample size less than 50% or lacked data about children. It is important to note that this article was based on existing research and did not involve any new investigations into human or animal subjects conducted by the authors.

Discussion

Campylobacter jejuni infection in Middle Eastern children with gastroenteritis

The rate of Campylobacteriosis across human populations exhibits substantial variability, being observed in low-income countries at 1.7% to 62.7%. While, in animals, the prevalence of Campylobacter shows considerable variation, ranging from 1.2% to 80%.^[1] it has been demonstrated that the rate of Campylobacter among the human population in the Middle East ranges from 1% to 22%. ^[25], ^[26] A study conducted in Syria has demonstrated a low rate of campylobacter infection in children. The study also revealed a significant positive association between C. jejuni infection and cases of childhood diarrhea. ^[27] In addition the low prevalence of campylobacter infections also reported in Palestine and Qatar according to the available data. ^[28], ^[29] While, the moderate rates of campylobacteriosis were listed among children of Jordan,^[30] Lebanon, ^[31], ^[32] Iran, ^[33], ^[34], ^[35], ^[36], ^[37], ^[38] Iraq, ^[39], ^[40], ^[41] Oman, ^[42] and Yemen. ^[43] On other hand, high prevalence rates of pediatric campylobacteriosis reported in Egypt, ^[10], ^[44], ^[45] Israel, ^[46] and Turkey. ^[24] According to the published data, there were discrepancies in the rates of Campylobacter infections among children in the Middle East ([Table 1]). The fluctuations in the rate are linked to disparities in the detection methods, variations in the age of the targeted population, and additional factors that may enhance infection. Research conducted in both industrialized and developing nations has identified specific risk factors that may cause differences in rate of campylobacteriosis among children, including female gender, shortened natural lactation periods, lower education among younger mothers, and the lack of regular water purification source.^[16], ^[47], ^[48] Furthermore, Campylobacter species are reported more frequently in diarrheal cases within many low-and middle-income countries that share similar conditions to those in the Middle East. For example, the prevalence rate of Campylobacter infections in South Asian children ranges from 3.2% to 17.4%, compared to 0% to 13% in non-diarrheal cases. ^[47] Moreover, recent data from Pakistan documented that 54.6% of diarrheic stool samples from hospitalized children under 5 years old tested positive for C. jejuni culture. ^[49] Likewise, in a low-resource tropical community in Peru, recent data from whole-genome shotgun metagenomic sequencing indicated that over 65% of the acute diarrheal samples of children under 2 years contained co-infections with multiple Campylobacter species within a single stool sample. ^[50]

It was demonstrated that C. jejuni serotype HS4c had the highest occurrence worldwide, accounting for 12.6% of cases. Nevertheless, the primary capsule variations differed depending on the geographic location. In particular regions, serotypes such as HS2, HS3c, HS4c, HS5/31, HS8/17, and HS10 were among the top ten frequently observed. ^[51] A recent data pointed out that C. jejuni CC21 and CC257 clonal complexes were common among children in Iran and HS23/36, HS2, HS4 and HS19 were prominent capsular genotypes of isolates.^[33]

While the data on pediatric Campylobacteriosis in the Middle East remains limited ([Figure 2]), the available information underscores the significance of compylobacteriosis as a prominent health challenge, particularly within low-and-middle-income countries of Middle East. This gap highlights the need for further studies and underscores the public health importance of addressing Campylobacter infections in children, providing a more complete picture of its challenges in this region.

Countries	Period of Study and sample size (Not: The samples from all studies per country were aggregated as one sample)	Campylobacter spp.	C. jejuni (out of total %)	C. coli (out of total %)	Referencs
Egypt	181 samples were collected from children and adult humans from 2011 until 2018.	26-85.7% (PCR)	12.3-71.4%	2.8-14.3%	[10], [44], [45]
Jordan	122 blood samples from patients under 19 years.	NA	21.3% (Seroprevalence IgG and IgA)	NA	[30]
Iran	Samples of stool were obtained from a group of 1902 children who were experiencing diarrhea during the period of 2012 till 2018.	6 - 11.6% (culture) 14.8% (PCR)	19.5% (culture) 33-95% (PCR).	4.8%	[33], [34], [35], [36], [37], [38]
Iraq	A total of 620 cases of diarrhea were recorded among children under the age of 10 during 2017 till 2020	8-17%	75% (PCR)	-	[39], [40], [41]
Israel	843 specimens from Arab Christian as well as Muslim, and Jewish, children collected from January 2003 till December 2012	53.3%	86.7%	4.5%	[46]
Lebanon	655 fecal samples were gathered from kids during 2016-2018.	12.02- 24.7%	83.2%	19.9%	[31], [32]
Oman	790 fecal specimens were gathered from different aged patients who suffered from gastroenteritis during the period of 2019	-	10.2%	-	[42]
Palestine	132 diarrhea samples from all age patients (75% under 5 years) in 2010	2.2%	-	-	[28]
Qatar	Fecal samples collected from different age groups patients who suffered from for the period 23-2013	1.73–2.06%	-	-	[29]
Turkey	8528 Stool Samples were collected for different ages groups during 2010 to 2016	71% in Children. 52.2% in age group 0-5 years (PCR) & 21.7% in cohort of 6-14years (PCR).	NA	NA	[24], [52]
Syria	73 fecal specimens had been obtained from diarrheic children under 14 at two local hospitals between September and December 2017.	6.84%	4.10%	2.73%	[27]
Yemen	A total of two hundred fecal samples from children under the age of twelve were acquired at General Thamar Hospital and private laboratories within the timeframe spanning from February to November in the year 2011.	13.50%	70.4%	22.22%	[43]

Table 1 Epidemiology of Campylobacter Infection in children of Middle Eastern countries.

Antimicrobial resistance of C jejuni in pediatric papulation in middle East

Antimicrobial resistance of campylobacter spp affects both developed and developing nations, this may be related to many factor including introduction of antibiotics in animal husbandry, notably poultry feed. ^[53], ^[54] There were indications revealed that the resistant C. jejuni may not only be present in chicken supplies but also in animals and feral fowls, serving as potential reservoirs and posing a risk for the spread of resistant bacteria. ^[55], ^[29] In addition, studies in the Middle East regions have demonstrated an increase in the resistance rate of Campylobacter spp. ^[56], ^[57] The presence of multidrug-resistant (MDR), extensively drug-resistant (XDR), and pan-drug-resistant (PDR) Campylobacter species has also been reported in the Middle East. ^[44]

There are five primary categories of antibiotics commonly used to treat campylobacter infections. These categories include aminoglycosides, beta-lactams, fluoroquinolones, macrolides, and tetracyclines, antibiotics typically reserved for use in severe illness to aid recovery rather than being necessary for every infection.^[58] Campylobacter species have evolved multiple mechanisms to counter the selective pressure caused by using antibiotics in both veterinary and human medicine. These mechanisms include modifying or mutating the targets of antimicrobial agents, modifying or inactivating antibiotics directly, and reducing the accumulation of drugs as result of drug efflux pumps. These adaptations allow Campylobacter to acquire resistance to antibiotics, enabling its survival and proliferation in environments where these drugs are present. ^[59] It was demonstrated that the presence of imipenem-resistant isolates with metallo-β-lactamase (MBL) genes raises concerns for public health in the third world. ^[49] Furthermore, Campylobacter shows high Tetracycline and Ciprofloxacin resistance via CmeABC efflux pumps and acquired resistance genes like tetO and gyrA. These multiple, simultaneous mechanisms demonstrate the organism's advanced strategies to develop high antibiotic tolerance, overcoming diverse antimicrobial classes.^[60], ^[61] Moreover, the genetic elements of Campylobacter that harbor clusters of genes conferring resistance to aminoglycosides and macrolides were discovered. These discrete genetic elements concentrate various resistance determinants against these two antibiotic classes in one location. It enables Campylobacter to readily develop cross-resistance against these important antibiotic categories. ^[59]

A recent investigation carried out in Egypt on 120 isolates of C. jejuni and C. coli sourced from human samples and chickens pointed out that 75% of isolates were MDR, 20.8% were XDR, and 4.2% were PDR isolates. ^[44] The complete resistance against Ampicillin in C. jejuni was reported in Egypt, Iraq, and Yemen.^[41], ^[44], ^[62] Meanwhile, it was demonstrated that 40.3% of isolates in one Turkish study had Ampicillin non-susceptibility.^[52] On other hand approximately a quarter of isolated strains, exhibited a resistant capacity for Ampicillin in studies conducted in Lebanon, ^[31] and Iran.^[35] High Ciprofloxacin resistance rates were documented in research data from Israel, ^[63] Egypt, ^[44] Oman, ^[42] Turkey,^[52] and Iran.^[35] Unfortunately, C. jejuni showed completed non-susceptibility for Erythromycin in Egypt,^[44] as well as a high resistant rates were reported in Iraq and Palestine. ^[40], ^[42] In contrast moderate rate of resistance against Erythromycin was found in Iran. ^[35] While low Erythromycin non-susceptibility rate was documented in other regions of Middle East ([Table 2]). As well a high Gentamycin resistance was illustrated in Egypt, ^[44] in compare with low rate or no updated data in other countries. Complete Tetracycline non-susceptibility was listed in Egypt ^[44] and Iraq, ^[41] whereas high resistant rate was indicated in Israel, Iran, and Oman. ^[35], ^[42], ^[63] The resistant prevalence of C. jejuni against Trimethoprim Sulfamethoxazole was found at 100% in one investigation form Egypt. ^[44] At the same time the high resistance of Trimethoprim Sulfamethoxazole was demonstrated in publications from Iraq and Turkey. ^[40], ^[52]

Although there is scant data about Campylobacter species isolated from children in the Middle East, multiple resistant strains of Campylobacter from human sources have been documented in many recent publications from the Middle East regions. ^[57], ^[64], ^[65] The observed resistance patterns in Campylobacter in the Middle East may be linked to several factors, with self-medication and antimicrobial abuse remaining a significant contributing factor that create such issue.^[66], ^[67], ^[68] This circumstance poses a significant challenge in the treatment of Campylobacter infections as some strains have become resistant to multiple antibiotics, limiting the effectiveness of available treatment options. Therefore, utilizing antibiotic sensitivity testing can help guide the selection of the most effective antibiotic for treatment. This approach ensures that the chosen antibiotic is tailored to the specific strain of Campylobacter, optimizing the chances of successful treatment, and minimizing the development of antibiotic resistance.^[69] However, it is important to observe that the occurrence of multi-drug resistance among microbes is widespread and has notable implications particularly in nations with lower economic resources and middle-income status.^[70]

Countries	Study Period	Antimicrobial agents
AMP	CIP	E	GN	TE	STX
Egypt	2017-2018	100%	84%	100%	92%	100%	100%	[44]
Lebanon	2016-2017	30.8%	17.8%	4.1%	NA	22.9%	NA	[31]
Iran	2015	28.8%	0-71.1%	33.6-68.8%	8.8-50%	17-82.2%	NA	[35], [37]
Iraq	2019-2020	100%	26.9%	91.6%	34.6-50%	100	91.6%	[40], [41]
Israel	2015-2021	NA	95%	0.5%	2.1%	93%	NA	[63]
Oman	2019	NA	26.9-80%	0	NA	80%	NA	[42]
Palestine	2010	NA	33.3%	75%	NA	NA	NA	[28]
Qatar	2005 -2012	NA	63.2%	8.6%	0	0	0	[28]
Turkey	2010-2011	40.3%	74.3%	5.9- 6.3%	NA	25%	92.6%	[52], [61]
Yemen	2012-2013	100%	46.2	NA	38%	34.7%	NA	[62]

Table 2 Antimicrobial resistance of C. jejuni in children of middle east

Current challenges of campylobacter infections among middle eastern children

The access to public health interventions and healthcare is significantly limited in some regions of Middle East.^[71] Furthermore, the prevalence of diarrhea among children aged less than 5 years was high, especially in politically instable countries like Yemen where 29.07% of children were suffered from acute diarrhea. The highest rates were observed among those who were under 12 months old.^[72] The incidence of diarrhea among children under the age of five in Yemen was 7.0 (5.5-8.9) episodes per person-year. ^[73] Unfortunately, this challenges is compounded by self-medication that remains a common behavior in many regions of the Middle East. ^[66], ^[67], ^[68] Similarly, in some regions of the Middle East, physicians feel highly pressured to administer broad-spectrum antibiotics due to the unavailability of antimicrobial susceptibility tests that guide antibiotic choices for prescriptions.^[74] In addition, the diet significantly impacts C. jejuni infection, influencing micronutrient availability, microbiome composition, and triggering a lasting immune response in children exposed early. However, short-term consequences include poor nutrient absorption, oral vaccine failure, impaired cognitive function, and increased mortality rates in children under five. ^[75] Likewise, high antibiotic resistance rates have been reported in Campylobacter isolates collected from human, animals, animal products, and food sources across various regions of the Middle East. ^[2], ^[14], ^[26], ^[76], ^[77] Furthermore, many virulence genes have been demonstrated in Campylobacter isolates gathered from humans and other sources in the regions of the Middle East. ^[77] This complex situation poses significant challenges for the children of the Middle East and needs urgent interventions.

References

1. N Gahamanyi, LEG Mboera, MI Matee, D Mutangana, EVG Komba. Prevalence, Risk Factors, and Antimicrobial Resistance Profiles of Thermophilic Campylobacter Species in Humans and Animals in Sub-Saharan Africa: A Systematic Review. Int J Microbiol 2020. [Google Scholar] [Crossref]
2. I Habib, MY Ibrahim Mohamed, AG Lakshmi, M Khan, D Li, S Sahibzada, D. Genomic characterization of molecular markers associated with antimicrobial resistance and virulence of the prevalent Campylobacter coli isolated from retail chicken meat in the United Arab Emirates. Curr Res Food Sci 2022. [Google Scholar] [Crossref]
3. . World Heath Organization (WHO). Diarrhoeal disease. 2017. [Google Scholar]
4. V Velev, M Pavlova, E Alexandrova, I Ivanov, M Popov. Campylobacter infection in children and adults in Bulgaria: comparative characteristics and antimicrobial resistance. Biotechnol Biotechnol Equip 2022. [Google Scholar]
5. FW Bartz, LB Teixeira, R Schroder, AFDM Santos, P Trindade, EC Tondo. First Fatal Cases due to Escherichia coli O157 and Campylobacter jejuni subsp. jejuni Outbreak Occurred in Southern Brazil. Foodborne Pathog Dis 2022. [Google Scholar]
6. TT Kara, S Yilmaz, H Ozdemir, ZB Ozcakar, AD Aysev, E Ciftci. Campylobacter jejuni: un agente infrecuente de peritonitis en un niño con diálisis peritoneal. Arch Argent Pediatr 2016. [Google Scholar]
7. S Al-Shaikh, A Senok, A Ismaeel, G Botta. Invasive capabilities of Campylobacter jejuni strains isolated in Bahrain: Molecular and phenotypic characterization. Acta Microbiol Immunol Hung 2007. [Google Scholar]
8. YT Guo, CA Hsiung, FT Wu, H Chi, CY Huang, CC Liu. Clinical manifestations and risk factors of campylobacter gastroenteritis in children in Taiwan. Biomed J 2023. [Google Scholar] [Crossref]
9. NO Kaakoush, N Castaño-Rodríguez, HM Mitchell, SM Man. Global epidemiology of campylobacter infection. Clin Microbiol Rev 2015. [Google Scholar]
10. WF El-Tras, HR Holt, AA Tayel, NN El-Kady. Campylobacter infections in children exposed to infected backyard poultry in Egypt. Epidemiol Infect 2015. [Google Scholar]
11. K Diriba, E Awulachew, A Anja. Prevalence and associated factor of Campylobacter species among less than 5-year-old children in Ethiopia: a systematic review and meta-analysis. Eur J Med Res 2021. [Google Scholar] [Crossref]
12. N Abdollahpour, B Zendehbad, A Alipour, J Khayatzadeh. Wild-bird feces as a source of Campylobacter jejuni infection in children’s playgrounds in Iran. Food Control 2015. [Google Scholar] [Crossref]
13. KM Alarjani, MF Elkhadragy, AH Al-Masoud, HM Yehia. Detection of Campylobacter jejuni and Salmonella typhimurium in chicken using PCR for virulence factor hipO and invA genes (Saudi Arabia). Biosci Rep 2021. [Google Scholar] [Crossref]
14. DA Almashhadany. Isolation, biotyping and antimicrobial susceptibility of Campylobacter isolates from raw milk in Erbil city. Iraq. Ital J Food Saf 2021. [Google Scholar] [Crossref]
15. MI Abd El-Hamid, NK Abd El-Aziz, M Samir, ESY El-Naenaeey, EM Abo Remela, RA Mosbah. Genetic Diversity of Campylobacter jejuni Isolated From Avian and Human Sources in Egypt. Front Microbiol 2019. [Google Scholar] [Crossref]
16. MA Haque, JA Platts-Mills, E Mduma, L Bodhidatta, P Bessong, S Shakoor. Determinants of Campylobacter infection and association with growth and enteric inflammation in children under 2 years of age in low-resource settings. Sci Rep 2019. [Google Scholar] [Crossref]
17. HJ Willison, BC Jacobs, PA Van Doorn. Guillain-Barré syndrome. Lancet 2016. [Google Scholar]
18. R Spiller, K Garsed. Postinfectious Irritable Bowel Syndrome. Gastroenterology 2009. [Google Scholar]
19. JE Pope, A Krizova, AX Garg, H Thiessen-Philbrook, JM Ouimet. Campylobacter Reactive Arthritis: A Systematic Review. Semin Arthritis Rheum 2007. [Google Scholar]
20. J Keithlin, J Sargeant, M K Thomas, A Fazil. Systematic review and meta-analysis of the proportion of Campylobacter cases that develop chronic sequelae. BMC Public Health 2014. [Google Scholar] [Crossref]
21. M I Hossain, S Nasrin, R Das, P Palit, A Sultana, RA Sob. Symptomatic and Asymptomatic Campylobacter Infections and Child Growth in South Asia: Analyzing Data from the Global Enteric Multicenter Study. Am J Trop Med Hyg 2023. [Google Scholar]
22. AA Dabbousi, M Osman, F Dabboussi, M Hamze. High rates of macrolide and fluoroquinolone resistance in human campylobacteriosis in the Middle East and North Africa. Future Microbiol 2022. [Google Scholar]
23. HA Al-Hamadani, ZF Saleh. Detection of Campylobacter spp. in children diarrhea by using Polymerase Chain Reaction PCR technique in Al-Diwanyiah Governorate. Al-Qadisiyah J Vet Med Sci 2011. [Google Scholar]
24. C Eryıldız, N Şakru, K Tabakçıoğlu, MC Uğur, SBukavaz. Molecular Identification of Campylobacter Species Isolated from Patients with Gastroenteritis in Edirne, Turkey. Cyprus J Med Sci 2022. [Google Scholar]
25. D Babazadeh, R Ranjbar. Campylobacter Species in the Middle East. J Vet Physiol Pathol 2022. [Google Scholar]
26. S Abukhattab, H Taweel, A Awad, L Crump, P Vonaesch, J Zinsstag. Systematic Review and Meta-Analysis of Integrated Studies on Salmonella and Campylobacter Prevalence, Serovar, and Phenotyping and Genetic of Antimicrobial Resistance in the Middle East-A One Health Perspective. Antibiotics (Basel) 2022. [Google Scholar] [Crossref]
27. N Shahin, N Daood. Study of spread the Campylobacter jejuni among children with Diarrhea. Res J Pharm Technol 2019. [Google Scholar]
28. AA Elmanama, N Abdelateef. Antimicrobial Resistance of Enteric Pathogens Isolated from Acute Gastroenteritis Patients in Gaza strip, Palestine. Int Arab J Antimicrob Agents 2012. [Google Scholar] [Crossref]
29. H Ghunaim, JM Behnke, I Aigha, A Sharma, SH Doiphode, A Deshmukh. Analysis of resistance to antimicrobials and presence of virulence/stress response genes in Campylobacter isolates from patients with severe diarrhoea. PLoS One 2015. [Google Scholar] [Crossref]
30. MM Obaidat. Seroprevalence and risk factors for Campylobacter jejuni seropositivity in Jordan. Infect Dis (Auckl) 2019. [Google Scholar]
31. JN Ibrahim, E Eghnatios, A El Roz, T Fardoun, G Ghssein. Prevalence, antimicrobial resistance and risk factors for campylobacteriosis in Lebanon. J Infect Dev Ctries 2019. [Google Scholar]
32. G Ghssein, R Awada, A Salami, HF Bahmad, A Awad, WH Joumaa. Laboratory Findings and Clinical Characteristics of Campylobacteriosis Agents among Hospitalized Children with Acute Gastroenteritis in Lebanon. Pediatr Gastroenterol Hepatol Nutr 2021. [Google Scholar]
33. M Sarhangi, B Bakhshi, S N Peeraeyeh. High prevalence of Campylobacter jejuni CC21 and CC257 clonal complexes in children with gastroenteritis in Tehran, Iran. BMC Infect Dis 2021. [Google Scholar] [Crossref]
34. M Ghorbanalizadgan, B Bakhshi, AK Lili, S Najar-Peerayeh, B Nikmanesh. A molecular survey of Campylobacter jejuni and Campylobacter coli virulence and diversity. Iran Biomed J 2014. [Google Scholar]
35. E Abbasi, A Van Belkum, E Ghaznavi-Rad. Quinolone and Macrolide-Resistant Campylobacter jejuni in Pediatric Gastroenteritis Patients from Central Iran. Microb Drug Resist 2019. [Google Scholar]
36. M Barati, A Taghipour, B Bakhshi, S Shams, M Pirestani. Prevalence of intestinal parasitic infections and Campylobacter spp. among children with gastrointestinal disorders in Tehran, Iran. Parasite Epidemiol Control 2021. [Google Scholar] [Crossref]
37. S Rastyani, M Y Alikhani, I Sedighi, S Kazemi, HF Kohan, MR Arabestani. Campylobacter jejuni and Campylobacter coli in Children With Acute Diarrhea in Health Centers of Hamadan, Iran. Avicenna J Clin Microbiol Infect 2015. [Google Scholar] [Crossref]
38. M Salehi, E Shafaei, Z Bameri, S Shareki Zahedani, M Bokaeian, M Bokaeian. Prevalence and Antimicrobial Resistance of Campylobacter jejuni. Int J Infect 2014. [Google Scholar]
39. A Harb, S Abraham, B Rusdi, T Laird, M O’dea, I Habib. Molecular detection and epidemiological features of selected bacterial, viral, and parasitic enteropathogens in stool specimens from children with acute diarrhea in Thi-Qar Governorate. Iraq Int J Environ Res Public Health 2019. [Google Scholar]
40. GN Khalaf, TA Abdulrahman. Prevalence of Campylobacter Species in Diarrheal Samples of Children Less than 10 Years. Indian J Forensic Med Toxicol 2020. [Google Scholar]
41. Shh Alsafar, AR Abd, I G Mahdi, Al-Tameemi Tta. Identification and isolation of Campylobacter jejuni and C. upsaliensis from bovine local milk, milk products, and human stool samples by molecular technique in Karbala province. J Kerbala Agric Sci 2023. [Google Scholar]
42. AAS Alsalmi, SA Al-Busafi, RNS Al-Lamki, M Mabruk. The Ecology and Antibiotic Resistance Patterns of Gastrointestinal Tract Infections in A Tertiary Care Hospital in Oman. J Pure Appl Microbiol 2021. [Google Scholar]
43. ARA Humaid, DA Al-Mashhadany, FM Al-Dulaimy. Incidence of Campylobacter Species in Faeces of Children in Thamar Province, Yemen. Fac Sci Bull 2013. [Google Scholar]
44. AM Ammar, MI Abd El-Hamid, RMS El-Malt, DS Azab, S Albogami, MM Al-Sanea. Molecular Detection of Fluoroquinolone Resistance among Multidrug-, Extensively Drug-, and Pan-Drug-Resistant Campylobacter Species in Egypt. Antibiotics (Basel) 2021. [Google Scholar] [Crossref]
45. NO Khalifa, JSA Afify, NS Rabie. Zoonotic and molecular characterizations of Campylobacter jejuni and Campylobacter coli isolated from beef cattle and children. Glob Vet 2013. [Google Scholar]
46. W Sakran, Z Hexner-Erlichman, R Spiegel, H Batheesh, R Halevy, A Koren. Campylobacter gastroenteritis in children in north-eastern Israel comparison with other common pathogens. Sci Rep 2020. [Google Scholar] [Crossref]
47. M Murugesan, D Abraham, P Samuel, SS Ajjampur. Campylobacter diarrhea in children in South Asia: A systematic review. Indian J Med Microbiol 2022. [Google Scholar]
48. DF Hlashwayo, B Sigaúque, EV Noormahomed, SMS Afonso, IM Mandomando, CG Bila. A systematic review and meta-analysis reveal that Campylobacter spp. And antibiotic resistance are widespread in humans in sub-Saharan Africa. PLoS One 2021. [Google Scholar]
49. Z Noreen, F Siddiqui, S Javed, B W Wren, H Bokhari. Transmission of multidrug-resistant Campylobacter jejuni to children from different sources in Pakistan. J Glob Antimicrob Resist 2020. [Google Scholar] [Crossref]
50. CT Parker, F Schiaffino, S Huynh, MP Olortegui, PP Yori, PFG Bardales. Shotgun metagenomics of fecal samples from children in Peru reveals frequent complex co-infections with multiple Campylobacter species. PLoS Negl Trop Dis 2022. [Google Scholar] [Crossref]
51. TN Clarke, MA Schilling, LA Melendez, SD Isidean, CK Porter, FM Poly. A systematic review and meta-analysis of Penner serotype prevalence of Campylobacter jejuni in low- and middle-income countries. Fratamico P. PLoS One 2021. [Google Scholar] [Crossref]
52. T Kayman, S Abay, H Hızlısoy. Identification of Campylobacter spp. isolates with phenotypic methods and multiplex polymerase chain reaction and their antibiotic susceptibilities. Mikrobiyol Bul 2013. [Google Scholar]
53. X Qin, X Wang, Z Shen. The rise of antibiotic resistance in Campylobacter. Curr Opin Gastroenterol 2023. [Google Scholar]
54. L Ford, J M Healy, Z Cui, L Ahart, F Medalla, LC Ray. Epidemiology and Antimicrobial Resistance of Campylobacter Infections in the United States. Open Forum Infect Dis 2005. [Google Scholar]
55. J Aksomaitiene, S Ramonaite, E Tamuleviciene, A Novoslavskij, T Alter, M Malakauskas. Overlap of antibiotic resistant Campylobacter jejuni MLST genotypes isolated from humans, broiler products, dairy cattle and wild birds in Lithuania. Front Microbiol 2019. [Google Scholar]
56. MM Said, H El-Mohamady, FM El-Beih, DM Rockabrand, TF Ismail, R Monteville. Detection of gyrA Mutation Among Clinical Isolates of Campylobacter jejuni Isolated in Egypt by MAMA-PCR. J Infect Dev Ctries 2010. [Google Scholar]
57. C Eryıldız, N Sakru, G Kuyucuklu. Investigation of Antimicrobial Susceptibilities and Resistance Genes of Campylobacter Isolates from Patients in Edirne, Turkey. Iran J Public Health 2022. [Google Scholar]
58. . Centers for Disease Control and Prevention. Information for Health Professionals | Campylobacter. 2023. [Google Scholar]
59. Z Shen, Y Wang, Q Zhang, J Shen. Antimicrobial Resistance in Campylobacter spp. Microbiol Spectr 2018. [Google Scholar] [Crossref]
60. S Sharifi, B Bakhshi, S Najar-Peerayeh. 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. [Google Scholar] [Crossref]
61. T Kayman, S Abay, F Aydin, O Şahin. Antibiotic resistance of Campylobacter jejuni isolates recovered from humans with diarrhoea in Turkey. J Med Microbiol 2019. [Google Scholar]
62. NM Baghza. Bacterial Profile And Antimicrobial Susceptibility Pattern Among Food Poisoning Patients In Dhamar City, yemen. Fac Sci Bull 2014. [Google Scholar]
63. O Tsafrir, H Rohana, L Bousani, K Orsan, K Abozaid, M Azrad. Clinical isolate characteristics and demographics of patients with C.jejuni and C.coli infections in Northern Israel. Epidemiol Infect 2024. [Google Scholar] [Crossref]
64. H Hizlisoy, P Sagiroglu, M Barel, A Dishan, C Gungor, K Koskeroglu. Campylobacter jejuni and Campylobacter coli in human stool samples: antibiotic resistance profiles, putative virulence determinants and molecular characterization of the isolates. World J Microbiol Biotechnol 2023. [Google Scholar]
65. M Ilktac, B Ongen. Molecular Typing of Campylobacter jejuni and Campylobacter coli of Human Strains Isolated in Turkey Over an Eight-Year Period. Clin Lab 2020. [Google Scholar]
66. A Halboup, A Abdi, M Ahmed, F Al-Qadasi, G Q Othman. Access to antibiotics without prescription in community pharmacies in Yemen during the political conflict. Public Health 2020. [Google Scholar] [Crossref]
67. AA Rasheed, U Yagoub, H Alkhashan, O Abdelhay, A Alawwad, AA Aboud. Prevalence and Predictors of Self-Medication with Antibiotics in Al Wazarat Health Center, Riyadh City, KSA. Biomed Res Int 2016. [Google Scholar] [Crossref]
68. K Kasim, Hassan H. Self Medication Problem in Egypt: A Review of Current and Future Perspective. Int J Curr Res Rev 2018. [Google Scholar] [Crossref]
69. Y Behailu, S Hussen, T Alemayehu, M Mengistu, DA Fenta. Prevalence, determinants, and antimicrobial susceptibility patterns of Campylobacter infection among under-five children with diarrhea at Governmental Hospitals in Hawassa city, Sidama, Ethiopia. A cross-sectional study. PLoS One 2022. [Google Scholar]
70. A Amran. Antibiotics susceptibility patterns of bacterial isolates from clinical samples in Thamar. Ann Agric Sci Moshtohor 2018. [Google Scholar]
71. M Leung. Phenotypic and genotypic diversity in Streptococcus pneumoniae strains in Tanzania and the United Kingdom. (Doctoral thesis). London: UCL Discovery. 2012. [Google Scholar]
72. M Bin Mohanna, N Al-Sonboli, . Prevalence of diarrhoea and related risk factors among children aged under 5 years in Sana’a, Yemen. Hamdan Med J 2018. [Google Scholar] [Crossref]
73. C El Bcheraoui, AO Jumaan, ML Collison, F Daoud, AH Mokdad. Health in Yemen: losing ground in war time. Global Health 2018. [Google Scholar] [Crossref]
74. ESF Orubu, N Al-Dheeb, C Ching, SB Jawdeh, J Anderson, R Sheikh. Assessing Antimicrobial Resistance, Utilization, and Stewardship in Yemen: An Exploratory Mixed-Methods Study. Am J Trop Med Hyg 2021. [Google Scholar]
75. A E Schnee, WA Petri. Campylobacter jejuni and associated immune mechanisms. Curr Opin Infect Dis 2017. [Google Scholar]
76. M Elmalı, HY Can. Antimicrobial susceptibility and virulence-associated genes in Campylobacter isolates from milk and wastewater in Hatay. Turkey. Cienc Rural 2019. [Google Scholar] [Crossref]
77. AMA Barakat, KAA El-Razik, HA Elfadaly, NS Rabie, SA. Sadek, AM Almuzaini. Prevalence, molecular detection, and virulence gene profiles of Campylobacter species in humans and foods of animal origin. Vet World 2020. [Google Scholar]